Global Change in Multispecies Systems Part 1 PDF

ADVANCES IN ECOLOGICAL
RESEARCH
Series Editor
GUY WOODWARD
School of Biological and Chemical Sciences
Queen Mary University of London
London, UK
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CONTRIBUTORS
Cecilia Alonso
Ecologı́a Funcional de Sistemas Acuáticos, Centro Universitario Regional Este (CURE),
Universidad de la República, Ruta, Rocha, Uruguay
Isabel Alves-Dos-Santos
Departamento de Ecologia, Instituto de Biociências, Universidade de São Paulo, São Paulo,
São Paulo, Brazil
Matı́as Arim
Departamento de Ecologı́a y Evolución, Facultad de Ciencias, Centro Universitario
Regional Este (CURE), Universidad de la República, Burnett s/n; Facultad de Ciencias,
Universidad de la República, Iguá, CP 11400, Montevideo, Uruguay, and Center for
Advanced Studies in Ecology and Biodiversity (CASEB), Depto. de Ecologı́a, Facultad de
Ciencias Biológicas, Pontificia Universidad Católica, CP 6513677, Santiago, Chile
Patrick D. Armitage
Freshwater Biological Association River Laboratory, East Stoke, Wareham, Dorset, United
Kingdom
Wolf E. Arntz
Alfred Wegener Institute for Polar and Marine Research, Bremerhaven, Germany
Esteban R. Barrera-Oro
Instituto Antártico Argentino and CONICET, and Museo Argentino de Ciencias Naturales
‘Bernardino Rivadavia’, Buenos Aires, Argentina
Meryem Beklioğlu
Department of Biology, Limnology Laboratory, Middle East Technical University,
Üniversiteliler Mahallesi, Dumlupınar Bulvarı, Çankaya, Ankara, Turkey
Alice Boit
Department of Ecology and Ecosystem Modeling, Institute of Biochemistry and Biology,
University of Potsdam, Potsdam, Germany
Thomas Brey
Lee E. Brown
School of Geography, University of Leeds, Leeds, United Kingdom
Sandra Brucet
European Commission, Joint Research Centre, Institute for Environment and Sustainability,
Ispra, Italy
Daniel W. Carstensen
Department of Bioscience, Aarhus University, Aarhus, Denmark
ix
x Contributors
Marcus A.M. De Aguiar

Instituto de Fı́sica Gleb Wataghin, Universidade Estadual de Campinas, Campinas, São
Paulo, Brazil
Yoko L. Dupont
Scott D. Dyer
Procter & Gamble, Cincinnati, Ohio, USA
Francois K. Edwards
Centre for Ecology and Hydrology, Wallingford, United Kingdom
Leslie Faggiano
Institute of Aquatic Ecology, Universitat de Girona, Girona, Spain, and Laboratoire
Evolution et Diversité Biologique, Université Paul Sabatier, CNRS, Toulouse Cedex 9,
France
Stefan Geisen
Department of Terrestrial Ecology, Institute of Zoology, University of Köln, Biozentrum
Köln, Köln, Germany
Julieta Genini
Departamento de Botânica, Laboratório de Fenologia, UNESP Univ Estadual Paulista,
Rio Claro, São Paulo, Brazil
Iván González-Bergonzoni
Regional Este (CURE), Universidad de la República, Burnett s/n, Maldonado, Uruguay,
and Department of Bioscience, Aarhus University, Vejlsøvej, Silkeborg, Denmark
Angélica L. González
Department of Zoology, University of British Columbia, Vancouver, British Columbia,
Canada
Guillermo Goyenola
Regional Este (CURE), Universidad de la República, Burnett s/n, Maldonado,
Uruguay
Paulo R. Guimarães Jr.
São Paulo, Brazil
Melanie Hagen
Rebecca M.L. Harris
School of Geography, Earth and Environmental Sciences, University of Birmingham,
Edgbaston, Birmingham, United Kingdom
Carlos Iglesias
Regional Este (CURE), Universidad de la República, Burnett s/n, Maldonado, Uruguay
Contributors xi
Ute Jacob
Institute for Hydrobiology and Fisheries Science, University of Hamburg, Hamburg, Germany
Gareth B. Jenkins
School of Biological and Chemical Sciences, Queen Mary University of London, London,
United Kingdom
Erik Jeppesen
Department of Bioscience, Aarhus University, Vejlsøvej, Silkeborg, Denmark; Greenland
Climate Research Centre (GCRC), Greenland Institute of Natural Resources, Kivioq,
P.O. Box 570 3900, Nuuk, Greenland, and Sino-Danish Centre for Education and Research
(SDC), Beijing, China
Pedro Jordano
Integrative Ecology Group, Estación Biológica de Doñana, CSIC, Sevilla, Spain
Christopher N. Kaiser-Bunbury
Michael Kaspari
Department of Zoology, University of Oklahoma, Norman, Oklahoma, USA,
and Smithsonian Tropical Research Institute, Balboa, Panama
W. Daniel Kissling
Rainer Knust
Sarian Kosten
Department of Aquatic Ecology and Water Quality Management, Wageningen University,
Wageningen, The Netherlands, and Leibniz-Institute of Freshwater Ecology and Inland
Fisheries (IGB), Berlin/Neuglobsow, Germany
Carla Kruk
Laboratory of Ethology, Ecology and Evolution, Instituto de Investigaciones Biológicas
Clemente Estable, Italia, CP 11600, and Ecologı́a Funcional de Sistemas Acuáticos,
Limnologı́a, IECA, Facultad de Ciencias, Universidad de la República, Iguá, CP 11400,
Montevideo, Uruguay
Gissell Lacerot
Ecologı́a Funcional de Sistemas Acuáticos, Centro Universitario Regional Este (CURE),
Universidad de la República, Ruta, Rocha, Uruguay
Sandra Lavorel
Laboratoire d’Ecologie Alpine, CNRS UMR 5553, Grenoble Cedex 9, France
Mark E. Ledger
Edgbaston, Birmingham, United Kingdom
Kate P. Maia
São Paulo, Brazil
xii Contributors
Felix C. Mark
Pablo A. Marquet
Center for Advanced Studies in Ecology and Biodiversity, Institute of Ecology and
Biodiversity, Pontificia Universidad Catolica de Chile, Santiago, Chile, and The Santa
Fe Institute, Santa Fe, New Mexico, USA
Flavia M. Darcie Marquitti
São Paulo, Brazil
Néstor Mazzeo
Regional Este (CURE), Universidad de la República, Burnett s/n, and South American
Institute for Resilience and Sustainability Studies (SARAS), Maldonado, Uruguay
Órla Mclaughlin
Environmental Research Institute, and School of Biological, Earth, and Environmental
Sciences, University College Cork, Cork, Ireland
Mariana Meerhoff
Regional Este (CURE), Universidad de la República, Burnett s/n; Department of
Bioscience, Aarhus University, Vejlsøvej, Silkeborg, Denmark, and South American Institute
for Resilience and Sustainability Studies (SARAS), Maldonado, Uruguay
Alexander M. Milner
Edgbaston, Birmingham, United Kingdom, and Institute of Arctic Biology, University
of Alaska, Fairbanks, Alaska, USA
Katja Mintenbeck
Eugenia Moreira
Instituto Antártico Argentino and CONICET, Buenos Aires, Argentina
L. Patricia C. Morellato
Departamento de Botânica, Laboratório de Fenologia, UNESP Univ Estadual Paulista,
Rio Claro, São Paulo, Brazil
Shigeta Mori
Forestry and Forest Products Research Institute, Tsukuba, Japan
Christian Mulder
National Institute for Public Health and the Environment (RIVM), Bilthoven, The Netherlands
Eoin J. O’Gorman
United Kingdom
Contributors xiii
Jens M. Olesen
Juan Pablo Pacheco
Claus Rasmussen
Axel G. Rossberg
Centre for Environment, Fisheries and Aquaculture Science (Cefas), Lowestoft Laboratory,
Suffolk, United Kingdom, and Medical Biology Centre, School of Biological Sciences,
Queen’s University Belfast, Belfast, United Kingdom
Robert W. Sterner
Ecology, Evolution & Behavior, University of Minnesota, St. Paul, Minnesota, USA
Anneli Strobel
Franco Teixeira-de Mello
Kristian Trøjelsgaard
Jason M. Tylianakis
School of Biological Sciences, University of Canterbury, Christchurch, New Zealand
Mariana Morais Vidal
São Paulo, Brazil
Winfried Voigt
Community Ecology Group, Institute of Ecology, Friedrich Schiller University, Jena,
Germany
J. Arie Vonk
Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam,
and Institute for Water and Wetland Research, Radboud University Nijmegen, Nijmegen,
The Netherlands
Diana H. Wall
Department of Biology & Natural Resource Ecology Laboratory (NREL), School of Global
Environmental Sustainability, Colorado State University, Fort Collins, Colorado, USA
Guy Woodward
United Kingdom
PREFACE
Editorial Commentary: Global Change
in Multispecies Systems Part 1
Ute Jacob*, Guy Woodward†
*Institute for Hydrobiology and Fisheries Science, University of Hamburg, Hamburg, Germany
†
School of Biological and Chemical Sciences, Queen Mary University of London, London, United Kingdom
Evaluating the consequences of global change is a major challenge in current

research, especially in the light of rising concerns over anthropogenic im-
pacts in general and climate forcing and its potential impacts on ecosystems
in particular (Daufresne et al., 2009; Parmesan, 2006; Parmesan and Yohe,
2003; Raffaelli, 2004; Sarmiento et al., 2004; Walther et al., 2002;
Woodward et al., 2010a,b). To address how multispecies systems might
change over the next century, ecologists need to focus on how their
properties will be affected by the main drivers behind global change that
have already been identified (Sala et al., 2000; Thomas et al., 2004), as
well as dealing with emerging and potentially synergistic multiple stressors
(e.g. Feuchtmayr et al., 2009; McKee et al., 2003; Memmott et al., 2007;
Moss et al., 2003). This collection of papers in Volume 46 of Advances in
Ecological Research represents the first of a set of three under the theme of
Global Change in Multispecies Systems, each of which contains a different
blend of papers from both empirical and theoretical approaches: this
commentary is concerned primarily with the papers appearing in this and
the two subsequent volumes, while briefly placing them in the wider
context of recent advances in the field, rather than giving an in-depth
review.
Global ecological change is driven by a suite of environmental parame-
ters that control the structure and dynamics of multispecies systems (Thomas
et al., 2004; Tylianakis, 2009; Woodward et al., 2010a). The main drivers
investigated in Volumes 46–48 include land use change and habitat
fragmentation (Hagen et al., 2012), drought (Ledger et al., 2012a,b) and
other components of climate change (Meerhoff et al., 2012; Mintenbeck
et al., 2012; Möllmann and Diekmann, 2012; O’Gorman et al., 2012;
Peck et al., 2012), eutrophication (Jeppesen et al., 2012), and resource
overexploitation (Peck et al., 2012; Rossberg, 2012). Other aspects of
global change that are touched on in the papers published here and in
xv
xvi Ute Jacob and Guy Woodward
other recent volumes in the series include invasive species (Jacob et al., 2011;
Woodward et al., 2010a,b), marine and freshwater acidification (Layer et al.,
2010; Mintenbeck et al., 2012; Peck et al., 2012), and agricultural
intensification (Feld et al., 2011; Hladyz et al., 2011a,b; Mulder et al.,
2011, 2012). There is also considerable potential for synergies to arise
from different combinations of these stressors, as it is rare that a single
driver will be operating in isolation, but these interactive effects are still
poorly understood (Feld et al., 2011; Friberg et al., 2011; Woodward
et al., 2010a,b).
In terms of response variables, the six papers in this volume are concerned
primarily with populations, communities and ecosystems over ecological
timescales, whereas some of those in the two subsequent volumes encompass
an even wider range of organisational levels (e.g. genes, individuals: Moya-
Laraño et al., 2012; O’Gorman et al., 2012) and spatiotemporal scales
(e.g. eco-evolutionary dynamics of food webs: Moya-Laraño et al., 2012).
Habitat fragmentation is one of the key threats to both global and local
biodiversity, as species and higher-level responses will be determined by
their spatial context and source-sink dynamics within the landscape
(Raffaelli, 2004). Surprisingly, though, very little attention has been paid
to gauging how ecological networks (e.g. food webs, mutualistic networks)
might be affected by habitat size or fragmentation, despite the fact that the
configuration and strength of interactions between species may be just as im-
portant as the identity and number of species themselves (Hagen et al., 2012;
McLaughlin et al., 2010). Even less attention has been paid to how potential
synergistic effects of additional stressors, such as climate change, may amplify
or mitigate the effects of habitat fragmentation. Here, Hagen et al. (2012)
make a first attempt at considering how best to integrate spatial and
ecological networks, to explore the effects of dispersal, colonisation,
extinction and habitat fragmentation on network structure and dynamics.
They also make the first steps towards embedding network approaches
more explicitly within applied and landscape ecology and ideas arising
from metacommunity theory, highlighting the great potential for
improving on the current species-based or habitat-centric approaches to
management and conservation of biodiversity in the face of global
change. Hagen et al.’s paper reflects a growing realisation within the
applied ecology fraternity that effective monitoring, management and
conservation of multispecies systems must move beyond the spatial and
temporal boundaries that are typically used to delimit them at present.
The potential for eco-evolutionary dynamics to create feedbacks in
Preface xvii
fragmented food webs are also touched on, with species both responding to
and shaping their biotic and abiotic environment over a range of timescales.
These points are covered in greater depth in the preceding and subsequent
volumes by Melian et al. (2011) and Moya-Laraño et al. (2012), which
represent pioneering attempts to bridge the gap between ecology and
evolution in multispecies systems.
Understanding the likely cause-and-effect relationships behind global
change in natural systems requires an understanding of how they change
through both time and space. These themes recur throughout these three vol-
umes, especially in those papers focused on fresh waters (Jeppesen et al., 2012;
Ledger et al., 2012a,b; Meerhoff et al., 2012; O’Gorman et al., 2012). These
seemingly fragile ecosystems cover only a tiny percentage of Earth’s surface,
yet they are disproportionately important, especially in terms of the
biodiversity they hold and the ecosystem goods and services they provide.
They are also fragmented islands of water in a predominantly terrestrial
landscape (Hynes, 1975), and as such, they are vulnerable to an array of
anthropogenic stressors (Hladyz et al., 2011a,b), especially as much of the
world’s human population lives clustered close to their shores or on their
floodplains. In the context of climate change, the analysis of flood and
drought risks is critically important for preserving the structure and
functioning of fresh waters (Milly et al., 2006). Unfortunately, our ability
to make accurate and predictive assessments is still severely constrained by
the current lack of data and understanding, with most examples to date
being limited to correlational studies (Lake, 2003). Here an attempt to help
redress this balance is made by the Ledger et al. (2012a,b) paper, which
presents a comprehensive set of results building from earlier studies (Ledger
and Hildrew, 2001; Ledger et al., 2008, 2009) in one of the first mesocosm
field experiments to measure the effects of drought on replicate
macroinvertebrate communities, providing a rare experimental test of
community resilience in aquatic ecosystems at intergenerational scales. The
communities were resilient to relatively low-frequency disturbance
(quarterly droughts), but the capacity for recovery was soon exceeded as
disturbance frequency increased (monthly droughts), skewing community
structure and functioning. This highlights how multispecies responses to
climate change may be highly non-linear, with marked thresholds and
tipping points, rather than a simple progressive and gradual erosion of
ecological integrity.
The Ledger et al. (2012a,b) study isolates a single component of climate
change (drought), as does the O’Gorman et al. (2012) study in Volume 47,
xviii Ute Jacob and Guy Woodward
although the latter focuses on the effects of warming on stream ecosystems.

Climate change is among the most important but also most complex drivers
of global change, and quantifying and anticipating its effects on the structure
and functioning of multispecies systems are daunting. This is especially
challenging because climate change represents an amalgam of changes in
both the abiotic (atmospheric and hydrological) and the biotic (invasions,
extinctions and evolution) environments, in addition to the enormous
scope for unexpected feedbacks to arise between these components.
Identifying correlations between climate variables and the biota is there-
fore only a beginning, and we need to move rapidly beyond the species-
centric bioclimatic envelope approach to address responses in multispecies
systems (Pearson and Dawson, 2003). A deeper mechanistic understanding
is needed urgently, and considerable effort is being devoted to achieving this
goal via the use of increasingly sophisticated experiments and models. While
this gap in our knowledge is being bridged, correlational data continue to
provide invaluable insights and help guide further studies by providing
the wider context within which to search for likely mechanisms (e.g.
Konig et al., 2002; Milner et al., 2000, 2008, 2009; Rawcliffe et al.,
2010), as shown here in a new synthesis by Meerhoff et al. (2012), even
though they cannot demonstrate causality unequivocally. Community or
ecosystem responses to climate change are likely to be complex, because
species populations interact within their respective ecological networks
at both ecological and evolutionary timescales (Melian et al., 2011;
Moya-Laraño et al., 2012; Olesen et al., 2010; Woodward et al.,
2010a). Competition, natural enemies, and physiological constraints
(among many others) influence species distributions, and these will
change with both the climate and shifts in local communities on a
global scale (Möllmann and Diekmann, 2012; Walther, 2010;
Woodward et al., 2010a,b). Here, Meerhoff et al. (2012) provide an
overview of multispecies responses to climatic change, as detected using
space-for-time substitutions in lake ecosystems. They consider not only
structural properties (species richness, biomass, density, body size) but
also processes (e.g. reproduction, the intensity of trophic interactions
and potential for top-down control of resources by consumers) for the
major taxonomic and functional groups within food webs across a broad
latitudinal range. This approach is complemented in the subsequent
volume by O’Gorman et al. (2012), who also employ space-for-time
substitution, but within a single catchment, to assess the effects of
warming in fresh waters.
Preface xix
Mintenbeck et al. (2012) also use a model system approach, this time
focusing on the seas of the high Antarctic, where fishes play a central role
in the food web, as highlighted previously by Jacob et al. (2011). These
key taxa are important conduits of energy and also often agents of top-down
control, yet they are affected by climate change in different ways: directly,
via increasing water temperatures and/or CO2 concentrations and decreas-
ing salinity; indirectly, via changes in food web structure and dynamics, and
by habitat change due to sea-ice retreat and scouring of the sea floor. They
identified potential bottlenecks arising from the loss of key species, which
could ripple through the entire food web, altering the ecosystem as a whole.
Highly connected or “strategically positioned” nodes within food webs can
exert powerful effects and may even trigger trophic cascades or regime shifts
in extreme cases, which could not be predicted without considering how
they are connected to other species in the system. These ideas, which are
well-supported by both data and theory (e.g. Dunne et al., 2002; Jacob
et al., 2011; Jeppesen et al., 2003; Kishi et al., 2005; Montoya et al.,
2009), resurface several times in Volumes 46–48 (e.g. Mintenbeck et al.,
2012; O’Gorman et al., 2012). In contrast, other systems seem relatively
robust to perturbations (e.g. Twomey et al., 2012): the challenge is to be
able to identify what attributes of multispecies systems make them
especially vulnerable, or stable, in the face of the drivers of global change.
It is also increasingly clear that not all ecological response variables are
equally sensitive and that huge change at one level of biological
organisation might have little effect at another: for example, if different
species have similar ecological roles, ecosystem functioning may be
maintained in the early stages of species loss (Petchey et al., 2004; Reiss
et al., 2009). For instance, in this volume, Ledger et al. (2012a)
demonstrate dramatic shifts in population abundances, community
composition and biomass production in response to drought, yet many
structural food web attributes remain highly conserved (Ledger et al.,
2012b; Woodward et al., 2012).
Overfishing is an unfortunately familiar example of resource overex-
ploitation that threatens marine biodiversity on a global scale, and its con-
sequences across multiple levels of organisation are also considered by
Rossberg (2012), who presents a novel, elegant and yet comprehensive an-
alytic approach to modelling the dynamics of marine ecosystems. This offers
an important means of improving our understanding of the mechanisms that
control community and population size structure and likely responses to
perturbations. Although focused primarily on marine fisheries, many of
xx Ute Jacob and Guy Woodward
these principles can clearly be extended to many other aquatic and terrestrial
systems, where, for example, size-spectra and other allometric scaling ap-
proaches are rapidly gaining favour (e.g. Mulder et al., 2012) as cross-
fertilisation between these previously disparate disciplines gathers apace
(Jennings and Brander, 2010; Woodward et al., 2011).
ON THE WISHLIST: BETTER DATA AND PREDICTIVE

FRAMEWORKS
Global change will continue to challenge theoretical ecologists, em-
pirical scientists, and conservation biologists over the coming decades as
both natural and managed multispecies systems are exposed to ever-
increasing levels of environmental stress from a growing range of sources
(Feld et al., 2011; Friberg et al., 2011; Woodward et al., 2010a). The six
papers presented here, and those that will follow in Volumes 47 and 48,
provide just a glimpse of the scale of the task ahead, but they also offer
some glimmers of hope as to how we might take the necessary first steps
into this huge and largely uncharted territory.
Monitoring and assessment of medium- to long-term impacts of global
change on multispecies systems is needed across a wide range of
organisational levels: from molecules, to individuals, to entire ecosystems
(Purdy et al., 2010), and we need to understand the role of both ecological
and evolutionary drivers at appropriate timescales (Melian et al., 2011;
Moya-Laraño et al., 2012). Ideally, studies of entire multispecies
communities should span a wide range of organism sizes and trophic
levels (e.g. Hagen et al., 2012; Meerhoff et al., 2007, 2012; Mulder et al.,
2012; O’Gorman and Emmerson, 2010), as well as helping to align more
strategic multidisciplinary research to aid the longer term development of
the field as a whole (Woodward et al., 2011). The various topics
addressed here and in related volumes bridge several disciplinary gaps,
including (1) the effects of nutrients on biomass and production (Jeppesen
et al., 2012), (2) energy and material flows through ecosystems (Mulder
et al., 2011, 2012; Yvon-Durocher et al., 2010), (3) the ecological effects
of species richness and the roles of microbial organisms (Mulder et al.,
2012; Perkins et al., 2010; Ptacnik et al., 2010), (4) the role of feeding
behaviour in system dynamics and trophic controls (Jacob et al., 2011;
Layer et al., 2010, 2011; Mintenbeck et al., 2012), (5) the dynamics of
communities and links between different ecosystem types (Hagen et al.,
2012; Hladyz et al., 2011a,b; Layer et al., 2010), (6) the combined effects
Preface xxi
of body size and behaviour in determining the structure and dynamics of

food webs (Jacob et al., 2011; Mintenbeck et al., 2012; O’Gorman and
Emmerson, 2010), and (7) the impacts of external drivers on food web
dynamics and functioning (Mulder et al., 2012; Woodward et al., 2010a).
Several common threads link the different conceptual frameworks that
span these various topics, emphasising the importance of tackling
multispecies system studies with a variety of theoretical and empirical
approaches.
A MATTER OF TIME AND SPACE: TEMPORAL AND

SPATIAL SCALE AND LEVELS OF ORGANISATION
The impact of global change in multispecies systems is intimately con-
nected to the spatiotemporal scales of system variability. Climate change is
already affecting natural systems, as is clear from the ample data on shifts in
the seasonal timing of reproduction and migration, in body size and species’
distribution ranges (Peck et al., 2012; Visser, 2010). The spatial distribution
and impact of a species in an environment are a consequence of a combina-
tion of both intrinsic and extrinsic factors that govern its population dynam-
ics and how it interacts with others (Layer et al., 2010; Nakazawa et al., 2011;
Olesen et al., 2010; Riede et al., 2010). Intrinsic factors include dispersal,
growth, survival and reproduction, constrained by physiological and
morphological capabilities, whereas extrinsic factors include the spatial
and temporal variation in physicochemical conditions required for
populations to be viable (Layer et al., 2010, 2011; Mintenbeck et al.,
2012; Mulder et al., 2012), in addition to sufficient habitat availability
(Hagen et al., 2012; Ledger et al., 2012a,b).
Prey availability and predation risk are important determinants of habitat
use, but both vary across spatial (and temporal) scales. In multispecies
systems, consumer and resource distributions may covary at large spatial
scales but do not necessarily coincide at small spatial scales: in extreme cases,
opposite trends may even be evident (e.g. positive aggregative responses of
predators to prey in local patches, but negative correlations in their abun-
dance across habitats) (Hagen et al., 2012; Olesen et al., 2010). Rates of
growth, survival and reproductive success of species in multispecies
systems are intimately linked to spatial and/or temporal variability in the
composition and abundance of potential prey items. Within multispecies
systems, foraging theory can be developed as a useful framework for
describing changes in species behaviour in response to global stressors,
xxii Ute Jacob and Guy Woodward
and contributions here (e.g. Hagen et al., 2012) and in recent or

forthcoming volumes (e.g. Moya-Laraño et al., 2012; Olesen et al., 2010)
provide a foundation for pursuing these challenges in future research and
for coupling them more explicitly with metacommunity theory (Hagen
et al., 2012).
A QUESTION OF TRAITS
Functional traits of species and systems are important (Litchman et al.,
2007; Mulder et al., 2012; Perkins et al., 2010; Ptacnik et al., 2010; Reiss
et al., 2009) controls of many ecosystem processes—perhaps even more
so than taxonomic identity—yet our mechanistic understanding is still far
from complete (Jacob et al., 2011).
Here, Mulder et al. (2012) provide a collection of empirical examples
from aquatic and terrestrial ecosystems examining how biodiversity supports
ecosystem functioning, both within and across trophic levels. They also pro-
vide an in-depth evaluation of B–EF relationships that includes aspects of
taxonomic diversity, functional categorisation and metabolic scaling, as well
as suggesting rules for their appropriate use. This study complements several
others that have appeared in recent volumes (e.g. Perkins et al., 2010;
Ptacnik et al., 2010) and draws the conclusion that, while community
complexity and the abundance of organisms reflect functional diversity,
the influence of biodiversity (in terms of species richness) on community
stability and ecosystem functioning is less clear. This highlights the need
for a more mechanistic framework, based on functional traits that drive
community structure and ecosystem processes, for understanding how
altering species composition will affect community stability and the
provisioning of ecosystem services in response to global change (Palmer
and Febria, 2012).
To achieve this, a clear understanding of what the functional character-
istics really are is needed to make the appropriate choice of the relevant traits:
several papers in recent volumes have focused on body size (Arim et al.,
2011; Gilljam et al., 2011; Jacob et al., 2011; Nakazawa et al., 2011;
Perkins et al., 2010; Woodward et al., 2010a,b), whereas others have
revealed how other traits that may be correlated with size (dispersal
ability in fragmented habitats) or orthogonal to it (sociality, taxonomy)
also need to be taken into account (Hagen et al., 2012; Henri and van
Veen, 2011; Jacob et al., 2011; Ledger et al., 2012a,b; Meerhoff et al.,
2012; Moya-Laraño et al., 2012; Mulder et al., 2012). Developing a trait-
Preface xxiii
based framework that can incorporate these different functional properties

could provide a more unified platform for understanding and predicting
how multispecies systems will respond to the multiple drivers of global
change (Spooner and Vaughn, 2008). In essence, this re-emphasises the
need to view biodiversity as more than just species richness, and the use
of traits also forges an appealing intuitive link to how species interact
within ecological networks, providing a useful bridge between the
structural and functional attributes of multispecies systems.
Multispecies systems are complex but that does not necessarily mean they
are unpredictable. We know, for instance, that large species are especially
vulnerable to many drivers of global change (Jennings and Brander, 2010;
Perry et al., 2010; Raffaelli, 2004) and that these species have many
functional attributes linked to their autecology and synecology that
should also respond predictably (Ings et al., 2009; Woodward et al.,
2012). For instances, as the largest fishes are removed selectively by
overharvesting, the trophic height of the food web as a whole should
decline, just as is seen throughout the world’s fisheries (Ings et al., 2009;
Rossberg, 2012).
Detecting significant impacts and potential synergies among global
change drivers in complex multispecies systems is an important, but chal-
lenging, task. If the community structure is (relatively) simple, we may be
able to analyse the roles of different species relatively easily simply by deter-
mining how environmental impacts translate into species loss. However, as
most communities contain complex food webs in reality, it is far harder to
envisage the full range of responses. One approach to dealing with such
complexity is to focus on the functional traits of species, in order to identify
their main defining role within the system, rather than becoming too be-
holden to the Latin binomial, especially as many species are cryptic and/
or incompletely described in many systems, particularly in the Tropics
(Hagen et al., 2012; Jacob et al., 2011; Meerhoff et al., 2012; Mulder
et al., 2011; Purdy et al., 2010).
THE NEXT STEPS FORWARD . . .

Global change affects biodiversity and ecosystem functioning and will
ultimately lead to the emergence of novel ecological communities. While
the separate effects of the main drivers, such as climate change, habitat loss
and pollution, as well as species loss and gain, are becoming increasingly well
documented, still very little is known about their consequences when acting
xxiv Ute Jacob and Guy Woodward
in concert (Walther et al., 2002; Woodward et al., 2010a). Predicting the

combined effects of multiple and interacting drivers represents a
significant challenge and highlights where the next major advances need
to be made as a matter of urgency. We need to be able to identify the
critical gaps in our current knowledge and to gauge the extent to which
they might be addressed with existing data, or whether new primary
research is required. As time is short, we do not have the luxury of
always being able to wait for the empirical data to catch up with the
theoretical explorations of what the future might hold, so modelling is
certain to become increasingly important.
It is also essential to develop studies that can integrate applied and basic
research and empirical and theoretical approaches so that management re-
gimes in the “real world” can cope with the anticipated changes in future
biodiversity (Feld et al., 2011).
An essential prerequisite for sustaining our own species in the lifestyle to
which we have become accustomed in the twenty-first century into the future
is to ensure that natural systems continue to provide the services required for
human well-being. A mix of observation, experimentation, modelling and syn-
thesis that can be applied across a wide array of ecological communities is
needed to develop the necessary predictive frameworks (e.g. Rossberg,
2012). From the empirical perspective, we will need to employ a mixed ap-
proach that combines model systems with more extensive comparative
approaches, and there are encouraging signs that such studies are becoming
more commonplace. Much of this is largely fortuitous, as previously established
research programmes that were set up decades ago in a few model systems start
to bear often unexpected fruit, as long-term trends start to emerge (e.g.
Hildrew, 2009; Kratz et al., 2003; Lane, 1997; Layer et al., 2011). There is
also an active movement in contemporary ecology towards integrating
experiments, surveys and models within the same system, especially as
interdisciplinary, collaborative research becomes evermore common practice
(e.g. Layer et al., 2010, 2011; O’Gorman et al., 2012; Twomey et al., 2012).
In conclusion, it is clear that impacts of environmental stressors and
global change often cannot be predicted reliably from single-factor and
single-species studies because different drivers affect community structure
and functioning in different and potentially synergistic ways. To attain a
more complete understanding, we need to adopt a more integrated approach
that spans multiple organisational levels, disciplines and spatiotemporal scales
of study. The six papers compiled in this thematic volume, and also in the
two subsequent volumes, should help us move closer to achieving this goal.
Preface xxv
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Distributional (In)Congruence
of Biodiversity–Ecosystem
Functioning
Christian Mulder*,1, Alice Boit{, Shigeta Mori{, J. Arie Vonk},},
Scott D. Dyer||, Leslie Faggiano#,**, Stefan Geisen{{,
Angélica L. González{{, Michael Kaspari}},}}, Sandra Lavorel||||,
Pablo A. Marquet##,***, Axel G. Rossberg{{{,{{{, Robert W. Sterner}}},
Winfried Voigt}}}, Diana H. Wall||||||
*National Institute for Public Health and the Environment (RIVM), Bilthoven, The Netherlands
{
Department of Ecology and Ecosystem Modeling, Institute of Biochemistry and Biology, University of
Potsdam, Potsdam, Germany
{
Forestry and Forest Products Research Institute, Tsukuba, Japan
}
Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, The Netherlands
}
Institute for Water and Wetland Research, Radboud University Nijmegen, Nijmegen, The Netherlands
‖
Procter & Gamble, Cincinnati, Ohio, USA
#
Institute of Aquatic Ecology, Universitat de Girona, Girona, Spain
**Laboratoire Evolution et Diversité Biologique, Université Paul Sabatier, CNRS, Toulouse, France
{{
Department of Terrestrial Ecology, Institute of Zoology, University of Köln, Biozentrum Köln, Köln,
Germany
{{
Department of Zoology, University of British Columbia, Vancouver, British Columbia, Canada
}}
Department of Zoology, University of Oklahoma, Norman, Oklahoma, USA
}}
Smithsonian Tropical Research Institute, Balboa, Panama
‖‖
Laboratoire d’Ecologie Alpine, CNRS, Grenoble, France
##
Center for Advanced Studies in Ecology and Biodiversity, Institute of Ecology and Biodiversity, Pontificia
Universidad Catolica de Chile, Santiago, Chile
***The Santa Fe Institute, Santa Fe, New Mexico, USA
{{{
Centre for Environment, Fisheries and Aquaculture Science (Cefas), Lowestoft Laboratory, Suffolk,
United Kingdom
{{{
Medical Biology Centre, School of Biological Sciences, Queen’s University Belfast, Belfast, United Kingdom
}}}
Ecology, Evolution & Behavior, University of Minnesota, St. Paul, Minnesota, USA
}}}
Community Ecology Group, Institute of Ecology, Friedrich Schiller University, Jena, Germany
‖‖‖
Department of Biology & Natural Resource Ecology Laboratory (NREL), School of Global Environmental
Sustainability, Colorado State University, Fort Collins, Colorado, USA
1
Corresponding author: e-mail address: christian.mulder@rivm.nl
Contents
1. Introduction 3
1.1 Vexing drivers and responses 3
1.2 Contrasting dichotomies 5
1.3 Aims of our study 9
2. Scaling B–EF 11
2.1 Implications of scaling 11
2.2 Green world allometry 13
2.3 Allometry and management 15
Advances in Ecological Research, Volume 46 # 2012 Elsevier Ltd 1

ISSN 0065-2504 All rights reserved.
http://dx.doi.org/10.1016/B978-0-12-396992-7.00001-0
2 Christian Mulder et al.
3. Constraining B–EF 16
3.1 Allometry rules the world 16
3.2 How local biodiversity determines individual abundances at taxocene level 18
3.3 The extent to which scaling changes between taxocenes 24
4. Predicting B–EF 26
4.1 B–EF and functional redundancy in the blue world: Theoretical background 26
4.2 Inland water biodiversity: Effects of landscape complexity on B–EF 29
4.3 Inland water biodiversity: Vulnerability of B–EF across ecoregions 37
4.4 Population fluctuations at standardized taxonomical resolution: A virtual case
study 39
4.5 Superimposed disruption of fish biodiversity on cascading interactions 42
5. Conceptual Unification 44
5.1 Articulating B–EF in terrestrial ecosystems 44
5.2 Articulating B–EF in aquatic ecosystems 46
6. System-Driven B–EF 48
6.1 Elemental changes within one taxocene: Less is more 48
6.2 Elemental changes across taxocenes: Community mismatches 50
7. Coda 54
Acknowledgements 55
Appendix 56
References 72
Abstract
The majority of research on biodiversity–ecosystem functioning in laboratories has con-
centrated on a few traits, but there is increasing evidence from the field that functional
diversity controls ecosystem functioning more often than does species number. Given
the importance of traits as predictors of niche complementarity and community struc-
tures, we (1) examine how the diversity sensu lato of forest trees, freshwater fishes and
soil invertebrates might support ecosystem functioning and (2) discuss the relevance of
productive biota for monophyletic assemblages (taxocenes).
In terrestrial ecosystems, correlating traits to abiotic factors is complicated by the
appropriate choice of body-size distributions. Angiosperm and gymnosperm trees,
for example, show metabolic incongruences in their respiration rates despite their pro-
nounced macroecological scaling. Scaling heterotrophic organisms within their mono-
phyletic assemblages seems more difficult than scaling autotrophs: in contrast to the
generally observed decline of mass-specific metabolic rates with body mass within
metazoans, soil organisms such as protozoans show opposite mass-specific trends.
At the community level, the resource demand of metazoans shapes multitrophic
interactions. Hence, population densities and their food web relationships reflect func-
tional diversity, but the influence of biodiversity on stability and ecosystem functioning
remains less clear. We focused on fishes in 18 riverine food webs, where the ratio of
primary versus secondary extinctions (hereafter, ‘extinction partitioning’) summarizes
the responses of fish communities to primary species loss (deletions) and its conse-
quences. Based on extinction partitioning, our high-diversity food webs were just as
(or even more) vulnerable to extinctions as low-diversity food webs.
Distributional (In)Congruence of Biodiversity–Ecosystem Functioning 3
Our analysis allows us to assess consequences of the relocation or removal of fish

species and to help with decision-making in sustainable river management. The study
highlights that the topology of food webs (and not simply taxonomic diversity) plays a
greater role in stabilizing the food web and enhancing ecological services than is
currently acknowledged.
ABBREVIATIONS
B biomass
B–EF biodiversity–ecosystem functioning
C carbon content
C connectance of a food web or network
eNPP ecosystem’s Net Primary Productivity
FD functional diversity
L trophic links
m mass at individual level
M mass average at population level (site-specific)
M species-specific estimate of body-mass average
MIH More Individuals Hypothesis
N numerical abundance at population level
N nitrogen content
P phosphorus content
PD fraction of primary deletions (1 – #SD)
R metabolic rate at individual level
RSD robustness against SD
S number of species within one monophyletic taxocene (taxonomic diversity)
SD fraction of secondary deletions (1 – #PD)
All substances, in so far as they can be perceived in space at the same time, exist in
a state of complete reciprocity of action.
Immanuel Kant (1781) Kritik der reinen Vernunft: Dritte Analogie.
1. INTRODUCTION
1.1. Vexing drivers and responses

Despite scientific rationalism, too many generalizations and recent extrapo-
lations on the so-called sixth Great Extinction Event are widely supported
and spread by modern media (criticism on NGO’s statements and current
concerns already by Mann, 1991). On the one hand, the growing human
impact on Earth is beyond discussion and many scientists even assigned
the term Anthropocene to the present epoch (Crutzen, 2002; Estes et al.,
2011). On the other hand, forecasting global changes is hampered by the
lack of consensus on interactions among the causes (e.g. Sala et al., 2000), the
existence of overstating implications (e.g. ‘taxa committed to extinction’ by
Thomas et al. (2004a) are soon claimed as lost in many press releases) and
contradictory conclusions (e.g. Samanta et al., 2010 vs. Xu et al., 2011).
Too often, in the public opinion, biodiversity seems therefore to sound
vague despite of full awareness of resource exploitation and habitat loss.
Hence, a dangerous consequence that must be avoided is a possibly
growing cynicism and complacency about the current changes at
planetary scale as a whole, although the interest with which policy-
decision makers and stakeholders look to models is higher than ever.
Given that biodiversity on Earth is only superficially explored, functional
groupings used up to date have arisen from a pragmatic approach to catego-
rize biota into ecologically meaningful aggregates (Brussaard, 2012;
Kerkhoff et al., 2005; Loreau et al., 2001). For example, body size,
among other (frequently related) traits, is ultimately important in
determining interaction strengths between consumers and resources.
Moreover, organisms of different sizes can have very different effects on
ecosystem functioning (EF), both within and among species (Perkins
et al., 2010; Reiss et al., 2010, 2011). Size measurements can be carried
out at either the individual or the species level, might be used
comparatively across species, and have the power to become more
directly correlated with properties that influence the performance of
organisms and communities (Hodgson et al., 1999; Ledger et al., 2012;
McGill et al., 2006).
Life is a matter of scale: faunal dispersal over broad spatial scales favours
plasticity (Sultan and Spencer, 2002), in contrast to vascular plants, for which
adaptation is limited by seed dispersal mechanisms (Hagen et al., 2012;
Olesen et al., 2010). Differently sized plants with variable leaf N and P
contents may affect ongoing ecological processes, either actively, due to
their direct influence on decomposition efficiency, or passively, through
biomass production (Bradford et al., 2002; Fortunel et al., 2009; Garnier
et al., 2004; Reich et al., 2010). Further, plants change the amount and
composition of root exudates depending on life form (Du Rietz, 1931;
Raunkiaer, 1934; Walter, 1964) and nutrient status (Johnson, 2010;
Ladygina and Hedlund, 2010; Lipton et al., 1987; Lynch and Ho, 2005;
Richardson et al., 2009; Yoneyama et al., 2007).
Still, most researchers have not addressed the role of size as an effect trait
at the species level, but have instead preferred to address the response trait as
biomass at community level, as for many aboveground ecosystems with
different productivity (e.g. Hartnett and Wilson, 1999; Klironomos et al.,

2000; Wardle, 2002; Watkinson and Freckleton, 1997). Given the
correlation between response and effect traits, that is, the ‘response–effect
hypothesis’ (Lavorel and Garnier, 2002), the complexity and (mutual)
importance of such direct and indirect interactions among biodiversity,
EF and the environment is challenging (Bradford et al., 2002;
Lavorel et al., 2009; Zobel, 1997). A resulting niche complementarity is
in fact the product of not only species interactions but also a direct
consequence of combinations of traits (Flombaum and Sala, 2012).
Hence, many of these phenomena are interwoven and are commonly
merged together into ‘services’, like nutrient availability, soil structure,
water regulation, biological pest control and resilience (Millennium
Ecosystem Assessment, 2005).
Effects of dominant species at the ecosystem level (whether a certain
community composition is necessary to form and support a given ecosystem)
and the EF are two ‘linchpins’ which matter at several levels (Perrings et al.,
1992, 2011). Due to closely interrelated mechanisms, B–EF relationships
have been described at many operational levels in an attempt to forecast
effects of global change: although determinants of structural variability
across different operational levels are not fully understood yet, changes in
organismal, demographic and abundance responses might be predicted by
nutrient availability or disturbance (Caswell and Cohen, 1991; Elser and
Urabe, 1999; Lavorel et al., 1997; Sterner and Elser, 2002; Suding et al.,
2003; Tilman, 1988).
1.2. Contrasting dichotomies

EF depends on ‘dynamic relationships within species, among species and be-
tween species and their abiotic environment, as well as the physical and
chemical interactions within the environment’ (Millennium Ecosystem
Assessment, 2005; UNEP/Convention on Biodiversity, 2004; Wall,
2008). Quantifying EF in terms of biomass, productivity and size
structure within and among different ecosystems is important in ecology
as it can provide clues about the underlying processes that shape
communities. But how close to reality are the correlations between EF
and biodiversity? And why are so many research papers and their related
questions scale-specific? An excellent starting point would be Waide et al.
(1999), who performed an authoritative and extensive meta-analysis of
the correlations between biomass and/or production (both excellent
Linear response (%) Quadratic response (%)

80 75 70 65 60 55 50 45 40 35 30 25 20 15 10 5 5 10 15 20 25 30 35 40 45 50 55 60 65 70 75 80
Algae Algae
Direct correlation
U
-shaped
Inverse correlation U-shaped
Cormophytes Cormophytes
Direct correlation
U
-shaped
Terrestrial invertebrates Terrestrial invertebrates

Direct correlation
U
-shaped
Aquatic invertebrates Aquatic invertebrates

U
Direct correlation -shaped
Fishes Fishes
Direct correlation
U
-shaped
Herps Herps
Direct correlation
U
-shaped
Birds Birds
Direct correlation
U
-shaped
Mammals Mammals
Direct correlation -shaped
U
Figure 1 Meta-analysis of the biomass/production and biodiversity relationships pub-

lished between 1967 and 1996, modified from Waide et al. (1999). For each of these
groups of organisms, the amount of biomass–biodiversity studies was set equal to
100%: Trends in biomass as predicted by biodiversity (here, B–EF relationships) can
be either linear or quadratic, including unimodal and U-shaped distributions, and
can be lumped into different subunits (in grey). The horizontal sum of the black units
is always 100%, because the difference is the percentage of non-significant trends.
The vertical sum of the grey subunits is equal to the black unit just above them.
proxies to quantify EF) and biodiversity published between 1967 and 1996,
summarized in Fig. 1.
The relationships between biodiversity and primary productivity show
the extent to which, under different scales, most controlling processes differ
as well, because biodiversity is not merely a simple function of primary pro-
ductivity, but it may feed back onto it (Adler et al., 2011; Fridley, 2001;
Hooper et al., 2005; Loreau et al., 2001). In reality, experimental
communities in the field (e.g. Dukes et al., 2005; Menge and Field,
2007) and in micro- or mesocosms (e.g. Benton and Beckerman, 2005;
Hunting et al., 2012; Reiss et al., 2011) represent one assemblage of
randomly chosen species from a virtually available species pool (Huston,
1997; Naeem, 2008).
According to Lepš (2001), this can be a problem with the design of ex-
periments, as the responses to change determining the success of an exper-
imental community must be viewed with caution, due to either species that
avoid competitive exclusion under low productivity, or species adapted to

productive environments given the limited number of species able to com-
pete in high-nutrient environments. Regardless of the species pool and ex-
perimental design, if vascular plants (cormophytes) share a significant
response, they tend to have a bell-shaped (unimodal) biomass–biodiversity
relationship (cf. Adler et al., 2011; Fig. 1). In contrast, for algae, both bio-
mass/productivity proxies seem to have no linear response with increasing
biodiversity, and for herps, there is only evidence of direct linear correlations
with increasing diversity of amphibians and reptiles (Fig. 1).
Fishes are a powerful example for contrasting biomass–biodiversity cor-
relations: along a biodiversity gradient, does function respond linearly or
not? Considering that fishes are commonly overexploited (FAO, 2000) de-
spite their intrinsic capacity to respond to environmental changes, fish as-
semblages must be representative in their abiotic and biotic properties as
well as their faunal composition for a range of sites. The proxies for aquatic
and terrestrial invertebrates are even more contrasting, with direct correlates
with soil biodiversity less than three times more frequent than inverse cor-
relates (Fig. 1). If so, contrasting biomass–biodiversity relationships within
and between taxonomic groups might have clear implications for the
ecosystem.
During the same period of the extensive review by Waide and others,
Hector et al. (1999, 2002) published BIODEPTH, resulting in a flood of
B–EF studies showing robust linear trends on one side and strongly debated
statistical arguments on the validity of the experimental design on the other
(e.g. Cottingham et al., 2001; Huston et al., 2000). Few experimental
studies have since measured biodiversity and biomass production: in those
cases, discontinuous relations between biodiversity and productivity, rather
far from linearity, were shown (Boit et al., 2012; Roscher et al., 2008).
There is compelling evidence that process rates associated with animals
that influence ecosystem services vary with body size: small organisms vary
more rapidly in population density and behave differently from larger organ-
isms (Fenchel and Finlay, 1983; Huston and Wolverton, 2011; Sterner and
Elser, 2002), such as having a very different metabolic capacity per unit
biomass if an assemblage is comprised of many small versus a few large
individuals (Perkins et al., 2010). At individual and population levels,
plants exhibit contrasting responses to the animal framework of Table 1:
plants are mostly growing slowly in unfertile ecosystems (i.e. low eNPP),
although they may live longer. For animals, tradeoffs in physical,
biochemical and ecological constraints related to parental energy
Table 1 Predictions of ecologically and evolutionarily relevant properties for low and
high net primary production scenarios across organizational levels as defined by Huston
and Wolverton (2011); table modified (Michael Huston, personal communication) and
redrawn with permission from ESA
Low eNPP High eNPP
Culture, Small stature, short Large stature, tall
socioeconomics
Low per capita income High per capita income
Malnutrition, vitamin Good health, nutrition
deficiencies
Homes small, crowded Homes large, spacious
Low educational attainment High educational levels
Small social groups, Hierarchy social stratification
cooperation
Community Facilitation, mutualism Competition, aggression
common common
Small species predominate Large species dominant
High species evenness Low species evenness
High species richness Low species richness
Species ‘K’ traits predominate ‘r’ and ‘K’ traits present
Sensitive to mortality Robust to mortality
Locally rare Locally common
Small average size Large average size
Population Low emigration rate High emigration rate
Low biomass density High biomass density
Low population density High population density
Low rate of increase High rate of increase
Individual Poor health, strength Good health, strength
Low longevity High longevity
Few or small offspring Many or large offspring
Low adult size High adult size
Low growth rate High growth rate
Low birth mass High birth mass
Ubiquitous biogeochemical effects of nutrients and proteins on organisms support at ecosystem level an
elemental-affected net primary production (eNPP).
investment have been hypothesized to be responsible for many observed

body growth patterns and behavioural traits (e.g. Blomberg et al., 2003;
Bongers, 1999; Calder, 1984; Carbone et al., 2011; Guénard et al., 2011;
Hendriks and Mulder, 2008, 2012; Peters, 1983; Suding et al., 2003).
Many of these faunal attributes are mentioned in Table 1, such as
offspring number, dispersal rate, maximum lifespan and territory, and
vary predictably with the organism’s body size with respect to the species’
phylogenetic position (Guénard et al., 2011).
Body size remains a fundamental determinant of an organism’s ecology,
including territory and niche (Jenkins et al., 2007; Werner and Gilliam,
1984), and is one of the most-studied aspects of animal ecology (Blackburn
and Gaston, 1994; Isaac and Carbone, 2010). Therefore, we can
hypothesize that ‘body size’ might at least constrain the dispersal rate,
population density and ‘foraging’ of smaller organisms in a different way
from those of larger organisms (e.g. Castle et al., 2011; Finlay, 1998, 2002;
Foissner, 2006, 2008; Hagen et al., 2012; Mulder and Elser, 2009). And if
so, consistent relationships between bio(geo)chemistry and multitrophic
interactions will open exciting ways to assess EF (Friberg et al., 2011).
1.3. Aims of our study

While framing our questions on B–EF relationships is relatively straightfor-
ward, testing them is not. Biodiversity collectively refers to all aspects of bi-
otic diversity (Naeem et al., 1999) and its effects are believed to differ among
ecosystem types (Hooper et al., 2005; Schmid et al., 2009). To avoid possible
confusion, biodiversity will be used here for ‘biodiversity as a whole’, S
(species diversity) for taxonomic diversity and FD for functional diversity.
As Ghilarov addressed (2000: p. 410), any meaning of biodiversity for EF
is strictly dependent on the definitions of ecosystem types and EF; like
Ghilarov—and Lindeman (1942) before him—we adhere here to a
functional definition of the ecosystem, separated from the surrounding
‘environment’. For this purposes, we chose monophyletic ecological
assemblages (‘taxocenes’ sensu Hutchinson, 1978) as units to investigate
numerical abundance and species diversity relationships (Kaspari, 2001).
Productivity and species diversity are influenced by resource limitation and
nutrient supply (Allen et al., 2005; Brown et al., 2004; Hubbell, 2001;
Huston and Wolverton, 2009; Mulder et al., 2005a; Sterner and Elser,
2002). Hence, the total number of coexisting individual monophyletic
assemblages is hypothesized to reflect the ability to harvest and divide
energy within a single taxocene (Kaspari, 2001).
Previous attempts to compare different monophyletic assemblages with

each other show an unrecorded parallel among insect, bird and plant species
(Thomas et al., 2004b). In an attempt to foster a new mechanistic debate,
which is important for understanding EF (Chapin et al., 2000), we selected
three characteristic taxocenes from the plant and animal kingdoms as well:
vascular plants (seagrasses and forest trees), terrestrial invertebrates (soil nem-
atodes and social insects) and freshwater fishes. These three taxocenes are
representative of two terrestrial systems, the ‘green world’ (Polis, 1999)
and the ‘brown world’ (Allison, 2006), and one aquatic system, the ‘blue
world’ (Fig. 2). We also focus on two harsh soils systems, the Atacama Desert
with its hypolithic communities of underneath living phototrophs and the
Antarctic Dry Valleys with their extremely low biodiversity (Wall, 2008),
and two temperate, human-disturbed biota, the rivers of Ohio
(Burton et al., 2012), and agroecosystems across the Netherlands (Mulder
et al., 2011a–c).
We believe that our study has broad implications with respect to developing
more effective management of our biotic resources and consequently we shall:
Blue world
Ecological Metabolic
networks scaling
B–EF
Brown Green
world world
Biological
stoichio-
metry
Figure 2 Operational classification of the blue world (water compartment), the brown
world (belowground) and the green world (aboveground). The overlapping parts ad-
dress the kind of B–EF responses measured in this study for three independent
taxocenes (freshwater fishes, soil invertebrates and vascular plants). Photo credits: Scott
D. Dyer, Shigeta Mori and Winfried Voigt, respectively.
1. analyze biodiversity–productivity relationships in the framework of EF

to provide empirical evidence for allometric scaling in reference to eco-
logical stoichiometry,
2. relate the environmental abiotics to presence, mass and abundance of or-
ganisms within taxocenes, to assess the importance of species traits that
can be seen as stoichiometrically similar and
3. investigate the extent to which aquatic and terrestrial communities com-
posed of species that are stoichiometrically similar may differ from those
where species have wide differences in their elemental composition.
2. SCALING B–EF
2.1. Implications of scaling
The scaling of the rates of organismal functions with body size in commu-
nities or ecosystems is effectively addressed by allometry, a central—
although still somewhat controversial—feature of ecosystems. Allometric
scaling has been successfully used, among others, in macroecology
(e.g. Arim et al., 2011; Brown et al., 2004; Jacob et al., 2011;
Nakazawa et al., 2011; Savage et al., 2004; Storch et al., 2007; West
and Brown, 2004), ecological stoichiometry (Mulder and Elser, 2009),
the assessment of human-induced biomass exploitation by fishing
(Jennings and Blanchard, 2004; Jennings et al., 1999), the impact of
global warming on freshwater communities (Dossena et al., 2012;
Yvon-Durocher et al., 2010, 2011a) and even for the characterization
of fossil food webs (Dunne et al., 2008).
The ecological implications of scaling are great. Figure A1 shows that
allometric diversity–yield relationships between species mass and species
density (mass–abundance) can be translated into ecological processes trans-
cending discrete boundaries. The metabolic rate, in particular, can be easily
estimated by allometric scaling (Enquist et al., 1999; Ernest et al., 2003;
Mulder et al., 2005b), with the metabolic respiration rate per capita, R, as
function of the individual organismal body mass m:
R / m /4
3
½1
A notable example of such research beyond biogeographical boundaries
comes from a continental transect across Asia, where the field investigation
of tree species of different ages (from saplings up to giant trees) is possibly the
best physiological example of macroecological scaling (Fig. 3, recalculated from
Mori et al., 2010) in which respiration and fresh weight were determined for
4
Tree shoots
3 Shoots + roots
Log respiration mmol CO2 / tree / s (20 °C)
-1
-2
-3
-4
-5
-6
-6 -5 -4 -3 -2 -1 0 1 2 3 4 5
Log body mass (kg fresh weight)
Figure 3 Power laws at autecological scale: plant allometry is perfect for physiological
forecasting from saplings up to giant trees. Original data by S. Mori on 320 angiosperms
and 120 gymnosperms: all the respiration measurements were made at 20 C and sep-
arate scaling analyses for the aboveground part and the whole-tree mass are shown in
Fig. 4. Methods, locations and data are further described in Mori et al. (2010). These au-
thors show that a robust non-isometric scaling of respiration versus fresh weight occurs
across all pooled data along one continental transect across Asia, in contrast to previ-
ously reported shifts of angiosperms versus gymnosperms and saplings versus adult
trees reported in Reich et al. (2006) and Makarieva et al. (2008). The latter debate has
been addressed among others by Hedin (2006) and Enquist et al. (2007).
440 trees. The respiration and photosynthesis of plants are opposite and revers-
ible chemical reactions: plant respiration is closely related to translocation of
photosynthate, uptake of soil nutrients, N-assimilation, protein turnover,
resulting in biosynthesis of new biomass (Amthor, 2000), although considerable
discussion on the actual implications of respiration is ongoing (Thornley, 2011
and references therein). Plant size is also known to scale inversely with foliar
nutrient (N and P) contents (e.g. Elser et al., 2010). The complexity of these
physiological processes makes the scaling of production and metabolism of
(photo)autotrophs an important and rapidly growing area in the field of global
change biology, especially because of the temperature dependence of the met-
abolic rates involved (Yvon-Durocher et al., 2010, 2012).
2.2. Green world allometry

A mechanistic explanation which merges allometry with ecological stoichi-
ometry was hypothesized by Reich (2000): given that shaded species re-
stricted to the understory might allocate nitrogen differentially, the
saplings of tall trees can possibly allocate less nitrogen to photochemical
compounds—and proportionally more nitrogen to compounds directly in-
volved in CO2 fixation—than the saplings of shorter species. Different light
responses and nitrogen allocations are well-known for many plants, such as
the Solidago altissima forb investigated by Hirose and Werger (1987), lending
empirical support to this hypothesis.
A further comparison of the trend embedded in Fig. 3 at a finer scale
reveals that although the predicted respiration rates (mmol CO2/tree/s) for
small adults are rather comparable, the differences between gymnosperm
and angiosperm saplings and between their respective adults are remark-
able (Fig. 4). This occurs for both the aboveground masses and for the
whole trees and enables the investigation of the magnitude of carbon
uptake and loss through CO2 exchange (Fig. 4). Mori et al. (2010)
selected trees of various heights and ages spanning from the smallest to
the largest tree species in each forest to cover the full width of individual
respiration rates.
It must be noted that in any forest community, the depressed trees with a
small amount of leaves are not always the smallest tree species. Therefore,
some of the smallest trees have much of their adventitious branches adapted
to the environments in a forest canopy gap, and relatively high specific res-
piration rates per individual mass in contrast to dominant tree species.
Smaller trees determine the understory and play therefore an important role
in maintaining the sustainability of natural forests.
The observed differences between angiosperm and gymnosperm trees were
unexpected. Ernest et al. (2003) compared the plants with metazoan taxocenes
and found that the metabolic scalings for either ‘all plants’ or ‘all organisms’ (i.e.
387 plants and 360 metazoans pooled together) were 3/4 (absolute) and 1/4
(mass-specific). Metazoan mass-specific metabolic rates with body mass can
change (Glazier, 2005, 2010; Lovegrove, 2000; White, 2010), among others
due to different thermal responses across life stages (Forster et al., 2011),
whereas the protozoan metabolic rates can even be completely unrelated to
their body mass (Makarieva et al., 2008). Protozoan metabolism deviates
from allometric scaling rules: protist groups are widely scattered all over the
eukaryotic tree of life (Adl et al., 2005), differ fundamentally in morphology
4
Above ground
Log respiration mmol CO2 / shoot / s (20 °C)

3 Aboveground angiosperms
Aboveground gymnosperms
2 Fresh weight Respiration rate
Gymnosperm Angiosperm
1 (shoot kg) (mmol CO2) (mmol CO2) (adimensional)
0 0.0001 0.00011 0.00023 0.51

0.001 0.0008 0.0015 0.56
-1
0.01 0.006 0.009 0.62
-2 0.1 0.04 0.06 0.69
-3 1 0.3 0.4 0.76
log10(R) = 0.8108 log10(mang) - 0.4033 10 2.1 2.6 0.84
-4 2
R = 0.9671
100 15.3 16.5 0.93
-5 log10(R) = 0.8543 log10(mgym) - 0.5228 1000 109.7 106.9 1.03
2
R = 0.9806
10,000 784.15 691.67 1.13
-6
-6 -5 -4 -3 -2 -1 0 1 2 3 4 5
Log kg fresh weight (shoot, symbols filled)
Log respiration mmol CO2 / shoot + root / s (20 °C)
4
Above and below ground
3 Whole angiosperm trees
Whole gymnosperm trees
2 Fresh weight Gymnosperm Angiosperm Respiration rate
(whole-tree kg) (mmol CO2) (mmol CO2) (adimensional)
1
0.0001 0.00013 0.00022 0.57
0 0.001 0.0009 0.0015 0.62
-1 0.01 0.007 0.010 0.68
-2
0.1 0.05 0.06 0.75
1 0.3 0.4 0.82
-3 10 2.4 2.7 0.90
log10(R) = 0.8181 log10(mang) - 0.3836
-4 2
R = 0.9752 100 17.5 17.9 0.98
log10(R) = 0.8572 log10(mgym) - 0.4706
1000 126.2 117.7 1.07
-5 2
R = 0.9794 10,000 908.24 774.11 1.17
-6
-6 -5 -4 -3 -2 -1 0 1 2 3 4 5
Log kg fresh weight (whole tree, symbols filled)
Figure 4 Plant physiological efficiencies for gymnosperm and angiosperm trees as predicted by the scaling analyses for the aboveground part
(upper panel) and the whole-tree weight (lower panel). In the headers from left to right, the fresh weight of the plant (kg shoots), the tree respiration
at 20 C in mmol CO2 forecasted for gymnosperms and angiosperms, and the physiological efficiency rate between gymnosperm and angiosperm
trees of the same weight. The aboveground part of angiosperm saplings is about two times as efficient in the respiration rate as the shoot of gym-
nosperms of the same weight. For taller trees (> 100 kg fresh shoot weight), the switch in the aboveground respiration for (adult) gymnosperms
versus angiosperms is expected to occur around 600 kg fresh shoot weight. For the whole tree, angiosperm saplings remain much more efficient in
the respiration rate than gymnosperm saplings or small adults. Physiological efficiency switches for whole-tree respiration are expected to occur
between 100 and 1000 kg. Raw data from Shigeta Mori.
and can show contrasting relationships between metabolic rates and body mass
(Makarieva et al., 2008; Reiss et al., 2010).
According to the data of Makarieva et al. (2008), the metabolic rate of free-
living amoebae scales with their body mass to the 1/6 power, opposite to
non-amoeboid parasites (i.e. human endopathogenic protozoans) whose met-
abolic rate scales with body mass to the 1/6 power. One feature is that we might
speculate that non-amoeboid parasites are adapted to constant, high temper-
atures and downregulate gene expression or even lose genes as organelles, that
is, mitochondria, are commonly lost by such parasites (Cavalier-Smith, 1993;
Walker et al., 2011). Thus, we may need to take the external conditions, that is,
the host, into consideration to evaluate metabolic rates or generally treat
obligate parasites separately. Another feature is that in the case of free-living
protist groups, this might indicate that locomotion in viscous water is less
energy demanding for amoebae which move forward attached to surfaces
and do not swim actively like ciliates and flagellated organisms. Amoebae
were already regarded by Fenchel and Finlay (1983) to be metabolically
different from other protozoans. In summary, currently available data do
not enable the recognition of global allometric trends between and within
all taxocenes occurring in the green, brown or blue worlds.
2.3. Allometry and management

These allometric approaches to B–EF relationships have been applied in-
creasingly in the real-world setting of assessing human impacts on fisheries
and understanding the causes and consequences of the current global col-
lapses in fish stocks. On a local scale, the taxocene that describes the fish as-
semblage provides not only critical ecosystem processes but also goods and
services of huge economic value to humans. The historical correlations be-
tween density-dependent stocks, mesh size, fishing efforts and resulting
overexploitation are clearly evident (e.g. Cardinale and Svedang, 2004;
Jackson et al., 2001; Walters and Maguire, 1996) and have consequently
contributed to make allometry an accepted tool in fisheries and marine
sciences (Jennings, 2005; Shin et al., 2005; White et al., 2008; Section 4.5).
Despite the abundance of papers unravelling aspects of the blue world,
fewer examples are known for the green and the brown world. Although a
comparable correlation between canopy density and forest productivity also
seems to be a representative example of B–EF congruences, the data by Mori
et al. (2010) also show B–EF incongruences between the metabolic scaling
of angiosperms and gymnosperms (Fig. 4). Lumping the variability of
individual metabolism in a community (e.g. roughly comparing angio-

sperms with gymnosperms or evergreen trees with deciduous trees) sums
over the limits of forecasting (Fig. 3).
Our findings might have implications for different aspects of forest man-
agement: in conservation management, significant carbon stocks are protected
in living biomass, whereas in sequestration management, carbon is retained in
ecosystems by (increasing) reforestation. The decomposition process of con-
verting the organic carbon in the (surface or root) litter to CO2, making ni-
trogen available for plants without rhizobia, is influenced by the chemical
nature of carbon compounds (cellulose vs. lignin), by the kind of mycorrhi-
zal symbiosis, by root exudates and by the microbial pools (bacteria vs. fungi)
that support plant life and therefore ultimately underpin terrestrial EF
(Beerling and Woodward, 2001; Gams, 1992; Lynch and Whipps, 1990;
Moore et al., 2004).
Although the capability of plants to sequester carbon and emit CO2 to
the atmosphere varies across species (Bala et al., 2007), allometry has been
used scarcely to forecast or manage global changes (Fahey et al., 2010).
Size-related allometry provides dynamic tools for wild and domestic popu-
lation management, such as in the framework of restoration ecology, reduc-
ing carbon footprints and implementing activities to minimize deforestation
effects. Despite many countries focusing on conservation (e.g. planted trees
must belong to native species) or thinning wood, a sustainable agroforestry
management should avoid the current large-scale recommendation of gym-
nosperm trees (such as in United Kingdom, see www.direct.gov.uk/
thebigtreeplant, and in the United States, see http://apps.fs.fed.us/fido) be-
cause the different capabilities of gymnosperm and angiosperm adults to emit
CO2. Such considerations will surely demand more attention during the
planning of afforestation projects in the near future, especially given the in-
creasing socioeconomic momentum behind developing low-carbon-based
economies.
3. CONSTRAINING B–EF
3.1. Allometry rules the world
There is a need to investigate B–EF to gain understanding of the biological
and ecological factors underpinning sensitivities and traits of species in the
context of environmental stressors. In the previous sections, we show the
extent to what EF may become recognizable with macroecological ap-
proaches such as allometric scaling. Allometry is a suitable method to assess
the emergent characteristics of large data sets of organisms (Jonsson et al.,

2005; Marquet et al., 2005). According to Brown et al. (2004) and
Marquet et al. (2004), the fundamental rules of chemistry, physics and
biology provide the means to link individual organisms and their populations
to ecosystems and their ecological processes. However, although ‘it is clear
that scaling relationships hold best when examining patterns across a wide
spectrum of body sizes’ (Tilman et al. (2004): p. 1798), Brown and Gillooly
(2003) show that separate taxocenes derived from small data sets exhibit
biomass and mass–abundance scaling relationships that can be opposite from
the scaling relationships for all data sets together (Cohen et al., 2003). These
divergent relationships raise the question about predictability of species
sensitivity to stoichiometrically driven processes, even within comparable
size classes. For instance, certain taxa sharing comparable sizes may occupy
the most extreme trophic positions not only in a food web but even within
a loop, as in the case of viruses as top predators (despite their viral host
specificity) and bacteria as basal producers (e.g. Thingstad, 2000). Therefore,
it seems difficult to always extrapolate (opposite) results to a wider context,
although similarities in the response of phyla and biota become more evident
as soon as studies are addressed across scales.
Some, but not all, organisms can be easily identified at species level and a
comparable methodology does not per se imply equivalent taxonomic reso-
lution: microbial taxa, which drive so many ecosystem processes, remain a
particular challenge in this respect (Mulder et al., 2005a,b, 2009; Purdy et al.,
2010; Reuman et al., 2009). Regardless of their Latin binomial, all taxa
within one community can be modelled using either the unbinned body
mass (size) versus numerical abundance scaling or the binned biomass-size
spectrum. Successful examples on large-scale investigations come from
the blue world (Clarke and Johnston, 1999; Cohen et al., 2003; Killen
et al., 2010; Pope et al., 1994, 2006), focusing on traits for behavioural
adaptation (like in the case of suspension feeders: Goldbogen et al., 2012;
Jeschke et al., 2004; Jrgensen, 1966). Investigations on whales in
particular show extreme trophic positions in pelagic ecosystems, because
the huge baleens are not only able to feed on very small prey (Goldbogen
et al., 2012; Jacob et al., 2011), in contrast to toothed whales and teleosts,
but are specialized to feed on patchy resources. Moreover, trophic levels
do not imply a discrete body size (Borgmann, 1987), for although sharing
the same trophic level across a wide size distribution, phytoplankton
belonging to smaller size classes may achieve faster nitrogen uptake rates
than phytoplankton belonging to large size classes (Hein et al., 1995).
This is in contrast to the nitrogen uptake by zooplankton, whose smaller

individuals are forced to feed on algae only and whose larger individuals
can feed on both phytoplankton and zooplankton (Boit et al., 2012; Fry
and Quiñones, 1994; Ptacnik et al., 2010). Body size is thus a
fundamental trait for both autotrophs and heterotrophs, as a taxon
occupies in a size-based model a much more defined position than it does
in a trophic level model’ (Cohen, 1994; Cousins, 1980).
Body size can also greatly influence ecological interactions among terres-
trial organisms, although perhaps less obviously so than in the blue world,
with important consequences at the community and ecosystem level
(Yvon-Durocher et al., 2011b). The metabolic scaling of a given organism
(Calder, 1984; Damuth, 1981, 1991; Peters, 1983) is one of the best
examples of B–EF because functional scaling is species-independent (i.e.
unrelated to taxonomic diversity). Across species and within one or more
taxocenes, many physiological models may hold. Figure 5 shows that
pollinating insects (here, some extremely diverse bees, wasps, butterflies
and moths) can cover the entire allometric range of reported
measurements. The metabolic rate (R) of all insects (data recomputed
from the publicly available data of Chown et al., 2007) scales with insect
mass to the 0.87 (0.02 SE) power, but different metabolic scaling
exponents are recognizable within finer taxonomic groupings. Scaling
with mass to the 0.78 (0.06) and the 0.72 (0.03) power, respectively,
hymenopterans and coleopterans are the groupings closest to the scaling
exponent for the metabolic rate for all insects. In the upper part of
the scatter-plot of Fig. 5, the metabolic rates of lepidopterans and
orthopterans scale to the 0.67 ( 0.06) and the 0.60 ( 0.09) power,
respectively (much lower than the isopterans, which scale isometrically
with mass to the 1.04 (0.18) power). Some dipterans, hemipterans and
coleopterans (two genera of Curculionidae) have the lowest metabolic
rate among all insects. Given the ubiquity of insects in freshwater
ecosystems, their different allometric scaling must have implications for
the blue world as well and should be addressed in the future.
3.2. How local biodiversity determines individual abundances

at taxocene level
The number of species is believed to be particularly critical for B–EF in environ-
ments with low biodiversity, where there is less scope for redundancy to be
manifested (i.e. 1–10 species; Wall, 2007). For protozoa and microorganisms,
5
Other insects metabolic rate
Isoptera metabolic rate
Hymenoptera metabolic rate
4 Coleoptera metabolic rate
Orthoptera metabolic rate
Insect metabolic rate (log mW)
Lepidoptera metabolic rate

3
-1
-5 -4 -3 -2 -1 0 1 2
Insect weight (log mg)
Figure 5 Power laws at synecological scale: allometry is suitable for functional
forecasting of brown food web invertebrates such as insects. All eusocial insects like
size-polymorphic colony ants (Hymenoptera) and termites (Isoptera) are additionally
marked by one cross. Raw data from Chown et al. (2007, their Supplementary Material);
these authors converted different metabolic rates from scientific literature to micro-
watts assuming Q10 ¼ 2.0 at 25 C. Values for the scaling exponents vary among groups
and fall approximately between 2/3 and 1.
rare species are likely to compose the majority of species within a habitat (Dawson
and Hagen, 2009; Finlay, 1998). Less abundant microorganisms might have
pronounced bottom-up effects, as shown for several bacterial species under
lab conditions (Höppener-Ogawa et al., 2009). This holds for soil
invertebrates as well: in the McMurdo Dry Valleys of Antarctica, there may
be three to five (or even fewer) nematode species (Moorhead et al., 2002;
Treonis et al., 1999, 2000). However, the numerical abundances of
nematodes in pristine Antarctica can be comparable to those of temperate
agroecosystems (Fig. 6), in apparent contradiction to the More Individuals
Hypothesis (MIH), as originally defined by Srivastava and Lawton (1998),
who related the higher biodiversity of productive locations to the ability of such
sites to support large populations of each species. However, although the most
A B
Figure 6 What do the extreme desert of the Taylor Valley in Antarctica and one recov-
ered sea clay in the Netherlands have in common? One soil sample might contain an
almost equal abundance of soil nematodes, but with greatly contrasting numbers of
species. Photo credits: Diana H. Wall/Emily Stone (A) and Christian Mulder (B).
productive sites of that study (physically isolated water-filled microhabitats such as

tree holes; see further Hagen et al., 2012) contained more species (Srivastava and
Lawton, 1998), this was not a matter of more individuals, as the increase in species
richness with productivity occurred only when the energy amount was reduced.
Assuming that the opposite holds as well (the fewer the species, the lower
the total abundance), smaller populations under low productivity are likely
to be prone to extinction. In that case, the polar deserts are a unique excep-
tion, because they do not only support fewer species, but exhibit large
populations with far more individuals (Wall, 2007, 2008). The low
human-induced disturbance in most deserts makes such environments
attractive to assess the ecosystem responses to climate and therefore, other
drylands received more attention as well. Recently, Maestre et al. (2012)
clearly show that sustainability and multifunctionality (defined, among
others, as the ecosystems’ ability to maintain productivity, to support
carbon storage and to buildup nutrient pools) are positively related to
species richness. Deserts like those investigated by Maestre et al. (2012)
and the Antarctic Dry Valleys are most valuable to test the MIH because
drylands are less affected by sampling effects and patchiness, in contrast to
fragmented landscapes such as the moss carpets of Gonzalez et al. (1998).
Deserts can therefore reveal the key function (if any) of biodiversity sensu
lato under environmental stress.
To test the MIH model of Srivastava and Lawton (1998), we analyzed

the nematofauna from 200 agroecosystems with different habitat fertility
(Mulder and Vonk, 2011), that is, productivity proxies: in contrast to the
first study, where the authors used debris, we used primary nutrients to char-
acterize productivity. Being the Shannon-Wiener index function of the
(number of) species and given that higher values indicate even species dis-
tribution, Fig. A2 shows a hump-shaped relationship for both the exponen-
tial Shannon index and the taxonomic diversity of nematodes. Soil fertility
(i.e. resource supply) and nematode species richness seem there to be
interdependent (a classical B–EF example), indirectly supporting the histor-
ical paradigm that productivity drives species richness in contrast to the con-
temporary view that species richness drives productivity (Cardinale et al.,
2009; Gross and Cardinale, 2007). However, such a set of variables might
have a predictive power that dynamically changes in space (e.g. Hurlbert
and Jetz, 2010; Huston, 1994, 1997; Loreau and Hector, 2001), possibly
due to sampling bias or species competition, and in time (e.g. Kaspari
(2005) for temperature and Yee and Juliano (2007) for phenology).
Spatial scaling predicts a positive decelerating relationship between
abundance and species richness in a way comparable to the MIH: in the sam-
pling hypothesis, for a given species pool, a tropical plot should per se contain
more species than a low-productivity boreal plot. Kaspari et al. (2003) tested
this by randomly sampling simulated m2 plots with 1, 2, . . . n individuals
from the measured species pool for a site and compared that curve with those
observed. Where species richness versus total abundance relationships is pre-
dictable, it is at such a large aggregation that abundance reflects immigration
and/or extinction processes, an intriguing topic when considering that over
100 ant species can be found in 100 m2 of forest (Kaspari et al., 2001).
To test the extent to which EF increases with biodiversity, we plotted
several communities of invertebrates, from ants in pristine rainforests and
temperate forests up to nematodes and non-flying arthropods in deserts in
the southern hemisphere. All numerical abundances in Fig. 7 were
converted to densities per m2. Assuming the N of the entire population
within one taxocene represents a proxy for local resource availability, the
taxonomic diversity within one taxocene (e.g. the number of arthropod spe-
cies) scales directly with the abundance of all individuals (e.g. all the arthro-
pods of a given location as in Mulder et al., 2005a). All significant
species–density relationships of Table 2 follow power laws with exponents
smaller than ½ (i.e. the total species diversity within one taxocene increases
monotonically with abundance N), whereas density–species relationships
1,000,000
Invertebrate abundance (counts/m2)
10,000
100
Temperate soil microarthropods

Temperate soil enchytraeids
Temperate soil nematodes
Temperate litter nematodes
Antarctic desert nematodes
Total colony ants in leaf litter
Total colony ants in canopy
Mediterranean macroarthropods
Chilean desert macroarthropods
1
1 2 4 8 16 32 64 128 256
Invertebrate biodiversity (species density)
Figure 7 Direct B–EF correlations between species density (biodiversity) and total
abundance of individuals are expected to be widespread in comparable plots. Ants data
downloadable from Weiser et al. (2011); polar nematofauna from the Taylor Valley,
Antarctica, as in Courtright et al. (2001: their Table III) and Barrett et al. (2006: their
Table IV); temperate nematofauna downloadable from Mulder and Elser (2009) and Mul-
der and Vonk (2011). Macroarthropods from the coastal zone of the Atacama Desert,
Chile, were described in González et al. (2011); temperate soil microarthropods—mites
and collembolans—described in Mulder et al. (2005a); Dutch data on soil enchytraeids
from grasslands, heathlands and forests are novel; data on the litter nematofauna from
pine forests in the Netherlands and on the litter macroarthropods from a Mediterranean
beech forest in Italy are unpublished (C. Mulder and G. Mancinelli, respectively). Please
note the two logarithmic scales, being different bases (2 and 10) used.
follow power laws with exponents larger than 1 (i.e. the total abundance
within one taxocene increases with species diversity S, cf. Fig. 7).
All macroarthropods in Fig. 7 had R2 ¼ 0.66 (P < 0.00001), rejecting the
null hypothesis of no correlation between density N and diversity S. With
different combinations, including or excluding soil and litter invertebrates,
respectively, the results for the taxocenes are given in Table 2, along with the
regression lines of density as function of biodiversity and vice versa. Assum-
ing that resource availability within a sampling area is homogeneous, differ-
ent distributions become recognizable, irrespective of environmental
conditions: smaller animals belonging to the micro- and the mesofauna
Table 2 Scaling at different aggregation levels of the total density N as function of biodiversity S and vice versa for the invertebrates shown in Fig. 7
ID Faunal taxocenes Environment types Plots N scales to S S scales to N Pearson's r Variance
explained (%)
A Microfauna Soil and litter 142 2.24 0.17 0.25 0.02 0.742*** 55.1
A1 Free-living soil nematodes Soil 120 1.70 0.26 0.16 0.02 0.521*** 27.1
A2 Moss-inhabiting nematodes Litter 22 3.15 0.34 0.26 0.03 0.901*** 81.2
B Mesofauna Soil 246 1.98 0.12 0.27 0.02 0.733*** 53.7
B1 Mites and other microarthropods Soil 146 1.24 0.13 0.32 0.03 0.635*** 40.3
B2 Enchytraeids Soil 100 0.21 0.16 0.09 0.06 0.136 <2
C Macrofauna Litter and canopy 259 1.42 0.06 0.46 0.02 0.809*** 65.5
C1 Litter macroarthropods Litter 225 1.40 0.06 0.49 0.02 0.831*** 69.2
C2 Canopy macroarthropods Canopy 34 1.26 0.24 0.37 0.07 0.680*** 46.3
Partial aggregation
A þ B2 Enchytraeids þ nematodes Soil and litter 242 2.18 0.14 0.23 0.01 0.704*** 49.6
A1 þ B Soil micro þ mesofauna Soil 366 2.04 0.10 0.25 0.01 0.721*** 52.0
B1 þ C Micro þ Macroarthropods Soil, litter and 405 1.66 0.13 0.17 0.01 0.529*** 28.0
canopy
Complete aggregation
A þ B þ C All taxocenes together Soil, litter and 647 1.48 0.11 0.15 0.01 0.472*** 22.3
canopy
N and S values were log10-transformed to measure strength and direction of their linear dependence by the Pearson’s correlation coefficient and the standard error. Such base-10 log–log
linear regressions can be easily transformed in power laws. Besides enchytraeids (P ¼ 0.179, implying a random, non-linear relationship), all these linear relationships were significant:
***(P < 0.00001). Note the steepness increase in abundance–biodiversity relationships from the larger-sized macroarthropods (here: colony ants under pristine conditions) down to the
microarthropods (mites and collembolans) and nematodes.
(like nematodes, enchytraeids, mites and collembolans) clearly have a much

higher average density per species than is true for larger macroarthropods
(ants, beetles, etc.). Although taxocenes showed significant positive corre-
lations between biodiversity and total abundance, enchytraeids showed
no significant trend (Table 2).
3.3. The extent to which scaling changes between taxocenes

The way in which the correlation between density N and number of species
S changed between taxocenes may largely be interpreted as secondary
tradeoffs (demographic responses to abiotic or biotic factors sensu Suding
et al., 2003). In 2006, Meehan classified the occurring taxa in his brown
world study into two broad guilds: ‘Grazers’, including soil nematodes, orib-
atid mites, collembolans and enchytraeids, and ‘Carnivores’, including
spiders, ants, chilopods and non-oribatid mites (these in apparent contrast
to freshwater literature, where grazers typically mean consumers of algae
and carnivores do not per se imply only piscivorous fishes). Notwithstanding
the difference of more than five orders of magnitude in the total faunal
density N (Fig. 7), for differently sized invertebrates the slopes of the
density–biodiversity regression lines were 1.42, 1.98 and 2.24 for litter
and soil macrofauna, mesofauna and microfauna, respectively (Table 2).
The exclusion of litter macroinvertebrates from our log(N) on log(S)
analysis makes the slope of the regression line steeper than lumping all in-
vertebrates together. This was expected, given that invertebrates using dif-
ferent resources (i.e. different fractions of energy supply, as in the case of
litter vs. canopy arthropods), collectively deplete energy more effectively
(Kaspari and Weiser, 2012). Hence, scaling to higher levels of aggregation
may track the ecosystem’s productivity (eNPP) more accurately (Kaspari and
Weiser, 2012). Scaling varied markedly between taxocenes, from the nu-
merical abundance of Neotropical canopy ants (highest eNPP), which scale
to the 5/4 power of (high) species diversity, up to the abundance of Antarctic
nematodes (lowest eNPP), which scale to almost the 7/2 power to their (low)
species diversity (Table 2).
Conversely, the log(S) on log(N) functions show a sharper increase
in steepness, varying from 0.25 to 0.27, and finally 0.46 for macrofauna,
mesofauna and microfauna, respectively. The coefficients of variation
(CVs ¼ 100 SD/degree average) for diversity S, as predicted by
density N, were higher than for density N as predicted by diversity
S (32.7% vs. 9.4%, respectively). Again, the power scaling differs from the
species diversity of litter nematodes, which scales to the 1/4 power to their
numerical abundance, up to the species diversity of litter arthropods, which
scales to the ½ power to their numerical abundance (Table 2). This reflects
an antagonism between belowground ‘Grazers’ and ‘Carnivores’, as the bio-
diversity of the entire ‘Grazer’ group scales to the 1/4 power of the total group
and the biodiversity of the entire ‘Carnivores’ group scales to ½ power of
the total group (Section 3.2).
Our results reflected those from other macroecological studies. Marquet
et al. (2005) found linearity of log-transformed total number of species S ver-
sus log-transformed mass average M: for South American mammals, their
log(S) on log(M) slope was close to 3/4. If we assume an isometric
mass–abundance scaling (a log(M) on log(N) regression slope equal
to 1, implying a constant biomass across populations), then N / M 1
(Cohen et al., 2003; Mulder et al., 2005b; Woodward et al., 2005a). In
Table 2, however, all soil invertebrates belonging to micro- and
mesofauna (nematodes, enchytraeids, mites and collembolans) share
S ¼ N0.25. If we merge these two equations together, we get for our soil
invertebrates
S¼N 0:25 ¼M 0:75

0:251 ¼M ½2
as expected from general metabolic scaling and macroecological theory
(Marquet et al., 2005; Storch et al., 2007; Wardle, 2006) and as
empirically supported by randomly chosen assemblages of soil nematodes
(Mulder and Vonk, 2011).
There are a few exceptions to this law (Eq. 2) in soil food webs, one of
which is the enchytraeids, which occupy only one trophic level (this
taxocene comprises strictly peripheral consumers of microbial resources).
In high productivity grasslands, soil microbivores like enchytraeids seem
to be the most sensitive to density-dependent regulation according to clas-
sical theory (Lack, 1954), but the relationship between the species diversity
and density of enchytraeids is the only non-significant correlation in Fig. 7.
Already in 1982, Standen recognized a certain tendency for sites with few
enchytraeid species to have high abundances (Standen, 1982), while sites
with many enchytraeid species rarely achieve high abundances (see also
Standen, 1980). The possibility that this ecologically important size-scaled
taxocene is also stoichiometrically different from others (like soil nematodes)
merits further investigation in the future.
4. PREDICTING B–EF
4.1. B–EF and functional redundancy in the blue world:
Theoretical background
Generalist feeding strategies and omnivory are well-known in the food web
literature (e.g. Gilljam et al., 2011; Woodward et al., 2010a). Therefore, a
quantification of the degree of redundancy within food webs, either as
interspecific or intraspecific (if at different life stages) differences in
trophic position and diet, is crucial for B–EF modelling. In contrast to
empirical studies, where complexity provides according to Polis (1998)
‘an interwoven matrix that holds . . . a community together’, few studies
have really addressed the role of the redundancy within a predator–prey
matrix (Reiss et al., 2009). The assignment to a specific guild (trait) is
important because it determines the amount (and vertical direction) of
possible links. For the classification of freshwater fish species, we followed
Goldstein and Simon (1999) and Goldstein and Meador (2004). Fish
species are good indicators of freshwater ecosystems health (e.g. Simon,
1999) and cover many feeding types (Attrill and Depledge, 1997). We
assigned fishes to five main feeding guilds: planktivore, detritivore,
invertivore, herbivore and carnivore sensu stricto (Table 3).
Assuming that no species is isolated and that all species are part of one
network with more subunits, then possible trophic links depict
consumer–resource interactions within the fish assemblages (Table 4 shows
empirically validated trophic links as recorded in current literature). After
Winemiller (1989), Martinez (1992) and Dunne et al. (2002, 2004),
interaction richness is defined as the trophic links L per species S, also
referred to as link density, and by connectance C. If both interspecific
and intraspecific effects are considered, C is defined as
L
C¼ ½3
S2
and if intraspecific effects are not considered, that is, the realized fraction of
all pair-wise interactions, besides cannibalism, as
L
C¼ ½4
½S ðS 1Þ
C as defined in Eq. (3) is used more frequently, and termed ‘directed con-
nectance’ (Beckerman et al., 2006; Ebenman and Jonsson, 2005; Martinez,
Table 3 Lessons from stress ecology. Abiotic predictors are known to affect the
occurrence of fish species (e.g. Hawkins, 2006; Hendrixson et al., 2007; Posthuma and De
Zwart, 2006), albeit fish traits are influenced as well, as expected by the relevant
properties across taxonomical and organizational levels from Table 1 (Huston and
Wolverton, 2011; but see Sterner and Elser, 2002). The fish traits at population level are
based on species assignment according to Goldstein and Meador (2004); traits at
individual level are based on empirical data across the State of Ohio
Fish traits Predictors

0 20 40 60 80 100
Small bodied
Habitat
Medium bodied Individual size
Examples: Drainage; channel; ecoregion
Large bodied
0 20 40 60 80 100 Toxicity
Broadcaster
Examples: Pesticides; metals; oestrogen
Simple-nester
Reproduction
Complex-nester Chemistry
behaviour
Migratory
Species
Examples: pH; hardness; dissolved oxygen

0 20 40 60 80 100
Planktivore
Detritivore Human impact
Invertivore Feeding diet Examples: Urbanization; rural intensity
Herbivore
Carnivore
1991). The ‘link density’ is also known as linkage density (Pimm et al., 1991;
Winemiller 1989, but see the original definition in Briand, 1985).
To avoid confounding C of different food webs by differences in sam-
pling methods, we focused in the next section on a consistent methodology
(Havens, 1992; Martinez, 1993; Romanuk et al., 2009). Rather than
computing the link density as the number of realized trophic interactions
per locally occurring species, we chose an adapted taxocene-specific web
connectance (hereafter, Ct as in Fig. A3), where the proportion of all
trophic links between fish species (i.e. who eats whom but not who eats
what) that are realized in one fish assemblage as derived from the matrix
in Table 4. Ct reflects either a dominance of generalists (high Ct values:
Table 4 Predator–prey matrix showing the dominant freshwater fish species occurring
in 18 rivers of Ohio, horizontally and vertically ranked according their average fresh
weight. Rows as resources, columns as consumers, black cells the realized trophic links
the largest consumer (predator) is plotted upper left of the table, the smallest consumer
(Etheostoma nigrum feeds on eggs of other fishes) is plotted bottom right. More details
in Table A1
Percopsis omiscomaycus
Semotilus atromaculatus
Pomoxis nigromaculatus
Micropterus punctulatus
Etheostoma caeruleum
Micropterus dolomieux
Micropterus salmoides
Aplodinotus grunniens
Etheostoma flabellare
Pimephales promelas
Nocomis micropogon
Ambloplites rupestris
Cyprinella spiloptera
Notropis stramineus
Pimephales notatus
Etheostoma nigrum
Carpiodes cyprinus
Ictalurus punctatus
Lepomis cyanellus
Pomoxis annularis
Lepomis gibbosus
Percina caprodes
Percina maculata
Fundulus notatus
Esox americanus
Pylodictis olivaris
Perca flavescens
Lepomis gulosus
Ameiurus natalis
Noturus flavus
Predators
Cottus bairdii
Umbra limi
Preys
Pylodictis olivaris 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Moxostoma anisurum 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Aplodinotus grunniens 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Ictalurus punctatus 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Carpiodes cyprinus 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Moxostoma breviceps 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Moxostoma duquesnei 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Moxostoma erythrurum 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Minytrema melanops 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Micropterus dolomieux 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Pomoxis nigromaculatus 1 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Pomoxis annularis 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Dorosoma cepedianum 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Hypentelium nigricans 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Ameiurus natalis 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Micropterus punctulatus 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Catostomus commersonii 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Micropterus salmoides 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Ambloplites rupestris 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Perca flavescens 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Esox americanus 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Lepomis gulosus 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Nocomis micropogon 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Lepomis gibbosus 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Noturus flavus 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Lepomis macrochirus 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Lepomis cyanellus 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Lepomis megalotis 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Semotilus atromaculatus 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Percina caprodes 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0
Notemigonus crysoleucas 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0
Luxilus cornutus 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0
Luxilus chrysocephalus 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0
Lepomis humilis 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0
Lampetra aepyptera 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0
Percopsis omiscomaycus 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0 0
Umbra limi 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0 0 0
Campostoma anomalum 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0 0
Cottus bairdii 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0 0
Clinostomus elongatus 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0
Phenacobius mirabilis 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0
Notropis photogenis 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0
Percina maculata 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0 0
Cyprinella spiloptera 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0
Etheostoma blennioides 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0
Hybopsis amblops 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0
Pimephales notatus 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0 0
Notropis atherinoides 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0
Lythrurus umbratilis 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0
Notropis buccatus 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0
Lythrurus fasciolaris 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0
Pimephales promelas 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0 0
Phoxinus erythrogaster 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0
Fundulus notatus 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0 0
Notropis stramineus 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0 0
Labidesthes sicculus 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0
Etheostoma flabellare 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0 0
Notropis volucellus 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0
Etheostoma caeruleum 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 0
Etheostoma zonale 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0
Etheostoma spectabile 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0
Etheostoma nigrum 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0
omnivory and piscivory dominate) or a skew towards specialists (low Ct

values: high sensitivity to environmental stress and low resilience).
The definition of species categories in a food web determines the inter-
actions (these two issues are mutually dependent for Cousins, 1996: p. 244)
and static food webs use aggregate attributes like connectance to predict
other aggregate attributes, such as the proportion of omnivores (Loreau,
2010: p. 56). However, based on our empirical knowledge of both
species-related traits and size-related guilds within the Pisces monophyletic

taxocene, the Ct proportion of all links is suggested to reflect the dominance
of piscivory without requiring a more systematic data structure.
Hence, being unrelated to other compartments or taxonomical groups,
Ct values indirectly represent the mutual fish behaviour within one taxocene
(Fig. A3), analogous to intraguild predation, which is a common feature
of many food webs, especially in the blue world (Woodward et al., 2010b).
4.2. Inland water biodiversity: Effects of landscape

complexity on B–EF
4.2.1 Streams and ecoregions
Fishes are mobile and useful to assess large-scale (and long-term) effects be-
cause many species cover a wide area during their lifespan. The taxonomy of
fish is well defined, reflecting their importance as a food resource. Three
American Midwestern ecoregions presenting a comparable number of sam-
pling sites were selected for a pilot study on Ohio fish assemblages: Eastern
Corn Belt Plains, Erie Drift Plain and Western Allegheny Plateau (Fig. A4).
These North-American regional communities were used to quantify and
compare the variation in fish body mass and the properties of individuals,
populations and assemblages across ecoregions.
An ecoregion is defined here as a unit of land that is homogenous with
respect to multiple landscape characteristics such as geology, soil character-
istics, natural vegetation and climate (after Wagner et al., 2007). The under-
lying assumption behind the use of ecoregions and watersheds is that
classification of surface waters will reduce natural within-class variation of
biological and ecological data (Gerritsen et al., 2000). Streams within
ecoregions generally respond in a broadly similar manner to comparable
management practices (Lyons, 1989), although heterogeneity in physical
habitat and water quality conditions may confound the measurement of their
biotic responses (cf. Feld et al., 2011; Friberg et al., 2011; Hawkins, 2006;
Larrañaga et al., 2010; Toepfer et al., 1998).
4.2.2 Computational methods

Fish species and their assemblages (numerical abundance, body size and inter-
actions) are hypothesis to reflect environmental conditions (e.g. Feld et al.,
2011; Layer et al., 2010, 2011). Our analyses of the freshwater fish
assemblages were performed at different levels: firstly, via the construction
of networks for sites sampled in a comparable way and secondly via the
calculation of size spectra and power laws to describe network topology.
At the first level, we used the US-EPA raw counts and body mass of in-
dividual fishes in the State of Ohio (www.epa.gov). After data mining, we
had 2656 fish taxocenes sampled in different ways. Electrofishing (often in
conjunction with seines or nets) was the principal sampling methods for fish
individuals in wadeable and boatable streams (Flotemersch, 2001): in wade-
able streams, block nets are placed downstream and upstream of the sampling
pool, in contrast to boatable streams, where boat-based electrofishing is done
throughout.
At the second level, an allometric assessment of the fish size distribution
was performed. We conducted analyses for the 2656 locations on possible
deviations from linearity of the upper tail of the binned biomass-size spec-
tra: reflecting the use of different sampling methods, the 534 boatable
streams exhibited three times lower standard deviations than the 2132
wadeable streams (0.0787 SD vs. 0.2440 SD, respectively). Based on the
allometric uncertainties in biomass estimates as derived from the size spec-
tra for all the locations (summarized in Fig. A5), we chose a subset of 302
locations unaffected by either habitat heterogeneity, sampling bias or sur-
vey differences, aiming for a consistent sampling methodology (in our case,
boatable streams).
Some of these fish assemblages will be discussed in the next sections. In
particular, we investigated whether the food web structure within one
taxocene might be relatively vulnerable to different static deletion sequences
to diagnose the magnitude of changes in biodiversity, for example, through
potential fish extinctions caused by ecological impacts in rivers, and allowing
for a more effective environmental management. We shall use three differ-
ent deletion scenarios:
1. the ‘connectivity descending’ scenario (we will erode from the top of
the food web where the most connected nodes are, thus well-
connected hubs will get removed as first, so it is likely that we remove
a top predator and only that node is gone and neighbouring nodes get
isolated),
2. the ‘connectivity ascending’ scenario (we will erode from the basis of the
food web where the less connected nodes are, thus we will get inevitably
a high probability of removing a resource which will starve its consumers
and the web will collapse with several secondary extinctions) and
3. the ‘random’ scenario (intermediate simulation, removing nodes ran-
domly from the top, the middle and the bottom of the food web).
4.2.3 Can a web be robust?

Most studies in the last decades have focused on the values of biodiversity.
When considering wide ranges in body size, species richness cannot have
one value per se, even if consistent resolution is used (Leaper and Raffaelli,
1999). These authors showed that different taxonomic resolutions affect al-
lometric scaling and they advocated the use of evenly resolved taxa (for in-
stance, all nodes at either species level, genus level or as life stages). The
horizontal axis of Fig. 8 shows a clear increase in the fish species diversity
(CV ¼ 36%, from 13 species up to 40 species) and the scatter suggests a
(weak) inverse correlation between the species diversity of the ecological
networks S and connectance Ct (Pearson’s product–moment correlation co-
efficient of 0.41, P ¼ 0.090), in partial agreement with theory (Havens,
1992; May, 1972; Winemiller, 1989). Connectance typically shows
greater variability for low-diversity aquatic webs, but 2/3 of our aquatic
webs fall into a narrow range between L/S2 ¼ 0.2 and 0.3. For
comparison, only 1/5 of the soil food webs addressed in Section 6.1 fall
into the same 0.2–0.3 range (4/5 share L/S2 < 0.2). These results are
notable because such differences in connectance values imply that fishes
attack up to three times more often other individuals within their own
taxocene than soil nematodes do.
A second feature that the food webs have in common is that although the
linkage density shows a strong direct correlation with biodiversity both in
the blue and brown worlds (Pearson’s r ¼ correlation coefficient of 0.90,
P < 0.00001 for the 18 freshwater food webs of Fig. 8 and Pearson’s
r ¼ 0.63, P ¼ 0.0016 for the 22 soil food webs in Mulder and Elser, 2009),
the most significant relationships between primary versus secondary extinc-
tions and food web attributes are provided by number of nodes and con-
nectance (Fig. 9). Although strong correlations between S and L/S as
well as S and L/S2 are acknowledged and may seem trivial here, the ecolog-
ical implications are great. The correlation between S and L/S is more than a
statistical artefact, because it indirectly shows the degree to which the pos-
sibility to encounter an(other) omnivore species in the food web increases
with a larger species pool. Hence, it also implies that the average linkage
density for a food web must increase with the total of investigated species.
According to Williams and Martinez (2004), with no information on
link-strengths, the short-weighted trophic level is the most accurate approx-
imation for quantifying trophic levels within (real) food webs that include
omnivory, cannibalism and mutual predation. In freshwater ecosystems, like
those investigated here (Table 4), fishes consume resources from many
Connectance/Species diversity
Connectance
Species diversity
Figure 8 Connectance in relationship to fish species diversity of 18 river food webs vi-
sualized with Network3D (Yoon et al., 2004). Two food webs are depicted as overlays
(solid boxes) because they fall into the same range in the connectance–diversity space
(cf. Table 5). The variability and maximum value of connectance are highest in low-
diversity webs, while high-diversity food webs (dashed frame) show a more consistent
connectance pattern according to the constant connectance hypothesis (please see the
text). The columns of this matrix show that food webs with similar (or even statistically
undistinguishable) biodiversity can have different linkage patterns.
trophic levels from hatching to death, including other fishes that were feed-
ing on them during early life stages (Froese and Pauly, 2005; Gilljam et al.,
2011; Layer et al., 2010; Montoya et al., 2006; O’Gorman and Emmerson,
2010; Woodward et al., 2010a). This structural complexity is reflected by
certain food web properties such as the mean of the short-weighted
trophic level, the characteristic path length and the probability that two
nodes linked to the same resource are clustered (Dunne, 2009).
Connectance (C) Linkage density (L/S) Biodiversity (S)

0.18 0.23 0.28 0.33 3.0 5.0 7.0 9.0 12 17 22 27 32 37
1.0 1.0
Deletions (descending)
Deletions (descending)
0.8 0.8
0.6 0.6
0.4 0.4
0.2 0.2
0.0 *** * 0.0

1.0 1.0
Deletions (ascending)
Deletions (ascending)
0.8 0.8
0.6 0.6
0.4 0.4
0.2 0.2
0.0 *** ** 0.0

1.0 1.0
Deletions (random)
Deletions (random)
0.8 0.8
0.6 0.6
0.4 0.4
0.2 0.2
0.0 *** *** 0.0

0.18 0.23 0.28 0.33 3.0 5.0 7.0 9.0 12 17 22 27 32 37
Connectance (C) Linkage density (L/S) Biodiversity (S)
Figure 9 Extinction partitioning for the 18 river food webs according to the ‘connectiv-
ity descending’ (upper three plots), the ‘connectivity ascending’ (middle three plots)
and ‘random’ (bottom three plots) scenarios along connectance (left part), linkage den-
sity (central part) and biodiversity (right part) gradient. The black part is the fraction of
species lost by primary deletions and the red part is the fraction of species lost by sec-
ondary deletions (all trends as moving averages). The mean primary deletion fraction in
the ‘descending’, ‘ascending’ and ‘random’ scenarios is 0.48, 0.56 and 0.83, respectively,
and the mean secondary deletion fraction until breakdown of the web is 0.52, 0.44 and
0.17, respectively. If statistically significant, significance is as follows: *P ¼ 0.035,
**P ¼ 0.003 and ***P < 0.001. Along our linkage density gradient, the fraction of second-
ary deletions in the descending scenario is very similar to the fraction of primary
deletions in the ascending scenario. See text for details.
One common measure of a food web’s vulnerability to extinctions is

the fraction of primary and secondary deletions until final collapse of the
web. For our fish assemblages (Table 5), the two fractions #PD and #SD
are roughly similar in the ‘connectivity descending’ scenario. In contrast,
the other scenarios (‘connectivity ascending’ and ‘random’) show consid-
erably higher fractions of primary deletions and less secondary extinctions
than ‘connectivity descending’ does. In Fig. 9, we show the extinction
partitioning for the 18 food webs according to the ‘connectivity des-
cending’, ‘connectivity ascending’ and ‘random’ scenarios. Food webs
are most sensitive to the ‘connectivity descending’ scenario because their
well-connected hubs get removed as first, so secondary deletions occur
rapidly, as neighbouring nodes get isolated (Fig. 9, upper left plot). Most
connected hubs are at the top in our food web structures. In the ‘con-
nectivity descending’ scenario, the threshold for web collapse is below
50% of primary deletions, that is, primary species loss. On the other
hand, in the ‘connectivity ascending’ scenario, we removed the less con-
nected (basal) node. As they are resources to others (Table 4), it is inev-
itable that as soon all of them have gone extinct, any web will collapse
quickly, with secondary extinctions becoming prevalent (Fig. 9, middle
left plot). Considering the average fraction of basal nodes in the 18 food
webs, the value of 51% (Table 5) is close to the average of 54% for the
threshold for web collapse in the ‘connectivity ascending’ scenario.
Therefore, the web must collapse quickly close to this point because
all basal nodes were already removed. This is the explanation why these
descending and ascending scenarios have similar thresholds, but behave
differently in reaching them (Fig. 9).
The random scenario differs from the previous scenarios because species
were removed from the middle, bottom and top of the web regardless of
their connectivity. Therefore, the web is not eroded systematically (either
removing all hubs, as in the upper part of Fig. 9, or all basal nodes, as in
the middle part of Fig. 9), but merely by chance. Hence, the probability
for each species occupying either a hub or a basal node to persist is, on
average, higher in the random scenario (Fig. 9, bottom plots). Random
changes in the resulting connectivity might generate large extinction
events (Solé et al., 1999: p. 159), but not in the freshwater assemblages
investigated here.
The average biodiversity of our food webs is 27 fish species: food webs
with a lower than average biodiversity have a higher than average con-
nectance, and vice versa (Table 5). Low-connected and more diverse webs
Table 5 Food web properties and vulnerability to simulated species deletion of 18 fish assemblages (location in Fig. A4) ranked according to
their initial biodiversity. Summary of properties (red) and vulnerability to three deletion sequences: connectivity descending (green),
connectivity ascending (yellow) and random (blue, 1000 simulations). S, Number of species; L/S2, connectance; L/S, linkage density; Top,
fraction of piscivorous species; Inter, fraction of intermediate species; Basal, fraction of zooplanktivorous species; Omni, fraction of species
eating on more trophic levels; GenSD, standard deviation of mean consumer generality; VulSD, standard deviation of mean consumer
vulnerability; ConnSD, standard deviation of connectivity for a consumer; SWTL, mean short-weighted trophic level; Char, characteristic path
length; Clu, mean cluster coefficient; # PD, fraction of primary deletions (¼ species deleted/initial species diversity); # SD, fraction of secondary
deletions; RSD, robustness against secondary deletions computed as RSD ¼ PD1/S with PD1 as number of primary deletions that caused the first
secondary deletion(s). If RSD equals # PD, all the secondary deletions occurred at the last primary deletion with web collapse.
Food web properties Descending Ascending Random

River name S L/S2 L/S Top Inter Basal Omni GenSD VulSD ConnSD SWTL Char Clu # PD # SD RSD # PD # SD RSD # PD # SD RSD
1 Cuyahoga River 12 0.32 3.83 0.08 0.50 0.42 0.50 1.05 0.66 0.39 1.73 1.30 0.36 0.58 0.42 0.17 0.42 0.58 0.42 0.78 0.22 0.66
2 Sandusky River 13 0.23 3.00 0.08 0.46 0.46 0.46 1.31 0.75 0.59 1.71 1.50 0.31 0.46 0.54 0.08 0.46 0.54 0.46 0.66 0.34 0.37
3 Mahoning River 13 0.37 4.77 0.08 0.54 0.38 0.54 1.01 0.54 0.27 1.76 1.21 0.43 0.62 0.38 0.46 0.46 0.54 0.46 0.82 0.18 0.60
4 Buck Creek 18 0.19 3.44 0.06 0.33 0.61 0.33 1.58 0.65 0.70 1.45 1.59 0.31 0.39 0.61 0.06 0.61 0.39 0.61 0.75 0.25 0.38
5 West Mahoning River 20 0.34 6.70 0.05 0.50 0.45 0.50 1.08 0.54 0.36 1.67 1.29 0.43 0.55 0.45 0.20 0.45 0.55 0.45 0.87 0.13 0.77
6 Duck Creek 22 0.27 6.05 0.05 0.50 0.45 0.50 1.23 0.59 0.49 1.72 1.42 0.38 0.55 0.45 0.09 0.45 0.55 0.45 0.80 0.20 0.44
7 Paint Creek East 24 0.18 4.25 0.04 0.29 0.67 0.29 1.69 0.61 0.76 1.38 1.63 0.33 0.33 0.67 0.04 0.67 0.33 0.67 0.81 0.20 0.50
8 Hocking River 24 0.25 5.92 0.04 0.46 0.50 0.46 1.31 0.62 0.56 1.64 1.49 0.39 0.50 0.50 0.04 0.50 0.50 0.50 0.82 0.18 0.48
9 Blanchard River 24 0.27 6.58 0.04 0.50 0.46 0.50 1.23 0.58 0.50 1.72 1.43 0.39 0.54 0.46 0.04 0.46 0.54 0.46 0.82 0.18 0.39
10 West Mahoning River 24 0.30 7.08 0.04 0.54 0.42 0.54 1.12 0.62 0.46 1.79 1.39 0.40 0.58 0.42 0.04 0.46 0.54 0.42 0.83 0.17 0.49
11 Hocking River 29 0.25 7.24 0.03 0.45 0.52 0.45 1.27 0.64 0.56 1.61 1.48 0.38 0.48 0.52 0.07 0.52 0.48 0.52 0.85 0.15 0.65
12 Scioto Brush Creek 30 0.26 7.93 0.03 0.43 0.53 0.47 1.35 0.49 0.53 1.59 1.46 0.42 0.47 0.53 0.17 0.60 0.40 0.60 0.88 0.12 0.76
13 Big Darby Creek 35 0.23 8.09 0.03 0.40 0.57 0.40 1.42 0.57 0.61 1.52 1.52 0.39 0.43 0.57 0.03 0.57 0.43 0.57 0.87 0.13 0.46
14 Paint Creek West 38 0.19 7.18 0.03 0.37 0.61 0.32 1.60 0.61 0.73 0.62 1.61 0.36 0.34 0.66 0.03 0.68 0.32 0.66 0.82 0.18 0.26
15 Little Miami River 39 0.24 9.38 0.03 0.44 0.54 0.44 1.35 0.58 0.59 1.58 1.51 0.41 0.46 0.54 0.05 0.64 0.36 0.54 0.88 0.12 0.59
17 Walhonding River 39 0.26 10.28 0.03 0.41 0.56 0.41 1.34 0.48 0.54 1.52 1.46 0.43 0.44 0.56 0.13 0.59 0.41 0.56 0.92 0.08 0.78
Average 27 0.26 6.74 0.04 0.44 0.51 0.44 1.31 0.59 0.54 1.52 1.46 0.39 0.48 0.52 0.10 0.54 0.46 0.53 0.83 0.17 0.51
behaved differently from highly connected and less diverse webs (Fig. 9).
In the ‘connectivity descending’ scenario, food webs with high connectance
were more robust (higher fraction of primary deletions until collapse) be-
cause the probability to remove a ‘resource node’ for other nodes was
low: it was far more likely that a top predator was removed. Webs with
higher connectance have a higher probability that there are still enough links
left so no species becomes isolated, limiting species loss to the primary de-
letion in each event. In contrast, in a ‘connectivity ascending’ scenario, the
food web is eroded from its base, starving predators of prey. So, low con-
nectance webs are more robust in this scenario because the resource node
has fewer predators that will also disappear when the resource node is gone.
In contrast, those webs with higher connectance collapse faster because
more secondary extinctions occur when one of the resource nodes is
removed.
The kind of deletion sequence clearly affects the vulnerability of the
network to species loss (Dunne et al., 2002; Fig. 9). To further evaluate
the importance of diversity and connectance on the vulnerability to species
deletions, we compared two creeks with intermediate biodiversity (Scioto
Brush Creek: S ¼ 30, Eastern Paint Creek: S ¼ 24), but different con-
nectance (Scioto Brush Creek: C ¼ 0.26, Eastern Paint Creek: C ¼ 0.18)
in the ‘connectivity descending’ scenario (Table 5). Figure A6 shows
how rapidly the total deletions equal S and the entire fish network disap-
pears. The shape of the blue curves reflects an increasing number of sec-
ondary extinctions and the number of trophic links per fish species
descends approximately linearly (Fig. A6B and D), with highly connected
species being the most vulnerable. The ‘threshold period’ until secondary
extinctions occur is 17% higher in Scioto Brush Creek than in Eastern
Paint Creek (Fig. A6A and C). Despite substantial biological improvement
in the environmental health of the Scioto Brush Creek (Burton et al., 2012;
OHIO-EPA, 2008), simulated secondary deletions with connectivity
descending happen quickly after only 20% of total species removed on
average, and all species are gone with on average about 47% of primary
deletions. Eastern Paint Creek’s web appears even more vulnerable,
with the first secondary extinction occurring at 17% of total species loss
and the food web collapses at only 33% of primary species loss. Low
linkage density implies that the removal of a highly connected node
(here, one fish species) results in a loss of fewer links than for webs with
higher linkage density (but lower connectance), limiting species loss to
primary deletion (Figs. 8 and 9).
4.3. Inland water biodiversity: Vulnerability of B–EF across

ecoregions
Another, less frequently discussed aspect of food web vulnerability to species
loss is the robustness RSD against secondary deletions, as measured by the
fraction of primary deletions that occurred in the web without triggering
a secondary extinction. The higher the RSD, the later the secondary extinc-
tions occur as a consequence of a primary one. Secondary species extinctions
mostly occur because a primary extinction creates an unfeasible interaction
between the predator and the lost prey (Table 4). The different topologies of
the webs (cf. Fig. 8) translated into greatly varying vulnerabilities to second-
ary extinctions in the three species deletion scenarios of Table 5 (Fig. 9). Sec-
ondary deletions occur much earlier in the ‘connectivity descending’ (RSD:
mean ¼ 0.10) than in the ‘connectivity ascending’ scenario (RSD:
mean ¼ 0.53). This again implies that, although the total number of primary
and secondary extinctions is similar in these two scenarios, the extinction pro-
cess to final web collapse is very different. Most webs in the ‘connectivity des-
cending’ start disintegrating early and continuously with one or a few
secondary extinctions following each primary one. In contrast, most webs
in the ‘connectivity ascending’ scenario only suffer primary extinctions for
a long time, but then break down suddenly with a high number of secondary
extinctions. The extinction processes in the ‘random’ scenario fall between
the two extremes (i.e. high and low vulnerability to secondary extinctions
for the descending and ascending scenarios) and are more similar to the ‘con-
nectivity ascending’ scenario (RSD: mean¼ 0.51). The standard deviations for
the 1000 random scenarios are low for the primary deletions (10% of the
mean) and high for the secondary deletions (50% of the mean).
The differences between the three deletion scenarios demonstrate that
web attributes as well as the order of species deletions have a considerable
impact on the (species) vulnerability to extinction events: that is, it is not
just biodiversity of nodes but also of the interactions within a food web that
will affect B–EF trajectories of species loss. On the other hand, even sites
from a polluted watershed such as the Hocking River (Burton et al.,
2012) seem to have intermediate connectances (Table 5), implying that sen-
sitive fish species that may have previously stabilized the web have already
been lost. Although higher connectance led to higher robustness against sec-
ondary extinctions in earlier studies (Dunne and Williams, 2009; Dunne
et al., 2002), our results only show such an effect (RSD > 0.1) for two
low-diversity webs (Cuyahoga and Mahoning rivers) and three webs of
intermediate to high species richness (West branch of the Mahoning
River, Scioto Brush Creek and Walhonding River). An explanation of this

effect for the low-diversity webs may be that they have higher connectance
(scales with S2), but also lower linkage density (scales with S) than other
webs (Table 5). For intermediate to high-diversity webs, higher
connectance may convey high robustness in some cases, but our results
also demonstrate the very opposite, namely that highly vulnerable webs
exist despite of high connectance and high linkage density (i.e. Big Darby
Creek, Blanchard River, Duck Creek, Hocking River, Paint Creek and
all three locations at the Little Miami River shown in Fig. 10).
Food webs (at least those in Fig. 9) are clearly more sensitive to deletion
sequences with ‘connectivity descending’ than to those with ‘connectivity
ascending’. Node connectivity plays a critical role for the vulnerability of the
food web regardless of species diversity and is largely independent of con-
nectance. Our results indicate that high-diversity webs are just as (or even
more than) vulnerable to static extinctions as low-diversity webs, a non-
intuitive result which may have important implications for ecosystem man-
agement. Since higher trophic levels are strongly interlinked with feeding
relationships, in contrast to the producer and herbivorous community, this
pattern implies that the loss of well-connected intermediate and top
A B Little Miami River C
n = 39 n = 40 n = 39
Upstream Downstream
Molar N:P ratio = 4.18 Molar N:P ratio = 1.89 Molar N:P ratio = 3.27
Total [P] = 0.29 mg/l Total [P] = 1.24 mg/l Total [P] = 0.483 mg/l
COD = 15 p.p.m. COD = 258 p.p.m. COD = 21 p.p.m.
Figure 10 Comparison of species diversity (n ¼ number of fish species) between three
locations along the Little Miami River, Ohio, United States (Fig. A4). Although biodiver-
sity is maintained, structural changes in food webs reflect subtle changes in water
chemistry, being the central assemblage—collected in a slowly streaming and
particulate-rich creek with most organic compounds and high P concentration—the
most vulnerable despite of its high connectance and high linkage density (Table 5).
The mean of all the coefficients of variation (CVs) for each environmental parameter de-
scribed by Dyer et al. (1998) for this watershed equals 33%. Below the arrow indicating
stream direction, the molar N:P ratio, the total phosphorus concentration and the chem-
ical oxygen demand (COD) in water are provided for each location.
predators is critical to the persistence of species. It could also increase the risk
of extinction cascades in ecosystems undergoing environmental and/or
anthropogenic change, as is the case in many freshwaters on a global
scale (Friberg et al., 2011; Woodward et al., 2012). Such a conclusion
has been partly corroborated by previous studies on both model food
webs (De Visser et al., 2011; Srinivasan et al., 2007) and empirical food
webs (Estes et al., 2011; O’Gorman et al., 2008). Given that the Ohio fish
data set comprises, besides predators and consumers, herbivore species only
as prey (Table 4), our statistics might have severe implications for extinction
risk in a broader context. In fact, even in consumer-free ecosystems, like
those modelled by Solé and Montoya (2006), species richness can drop and
taxocenes will collapse as soon colonization is no longer sufficient to
compensate for habitat fragmentation and habitat destruction.
Apart from connectivity, other species properties such as body size
(De Visser et al., 2011), relative abundances (Lyons and Schwartz, 2001)
and interaction strength (Allesina and Pascual, 2009) also play a decisive role
for a food web’s vulnerability to extinction events, especially in dynamic
species deletion simulations (Layer et al., 2010; Pimm, 1980; Quince
et al., 2005) and long-term empirical studies (Stachowicz et al., 2008).
This long-standing, complex issue of the diversity–stability relationship is
still controversial (Banašek-Richter et al., 2009; Montoya et al., 2006;
Rossberg et al., 2011) and many of its implications for B–EF relationships
remain open (as reviewed by Cardinale et al., 2006; Hooper et al., 2005).
When species diversity is maintained despite (increased) nutrient loading,
biodiversity may act as a kind of buffer against environmental disturbance
(Cardinale, 2011) and if this evidence holds for metazoans as well,
management or restoration of native fish species becomes desirable (Feld
et al., 2011). We provided here an overview that helps to quickly yet
coarsely assess the risk of species loss without time-consuming sampling
or modelling.
4.4. Population fluctuations at standardized taxonomical

resolution: A virtual case study
In both aquatic and terrestrial ecosystems, Srinivasan et al. (2007) and
De Visser et al. (2011) showed high sensitivity of (relatively pristine) food webs
to the loss of large, dominant or even common species. Moreover, such rare
species can inflate allometric relationships, depending on their occurrence and
distribution within size classes and areas with different spatial resolution
(Valcu et al., 2012; http://cran.r-project.org/package¼rangeMapper).
Since size spectra do not distinguish between species, they are easily measured
and more robust to inclusion/exclusion of rare species than is the case for
species-based community measures of allometric scaling, such as the trivariate
food webs that have gained increasing prominence in recent years (Woodward
et al., 2010b).
Mass–abundance scatter-plots have the advantage that they can more
consistently combine information and, in contrast to size spectra, can be
plotted as functions of either endogenous traits (body mass, mostly weight,
or body size, mostly length) or exogenous traits (typically numerical abun-
dance). Brown and Gillooly (2003) argued that only traits like endogenous
body mass can be used to predict numerical abundance. Unfortunately,
the inversion of the M and N axes in some papers published after Brown
and Gillolly’s plea contributed to a recent generation of terms which
slows down the research itself, as the resulting overlap in terminology
may confound many readers. Still, the predictive power of exogenous traits
such as N for M and/or B is often surprisingly high. If size-dependent
physiology of individuals within one taxocene is extended to entire
communities, the allometric scaling of the latter should converge on a
biomass-constant isometric line (among others, Cohen et al., 2003;
Hildrew, 2009; Mulder et al., 2005b; Rossberg et al., 2008; White
et al., 2007; Woodward et al., 2005a).
Previous analyses demonstrated that log(N), log(M) and log(B) are
strongly correlated, as theoretically expected (Brown and Gillooly, 2003;
Damuth, 1981; Mohr, 1940) and empirically shown (Cohen and
Carpenter, 2005; Cohen et al., 2003; Mulder et al., 2008; Reuman et al.,
2008). When the classical log–log mass–abundance linear regression model
logðN Þ ¼ a1 logðMÞ þ b1 ½5
is merged into the log-transformed biomass (originally weight times
abundance)
logðBÞ ¼ logðMÞ þ logðN Þ ½6
we can rewrite Eq. (6) as

logðBÞ ¼ logðMÞ þ a1 logðMÞ þ b1 ¼ ð1 þ a1 Þ logðMÞ þ b1 ½7
which is now in the form of a typical biomass-size spectrum
logðBÞ ¼ a2 logðMÞ þ b2 ½8
although the two intercepts b1 and b2 are not comparable to each other, in
contrast to both slopes which are correlated and are supposed to differ by one
unit from each other (Jennings and Mackinson, 2003; Mulder et al., 2008;
Schneider et al., 2012).
The linear allometric model of Eq. (8) was fitted to the locations in Ohio
separately (confidence interval 99%), and the lumped log(B) for all sampled
fishes was plotted at the middle of the respective size class along the binned
log(M) gradient. Binned and lumped log(B) with zero observations were ex-
cluded, because log(0) is undefined. Size bins can influence the resulting
power functions: our fish size spectra tend to show a fluctuating increase in
biomass with body size up to a peak near the largest mass-bins comparable
to those of Duplisea and Drgas (1999) in the blue world and to those of
Mulder et al. (2008, 2009) in the brown world. The huge influence of
larger (predatory and omnivorous) fishes is reflected by the regressions that
fit the dome before the site-specific modal size bin: the linear regressions
fitted to size spectra of the (boat-sampled) fish networks have positive
slopes ranging from 0.72 0.074 SE (min) up to 1.24 0.216 SE (max)
and the (from Eqs. 5–7 derived) mass–abundance linear regression slopes
are rather shallow (their power laws fluctuate between 1/4 and þ1/4, with
an average very close to 0). Mass–abundance positive slopes are known as
possible within a taxocene (e.g. Ulrich et al., 2005).
For fish assemblages with 1/4 power scaling, if population density had a
body mass scaling exponent of 0.25, a 10-fold increase in weight would
increase the fish population by 100.25, equal to a 1.78-fold increase in density.
Conversely, if population density had a body mass scaling exponent of 0.25,
a 10-fold increase in weight would decrease the population as a function
of 10 0.25, which is equal to a 0.56-fold decrease in density of the smaller
individuals. To illustrate these opposite trends for further interpretation
of freshwater biodiversity, some brief examples may be useful. Let us
imagine a very simple freshwater food web consisting of only four fish
species, namely Emerald Shiner (Notropis atherinoides), Yellow Perch (Perca
flavescens),Walleye (Stizostedion vitreum) and Muskellunge (Esox masquinongy).
Let their respective wet weights be 4, 40, 400 and 4000 g on a site-specific
average. After log-transformation, their log(M) will become 0.6, 1.6,
2.6 and 3.6. Given that with abscissa log(M) and with ordinate log(N)
populations fall approximately along a straight line with a negative slope
(e.g. Brown and Gillooly, 2003; Cohen et al., 2003; Damuth, 1981, 1987,
1991; Hildrew, 2009; Mulder et al., 2005b; Woodward et al., 2005a), we
assume for simplicity that the population densities of these four fish species
are equal to 100, 10, 1 and 0.1 individuals, respectively. After log-
transformation, their log(N) will become 2, 1, 0 and 1. Their specific
log(B) equals log(M) þ log(N) ¼ 0.6 þ 2 ¼ 1.6 þ 1 ¼ 2.6 þ 0 ¼ 3.6 1 ¼ 2.6.
Hence, these four fish populations will keep a biomass of 102.6 400 g
and, if plotted on log–log axes, the theoretically resulting linear regression
slope should be isometric. In the case of a 1/4 power scaling, keeping the
aforementioned weights and a comparable number of fishes, the
population densities of these species could be 60, 40, 30 and 10, and in the
case of a 1/4 power scaling, the respective densities should be 10, 30, 40
and 60. In the first case, the resulting specific fish biomass is negatively
correlated with the increase in fish body mass, whereas in the second case
the opposite occurs. In the case of the 534 boat-sampled sites (Fig. A5),
57.7% showed the negative mass–abundance scaling, albeit on average
only 1/8, but 42.3% showed a positive scaling for the bin approach.
4.5. Superimposed disruption of fish biodiversity

on cascading interactions
Cascade effects on other species and trophic levels, for instance due to either
invasive or extinct species, can potentially be quantified by allometric ana-
lyses and characterization of multitrophic interactions. Sterner and Elser
(2002) and Hall (2009) formalized the complexity of elemental constraints
and thresholds from stoichiometrically explicit perspectives, reviewing
several studies from microbiology to aquatic ecology, emphasizing how im-
portant the modulation of chemical imbalances between trophic levels can
be for understanding B–EF relationships.
In our study, we modelled the site-specific changes in total biomass
(Fig. 11, upper panel) and average weight (Fig. 11, lower panel) along gradients
of fish diversity (number of species, left plots) and molar N:P ratio (right plots).
The marked decrease in fish size with biodiversity (presumably a consequence
of decreasing energy at higher trophic levels) provides a measure for assessing
the sensitivity of these species-poor networks (less than 10 species) to preda-
tion, even though their environmental conditions (here, the molar N:P ratio)
can be considered optimal (Fig. 11D). The average mass of individual fishes
does not show a linear correlation with the molar N:P ratio of the water col-
umn, in contrast with previous studies where body size (both as fish length
and as fish weight) increased with the molar N:P ratio of cyprinids (Sterner
and George, 2000) but in line with more recent research, which shows marked
stoichiometric imbalances between the environmental availability and tissue
content of consumers in freshwaters (Lauridsen et al., 2012).
200 200
180
A 180
B
Site-specific total fish biomass (kg)

Site-specific total fish biomass (kg)
160 160
140 140
120 120
100 100
80 80
60 60
40 40
20 20
0 0
8 16 32 64 1 10 100 1000
Fish biodiversity (log2 scaled) Molar N:P ratio (water column)
1.2 1.2
C D
Site-specific average fish weight (g)

Site-specific average fish weight (g)
1.0 1.0
0.8 0.8
0.6 0.6
0.4 0.4
0.2 0.2
0.0 0.0
8 16 32 64 1 10 100 1000
Fish biodiversity (log2 scaled) Molar N:P ratio (water column)
Figure 11 Site-specific fish biomass (A, B) and average fish weight (C, D) related to fish
biodiversity (A, C) and water column N:P ratio (B, D) for freshwater fishes from boat-
sampled Ohio rivers (Fig. A5). Although American freshwater ecosystems are well-
known for their remarkably high N:P ratios (Cotner et al., 2010), the clump in the fish
biomass distribution reflects a certain (positive) bias in the amount of Ohio rivers with
‘lower’ N:P ratios, a log-normal distribution that is known to occur in large datasets
(Kattge et al., 2011). According to Pfisterer and Schmid (2002), the species-poor exper-
imental systems achieved under unperturbed conditions show a lower biomass produc-
tion than the species-rich experimental systems. The left panel clearly resembles their
grassland model, where in this case species-poor fish communities not only reduced
biomass production under unperturbed conditions (A), but also achieved the highest
individual body-size averages (C). The darkness of the grey effect suggests increasing
environmental perturbation as derived from abiotic data.
Since regularities might be expected in biodiversity and/or biomass dis-

tributions, to what extent can a possible introduction of specifically sized or-
ganisms be necessary to preserve ecosystems, for instance counteracting
negative effects of overfishing or habitat destruction? As early as 1955,
MacArthur pointed out that abundance of species can vary greatly, and that
if one species has an abnormal abundance, a community may be unstable
if the abundances of other species become inflated (MacArthur, 1955).
In Section 4.2.3, we have shown ‘cascade effects’ on occurring species after
simulated removal of fish species in 18 rivers (primary and secondary

deletions).
Simulated deletion sequences provide a clear picture of food webs re-
sponses to the possible removal of specific taxa (either consumers or re-
sources). In the field, small-scale manipulation experiments (enclosure/
exclosure of larger predators) often reveal that relatively few resources are
strongly depleted (Woodward and Hildrew, 2002; Woodward et al.,
2005b), although whole-lake manipulation experiments can provide a
different perspective. Large-scale manipulation experiments include
recruitment of Rainbow Trout (Oncorhynchus mykiss), that altered the
planktivory regime and the water quality (Elser et al., 1995), the addition
of Northern Pike (Esox lucius), which led to crashes in cyprinid minnow
populations (Carpenter et al., 2011; Elser et al., 1998, 2000), and the
replacement of planktivorous minnows with a comparable mass of
piscivorous bass (Ives et al., 1999), with consequent long-term changes in
the zooplankton biomasses (Ives et al., 1999; Jonsson et al., 2005). One
example for controlled alteration of abiotic factors are whole-lake N:P
treatments to prevent nitrogen limitation with consequences at different
trophic levels, as planktivore biomass was inversely related to piscivore
biomass (Carpenter et al., 2001) and changes in the fish-driven phosphorus
cycle (Carpenter et al., 1992). Given that low linkage density implies that
the removal or replacement of a highly connected species results in a loss
of fewer links than for webs with higher linkage density, the traits of
endangered (or recruited) fish species must be taken into greatest account.
5. CONCEPTUAL UNIFICATION
5.1. Articulating B–EF in terrestrial ecosystems

Different functional responses and effects within and across adjacent trophic
levels (x and x þ 1) can be articulated within a conceptual framework to
predict EF under future scenarios (Lavorel et al., 2009). To analyze B–EF
relationships, the application of such a framework requires that each com-
partment (box) is specified for individual species in terms of functional di-
versity (FD) and/or trait attributes and can be applied to most ecosystems
stepwise. We will use nutrient cycling and trophic interactions as examples
and will define the functional effect trait(s) contributing to the ecosystem
function at the trophic level most related to the function itself (x in Fig. 12)
and, if relevant, at the adjacent (x þ 1) trophic level.
Environmental pressure
Environmental Trophic
response response
Trophic level x + 1
Trophic level x
traits traits
Trophic Functional
effect traits effect traits
Ecosystem functioning
Figure 12 Framework articulating functional responses and effects within and across
two adjacent trophic levels to forecast ecosystem functioning. The analysis of the effects
of functional diversity on ecosystem functioning will then integrate the quantitative ef-
fects of diversity for the environmental response traits, the trophic effect traits, the tro-
phic response traits and the functional effect traits. This can be done by partitioning the
variance of the ecosystem functioning according to these trait types (Díaz et al., 2007).
According to us, such a framework can be applied to run specific scenarios of environ-
mental change in a predictive approach.
Step 1. Given that the environmental response traits are often taxon-
specific, if more than one functional effect trait is involved within the con-
sidered (sub)food web, then association patterns between different traits
need to be taken into account. The outcome is a trade-off among positive
and negative effects at adjacent trophic levels.
Step 2. Trophic effect traits and trophic response traits and associated pro-
cesses must be identified. In the case of ecological stoichiometry, for example,
the chemical quality of soil systems (C:N:P and [Hþ] either as pH or pOH) en-
hances the numerical abundance (and hence the biomass) of soil mesofauna
much more than the soil microfauna (Mulder and Elser, 2009). Moreover, soil
mesofauna incorporates most fungivores and microfauna incorporates most
bacterivores (Mulder et al., 2005a; Wu et al., 2011) and bacteria and fungi
respond to chemical resources in different ways according to their ability to
break down carbon- versus nitrogen-rich compounds (De Vries et al., 2006;
Hunt and Wall, 2002; Krivtsov et al., 2011; Wardle, 2002; Wardle et al., 2004).
Step 3. This step identifies the response traits for each of the trophic levels
(starting from the lowest, x in Fig. 12) to the environmental predictor of
interest. In the case of total soil phosphorus, a lower C:P ratio directly
favours larger arthropods (Mulder and Elser, 2009) and the proliferation
of bacteria with an r-like strategy (Makino et al., 2003). Given that
most microarthropods are predators or fungivores (Mulder et al., 2005a;
Wardle, 2002), a shift in the fungi-to-bacteria ratio is expected in soil
systems (De Vries et al., 2006; Mulder et al., 2009).
Step 4. Having established the relationships between functional effect
traits for a given environmental condition (or a predictor), the responses
of different trophic levels to pressure and multiple functional relationships
involved in a selected ecosystem service, the final analyses will allow the
translation of effects at individual or species level into actual ecological
processes at community (or even biome) level.
5.2. Articulating B–EF in aquatic ecosystems

The framework of Fig. 12 may be applied not only to a given ecosystem
process influenced by a range of contrasting conditions (and a comparative
analysis conducted in order to identify generic vs. contingent relationships),
but it can also identify (in)congruences in B–EF. Therefore, it is also poten-
tially suitable to assess the ecological risks of environmental pressure.
Eutrophication, for example, is a widespread kind of environmental
pressure which affects key ecosystem services. Global increase in use of urea
in both agriculture and manufacturing has resulted in increased run-off to
sensitive coastal systems and is important in the nitrogenous nutrition of
some harmful algal bloom species (Glibert et al., 2006). Reduction in water
quality directly influences important coastal ecosystems like seagrass
meadows (Waycott et al., 2009), which trap sediments and nutrients and
have a large net primary productivity (Orth et al., 2006). Seagrass meadows
are also sensitive to changes in turbidity and nutrient enrichment and
provide ecosystem services such as supporting commercial fisheries through
habitat provisioning and globally significant sequestration of carbon (Duarte
et al., 2005). Besides indirect effects of eutrophication due to reduction of
light penetration in the water column (changes in turbidity) and enhance
coverage by epiphytes (biological disturbance), direct effects include shifts
in nutrient ratios of seagrass leaves (Antón et al., 2011) which influence
grazing patterns and cause selective abrasion and even removal of the plants.
Leaves of persistent species such as Thalassia hemprichii have a lower C:N
ratio than leaves of the ephemeral Halodule uninervis or the intermediate
Cymodocea rotundata (Fig. 13). Seagrasses with higher C:N ratios have higher
palatability for sea urchins in situ (tropical seagrasses, Vonk et al., 2008) or for
Leaf number
0 I II III IV V
40
A T. hemprichii
Dense
30 Sparse
20
10
0
♦ 12.6 17.2 20.8 25.2
C:N ratio
▲ 13.5 17.4 20.5 24.7
12
Leaf dry weight (mg)
B H. uninervis
9
0
♦ 19.7 24.9 32.8 40.3
C:N ratio
▲ 19.0 24.1 32.2 35.4
20
C C. rotundata
15
10
0
♦ 18.9 19.8 25.2 33.2
C:N ratio
▲ 19.8 20.0 25.2 30.3
Figure 13 Example of trophic effect and trophic response traits (sensu Fig. 12) from the
green world: grazing pressure (vertical arrow) and elemental quality in three species
from seagrass meadows of the Spermonde Archipelago (Indonesia). Mean leaf weight
development SE of seagrasses in dense (♦) and sparse (▲) canopies (Vonk and Stapel,
2008) with comparable PO43 concentrations (in water columns: 0.24 and 0.23 mM and
in pore water: 0.39 and 0.40 mM, respectively). From top to bottom: (A) Thalassia
hemprichii, (B) Halodule uninervis and (C) Cymodocea rotundata (photo credits: Jan Arie
Vonk). All three seagrass species continuously produce leaf tissues at a fixed basal mer-
istem (Short and Duarte, 2001); the Roman number refers to the leaf layout during de-
structive counting (I is the youngest leaf, V the oldest leaf collected). The closed symbols
and lines represent the natural mixture of leaves and open symbols represent intact
leaves only. Leaf molar C:N ratios for dense and sparse canopies provided below each
plot; all samples (n ¼ 9) of 10–20 shoots per species, depending on size. Despite in-
creased palatability, T. hemprichii (A) appears to be the most resistant to grazing
pressure.
isopods in mesocosm (temperate seagrasses, Tomas et al., 2011). Contrasting

trophic effect and trophic response traits not only affect the composition of
seagrass meadows, but also enhance the nitrogen pool, with both the N con-
centration in aboveground seagrass biomass as the dominance of species with
lower C:N ratio higher in grazed treatments (Vonk et al., 2008). Similarly,
C:N of detrital resources in freshwaters, which is a key determinant of de-
composition rates (Hladyz et al., 2009), is also a function of both the sur-
rounding riparian vegetation and the nutrient status of the waterbody
itself (Hladyz et al., 2011).
6. SYSTEM-DRIVEN B–EF
6.1. Elemental changes within one taxocene: Less is more
Abiotics (pH and C:N:P) play a key role in determining the abundance of
diversity of the soil nematofauna and nutrients in particular enhance the pro-
ductivity (here, their total biomass) of free-living nematodes (Fig. 14) as well
as the unevenness of the soil nematofauna (Fig. A2). In P-enriched, inten-
sively managed soils (low N:P molar ratios), nematode total biomasses are
much greater than in sites with a (relatively) higher N:P molar ratio. In other
words, a lack of soil P in agroecosystems kills off the predatory nematodes or
strongly diminishes the abundance of all nematodes (Mulder and Vonk,
2011), and there is increasing evidence of similar patterns even in extreme
environments (Barrett et al., 2007).
Although comparable patterns have been detected among taxocenes
(Mulder and Elser, 2009, more details in Section 6.2), Fig. 14 shows that
the distribution of the free-living nematode biomass may overlap con-
strained bottom-up responses to microbial producers. Under higher grazing
pressure (low soil N:P), either the microbial activity is diminished or the
density of bacterial cells is low. In contrast, under lower grazing pressure
(high soil N:P), microbial activity can become stimulated and the density
of bacterial cells is high (Mulder et al., 2009; Reuman et al., 2009). If so,
given that most free-living nematodes are bacterial feeders, Fig. 14
resembles the classical ‘energy enrichment paradox’, which shows here at
both tails of the nematode distribution the exacerbated incongruences
between the bacterial autotrophs and the bacterivore nematodes under
either low or high N (cf. Hall, 2009 and references therein). Nematode
patterns seem comparable to those predicted by the ‘hump-backed
model’ (Grime, 1973, 1979), which used an arbitrary scale from 0 to 1
(Grime, 1977). Biomass may in fact increase with respect to the limiting
STxET pH Molar ratios N M B

(H O) C:N N:P C:P (# / kg soil) (mg dry wgt) (mg / kg soil)
2
HIMG 5.51 (0.06) 17.23 (0.41) 13.31 (0.56) 233.3 (14.2) 79,718 (7274) 0.046 (0.003) 3626 (391)
FCMG 6.40 (0.08) 13.86 (0.38) 8.97 (0.32) 123.7 (5.0) 58,740 (4121) 0.044 (0.003) 2606 (248)
FCAF 7.76 (0.03) 15.81 (0.60) 4.17 (0.56) 64.9 (8.1) 11,657 (1312) 0.035 (0.002) 391 (40)
LUAF 6.76 (0.05) 18.61 (0.26) 3.26 (0.09) 60.5 (1.3) 21,299 (3461) 0.058 (0.004) 1220 (208)
POMG 5.95 (0.05) 18.76 (0.37) 7.41 (0.28) 138.3 (5.6) 41,620 (1925) 0.059 (0.002) 2391 (133)
POAF 5.85 (0.06) 20.73 (1.16) 7.71 (0.96) 172.3 (27.3) 36,258 (3210) 0.052 (0.004) 1868 (275)
POSW 3.98 (0.08) 31.71 (2.27) 32.10 (2.96) 998.9 (105.0) 17,609 (1704) 0.027 (0.002) 486 (66)
10,000 22
R22 == 0.199
0.199 R == 0.280
0.280
Total biomass of soil nematodes (mg / kg)
8000
6000
4000
2000
0
0 10 20 30 40 50 60 70 80
Molar N:P ratio
Figure 14 Occurrence of environmental response traits in the brown world: synergetic
processes of land history and abiotics are reflected in the soil nematodes (upper panel:
nematode density (N), mean weight (M), biomass (B) and (SE) in brackets). From left to
right (upper photos) and from top to bottom (synoptic table), managed grasslands on
peat (HI MG), managed grasslands on clay (FC MG), arable fields on clay (FC AF),
arable fields on Loess (LU AF), arable fields on sand (PO AF), managed grasslands
on sand (PO MG) and shrublands on sand (PO SW). Lower molar N:P ratios seem
to enhance the productivity (biomass) of nematodes (lower panel), but also the uneven-
ness within the nematofauna (Fig. A2). Raw data from Mulder and Vonk (2011).
nutrient (here, phosphorus) via a saturating, non-linear function, whereas

diversity may increase, decrease or exhibit a hump shape (Sterner and
Elser, 2002 and Sterner, 2004, respectively). Our threshold of 13 is
supported by the two regression trends for high and low fertility (Fig. 14)
and is similar to the atomic N:P ratio by Cleveland and Liptzin (2007)
for soils and roughly comparable with the historical atomic N:P ratio of
16 by Redfield (1958) for the blue world. The left and right regression lines
of Fig. 14 show, in fact, a direct correlation between the total biomass of soil
nematodes and the soil N:P ratio until 13 (higher eNPP sites, see Table 1)
and an inverse correlation between biomass and N:P afterwards (lower
eNPP sites).
We found no consistent relationships between the average mass M and
the average predator–prey body-mass ratios across ecosystem types and soil
types (Mulder et al., 2011a). Widely distributed horizontal distributions of
M across environmental C:N:P transects (as those in Fig. 15) might revitalize
the discussion on the use of M as the best independent sole predictor for
mass–abundance scaling (compare Cohen et al., 2003; Hildrew, 2009;
Mulder et al., 2005b; Woodward et al., 2005a with Brown and Gillooly,
2003; Reuman et al., 2009). Indeed, it is the numerical abundance that
changes the most, not the mean mass, as expected from a well-known
direct correlation between population density and resource availability
(e.g. Kaspari, 2004; Meehan, 2006; Wardle, 2002) and Kaspari (2004)
focuses on the variable N instead of M. Under relatively stable
environmental conditions, this implies that EF might be driven more by
the total numerical abundances N of organisms than by their body-mass
average M or by the resulting total biomass (N M as in Fig. 14). Our

productivity gradients show that M values are real and vary from place to
place less than previously suspected (Kaspari, 2004).
The rather comparable M values are surprising and could make terrestrial
‘stable states’ questionable: as large-scale fluctuations of M values were not
observed along the C:N:P gradients (Mulder and Vonk, 2011), we might
wonder under which kind of environmental conditions (to be held constant
for a certain time span) such ‘stable states’ might actually occur in the brown
world. Moreover, an investigation by Gilljam et al. (2011) consistently
shows either underestimations or overestimations of predator–prey systems
as soon as the (derived) species-specific M averages were used instead of the
(original) site-specific weights at individual level m.
6.2. Elemental changes across taxocenes: Community

mismatches
Assuming that, at least in the brown world, numerical abundance N matters
more for EF than individual mass, we might continue to neglect the below-
ground variation of individual body-mass values within one taxon or, pos-
sibly, even within the same taxocene—as most soil ecologists currently do
(overview in Mulder et al., 2011b). If all taxa absorb energy at constant rate,
and the metabolic rate of an individual approximately follows a power law in
Log10 soil nematodes mean dry weight (ng)

Loamy soils Females only All Adults Juvenile life stages
Sandy soils Females only All Adults Juvenile life stages
1
0.75 1 1.25 1.5
Log10[C] - log10[N]
3
1
1.5 1.75 2 2.25 2.5 2.75
Log10[C] - log10[P]
3
1
0.25 0.5 0.75 1 1.25 1.5
Log10[N] - log10[P]
Figure 15 Occurrence of functional effect traits in the brown world. The soil types
influence the size of individual nematodes more than nutrient ratios do: from top to
bottom, the weighted differences in the body mass between the sandy soils (in green)
M (Brown et al., 2004; Peters, 1983; Savage et al., 2004), the energetic
equivalence hypothesis predicts a mass–abundance slope of 3/4.
Observing a mass–abundance slope less negative than (respectively, more
negative than) 3/4 suggests that larger invertebrates absorb more
(respectively, less) energy from the environment than smaller
invertebrates. However, rather few soil communities scale to the 3/4
power (Mulder et al., 2005b, 2009, 2011c), in contrast to species–density
scaling (Eq. 2). It should be noted, though, that the scaling power
strongly varies between ⅔ and 1 for mass–abundance relationships
(Mulder, 2010) and between ⅔ and 1 for metabolic rates (Glazier, 2010)
because the scaling exponents are sensitive to which taxa are included
(Boit et al., 2012; Glazier, 2005; Mulder et al., 2005b, 2009; Prothero,
1986; Reuman et al., 2008). Still, diverse patterns and clear trends remain
recognizable under comparable methodologies.
Few studies on food web manipulation have been performed in the
brown world, but Wardle et al. (2011) recently showed that ant exclusion
enhanced the first and third trophic level of soil food webs, increasing active
microbial biomass and predatory soil nematodes but not bacterial-feeding
nematodes (second trophic level). Assuming that larger mites (soil
mesofauna) are often predatory, one mesofaunal individual and (at least)
one microfaunal individual have to come together. The probability that this
happens increases approximately as the product of both population abun-
dances. Thus, if in a nutrient-richer soil both microfauna and mesofauna
would be two times more abundant, then the probability of encounter
would approximately increase by a factor 4, leading to over-proportionally
more feeding opportunities for the predatory mesofauna. But again, direc-
tions of the responses need to be specified as in the conceptual framework
and the loamy soils (in brown) of all the occurring nematodes per soil type together
fluctuate between 7.9% and 15.0%, implying that nematodes in loamy soils are smaller
than those in sandy soils. Averages were consolidated separately for C:N, C:P and N:P
ratios and log-transformed. Log–log linear regressions are just plotted for clarity,
although they are not significant: from top to bottom, log–log linear regressions for
all females (upper solid lines), all adults (dotted lines) and all juveniles (lower solid lines).
The cross-product soil type (ST) versus ecosystem type (ET) determines the total abun-
dance of individuals (and hence, the total biomass). This is rather surprising, given that
the Atom% Excess (APE) 13C and 15N for nematodes is known to be most sensitive to
enrichment (Crotty et al., 2011). Only arable fields and grasslands are shown: loamy
soils (41 sites, 1094 adults and 4936 juveniles) versus sandy soils (96 sites, 3504
adults and 10,819 juveniles); raw data from Mulder and Vonk (2011).
(Fig. 12): here, a log-linear decrease of mites and collembolans with decreasing
soil fertility (higher nutrient ratios), in contrast to a curvilinear increase of
bacterivore nematodes and fungi (cf. Santos et al., 1981). Therefore, regardless
of the kind of environmental adversity, soil mesofauna might increase over-
proportionally in enriched systems such as the real food web plotted on the
background of the four scatter-plots (a reference site marked by a cross) in
the composite (Fig. 16).
The results support the stoichiometric theory (Elser, 2006; Mulder and
Elser, 2009; Sterner and Elser, 2002) which predicts that animals with higher
P demands would suffer a competitive disadvantage due to poor
stoichiometric food quality. In Fig. 16, omnivorous species with lower P
demands are favoured. This seems to be the case within our soil
3.5 3.5
A 2
R = 0.8147 B 2
R = 0.7092
Log ratio microfauna to mesofauna
3 3
2.5 2.5
2 2
1.5 1.5
1 1
0.5 0.5
0 0
7.5 8 8.5 9 9.5 10 10.5 11 11.5 12 0.9 1 1.1 1.2 1.3 1.4 1.5 1.6 1.7 1.8
Soil pOH Log10[C] - log10[N]

3.5 3.5
2 2
R = 0.6114 R = 0.7144
C D
3 3
2.5 2.5
2 2
1.5 1.5
1 1
0.5 0.5
0 0
0.1 0.3 0.5 0.7 0.9 1.1 1.3 1.5 1.2 1.4 1.6 1.8 2 2.2 2.4 2.6 2.8 3 3.2
Log10[N] - log10[P] Log10[C] - log10[P]
Figure 16 Another example of trophic effect and trophic response traits (cf. Fig. 13). Log-
arithmic fits of differently body-size-scaled soil invertebrates across four quantitative
gradients of increasing environmental adversity as described by pOH (A), log-
transformed C:N ratio (B), N:P ratio (C) and C:P ratio (D) for Dutch dry heathlands (●),
abandoned grasslands (♦) and bio-organic farms (■). Lower soil fertility as in the heath-
lands plotted at the right of the scatters enhances the steepness of the microfauna to
mesofauna ratio. Springtails and enchytraeids get eliminated, relative to the over-
whelming increase of nematodes, by decreasing [N] and [P].
mesofauna, given that the P contents in the bodies of (predatory) mites are up
to three times lower than in detritivorous collembolans (0.5 body % P-in-
Acari vs. 1.4 body % P-in-Collembola; Martinson et al., 2008 and Schneider
et al., 2010, respectively). This means that invertebrates at higher trophic
levels have a higher P demand than those at lower trophic levels, at least in
the brown world. However, during the lifetime of metazoans, the P
demand is not necessarily inversely related to the P content as adult (like
the aforementioned mites with lower P content than other groupings
within the same taxocene); the P demand can, in fact, be needed during
growth for structural components like bony skeleton. In the case of fishes,
for instance, P demand and P content remain directly correlated with each
other (Lauridsen et al., 2012; Sterner and George, 2000).
Therefore, ecological stoichiometry and classical prey–predator chains
coexist and contribute to explain apparent difficulties in the application of
the Lotka–Volterra model in reality. Still, the possibility of a kind of top-
down control has to be taken into account (Wardle, 1999) and causal rela-
tionships must be directional and quantitative, such as the pathway analyses
performed by Perner and Voigt (2007) and Voigt et al. (2007). Comparing
this stoichiometric perspective across soil systems with the large number of
terrestrial B–EF studies, it remains surprising that the plea of Chase (2000) to
address phosphorus in terrestrial ecosystem types has remained largely
ignored by so many soil ecologists (but see Lynch and Ho, 2005).
7. CODA
Macroecology and ecological stoichiometry encompass a wide variety of
large-scale phenomena (cf. Gardner et al., 2001; Hall, 2009; Sterner and Elser,
2002), and allometric scaling can link large-scale macroecology to either
species- or community levels (Yodzis and Innes, 1992). Together, allometry
and ecological stoichiometry are suitable measures to catch the emergent
characteristics of large data sets distributed in time and space and offer a
reliable tool to outflank difficulties in the environmental assessment of
disturbed ecosystems. Like Yodzis and Innes (1992), we argue that allometry
and food web theory can be successfully integrated, even if the coupling
between biodiversity and EF is less stringent than commonly assumed.
In 2004, the plea for the conservation of ecosystem structure and func-
tioning as priority target came from the United Nations (UNEP/CBD,
2004). Alas, biological findings are often not strengthened for stakeholders
and policy-decision makers (Mann, 1991). Many of the studies of the
predominance of quarter-power scaling in biology have remained purely

descriptive so far, although there are exciting hints of a mechanistic expla-
nation for observed patterns in EF. The evenness in the structure of a food
web can be captured by allometric scaling and when the
resulting mass–abundance relationship is close to isometry, its
equitability roughly implies biomass evenness across trophic levels. Such
‘allometric metrics’ can take into account traits like the average body size
of given species that may often be independent from environmental
predictors, indirectly supporting the historical critique on biodiversity
by Hurlbert (1971).
Our survey on the understanding of B–EF relationships includes aspects
of taxonomic diversity, functional categorization and metabolic scaling as
well as rules for their appropriate use. Given the well-known role of traits
as predictors of niche complementarity and community structures, we have
considered empirical examples examining how biodiversity supports EF. As
model organisms, we chose fishes, plants and invertebrates and highlighted
distributional (in)congruences of these organisms, the current state of the
field and future challenges. Our review of independent case studies from
the blue, the brown and the green worlds shows that biodiversity (at least
the taxonomic diversity) as the key predictor for EF and multitrophic inter-
actions like those described in food web theory may be overemphasized.
There is an urgent need to galvanize ecologists from different subdisciplines,
bringing them together for so many existing questions (Carpenter et al.,
2009). A greater synergy between theoretical and empirical disciplines dur-
ing the construction of null hypotheses is necessary to allow a careful differ-
entiation between experimental design and EF. In the past, research on EF
was often diluted by a dichotomy between empirical reports (often as grey
literature), novel biology journals and theoretical journals, complicating data
mining of disparate data sets. Hence, generalization without oversimplifica-
tion becomes an important objective in its own right, with the ability to
identify traits that underlie species responses and ecological processes
(Grime, 1997). Such responses, especially when aggregated up to the biome
level, can provide critically important ways to predict ecosystem responses to
environmental changes at a global scale (Wall et al., 2008).
ACKNOWLEDGEMENTS
Anton M. Breure, Chris Holmes, Michael A. Huston, Katherine Kapo, Owen Lewis,
Giorgio Mancinelli, Shahid Naeem, Loreto Rossi, Torbjörn Säterberg, Paulo Sousa, Guy
Woodward and one anonymous referee with helpful comments on the earlier version of
this paper are gratefully acknowledged. We thank Microsoft Research for supporting the
development of Network3D, and Dennis Mischne, of the Ohio Environmental
Protection Agency, for making available biological monitoring data. S. M. thanks for the
financial support by KAKENHI Grants-in-Aid for Scientific Research (MEXT No.
22658051 and 23380094); J. A. V. acknowledges the WOTRO co-funding by the
Netherlands Foundation for the Advancement of Tropical Research (W86-168); M. K.
acknowledges the NSF funding No. 090221 (Collaborative Research RUI); A. G. R.
acknowledges a Beaufort Marine Research Award, funded under the Marine Research
Sub-Programme of the Irish National Development Plan; D. H. W. acknowledges the
NSF funding to the McMurdo Dry Valley LTER.
APPENDIX
A B
P Z F
BµM1/4 BµM0
Log N
EµM0
Log N
EµM–1/4
NµM–3/4 NµM–1
Log M Log M
C D
Landscapes
Forests
Log time
Log time
Stands
Crowns
Leaves
Log S Log M
Figure A1 Allometric scaling and diversity–yield relationships. Upper panel: dashed lines
describe three log–log relationships between species average weight M and species den-
sity N for total biomass B, upper line, energy rate E, middle line, and mass–abundance
for pelagic food webs across trophic levels (A) and
scaling, lower line, as function of M
within three taxocenes, namely the phytoplankton P, the zooplankton Z and the fishes
F (B). Lower panel: dynamic domains of scale (S) in time occupied by different entities
enable to address the variation in ecological processes across the discrete boundaries
of the investigated domains (C) and allow taking into consideration relationships into
a similar space-time domain (D). Adapted from Brown and Gillooly (2003), the upper
panels (A, B), and from Kerkhoff and Enquist (2007), the lower panels (C, D).
50
45
Nematode species richness 40
35
30
25
20
15
10
40
35
30
Exponential Shannon’s index
25
20
15
10
0
0 10 20 30 40 50 60 70 80
Molar N:P ratio
Figure A2 Soil abiotics and diversity–yield relationships for free-living nematodes. Di-
versity metrics that combine species richness with relative abundance, like the so-called
Hill numbers (here the exponential Shannon-Wiener index as in Hill, 1973), are not in-
dependent from the (number of) species themselves. We have chosen the molar N:P
ratio as proxy for the productivity of agroecosystems (Mulder and Vonk, 2011). If so, pro-
ductive sites show a higher value of the exponential Shannon-Wiener index (bottom)
and a higher amount of nematode species (top). Hence, in more productive sites, spe-
cies are more even in their spatial distribution than in less productive sites.
Interspecific and intraspecific interactions
L=1 L=4
S2 = 1 S2 = 4
A A B
A B
L=9
S2 = 9
C
Only interspecific interactions
A* A B
L=0 L=2
S × (S-1) = 0 S × (S-1) = 2
A B
L=6
S × (S-1) = 6
C
Figure A3 The extent to which one species (A) will feed on other species (here, B and C)
can be quantified by species connectivity according to metrical computations (explana-
tions in the text). Within one taxocene, Ct fluctuates between 0% (no trophic links at all)
and 100% (maximal aggressive behaviour) for both interspecific and intraspecific inter-
actions (directed connectance, upper panel) as for interspecific interactions only (inter-
active connectance, no cannibalistic links; lower panel). Here we show the maximal
number of possible trophic interactions within the same taxocene (Ct ¼ 100%), besides
the unique case of the polar nematode Scottnema (this most extreme condition—
marked by an asterisk—exhibits L ¼ 0, S (S 1) ¼ 0 and therefore Ct ¼ 0% in A*). Many
realized trophic links are suggested to reflect a dominance of generalists (high species
connectivity implies high omnivory and aggressive feeding behaviour, therefore high
resilience at taxocene level), in contrast to a low proportion of realized trophic links,
which reflects a skew towards specialists and immature life stages (low species connec-
tivity: low resilience).
OHIO, USA
3935990
13153379
13156205
3935996 15588706
13156389
57 15644284
15614706
61
15400342
55 0 50 100 km
3985304
5218143
15433162 18 Selected COMIDs
15419475 15420673
25243971 Level III Ecoregions
5233068 Eastern Corn Belt Plains
5231404 Eastern Great Lakes and Hudson Lowlands
70
3935990 Erie Drift Plain
Little Miami River 25243971

3935996
Huron/Erie Lake Plains
Interior Plateau
Southern Michigan/Northern Indiana Drift Plains
3489095 Western Allegheny Plateau
Figure A4 Geographical location of the 18 freshwater assemblages randomly selected

after allometric screening (Fig. A5). The rivers Scioto Brush Creek, Hocking (two times),
Big Darby Creek, Paint Creek (two times), Blanchard, Duck Creek, Little Miami (three
times), Buck Creek, Sandusky, Walhonding, Mahoning (three times) and Cuyahoga were
sampled between 2000 and 2007. Many locations (like those in Figs. 10 and A6) are in
the Eastern Corn Belt Plains (Ecoregion 55), the most variable in total phosphorus
(CV ¼ 88.6%), biochemical oxygen demand (85.5), chemical oxygen demand (118.6),
nitrite (125.0), ammonia (231.4) and total suspended solids (153.8), and the least
variable in hardness (CV ¼ 22.6%), nitrate (44.4), conductivity (24.6) and total
dissolved solids (25.4). Ecoregions as defined in: http://www.eoearth.org/article/
Ecoregions_of_Indiana_and_Ohio_%28EPA%29. GIS credit: Katherine Kapo.
15
Sampling by wading
Sampling by boat
13
Boat-sampled selection
SE for the fresh weight estimates
11
1
2 10 18 26 34 42 50 58
Fish species diversity
Figure A5 Possible effects of sampling methods associated with the allometric model
on uncertainty were investigated by selecting 2656 locations in Ohio sampled either by
boat or by wading. The uncertainty in the allometric estimates of the mean fresh bio-
mass (|SE| in grams) of the smallest fish populations in each fish assemblage shows that
the kind of sampling (boat or wading) and, indirectly, the river type (large, tributary,
etc.), inflates biomass estimates in low-diversity communities, supporting that boat
sampling provides the best estimates. As differences in sampling efforts are important
for appropriate data mining and computations, we confined our further analyses in the
aforementioned boat-sampled locations (Figs. 8 and A6; Table 5).
Scioto Brush Creek: species deletions

A 100 B 1.8
90
Species deleted (%)
1.6
80
1.4
Magnitude
70
1.2
60
1
50
0.8
40
30 0.6
20 0.4
10 0.2
0 0
0 5 10 15 20 25 30 35 40 45 50 0 5 10 15 20 25 30 35 40 45 50
Primary deletions (%) Primary deletions (%)
Eastern Paint Creek: species deletions

C 100 D 1.8
90 1.6
Species deleted (%)
80 1.4
70
Magnitude
1.2
60
1
50
0.8
40
0.6
30
20 0.4
10 0.2
0 0
0 5 10 15 20 25 30 35 0 5 10 15 20 25 30 35
Primary deletions (%) Primary deletions (%)

Connectance MeanSWTL
%PD %SD %Total
CharPathLen MeanClusterCoeff
Rel. L/S
Figure A6 Two case studies in central Ohio on static species deletion scenario ‘connec-
tivity descending’. The creeks are both tributaries of the Scioto River. The fish assem-
blages have different vulnerabilities to secondary deletions (Table 5; Fig 9). Data on
the left have been normalized for comparison. (A) The Scioto Brush Creek web with
n ¼ 30 only shows secondary deletions (% SD) from 15–50% of primary deletions
(% PD) until its final collapse. At the beginning, secondary extinctions are less than pri-
mary extinctions, becoming equal to (and later more than) primary extinctions (dashed
line indicates x ¼ y). (B) The Scioto Brush Creek's web properties during the species
deletion process, with the relative linkage density L/S quickly decreasing as highly
connected nodes disappear from the web. (C) In contrast to the previous river, the East-
ern Paint Creek with n ¼ 24 immediately shows more secondary extinctions than pri-
mary extinctions (line above the 1:1 dashed line). The food web collapses after only
33% of primary extinctions. (D) Most Paint Creek's web properties behave similarly to
those in (B).
Table A1 Occurrence and site-specific body mass (wet weight) of freshwater fishes in the 18 investigated rivers across Ohio
Weight (average of individual measurements in grams) versus COMID (7- and 8-digit code, GIS location in Fig. A4)
Species (Latin Please check whether the entries are aligned properly in this table. binomial, qualitative) Behavioural Level (1 or 2, numeric)
3489095 3935990 3935996 3985304 5218143 5231404 5233068 13153379 13156205 13156389 15400342 15419475 15420673 15433162 15588706 15614706 15644284 25243971
Ambloplites rupestris 2
36.0 113.3 115.0 46.7 48.3 32.0 0 25.0 0 0 120.0 90.0 0 62.0 110.0 61.8 93.7 120.0
Ameiurus natalis 2
0 0 0 0 0 0 0 0 0 0 54.0 0 0 0 177.0 0 202.0 0
Amia calva 2
0 0 0 0 0 0 0 0 0 0 1040.0 0 0 0 0 0 0 0
Ammocrypta pellucida 2
0 0 0 0 0 0 0 2.0 0 0 0 0 0 0 0 0 0 0
Aplodinotus grunniens 2
2382.1 865.0 1692.8 0 1100.0 677.2 0 0 0 0 2100.0 0 0 254.5 0 0 545.5 492.1
Campostoma anomalum 1
0 6.3 8.2 20.3 9.2 8.3 0 0 0 0 21.4 0 5.0 0 0 0 0 10.0
Carpiodes carpio 1
0 905.0 1028.0 0 1350.0 601.3 750.0 0 0 0 0 583.3 900.0 0 0 0 0 961.4
Carpiodes cyprinus 2
1400.0 991.7 0 0 1425.0 4.5 0 0 0 0 1100.0 384.2 400.0 140.0 0 0 0 0
Table A1 Occurrence and site-specific body mass (wet weight) of freshwater fishes in the 18 investigated rivers across Ohio—cont'd
Carpiodes velifer 1
700.0 631.3 0 0 0 261.7 0 0 0 0 650.0 0 0 0 0 0 0 703.0
Catostomus commersonii 1
0 0 0 178.1 0 0 245.0 202.4 242.4 4.0 0 3.0 0 160.0 907.8 154.5 571.4 0
Cottus bairdii 2
0 0 0 9.0 0 0 0 0 0 0 0 2.5 1.0 0 0 0 0 0
Cyprinella spiloptera 2
2.0 4.0 4.6 0 3.0 4.1 2.5 5.0 0 3.3 3.4 3.7 3.5 2.4 0 5.1 4.7 3.5
Cyprinella whipplei 2
0 8.8 4.6 0 0 2.0 0 0 0 0 0 0 6.0 0 0 0 0 3.6
Cyprinus carpio 2
0 2083.3 2511.0 1681.3 2994.4 0 1460.0 0 4911.8 1787.5 1495.7 2317.9 2236.1 3400.0 3012.5 2150.0 2338.5 2366.7
Dorosoma cepedianum 1
135.5 66.0 176.5 0 347.1 247.9 89.4 46.0 5.0 51.7 114.2 422.0 60.9 104.5 0 0 9.0 234.3
Erimystax dissimilis 1
0 0 0 0 8.9 2.0 0 0 0 0 8.6 0 0 0 0 0 0 0
Erimystax x-punctata 1
0 0 8.0 0 0 5.8 0 0 0 0 4.0 0 0 0 0 0 0 0
Continued
Esox americanus 2
0 0 0 0 0 0 0 52.5 38.6 0 0 12.0 5.0 0 15.0 0 0 0
Esox lucius 2
0 0 0 0 0 0 0 0 0 0 0 0 0 0 2400.0 0 0 0
Esox masquinongy 2
0 0 0 0 0 0 0 0 3991.7 0 0 0 0 0 0 0 0 0
Etheostoma blennioides 1
2.0 8.0 3.9 6.8 3.1 3.3 1.0 0 4.0 0 3.3 4.0 1.0 0 0 0 5.0 5.0
Etheostoma caeruleum 2
0 3.0 1.0 2.8 1.4 1.0 0 0 0 0 0 0 0 0 0 0 0 2.0
Etheostoma camurum 1
0 0 0 0 2.1 1.8 0 0 0 0 4.0 0 0 0 0 0 0 0
Etheostoma flabellare 2
0 0 0 0 0 0 0 7.3 0 0 0 0 0 2.0 0 0 0 0
Etheostoma nigrum 2
2.0 0 0 0 0 0 0 1.4 2.0 0 0 0 0 0 0 0 0 0
Etheostoma tippecanoe 1
0 0 0 0 0.8 1.4 0 0 0 0 0 0 0 0 0 0 0 0
Etheostoma variatum 1
0 4.0 4.9 0 7.5 2.5 0 0 0 0 3.6 0 0 0 0 0 0 5.0
Etheostoma zonale 1
0 4.0 1.8 2.1 0.8 1.7 0 2.0 0 0 1.0 1.5 1.3 0 0 0 0 1.9
Fundulus notatus 2
2.5 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2.0 0
Hiodon tergisus 2
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 217.0
Hypentelium nigricans 1
130.0 203.3 160.9 156.4 178.1 118.7 95.5 94.7 243.3 0 93.6 172.2 108.2 45.7 0 150.0 200.5 88.7
Ichthyomyzon fossor 1
0 0 0 0 0 0 0 12.5 0 0 0 0 0 0 0 0 0 0
Ictalurus punctatus 2
675.0 1512.5 1960.0 0 808.0 1.0 516.7 0 520.0 882.5 1757.1 1450.0 832.0 1115.0 0 0 250.0 1363.5
Ictiobus bubalus 1
0 2252.5 2215.7 0 0 1500.0 0 0 0 0 0 0 0 0 0 0 0 2500.0
Ictiobus cyprinellus 1
0 0 0 0 0 1900.0 0 0 0 0 0 0 0 0 0 0 0 1500.0
Ictiobus niger 1
0 0 0 0 450.0 0 0 0 0 0 0 0 0 0 0 0 0 0
Continued
Labidesthes sicculus 1
1.3 0 0 0 0 0 0 0 0 2.8 0 0 0 0 0 0 0 0
Lampetra aepyptera 1
0 0 0 0 0 0 0 0 0 0 0 11.0 0 0 0 0 0 0
Lepisosteus osseus 2
1000.0 0 725.5 0 410.0 0 0 0 0 0 0 0 0 0 0 0 0 120.0
Lepomis cyanellus 2
90.0 22.5 0 0 0 20.0 52.5 9.3 9.6 0 0 18.3 0 0 0 6.7 23.9 0
Lepomis gibbosus 2
0 0 0 0 0 0 0 25.0 90.0 0 0 0 0 0 37.4 0 0 0
Lepomis gulosus 2
0 0 0 0 0 0 0 60.0 0 0 0 0 0 0 0 0 0 0
Lepomis macrochirus 1
46.7 21.0 0 9.3 15.4 45.0 11.7 42.2 33.3 135.0 40.0 22.5 36.2 0 25.5 80.0 80.0 76.7
Lepomis megalotis 1
10.2 63.5 32.3 0 20.5 21.8 27.5 0 0 0 0 32.0 0 13.3 0 0 25.9 14.8
Lepomis microlophus 1
0 0 0 0 0 25.0 0 0 0 0 60.0 0 0 0 0 0 0 0
Luxilus chrysocephalus 1
4.3 2.0 2.0 28.0 0 3.0 2.0 0 0 0 2.0 0 0 0 0 0 0 0
Luxilus cornutus 1
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 21.1 0 0
Lythrurus fasciolaris 1
0 0 0 0 0 0 2.5 0 0 0 0 0 0 0 0 0 0 0
Lythrurus umbratilis 1
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2.0 0
Micropterus dolomieux 2
712.5 314.3 105.3 124.3 202.7 183.3 326.2 525.0 340.0 168.3 110.3 100.0 159.4 44.0 0 106.7 200.0 124.7
Micropterus punctulatus 2
46.8 140.0 0 0 192.5 49.4 0 0 0 0 187.0 475.0 96.0 170.0 0 0 0 10.0
Micropterus salmoides 2
57.5 90.0 0 0 15.0 0 85.0 70.0 134.3 621.6 233.3 11.3 2.3 169.5 171.8 0 85.7 0
Minytrema melanops 1
96.3 0 0 0 0 0 90.7 60.0 0 0 0 0 0 60.0 697.5 0 167.8 0
Morone chrysops 2
0 190.0 0 0 250.0 0 0 0 0 0 0 0 0 100.0 0 0 0 0
Morone saxatilis 2
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 220.0
Continued
Moxostoma anisurum 1
379.4 2075.0 2050.0 0 2150.0 1050.0 1240.0 0 0 0 855.3 560.0 728.8 413.9 0 0 0 1866.7
Moxostoma breviceps 1
51.7 296.0 416.3 0 0 285.0 295.0 0 0 0 229.1 0 0 0 0 0 0 215.2
Moxostoma carinatum 1
0 1950.0 0 0 2065.0 0 0 0 0 0 2245.5 0 0 550.0 0 0 0 0
Moxostoma duquesnei 1
78.3 714.5 814.8 476.9 153.8 700.0 650.0 0 0 0 330.0 750.0 0 0 0 0 0 379.3
Moxostoma erythrurum 1
48.6 526.0 559.6 450.0 398.6 7.3 384.5 51.3 0 0 171.5 391.3 331.0 176.8 0 166.2 386.5 372.8
Moxostoma macrolepidotum 1
0 0 0 0 447.5 0 0 0 0 0 0 0 0 100.0 0 0 0 0
Nocomis biguttatus 1
0 0 0 0 0 0 0 0 7.9 0 0 0 0 0 0 0 0 0
Nocomis micropogon 2
0 0 20.0 0 0 0 0 43.2 0 0 6.0 0 0 0 0 0 0 0
Notemigonus crysoleucas 1
0 0 0 0 0 0 0 0 15.0 0 0 0 0 0 17.4 0 0 0
Notropis amblops 1
0 0 0 0 0 0 0 0 0 0 2.4 0 0 0 0 0 0 0
Notropis atherinoides 1
3.0 2.3 1.7 0 0 2.0 0 0 0 0 0 0 0 1.9 0 0 18.7 1.1
Notropis buccatus 1
0 0 0 0 0 0 0 0 0 0 0 1.5 0 0 0 0 0 0
Notropis photogenis 1
2.0 0 2.0 9.2 5.8 2.0 5.9 0 0 0 8.7 0 0 0 0 0 0 0
Notropis rubellus 2
0 0 2.0 0 0 0 0 0 0 0 2.9 2.0 0 0 0 0 0 0
Notropis stramineus 2
0 0 2.3 0 1.9 1.2 0 0 0 0 2.0 2.0 2.5 0 0 0 3.0 1.5
Notropis volucellus 1
0 3.0 2.3 0 0 0 0 0 0 0 2.0 0 0 0 0 0 0 1.5
Noturus eleutherus 2
0 2.0 3.0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Noturus flavus 2
0 30.0 8.2 0 0 7.1 0 0 0 0 6.0 0 0 0 0 40.0 0 10.0
Noturus miurus 2
0 0 0 0 0 5.0 0 0 0 0 0 0 0 0 0 0 0 0
Continued
Noturus stigmosus 2
0 0 6.0 0 0 5.0 0 0 0 0 0 0 0 0 0 0 0 1.0
Perca flavescens 2
0 0 0 0 0 0 0 70.9 46.4 18.0 0 26.0 0 0 0 0 0 0
Percina caprodes 2
7.6 16.0 8.6 17.0 15.5 12.5 14.9 18.5 0 0 11.0 13.0 0 0 0 0 0 6.3
Percina maculata 2
0 0 0 0 0 0 0 0 0 0 4.0 0 0 0 0 0 0 0
Percina phoxocephala 1
0 4.0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 6.0
Percina sciera 1
0 0 0 0 0 0 0 0 0 0 0 0 12.0 0 0 0 0 0
Percopsis omiscomaycus 2
0 0 0 0 0 0 0 0 0 0 0 0 1.3 0 0 0 0 0
Phenacobius mirabilis 1
0 0 4.5 0 0 3.0 0 0 0 0 0 0 0 0 0 0 0 7.0
Pimephales notatus 1
2.6 2.9 2.7 8.0 3.0 1.4 2.0 3.0 4.0 3.8 2.3 0.8 2.5 0 0 3.0 3.1 1.6
Pimephales vigilax 2
0 2.0 1.0 0 0 2.0 0 0 0 0 0 0 0 0 0 0 0 2.4
Pomoxis annularis 2
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 80.0 116.0 0
Pomoxis nigromaculatus 2
0 0 200.0 0 0 0 215.0 0 51.8 250.0 280.0 0 0 0 139.7 0 0 0
Pylodictis olivaris 2
2700.0 1747.5 338.7 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2020.0
Semotilus atromaculatus 2
0 0 0 29.0 0 0 0 0 0 0 0 0 0.9 0 0 0 5.0 0
Stizostedion canadense 2
0 290.0 0 0 388.0 0 0 0 0 0 0 0 0 137.5 0 0 0 379.0
Stizostedion vitreum 2
0 0 484.0 0 0 0 0 150.0 0 455.6 0 0 0 0 0 0 0 0
Umbra limi 2
0 0 0 0 0 0 0 0 4.0 0 0 0 0 0 0 0 0 0
Please note: Occurrence (if present, weight is provided) and behavioural level: 0 = fish species absent in a given site; 1 = all fish species feeding upon preys from other taxocenes; 2 = piscivorous
fishes predating within their own taxocene but not within their own population (cannibalism excluded). All feeding traits and fish taxonomy according to www.FishBase.org version June 2011
accessed August 2011.
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Biodiversity, Species Interactions
and Ecological Networks in a
Fragmented World
Melanie Hagen*, W. Daniel Kissling*, Claus Rasmussen*,
Marcus A.M. De Aguiar{, Lee E. Brown{, Daniel W. Carstensen*,
Isabel Alves-Dos-Santos}, Yoko L. Dupont*, Francois K. Edwards},
Julieta Genini||, Paulo R. Guimarães Jr.}, Gareth B. Jenkins#,
Pedro Jordano**, Christopher N. Kaiser-Bunbury*, Mark E. Ledger{{,
Kate P. Maia}, Flavia M. Darcie Marquitti}, Órla Mclaughlin{{,}},
L. Patricia C. Morellato||, Eoin J. O'Gorman#, Kristian Trøjelsgaard*,
Jason M. Tylianakis}}, Mariana Morais Vidal}, Guy Woodward#,
Jens M. Olesen*,1
*Department of Bioscience, Aarhus University, Aarhus, Denmark
{
Instituto de Fı́sica Gleb Wataghin, Universidade Estadual de Campinas, Campinas, São Paulo, Brazil
{
School of Geography, University of Leeds, Leeds, United Kingdom
}
Departamento de Ecologia, Instituto de Biociências, Universidade de São Paulo, São Paulo, São Paulo, Brazil
}
Centre for Ecology and Hydrology, Wallingford, United Kingdom
‖
Departamento de Botânica, Laboratório de Fenologia, UNESP Univ Estadual Paulista, Rio Claro, São Paulo, Brazil
#
School of Biological and Chemical Sciences, Queen Mary University of London, London, United Kingdom
**Integrative Ecology Group, Estación Biológica de Doñana, CSIC, Sevilla, Spain
{{
School of Geography, Earth and Environmental Sciences, University of Birmingham, Edgbaston,
Birmingham, United Kingdom
{{
Environmental Research Institute, University College Cork, Cork, Ireland
}}
School of Biological, Earth, and Environmental Sciences, University College Cork, Cork, Ireland
}}
School of Biological Sciences, University of Canterbury, Christchurch, New Zealand
1
Corresponding author: e-mail address: jens.olesen@biology.au.dk
Contents
1. Introduction 91
2. Networks 94
2.1 Ecological networks 94
2.2 Spatial networks 100
2.3 Combining spatial and ecological networks 101
3. Habitat Fragmentation 103
3.1 General introduction 103
3.2 Fragment characteristics 107
3.3 Habitat edges 111
3.4 Matrix 114
3.5 Spatial and temporal turnover of species and individuals 117
3.6 Scales of habitat fragmentation 118
Advances in Ecological Research, Volume 46 # 2012 Elsevier Ltd. 89

http://dx.doi.org/10.1016/B978-0-12-396992-7.00002-2
90 Melanie Hagen et al.
4. Habitat Fragmentation and Species Traits 121

4.1 Plant traits 122
4.2 Animal traits 123
4.3 Species trait combinations 126
5. Habitat Fragmentation and Biotic Interactions 129
5.1 Mutualistic plant–pollinator interactions 129
5.2 Mutualistic plant–frugivore interactions 131
5.3 Mutualistic plant–ant interactions 132
5.4 Antagonistic interactions within food webs 134
5.5 Antagonistic host–parasitoid interactions 135
5.6 Summary of fragmentation effects on mutualistic and antagonistic
interactions 136
6. Effects of Habitat Fragmentation on Different Kinds of Networks 138
6.1 General introduction 138
6.2 Mutualistic plant–pollinator networks 138
6.3 Mutualistic plant–frugivore networks 150
6.4 Mutualistic plant–ant networks 153
6.5 Antagonistic food webs 154
6.6 Antagonistic host–parasitoid networks 160
6.7 General effects of habitat fragmentation on network properties 162
7. Habitat Fragmentation in a Meta-Network Context 164
7.1 Meta-networks and dispersal 166
7.2 Meta-networks and extinction 166
7.3 Meta-networks and colonisation 167
8. Effects of Habitat Fragmentation on the Coevolutionary Dynamics of Networks 169
8.1 The geographic mosaic theory of coevolution 169
8.2 Habitat fragmentation and its effects on basic components of GMTC 170
8.3 Habitat fragmentation and selection mosaics in ecological networks 171
9. Applications in Conservation and Agriculture 172
10. Conclusions 175
Acknowledgements 177
Appendix 177
References 181
Abstract
Biodiversity is organised into complex ecological networks of interacting species in local
ecosystems, but our knowledge about the effects of habitat fragmentation on such sys-
tems remains limited. We consider the effects of this key driver of both local and global
change on both mutualistic and antagonistic systems at different levels of biological
organisation and spatiotemporal scales.
There is a complex interplay of patterns and processes related to the variation and
influence of spatial, temporal and biotic drivers in ecological networks. Species traits
(e.g. body size, dispersal ability) play an important role in determining how networks
respond to fragment size and isolation, edge shape and permeability, and the quality of
Biodiversity, Species Interactions and Ecological Networks in a Fragmented World 91
the surrounding landscape matrix. Furthermore, the perception of spatial scale (e.g.
environmental grain) and temporal effects (time lags, extinction debts) can differ mark-
edly among species, network modules and trophic levels, highlighting the need to
develop a more integrated perspective that considers not just nodes, but the struc-
tural role and strength of species interactions (e.g. as hubs, spatial couplers and
determinants of connectance, nestedness and modularity) in response to habitat
fragmentation.
Many challenges remain for improving our understanding: the likely importance of
specialisation, functional redundancy and trait matching has been largely overlooked.
The potentially critical effects of apex consumers, abundant species and super-
generalists on network changes and evolutionary dynamics also need to be addressed
in future research. Ultimately, spatial and ecological networks need to be combined to
explore the effects of dispersal, colonisation, extinction and habitat fragmentation on
network structure and coevolutionary dynamics. Finally, we need to embed network
approaches more explicitly within applied ecology in general, because they offer great
potential for improving on the current species-based or habitat-centric approaches
to our management and conservation of biodiversity in the face of environmental
change.
1. INTRODUCTION
The planet’s ecosystems are losing biodiversity at an accelerating rate
(Dyer et al., 2010; Fahrig, 2003; Gonzalez et al., 2011; Millennium
Ecosystem Assessment, 2005) due to land-use change, deforestation,
agricultural intensification, pollution, urbanisation, climate change and
habitat fragmentation (Albrecht et al., 2007; Hanski, 2005; Ledger et al.,
2012; Meerhoff et al., 2012; Mintenbeck et al., 2012; Tilman et al.,
2001). The latter in particular could severely disrupt ecological networks
and the goods and services they provide (e.g. pollination in mutualistic
webs or biological control in food webs) as it is a rapidly growing
phenomenon throughout the world, yet its impacts on the higher
multispecies levels of organisation are still poorly understood.
A major challenge for predicting the consequences of changes on biodi-
versity is to understand the complexity of natural systems and the steps
needed to conserve them in a rapidly changing world. Biodiversity is
organised at local scales into complex networks of interacting species, which
provide the ecosystem processes that ultimately underpin the goods and ser-
vices of value to human societies (Rossberg, 2012). These links (italicised
terms, see Glossary) among interacting species are often ignored in the
context of global change even though they will disappear from local
communities as a precursor to local (and ultimately global) extinctions

(Albrecht et al., 2007; Fortuna and Bascompte, 2006; Sabatino et al.,
2010; Tylianakis et al., 2007; Woodward et al., 2010a). Understanding
the causes and consequences of the loss of species interactions therefore
promises to provide critical new insights into ecological responses to
perturbations (Mulder et al., 2012; Tylianakis et al., 2010).
The interplay between the abiotic environment and biotic complexity
over space and time makes natural ecosystems seemingly difficult to under-
stand. One simplifying approach is to study interactions among multiple
species in the framework of ecological networks (e.g. Fortuna and
Bascompte, 2008). These include both mutualistic (e.g. pollination, seed
dispersal networks) and antagonistic (e.g. food webs, host–parasitoid networks)
interactions, which could respond differently to disturbances, such as
fragmentation, which in turn determines their stability in terms of resilience,
resistance and robustness (Ings et al., 2009; Layer et al., 2010, 2011;
Woodward et al., 2010a).
Landscape changes may be caused by physical processes, biotic drivers
such as ecological engineers, and/or anthropogenic influences. Species will
reshuffle their population sizes and some links between species might be
rewired or break apart entirely (Tscharntke et al., 2005). Any seemingly re-
stricted spatiotemporal disturbance may ripple throughout the network of
interacting species, causing further (i.e. secondary) species and link pertur-
bations. New data analytical tools, such as network analysis, now form an
essential ingredient in the study of complex systems, with clear implications
for biodiversity research (Heleno et al., 2009; Kremen and Hall, 2005;
Tylianakis et al., 2008).
Habitat fragmentation is almost ubiquitous in both natural and human-
modified landscapes (Fig. 1), with consequences for biodiversity and species
interactions (Fahrig, 2003; Laurance et al., 2011; Tylianakis et al., 2007),
which in turn has implications for the entire ecological network. It
reduces habitat area and species connectivity, and the sizes and isolation
of remaining fragments are particularly critical to the long-term conservation
of biodiversity. Connectivity among fragments, the characteristics of the
matrix, the availability of corridors for movement between fragments, and
the permeability and structure of habitat edges are all important in this
context and affect the structure, persistence and strength of species
interactions (Fortuna and Bascompte, 2006). Certain species traits (e.g.
body size, dispersal ability, degree of specialisation or trophic rank) are
likely to be particularly crucial for assessing the higher-level consequences
A B
C D
E F
Figure 1 The ubiquity of fragmentation. Selected examples of common naturally and

artificially fragmented habitats from terrestrial and aquatic ecosystems, with hard
(aquatic–terrestrial) versus soft (aquatic–aquatic, terrestrial–terrestrial) boundaries.
From top left to bottom right are (A) pingos in the arctic; (B) tropical atoll islands;
(C) temperate river network and associated off-river habitats; (D) agricultural landscape
in Spain; (E) a portion of the Great Barrier Reef and (F) forest clearance in Amazonia.
of habitat fragmentation (Ewers and Didham, 2006), so functional attributes

may be just as important as taxonomic diversity in this context. The
invasion of functionally similar species, for example, may homogenise
ecological processes (McKinney and Lockwood, 1999; Olden et al., 2004).
Species at higher trophic levels, or with particular traits, that connect
different fragments or network modules, may act as important spatial couplers

or network stabilisers, essentially operating as network-level keystones.
Both the physical and biological worlds can be seen as networks
(Gonzalez et al., 2011): a (spatial) landscape network of habitat fragments
that provides the underlying matrix and habitat connectivity, and an ecolog-
ical species interaction network, driven by ecological and evolutionary pro-
cesses. Interactions between such different kinds of networks occur, but to
date such multiple interdependent networks have mainly been studied out-
side ecology (Buldyrev et al., 2010) and the consequences of habitat frag-
mentation on these (often interdependent) biological–physical systems
remain largely unexplored.
Here, we synthesise current knowledge about the consequences of hab-
itat fragmentation on different types of biodiversity within ecological net-
works. We begin by introducing the major characteristics and types of
ecological and spatial networks. We then review the spatial and temporal set-
tings of habitat fragmentation, including fragment characteristics, habitat
edges, matrix quality and permeability, spatial and temporal turnover of spe-
cies and individuals, and different scales of fragmentation. We illustrate how
habitat fragmentation effects depend on species traits, paying particular at-
tention to both mutualistic (plant–pollinator, plant–frugivore, plant–ant)
and antagonistic (host–parasitoid, food web) interactions, and we synthesise
current knowledge on likely consequences for ecological networks and
make suggestions about future research directions. Finally, we summarise
possible applications for conservation, agriculture and applied ecology in
general. Throughout the paper, we consider different kinds of interactions
and networks across a range of spatiotemporal scales.
2. NETWORKS
2.1. Ecological networks

Networks contain nodes and their links: in ecology, nodes may be individ-
uals, species populations, species, guilds, functional groups (e.g. body-size
groups), entire communities, or even entire networks, and interactions
can take many forms (e.g. plant–pollinator, plant–frugivore and pre-
dator–prey associations (Fig. 2)).
Links in an ecological network are defined in an interaction matrix. The
coarsest measure of link strength is simply the occurrence (presence/absence
A B C
D E F
G H I
Figure 2 Examples of biotic interactions. (A) Carpenter bee (Xylocopa flavorufa) polli-
nating cowpea (Vicia unguiculata) in Western Kenya (photo: M. Hagen). (B) Sunbird
(Cinnyris jugularis) pollinating palm inflorescences in Flores, Indonesia (photo: J. M.
Olesen). (C) Day Gecko (Phelsuma ornata) pollinating Gastonia mauritiana in Mauritius
(photo: C. Kaiser-Bunbury). (D) Long-tailed Macaque (Macaca fascicularis) consuming
figs on Lombok, Indonesia (photo: J. M. Olesen). (E) Green Imperial Pigeon (Ducula
aenea) consuming fruits of a palm (Corypha taliera) in Komodo, Indonesia (photo:
J. M. Olesen). (F) Seed dispersal of Casearia coriacea by ants in Le Pétrin, Mauritius
(photo: C. Kaiser-Bunbury). (G) Great Lizard Cuckoo (Coccyzus merlini) predating a
snake in Cuba (photo: J. M. Olesen). (H) African lion (Panthera leo) ‘resting’ after a biotic
interaction in Masai Mara, Kenya (photo: W. D. Kissling). (I) Crab spider predating a
bumblebee (Bombus cf. pascuorum) in Liguria, Northern Italy (photo: C. Kaiser-
Bunbury).
data), within qualitative networks, although it can be measured in many

ways (Berlow et al., 2004). For instance, for a plant–pollinator network,
the links may represent the number of visitors to a plant, number of visits,
number of pollen grains transferred to the stigma or number of pollen grains
siring seeds, seedlings or reproductive individuals. For food webs, numerous
measures and definitions have been described (see review by Berlow et al.,
2004), whereas in mutualistic networks the interaction frequency is the norm
(Vázquez et al., 2005). Both qualitative and quantitative interaction param-
eters allow not only the description of local community-level interactions,
but also the modelling of multispecies interactions across larger scales
(Kissling et al., 2012a).
Mutualistic and antagonistic networks represent the two main groups en-
countered in the ecological literature, and each has its own historical tradi-
tion (Olesen et al., 2012). Thus, antagonistic networks include ‘traditional
food webs’ (typically larger consumers kill and eat many individual prey; e.g.
Jacob et al., 2011; Layer et al., 2010, 2011; McLaughlin et al., 2010;
O’Gorman et al., 2010), host–parasitoid networks (e.g. Henri and van
Veen, 2011; Tylianakis et al., 2007), as well as less-familiar host–parasite
or pathogen networks (e.g. Lafferty et al., 2008). Mutualistic networks
include plant–flower visitor/pollinator (e.g. Memmott, 1999) and
plant–frugivore/seed disperser networks (e.g. Donatti et al., 2011;
Schleuning et al., 2011a), with less familiar forms including plant–ant
networks (Guimarães et al., 2007) and host–symbiont interactions (e.g.
gut microbiomes; Purdy et al., 2010). These categories are not
exhaustive, but they represent main foci of current ecological network
research (Ings et al., 2009). No doubt new forms of networks will appear
as this rapidly growing research field expands its horizons further: for
instance, interspecific competition within trophic levels has been largely
ignored to date, except in the context of trophic niche partitioning
within food webs, but such networks may become important, especially
in the context of habitat fragmentation, where space rather than food
may be limiting.
Food webs are traditionally divided into aquatic (freshwater and marine)
and terrestrial (aboveground and belowground) systems, although some of
the oldest food web studies included several habitats (e.g. Pimm and Lawton,
1980). These early ideas are now being revisited increasingly, with a focus
upon ‘spatial couplers’, such as allochthonous inputs at the base of the food
web, migratory top predators that link different local webs or species that
have both an aquatic and terrestrial life history (Jonsson et al., 2005;
Layer et al., 2010; McCann et al., 2005a,b; O’Gorman and Emmerson,

2010; Woodward et al., 2005).
Mutualistic and antagonistic webs are inherently difficult to compare di-
rectly (e.g. in their responses to fragmentation) because they differ in their
structure, dynamics and link type. The former are bipartite or bimodal, that
is, consisting of two interacting sets of taxa, whereas the latter are multi-modal,
that is, containing multiple trophic levels (e.g. producer–herbivore–predator).
One way to approach this might be to slice food webs up according to pairs of
interacting trophic levels into a series of bimodal networks, that is,
plant–herbivore, herbivore–predator and so on. Alternatively, mutualistic
networks, such as plant–pollinator networks, could be merged with other bi-
modal networks, for example, those of plant–herbivore or plant–fungi net-
works, to create networks of several interacting groups (see Fontaine et al.,
2011; L. Kromann-Gallop, personal communication). Until such an analysis
is made, it remains difficult to compare the properties of different kinds of net-
works directly (but see Olesen et al., 2006), although such comparisons are
theoretically possible (Thebault and Fontaine, 2010), and we therefore address
both types as separate cases throughout the paper.
2.1.1 Properties of mutualistic and antagonistic networks

Common measures of network structure include species and link numbers,
connectance, and linkage level distribution, many of which are important
because they make implicit connections between network complexity,
stability and resource partitioning in ecology (Berlow et al., 2009; Elton,
1927; MacArthur, 1955; May, 1972, 1973; McCann et al., 1998;
Warren, 1996; Williams and Martinez, 2000). These measures and their
significance in networks have been discussed extensively elsewhere
(Berlow et al., 2004; Ings et al., 2009; Olesen et al., 2010b), so we will
not cover them in detail here. Instead, we provide a brief overview of
the main concepts, with a specific focus on habitat fragmentation.
Networks also display recognisable substructural patterns, often in a
fractal-like manner, such that they may contain repeating motifs, modules
or compartments within the wider web (e.g. Olesen et al., 2007; Stouffer
and Bascompte, 2010). For example, food webs can be decomposed into
food chains, tritrophic chains and ultimately their pairwise individual
feeding links, each of which may display its own response to habitat
fragmentation (Woodward et al., 2012). These have received less attention
than the whole-network measures of complexity (e.g. connectance), but
in recent years considerable advances have been made, especially in the
study of mutualistic webs. Substructures could be especially important in the

context of habitat fragmentation, as they may represent some form of
‘network fragmentation’ related to spatial compartmentalisation. For
instance, connector species that link modules might be species with large
space requirements or long dispersal distances, that join otherwise spatially
distinct subwebs. The same principles may apply through time: for
instance, top predators move not only over wide distances but also tend to
be relatively long-lived, linking seasonally or spatiotemporally fragmented
subwebs together (Woodward and Hildrew, 2002a).
The two most common forms of network (sub)structure, nestedness and
modularity, have been studied intensively (Bascompte et al., 2003;
Lewinsohn et al., 2006; Olesen et al., 2007; Pimm, 1984). In a nested
network, the links of specialist species are well-defined subsets of the links
of generalists (Bascompte et al., 2003). Modularity describes subsets of
species (modules) that are internally highly connected, but poorly
connected to other such subsets of species (Olesen et al., 2007).
Nestedness and modularity have often been regarded as mutually
exclusive (Lewinsohn et al., 2005), but this is not necessarily true
(Fortuna et al., 2010; Olesen et al., 2007). Link patterns in bimodal
networks vary with presence of links and the frequency or intimacy of
interactions between partners (Olesen et al., 2008). If link presence and
intimacy are short and weak, the network may become nested and
modular, such as in pollination and frugivory/seed dispersal networks, but
if prolonged and tight, nestedness may be lost although modularity might
be retained, such as in host–parasitoid and plant–ant domatia networks.
Generalists and common species may be lost or ‘forced’ over
evolutionary time towards being more specialised and rare. Interaction
‘intruders’ may also break into the latter networks, making them more
nested. Such species are generalists and can also act as spatial couplers in
otherwise fragmented networks, as seen in plant–ant domatia networks
(Olesen et al., 2002).
2.1.2 Body size as a driver of ecological network structure

Body size is an important driver of structure and dynamics in many food
webs (Arim et al., 2011; Melián et al., 2011; Nakazawa et al., 2011),
especially in aquatic ecosystems (Jacob et al., 2011; Woodward et al.,
2005), and can give rise to substructures, such as feeding hierarchies
arising from gape-limited predation (Petchey et al., 2008; Woodward
et al., 2010b). Recent explorations of so-called trivariate webs, in which
feeding links are overlaid on mass-abundance plots, in marine (O’Gorman

et al., 2010), freshwater (Jonsson et al., 2005; Layer et al., 2010; Woodward
et al., 2012) and terrestrial (McLaughlin et al., 2010; Mulder et al., 2011)
systems have revealed strong size structure. Typically, energy flows from
many abundant, small resources to fewer, rarer and larger consumer
species, with many webs containing one or a few apex predators but
orders of magnitude more than basal species. These properties play an
important stabilising role in the face of species loss and other
perturbations (McLaughlin et al., 2010; O’Gorman et al., 2010), and
could be especially important in fragmented habitats (Ledger et al., 2012;
Woodward et al., 2012), where dispersal ability is also linked to body
size. While seemingly ubiquitous in food webs, these patterns have yet to
be described for mutualistic or host–parasitoid networks. More recently,
body size, abundance, biomass and link data have been used to assess a
range of substructural properties in aquatic food webs (Cohen et al.,
2009), including tritrophic interactions (i.e. the smallest modular
substructure beyond species pairs) and other recurring motifs (Woodward
et al., 2012). Given that network substructure is likely to be related to
both body size and spatiotemporal context, future work needs to focus
on the potential impact of habitat fragmentation on the robustness of the
underlying structural mechanisms in food webs and mutualistic networks,
although species traits (e.g. abundance) other than size might be more
important in the latter (but see Stang et al., 2006, 2009).
2.1.3 Species abundance as a driver of ecological network structure

Studies of ecological networks mostly focus on interactions among species
(e.g. network references in Bascompte et al., 2003; Olesen et al., 2007).
Individuals are the entities that are actually interacting, however, and as
such their encounter rates, sensitive to habitat fragmentation, drive
network structure (e.g. Petchey et al., 2010; Vázquez et al., 2009). For
instance, flower abundance can account for much of the variation in
linkage level of plants in pollination networks (Stang et al., 2006; but see
Olesen et al., 2008). The importance of abundance for the functional roles
of species in antagonistic networks is well known, but remains largely
unexplored in mutualistic networks. Often a few common species engage
in many interactions, and most rare species engage in few interactions (e.g.
Memmott, 1999). This skewed structure affects several network metrics
including nestedness, connectance and asymmetry (e.g. Blüthgen et al.,
2008), although sampling artefacts need to be ruled out (Fischer and
Lindenmayer, 2002; Lewinsohn et al., 2006; Vázquez, 2005; Vázquez et al.,

2007; Woodward et al., 2010b). The effects of spatiotemporal changes in
abundances on network structure remain relatively underexplored, but
they are potentially key issues in the context of habitat fragmentation.
2.1.4 Functional groups in ecological networks

Species within functional groups (Hobbs et al., 1995; Körner, 1993) may be
redundant, which is critical to network persistence under species extinction
scenarios (Kaiser-Bunbury et al., 2010; Memmott et al., 2004) and other
perturbations (Aizen et al., 2008; Kaiser-Bunbury et al., 2011; Tylianakis
et al., 2007). The species traits that determine functional groups in
ecological networks can differ within and between types of networks. In
pollination networks, functional diversity defined by morphological traits
might be vital for the persistence of diverse plant communities (Fægri and
van der Pijl, 1979; Fontaine et al., 2006) and can constrain interaction
patterns (Stang et al., 2006). In addition, functional groups can also be
defined by behavioural traits (e.g. generalist vs. specialist), lifespan and
temporal activity (e.g. seasonality of occurrence), phylogeny (similar roles
of closely related species) and place of origin (e.g. native vs. exotic),
which can influence pollination rates and species interactions (Fishbein
and Venable, 1996; Kandori, 2002; Raine and Chittka, 2005), or whole
pollination networks (Lopezaraiza-Mikel et al., 2007). Still remarkably
little is known about how relative abundance affects within-functional
group competition for the same resources at the network level.
2.2. Spatial networks

The analysis of multispecies ecological networks in a spatially explicit setting
is still in its infancy (Dale and Fortin, 2010; Kissling et al., 2012a), although
other types of networks have been investigated in spatial and landscape
ecology (Dale and Fortin, 2010). Here, nodes are considered as locations
(such as lakes or habitat fragments) and links define the connections
among them (Dale and Fortin, 2010). The nodes (e.g. habitat fragments)
have spatial coordinates and additional attributes related to size, shape,
habitat quality and so on. The links among them can be defined by their
distance or weight (e.g. measures of similarity in species composition
among locations). Links are usually bidirectional (i.e. symmetric), but
they can also be unidirectional, for instance, when the connection
between lakes is represented by water flow. Spatial networks can thus
form a conceptual basis for adding functional interrelations to habitat
connectedness and physical structure to ecosystems (Dale and Fortin, 2010;

Urban et al., 2009).
In a habitat fragmentation framework, spatial networks can quantify the
effects of losing nodes or links, for example, by mimicking the loss of habitat
patches or dispersal corridors for a single species within a meta-population
(Urban and Keitt, 2001; Urban et al., 2009). More complex measures of
species-specific landscape features, such as least-cost paths that describe
the movement of a species through a heterogeneous matrix habitat, can
also be integrated (Fall et al., 2007). The analysis of spatial networks in a
static landscape (Urban and Keitt, 2001) can be extended to capture
dynamic landscape processes that influence the persistence of patchy
populations (Fortuna et al., 2006). Island biogeography perspectives
(MacArthur and Wilson, 1967) can also be applied where separate
fragments are seen as ecological islands embedded in a matrix of varying
hostility.
Fragments can be connected via species that are present in both, creating
a bimodal (rather than a one-mode) network of fragments and species. Roles
can then be assigned to species and fragments according to their topological
role and position in the network (Carstensen and Olesen, 2009; Guimerà
and Amaral, 2005). Carstensen et al. (2012) used such an approach on a
large scale and identified island roles and modules on the basis of shared
avifaunas (i.e. biogeographic regions) and island characteristics.
2.3. Combining spatial and ecological networks

Regardless of whether it is possible to estimate landscape connectivity for all
interacting species or for only a few key species, an integrative approach be-
tween spatial and ecological networks is needed to evaluate population per-
sistence in fragmented landscapes (Gonzalez et al., 2011). This depends not
only on the amount of habitat and its distribution in the landscape, but also
on the position of each species within the ecological network (Solé and
Montoya, 2006). For instance, top predators are particularly vulnerable to
extinction in fragmented landscapes (Holyoak, 2000). Both spatial and eco-
logical networks have similar concepts and are analysed with similar tools
(Gonzalez et al., 2011), and integrating these into a single framework offers
a promising way to advance the field (Dale and Fortin, 2010; Fortuna and
Bascompte, 2008; Gonzalez et al., 2011; Olesen et al., 2010b).
Following Dale and Fortin (2010), a ‘graph of graphs’ can represent eco-
logical network properties (e.g. nestedness of a plant–animal network) as
nodes of a spatial network. In this way, one possibility is to view each local
population as a node in a network with two kinds of links: (i) dispersal of

individuals between fragments (local populations) and (ii) interactions be-
tween individuals of different species (e.g. pollination). The first kind of link
provides an evaluation of landscape connectivity or habitat availability
(Pascual-Hortal and Saura, 2006) for each species and the second kind gives
the role each species plays in the ecological network of species interactions,
such as its degree, centrality or contribution to nestedness. In this way, a value
of habitat availability at the landscape scale may be assigned to each species
plus a measure of its role in the ecological network(s), information that can
be combined to evaluate its persistence probability. Moreover, different spa-
tial configurations of habitats in the landscape and different arrangements of
ecological networks can be modelled to estimate the impacts of fragmenta-
tion on persistence probabilities.
Recent theoretical studies illustrate the potential of unexpected conse-
quences of the interplay between spatial and ecological networks by explor-
ing three-species food chains. As a simple example, we may consider a
tritrophic chain (Hastings and Powell, 1991) where a top predator Z feeds
on an intermediate predator Y and on a prey X, whereas Y feeds only on X,
with interactions ordered by body size (Z > Y > X). The local extinction of
Y in small patches jeopardises the survival of the large predator Z and may
lead to a overpopulation of X. Examples of outbreaks in spatially distributed
populations have indeed been described theoretically (Araújo and de Aguiar,
2007; Maionchi et al., 2006), showing that probable reduction in abundance
of intermediate species may have important indirect ramifications for other
species via their interactions in the ecological network. Recent experimental
work shows that although intermediate species may be lost, it is often the
larger species at the terminus of tritrophic chains that are especially prone
to local extinctions due to habitat fragmentation, leading a reduction in
the trophic level of the web as a whole (Woodward et al., 2012).
Theoretical studies further indicate that dynamical instabilities caused
by large dispersal abilities of predators, relative to their prey, in spatial net-
works create abundance heterogeneities among otherwise equivalent frag-
ments (Mimura and Murray, 1978; Nakao and Mikhailov, 2010; Rietkerk
et al., 2004). These so-called Turing patterns (Murray, 1993; Rietkerk
et al., 2004; Turing, 1952) represent the combined effect of species
dispersal, interactions and spatial configuration. They may also have
indirect consequences on other species by altering the composition of
potential prey, predators, competitors and mutualistic partners in
ecological networks among fragments. Such explorations of the interplay
between spatial and ecological networks highlight the need to focus on

understanding how fragmentation affects population dynamics within
multispecies systems.
3. HABITAT FRAGMENTATION
3.1. General introduction
Habitat fragmentation is often defined as a process during which a large ex-
panse of habitat is transformed into a number of patches of a smaller total
area, isolated from each other by a matrix of habitats unlike the original
(Wilcove et al., 1986). It increases discontinuity in the spatial patterning
of resource availability, affecting the conditions for species occupancy,
and ultimately individual fitness. Fragmentation can arise via both natural
and anthropogenic processes in terrestrial and aquatic systems (Figs. 1 and 3).
In the latter, fragmentation affects freshwaters (e.g. rivers and lakes) as
well as marine systems (e.g. oceans, coral reefs, seagrass meadows, kelp
forests, salt marshes and sea ice) (Box 1). In terrestrial systems, habitat
fragmentation can be induced by many drivers, including lava flows and the
conversion of forest to farmland (either grasslands or arable fields). Our focus
is primarily on anthropogenic fragmentation of pristine habitats, which is
occurring at an accelerating rate on a global scale. An illustrative example of
the effect of habitat fragmentation in the Atlantic Rainforest of Brazil is
provided in Box 2.
The effects of fragmentation on biodiversity depend on specific species
traits and characteristics of the fragments and the surrounding matrix (Ewers
and Didham, 2006; Fahrig, 2003; Henle et al., 2004). At least four effects
form the basis of most quantitative measures of habitat fragmentation
(Fahrig, 2003): (a) reduction in habitat amount, (b) increase in the number
of fragments, (c) decrease in fragment size and (d) increase in fragment
isolation. While habitat loss per se will reduce population sizes and,
ultimately, the loss of species and their links (Bierregaard et al., 1992;
Fahrig, 2003; Franklin and Forman, 1987; Saunders et al., 1991),
fragmentation includes a much wider array of patterns and processes and far
more complex consequences for biodiversity. We will review the
importance of fragment characteristics (size and isolation, including
connectivity and corridors), habitat edges (including edge permeability and
geometry) and matrix quality, before discussing spatial and temporal
turnover and the importance of scale.
Measures N
Reduced maintenance
Removal of barriers
10 km
Figure 3 Anthropogenic fragmentation of a European river network (Denmark,

E. Jutland, the city of Aarhus at the bay-center-right of map; map size: E-w 80km). Dots
indicate physical barriers (weirs, dams, impoundments) to fish migration, a major
source of human-mediated impacts (Feld et al., 2011). The map of the Gudenå catch-
ment, is derived from the River Basin Management Plan, reproduced courtesy of The
Danish Ministry of Environment.
BOX 1 Habitat Fragmentation in Aquatic Ecosystems

Fragmentation plays a key role in both terrestrial and aquatic ecosystems, includ-
ing freshwater, estuarine and marine systems (e.g. oceans, coral reefs and
seagrass meadows).
Freshwaters are commonly viewed as being bounded by hard edges as they
are ‘fragmented islands in a terrestrial sea’ (Woodward and Hildrew, 2002a), but
they also have soft boundaries within their borders (Figs. 5 and 16) imposed by
chemical gradients such as pH or salinity, especially where they mix with coastal
waters in estuaries. Human activity has accelerated the rate and extent of
fragmentation in freshwaters, particularly by overabstraction of water by
growing populations (Vörösmarty et al., 2010). Climate change is also to
exacerbate hydrological droughts (Poff and Zimmerman, 2010) via reduced
rainfall in many areas (Kundzewicz et al., 2008), potentially causing widespread
habitat loss and fragmentation (Boulton, 2003; Lake, 2003; Ledger et al., 2011).
During droughts, river flows decline, reducing the volume of wetted habitat
(water width and depth) and altering habitat structure, increasing water
temperature, reducing dissolved oxygen (Everard, 1996) and altering nutrient
supply (Dahm et al., 2003). In some regions, droughts occur predictably as
part of the natural hydrologic cycle and species are able to tolerate such
conditions (Bonada et al., 2007), but elsewhere unpredictable drought
fragmentation can have devastating effects on aquatic food webs (Ledger
et al., 2011).
Marine systems such as oceans, coral reefs and seagrass meadows are also
exposed to fragmentation. For instance, the open ocean might appear to be rel-
atively homogenous, but there are distinct vertical and horizontal regions sepa-
rated by physicochemical barriers, such as pycnoclines and frontal systems,
which are more permeable to larger organisms (e.g. anadromous and catadro-
mous fishes) than to the smaller organisms. Coral reefs experience increased rates
of habitat loss and fragmentation due to dynamite fishing (Fox, 2004; Raymundo
et al., 2007; Riegl and Luke, 1998; Wells, 2009), and coral bleaching is occurring
with increasing frequency due to rising sea temperature (Oliver and Palumbi,
2009). The loss of structural complexity in these fragmented coral landscapes
results in declining abundances and diversities of reef fish and mobile
invertebrates (Bonin et al., 2011; Coker et al., 2009; Graham et al., 2007;
Pratchett et al., 2008; Syms and Jones, 2000). Local extinctions are
proportionally greater for resource specialists than generalists (Munday, 2004).
Other marine systems include seagrass meadows, which form unique,
productive and diverse ecosystems (Bostrom et al., 2006; Duarte and Chiscano,
1999). They are affected by fragmentation through dredging and boating
effects, eutrophication, extreme weather events, urchin grazing and wasting
disease (Bostrom et al., 2006; Orth et al., 2006; Rasmussen, 1977; Walker and
Continued
BOX 1 Habitat Fragmentation in Aquatic Ecosystems—cont'd

McComb, 1992; Walker et al., 2006). While many studies suggest that
fragmentation of seagrass meadows has limited (Frost et al., 1999; Hirst and
Attrill, 2008; MacReadie et al., 2009), inconsistent (Bell et al., 2001) or even
positive (Eggleston et al., 1998; Hovel and Lipcius, 2001) impacts on epifaunal
diversity and abundance, fragmentation beyond a threshold level can lead to
rapid declines in species diversity and abundance (Reed and Hovel, 2006).
Other major marine habitats influenced by fragmentation include kelp for-
ests, salt marshes and sea ice. Habitat loss in kelp forests reduces biomass and
abundance of fish (Deza and Anderson, 2010). The die-off of salt marshes results
in changes in the behaviour of key grazers (snails) as they seek shelter from pre-
dation by blue crabs (Griffin et al., 2011; Silliman et al., 2005). Finally, increased
fragmentation of sea ice habitats results in declines in mating success and
searching efficiency of top predators such as polar bears (Molnár et al., 2011)
and in changes in phototrophic community structure and relative abundance
of dominant marine taxa (Mueller et al., 2006).
BOX 2 Habitat Fragmentation and its Effect on Brazilian

Atlantic Rainforest Trees
A good example of a biodiversity hotspot affected by fragmentation is the Bra-
zilian Atlantic rainforest landscape, which is dominated by a mosaic of small for-
est fragments usually embedded in a heterogeneous matrix of urban and
agricultural land (Ribeiro et al., 2009). The abundance and diversity of many taxa
(including frogs, lizards, small mammals and birds) are generally positively af-
fected by the surrounding matrix (Pardini et al., 2009, and see also Faria et al.,
2006, 2007), whereas the richness and abundance of shade-tolerant trees are
negatively affected and decline from large to small fragments (Pardini et al.,
2009). This indicates that increasing landscape heterogeneity might allow the
maintenance of higher diversity of animals, but that specialist tree species
depend on the maintenance of native forest patches (Pardini et al., 2009;
Ribeiro et al., 2009). In the more extreme scenario of a hyper-fragmented
Northeast Brazilian Atlantic forest (i.e. a landscape composed of pastures,
monoculture plantations and a few small native forest fragments), tree species
and reproductive trait diversity are lost (Lopes et al., 2009; Oliveira et al., 2008),
whereas early successional trees can proliferate in small forest remnants
(Tabarelli et al., 2008). An expansion of pioneer species in the edge dominated
habitats can be associated with changes in functional reproductive traits,
diurnal pollination systems, and loss of long-distance flying pollinators, self-
BOX 2 Habitat Fragmentation and its Effect on Brazilian

Atlantic Rainforest Trees—cont'd
incompatible breeding systems and large-seeded plant species. Furthermore,
phenological trait mismatches can occur, due to shifts in the proportions
annual versus supra-annual flowering (Lopes et al., 2009; Santos et al., 2008;
Tabarelli et al., 2010). Modelling efforts predict a pervasive long-term trend
towards vegetation dominated by early successional trees and impoverished
tree species composition (Pütz et al., 2011), with important implications for
plant–animal mutualistic networks. Specialised and long-distance moving
connector species in mutualistic networks such as large pollinators (bees or
hummingbirds) and seed dispersers (large birds) are likely to be particularly
vulnerable due to reduced floral diversity and quality arising from the
dominance of generalist pollination systems, and the large proportion of
species that are wind dispersed or which have small fleshy fruits (e.g. Lopes
et al., 2009; P. Morellato, unpublished data).
3.2. Fragment characteristics

Fragment characteristics are important for understanding fragmentation
effects on biodiversity (Table 1). Apart from original habitat loss per se
(Tilman et al., 1994), size (i.e. area) and degree of isolation of fragments
are important properties (Fahrig, 2003). For some taxa such as butterflies,
habitat heterogeneity seems to be a more important determinant of diversity
than fragment size and isolation (Kivinen et al., 2006; Rundlöf and Smith,
2006; Weibull et al., 2000), and this may be true for other herbivorous
insects as well.
The area needed to maintain populations is determined by fragment size,
with smaller patches generally containing fewer individuals and species than
larger patches (Debinski and Holt, 2000). The area effect on biodiversity can
be predicted from species–area curves (Sabatino et al., 2010), and the set of
species in smaller patches is often a fairly predictable subset of those in larger
patches (nested structure; e.g. Ganzhorn and Eisenbeiss, 2001; Hill et al.,
2011). Species richness in forest fragments in relation to fragment area
(Brooks et al., 1997; Ewers and Didham, 2006) can mirror the classic
species–area relationships known from island biogeography (MacArthur
and Wilson, 1967). To some extent, temporal effects are also dependent
on fragment size because what happens quickly in small fragments
happens slowly in larger fragments (Terborgh et al., 1997).
Table 1 Fragment characteristics and animal and plant traits, which are relevant for assessing fragmentation effects on biodiversity
Trait Importance of trait in relation to fragmentation References
Trait at fragment level
Size (area) The size of fragments determines the area available for population and Bender et al. (1998),
species persistence and influences extinction and immigration rates Fahrig (2003),
MacArthur and Wilson
(1967)
Isolation The degree of isolation of fragments represents the lack of habitat in Ewers and Didham
the surrounding landscape and has an influence on the movement and (2006), Fahrig (2003)
dispersal of species among fragments
Shape Convoluted fragment shapes can lead to increased turnover and variability in Ewers and Didham
population size when compared to fragments that are compact in shape (2006)
Edge effects Edges of fragments affect microclimate and animal abundances Laurance et al. (2011)
Matrix effects The surrounding matrix mediates edge effects and influences animal (e.g. Laurance et al. (2011)
pollinator and seed disperser) movements
Animals
Dispersal Species with high mobility are more likely to survive in fragmented Ewers and Didham
ability landscapes than species with low mobility. Low mobility or poor dispersal (2006), Thomas (2000)
ability of species is thus expected to increase species-level fragmentation
effects. For some butterflies, it has been shown that species with
intermediate mobility are more likely to decline in abundance following
habitat fragmentation than species with either high or low mobility
Table 1 Fragment characteristics and animal and plant traits, which are relevant for assessing fragmentation effects on biodiversity—cont'd
Habitat Habitat specialists are expected to be more affected by fragmentation than Ewers and Didham
specialisation habitat generalists. The matrix tolerance of a species might play an important (2006)
role here
(e.g. forest generalist vs. habitat generalist)
Trophic level Higher trophic levels are predicted to be more strongly affected by habitat Ewers and Didham
fragmentation than lower trophic levels (2006), Milton and
May (1976)
Dietary Species with broad dietary niches might be less impacted by fragmentation Bommarco et al. (2010)
specialisation than dietary specialists
Gap-crossing Species persistence in isolated fragments is strongly linked to gap-crossing Lees and Peres (2009)
ability ability
Body size Body size constrains animal space use and home range size. Home range size Greenleaf et al. (2007),
is expected to increase with habitat fragmentation, and home ranges of larger Haskell et al. (2002), Jetz
species are more sensitive to habitat fragmentation than those of smaller et al. (2004), Laurance
species et al. (2011)
Sociality Sociality can buffer against negative effects of fragmentation Aizen and Feinsinger
(e.g. social bees vs. solitary bees) or increase susceptibility to fragmentation (1994a,b), Bommarco
(e.g. obligate mixed-flock feeders in Amazonian forest birds) et al. (2010), Laurance
et al. (2011)
Continued
Table 1 Fragment characteristics and animal and plant traits, which are relevant for assessing fragmentation effects on biodiversity—cont'd
Plants
Dispersal mode Dispersal mode (e.g. abiotic vs. biotic) can be a key factor influencing species Montoya et al. (2008),
responses to habitat fragmentation Tabarelli et al. (1999),
Tabarelli and Peres
(2002)
Fruit/seed size Large big-seeded fleshy fruits tend to have few dispersal agents and are likely to Corlett (1998)
be more strongly affected by fragmentation than plant species with small fleshy
fruits
Pollination Plants depending on animals for pollination are probably negatively affected Aizen and Feinsinger
mode by habitat fragmentation (specifically isolation) than wind-pollinated species (1994a,b), Fægri and van
der Pijl (1979), Kolb and
Diekmann (2005)
Breeding Characteristics of breeding systems, for example, the degree of protandry, Jennersten (1988), Yu
system self-incompatibility or sex ratios, might be affected by fragmentation and Lu (2011)
Growth form Specific growth forms (e.g. clonal plants) might be more strongly affected than Dupré and Ehrlén
others (e.g. annuals) (2002), Kolb and
Diekmann (2005)
Seed bank Long-lived seed banks may prevent species from going extinct in small Dupré and Ehrlén
habitat fragments (2002)
The list highlights some key traits but is not intended to be exhaustive.
Isolation restricts the movement and dispersal of species among fragments

and depends on physical distance and matrix quality (Bender et al., 2003).
Two aspects of fragment isolation are particularly important: connectivity
and the availability of corridors. Connectivity is the degree to which the land-
scape permits or impedes movement among fragments (Taylor et al., 1993)
and is a species and system-specific parameter (Taylor et al., 2006;
Tischendorf and Fahrig, 2000). Its effect on biotic interactions (e.g.
pollination services) is therefore a complex function of the individual
responses of the different interacting species (for pollinators see e.g. Fenster
and Dudash, 2001; Herrera, 1988; Horvitz and Schemske, 1990; Moeller,
2005; Ricketts et al., 2006). Some species may primarily be influenced by
the distance to a fragment of a particular habitat, while others may be more
influenced by the quality or availability of the resource (e.g. nesting sites)
in adjacent habitats. One structural landscape characteristic of high
importance for connectivity is the presence of corridors, which can be
either natural or man-made. They are landscape elements that facilitate the
movement of organisms among fragments, promoting biotic connectivity
and synchrony (Hilty et al., 2006). Recent experiments have demonstrated
that corridors play a key role in maintaining plant and animal populations
and their interactions in fragmented landscapes, and that connected
fragments retain more species from native biota than isolated ones
(Damschem et al., 2006; Tewksbury et al., 2002). Their importance for
biodiversity conservation is still a moot point (Gilbert-Norton et al., 2010;
Noss, 1987; Simberloff and Cox, 1987; Simberloff et al., 1992), as in some
systems (e.g. tropical rainforests) corridors and fragments dominated by
secondary vegetation may be of limited value (Oliveira et al., 2008).
3.3. Habitat edges

Increased edge habitats, which may be natural (e.g. light gaps, rivers and
landslides in natural forests) or anthropogenic, are prominent features of a
fragmented landscape. Habitat edge and fragment shape are important de-
terminants of biodiversity (Ewers and Didham, 2006; Laurance et al.,
2011; Murcia, 1995), and strong effects on a variety of plant and animal
species are well documented (e.g. Bach and Kelly, 2004; Davies et al.,
2000; Gehlhausen et al., 2000; Laurance et al., 1998).
Three main physical and biological effects of edges are important in frag-
mented habitats (Murcia, 1995): (i) abiotic environmental changes across
edges; (ii) biological effects related to changes in species in the edge and
across the edge as a result of (i), and (iii) indirect biological effects, which
relate to how changes in (ii) cascade up and affect species via their antago-
nistic and mutualistic interactions.
Changes in abundance across a habitat edge depend on the taxonomical/
functional groups involved. Generalist species are often favoured in habitat
edges, because they offer access to new habitats and resources (e.g. pollina-
tors: Burgess et al., 2006, herbivores: Wirth et al., 2008, predators and nest
predation: Chalfoun et al., 2002; Lidicker, 1999), whereas specialists
typically decline (plants: Laurance et al., 1997, 2006a; Tabarelli et al.,
2008, insectivorous birds: Restrepo and Gómez, 1998, vertebrates:
Hansson, 1994, but see Pardini et al., 2009 for a multi-taxa approach).
Species that require different habitat types for different resources or life
history stages (e.g. nesting, feeding and foraging) are expected to benefit
from a structurally diverse habitat mosaic (including edges). For example,
solitary bees that nest above-ground forage in agricultural landscapes, but
nest in neighbouring natural habitats (Gathmann and Tscharntke, 2002).
Aquatic insects often rely on trees as ‘swarm-markers’ for breeding once they
have emerged from the water and crossed the aquatic–terrestrial boundary.
Similarly, riparian vegetation provides the main source of energy to many
stream food webs in the form of terrestrial leaf-litter, so the proximity to this
edge can determine the trophic basis for production for the entire system
(Hladyz et al., 2011b). Even predators can benefit from inputs from terres-
trial edges, with such subsidies supporting some stream fishes at densities far
beyond what in-stream production alone can support (Allen, 1951). Edges
also influence seed banks and the quality, abundance and diversity of seed
rain (Devlaeminck et al., 2005, Melo et al., 2006).
In forests, especially tropical ones, the increasing air temperature, light
incidence and decreasing relative humidity towards the edge (Didham
and Lawton, 1999; Kapos et al., 1997; Murcia, 1995) can affect plant
reproduction by shifting phenology and boosting flower and fruit
production (Burgess et al., 2006; Camargo et al., 2011; D’Eça Neves and
Morellato, in press; Kato and Hiura, 1999; Murcia, 1995) (Fig. 4). In
turn, important animal–plant interactions can be affected (Aizen and
Feinsinger, 1994a,b; Cunningham, 2000; Fleury and Galetti, 2006;
Galetti et al., 2006; Jordano and Schupp, 2000; Wright and Duber,
2001). Pollination rates at edges may decrease (Aizen and Feinsinger,
1994a,b; Burgess et al., 2006; Harris and Johnson, 2004; Hobbs and
Yates, 2003), increase (Burgess et al., 2006), or may not change at all
(Burgess et al., 2006), with implications for plant reproductive success
A B
100 Callistene minor 100 Cupania vernalis
100 100
0 0
C D
100 Guapira opposita 100 Pera obova
% Individuals
100 100
0 0
E F
100 100
Persea venosa Vochysia tucanorum
100 100
0 0
J FMAM J J A SOND J FMAM J FMAM J J A SOND J FMAM
Flower Fruit
Figure 4 Phenological response of trees occurring in the edge (shaded graphics) and
interior of a seasonal forest at Serra do Japi, Southeastern Brazil (after D'Eça Neves and
Morellato, in press). Positive responses (higher proportion of trees) for flowering were
detected in four of six species (Figure edge A to D). On the other hand, negative edge
effects on fruiting were detected for four species (Figure edge C to F). Although the fruit
production of the woody Cupania vernalis (Sapindaceae) was positively affected by frag-
ment edge (Figure edge B), Guimarães and Cogni (2002) observed a higher seed predation
of C. vernalis in the edges at the same study site. Therefore, differential phenological re-
sponses at the edges may change the visitation rates of pollinators, dispersers and seed
consumers, making it hard to predict the reproductive outcome to the plant.
(Burgess et al., 2006; Cunningham, 2000) and seed dispersal. The influence
on the latter may be either positive due to differences in animal densities,
foraging patterns, fruit display, plant size and vigour (Jordano and
Schupp, 2000), or negative via limited animal movement at edges
(Restrepo et al., 1999). Furthermore, recruitment and predation of seeds in

the forest interior might decrease relative to edges (Baldissera and Ganade,
2005; Fleury and Galetti, 2006; Jules and Rathcke, 1999; Restrepo and
Vargas, 1999, but see Cunningham, 2000; Guimarães and Cogni, 2002).
Besides the capability of a species to perceive suitable habitat fragments
and the connectivity of the landscape, its persistence in a fragmented land-
scape depends on its ability to cross the edge between fragment and matrix
(Morris, 1997; Stamps et al., 1987a; Stevens et al., 2006). Habitat edges can
be characterised as ‘hard’ or ‘soft’ according to their permeability. Hard
edges are boundaries which dispersing individuals rarely (if ever) cross,
although their permeability can vary with life history, for example, adults
or juveniles (Fig. 5). Soft edges are more permeable: for example,
bumblebees (Bombus hortorum) cross several habitat edges between
meadows, fields and gardens and move widely within a mosaic landscape
(Hagen et al., 2011). Changes in edge permeability (e.g. due to
degradation of the landscape matrix around a fragment) can alter
migration rates, as well as several other ecological and demographic
processes. For instance, population densities within the fragment may be
elevated, maturity delayed, and reproductive and growth rates reduced
(Abramsky and Tracy, 1979, 1980; Gliwicz, 1980; Lidicker, 1985; Myers
and Krebs, 1971; Stamps et al., 1987b).
Emigration rates (i.e. the proportion of dispersing individuals that leave
the fragment) from habitat fragments are also determined by the edge-to-size
ratio and the shape of the habitat edge (Nams, 2011). For instance, Hardt and
Forman (1989) found forest herbivores to concentrate in the grassy areas
where the edge intrudes into the forest. Some pollinating bee species
(e.g. Bombus lapidarius; Rasmussen and Brdsgaard, 1992) avoid edges while
foraging for pollen within fragments, while responses of birds to edges vary
markedly among species and edge types (Sisk and Battin, 2002).
3.4. Matrix
The matrix surrounding fragments also influences their structure and dy-
namics (Brotons et al., 2003; Cook et al., 2002; Prevedello and Vieira,
2011; Prugh et al., 2008). Among forest fragments, matrix quality can
range from a completely deforested agricultural landscape to mature
secondary growth, varying immensely in hostility and permeability to
each species. Matrix quality thus determines connectivity, dispersal and
associated mortality rates, and its influence may even override those of
60
50 Adult Larvae
Frequency (%)
40
30
20
10
0
2 4 6 8 10 12 14 16 18
Pairwise difference (km)
60
50 Adult Larvae
40
Frequency (%)
30
20
10
0
2 4 6 8 10 12 14 16 18
Pairwise difference (km)
Figure 5 Frequency distribution of pairwise distances for all individual streams in the
Ashdown Forest network, Sussex, UK (Fig. 16), for both adult winged insects (solid black
bars) and immature aquatic insects and other solely aquatic organisms, including fishes,
molluscs, Crustacea and other groups (white bars). (A) The River Medway network and
(B) the River Ouse network. Note: inter-catchment exchange is not included here, since
although it is feasible in the aerial phase, none of the solely aquatic taxa in these webs
are able to cross the marine–freshwater boundary, which acts as a ‘hard’ boundary for all
the insect species that dominate these food webs. Aquatic invertebrates are incapable
of crossing from one network to the other, due to the lack of suitable corridors. Fewer
than 1% of all fish species can make the transition between fresh and salt water (brown
trout and common eels are the only notable exceptions within the river networks shown
here), so for many taxa these two catchments are in reality separated by 100s of
kilometres of an insurmountable physicochemical barrier even though the local webs
may be just a few kilometres apart in the upper headwaters. There is also likely to be an
evolutionary spatiotemporal component to fragmentation here, as these catchments
have likely been flowing in different directions and hence effectively isolated for many
taxa since the retreat of the ice sheets at the end of the last glaciation.
fragment area and isolation (Cook et al., 2002; Ewers and Didham, 2006).
A high-quality matrix (e.g. forest regrowth) can minimise edge effects by
supporting a proportion of the communities in the fragments (Laube
et al., 2008; Pardini et al., 2009 and references therein).
A diverse and structurally complex, anthropogenic matrix may even har-
bour a significant fraction of the original biota, potentially reducing biodi-
versity loss (Lindenmayer and Luck, 2005; Pardini et al., 2009). For instance,
in Western Kenyan rainforest, some bird species (11% out of 194 forest-
dependent species; Bennun and Njoroge, 1999) also used the
heterogeneous farmland close to the forest as feeding habitat, gaining
access to additional food resources outside their core habitat (Laube et al.,
2008). Thus, agroecosystems with a diverse habitat structure can have at
least some capacity to compensate for forest loss. Indeed, several
frugivorous bird species use native and exotic fruiting trees in the
farmland around the same forest, increasing seedling establishment
(Berens et al., 2008; Eshiamwata et al., 2006), suggesting the matrix can
aid fragment regeneration and restoration (Fisher et al., 2010). Further,
bee diversity is higher than in the nearby forest, so the farmland may
even act as a ‘pollinator rescue’, supporting pollination services inside the
forest (Hagen and Kraemer, 2010). Other studies have reported positive
influences of natural forest on pollination interactions in farmland (e.g.
Florida, USA: Artz and Waddington, 2006; North Queensland, Australia:
Blanche et al., 2006).
Matrix quality can also be important for food webs. A recent study has
shown how the invasion of the terrestrial edge habitat can cause a collapse in
food web structure and ecosystem processes of an adjacent stream, by alter-
ing the porosity of energy flux across the ecotone (Hladyz et al., 2011a).
Here, the native terrestrial matrix through which the stream would normally
flow is either in the form of the mixed deciduous woodland climax commu-
nity, or rough pasture maintained by low intensity farmland. The invasive
tree Rhododendron ponticum forms dense, dark monocultures that outcompete
native riparian plant species and cast a deep shade over the stream food webs.
Invasions can occur within either of these starting conditions, although they
are accelerated by anthropogenic disturbance along the aquatic–terrestrial
fragment–matrix edge. Because the tough, leathery leaves of the invader
are also a poor-quality food source, being very high in C:N and lignin
content (Hladyz et al., 2009), they effectively shut down the detrital path-
way at the base of the stream food web, which is normally fuelled by
leaf-litter when the matrix is dominated by oak woodland. The invader
also suppressed the alternative energy source supplied by algal–herbivore

pathways that would otherwise dominate when the terrestrial matrix is
rough pasture, by shading the stream channel (Hladyz et al., 2011a). Con-
sequently, invasive species can harden the fragment–matrix boundary, by
reducing the permeability of energy transfer. Additional recent evidence
from a pan-European study suggests that riparian alterations tend to suppress
animal–resource interactions at the base of stream food webs, increasing
reliance on microbial-driven rather than invertebrate-driven processes
(Hladyz et al., 2011b).
3.5. Spatial and temporal turnover of species and individuals

Spatial and temporal turnover in species composition among habitats in a
fragmented landscape can be pronounced. For instance, Hagen and Kraemer
(2010) found high turnover rates in bee species composition between open
farmland, forest–farmland edge and forest interior: almost 50% of all bee spe-
cies in this landscape mosaic occurred in all three habitat types, indicating a
high edge permeability or a so-called soft edge.
In contrast, in a European meadow, pollinator species did not cross the
edge into the adjacent forest, whereas herbivores and pathogens did
(L. Kromann-Gallop, personal communication). Shifts in behaviour (e.g.
flower visitation rates) may also occur among individuals of the same species
of pollinator, leading to differences in fruit and seed set among habitats (Kai-
ser et al., 2008). Additionally, the roles of species in an ecological network
(e.g. peripherals, connectors, module hubs and network hubs; Olesen et al.,
2007) can change when crossing habitat borders (M. Hagen et al.,
unpublished data). Of 35 species (8 plant and 27 bee species) occurring in
all three habitats in a forest–agriculture landscape, 23 (3 plants, 20 bees)
had similar roles in all habitats, as did 11 (4 plants, 7 bees) species in two
of the three habitats, and one plant had a different role in each habitat.
Due to physical changes at habitat edges, phenological shifts in interac-
tions may arise, resulting in a complex interplay between spatial and tempo-
ral turnover. Edges and interiors may therefore differ in the timing of
resource availability and network structure and dynamics. Unfortunately,
detailed data remain scarce (Kato and Hiura, 1999; Ramos and Santos,
2005), but an increase in flower production at forest edges associated
with high light incidence and temperatures have been reported for some
species (Alberti and Morellato, 2010; Camargo et al., 2011; Fuchs et al.,
2003; Kato and Hiura, 1999; Ramos and Santos, 2005). D’Eça Neves and
Morellato (in press) compared the phenology of tree species between forest
edge and interior in Southeastern Brazil and found a higher proportion of
reproductive trees along the forest edge (59% flowering and 73% fruiting)
than inside the forest (47% flowering and 29% fruiting), and flowering
and fruiting were more seasonal in the latter. As individual tree species
can respond differently to edge effects (Fig. 4), the synchrony and degree
of overlap between the interaction partners in an ecological network may
be affected by this aspect of habitat fragmentation (e.g. Hegland et al.,
2009; Memmott et al., 2007).
The predominance of generalism and seemingly high plasticity of inter-
actions in many ecological networks may reduce the effects of spatial and
temporal mismatches. The available literature, albeit scarce, indicates that
pollination networks are fairly robust against such mismatches (see Hegland
et al., 2009) and the same may be true for food webs, which are typically
even more generalised (Ings et al., 2009). Plants and pollinators exposed
to similar environmental changes may react in synchrony, decreasing the oc-
currence of mismatches (Hegland et al., 2009). In pollination networks, high
turnover in species composition and interactions over time are well docu-
mented (Alarcón et al., 2008; Dupont and Olesen, 2009; Olesen et al., 2008;
Petanidou et al., 2008), but the consequences of adding the spatial
component of a fragmented landscape to temporal mismatches are
virtually unknown.
3.6. Scales of habitat fragmentation

Fragmentation operates over many spatial and temporal scales (Levin, 1992),
from tiny water bodies within individual plants (Phytotelmata; Box 3) to
successional processes across entire landscapes, for instance, as stream net-
works develop following glacier retreat (Brown and Milner, 2012;
Jacobsen et al., 2012; Woodward and Hildrew, 2002a). Individual
organisms perceive the world at different spatial and temporal scales and
thus will respond to fragment characteristics, habitat edges and matrix
permeability in different ways. Within food webs, consumer–resource
perceptual disparities may be pronounced, closely coupled to the
relationship between body size and environmental grain: for example,
single-celled algae and small invertebrates at the base of aquatic food
webs are many orders of magnitude smaller than the large vertebrates at
the top (e.g. Cohen et al., 2009; Layer et al., 2010). The immediate
environment within which a diatom spends its (short)life attached to a
substrate particle on a streambed is thus shaped largely by small-scale
BOX 3 Phytotelmata—Small Aquatic Worlds in a Highly

Fragmented Landscape
Phytotelmata (from Ancient Greek, meaning ‘plant ponds’) are small water bodies
within plants that exist as aquatic refugia within a much larger terrestrial ecosys-
tem. Examples include tree holes, bamboo internodes, pitcher plants, tank bro-
meliads and water-retaining plant axils (Kitching, 2001). Phytotelmata have been
intensively studied as they represent naturally replicated systems containing dis-
crete communities and food webs within individual plants (Reuman et al., 2009).
The macrofaunal assemblages they contain can range from 2 to 20 species
(Kitching, 2001) and are often dominated by arthropods, although annelids, frog
tadpoles and molluscs have also been recorded (Kitching, 2000). In addition, they
contain a diverse range of microscopic life, including rotifers, protozoa and bac-
teria (Buckley et al., 2010; Kneitel and Miller, 2002).
Phytotelmata can be regarded as insular systems (Kitching, 2001), and they have
been useful models for testing island biogeography theory (MacArthur and Wilson,
1967). An investigation of the macrofaunal diversity in epiphytic bromeliads shows
that species richness increases with phytotelma size and physical habitat complexity
(Armbruster et al., 2002; Buckley et al., 2010; Srivastava, 2006). Phytotelmata
are extremely isolated as the surrounding matrix (e.g. terrestrial forest) is
hostile. There is no connectance between phytotelmata via corridors, so the
aquatic–terrestrial boundary presents a discrete hard edge between fragments.
This can only be overcome in the adult phases of phytotelma-inhabiting species,
for example, as winged phase of aquatic insects or after metamorphosis in tadpoles.
In addition to these hard edges, there can also be soft edges that act as second-
ary filters among separated phytotelmata. For instance, the physicochemical envi-
ronment differs within each plant so that some hoverflies avoid bamboo internodes
with low pH for oviposition (Kurihara, 1959) or mosquito larvae exhibit reduced sur-
vivorship with rising pH in tree holes (Carpenter, 1982). During extreme rainfall
events, extensive flushing and recharging of the aquatic reservoir can occur and
thus provide potential connectance among phytotelmata. The nutrient content
(Carpenter, 1982) and pH (Clarke and Kitching, 1993) of phytotelmata can vary
widely, and these varying levels of habitat restriction and fragmentation can create
a ‘hierarchy of fragmentation’, with the imagines of phytotelm invertebrates being
exposed to a less fragmented environment than the juvenile stages.
Phytotelmata fragmentation will have pronounced effects on the structure
and function of ecological networks formed within such water bodies. Whilst
there are examples of mutualistic interactions within pitcher plants (Clarke and
Kitching, 1993), the vast majority of described phytotelma networks are antago-
nistic, and there is evidence for both bottom-up and top-down control within the
food web (Hoekman et al., 2011; Kneitel and Miller, 2002). At least three discrete
levels of fragmentation are apparent, from local to larger landscape scales (e.g.
bromeliad leaf pools within a plant; phytotelmata within a single terrestrial
matrix vs. multiple, fragmented terrestrial matrices).
forces related to fluid viscosity or nutrient diffusion, whereas the herbivores

that eat it will be more influenced by factors such as availability of physical
refugia from predators (who in turn operate at larger scales), channel
discharge or water depth (Woodward and Hildrew, 2002a; Woodward
et al., 2010a). Thus, the fragment size within which each species operates
tends to increase up the food chain, and the species’ perception of edges
also changes. In terms of ‘flow habitats’ in stream ecosystems, individual
diatoms will be strongly influenced by boundary layer effects within the
nearest few millimetres, herbivorous macroinvertebrates will respond to
near-bed velocity and microhabitats at the scale of centimetres to metres,
and predatory fish will respond to the availability of suitable territories at
the pool-riffle or macrohabitat scale. The largest, most mobile, migratory
species may even respond at the scale of the entire river catchment
(Woodward and Hildrew, 2002a).
Most fragmentation studies usually focus on a particular spatial scale:
Doak et al. (1992) reviewed 61 primary research papers on the effects of hab-
itat fragmentation on population structure of terrestrial arthropods, all of
which were conducted at a single spatial scale. In general, studies that
account for fragmentation on different spatial scales are rare (but see
Garcia and Chacoff, 2007; Schleuning et al., 2011b; Stephens et al.,
2003). Forest fragmentation (large-scale reduction of fragment size) can
affect ecosystem processes indirectly by changes in biodiversity, whereas
selective logging (local scale) influenced ecosystem processes (e.g.
pollination and seed dispersal) by modifying local environmental
conditions and resource distributions (Schleuning et al., 2011b).
Many long-term consequences only become apparent after many decades
(Laurance et al., 2011), yet most studies of anthropogenic fragmentation have
been conducted over much shorter periods (Ewers and Didham, 2006), which
may not be sufficient to detect the full range of responses. Nevertheless, em-
pirical studies suggest that time lags in species responses at such time scales
are very common (Ewers and Didham, 2006; Laurance et al., 2006b).
While population densities may increase in the short term as survivors are
concentrated in remaining patches, in the long term, species abundance and
richness decline (Debinski and Holt, 2000) because some can survive for up
to several generations under unsuitable habitat conditions before eventually
going extinct (‘extinction debt’; Tilman et al., 1994). Extinction debts can
be pronounced if many species are near the threshold capacity of the
landscape that ensures meta-population persistence (Hanski and Ovaskainen,
2000). Time-lagged responses of species to fragmentation are not only
observed for long-lived trees, but also for other organism groups such as
vertebrates and insects (Ewers and Didham, 2006; Metzger et al., 2009).
Considering such time lags thus becomes especially important for evaluating
fragmentation effects on species interactions and ecological networks.
Time lags are most pronounced where generation times strongly differ be-
tween interacting or dependant species (Kissling et al., 2008, 2010). For
instance, in climate change impact assessments, low dispersal rates and long
generation times of woody plants can slow distributional responses, with
important consequences for bird species that depend on such plants for
habitat and food (Kissling et al., 2010). In a fragmentation context, the
different generation times of invertebrates and vertebrates, parasites and
hosts, and species from different trophic levels in plant–animal mutualistic
systems might lead to contrasting responses of interacting species, thus
disrupting existing networks. For instance, long-lived vascular plants in
European grasslands showed time-delayed extinctions whereas short-lived
butterflies did not, even after 40 years (Krauss et al., 2010). This suggests
that interacting species (at different trophic levels) have different extinction
debts, so co-extinctions associated with long-lived taxa might amplify
future biodiversity loss even without any further fragmentation occurring.
Given the various levels of complexity and spatiotemporal scales
involved, a hierarchical approach seems necessary for understanding the
effects of habitat fragmentation on species interactions, ecological networks
and community-level changes (Didham et al., 2012; Urban et al., 1987).
4. HABITAT FRAGMENTATION AND SPECIES TRAITS

In addition to landscape attributes, species traits also modulate the ef-
fects of fragmentation (Aguilar et al., 2006; Ewers and Didham, 2006;
Fahrig, 2003; Henle et al., 2004). For instance, overall species richness of
butterflies in Europe and America decreases with fragmentation, but
those with low dispersal ability, a narrow larval feeding niche and low
reproduction are most strongly affected (Öckinger et al., 2010). In
addition, intraspecific variation in phenotypic traits may ultimately affect
community patterns, such as the distribution of niche width (Bolnick
et al., 2011). In general, seemingly contradictory responses might be
better explained by considering the role of species traits (Ewers and
Didham, 2006). In this section, we briefly review fragmentation-relevant
traits for plants and animals and then highlight the potential importance
of species trait combinations for understanding the consequences of

fragmentation for biodiversity and ecological networks.
4.1. Plant traits

Important plant traits for persistence in fragmented landscapes include seed
dispersal, pollination and breeding system, growth form and seed bank
(Table 1). Two aspects of seed dispersal are particularly relevant: dispersal
mode and fruit traits (e.g. fruit and seed size). The former (abiotic dispersal
by wind or via animal vectors) can strongly influence how the relative abun-
dance of tree species responds to habitat fragmentation (Fægri and van der Pijl,
1979; Montoya et al., 2008; Tabarelli and Peres, 2002; Tabarelli et al., 1999).
Additionally, fruit traits that influence frugivore choice (fruit size, edibility of
the peel, defensive chemistry, crop size and phenology: Buckley et al., 2006)
will influence the responses of fleshy-fruited plants to habitat fragmentation.
Large, big-seeded fruits, which are consumed by only a few vertebrate
species, might be most vulnerable to fragmentation (Corlett, 1998), and
fruit size and colour may be crucial for plant colonisation of habitat
fragments (Shanahan et al., 2001), where certain trait combinations attract
a specific set of animal dispersers (e.g. birds vs. bats).
Plants also differ in their dependency on pollinators (e.g. Aizen and
Feinsinger, 2003; Bond, 1994), and this can determine their vulnerability
to fragmentation. Certain plants traits are especially important to attract
pollinators and to exclude floral reward robbers, for example, flowering
phenology, amount and quality of pollen and nectar, and structural
complexity of the flower. Habitat fragmentation may contract flowering
periods because abundant plant species should have longer population-
level phenophases than rarer species (but see Morellato, 2004), increasing
the risk of losing pollinators, which could further reduce plant fitness
(Aizen and Feinsinger, 1994a,b).
Within species, flower morphology can vary among habitats: certain
plants in urban fragments have more, but smaller flower heads, which
may decrease floral attractiveness and affect pollinator behaviour (Andrieu
et al., 2009). Changes in pollinator behaviour could increase self-pollen de-
position (Aizen and Feinsinger, 1994a,b), and drive a divergence in the
evolution of floral traits in fragmented populations (Kingsolver et al.,
2001; Pérez-Barrales et al., 2007). Demographic, environmental and
genetic stochasticity are likely to be most pronounced in small fragments
(Matthies et al., 2004; Willi et al., 2005), and the latter may trigger a loss
of self-compatibility alleles due to genetic drift, increasing inbreeding and

genetic erosion (Ellstrand and Elam, 1993; Lande, 1988; Menges, 1991;
Young et al., 1996; but see Aizen and Feinsinger, 1994a,b).
Differences in breeding systems can affect plant species responses to frag-
mentation. For instance, the herb Dianthus deltoides (Caryophyllaceae) is
protandrous (i.e. anthers open before stigmas ripen) but in small fragments
it becomes homogamous (i.e. the male and female sexual parts ripen simul-
taneously), increasing the probability of self-fertilisation (Jennersten, 1988).
Self-compatible plants are often facultatively dependent on pollinators,
whereas self-incompatible species are obligate outcrossers, relying exclu-
sively on pollinators (e.g. Aguilar et al., 2006). Sex ratios in dioecious species
might also be sensitive to fragmentation. In China, populations of the dioe-
cious tree Pistacia chinensis (Anacardiaceae) were surveyed on islands of dif-
ferent size in a recently flooded reservoir (Yu and Lu, 2011): small islands
with poor soils had a male-biased sex ratio, whereas large and nutrient-rich
islands had a stable 1:1 ratio. Such drops in effective population size on small
islands could accelerate population extinction.
4.2. Animal traits

The key animal traits in relation to fragmentation are dispersal ability, niche
width, body size and sociality (Table 1), with the first two being especially
important (Bommarco et al., 2010; Ewers and Didham, 2006). Species with
high dispersal ability are less likely to be affected by fragmentation (Hanski
and Ovaskainen, 2000; Öckinger and Smith, 2007; Roland and Taylor,
1997). For example, solely aquatic invertebrates must swim long distances
if they are to colonise new streams in a river system, encountering many
potential barriers to dispersal (Fig. 5), whereas larvae with winged adult
phases can reach these new habitat fragments relatively easily. Although
the abundance of adult phases of aquatic invertebrates (such as stoneflies)
decreases exponentially with distance from their ‘home stream’, with the
rate of decline varying with matrix permeability (Fig. 6), only a few
gravid females may be needed to (re)populate an entire food web due to
high-density-dependent predation on early life stages (e.g. Hildrew et al.,
2004). This can lead to increased genetic differentiation in adult
populations at larger distances between streams, highlighting the potential
for genetic-level impacts of soft versus hard barriers to dispersal (Fig. 7).
Species with a wider dietary or habitat niche will also be less susceptible
to fragmentation. Generalists may survive in very small patches by using
1600
1400
Total no.individuals caught
1200
1000
800
600
400
200
0
0 20 40 60 80
Horizontal distance from stream edge (m)
Figure 6 Lateral dispersal of winged adults of a common stonefly species (Leuctra nigra)
from the stream edge through the terrestrial matrix (woodland—black circles; open
land—white circles) within the Ashdown Forest, UK (see Fig. 16). Total number of males
and females caught in passive Malaise traps are shown on the y-axis, with exponential
declining models fitted for each habitat type [woodland: y ¼ 1.517 exp( 0.055*x;
R2 ¼ 0.99, F ¼ 665.2, p < 0.001); open land: y ¼ 903 exp( 0.065*x; R2 ¼ 0.99,
F ¼ 324.6, p < 0.001)]. Redrawn after Petersen et al. (1999).
resources in both the fragment and the surrounding matrix (Andren, 1994).
Specialists might find their resources (e.g. specific food plants) retained
in only a few fragments, and habitat specialisation can further restrict their
distribution. Some specialists also have a narrow geographic range (Gaston,
1988; Roy et al., 1998) again increasing the vulnerability to fragmentation.
Finally, the trophic rank of a species is important and those at higher trophic
levels are expected to be more sensitive because of their lower carrying
capacity (Didham et al., 1996; Hance et al., 2007; Holt, 2002; Kruess and
Tscharntke, 1994; Steffan-Dewenter and Tscharntke, 1999; Steffan-
Dewenter, 2003; Tscharntke et al., 2002; Tylianakis et al., 2007; van
Nouhuys, 2005, Vanbergen et al., 2006) and there is evidence from
experimental food webs that this is indeed the case, although it is just one
of several determinants (Ledger et al., 2012; Woodward et al., 2012).
Body size is a key trait as it determines home range size and dispersal
ability for many species (Castle et al., 2011; Greenleaf et al., 2007; Haskell
et al., 2002; Jetz et al., 2004; Leck, 1979; Lindstedt et al., 1986; Milton
and May, 1976; Schaffer, 1981; Willis, 1979), and large species are often
0.3
0.2
FST/(1-FST)
0.1
0.0
0 2 4 6
-0.1 In (distance) km
10 km 20 km 100 km 500 km
Figure 7 Genetic differentiation as an exponential function of geographical distance
among 33 populations of a predatory caddisfly species (Plectrocnemia conspersa) across
Britain, including 10 sites within the Ashdown Forest (Figs. 5, 6 and 16). Like all
freshwater insects, this species has a larval aquatic phase and a winged terrestrial
adult phase. The former are typically constrained to living in fragmented acid
headwaters (where they are often top predators) within river networks, whereas the
latter can disperse across land to connect otherwise isolated food webs. The genetic
data above reveal panmictic populations at the regional catchment scale, with
significant differentiation (measured as FST/(1 FST) based on allozyme frequency
data) occurring only at larger scales of fragmentation. Even though dispersal across
large distances is a rare event (e.g. Fig. 6), only a few gravid females may be needed
to repopulate an entire food web due to high fecundity combined with strong
density-dependent mortality early in the life cycle (Hildrew, 2009; Hildrew et al.,
2004). Redrawn after Wilcock et al. (2003).
especially vulnerable—unless they are able to span the gaps between fragments
(Crooks, 2002; Ewers and Didham, 2006; but see Laurance et al., 2011). In
Amazonia, wide-ranging forest bird species (van Houtan et al., 2007) and
primates (Boyle and Smith, 2010) are more vulnerable to fragmentation
than those with smaller territoria, and species with limited spatial
requirements such as small mammals, non-trap-lining hummingbirds and
ants are generally less susceptible (Laurance et al., 2011). Besides body size,
restricted mobility, resource specialisation, low annual survival rate, high
population variability, and terrestrial foraging and nesting increase
vulnerability among birds to fragmentation (Sieving and Karr, 1997).
Species that are large and/or rare are especially vulnerable to the effects of
habitat fragmentation by drought in stream food webs (Ledger et al., 2012).
In bees (Box 4), relationships between habitat loss and species traits have
been intensively studied (Krauss et al., 2009; Moretti et al., 2009; Steffan-
Dewenter et al., 2006), with diet width and sociality being especially
important (Aizen and Feinsinger, 1994a,b; Klein et al., 2003; Öckinger
and Smith, 2007; Rundlöf et al., 2008; Steffan-Dewenter et al., 2002).
Social bees are expected to outperform solitary taxa in harvesting
resources because of their higher foraging and food-provision capacity
(e.g. Bommarco et al., 2010) and communication systems (e.g. the
waggle-dance in honeybees). Social bee species are always diet generalists,
because their long-lasting colony needs food throughout the year,
although there are differences between tropical and temperate areas. In
temperate regions, wild social bees (Bombus spp.) appear to be less
sensitive to habitat fragmentation than solitary bees (Steffan-Dewenter
et al., 2002), whereas in the tropics solitary bees appear to be less
sensitive to land-use change than social stingless bees (Aizen and
Feinsinger, 1994a,b), probably due to their specialisation on forest as
nesting habitat (Roubik, 1989, 2006). In bumblebees (Bombus spp.),
long-tongued species have declined more than short-tongued ones due to
changes in agricultural practices and habitat fragmentation (Bommarco
et al., 2012; Dupont et al., 2011), and late-season species have declined
more than early-season species (Fitzpatrick et al., 2007).
4.3. Species trait combinations

Any given species comprise a suite of traits, some of which are strongly
correlated, whereas others may be orthogonal (Herrera, 2009). Data on
individual traits of species, however, are insufficient for predicting
fragmentation effects on biodiversity (Ewers and Didham, 2006): rather,
their combination and the wider ecological context are both key here.
For more detailed examples, see the textboxes on bees (Box 4) and avian
frugivores (Box 5).
A combination of body size, diet, dispersal ability, habitat specialisation
and sociality may be needed to predict species responses to fragmentation
(Boyle and Smith, 2010; Milton and May, 1976). For instance, among
European bees, large dietary generalists are less affected by fragment area
than small generalists, whereas small specialists may be less affected than
large specialists (Bommarco et al., 2010). In Amazonian forest
BOX 4 Bees as Network Nodes

Bee species vary widely in body size, foraging mode, social organisation, seasonal
activity and specialisation on flower resources. These characteristics play an im-
portant role for the structure and dynamics of plant–pollinator networks. Large
body size reflects the capacity to fly longer distances, and genetic markers and
radio-tracking techniques are increasingly used to estimate actual flight distances
(Darvill et al., 2004; Hagen et al., 2011). Small stingless bees (e.g. Plebeia and
Tetragonisca) often fly distances of up to 1 km while flight distances for larger
Melipona species can be > 2 km (Araújo et al., 2004). The largest orchid bees
(Eulaema; 18–31 mm) can fly up to 23 km, including the crossing of unsuitable
matrix habitat such as open waters for several kilometres (Janzen, 1971;
Wikelski et al., 2010). In this bee group, patrolling flights of males can reach
long distances and thus disperse pollen among fragmented plant populations.
Large bees (e.g. Xylocopa, Bombus, Centris, Epicharis, Eulaema and Oxaea) are
hence particularly important for connecting habitat fragments. However, bee
mobility also depends on the abundance of food resources and on the
amount of floral awards.
Sociality and behavioural differences also affect bee species responses to
habitat fragmentation. Not all are as highly eusocial as the honeybees (Apis
spp.) and the stingless bees (Meliponini): most species are solitary (the female
performs all tasks) or subsocial and semisocial (some cooperation among the fe-
males). These differences in social organisation can strongly influence network
topology due to differences in the abundance of individuals in the nest (one,
few, hundreds or thousands). Most eusocial species have perennial colonies, tend
to be floral resource generalists and need resources throughout the year, at least
in the Tropics, and these tend to be key species or hubs in ecological networks.
Most bee species in the tropics are also multivoltine (multiple generations per
year), and some (e.g. Xylocopa) are long-lived, which can affect the temporal dy-
namics of plant–pollinator interactions due to differences in abundance and phe-
nophase length. In arctic or temperate regions, where climatic seasonality is
pronounced and univoltine bee species are dominant, temporal dynamics in
the structure of plant–pollinator networks have already been empirically demon-
strated (Olesen et al., 2008).
Resource specialisation also influences network structure (e.g. the range of
available nectar plants is broader than that of pollen plants) because nectar is
mainly consumed by the adults whereas pollen is used in the brood cell to feed
the larvae (Cane and Sipes, 2006). In general, oligolectic bees are recognised for
their specialised floral niches whereas polylectic bees (e.g. social species such as
Apis, Bombus and Meliponini) visit a wide range of plants (including flowers of
different morphology, colour, size, etc.): within the interaction network, the latter
species represent highly connected nodes.
BOX 5 Avian Frugivores and Seed Dispersal in a Fragmented

World
Avian frugivores predominate in warm and wet climates of the world's tropical and
subtropical regions (Fleming et al., 1987; Kissling et al., 2009). Of the >1200
frugivorous bird species worldwide, most ( 50%) are found within the order
Passeriformes (perching birds) (Kissling et al., 2009, 2012b), with a body mass of
usually < 200 g. Over 100 species of frugivores are also found in the orders
Columbiformes (doves and pigeons), Psittaciformes (parrots) and Piciformes
(woodpeckers, toucans, barbets, honeyguides) (Kissling et al., 2009, 2012b). The
spatial distribution patterns vary among bird orders with frugivorous perching
birds and parrots dominating in the Neotropics and frugivorous pigeons and
hornbills prevailing in Southeast Asia (Kissling et al., 2009). Given the spatial
heterogeneity of future land-use changes on bird distributions (Jetz et al., 2007)
and the taxonomic and geographic differences in frugivores among regions
(Kissling et al., 2009), the global consequences of habitat fragmentation for seed
dispersal of fleshy-fruited plants are likely to be complex.
At the landscape scale, the effectiveness of seed dispersers is characterised by
the quantity and quality of seed dispersal (Schupp et al., 2010), which in turn is de-
pendent upon body size and associated life history behavioural traits. Due to their
requirements for extensive home ranges, large frugivorous birds are especially ex-
tinction prone in small fragments (Renjifo, 1999; Uriarte et al., 2011). The ability to fly
long distances allows large-bodied frugivores to connect habitat patches (Lees and
Peres, 2009; Spiegel and Nathan, 2007). Habitat fragmentation can cause changes
in the movement patterns of frugivores, with consequences for seed dispersal
(Lenz et al., 2011), especially for plants with large, big-seeded fruits because
their dispersal often only depends on one or a few large frugivores (Corlett,
1998; Guimarães et al., 2008). Seed dispersal effectiveness of plants with smaller
fruit largely depends on the range of frugivore body sizes in the network, with
smaller frugivores allowing for within-patch dispersal and larger frugivores for
between-patch dispersal (Spiegel and Nathan, 2007). In addition to body size
per se, gut retention times and movement velocities of frugivores also
determine seed-dispersal distances (Schurr et al., 2009). The interplay of animal
behaviour, plant and animal traits, and the specific characteristics of the
landscape thus produce complex seed dispersal kernels (Morales and Carlo,
2006) and seed dispersal effectiveness landscapes (Schupp et al., 2010).
fragments, the most capable gap-crossers among birds are medium or large
species of insectivores, frugivores and granivores, and these species
dominate in small patches (Lees and Peres, 2009). Certain species trait
combinations can amplify (or mitigate) vulnerability to fragmentation.
For instance, on Barro Colorado Island (Panama), the largest bird was
the Black-faced Antthrush (Formicarius analis), which also had low annual
recruitment and survival rate, and this potent combination of traits, which
are often combined in many other species, could explain why it went
extinct particularly rapidly as its habitat fragmented (Sieving and
Karr, 1997).
Trait matching between interacting plants and animals could affect
higher-level responses to fragmentation. For instance, interactions in some
plant–pollinator networks show size matching, that is, insect species with a
long proboscis visit a wider range of flowers than do species with a short pro-
boscis (e.g. Borrell, 2005; Corbet, 2000; Goldblatt and Manning, 2000;
Harder, 1985; Stang et al., 2009).
Developing a combined trait-response framework could provide impor-
tant future advances in assessing fragmentation effects in ecological net-
works. Additionally, interaction effects between fragment characteristics
(see Section 3.2) and species traits could also be important. Network analysis
offers a potentially powerful way to identify modules of species with similar
responses to fragmentation, which then may be analysed with respect to
their trait combinations (Verdú and Valiente-Banuet, 2011).
5. HABITAT FRAGMENTATION AND BIOTIC

INTERACTIONS
In the previous sections, we have examined the importance of land-
scape structure (e.g. fragment characteristics, habitat edges, matrix) and spe-
cies traits for assessing the consequences of habitat fragmentation on
biodiversity: here, we turn our attention to impacts on species interactions,
the strengths and outcomes of which (Fig. 2) vary spatially and over time.
This spatial dependency arises because the probability of an encounter be-
tween predator and prey, pathogen and host, or mutualistic animals and their
plants has a landscape context, and hence sensitivity to fragmentation.
5.1. Mutualistic plant–pollinator interactions

Pollination and, hence, plant reproduction can be strongly affected by hab-
itat loss and fragmentation (Fægri and van der Pijl, 1979; Jennersten, 1988;
Kearns et al., 1998; Olesen and Jain, 1994; Rathcke and Jules, 1993; Renner,
1998) (for examples see also Box 4).
Due to habitat fragmentation, pollinator communities could become
more homogenous, and generalists (Ewers and Didham, 2006) and intro-
duced species (e.g. Do Carmo et al., 2004) may replace natives and dominate
interactions, potentially altering the reproductive output of the plant com-

munity. However, the effect on pollen dispersal and pollination effectiveness
may strongly vary among species, without necessarily being related to a spe-
cies habitat niche: habitat generalists and invasive pollinators can either be
less (Didham et al., 1996; Do Carmo et al., 2004) or, in some cases, more
effective pollinators than habitat specialists (Dick, 2001).
Fragmentation can isolate host plant patches, reducing genetic and
ecological exchange among them. Although still little is known about
precise flight distances and movement patterns of pollinators at the land-
scape scale (Hagen et al., 2011), body size influences the genetic con-
nectance of, and pollen flow among, distant plant populations (Pasquet
et al., 2008). The effective movement of pollinators may be tracked
by paternity assignment of seeds and pollen (Lander et al., 2011), and
the influence of landscape configuration on pollinator movement (e.g.
for trap-lining species) can be incorporated into the analysis (Lander
et al., 2011).
The reproductive output of plants can vary with pollinator composition,
abundance and behaviour (Lamont and Barker, 1988; Lamont et al., 1993).
Although visitation rates are expected to be influenced by habitat
fragmentation, the results are inconclusive: some pollinators are more
abundant in larger fragments (Sih and Baltus, 1987), some are equally
abundant (Jennersten, 1988), while others are rarer in fragments (Sih and
Baltus, 1987; Strickler, 1979). Temporal aspects such as phenological
changes influence how fragmentation affects plant–pollinator interactions
(Memmott et al., 2007). When fragmentation reduces plant species
richness, food shortages could reduce pollinator diversity, especially
among long-living insects, such as bumblebees (Memmott et al., 2007).
The local extinction of pollinators might not always have consequences
for interacting plants, if redundant species can compensate. For instance, the
Hawaiian tree Freycinetia arborea (Pandanaceae) was once pollinated by now
extinct birds, but has recently been rescued from extinction by an introduced
white-eye bird (Zosterops sp.) that replaces previous pollinator species (Cox,
1983). If redundancy is not evident, even the loss of single interactions can
initiate waves of further extinctions (Nilsson et al., 1992; Olesen and Jain,
1994). For instance, the orchid Cynorkis uniflora is a mountain rock plant
highly specialised upon a few pollinating sphingids in Madagascar (Nilsson
et al., 1992). The host plants of the larvae of these sphingids are found in
nearby forests, and the delicate orchid–pollinator adult/larva interactions
are highly vulnerable to forest loss and fragmentation. The extinction of
the pollinating hawkmoths can trigger the loss of orchids and initiate a
‘cascade of linked extinctions’ (Myers, 1986).
5.2. Mutualistic plant–frugivore interactions

Mutualistic interactions between fleshy-fruited plants and frugivores play a
central role for assessing the consequences of habitat fragmentation on bio-
diversity, especially in the Tropics (Box 5). Frugivorous vertebrates are the
focal seed dispersers because only very few invertebrates (e.g. ants, earth-
worms and grasshoppers) play this role (Duthie et al., 2006; Rico-Gray
and Oliveira, 2007; Willems and Huijsmans, 1994).
Larger animal species are expected to be particularly sensitive to habitat
fragmentation (Haskell et al., 2002), and there is supporting evidence of this
for frugivorous birds (e.g. Sub-Andeans: Renjifo, 1999; Amazonia: Uriarte
et al., 2011). The proportion of fruit in primate diets is positively correlated
with home range size (Milton and May, 1976) and species persistence in for-
est fragments (Boyle and Smith, 2010). The disappearance of large frugivores
thus decreases the probability of long-distance dispersal of fleshy-fruited
plants from small patches and fragments (Fragoso, 1997; Fragoso et al.,
2003; Spiegel and Nathan, 2007; Uriarte et al., 2011). The response of
small-to–medium-sized frugivores to fragmentation is probably driven by
species’ habitat specialisation and matrix tolerance, and their ability of
gap-crossing (Table 1). Compared to medium-sized frugivores, meso-
predators (i.e. medium-sized carnivorous habitat generalists) move more
freely between matrix and fragment (Terborgh et al., 1997).
The traits of fleshy-fruited plants determine frugivore choice and hence
endozoochorous seed dispersal and the relationship between fruit size, con-
sumer size and gape width is the key (Buckley et al., 2006; Burns and Lake,
2009; Jordano, 1995; Lord, 2004). Small fruits are typically consumed by a
wide range of potential seed dispersers, including many species that thrive in
small forest fragments and degraded landscapes (Corlett, 1998). However,
large, big-seeded fruits tend to have fewer dispersers, and the very largest
may depend on only one or a few species (Corlett, 1998). Consequently,
these species are the specialists in the network and most vulnerable to
fragmentation. More generally, the proportion of fleshy-fruited species is
likely to decrease in smaller fragments (Tabarelli and Peres, 2002).
Beyond fruit size, the presence of an inedible pulp, defensive chemicals,
crop size, fruit colour and fruiting phenology also influence frugivore choice
(Buckley et al., 2006; Voigt et al., 2004; Willson and Whelan, 1990), but if
and how they relate to fragmentation is currently unclear. Pre-and post-

ingestion processing of fruit and movement of consumers determine
seed-dispersal distances and plant establishment patterns (Buckley et al.,
2006; Schurr et al., 2009; Spiegel and Nathan, 2007). The mean dispersal
distance of endozoochorously dispersed seeds depends upon a
combination of frugivore body size, mobility and gut retention time
(Schurr et al., 2009). Large frugivores (e.g. the trumpeter hornbill
Bycanistes bucinator) may change their movement patterns, with unimodal
seed-dispersal distribution within forests but bimodal distribution in
fragmented agricultural landscapes (Lenz et al., 2011). Individual fruiting
trees, even exotic ones, in farmland may be important food sources for
the frugivore community and thus represent foci for seed dispersal and
forest regeneration, even in highly degraded landscapes (Berens et al.,
2008; Fisher et al., 2010).
5.3. Mutualistic plant–ant interactions

Another type of mutualism that is important in a fragmentation context is
the interaction between ants and plants in defensive mutualist systems
(Box 6).
The intimacy of this interaction (i.e. the degree of biological association
between individuals of interacting species) varies, and this could determine
how plant–ant interactions respond to habitat fragmentation. Some plant–ant
defensive mutualisms, such as extrafloral nectary-based mutualisms, are typ-
ical among free-living species (Guimarães et al., 2007), that is, each individual
ant and plant can interact with dozens of partners from different species
through its lifespan. These are therefore similar to most of the pollination
and seed dispersal interactions with respect to degree of interaction intimacy
(Guimarães et al., 2007). In contrast, many plant–ant mutualisms are symbi-
otic, that is, one individual plant hosts an ant colony and, as a consequence,
individuals (the plant and the ant colony in this case) interact with one or a few
partners through their lifetime (Fonseca and Benson, 2003; Fonseca and
Ganade, 1996). Few studies have investigated how environmental change
affects the network structure of plant–ant interactions (Diaz-Castelazo
et al., 2010), but information about these mutualistic interactions is
becoming increasingly available.
Key traits in extrafloral nectary interactions include ant body size
(Chamberlain and Holland, 2009) and the distribution of ant and/or plant
abundances (Chamberlain et al., 2010), which are likely to change with
BOX 6 Interactions Between Ants and Plants

Ants form one of the dominant groups in terrestrial ecosystems, and they interact
in multiple ways with plants (Rico-Gray and Oliveira, 2007), as seed predators
(Rico-Gray and Oliveira, 2007), leaf-harvesters (Oliveira et al., 1995; Pizo and
Oliveira, 2000) and mutualistic partners (Christianini and Oliveira, 2009; Palmer
et al., 2008; Rico-Gray and Oliveira, 2007). Although ant pollination is rare
(Beattie, 1985; Gómez, 2000), ants are among the main seed dispersers of
many plant species (Culver and Beattie, 1978; Pizo et al., 2005). In some
tropical ecosystems, ants form gardens (Davidson, 1988), actively dispersing
seeds of plants and nesting within the plant parts. Finally, ants are among the
most conspicuous defensive mutualists of plants (Rico-Gray and Oliveira,
2007), which offer extrafloral nectar, other food resources and/or nesting sites
such as domatia.
Recent studies of extrafloral nectary assemblages suggest ant body size
and species abundance are important in shaping patterns of interactions: the
number of interactions increases with ant body size (Chamberlain and Holland,
2009; Chamberlain et al., 2010). These results mirror those often reported in
predator–prey interactions (Sinclair et al., 2003) and plant–frugivore mutualisms
(Jordano, 2000). Several hypotheses suggest that the effects of ant body size
are more indirect than direct, with larger ants interacting with more plant
species than smaller ants because they (i) forage over a greater area, (ii) are
more widely distributed or (iii) because of size-driven competition hierarchies
(Chamberlain and Holland, 2009). In the latter scenario, larger ants, that often
recruit fewer workers when foraging, are outcompeted by smaller recruitment-
efficient ant species from the optimal resources, leading to an increase in the
number of plants the larger ants interact with.
habitat fragmentation. The effects of fragmentation can differ among ant

functional groups (Pacheco et al., 2009; Wirth et al., 2008), and it may
even benefit some plant–ant networks, which often naturally occur in
habitat edges (e.g. Cecropia spp and its ant partners). Predicting which ant
or plant species will be affected, and how, requires an understanding of the
underlying traits shaping these interactions. The challenge is that we still
need to improve the taxonomy of a considerable fraction of ant species,
and the natural history of many species still remains unknown. In this
context, the phylogenetic relatedness of interacting species is a proxy for
non-random trait distributions.
Understanding the ecological and evolutionary dynamics in these com-
plex fragmented landscapes faces challenges similar to other kinds of
interaction. For example, plant–ant interactions involve organisms that differ

radically in how they perceive their environment. Ants are small, short-lived
organisms, whereas plants are much larger and often longer-lived. Thus, they
will perceive the effects of habitat fragmentation at distinct scales and will re-
spond in different ways. Additionally, all plants and most ant colonies are es-
sentially fixed in space, whereas most other plant–animal mutualisms involve
a fixed individual (e.g. plant) and a mobile forager (e.g. pollinator). Thus, dis-
persal of both ants and plants is a between-generation process, which may lead
to as yet unexplored meta-community dynamics that differ from other types of
network. Moreover, plant–ant protective mutualisms are based on indirect
benefits: plants benefit from a trophic cascade caused by ants attacking her-
bivores (Perfecto and Vandermeer, 2008; Vandermeer et al., 2010). Thus,
if habitat fragmentation changes the intensity of herbivory, it also changes
the fitness consequences of the mutualism (see Palmer et al., 2008).
5.4. Antagonistic interactions within food webs

While the previous sections have focused on mutualistic interactions, we now
address antagonistic interactions, specifically food webs. Body size is a key de-
terminant of predator–prey interactions in many food webs (Emmerson and
Raffaelli, 2004; Woodward et al., 2005), with large predators typically
consuming smaller resources (Layer et al., 2010; McLaughlin et al., 2010),
especially in aquatic systems. As a result, trophic height tends to increase
with body mass (Jonsson et al., 2005; O’Gorman and Emmerson, 2010),
although predator–prey body mass ratios may decline (Brose et al., 2006;
Jonsson and Ebenman, 1998; Mulder et al., 2011). Since large species are
most susceptible to habitat fragmentation due to their perception and use
of resources over larger distances (Holt, 1996) and their need for larger
home ranges (Haskell et al., 2002), top predators should be especially
prone to extinction. As they often exert strong effects within food webs,
their loss could have severe implications for network structure and stability,
although recent field experiments suggest that this might be primarily via
direct effects of their loss from the system rather than more subtle indirect
food web effects per se (Woodward et al., 2012).
Habitat fragmentation can reduce encounter rates and hence interaction
strengths within food webs. This may ultimately decouple pairwise interac-
tions, leading to a simpler and potentially more fragmented food web, since
the starting point at which a food web assembles is the level of interactions
among individuals. In many food webs, predators (and other non-predatory
consumers) are often far from satiation as indicated by the high proportions
of relatively empty predator guts compared with what they could consume if
feeding rates were maximal (Woodward and Hildrew, 2002b). This suggests
that encounter rate is a key determinant of the strength of predator–prey
interactions and network structure (Petchey et al., 2010; Woodward
et al., 2010b).
In a fragmented landscape, encounter rate can be influenced at different
spatial and temporal scales, from short-term patch-scale aggregative re-
sponses of predators to their prey within particular fragments during distur-
bance events (e.g. Lancaster, 1996) to larger scale habitat-level effects that
reflect longer-term depletion of prey by predators.
Handling time is also important for food web structure and dynamics, but
it is difficult to envisage how it might be affected by fragmentation, as it
seems likely to be relatively robust to this kind of disturbance (e.g. in contrast
to the effect of temperature changes). Thus, encounter rate rather than
handling time might change under increasing levels of fragmentation, and
the relative importance of the two rates could be key for predicting the
higher-level effects in food webs (e.g. Petchey et al., 2010).
As in mutualistic networks, the scale and environmental grain of frag-
mentation will also interact with species life histories to determine food
web effects. For instance, in fresh waters undergoing fragmentation (e.g.
temporary pools formed by the retreat or drying of waters from floodplains),
food web interactions can be intensified in the short (i.e. intragenerational)
term if predators and prey are concentrated in increasingly smaller patches.
Conversely, fragmentation may weaken top-down effects in the longer
(intergenerational) term if large predators are lost from small habitat patches.
Here, meta-population and source–sink dynamics and the ability of preda-
tors and prey to recolonise isolated or small habitat patches may be key, and
species traits such as body size, behaviour, life history and taxonomic identity
will influence these dynamics (Ledger et al., 2012).
5.5. Antagonistic host–parasitoid interactions

Antagonistic host–parasitoid interactions can also be affected by habitat frag-
mentation, and the degree of specialisation of parasitoids on their host is
likely to be critical aspect here. When the host is restricted to certain plant
species or habitats, highly host–specific parasitoids will experience land-
scapes as islands within a sea of unusable matrix. Conversely, for a more gen-
eralist parasitoid, capable of using hosts from different habitats, the landscape
represents a mosaic of variable-quality patches. Fragmentation should there-

fore have increasingly negative effects on more specialised parasitoids, and
several empirical studies support this conclusion (moth parasitoids: Elzinga
et al., 2007; aphid parasitoids: Rand and Tscharntke, 2007; leafminer para-
sitoids: Cagnolo et al., 2009; parasitoids of cavity-nesting bees and wasps:
Holzschuh et al., 2010). These findings suggest that the effects of fragmen-
tation on parasitoids will largely be mediated by altered host distributions,
which are often coupled to plant densities (for herbivorous hosts) at the
patch scale (Albrecht et al., 2007; Amarasekare, 2000; Cronin et al.,
2004; Holzschuh et al., 2010; Kruess, 2003; Schnitzler et al., 2011;
Vanbergen et al., 2007).
Although within-patch effects may be important in determining par-
asitoid densities, the location of refuge habitats, parasitoid attack rates and
dispersal ability will determine parasitoid–host dynamics at a landscape
scale (Mistro et al., 2009). The survival of a parasitoid meta-population
will thus largely depend on individual dispersal abilities, and body size
constraints might be important here (Roland and Taylor, 1997). Further-
more, dispersal limitation may moderate parasitoid–host interactions
(Thies et al., 2005) because higher trophic levels are likely to be most
negatively affected by fragmentation (Holt, 1997). The species-specific
extent of dispersal limitation could ultimately determine the relative com-
petitive success of different parasitoid species and how they experience
the host landscape (van Nouhuys and Hanski, 2002). As a consequence
of habitat fragmentation, attack and parasitism rates can change depending
on the fragment isolation, matrix quality and the amount of suitable
habitat in the landscape (Cronin, 2003; Kruess and Tscharntke, 2000;
Roland and Taylor, 1997). The combination of within-patch effects
(habitat quality, host abundance), landscape characteristics (fragment
characteristics) and species traits (e.g. dispersal ability and body size)
can thus ultimately produce a variety of outcomes for parasitoid–host
interactions.
5.6. Summary of fragmentation effects on mutualistic and

antagonistic interactions
The responses of biotic interactions to habitat fragmentation are complex,
but several key themes arise repeatedly for both mutualistic and antagonistic
interactions. The core question is how habitat fragmentation (e.g. fragment
size and isolation) will change the links between species, and these are, in
turn, a product of the functional traits of the interacting species (e.g. body
size, dispersal ability, level of specialisation).
A key species trait is body size because it affects how species interact and
their responses to habitat fragmentation. Its importance is evident in
plant–pollinator interactions (e.g. proboscis length and size of floral struc-
tures), plant–frugivore interactions (e.g. gape width and fruit sizes), plant–ant
interactions (e.g. size-driven competition hierarchies) and food webs (e.g.
predator–prey mass ratios). Beyond general effects of body size and trophic
rank on species interactions, the size of an animal (or plant) also correlates
with a suite of other fragmentation-relevant traits. In particular, body size
determines dispersal ability and movement distances of some taxa, a funda-
mental aspect for persistence in a fragmented landscape. Body size measures
are often used as proxies for estimating movement distances indirectly,
including body mass for birds and mammals (Haskell et al., 2002; Jetz et al.,
2004), measures of wing shape in birds (Dawideit et al., 2009), and body
length, intertegular span or wing span for insects (Cane, 1987; Greenleaf
et al., 2007; Michener, 2007; Rogers et al., 1976). Similarly, fruit sizes can
be used as a proxy for long-distance dispersal in fleshy-fruited plants, at
least when body sizes of their extant vertebrate dispersers are correlated
with seed dispersal effectiveness (sensu Schupp et al., 2010). Given the
tremendous differences in body sizes among species involved in interactions
(e.g. insects vs. vertebrates), responses of different-sized mutualists and
antagonists should vary markedly even within the same level of fragmentation.
Specialisation also influences how fragmentation affects mutualistic and
antagonistic interactions. The degree of habitat specialisation (e.g. forest de-
pendence or matrix tolerance) is important because mutualistic and antag-
onistic interactions will change, as specialised species are lost as
fragmentation proceeds. Dietary specialisation is particularly important in
antagonistic interactions, but also in many mutualistic interactions. In this
context, trophic redundancy may be key to buffering species losses. For in-
stance, in mutualistic interactions, the functional loss of a species may be
compensated by another species of similar size (cf. Zamora, 2000). As
body-size distributions are typically skewed towards small species
(Woodward et al., 2005), the potential for functional redundancy decreases
with increasing body size (and trophic status). Consequently, large species
may be functionally more important for conserving size-dependent ecosys-
tem services, that is, seed dispersal and pollination in mutualistic networks,
pest control by predators and biomass production for human consumption in
fisheries (Rossberg, 2012).
A couple of other aspects, such as the role of animal behaviour, emerge as

important drivers of how fragmentation will affect biotic interactions, but
they might be specific to a particular interaction type. In plant–frugivore in-
teractions, movement behaviour and gut retention times of frugivores will
influence seed dispersal kernels at the landscape scale (Box 5). Flower and
fruit handling behaviour are strongly species-specific and will alter pollina-
tion and seed dispersal effectiveness in mutualistic networks. Furthermore,
differences in sociality (e.g. solitary vs. social bees) will influence spatiotem-
poral abundances of individuals and resource specialisation. To some extent,
such behaviours are phylogenetically conserved, so taxonomic identity can
provide important information in this regard. Unfortunately, in many in-
stances, we still know little about the natural histories of interacting species
and the importance of link strength, especially in tropical regions, which at
present constrains our ability to generalise about fragmentation effects on
mutualistic and antagonistic interactions.
6. EFFECTS OF HABITAT FRAGMENTATION ON

DIFFERENT KINDS OF NETWORKS
6.1. General introduction
Habitat fragmentation influences biodiversity at different organisational
levels, from individuals to species populations, communities and multi-
species ecological networks (e.g. Didham et al., 1996; Hill et al., 2011;
Krauss et al., 2010). To date, little is known about how ecological
networks of interacting individuals and species change in response to
habitat fragmentation. Here, we address potential consequences for the
structure of mutualistic and antagonistic networks (rather than only
interactions per se, see Section 5).
6.2. Mutualistic plant–pollinator networks

Pollination networks are the most species-rich of all mutualistic networks,
globally involving 88% of all angiosperm species, at least 1 million insect spe-
cies belonging to several orders, about 1000 species of birds, hundreds of
lizards and perhaps more than 100 mammals (Carstensen and Olesen,
2009; Olesen and Valido, 2003; Ollerton et al., 2011; Box 7). This
translates into a rich functional diversity with respect to body size,
morphology, mobility, behaviour and breeding systems, which further
leads to a wide variety of adaptive strategies for locating, accessing and
exploiting resources. These strategies vary in space and phenotypic
plasticity, further complicating our efforts to predict outcomes of ongoing

habitat fragmentation processes.
First, habitat fragmentation reduces overall species abundance in pollina-
tion networks and then later species and link richness (e.g. Aizen et al., 2008;
Morales and Aizen, 2006), for example, butterfly species richness and
BOX 7 Diversity and Mobility of Pollinators

Pollinators are known from a wide variety of invertebrate and vertebrate taxa, but
not all groups are equally represented in all networks. There is considerable spa-
tial variation, for example, bird pollination is rare on mainland in Europe whereas
it is common on European islands (Dupont et al., 2004; Kraemer and Schmitt,
1999; Olesen, 1985; Olesen and Valido, 2003; Ollerton et al., 2003). Similarly,
bat pollination is common in the Tropics but virtually unknown from
temperate or arctic regions (Proctor et al., 1996; however, see Ecroyd, 1993).
The taxonomic diversity of flower-visiting animals translates into a broad
range of species traits. For example, body size may vary up to 2000-fold, from
tiny insects (e.g. wasps with a body length of 0.2 mm) to large mammals (e.g.
flying foxes, up to 400 mm in body length), while body size in plant–frugivore
networks may typically vary over one or two orders of magnitude between
small birds and mammals (Fleming et al., 1987). The high diversity of
pollinators results in different strategies for accessing and exploiting floral
resources and in a high variability of how species respond to environmental
disturbances (Kearns, 2001). For instance, flies show very complex and varied
life histories, with larval habitats ranging from predatory through saprophytic
and parasitic. In contrast, bees rely on floral resources during all their life
stages (Michener, 2007). Thus, in flies, larval food supply might be more
important for responses to habitat fragmentation than flower availability to
the adult forms (Bankowska, 1980).
Foraging distances of pollinators range from a few metres to several
kilometres (excluding migration), and almost all taxonomic groups contain sed-
entary as well as highly mobile species. For insects, which comprise the largest
and most diverse group of pollinators, large amplitudes of foraging ranges have
been reported: small solitary bees may fly only a few hundred metres whereas
larger species can fly 10–20 km (Box 4). Much less is known about space use
and foraging ranges of other pollinator groups, although in syrphid flies, a
species-rich group of important flower-visitors, a few species may migrate over
hundreds of kilometres (Torp, 1994), while resident species tend to stay within
a very limited area. Beetles, a relatively minor group among pollinators, tend
to be sedentary and less mobile than other groups (Proctor et al., 1996). Butter-
flies can be classified into three mobility classes: sedentary, intermediately mobile
Continued
BOX 7 Diversity and Mobility of Pollinators—cont'd

and migrant species. While migrants may disperse hundreds to thousands of
kilometres, sedentary species are very local, often limited to one patch of food
plants (Pollard and Yates, 1993). A small group of flower-visitors are the lizards,
which appear to be important for pollination on islands (Olesen and Valido, 2003).
Little is known about their foraging ranges (Nyhagen et al., 2001), but for the com-
mon and widespread, generalist flower-visiting endemic gecko Phelsuma ornata
in Mauritius, 89% of marked individuals were re-sighted on the next day less than
15 m from the place of release, while maximum dispersal range was < 90 m
(Nyhagen et al., 2001). The foraging range of nectarivorous birds depends both
on body size and behaviour (Craig et al., 1981; Gill and Wolf, 1975). For
hummingbirds, these interconnected attributes can translate into different
community roles (Feinsinger, 1978). For instance, some species are trap-liners
tracking spatially dispersed flower resources in a repeated route whereas
other species are territorial and defend clumped resources, highlighting the
potential for behavioural traits to determine the network consequences of
fragmentation (Laurance, 2004).
composition per fragment decline with fragmentation (Öckinger et al.,

2010). This process is called network contraction (Fig. 8; Valladares
et al., 2012).
In pollination networks, abundance of species is positively correlated to
their linkage level (Fig. 9; Olesen et al., 2008; Stang et al., 2009). During
fragmentation, some pollination systems may disappear completely as
abundance declines (Girao et al., 2007). In pollination networks, plants are
generally longer-lived than their pollinators, resulting in an accumulation
of time-delayed plant extinctions (Krauss et al., 2010). Thus, rare specialist
pollinators (linkage level 2 links to other species), which constitute about
half of all pollinator species in networks, are the first to go (Olesen, 2000).
However, fewer pollinator species in a network does not necessarily
compromise the fecundity of all plants, because the outcome depends also
on the effectiveness of the pollinators (Perfectti et al., 2009). It can even be
beneficial if the most abundant pollinators are the most effective, because
other pollinators, which might be less efficient or less specialised pollinators
or even nectar and pollen robbers, disappear (Genini et al., 2010).
However, according to a supposed positive complexity–stability
relationship, fewer species and links in pollination networks lower their
disturbance resilience (e.g. Okuyama and Holland, 2008).
Plants sorted from left to right

according to increasing nectar tube
length n
A clade of
animals sorted Observed
from top to links
bottom
according to
decreasing
tongue length
t
Forbidden links
due to
constraints
(including
phenological
uncoupling)
Figure 8 Pollination network contraction. During habitat fragmentation, pollinator spe-

cialists at the bottom left of the interaction matrix and plant specialists at the top right
go extinct because of their low abundance. The first links to go extinct lie in concave
bands running between lower left and upper right corners. Consequently, the matrix
shrinks, that is, the links become more and more concentrated in the upper left corner
of the matrix.
Survival
probability
Abundance Food / nest site Foraging behaviour
preference
Long-distance foraging
Generalist
Common
Local foraging
Specialist
Rare
Decrease in response strength to HF

Figure 9 A simplified framework illustrating how the survival probability of pollinator
species in response to fragmentation is hierarchically constrained by species traits.
Local pollination networks trapped in single fragments tend to have

higher connectance, because species number decreases and generalists are
expected to survive better than specialists (Barbaro and van Halder, 2009;
Girao et al., 2007; Koh, 2007; Steffan-Dewenter and Tscharntke, 2002;
Williams, 2005; Williams et al., 2009; but see Ashworth et al., 2004).
Furthermore, generalists may opportunistically switch or rewire their
links depending on resource availability, making them less prone to
secondary extinctions (Kaiser-Bunbury et al., 2010) by forcing new links
closer to the upper left corner or the interaction matrix (Figs. 8 and 9).
This will tend to make the pollinator community more homogenous
(Ewers and Didham, 2006). Introduced species, which also tend to be
generalists, tend to replace specialists, and this can influence the
reproductive output of the plant community (e.g. Didham et al., 1996;
Do Carmo et al., 2004) or more so (Dick, 2001).
6.2.1 Nestedness
The different ways networks are structured affect the dynamics of their com-
munities and populations: identifying these patterns and their fundamental
determinants makes it possible to predict the outcomes of habitat fragmen-
tation. A distinctive property of mutualistic networks and food webs is their
nested architecture (Fig. 8; Bascompte et al., 2003; Kondoh et al., 2010).
Neutral models can be formulated to track interactions between two
species with power law/lognormal (POLO) rank abundance distributions
(Halloy and Barratt, 2007), that is, if individuals in two interacting species
link randomly irrespectively of any species traits, except abundance (‘the
neutral theory of biodiversity’; Hubbell, 2001), then the link pattern
becomes strongly nested, and even more so than in real networks.
Abundance alone may explain 60–70% of nestedness in empirical
networks (Krishna et al., 2008), although perturbations push communities
away from a POLO distribution (Halloy and Barratt, 2007). The same
neutral model with abundance variation also produces a nested pattern in
plant–frugivore networks (Burns, 2006).
Abundance distributions show the importance of short-term disturbance
regimes, whereas body-size distributions show more long-term community
effects (Halloy and Barratt, 2007). Extending this to networks, certain nested
link patterns to reflect systems at or close to equilibrium and deviations from
such patterns may therefore be interpreted as a measure of disturbance: al-
though this has yet to be tested formally, it could provide an important new
biodiversity metric to gauge higher-level responses to environmental stressors.
6.2.2 Link switching

The strong effect of abundance is often evident, even in spite of the highly
dynamical nature of linkage (Olesen et al., 2008, 2010b; Petanidou et al.,
2008). An adaptive strategy to cope with spatiotemporal environmental
dynamics is link switching or rewiring (Zhang et al., 2011). During
network assembly or spatiotemporal changes in environmental conditions,
linkage can become increasingly nested as species continuously switch or
rewire partners to enhance their fitness gain from other species. Most
often, these switches are to species with a higher abundance of more easily
exploitable resources, that is, switches towards increasing abundance and
trait matching (‘The resource attraction principle’; Halloy, 1998). Thus,
link switching can place a high selective premium on the ability of an
individual to track resources by optimal diet choice and to exploit all
resources above a given threshold quality (MacArthur and Pianka, 1966),
that is, a more valuable resource becomes a more generalist node in the
network, whereas a consumer with a lower choice threshold becomes a
more generalist node (Kondoh et al., 2010).
When the landscape fragments, an increase in the intensity of fluctuations
of species abundance is expected, and consequently, the ability to do link
switching and resource tracking becomes increasingly critical. In mutualistic
network models, including link switching into linkage assembly models in-
creases the robustness of networks (Zhang et al., 2011). Consequently, spe-
cies such as resource specialists that cannot track increasingly unpredictable
resources are vulnerable to extinction. In networks, we have two kinds of
specialists, ecological and evolutionary: the former because they are rare
(or they feed on very few resources) and the latter because of their evolution-
ary history (low ability to switch resource). Thus, the loss of specialists dis-
appear from networks during fragmentation may arise for different reasons.
6.2.3 Modularity
A commonly investigated linkage pattern in pollination networks is modu-
larity (Olesen et al., 2007). The number of modules depends primarily on
the size of the network. Modules may further have their own ‘deeper’ link
pattern, for example, submodularity and subnestedness (Fig. 10). Modules
are interconnected by species playing specific roles, viz., super-generalists
or network hubs and connectors. Three per cent of species in pla-
nt–pollinator networks are super-generalists, linking to many species within
and outside their own module; 11% are connectors with a few links, but a
high proportion of these links to other modules (Olesen et al., 2007). In the
early stages of fragmentation modules shrink in size, that is, the nestedness
tails are ‘cut off’, and ultimately only the connectors and hubs are left leaving
a topologically simplified network (Carvalheiro et al., 2011). This may ini-
tiate an irreversible transition phase or regime shift in network structure and
dynamics (Kaiser-Bunbury et al., 2011), because at a certain size threshold
modules begin to merge or even disappear. Through extinction and
resource switching among generalists, the network slowly collapses by losing
its modular structure.
6.2.4 Body size

Besides abundance per se, its close correlate body size also has a strong ex-
planatory power of network properties. Body size is an important proxy
for many ecological attributes in food webs (Woodward et al., 2005) and
maybe also with respect to the response of pollinators to fragmentation.
Body size has a huge span in pollinator communities, from tiny 1 mg par-
asitoids to the largest extant pollinator, the 3–4 kg Malagasy Black-White
Ruffed Lemur (Varecia variegata), that is, a difference of six orders of magni-
tude. For comparison, in a lake food web, there may be difference of 10 or-
ders of magnitude in body size (Woodward et al., 2005). However, the
general relationship between linkage level (and thus network position)
and body size in pollination network is not clear, although in Caribbean pla-
nt–pollinator networks, larger hummingbirds are more specialised than
smaller hummingbirds (Dalsgaard et al., 2008).
An equivalent property of the flower is the extent to which floral rewards
are accessible. Stang et al. (2006) reintroduced the term nectar-holder depth,
that is, the depth from the opening of the flower and down to the surface of
the nectar inside the flower. If a flower has a nectar-holder depth n, then
legitimate pollinators have a tongue length t n. If t < n, then the link be-
tween the species pair is ‘forbidden’, that is, morphologically constrained
(Olesen et al., 2010a). Thus, the relationship between t and n becomes tri-
angular, with generalist pollinators and plants having a high t and low n, re-
spectively (Fig. 11; Corbet, 2000; Stang et al., 2006, 2007), as has been
observed in several pollinator groups (Borrell, 2005). Tongue length and
nectar-holder depth are both correlated with abundance, that is, abundant
species have a high t or a low n. Since t and body size are positively
correlated (Corbet, 2000; Stang et al., 2006) or, in fact, triangularly
related (short-tongued pollinators vary considerably in body size, whereas
long-tongued species are all large), large pollinators should, in theory, be
more generalised. However, the evolution of a long tongue in insects
A Plants
Pollinator hub
Pollinator connector
Module
Pollinator hub
Pollinator connector
Pollinators
Submodule
Plant Nestedness
hub isocline
Pollinator hub
Plant
connector
Pollinator hub
Fragments
Pollinator
connector
Pollinator
connector
Figure 10 Expected scenario of the destruction of network modularity during habitat

fragmentation. (A) An intact network in a non-fragmented landscape. The network has
five modules, and three of these are submodular with several submodules (J. M. Olesen,
unpublished data); two modules are so small that no modularity can be detected. How-
ever, the entire network and four of the modules have a level of nestedness that can be
detected; this is indicated with the curved ‘isoclines’ sensu Atmar and Patterson (1993).
continued
3 Fragments
Figure 10—cont’d Most links are to the left of the isocline. Hubs and connectors are
shown as bars. (B) The progressing habitat fragmentation has now caused the network
to fragment as well. The network is present in two fragments: a large and a small one,
and is only connected by one pollinator species. Many of the specialists of both
pollinators and plants are gone and only three modules are left in the large fragment.
The plant community has mainly lost its outcrossing herbs. The upper left two modules
are the same as in (A), whereas the central one is the result of fusion of two modules in
(A). This increases connectance as shown by the change in position and shape of the
isoclines. A few submodules are still left. (C) The network has now got its modularity
completely destroyed by habitat fragmentation. The entire network is now reduced
to three single independent modules, each isolated in their own fragment. Most species
remaining are generalists, and connectance is high. Many plants from (B) are still
alive. They are selfing herbs and long-lived trees, and some of them constitute an
extinction debt.
may be a generalist strategy as it allows pollinators to exploit a higher

diversity of flowers. Borrell (2005) observed the same triangular
relationship between tongue length of euglossine bees and nectar tube
length (Fig. 11). In fact, the relationship is, upon closer inspection, more
trapezoid-like, indicating that long-tongued bees may have problems
with nectar extraction from shallow flowers and that super-generalists
have an intermediate tongue length (Fig. 12). These details are, however,
still poorly explored.
Stang et al. (2007) simulated extinction scenarios based on field data and
found that if abundance is the only determinant then there is no difference in
extinction risk between generalists and specialists, whereas an inclusion of
Forbidden area due to nectar

extraction constraints?
40
35
Bee tongue length (mm)
30
25
20
15
10
20 25 30 35 40 45
Flower tube length (mm)
Figure 11 A triangular relationship between flower tube length (n, nectar-holder depth,
sensu Stang et al. (2006)) and euglossine bee tongue length (t) (data from Borrell, 2005).
Upon a closer look, the relationship may be trapezoid, because bees with the longest
tongue have problems handling shallow flowers with easily accessible nectar.
nectar-holder depth and tongue length constraints gave an increased extinc-

tion risk with increasing n and decreasing t.
Body size is also related to mobility and reproduction (e.g. Greenleaf
et al., 2007; Nieminen, 1996; Öckinger et al., 2010; van Nieuwstadt and
Ruano Iraheta, 1996; Woodward et al., 2005). Expectations are that (i)
highly mobile species are less affected by fragmentation than less mobile
species; (ii) specialists require larger fragments to fulfil their demands and
are also less likely to use the surrounding matrix than generalists and (iii)
r-species are expected to suffer less from fragmentation than K-species,
because of their higher reproductive output, which means relatively more
emigrants to other fragments. All three hypotheses were confirmed in a
study by Öckinger et al. (2010).
The mobility of pollinators affects their population dynamics, genetic
structure and life history but also the other species with which they interact
(Greenleaf et al., 2007), for example, large-bodied pollinators mediate a lon-
ger pollen flow, but also require more energy from their flowers. In many
taxa, mobility increases non-linearly with body size (e.g. Steffan-Dewenter
and Tscharntke, 1999). The specific movement pattern is of importance
25
20
Linkage level of bees
15
10
0
10 15 20 25 30 35 40
Bee tongue length (mm)
Figure 12 Linkage level, that is, number of visited plant species, of euglossine bees is an
increasing function of their tongue length (data from Borrell, 2005). However, linkage
level seems to peak between 30 and 35 mm, and the bees with longest tongue avoid
some flowers (Fig. 11).
here and the influence of a certain landscape configuration on pollinator

movement behaviour can also be incorporated into the analysis (Lander
et al., 2011). Some species mediate a more linear pollen flow, for example,
large bees and trap-lining hummingbirds, than others and such species may
be key hubs or connectors.
In pollination networks, plants with limited modes of attracting
pollinators over long distances suffer most from isolation. For example,
visual cues tend to be more spatially restricted than scent, which can at-
tract pollinators over considerable distances, for example, hawkmoths
(Dudareva and Pichersky, 2006). Amongst generalist pollinators, those
that can forage over longer distances due to morphological and behav-
ioural traits can access distant, more isolated resources, and this increases
their chance of persistence in fragmented pollination networks. It is im-
portant to highlight that this relationship occurs under increasing isolation
scenarios, while habitat loss per se is likely to have the strongest adverse
effects on large-bodied, long-distance flying animals with high resource
requirements.
Plants differ in their dependence on pollinators and seed set by obligate
selfers, for instance, should be unaffected by habitat fragmentation, whereas
facultative selfers may be more affected in terms of seed quality than

quantity. Wind-pollinated plants are also expected to suffer less from
fragmentation than those pollinated by animals due to their long-distance
pollen flow. An important determinant of linkage level in the network-
participating plant community is flower morphology, especially level of
flower openness (accessibility to the interior of the flower), which should
increase with the number of pollinator species, although in reality the
relationship is more complex (Olesen et al., 2007).
6.2.5 Four fragmentation scenarios

Assuming that the response of pollinators to habitat loss and fragment isola-
tion is driven by body size, which could be true for some pollinators such as
birds or specific bees, we can outline a simplified framework of how
plant–pollinator networks will change in response to fragmentation
(Fig. 13). In a system with large and poorly isolated fragments, a
plant–pollinator network will consist of many links, including small-,
medium- and large-bodied pollinators (Fig. 13A). If fragments become
smaller in size, but are similarly isolated, resource availability and nesting sites
will decline to critical levels, forcing species to move between fragments to
maintain population sizes. Very small species with low resource require-
ments are more likely to survive, but species and link diversity of interme-
diate species with low mobility should decline due to a lack of resources
within single fragments. Large species, however, should decline due to lim-
ited resource availability across fragments in the landscape (Fig. 13B).
Maintaining large fragments but increasing the level of isolation will have
a weak impact on small species as they can persist within fragments. Large
species are likely to survive as they can move between distant fragments
due to their large foraging ranges or dispersal abilities (Fig. 13C). The most
affected species are expected to be those of intermediate size, with habitat
requirements exceeding the fragment size but are unlikely to move the large
distances between fragments. The worst-case scenario is that only small frag-
ments remain that are separated by relatively large distances (Fig. 13D).
Then, only some small and maybe intermediate generalist species will be able
to persist and movements among fragments will be rare. As a consequence,
the network is strongly depleted and highly skewed towards small species
(Fig. 13D). Given this simplified framework, the number of links in a
plant–pollinator network is expected to change in predictable ways as a
consequence of habitat loss and isolation (see the two graphs to the right
in Fig. 13).
A B
A B A B D
# Links in network
Increasing isolation
Small pollinators/frugivores AA
Medium-sized pollinators/frugivores
Large pollinators/frugivores
Habitat loss
Plant C D A C D
Fragment
Isolation
Increasing habitat loss
C D
Figure 13 Simplified framework for the response of pollination and seed dispersal net-
works to habitat loss and isolation. The illustrated framework assumes that body size is
the key trait for the response of pollinators and frugivores to fragmentation. In (A), a
system with large and poorly isolated fragments contains a plant–pollinator/frugivore
network with many links, including small-, medium-sized and large-bodied animals. In
(B), fragments become smaller in size (but with a similar degree of isolation), resulting in
a decline of small and intermediate species with low mobility and a loss of large-bodied
species. In (C), large fragments have an increased level of isolation with weak impacts on
small species and more pronounced effects on intermediate and large-bodied species.
In (D), a landscape with small and isolated habitat fragments only sustains some small,
and maybe intermediate, generalist pollinators or frugivores. The bipartite networks de-
pict hypothetical pollination or seed dispersal networks covering the entire landscape.
The number of plant species is kept constant. The two graphs on the right hand illus-
trate how the number of links in these plant–animal networks changes as a conse-
quence of habitat loss and isolation under this simplified framework.
6.3. Mutualistic plant–frugivore networks

Frugivores include a large diversity of taxa, from annelids to elephants, and
fish and herps, spanning body masses from a few grams to several tonnes.
Plants that produce fleshy fruits and rely on animals for seed dispersal are also
diverse and differ in fruit size, seedling vigour, phenophase length and so on.
In terms of the potential effects of habitat fragmentation, it matters which
critical frugivore or plant life strategies are correlated within a network.
For example, rare species might be more prone to local extinction following
fragmentation (Davies et al., 2004) but they could be occupying peripheral
positions in the network, or may be central species. Body mass influences
population viability in fragmented landscapes (see e.g. Galetti et al., 2009
for mammals), but we are not aware of any studies to date that have mapped
this onto plant–frugivore networks.
The overall response of such networks to fragmentation will depend on
the array of species traits in the interacting assemblage. Differential responses
and susceptibility among frugivore species will cause variation in incidence
functions (Gilpin and Diamond, 1981) of each species across fragments in a
complex landscape (Fig. 14), determining variation in survival probability in
Incidence (J)
Fragment size (A)
Figure 14 Incidence functions of frugivore species along a gradient of habitat loss (frag-
mentation). Incidence functions (top) represent the fraction of habitat patches of a
given size where a frugivore species is present. Large-bodied frugivores will most likely
disappear from small- and medium-sized fragments, while small-bodied frugivores
would be the only species present in the small remnants. Variable incidence functions
will thus result in differences in specific composition (species richness, relative abun-
dance) of different fragments which, in turn, will cause large variations in network to-
pology and structure (bottom).
fragments of variable area. This will typically result in different richness and
composition of the local plant–frugivore assemblages among fragments, with
reciprocal influences between them (Kissling et al., 2007). Patterns of frag-
ment occupation will be driven by colonisation/extinction dynamics, which
will depend on how species respond to loss of habitat area and/or increasing
distance and isolation among fragmented patches (Luck and Daily, 2003).
While Fig. 14 illustrates the depauperation of frugivore assemblages, a similar
scenario could be envisaged for fruiting plants, showing, for example, var-
iable incidence functions associated with seed mass or fruit-size variation.
The figure is inspired by trends in the composition of avian frugivore assem-
blages in the Atlantic forest of SE Brazil (Fadini et al., 2009; M. Galetti, per-
sonal communication; also see Estarada et al., 1993; Githiru et al., 2002;
Graham, 2002). This highly fragmented landscape is impacted not only
by habitat loss processes but also by different levels of hunting and
poaching that, taken together, drive dramatic local changes in frugivore
abundance across fragments (see e.g. Almeida-Neto et al., 2008; Galetti
et al., 2009). Large tracts of Atlantic rainforest harbour reasonably
complete frugivore assemblages and associated dispersal services to
the plants (Fig. 14), yet the smaller fragments contain impoverished local
communities that invariably lack the larger frugivores, such as toucans,
large cracids and cotingids, whereas the dominant frugivores are thrushes
and thraupids. The overall effect is highly transformed interaction
networks in the fragments (Fig. 14, bottom) with reductions in degree,
and potentially drastic increases in modularity due to loss of large super-
generalist frugivores. This also reduces nestedness, largely due to
the missing ‘glueing’ interactions that the generalists provide (Olesen
et al., 2010a).
Plant–frugivore networks could exhibit similar responses to fragmenta-
tion to those described for pollination networks (Fig. 13), as the main rel-
evant traits (e.g. body mass) are similar. The plant–frugivore networks in
landscapes with large and well-connected fragments will harbour reasonably
complete networks, with diverse interactions in nested assemblages
(Fig. 13A). Most frugivorous birds, for instance, include generalised foragers
with flocking behaviour and seasonally altitudinal migrants; many should
have high mobility and dispersal abilities. Santos et al. (1999) reported that
drastic alterations of local thrush assemblages in juniper fragments in central
Spain mainly occur in the smallest fragments (also see Luck and Daily, 2003).
If fragment area becomes reduced, but still maintaining good connectivity,
some large species may still be lost because of reduced home range sizes and
resource abundance. As for plant–pollinator networks, small species with

reduced resource requirements are likely to survive (e.g. small avian frugi-
vores with mixed diets, not relying extensively on fruit), while species and
link diversity of small- and medium-bodied species with low mobility and
large species should decline (Fig. 13B). With increased isolation, small spe-
cies may persist in medium-sized and even small fragments, whereas the per-
sistence of larger species will depend on their ability to disperse among
fragments (Fig. 13C). As with the pollination networks, seed dispersal inter-
action networks in landscapes with both reduced fragment area and poor
connectivity should be more prone to collapse (Fig. 13D; see e.g. Santos
et al., 1999). Then, only some small, and maybe intermediate, generalist
species will be able to persist and movement among fragments will be rare.
The small fragments cannot support large species, and the network is again
strongly biased towards a few small species (Fig. 13D).
Fragmentation and habitat loss will ultimately induce the loss of specific
nodes (either plants or animals), reduced population densities of mutualistic
partners, resulting in dramatic losses of important functional attributes. For
example, in some Pacific islands, populations of flying foxes are periodically re-
duced by hurricanes to a point beyond which their capacity to disperse the seeds
of big-seeded trees decreases dramatically (McConkey and Drake, 2006). Such
functional losses will not take place at random, but will be concentrated in cer-
tain species, like larger frugivores and large-fruited plants. In summary, the main
consequences of fragmentation for plant–frugivore networks will depend upon
the extent that key traits determining susceptibility of species correlate (or
match) with traits that define their functional roles in the network.
6.4. Mutualistic plant–ant networks

Symbiotic and free-living plant–ant mutualisms are organised in networks
that differ markedly in their structure (Blüthgen et al., 2007; Fonseca and
Ganade, 1996; Guimarães et al., 2007): for example, those that include
extrafloral nectaries are often nested, whereas symbiotic, plant–ant
networks are always strongly modular (Guimarães et al., 2007). These
correlations between biological attributes and network structure can be
used to infer likely responses to habitat fragmentation.
If habitat fragmentation affects ant species of distinct body sizes differ-
ently (see Section 5.3), the same will be true for the highly and poorly con-
nected species. At present, the underlying mechanisms linking ant body size
to the number of interactions and the degree of overlap among partners are
unknown, making it difficult to predict the consequences for species
networks, even if there is a clear body size-biased effect of habitat fragmen-

tation on species composition (however, see Chamberlain and Holland,
2009). Thus, it is fundamental to develop a better understanding of how
ant body size is related to network structure in plant–ant interactions to pre-
dict the fate of these networks facing habitat fragmentation.
Phylogeny is an important predictor of the structure of symbiotic net-
works (Fonseca and Ganade, 1996), which are composed of modules that
often contain closely related ant and/or plant species. This strong associa-
tion between phylogeny and network structure is predicted as a conse-
quence of a ‘complex coevolutionary handshaking’ among interacting
partners (Thompson, 2005). This relationship should enable responses of
plant–ant networks to fragmentation to be predicted, if sensitive groups
of taxa can be identified a priori: if the phylogenetic signal is very strong,
such as in symbiotic plant–ant interactions, susceptibility traits and traits
shaping the role of a species within a network are likely to be strongly
correlated.
Key questions that need to be addressed include how nestedness will alter
with changes in ant species richness and composition: the current evidence,
although still limited, suggests the nested structure of extrafloral nectary net-
works to be robust to species turnover and invasions (Diaz-Castelazo et al.,
2010). It is also important to understand how the strong modularity of sym-
biotic networks is affected by habitat fragmentation, which has the potential
to cause the emergence, loss or even fusion of modules (e.g. via invasions of
generalist ant species). In a fragmented landscape, one could imagine the cre-
ation of a mosaic of plant–ant networks varying in species composition and
consequently in nestedness and modularity.
6.5. Antagonistic food webs

The effects of fragmentation on food webs have been surprisingly over-
looked. In terrestrial systems, we can envisage fragmented networks in
the classical biogeography sense when they are situated within islands within
an aquatic matrix. An example of this comes from recent work carried out in
Ireland (McLaughlin et al., 2010). The Gearagh woodland, located in the
floodplain of the River Lee in County Cork, is composed of a complicated
braided river system composed of approximately 13 channels, each 1–7 m
wide. The main channels are stabilised by tree roots, which create a mosaic
of small islands due to the accumulation of detrital material and fallen trees
over time. A food web study, examining the trophic structure of the inver-
tebrate community on series of 16 islands, ranging in size from 4.5 to
40.8 m2 found that, on average, the larger islands contained more species and
links than the smaller islands, and network structure consequently differed
markedly among fragments (Fig. 15).
Fragmentation of food webs can also occur in other lateral (i.e. across
landscape) and temporal dimensions, as well as via fractal branching pattern
Gearagh regional web
13.00
Local island webs
20.97
16.38
13.22 15.96
4.05
29.82 4.06
8.64
6.92
4.72
13.37
40. 83
15.30
Area (m-2)
5.83
5
Island
8.55
Channel
Figure 15 Schematic representation of the riverine network with the Gearagh forest,
Ireland. Individual islands are inserted beside the river channel in which they were lo-
cated (McLaughlin et al., 2010). The Gearagh is a complicated braided river system com-
posed of approximately 13 channels, each 1–7 m wide. The study site was comprised of
a small proportion of these channels. The stabilising effect of the tree roots within the
main river channels, in conjunction with the accumulation of detrital material and tree
falls, has resulted in the above mosaic of small islands. The diameter of the web from
each island is scaled linearly with species richness: the larger webs are found in the
larger fragments. Note: each web contains the same number and positioning of nodes
as in the global web: solid black nodes represent macroinvertebrate taxa present within
the depicted web and grey nodes indicate taxa present in the global web but absent
from the depicted web.
dimensions (e.g. in river networks) (Box 1; Fig. 16). Additionally, vertical

fragmentation, which is even more rarely considered, can occur, such as
in mountainous regions (Box 8; Fig. 17).
The loss of large consumers at higher trophic levels due to habitat frag-
mentation should result in a decreased overall trophic height of the food
web, driven by shorter food chains (e.g. Byrnes et al., 2011; O’Gorman
and Emmerson, 2009; Woodward et al., 2012). This could also lead to an
increase in the proportion of top consumers relative to intermediate
species, as the latter are effectively promoted to the termini of food
LOCAL(STREAM)CATCHMENT REGIONAL GLOBAL

(CATCHMENT) (INTER-CATCHMENT)
6.6
NETWORK NETWORK
6.5
6.7
River Medway
6.1
6
5.9
Ashdown
6.5
5.3
6.1
6.4
5 pH
Stream
Watershed
6.5
6.5
Forest
6 5
River Ouse
6.7
6.6
Figure 16 Ecological network structure of stream food webs from the Ashdown Forest,
UK, shown from local to regional to global networks. Note: each web contains the same
number and positioning of nodes as in the global web: solid black nodes represent
macroinvertebrate taxa present within the depicted web and grey nodes indicate taxa
present in the global web but absent from the depicted web (Fig. 15). Web diameter has
been scaled to the number of nodes as a % of those in the global web: thus the smallest
web also contains the fewest species. All streams are headwaters of either (a) River Med-
way or (b) River Ouse, which are separated into discrete watersheds (separated by the
dashed east–west line) that flow predominantly either north or south into the sea. In-
dividual networks are constrained by the ‘hard’ boundary of the water's edge and the
‘soft’ boundary of a physiochemical gradient (indicated by mean stream pH, within cir-
cles adjacent to each web). All individual streams can be viewed as a fragmented com-
ponent of the catchment network, which in turn is a component of the global network.
The increasing complexity of the network can be seen as the number of nodes and con-
sequently the number of interactions increases once the fragmented nature of the land-
scape and habitat is discounted.
BOX 8 Fragmentation of Mountainous Aquatic Food Webs

Habitat fragmentation is typically considered in lateral (i.e. across landscape) and
temporal dimensions, but vertical fragmentation is also possible, for example, in
mountain ecosystems. At high altitudes, glacier retreat and changes to the mag-
nitude of snowpack accumulation and their duration are likely to cause major
changes to aquatic ecological networks within an already fragmented landscape
(e.g. Brown et al., 2007, 2012; Finn et al., 2010; Jacobsen et al., 2012; Milner et al.,
2009). There are strong upstream to downstream gradients in aquatic biological
assemblages in these systems, driven predominantly by changes in stream water
temperature and the geomorphological stability of the river channel (Milner et al.,
2001). Consequently, alpine river food webs are highly fragmented along even
short distances (kilometres), with high turnover of species, food web links and
species’ contributions to secondary production (e.g. Fig. 17). In non-glacial
mountain rivers, altitudinal pressure effects on the saturation of dissolved
oxygen can impart major effects on community composition (Jacobsen, 2008).
Montane aquatic ecosystems that rely on meltwater are particularly
susceptible to fragmentation, particularly in situations where decreases in
meltwater production lead to drying of some river sections (e.g. Malard et al.,
2006). Natural occurrences of river ecological network fragmentation are also
evident where lakes introduce discontinuities into the system (Milner et al.,
2011; Monaghan et al., 2005). Alpine lakes lead to notable changes in
community composition and the relative abundance of morphological and
biological traits relative to the nearby flowing waters, but may be insufficient
to prevent insect dispersal and thus genetic differentiation within river valleys
(Monaghan et al., 2002). Fish may be restricted to lower altitudes due to
thermal or geomorphological barriers (e.g. falls, canyons; Evans and Johnston,
1980), thus preventing their upstream migration to avoid warming. Therefore,
the more productive and species-rich aquatic food webs at lower altitude sites
(e.g. Fig. 17) may fragment as some mobile organisms such as invertebrates
are able to migrate to higher altitudes. The immigration of ‘lowland’ species to
higher altitudes may also upset the balance of these food webs, causing
fragmentation but also succession. Additionally, at higher latitudes, there may
be fragmentation as the range of some amphibians (e.g. Pyrenean Brook
Newt, Calotriton asper) expands from currently clear water habitat (Parc
National des Pyrénées, 2005) into glacier-fed rivers that are receiving less
meltwater (and proportionally more groundwater) with glacier retreat.
chains as the largest higher-level predators are lost (see O’Gorman and
Emmerson, 2010; Woodward et al., 2012). Loss of large species at high
trophic levels is also likely to result in reduced linkage density (Montoya
et al., 2005; O’Gorman et al., 2010) and connectance (O’Gorman and
Emmerson, 2010) within local networks, as well as reduced
Lac d’Oredon
1850 m
1 km
2150 m
Pic Mechant
(2944 m)
2370 m
2839 m
Basal resources
Primary consumers
Predators
Pic d’Estaragne
(3006 m)
Figure 17 Stream benthic food webs along an altitudinal gradient in the Estaragne
catchment, French Pyrénées. Light grey circles denote basal resources; dark grey de-
notes primary consumers; black denotes predators. Three food webs are displayed
for (i) 2370 m altitude, maximum water temperature (Tmax) ¼ 4.5 C, no. species (S) ¼
16, no. links (L) ¼ 46, secondary production (2P) ¼ 4.9 g m 2 year 1; (ii) 2150 m altitude,
Tmax ¼ 8.5 C, S ¼ 25, L ¼ 93, 2P ¼ 6.55 g m 2 year 1 and (iii) 1850 m altitude,
Tmax ¼ 138 C, S ¼ 30, L ¼ 87, 2P ¼ 7.6 g m 2 year 1. The individual food webs are frag-
mented as the individual study sites are separated by soft boundaries. Together, these
food webs combine to a composite web of 41 species with 164 links. Figures redrawn
from Lavandier and Décamps (1983) and Lavandier and Céréghino (1995).
compartmentalisation, which could make the web less robust to secondary

extinctions (Dunne et al., 2002), although this is not necessarily the case if
there is high redundancy in the system (Woodward et al., 2012). Large
species may have weak per unit biomass interactions with their prey and
high functional uniqueness (O’Gorman et al., 2011), so their extinction
could increase the overall interaction strength within the system. This
may reduce stability (see McCann et al., 1998; Neutel et al., 2002), while
loss of functional trait diversity will alter ecosystem process rates and
functioning (Petchey and Gaston, 2006).
Body-mass-driven extinctions due to habitat fragmentation may cause an
overall increase in the predator–prey body mass ratio, assuming that larger
predators eat prey closer to their own body mass (Brose et al., 2006). Smaller
predator–prey body mass ratios have been linked to longer food chains due
to their stabilising properties (Jennings and Warr, 2003; Jonsson and
Ebenman, 1998; however see Mulder et al., 2009; Reuman et al., 2009),
so increases could raise the probability of catastrophic phase shifts or total

collapse. Conversely, in systems where large predators are considerably
larger than their prey (e.g. fish eating invertebrates vs. invertebrates
feeding on other invertebrates), the loss of these consumers could
increase stability of the food web, as appears to be the case in headwater
streams where fish are lost due to habitat loss and fragmentation arising
from chemical and/or physical barriers (Layer et al., 2010, 2011).
The response of freshwater food webs to fragmentation by droughts
(Box 1) has been characterised recently by manipulating flows in a series
of artificial stream mesocosms (Ledger et al., 2008, 2011, 2012;
Woodward et al., 2012; Fig. 18). These model systems reflected the
abiotic conditions, biodiversity and food web properties of natural
streams (Brown et al., 2011; Harris et al., 2007; Ledger et al., 2009).
The results of this fragmentation experiment revealed some dramatic
impacts on the food webs: consistent with the higher trophic rank
hypothesis (e.g. Holt, 1996), top predators’ production declined by
>90%. Among the primary consumers, production of shredder
detritivores was also suppressed (by 69%), whereas the base of the food
web was relatively unaffected (Ledger et al., 2011, 2012). Contrasting
responses were evident among functional groups, ranging from
extirpation to irruptions in the case of small midge larvae, although
production of most species was suppressed. The ratio of production to
biomass increased, reflecting a shift in production from large, long-
lived, taxa to smaller taxa with faster life cycles (Ledger et al., 2011).
Fragmentation by drought caused high mortality and the partial collapse
of the food web from the top-down (Ledger et al., 2012) as well as
reversing successional dynamics of benthic algal assemblages (i.e. basal
resources), with effective colonists replacing competitive dominants
(Ledger et al., 2008, 2012). The general shift in biomass flux from
large to small species could not fully compensate for the overall biomass
flux. Many other network characteristics (e.g. connectance) were,
however, conserved, suggesting some higher-level properties might
be conserved even when exposed to extreme perturbations (Woodward
et al., 2012).
Fragmentation can also affect marine food webs (Box 1). Coral bleaching
creates fragments of surviving coral surrounded by reef pavement and coral
rubble, with consequences for top-down control as average food chains
shorten, generalist species proliferate and phase shifts may occur (Hughes,
1994). Simulations of fragmentation processes in Caribbean coral reefs indicate
that species losses due to body size or diet constraints will lead to decreases in
Regional web (all spatial replicate webs and both treatments combined)
Controls (permanent flow) Fragmentation (drought perturbation)
Summary web Summary web
C1 C2 C3 C4 D1 D2 D3 D4
Spatial replicate webs Spatial replicate webs
Figure 18 Impacts of habitat fragmentation caused by drought in experimental stream

food webs: results from a long-term field experiment in artificial streams (Brown et al.,
2011; Ledger et al., 2008, 2009, 2011). Drought can have patchy effects in river networks
and individual stream channels can be viewed as fragmented patches in the wider
riverscape. Note the two experimental treatments (monthly drought disturbance vs.
permanent flow) were randomised spatially among the eight stream channels, but
are grouped into two blocks here for illustrative purposes. The diameter of the
circular webs is scaled according to species richness relative to the global web for
the combined network. Solid nodes represent species present in a given web; open
nodes represent those found in the global but not in local web (Figs. 16 and 17).
Droughts simplified the networks with marked impacts on large rare species high in
the web.
number of links and changes in connectance and food chain length (Fig. 19).
Human-induced fragmentation in seagrass food webs could further lead to
fewer trophic groups and top predators, lower maximum trophic levels,
shorter food chains and prey-dominated communities (Coll et al., 2011). In
kelp forests, habitat loss and fragmentation due to storms simplify marine food
webs, mainly by decreasing diversity and complexity at higher trophic levels,
resulting in shorter food chains (Byrnes et al., 2011). The effects of habitat frag-
mentation on food webs, although little studied, can be pronounced.
6.6. Antagonistic host–parasitoid networks

Besides food webs, several examples from other multitrophic systems give an
indication of how antagonistic host–parasitoid networks may be affected by
fragmentation (Cronin, 2004; Kruess, 2003; Thies et al., 2005). However,
Intact Caribbean coral reef
S = 247
L = 3288
C = 0.054
FCL = 3.12
-25% largest species -25% most specialist
S = 185 S = 185
L = 1185 L = 2413
C = 0.035 C = 0.071
FCL = 3.01 FCL = 3.22
-50% most specialist
-50% largest species

S = 123 S = 123
L = 683 L = 1594
C = 0.046 C = 0.11
FCL = 2.89 FCL = 3.19
-75% largest species
-75% most specialist
S = 61 S = 61
L = 258 L = 384
C = 0.069 C = 0.10
FCL = 2.61 FCL = 2.77
Figure 19 Simulated consequences of fragmentation-driven extinction scenarios on

the network properties of a Caribbean coral reef. As species (S) are lost according to
body size, the number of links (L) in the web decreases exponentially, leading to
unpredictable fluctuations in connectance (C) and a linear decrease in mean food chain
length (FCL). As species are lost according to diet specialisation, L decreases linearly,
leading to an overall increase in C and FCL until a critical threshold is reached and
the system undergoes a phase shift to a new state (e.g. macroalgae dominated). Coral
reef photos are used by kind permission of José Eduardo Silva, Stephen Leahy, Nick Gra-
ham and James Acker (respective photo credits, from top to bottom).
because species respond differently to fragmentation effects, it is currently

not possible to predict whether some will compensate for others, and
therefore how overall parasitoid–host network structure will be affected,
although progress is being made in this area. For instance, in restored and
adjacent intensively managed meadows, the abundance and parasitism
rates of bee hosts decreased with increasing distance from restored
meadows and the diversity of interactions declined more steeply than the
diversity of species (Albrecht et al., 2007). This suggests a strong impact of

habitat fragmentation on trophic networks and that interaction diversity
might decline more rapidly than species diversity in fragmented systems.
Another study examined host–parasitoid networks of specialist leafminers
and their parasitoids on individual oak (Quercus robur, Fagaceae) trees in
different landscape contexts (Kaartinen and Roslin, 2011). Isolated
patches had fewer species and different composition than well-connected
patches, but the quantitative metrics of network structure (interaction
evenness, linkage density, connectance, generality or vulnerability) were
unaffected, indicating some degree of functional compensation across
species. More case studies are now needed to test the generality of
fragmentation effects in host–parasitoid networks.
6.7. General effects of habitat fragmentation on network

properties
The examples above illustrate that the properties of mutualistic and antag-
onistic networks can be strongly affected by habitat fragmentation, although
this field is still very much in its infancy (Burkle and Alarcón, 2011; Fortuna
and Bascompte, 2006; Gonzalez et al., 2011). Simulation studies indicate
that mutualistic networks can be buffered to some extent against habitat
fragmentation (Fortuna and Bascompte, 2006). Real communities might
persist for longer but start to decay sooner than randomly generated
in silico communities, with resilience against fragmentation being
provided by degree or link heterogeneity (Jordano et al., 2003),
nestedness (Bascompte et al., 2003), compensatory responses and/or
redundancy (Ledger et al., 2012).
Species and link richness vary with habitat area, with the latter seemingly
being more sensitive to fragmentation than the former (Sabatino et al.,
2010), that is, as a local habitat shrinks, interactions are lost faster than
species. This might be related to a reduced abundance of species (without
initially going extinct), which reduces interaction probability (encounter
rate). It might also be a consequence of several species having more than
just one interaction, although ecological networks are highly skewed
(Jordano, 1987). Habitat fragmentation influences the strength and timing
of species interactions, which can cause cascading secondary extinctions
in networks (Solé and Montoya, 2006; Terborgh et al., 2001; Tylianakis
et al., 2008).
Nestedness and other network structure parameters are often determined

by relative species abundances (Krishna et al., 2008). Given that habitat frag-
mentation reduces abundance (Hadley and Betts, 2012), nestedness should
change with increasing fragmentation. Fragment area and trophic level or
dietary guild identity are likely to influence the degree of nestedness in frag-
mented landscapes (Hill et al., 2011). Furthermore, effects of vegetational
aggregation (clustering of plants in a landscape) and mobility of species
can affect network properties, especially in antagonistic and plant–frugivore
networks, while these influences on plant–pollinator network structure may
be less pronounced (Morales and Vázquez, 2008).
Habitat fragmentation can also influence network substructure (modu-
larity or compartmentalisation) and the extinction of top consumers may
disconnect spatially segregated ecological networks and thus increase mod-
ularity. The opposite effect may be triggered by the invasion of hyper-
generalist species, which connect distinct modules and reduce modularity
in fragmented landscapes (Aizen et al., 2008). At some point, the local net-
work must reach a critical level, below which modularity no longer exists.
Thus, the modular structure disintegrates before the local network disap-
pears completely. Using a spatial network approach, modularity analysis
may lump similar fragments together based on their constituent species
(for a biogeographical example, see Carstensen et al., 2012). Fragments
within the same landscape might therefore have more similar dynamics
and trajectories of change in species composition than those in other land-
scapes (‘landscape-divergence hypothesis’; Laurance et al., 2007), which
could be tested with modularity analyses if data from several fragmented
landscapes are available.
Fragment size and isolation affect the composition of ecological net-
works: while large areas can support most interactions needed for normal
functioning, small fragments will contain only a core group of species and
fewer important interactions (see Section 7). The degree of specialisation
of a species will determine whether it can persist, with generalist mutualists
being least likely to suffer extinction (Fortuna and Bascompte, 2006). Matrix
quality also determines the impact of fragmentation on networks as it defines
landscape permeability. Network susceptibility will thus depend on species
composition, interaction types and landscape properties (Bender and Fahrig,
2005): one could argue that large fragments have a higher conservation value
due to the increased likelihood of modularity, which reduces the risk of the
spread of disturbances.
7. HABITAT FRAGMENTATION IN A META-NETWORK

CONTEXT
Meta-population ecologists envision a natural landscape as consisting of
suitable habitat patches (fragments) containing local species populations, con-
nected through dispersal (Hanski, 1998). Local extinction and colonisation
create a dynamic state (Hanski and Simberloff, 1997), determined by the iso-
lation of the patches (including matrix permeability) and the reproductive po-
tential of each population. Likewise, the extinction probability in a given
patch is related to its isolation (how likely the patch is to receive immigrants),
area (small patches often have smaller populations, which are more vulnerable
to stochasticity) and quality (MacArthur and Wilson, 1963; Hanski, 1998,
1999). Thus, patches are often divided into sources and sinks, depending
on whether the populations are producing an excess of individuals or are
relying on a net input to persist (Hanski and Simberloff, 1997).
Single-species meta-population models have been extended to models of
two or more interacting species, which, through antagonistic or mutualistic
interactions, modify the dynamics of each other, alongside traditional meta-
population dynamics (extinction and colonisation) (Hanski, 1999; Nee
et al., 1997; Prakash and de Roos, 2004). Intriguingly, Nee and May
(1992) demonstrated that species interactions (superior competitor and
inferior coloniser vs. inferior competitor and superior coloniser) may
change species composition in remnant patches in a fragmenting landscape.
The complexity of the mathematical models describing the dynamics of
meta-populations increases rapidly as more species are added (Klausmeier,
2001), but in reality, habitat fragmentation affects whole communities of
multiple species interacting simultaneously.
With an implicit reference to meta-populations and meta-communities
(Hanski, 1999; Hanski and Gilpin, 1997), meta-networks can be defined
as a set of spatially distributed local networks connected by species
dispersal and influenced by colonisation and extinction dynamics (Fig. 20).
These meta-networks can be considered as a combination of spatial and
ecological networks (see Section 2) in a meta-population context. To date,
little work has been done in this field, although such approaches offer a
promising means for assessing (1) dispersal and movement between local
networks, (2) the colonisation and extinction of species in local networks
and (3) implications of habitat fragmentation on the topology of local
networks.
Figure 20 Ecological networks in a meta-network context. A fragmented landscape

consists of local habitat fragments separated by a more or less permeable matrix. Within
each habitat fragment, networks of interacting species can be found which differ in their
structure and degree of complexity. A fragmented landscape usually contains frag-
ments of different sizes at different degrees of isolation. Here, it is illustrated how a
big fragment, containing many interacting species, may support minor fragments via
species dispersal and thereby contribute to the maintenance of species composition
and local network structure. However, small fragments are not able to support all spe-
cies and isolated fragments are less likely to receive immigrants, and thus, some species
and interactions (hence, links) will be lost. The thickness of the ‘bridges’ between frag-
ments represents the relative degree of species movement between them. In some
cases, dispersal might be bidirectional while in others (especially between large and
small fragments) movement might be unidirectional, that is, from a source to a sink.
Note that the most specialised species are likely to be the most vulnerable. A different
effect on network structure will emerge if criteria other than specialisation are used.
7.1. Meta-networks and dispersal

Dispersal and movement of species among patches may be density-dependent
or density-independent (Hansson, 1991; Kuussaari et al., 1996; Sæther et al.,
1999 and references therein). Low-density dispersal may, for example, be due
to a failure in locating mates or specialised mutualists. When locating
specialised mutualists, it is the density of the interacting partner that is
critical for moving and dispersing. High-density dispersal, on the other
hand, may be a result of resource competition among conspecifics or other
species. Here again, the network approach offers promise, as it not only
specify who is interacting with whom, but also who is interacting with the
same partner and thereby, potentially, competing for the same resources. If
a landscape becomes more fragmented over evolutionary relevant time
scales, increased (mean and long-distance) dispersal rates will be selected
for. For example, some sphingid male hawkmoths have evolved a strong
olfactory sense enhancing their dispersal success and experienced meta-
network-level selection for increased dispersal rates (Hanski, 1999).
Within a meta-population, dispersal may be unidirectional, that is, from a
source to a sink (Pulliam, 1988), and analogies may be drawn with meta-
networks (Fig. 20). In meta-population theory, a population is regarded as a
source, if the intrinsic rate of increase (r) of the population is r > 0, and a sink
if r < 0 (Leibold et al., 2004; Pulliam, 1988). However, a local network
could be a source for some species but a sink for others (Pulliam, 1988).
Thus, when assigning the label source or sink to a local network, a better
approach might be to look at the overall intrinsic rate of increase for all the
species. As such, a local network could be regarded as a source, if it has a net
increase in species (R > 0, where R equals the number of species with r > 0
minus the number of species with r < 0), and a sink, if it has a net loss of
species (R < 0), while neglecting immigration. The immigration of species is
necessary to maintain both the species composition and interaction
structure. Thus, for the network to persist, the rescue (Brown and Kodric-
Brown, 1977) of individual species is essential. If some species go extinct,
effects may cascade out to other parts of the local network, reducing the r of
other species (either directly or indirectly), and triggering further cascading
extinctions (e.g. Palmer et al., 2008).
7.2. Meta-networks and extinction

From a meta-network perspective, extinction and colonisation can be en-
visaged on several organisational levels, for example, the interaction-,
species-, local network-, meta-network-, local patch- and regional level.
In an extreme case, an entire local patch might disappear, and with it the
complete local network with its species and interactions.
As a local patch shrinks, some species and links will go extinct (Pauw,
2007; Rodrı́guez-Cabal et al., 2007), the consequences of which will
depend on the network and ecosystem type. For instance, in antagonistic
networks, mesopredator release (Crooks and Soulé, 1999) may trigger
secondary extinctions. In contrast, in a mutualistic system, the loss of
interactions could have negative effects on the immediate interaction
partners, if there is limited functional redundancy among
species (cf. Zamora, 2000). Since many species are taking part in both
mutualistic and antagonistic interactions simultaneously (Fontaine et al.,
2011), foreseeing the outcome of species loss on local networks is a
challenging task.
Although reduction of habitat area does not always result in complete
extinctions, it often reduces species abundances (Fahrig, 2003), with detri-
mental consequences for mutualistic partners (or consumers in food webs).
A reduced abundance would, all else being equal, result in a reduced
interaction frequency. Within pollination networks, this can lower plant
fecundity (Pauw, 2007); in food webs, it can reduce predation pressure.
Additionally, interactions might disappear if interaction partners are not lost
but reduced to encounter probabilities approaching zero. Depending on
whether the involved species have alternative partners, interaction extinc-
tion may lead to local species loss. If all local patches decrease sufficiently
in area, the meta-network eventually fragments.
7.3. Meta-networks and colonisation

Both the abundance of the individual populations and the local species rich-
ness influence colonisation success. The more abundant and diverse the spe-
cies are in the local habitat, the more difficult it is to colonise the local
network, due to community closure, for instance (Hanski, 1999;
MacArthur and Wilson, 1963). However, generality and competitiveness
of the existing species and the area, isolation and quality of the local
patch are also important factors (MacArthur and Wilson, 1963). Thus,
the traits of both residents and colonists and fragment characteristics
determine colonisation. For example, generalisation among the resident
species may make it more difficult for colonists to find a vacant resource
that is not already exploited. On the other hand, there may be many
potential interaction partners, as predicted by the theory of preferential
attachment (Barabási et al., 1999; Jordano et al., 2003; Olesen et al.,
2008). Thus, the effects of generalisation depend to a large extent on which

community (mode) is exhibiting this trait (e.g. plant or pollinator trophic
level in a bimodal network) and which is colonising.
It becomes more difficult to invade local networks that are characterised
by a large number of generalist species, which might partly explain slow
recovery of freshwater food webs from acidification (Layer et al., 2010,
2011). Networks consisting of many pairwise mutualistic interactions, for
example, having tightly coevolved traits, might be more resistant to
colonisation because species might be better able to compete for their
resources.
The seminal work on island biogeography theory (MacArthur and Wil-
son, 1963) and later elaborated by other authors (e.g. Brown and Kodric-
Brown, 1977; Whittaker et al., 2008) is especially relevant in this context:
patches that are close to a source of dispersing species will, all else being
equal, receive more colonisers and be less prone to extinction as they are
more likely to be rescued (Brown and Kodric-Brown, 1977). As such, pat-
ches close to a source should therefore be better able to retain network struc-
ture than distant patches (of equal size).
As an additional consideration, bipartite ecological networks consisting
of plant–pollinators or plant–seed dispersers contain both mutualistic and
competitive interactions. On the one hand, plants and animals are involved
in mutualistic interactions that might range from facultative to obligate,
while pollinators interact competitively for resources (Goulson, 2003), as
do some plants for pollinators (Morales and Traveset, 2009; Vamosi et al.,
2006). Other plants do not compete (Hegland and Totland, 2008;
Ollerton et al., 2003) or may even facilitate the pollinators of other
species (Sargent et al., 2011). In cases of competition, the immigration,
colonisation and extinction processes are governed by both antagonistic
and mutualistic events depending on whether the interaction is related to
similar nodes in the network. As a consequence, the simultaneous
integration of both antagonistic and mutualistic network models
(Klausmeier, 2001; Nee et al., 1997) might be needed. This will
dramatically complicate any modelling process, especially when dealing
with ecological networks of natural sizes (in a database of 54 community-
wide pollination networks, species richness ranges from 16 to 952 species
with a median of 105; Trjelsgaard and Olesen, in press and similar-sized
food webs are listed in Ings et al., 2009). Like extinction probability,
colonisation ability will depend on species traits, including body size,
mobility and generality. Generalists are often considered relatively good

colonisers (Hanski, 1999), as are larger animals (Hoekstra and Fagan,
1998; Lomolino, 1985; Sutherland et al., 2000).
8. EFFECTS OF HABITAT FRAGMENTATION ON THE

COEVOLUTIONARY DYNAMICS OF NETWORKS
So far we have focused upon the ecological consequences of habitat
fragmentation, while only briefly touching on evolutionary processes. For
example, we implicitly assume that a species is more likely to die out due
to the loss of its mutualistic partners or prey instead of natural selection
leading to rapid evolution of new interactions (e.g. Rezende et al., 2007).
However, there is increasing evidence that human-driven evolutionary
change can occur on very short (‘ecological’) time scales (Darimont et al.,
2009), which has implications for ecological networks. A first step in this
direction might be to use the geographic mosaic theory of coevolution
(GMTC) (Thompson, 2005) to describe how selection will vary across frag-
mented landscapes and how that might influence species interactions and
ecological networks.
8.1. The geographic mosaic theory of coevolution

The GMTC assumes that the evolutionary dynamics of species interactions
are affected by the spatial configuration of potentially interacting populations
(Thompson, 2005). GMTC models assume that (i) species interact in
discrete habitat patches, (ii) selective pressures associated with interactions
vary across space (hereafter geographic selective mosaics) and (iii) gene flow
mixes traits among populations (Gomulkiewicz et al., 2000; Nuismer and
Doebeli, 2004; Nuismer and Thompson, 2006; Nuismer et al., 1999, 2000).
Geographical mismatches among potentially interacting species, geo-
graphically selective mosaics and gene flow will lead to unique evolutionary
dynamics that cannot be predicted by single-site models. Space is a key
component of this theory, affecting evolutionary dynamics in three ways.
First, geographical variation in genotype distributions among populations
will alter fitness. Second, space generates geographic selective mosaics
where there is spatial variation in the function that connects the fitness of
genotype in one species with that of its interacting partner. The geographic
selective mosaics occur if the fitness and, consequently, selective pressures
are determined by an interaction of two genotypes (G) and by the environ-

ment (E) (i.e. G G E). Third, the spatial configuration of sites will affect
gene flow across populations (Nuismer et al., 2000).
8.2. Habitat fragmentation and its effects on basic components

of GMTC
Habitat fragmentation could affect the GMTC for two-species interactions
through its basic components: the patches, species interactions, gene flow
and by changing the environment in which the interactions occur. The
resulting poorly connected patches will be smaller than natural patches.
The within-patch variation will increase due to contrasting selection and
stochastic genetic variation in the many fragmented subpopulations of a
given species. In this sense, the unique (biotic) history of each fragment
might lead to an equally unique combination of abiotic factors that might
affect the selective pressures on the interaction.
If the landscape is perceived by a given species as a composition of isolated
fragments, a break-up of interactions in some patches is expected. For in-
stance, the local extinction of some top predators in rainforest fragments
can lead to the loss of key predator–prey interactions that can affect the whole
ecosystem via trophic cascades (Terborgh et al., 2001). The same is true for
some large frugivores, whose extinction may lead to the loss of key interac-
tions with large-seeded plants (Guimarães et al., 2008). On the other hand,
new interactions could also be created by invasive species that might be able
to persist in the fragments but not in the original connected environment, as
open-habitat species may eventually use secondary forest fragments or species
that were present before fragmentation ‘rewire’ their interactions due to some
interacting partner loss. At present, the consequences of losing (or gaining)
such key species on the selective pressures associated to interactions remain
virtually unknown from a fragmentation perspective.
Habitat fragmentation could also alter the relevance of certain interac-
tions, via changes in abundances of interacting species. Species abundance
shapes ecological networks and common species are often also highly con-
nected (e.g. Krishna et al., 2008). Changes in abundance due to fragmenta-
tion may, in turn, affect the selective pressures associated with particular
interactions. An additional related factor is the reduction of gene flow across
patches, which might ultimately have major consequences on species evo-
lution and coevolution (Nuismer et al., 1999). Mathematical models of
GMTC suggest that gene flow can have unexpected evolutionary conse-
quences for local adaptation in pairwise interactions (Nuismer et al., 1999).
8.3. Habitat fragmentation and selection mosaics in ecological

networks
Examining the GMTC in a fragmentation setting is especially challenging in
species-rich networks, because the dynamical consequences of network
structure are not simply the sum of the dynamics of pairwise interactions.
For instance, if a network has N species in a continuous habitat, there are
2N possible combinations of species for any given habitat fragment. Again,
simplification is the route to address this challenge and we need to learn first
more about which are the most relevant components of ecological networks
to understand how they affect the speed and direction of evolutionary change.
Recent studies are starting to explore the role of species ecological net-
works in shaping evolutionary dynamics. For instance, ecological networks
of interacting species might favour the maintenance of high levels of trait
diversity (Fontaine et al., 2011). Explorations of the evolutionary dynamics
in species ecological networks by integrating field data, evolutionary models
and tools derived from statistical mechanics are still in their infancy. In mu-
tualistic networks, evolutionary dynamics appear to be shaped mainly by a
few super-generalist species that interact with multiple modules (Olesen
et al., 2007). Such species shape the evolution and coevolution in these net-
works in multiple ways (Guimarães et al., 2011). First, they increase the fre-
quency of evolutionary cascades through a small-world effect, by reducing
path length between species within the network. Second, they create asym-
metric dependencies among species, reducing the potential of reciprocal se-
lection. Third, they impose similar selective pressures over multiple
components of the network, promoting convergence in species traits
(Guimarães et al., 2011). The hypothesised effects of super-generalists pro-
vide the first steps in predicting the potential evolutionary consequences of
habitat fragmentation in ecological networks.
Changes in species composition will be particularly relevant if super-
generalists are affected. For instance, the probability of local extinction in-
creases with body size (Gaston and Blackburn, 1995), which is itself often
positively associated with generalisation in both antagonistic predator–prey
and mutualistic seed dispersal interactions. Thus, size-based extinctions are
more likely to lead to the extinction of super-generalists and this could con-
ceivably lead to an increase in the role of reciprocal selection. Furthermore,
it could reduce the frequency of evolutionary cascades, ultimately favouring
trait dissimilarity (i.e. mismatches) within interacting assemblages. In con-
trast, the introduction of generalist exotic species, such as honeybees, may
favour convergence among plants (Guimarães et al., 2011). Therefore,

habitat fragmentation may change the evolutionary dynamics within species
networks, especially if super-generalists die out or invade newly fragmented
habitats.
If the degree of habitat loss and fragmentation leads to a set of very small
and disconnected fragments, each should have tiny and semi-autonomous
networks with little dispersal among them (Fig. 20). These networks would
be unlikely to contain super-generalist species that rely upon a diversity of
partners to survive. Species that specialise on a few partners, such as large-
seeded plants that use large vertebrates for dispersal, will also be absent
(Da Silva and Tabarelli, 2000). Consequently, these tiny networks should
contain species with relatively homogeneous interaction patterns, with no
one species dominating evolutionary or coevolutionary processes in the net-
work. Moreover, divergence in population traits due to local adaptation may
occur if these small networks are also isolated. Finally, the role of species
across networks is not fixed, although we still know little about this (but
see Marquitti, 2011). Changing the abiotic and biotic features in a given
patch, habitat fragmentation could alter both the ecology and evolution
of interacting species. For example, forest fragmentation might suppress
the population of a super-generalist species, transforming it to a peripheral
species in the network and consequently reducing its ecological relevance
and as well affecting evolutionary trajectories within the entire community.
Predicting evolutionary consequences of fragmentation on networks is
still limited by a relative lack of both data and a mature theoretical frame-
work. Theoretical studies using two-species models suggest that the coevo-
lutionary dynamics may be qualitatively changed because of gene flow
(Nuismer et al., 1999), and the potential for new evolutionary dynamics
is even higher in a species-rich and fragmented network. The challenge
ahead is to develop approaches to model these complex dynamics in ways
that allow hypotheses to be tested in the field.
9. APPLICATIONS IN CONSERVATION AND

AGRICULTURE
The effects of habitat loss and fragmentation on biodiversity are evi-
dent on a global scale, and researchers and managers must develop ways to
understand and mitigate them (Bazelet and Samways, 2011). For instance,
many European bird species have declined as agricultural intensification
has resulted in the increasing fragmentation and isolation of natural habitats
(Donald et al., 2001; Tscharntke et al., 2005), and yet the consequences of
losing these often key species from mutualistic or antagonistic networks are
still largely unknown. What is clear, however, is that the effects of habitat
fragmentation are not evenly distributed within or among networks (e.g.
Cagnolo et al., 2009).
The growing appreciation that the importance of network structure for
ecosystem stability and functioning recognises that it is linked intrinsically
to applied goals, such as biodiversity conservation (Kaiser-Bunbury et al.,
2010; Tylianakis et al., 2010) or agricultural production (e.g. MacFadyen
et al., 2011). Yet for network approaches to become fully integrated into eco-
system management, two objectives must be met. First, a conceptual chal-
lenge will be to demonstrate that complex network approaches add value
to current practices. Underpinning this is the need to identify which specific
attributes of networks require the greatest attention and which offer the best
yield-to-effort reward. Second, a variety of practical hurdles need to be over-
come, both in the quantification of network attributes using empirical data
that can be feasibly obtained and in the application of concepts to practice
(Tylianakis et al., 2010).
Gathering conceptual support for the adoption of network tools is the
easier of these two objectives. The importance of network structure for
properties such as system stability, and recognition that this can be altered
even when species richness is not (e.g. Tylianakis et al., 2007), suggests that
landscape degradation may be altering ecosystems in ways that cannot be
detected by simple species-centric measurements. Furthermore, species can-
not survive without their interacting partners, so there is an inherent need to
consider the resources and mutualists of any species we wish to conserve.
Additionally, the extinction sequence of species and interactions from a net-
work during the fragmentation process (e.g. Sabatino et al., 2010) could pro-
vide guidance on the order in which species should be (re)introduced during
restoration (Feld et al., 2011). A network perspective can also help predict
the indirect effects of species additions or deletions (Carvalheiro et al., 2008).
A major challenge now is to identify the most relevant aspects of network
architecture for agriculture and conservation within fragmented landscapes,
whilst taking into account the huge complexity of these networks.
One promising avenue in this context is to focus on some key components
(e.g. species, links, functional roles, modules), as identified via network anal-
ysis, that are needed for the system to function ‘normally’. For example, ev-
idence is growing that super-generalists are the backbone of many networks,
potentially governing their ecological and evolutionary dynamics (Guimarães
et al., 2011; Olesen et al., 2007), which could provide clues as to how best to
conserve or restore fragmented landscapes. There is also plenty of evidence
that top predators can have cascading effects in marine, terrestrial and
freshwater ecosystems worldwide (Estes et al., 2011), and many of these
are also highly generalised. The reintroduction of locally extinct generalists
may assist the restoration of previous ecosystem states whereas the removal
of non-native super-generalists may be the first step needed to restore
fragments and landscapes to their prior condition.
In addition to the presence or absence of apex consumers and super-
generalists, several other network metrics can be important from a conser-
vation perspective. Tylianakis et al. (2010) argued that conservation could
focus on network attributes that confer stability or maximise rates of ecosys-
tem functioning. Nestedness, compartmentalisation, degree distributions, in-
teraction diversity and the presence of weak links are all potentially useful
metrics, but some of these are sensitive to sampling effort. Thus, the best
approach to conservation of complex networks could involve the monitor-
ing and/or restoration of a suite of network metrics, at least if preserving sta-
bility and functioning are the primary objectives (Tylianakis et al., 2010).
These would likely include measures of connectedness (such as connectance
or link density), which would relate to functional redundancy and the prob-
ability of secondary extinctions following species loss. Furthermore,
compartmentalisation or modularity (particularly to avoid the spread of pol-
lutants or perturbations) and nestedness (to maintain robustness of function-
ing following local extinctions) are likely to be key network properties for
restoration and conservation.
Despite being important in theory, measuring network metrics accurately
and manipulating them empirically remains a hurdle to the implementation of
a more ‘link-focused’ management. Simulations of sampling can help reveal
which metrics may be least sensitive to sampling effort (Nielsen and
Bascompte, 2007; Tylianakis et al., 2010), and these may be the optimal
candidates for biomonitoring. A number of questions still need to be
addressed before network conservation can be put into practice. At the
most basic level, we need to know how the survival or conservation of a
species in a fragmented landscape is affected by its biotic context, that is,
the number and kinds of links connecting that species to others within the
network. Second, we need to identify the traits of species that determine
their role within the network, so that we can begin to predict and restore
network structure. For example, species traits such as body size and
morphology (e.g. Stang et al., 2007, 2009; Woodward et al., 2005) are
known to influence network structure, and techniques have recently been
developed to calculate the contribution of a species to network nestedness
and persistence (Saavedra et al., 2011). As ecologists further unravel these

traits, we can start to move towards developing a predictive framework for
network architecture given community-wide traits of species (Gilljam
et al., 2011; Petchey et al., 2008; Woodward et al., 2010b). Third, we
need to better understand the relationship between physical structure and
network architecture. Evidence that complex habitat structures can
impede the realisation of potential interactions (Laliberté and Tylianakis,
2010) requires consideration in the restoration of complex (e.g. forest)
habitats and provides a potential avenue for reducing the impact of
undesirable or strong destabilising interactions.
10. CONCLUSIONS
Our synthesis provides ample evidence that the consequences of hab-
itat fragmentation for biotic communities and ecological networks are
highly complex, but that does not mean they are unpredictable. At least five
components of this complexity become immediately apparent. First, there is
spatial complexity in the fragmentation process due to variation in landscape
structure in terms of fragment size and isolation, connectivity, matrix qual-
ity, edge permeability and geometry. Second, fragmentation can affect the
temporal dynamics of interacting taxa (e.g. flowering and fruiting phenol-
ogies), and long-term consequences on interacting species may become
apparent only after several decades. For instance, time lags will increase
the probability of co-extinctions, especially when generation times strongly
differ between interacting taxa. Third, responses by fragmentation- and
network-relevant traits differ among species. The perception of fragmenta-
tion (e.g. environmental grain) by individual species, key traits and com-
plexes (e.g. body size in food webs), and trait matching between
interacting species might be particularly relevant for assessing the conse-
quences of fragmentation. Fourth, there is complexity in the biological
and analytical details of networks, which differ in type (e.g. mutualistic
vs. antagonistic; bimodal vs. multi-modal). Effects of dispersal, colonisation
and extinction need to be integrated (e.g. in meta-networks). Fifth, there is
an evolutionary component to network responses to habitat fragmentation.
The geographic settings of habitat configuration and selective mosaics might
lead to rapid evolutionary changes, even at short ‘ecological’ time scales.
Finally, these five complexity components may interact, creating potential
synergies.
How can we usefully address and simplify this extreme complexity that
originates from different spatial and temporal scales and organisational levels?
First, we need to understand how individual links among interacting species
are affected by habitat fragmentation, both in a spatial and temporal setting.
These include phenologies and encounter rates and how they vary across
space, time and levels of fragmentation. Second, there is overwhelming ev-
idence that species are not equally important for ecosystem functioning and
that a few exert disproportionate effects. These include large species at high
trophic levels (e.g. top predators), abundant species and super-generalists.
Such species can provide the structural backbones of ecological networks,
shape evolutionary dynamics or initiate cascades of network changes. Thus,
one way to circumvent the apparent complexity is to focus initially on un-
derstanding how fragmentation affects these key species and their links.
Third, we need to gauge the extent of functional redundancy in ecological
networks and to what extent habitat fragmentation disproportionally affects
functionally unique species. This includes a better understanding of the role
of specialisation, functional grouping and trait matching in ecological net-
works. Finally, we need to understand in more detail how network prop-
erties (e.g. connectance, linkage level, nestedness, modularity) and the
roles of species in networks (e.g. hubs, connectors, spatial couplers) are
affected by habitat fragmentation. This will become particularly interesting
as we begin to link different types of networks, for example, when combin-
ing spatial with ecological networks or when moving from simple networks
to meta- and super-networks.
There is a clear need to consider ecological and evolutionary processes of
multispecies interactions in a network context to understand how habitat
fragmentation affects biodiversity. Such an approach will become increas-
ingly feasible as the availability of large databases, appropriate software
and comparative studies continue to increase apace. We envisage a hierar-
chical approach to understand how individuals, populations, pairwise inter-
actions, ecological networks and ultimately networks of networks are
affected by fragmentation. For network approaches to become integrated
into conservation, agriculture and ecosystem management, we need to find
ways to simplify the inherent complexity and to measure and monitor
management-relevant network properties. A link-based management
approach has great potential to aid biodiversity conservation and restoration
by highlighting the immense importance of biotic interactions and ecolog-
ical network stability for ecosystem functioning.
ACKNOWLEDGEMENTS
This paper was developed and written during and after two workshops sponsored by the
Danish Agency for Science, Technology and Innovation (FNU) under the international
network call (Application title: ‘Ecological Network Analysis in an Agricultural
Landscape’). In addition, we acknowledge support from the Danish Council for
Independent Research | Natural Sciences (M. H.; J. M. O.; and via a starting
independent researcher grant (11-106163) to W. D. K.), the Carlsberg Foundation
(C. R.), the Villum Kann Rasmussen Foundation (W. D. K., VKR09b-141 to J.- C.
Svenning), the Brazilian Council for Science CNPq (M. A. M. D. A., L. P. C. M.) and
the Swiss National Science Foundation (C. N. K. -B.). M. A. M. D. A., J. G., P. R. G.,
F. M. D. M., K. P. M., L. P. C. M. and M. M. V. were partially supported by Fundação
de Amparo a Pesquisa do Estado de São Paulo (FAPESP), J. M. T was funded by a
Rutherford Discovery Fellowship, and M. M. V. was partially supported by CAPES. G.
B. J. and E. J. O. were supported by UK Natural Environment Research Council grants
awarded to G. W. (Ref: NE/I528069/1; NE/I009280/1). We are most grateful to C.
Mulder for his many corrections and comments.
APPENDIX
Methods for Ashdown Forest case study of food webs in
fragmented river networks
A.1 Site description and food web construction
Ashdown Forest in Sussex, UK (National Grid Reference TQ 520300)
contains the spring-fed headwaters of two rivers, the Ouse—which flows
south into the English Channel—and the Medway, which flows north
and joins the Thames estuary. The catchments of both streams lie in the cen-
tre of the Weald in SE England, on hills of soft, fine sandstone (Ashdown
Sands). Further description of the site can be found in Townsend et al.
(1983). Sixteen streams were sampled in this study, and pH was recorded
in 1976 and 1994, and an average value was calculated for each stream. Five
randomly dispersed Surber samples (sample-unit area 0.0625 m2; mesh ap-
erture 330 mm) were collected from each of the 16 streams in October 1976,
1984 and 1994 (Gjerlv et al., 2003; Townsend et al., 1987) (total n sample-
units ¼ 240). The benthos was disturbed to a depth of approximately 5 cm
and all macroinvertebrates collected were preserved in the field and
subsequently sorted. Taxonomic identification was standardised to the
highest common level of resolution (usually to species) across all webs
(Woodward et al., 2002a). Several of the more difficult to identify taxa
were aggregated: for example, all members of the Tanypodinae sub-
family were presented as a single node. Feeding links were taken from
direct observed interactions (gut contents analysis) in Broadstone Stream

(Woodward et al., 2010b) and elsewhere within these two river networks
(e.g. Layer et al., 2010, 2011), and this dataset was augmented with
feeding links inferred from known interactions described in the literature
from different systems (Brose et al., 2006; Gilljam et al., 2011; Lancaster
et al., 2005; Warren, 1996; Woodward et al., 2008, 2010b). Additional
feeding link data were supplied by F. Edwards (unpublished data).
GLOSSARY
Note that some of the terms in this glossary have alternate meanings, and some
also have general and specific definitions (e.g. complexity) in different disciplines
(e.g. in food webs vs. mutualistic networks; in landscape ecology vs. ecological
network ecology), which can lead to potential misunderstandings when under-
taking interdisciplinary research. We have highlighted these with ‘*’, below.
Antagonistic network (p. 96) A network with associations between organisms in which
one benefits at the expense of the other, for example, food webs, host–parasitoid net-
works and competitive networks.
*Asymmetry (p. 199) In a network context, a property of nested assemblages (e.g. mu-
tualistic networks). Specialist plants interact just with generalist animals, while generalist
animals use a broad range of host plants, including both specialists and generalists. It also
refers to inequality of strong and weak interactions between species or nodes, competi-
tion or energy flow within a network.
Bimodal networks (p. 97) Pollination and seed dispersal networks are by definition bi-
modal (bipartite or two-mode), linking two sets of taxa (e.g. flower-visitors and plants, or
frugivores and plants). They are often best represented by two-level bipartite graphs.
Host–parasitoid networks or food webs that consider just two trophic levels also fall un-
der this definition.
Boundary (p. 117) A border (or edge) between contrasting habitat patches that delimits
the spatial heterogeneity of a landscape.
Centrality (p. 102) A measure of the importance of a node as a focal point within a net-
work. There are various types of centrality measures for any node within a network, such
as degree (the number of nodes that a focal node is connected to), closeness (the inverse
sum of shortest distances to all other nodes from a focal node) and betweenness (the de-
gree to which a node lies on the shortest path between two other nodes).
Coevolutionary dynamics (p. 91) Coevolution is the process of reciprocal evolutionary
change between interacting species, driven by natural selection. This may lead to coevo-
lutionary dynamics, whereby changes in gene frequency in one species trigger reciprocal
changes in the other interacting species.
Compartment (p. 97) An assemblage of species within a network. Specific definitions
vary depending on the point of view of the constituent organisms. Density view: an as-
semblage of species that are highly connected to each other. Predator view: an assemblage
of species that share a large number of prey. Prey view: an assemblage of species that share
a large number of predators. See also module below.
Compartmentalisation (p. 98) The development of groups of species or ‘topological

compartments’ that have a higher probability of interacting with one another than with
other species in the network. See also modularity below.
*Complexity (p. 92) Property or set of properties that characterise systems composed of
many interacting parts or elements. In organised complexity, the non-random or
correlated interaction among the parts generates emergent properties, that is, proper-
ties not carried or dictated by individual parts. In ecology, complexity can be used as
a general term (to describe a large number of interacting nodes) or with a more specific
definition, for example, the average number of trophic links per species within a whole
food web.
Connectance (p. 91) The proportion of all possible interactions within a system that are
realised. This is typically measured as directed connectance, the proportion of docu-
mented directed links out of the maximum number of possible directed links in the food
web, that is, the number of links (L) divided by the number of species (S) squared, L/S2.
Connectors (p. 143) Species that link different modules within a network together. For
example, large-bodied species, which disperse widely and thus link subwebs together
(e.g. avian predators in a fragmented landscape).
Corridor (p. 92) Long, thin strips of habitat that connect otherwise isolated habitat pat-
ches. They reduce local extinction risk by connecting isolated populations and by pro-
moting gene flow.
Degree distribution/linkage level distribution (p. 97, 174) The probability distribu-
tion of the number of links per node, typically measured over an entire network.
Domatium(-a) (p. 98) Specialised chamber(s) in different plant parts, providing refuge
for predatory arthropods.
Ecological network (p. 91) A representation of biotic interactions in a multispecies com-
munity, in which pairs of species or other forms of taxonomic or functional aggregates
(nodes) are connected when they are interacting (links), both directly and indirectly (e.g.
sharing the same resource but not directly linked). There are three broad categories—
food webs, host–parasitoid and mutualistic networks.
*Edge (p. 90) In a landscape context, the (artificial) boundaries of habitat fragments. Also
used as a synonym for link in network analysis, highlighting the need for clarity when
using this term in interdisciplinary studies.
Edge permeability (p. 103) The extent to which a species can move through a physical
border, for example, from a fragment to the surrounding matrix. A ‘hard’ edge contains
an impenetrable boundary which dispersing individuals virtually never cross, for exam-
ple, a physical barrier such as an ocean surrounding an island. A ‘soft’ edge is more per-
meable to emigrating individuals than a hard edge, for example, the boundary between a
meadow and a garden.
Environmental grain (p. 91) The scale of environmental variation (temporal or spatial),
relative to the temporal/spatial scales of activity of the organisms, that is, a description of
the organism’s ‘perception’ of its own environment.
Fragments (p. 92) Habitat that was once continuous but has become divided into discrete
patches. Fragments are separated by and embedded within areas (matrix) with abiotic and
biotic properties different from the previously continuous habitat (see habitat fragmentation
below).
Functional group (p. 94) A group of species or taxa with a similar response to a given
factor. This may also include trophic species, groups of taxa that share the same set of
predators and prey.
Functional redundancy (p. 91) The idea that some species perform similar roles in com-
munities and ecosystems and may therefore be substitutable with little impact on system
properties.
Generalist (p. 98) A species that is able to thrive in a wide variety of environmental con-
ditions and/or can make use of a variety of different resources.
Habitat fragmentation (p. 90) A process during which a large expanse of habitat is trans-
formed into a number of smaller patches of smaller total area, isolated from each other by
a matrix of habitats unlike the original. The effects of this process may include some, but
not all of the following: (1) reduction in habitat amount, (2) increase in number of habitat
patches, (3) decrease in size of habitat patches and (4) increase in isolation of patches.
Higher trophic rank hypothesis (p. 159) Species found at higher trophic levels tend to
have a stronger relationship with area than species found at lower trophic levels as they
have larger space and resource requirements. As such, species found at high trophic levels
should have a higher susceptibility towards habitat fragmentation.
Host–parasitoid networks (p. 92) A specific form of antagonistic ecological network in
which parasitoids benefit and subsist off their hosts. They may also contain information
about hyperparasitoids (parasitoids that attack other parasitoids). These networks often
involve a high degree of specialisation.
Hub (p. 91) Highly linked species within their own module of a network.
Interaction intimacy (p. 132) Degree of biological association between individuals of
interacting species, for example, host–parasite during all of their life or only part of their
lifespan.
*Interaction strength (p. 134) The magnitude of the effect of one species on another me-
diated by their pairwise interaction. This can be measured in a variety of ways, including
experimental and theoretical approaches, or using allometric body-size scaling relationships.
Invasive species (p. 117) Species that arrive, become established and subsequently dis-
perse in a community where they did not previously exist in historical time.
Link (p. 91) The pairwise interaction between two nodes in a network.
Linkage level (p. 97) Number of links per species.
*Matrix (p. 91) A landscape that has undergone fragmentation, often leading to a heter-
ogenous habitat. Also quantifies the pairwise interactions between multiple species in a
network, for example, qualitative (presence/absence of an interaction) or quantitative
(coefficients reflecting interaction strengths, such as the Community or Jacobian matrix).
The different meanings of this term in different fields of ecology highlight the importance
of clarity in interdisciplinary studies.
Matrix permeability (p. 118) The property of a habitat matrix that describes the extent to
which species can move through it, that is, between fragmented habitat patches.
Meta-populations/meta-communities (p. 101, 164) Potentially unstable local
populations inhabiting discrete habitat patches, which persist at a larger scale via dispersal.
Module/modularity (p. 91) Ecological networks consist of link-dense and link-sparse
areas. Link-dense regions are termed compartments or modules. Species within a module
are linked more tightly together than they are to species in other modules. The extent to
which species interactions are organised into modules is termed the modularity of the
network. Modularity may reflect habitat heterogeneity, divergent selection regimes
and phylogenetic clustering of closely related species.
Mutualistic networks (p. 96) Networks where both groups benefit from each other. Ex-
amples include plant–animal interactions (typically pollinators, frugivores, ants),
plant–mycorrhizal systems, coral–zooxanthellae associations and many other networks

involving microbial endosymbionts. These networks do not exist on multiple trophic
levels, unlike antagonistic networks.
*Nestedness (p. 91) A distinctive pattern of mutualistic community assembly showing
two characteristics, namely, asymmetrical specialisation (specialists interacting with gen-
eralists) and a generalist core (generalists interacting with generalists). Nestedness occurs
when specialist species interact with a proper subset of species with which more gener-
alised species interact. Nestedness can also describe niche overlap in antagonistic net-
works: for instance, where predator diets are arranged hierarchically on the basis of
body size in food webs.
Nodes (p. 94) In an ecological network, nodes mostly refer to species or trophic groups of
species. In a broader context, however, nodes can also refer to individuals, populations,
functional groups (e.g. body-size or feeding groups), guilds, communities or even entire
networks.
Sink (p. 135) A habitat in which mortality exceeds production and is reliant on immigra-
tion to maintain population levels.
Spatial network (p. 94) A network, or weighted spatial graph, where the nodes have a
location and the links have lengths and also a magnitude or weight.
Specialist (p. 98) A species that can only thrive in a narrow range of environmental con-
ditions and/or has a limited diet.
Super-generalist (p. 91) Species with a very high level of generalisation compared to co-
existing species. In a network context, they will have a much higher linkage level and
centrality than the other species. They are often super-abundant, density-compensating
island species.
Super-network (p. 176) Expanding the network study from looking at single bipartite
networks to multiple bipartite networks (e.g. plant–pollinator, plant–herbivore and
plant–pathogen networks).
Topological role (peripherals, connectors, module and network hubs)
(p. 101) Functional role of a node in the network in relation to the modular structure.
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Climate Change Impacts on
Community Resilience: Evidence
from a Drought Disturbance
Experiment
Mark E. Ledger*,1, Rebecca M.L. Harris*, Patrick D. Armitage{,
Alexander M. Milner*,{
*School of Geography, Earth and Environmental Sciences, University of Birmingham, Edgbaston,
Birmingham, United Kingdom
{
Freshwater Biological Association River Laboratory, East Stoke, Wareham, Dorset, United Kingdom
{
Institute of Arctic Biology, University of Alaska, Fairbanks, Alaska, USA
1
Corresponding author: e-mail address: m.e.ledger@bham.ac.uk
Contents
1. Introduction 212
1.1 Disturbance, community structure and climate change 212
1.2 Disturbance and diversity 213
1.3 Climate change and drought disturbance in streams 214
1.4 Mesocosm experiments 215
2. Methods 217
2.1 Mesocosms 217
2.2 Experimental design and application 219
2.3 Sampling and processing 220
2.4 Statistical analysis 220
3. Results 223
3.1 Disturbance effects on community descriptors 223
3.2 Disturbance effects on community structure 225
3.3 Disturbance effects on temporal dynamics 230
4. Discussion 231
4.1 Disturbance and diversity 233
4.2 Resilience and disturbance frequency 233
4.3 Resilience and ecosystem functioning 235
4.4 Disturbance and community development 237
4.5 Drought as an environmental filter 238
5. Conclusions 239
Acknowledgments 240
Appendix A 241
Appendix B 249
References 253

http://dx.doi.org/10.1016/B978-0-12-396992-7.00003-4
212 Mark E. Ledger et al.
Abstract
Climate change is expected to alter disturbance regimes with profound effects on the
structure and dynamics of ecological communities. In many regions, climate models fore-
cast shifts in precipitation patterns that will exacerbate droughts in rivers and streams, yet
ecological impacts on freshwater ecosystems remain poorly understood. We report the
results of a stream mesocosm experiment designed to test the effect of drought on the
resilience of replicate macroinvertebrate communities, via direct manipulation of flows.
Drying disturbances applied at high (monthly) and low (quarterly) frequency over
21-months had contrasting effects on the structure and temporal dynamics of the com-
munities. Macroinvertebrates were resilient to low-frequency disturbance, sustaining
abundant and diverse communities, which developed over experimental time. By com-
parison, high-frequency disturbance exceeded the capacity for recovery, skewing com-
munity structure, and generated relatively impoverished, static assemblages dominated
by fewer species. Species responses ranged from extirpation to irruption, with smaller
short-lived taxa ( 1 generation per year), notably chironomids and worms, replacing
larger taxa with longer life cycles ( 1 generation per year). This research provides one
of the first experimental tests of resilience to drought in aquatic ecosystems.
1. INTRODUCTION
1.1. Disturbance, community structure and
climate change
Climate change is one of the most critical disturbances imposed on natural
systems on a global scale. Its effects at the higher (multispecies) levels of
organisation are still poorly understood, although this area has recently
seen dramatic increases in research activity (e.g. Dossena et al., 2012;
Mintenback et al., 2012; Perkins et al., 2010). It is in itself a compound
stressor, associated with changes in temperature and atmospheric
conditions, and it can also interact with the effects of other local or
regional perturbations, including eutrophication, acidification and habitat
fragmentation (Hagen et al., 2012; Layer et al., 2010, 2011; Meerhoff
et al., 2012; Olesen et al., 2010).
Disturbance is integral to the organisation of the globe’s freshwater, ma-
rine and terrestrial ecosystems (Sousa, 1979) and can be defined as ‘any
discrete event in time that disrupts the structure of an ecosystem, commu-
nity, or population, and changes resource availability or the physical envi-
ronment’ (Pickett and White, 1985). The spatial and temporal occurrence of
such events define a system’s disturbance regime, in terms of frequency,
intensity, timing, duration, extent and severity (Pickett and White, 1985).
Resilience and Disturbance Frequency 213
In many regions, natural disturbance regimes have been modified by human

activities (Turner, 2010). In the near future, disturbances as diverse as fire,
floods, drought, hurricanes and landslides are expected to increase in
frequency in many parts of the world due to human intervention (Turner,
2010). Since many disturbances are also associated with strong climate forcing,
future intensification of weather extremes could have profound impacts on
habitats, communities and ecosystems.
Extreme events can be characterised by their strength, timing and
abruptness relative to the life cycles of affected organisms (Jentsch et al.,
2007). In Europe, for example, climate models predict increased incidence
of extreme events in future, including heat waves, heavy precipitation,
drought, wind storms and storm surges (Beniston et al., 2007) that are likely
to cause disturbances and trigger profound changes in local ecosystems that
are disproportionate to their short duration. It is often challenging to assess
the impact of extreme events on ecosystems because of their rarity and
unpredictability, so controlled experiments have been advocated as a more
logistically feasible alternative, which can also provide insight into underly-
ing mechanisms ( Jentsch et al., 2007).
1.2. Disturbance and diversity

Several theoretical models predict how increasing disturbance might reshape
diversity in natural communities (e.g. Connell, 1978; Huston, 1979; Petraitis
et al., 1989), yet despite decades of research, no clear patterns have emerged
among empirical studies (Miller et al., 2011). Disturbance effects on species
diversity are often expressed graphically as diversity–disturbance
relationships, which plot a descriptor of species diversity (e.g. richness)
against a descriptor of disturbance (e.g. frequency). The influential
intermediate disturbance hypothesis (Connell, 1978) predicted a unimodal
relationship between diversity and disturbance, whereby low disturbance
leads to competitive exclusion and high disturbance filters out all but the
most opportunistic disturbance-adapted species. Evidence in support of the
intermediate disturbance hypothesis (IDH) came from communities
characterised by high rates of competitive exclusion (e.g. Lubchenco, 1978;
Sousa, 1979), but several recent studies revealed that unimodal
diversity–disturbance relationships are far from ubiquitous (Mackey and
Currie, 2001), and there are many examples of positive (e.g. Armesto and
Pickett, 1985; Fox, 1985) and negative (e.g. Death and Winterbourn,
1995; Wilson and Tilman, 1991) relationships across different ecosystem
types. Despite widespread and extensive research on disturbance dynamics,

ecologists still lack a clear predictive understanding as to how changing
disturbance regimes will affect multispecies systems (e.g. Death, 2002;
Miller et al., 2011).
1.3. Climate change and drought disturbance in streams

Disturbance is expected to play an important role in governing ecosystem
responses to future changes in climate (Easterling et al., 2003), and antici-
pated increases in the frequency and intensity of disturbance events
(IPCC, 2007) may alter biodiversity and ecosystem functioning in the future
(Daufresne et al., 2007; Ledger et al., 2008). For example, climate change is
expected to alter precipitation patterns at global, regional and local scales
(Beniston et al., 2007; IPCC, 2007), with consequences for the temporal
and spatial distribution of water across and within ecosystems (Acuña and
Tockner, 2010; Vörösmarty et al., 2010). Water scarcity is one of this
century’s most pressing environmental issues (Schindler and Donahue,
2006) and climate-induced shifts in the availability of water are likely to
increase the incidence of drought which can be further exacerbated at
supraseasonal scales by overabstraction of water for human use, as an
additional indirect consequence of climate change (Chessman, 2009; Poff
and Zimmerman, 2010).
Droughts, defined here as low-flow periods unusual in their frequency,
duration, extent, severity or intensity, occur naturally in many rivers and
streams during times of low rainfall (Boulton, 2003). In Mediterranean
regions regular stream drying occurs as a natural part of the hydrologic cycle
and stream biota possess traits adapted to tolerate or escape dry conditions
(Bonada et al., 2007). By contrast, drought events occurring unpredictably
may have devastating effects in river communities containing few drought-
adapted species (Lake, 2003). Across Europe, drought has already increased
dramatically in frequency over the past 30 years (IPCC, 2007). Despite
this growing prevalence, research on the ecological impacts of drought in
rivers and streams lags behind that of other forms of disturbance, especially
floods (James et al., 2008; Sponseller et al., 2010). Flow is widely regarded as
a master variable that shapes the ecological characteristics of rivers and
streams (Poff and Zimmerman, 2010), and extreme events like drought
are known to exert strong selective pressure on populations, influencing
their relative success, and both the lethal and sub-lethal effects on stream
biota have the potential to profoundly alter biodiversity, food web structure
and ecosystem functioning (Daufresne and Boët, 2007; Ledger et al., 2011;
Woodward et al., 2012). Under climate change, uncharacteristically frequent

or intense (Beche et al., 2009; Gurvich et al., 2002) droughts may drive
species beyond their ‘hydrological envelope’—just as global warming
can drive species populations beyond their ‘thermal envelope’ (Ledger
et al., 2008; Woodward et al., 2010). These novel disturbance regimes
challenge the capacity of river systems to recover and could elicit
unforeseen dynamics that erode the supply of ecological goods and
services, including the maintenance of viable fisheries or waste-processing
capabilities. Drought impacts are also likely to be contingent upon the
many facets of the hydrologic regime itself, and the imperative now is to
develop approaches to explore how the frequency, intensity and duration
of low-flow periods influence aquatic systems (Ledger et al., 2011; Poff
and Zimmerman, 2010).
Freshwater organisms possess traits that confer a degree of resistance
(ability to withstand disturbances; Pimm, 1984) and resilience (tendency
to return to a reference state after disturbance; Chapin et al., 2002)
that together govern their ecological stability and associated bio-
diversity–ecosystem functioning relationships (Ptacnik et al., 2010). Here,
we define ecological stability simply as the propensity for a system to
maintain its species composition in the face of disturbance (Woodward
et al., 2002). Several reviews indicate that where droughts occur
unpredictably, biotic resistance is typically low whereas resilience is more var-
ied, and may be related to life-history traits such as body size and voltinism, or
rarity (Lake, 2003; Ledger et al., 2011). The rate of community recovery
following drought episodes may be relatively rapid (days-months) but local
species loss, strongly skewed abundance patterns, and other biological
legacies may markedly delay it or divert its trajectory (Lake, 2003; Ledger
et al., 2006). Drought disturbances may also skew community dynamics,
either by accelerating species turnover or by decelerating or arresting
successional processes in stream benthic habitats (Ledger et al., 2008) and
recovery may be difficult to establish, especially given the inherently
dynamic and patchy nature of many freshwater communities in both space
and time (Hagen et al., 2012; Olesen et al., 2010).
1.4. Mesocosm experiments

Droughts occurring unpredictably in natural systems can be a challenge to
study and research to establish the ecological effects of these events is inevi-
tably opportunistic and often beset by confounding gradients and/or lacking
adequate controls or pre-impact data (James et al., 2008; Lake, 2003).
Controlled manipulative experiments are required to overcome these

confounding influences and to identify the mechanistic basis of cause-and-
effect relationships that cannot be resolved via field survey approaches (e.g.
Jentsch et al., 2007; Ledger and Winterbourn, 2000; Ledger et al., 2002,
2011; Woodward et al., 2012). However, laboratory-based flume or
microcosm studies inevitably sacrifice realism for control and replication,
undermining the validity of extrapolating to relevant spatiotemporal scales
and levels of biological complexity needed to understand system-level
responses (Harris et al., 2007; Ledger et al., 2009). In this study, we adopt
a novel experimental approach using mesocosms that circumvent the
shortcomings of correlational studies (see Dewson et al., 2007; Ledger
et al., 2008) while maintaining greater realism than would be possible in
smaller scale (e.g. laboratory flumes or microcosms) manipulations. The
main objectives of this study were (1) to examine how drying disturbances
induced by supraseasonal drought affects stream macroinvertebrate
communities and (2) to characterise how the resilience of biota is
challenged by disturbances of different frequencies. A series of stream
mesocosms fed by a chalk stream were used to simulate drought
disturbance episodes, via a direct manipulation of flows (see Ledger et al.,
2008, 2011). Mesocosm-scale research provides the means to make direct
comparisons among replicated communities under different,
experimentally applied, flow regimes, and when conducted for at least one
generation of the longest-lived organism, perturbation experiments can
yield insights into the intergenerational responses within and across food
webs (Woodward et al., 2012; Yodzis, 1988). Previous research has
shown that the mesocosms used in this study are both replicable and
realistic for water quality and biodiversity (algae and macroinvertebrates)
(Harris et al., 2007; Ledger et al., 2009) and contain complex food webs
with structural properties (e.g. connectance, path lengths, degree
distributions) which shape ecological responses to stress that are
consistent with those of natural systems (Brown et al., 2011; Ledger
et al., 2011; Woodward et al., 2012).
The mesocosm experiment was used to test three hypotheses: first, that
drying disturbance would restructure benthic macroinvertebrate communi-
ties, with the extent of the effect contingent upon the frequency of occur-
rence of disturbance events. We expected that small species with fast life
histories would replace larger taxa with longer life cycles, consistent with
theory (Brown et al., 2004; Pianka, 1983). Second, we proposed that
species richness would peak at intermediate levels of disturbance
(Connell, 1978) and third, we proposed that disturbance would arrest the
process of macroinvertebrate community development over time, with
the extent of the constraining effect greatest in patches disturbed at high
frequency (HF).
2. METHODS
2.1. Mesocosms
Research was conducted between February 2000 and February 2002 using a
series of stream mesocosms at the Freshwater Biological Association River
Laboratory, East Stoke, Dorset, UK (50 400 4800 N, 2 110 0600 W). The meso-
cosms were arranged in four spatial blocks next to a chalk stream (Fig. 1).
Each block of mesocosms contained three stainless-steel linear channels (each
width 0.33 m, length 12 m, depth 0.30 m) fed unfiltered water by gravity
from the stream (containing invertebrates, algae and detritus) through a
branching 110 mm diameter pipe (Harris et al., 2007). The upper end of each
mesocosm channel was closed and fitted with a flow control valve whereas the
lower end was open, allowing free drainage of water and suspended particles
into an outlet stream. Each mesocosm was positioned 5 cm below the inlet
and 10 cm above the outlet to avoid transfer of biota among the channels.
Mesocosms were filled to 20 cm depth with clean substrate dominated by
chert gravel (volumetric proportions of particle sizes, 85% 11–25 mm, 5%
2–11 mm, 5% 0.35–2 mm, 5% < 0.35 mm), matching the source stream
(Harris et al., 2007). Consistent with many chalk streams, mesocosms did
not have extensive hyporheic zones (Trimmer et al., 2010), but substrata
provided refugia for suitably adapted species during drying disturbances
(Harris, 2006). Physicochemical conditions were highly congruent among
mesocosms (Harris et al., 2007) and closely paralleled those of the source
stream (Ledger et al., 2009). During the main study period, water temperature
(mean 12.2 C) varied seasonally, with summer maxima (18.7 C in June
2000) and winter minima (6.0 C in December 2001). Inflowing water
was nutrient rich (mean PO4: 0.16 mg L 1; NO3: 5.62 mg L 1 from March
2000–February 2002) with high pH (mean 8.1) and conductivity (mean
460 mS cm 1) (Harris et al., 2007). Outside the experimentally simulated
dewatering periods, discharge in the mesocosms was stable (cross treatment
mean 0.005 m3 s 1), with mean water velocity (at two-thirds depth) and
depth over the gravel of 0.20 m s 1 and 81 mm, respectively, and water
residence times were short (mean 66 s) (Harris, 2006).
Parent stream channel
Feeder pipes
Block 1 Block 2 Block 3 Block 4
Figure 1 Schematic diagram (A) and photograph (B) of the stream mesocosm facility at
the Freshwater Biological Association River Laboratory, Dorset, UK. Four blocks of three
stream mesocosms (each channel 12 m length 0.3 m width) were fed water through
pipes (6 m length) from the parent stream. Water flow (direction indicated by arrows) in
to each mesocosm was controlled by a valve. Each block contained one undisturbed
control, one low-frequency (LF) and one high-frequency (HF) disturbed channel.
2.2. Experimental design and application

Unfiltered water from the source stream was diverted into the mesocosms to
initiate colonisation and community development (February-March 2000).
Macroinvertebrate colonisation was either passive, in drift from the source
stream, or by adult oviposition (Ledger et al., 2009). Two months immedi-
ately after the the initial colonization period an experiment was established
consisting of two drought disturbance treatments—low-frequency (LF)
and high-frequency (HF) flow cessation—and an undisturbed control
(Table 1). Disturbance regimes were short periods (6-day) of flow cessation
applied at either approximately quarterly (LF treatment, 99-day dry/wet
cycles, 7 disturbance events) or monthly intervals (HF treatment, 33-day
dry/wet cycles, 20 disturbance events). By contrast, flows in controls
remained uninterrupted for the duration of the experiment (693 days,
Table 1). The dewatering treatments mimicked severe drought conditions
in which low fluctuating water levels repeatedly disturb patches of the river
bed over a prolonged period, as might be expected in supraseasonal drought
scenarios (see Ledger et al., 2008, 2011). These events are expected to
become more frequent in the UK under Intergovernmental Panel on
Climate Change (IPCC) scenarios (Vidal and Wade, 2009). Disturbances
were applied by slowly closing inflow ducts and allowing water to drain
from the channels over the course of several days. During dewatering,
surface flows ceased and drying of exposed substrata occurred in patches,
whereas the interstices beneath the bed surface remained wet, and small
pools persisted at intervals along the length of the dewatered channels,
providing refugia for suitably adapted species (Harris, 2006). Surfaces of
Table 1 Disturbance treatments applied in stream mesocosms

Drying disturbance
High frequency Low frequency Control
Mean dry days per cycle 6 6 0
Mean wet days per cycle 27 93 693
Disturbance events (n) 20 7 0
Total duration (d) 693 693 693
% time disturbed 16.7 5.6 0
exposed substrata dried at ambient rates, such that the stress experienced by
organisms stranded in the mesocosms was consistent with those in adjacent
naturally drying stream reaches (Harris, 2006; Ledger et al., 2008). A blocked
experimental design (Zar, 1999) was used in which each treatment was
replicated four times, with each block of channels containing each drought
treatment (i.e. HF and LF disturbance) and a control (4 blocks 3
treatments ¼ 12 channels in total; Fig. 1).
2.3. Sampling and processing

Benthic macroinvertebrates were sampled monthly (21 occasions) in each
mesocosm, immediately before disturbances were applied. On each occa-
sion, a small Surber sample (0.025 m2, 300 mm mesh) was taken from the
upper, central and lower section of each channel. Animals in samples were
later sorted from debris, identified to the lowest practicable taxonomic unit
(species or genus) and counted. Data from each of the three mesocosm sec-
tions were combined to provide a single estimate of macroinvertebrate
species composition for each replicate mesocosm on each sampling
occasion.
2.4. Statistical analysis

Repeated-measures analysis of variance (RM-ANOVA) was used to test the
main effect of disturbance frequency (between-subject factor), time (within-
subject factor) and their interaction, on (1) macroinvertebrate taxon
richness, (2) abundances (numbers m 2) of core taxa and (3) community
similarity metrics (Jaccard’s and Spearman’s rank coefficients). For core taxa
(> 1% total abundance), ANOVA summary statistics are reported in Table 3,
with full tables provided in Appendix B. Data were log-transformed, and
where necessary, departures from sphericity were corrected using the
Huynh–Feldt adjustment. One-way ANOVA with Tukey HSD tests were
used subsequently to examine differences between treatment means at
endpoints. Sequential Bonferroni corrections were applied to groups of tests
to preserve an alpha of 0.05 (Rice, 1989).
Resilience of community structure was assessed using two standard
methods (Bradley and Ormerod, 2001). First, within each mesocosm block,
Spearman’s rank correlation coefficients were used to compare
macroinvertebrate relative abundances in controls with those of each dis-
turbed treatment, with high positive values (maximum þ1) indicating high
stability. Second, resilience of taxonomic composition was assessed using

Jaccard’s coefficient of similarity (J; Magurran, 2004): J(AB) ¼ j/(a þ b j)
where a is the number of taxa in control assemblage A, b is the number
of taxa in disturbed assemblage B within the same experimental block
and j is the number of taxa common to both assemblages, with values of
J ranging from 0 (no similarity, low resilience) to 1 (complete similarity,
high resilience). For both of these measures of community resilience,
pairwise comparisons between controls and each disturbance treatment
(LF, HF) within a each block were made at every endpoint (4 blocks 21
endpoints).
A series of partial constrained ordinations (redundancy analysis,
RDA) was performed using CANOCO 4.5 (ter Braak and Šmilauer,
2002) to establish the effect of the disturbance regimes on community
structure. Accordingly, three ordinations incorporating various combi-
nations of explanatory variables and covariables were used to test for
terms analogous to univariate repeated-measures ANOVA (Lepš and
Šmilauer, 2003), and specifically explored effects of disturbance treat-
ment, time, and their interaction on macroinvertebrate community
composition (see Table 2). Linear ordination was used because gradient
lengths on a preliminary DCA were short (<2 SD). In the analyses, dis-
turbance treatment, experimental block, mesocosm units and season
were coded as binary dummy variables (0 or 1), and sampling occasions
(endpoints) were coded as either dummy variables or as quantitative
Table 2 Results of partial redundancy analyses (1–6) examining macroinvertebrate

community structure in stream mesocosms, based on numerical (1–3) or relative (4–6)
abundance
Analysis Explanatory variables Covariables % var r F P
1 Treatment Time, block 10.5 0.85 26.51 0.001
2 Time Treatment, block 14.5 0.96 38.30 0.001
3 Treatment time Mesocosm, time 3.2 0.76 5.90 0.001
4 Treatment Time, block 8.3 0.85 20.56 0.001
5 Time Treatment, block 14.8 0.96 39.20 0.001
6 Treatment time Mesocosm, time 2.7 0.82 5.01 0.001
% var: percentage of species variability explained by the first ordination axis; r: species-environment cor-
relation of the first axis; F, P: F-ratio and corresponding probability value of each Monte Carlo permu-
tation test. ‘Mesocosm’ denotes use of dummy identifying variables for stream channels.
variables (experimental time, days), to test temporal effects as both dis-

crete and continuous variables. Macroinvertebrate abundance data were
ln-transformed densities (numbers m 2). In the first analysis, the effect
of drought on the macroinvertebrate assemblage was determined using
the three treatments as dummy explanatory variables (0 or 1) and the
four blocks and 21 times as dummy (0 or 1) covariables. Thus, variance
attributable to time, related to shifts in community composition among
seasons and endpoints, together with progressive change during the exper-
iment, was partialled out to reveal underlying differences among the three
treatments. In a second analysis, temporal variation in community compo-
sition was determined with time coded as 21 dummy explanatory variables
and mesocosm identifiers used as covariables, to partial out variance among
channels related to treatment or block effects. A third ordination examined
the interaction between treatment and time, with each combination of
treatment time entered as an explanatory variable. In this analysis, meso-
cosm units and experimental time were entered as covariables, removing the
‘main effect’ of each treatment in each mesocosm, thereby revealing vari-
ance specific to particular treatments through time (Lepš and Šmilauer,
2003). The ordinations above were performed on macroinvertebrate species
data as both absolute densities (in the CANOCO analysis ‘non-
standardised’, analyses 1–3 in Table 2) and as proportions of total abundance
(i.e. ‘centred and standardized’, analyses 4–6 in Table 2). In each case, a
restricted Monte Carlo permutation test (999 permutations) to account
for non-independence within the data was used to test the significance
of the model.
Redundancy analysis was also used to determine the degree of com-
munity development (succession) over time in each treatment
(Woodward et al., 2002). Again, this method was most appropriate
because a preliminary DCA revealed short time-constrained gradient
lengths (<2 SD) (ter Braak and Šmilauer, 2002). Community develop-
ment was analysed for each individual replicate mesocosm community
(n ¼ 12 analyses) and overall for each treatment (n ¼ 3 analyses) (see
Table 4). In the partial RDA analysis, elapsed experimental time (days)
was used as a single constraining explanatory variable and mesocosm
units and seasons were entered as covariables. The percentage of varia-
tion explained by the first RDA axis quantified the strength of any linear
time trend in community structure, and a Monte Carlo permutation test
(999 permutations) was used to assess the statistical significance (P < 0.05)
of the trend.
3. RESULTS
3.1. Disturbance effects on community descriptors
A total of 127 macroinvertebrate taxa were collected from the mesocosms dur-
ing the experimental period, with the overall number of taxa encountered
within individual treatments decreasing with increasing disturbance frequency
(control 114 taxa, LF disturbance 106, HF disturbance 100, Appendix A). In
total, 26 taxa present in controls were absent from drought-disturbed channels,
most notably rare (<1% total numbers) Trichoptera (8 taxa), Coleoptera (5),
Ephemeroptera (4), Diptera (3) and Gastropoda (3). Overall, HF disturbance
excluded more taxa (20 control taxa absent) than the LF treatment (17 control
taxa absent). A further 12 taxa, including rare semi-aquatic Diptera (6 taxa),
were found only in the drought-disturbed channels (Appendix A). RM-
ANOVA revealed that macroinvertebrate taxon richness varied significantly
with disturbance treatment (F2,6 ¼ 29.87, P ¼ 0.001), experimental time
(F20,120 ¼ 40.18, P < 0.0005) and their interaction (F40,120 ¼ 2.46,
P < 0.0005), but there was no effect of mesocosm block (F3,6 ¼ 3.57,
P ¼ 0.086). One-way ANOVAs with multiple comparisons showed that taxon
richness under LF disturbance (endpoint mean 30.2 1.5 taxa) was not signif-
icantly different from undisturbed controls (mean 32.6 1.6 taxa, Tukey HSD,
P < 0.05) at any endpoint, whereas by contrast, richness in HF disturbance
treatments (mean 24.1 1.2 taxa) was significantly lower than in controls
(by a mean of 26%) at 13 endpoints (P < 0.05, Fig. 2A).
Mean total abundance (numbers m 2) of macroinvertebrates varied among
treatments and sampling endpoints, with peaks in summer and troughs in winter
(Fig. 2B). RM-ANOVA revealed non-significant main effects of treatment
(F2,6 ¼ 0.55, P ¼ 0.606) and block (F3,6 ¼ 2.74, P ¼ 0.131), whereas time effects
(F20,120 ¼ 51.46, P < 0.0005) and the interaction between treatment and time
(F40,120 ¼ 2.99, P < 0.0005) were statistically significant, the latter reflecting var-
ied effects of the drying among endpoints. Although mean abundances in LF
(12,235 1972 m 2) and HF treatments (12,958 2434 m 2) were similar
to controls (12,093 1618 m 2) ANOVA with multiple comparisons revealed
HF drought significantly (Tukey P < 0.05) increased abundances in summer
and reduced them in autumn and winter (Fig. 2B).
Stability in rank abundance of the fauna between control and disturbed
assemblages depended on drying frequency (RM-ANOVA, F1,3 ¼ 600.67,
P < 0.0005), time (F20,60 ¼ 5.16, P < 0.0005) and their interaction
(F20,60 ¼ 2.76, P ¼ 0.001). Declining resilience was evident with increasing
A
50
40
Taxon richness
30
20
10
0
1.5.00 10.12.00 21.7.01 1.3.02
B
100,000
Abundance (numbers m-2)
10,000
1000 Control
LF
HF
100
1.5.00 10.12.00 21.7.01 1.3.02
Date
Figure 2 Mean (1 SE) taxon richness (A) and total abundance (numbers m 2) (B) of
macroinvertebrates in mesocosms disturbed at high frequency (HF), low frequency (LF)
and in undisturbed controls (C) over 21 months.
disturbance frequency, as revealed by Spearman’s rank correlation coeffi-

cients (LF mean ¼ 0.80 0.02, HF mean ¼ 0.45 0.03; Fig. 3A), and was
statistically significant on most sampling occasions (t-tests, P < 0.05). Simi-
larly, Jaccard’s coefficients were consistently lower in HF disturbance treat-
ment (LF mean ¼ 0.55 0.01, HF mean ¼ 0.47 0.01; Fig. 3B), indicating
greatest community dissimilarity from controls, as revealed by a RM-
ANOVA with statistically significant effects of treatment (F1,3 ¼ 76.87,
P ¼ 0.003), time (F20,60 ¼ 4.73, P < 0.0005) and a non-significant interac-
tion term (F20,60 ¼ 1.44, P ¼ 0.140).
A
1
0.8
Correlation coefficient (r)
0.6
0.4
0.2
B
0.8
0.6
Jaccard's J
0.4
Control-LF Control-HF
0.2
1.5.00 10.12.00 21.7.01 1.3.02
Date
Figure 3 Resilience of macroinvertebrate communities to drought disturbance, as
revealed by Spearman's rank correlation coefficients (A) and Jaccard's similarity coeffi-
cients (B) comparing LF disturbance and HF disturbance treatments with undisturbed
controls.
3.2. Disturbance effects on community structure

Drought disturbance had significant effects on macroinvertebrate community
structure (RDA, Table 2) and on the abundances of the main constituent
species (RM-ANOVA, Table 3). In undisturbed controls, communities
Table 3 Summary of repeated-measures analysis of variance (RM-ANOVA) testing the

main effects of drought treatment, mesocosm block (between-subject factors) and time
(within-subject factors), and the interaction between treatment and time, on
abundance (numbers m 2) of 12 core taxa (full RM-ANOVA tables in Appendix B)
Taxon Treatment Time Treatment time Post hoc
G. pulex 0.003 < 0.0005 0.043 C, LF > HF
Pisidium sp. 0.035 < 0.0005 < 0.0005
Chironomini 0.018 < 0.0005 < 0.0005
Tanytarsini 0.571 < 0.0005 0.001
Diamesinae 0.005 < 0.0005 0.001
Orthocladiinae 0.031 < 0.0005 0.012
Ceratopogonidae < 0.0005 < 0.0005 0.196 C > LF, HF
P. antipodarum 0.243 < 0.0005 0.011
R. peregra 0.010 < 0.0005 < 0.0005
Tubificidae 0.608 < 0.0005 < 0.0005
Naididae 0.032 < 0.0005 0.046
P. flavomaculatus 0.003 < 0.0005 < 0.0005
Bold denotes statistically significant P values following sequential Bonferroni correction.
were dominated numerically by 17 core taxa (each >1% total numbers)

which collectively accounted for 89% of total numbers, together
with 97 rare taxa that contributed a further 11% (Fig. 4; Appendix A).
Core taxa in controls were Tanytarsini midge larvae (1917 545 individ-
uals m 2), Tubificidae worms (mean 1843 378 m 2), Orthocladiinae
midge larvae (1435 746 m 2), Gammarus pulex L. amphipods
(1165 319 mm 2), Naididae worms (976 429 m 2), Chironomini
midge larvae (677 120 m 2), Potamopyrgus antipodarum J.E. Grey gastropods
(562 154 m 2), Radix balthica (L.) gastropods (363 155 m 2), Pisidium sp.
bivalves (360 116 m 2), Diamesinae midge larvae (253 152 m 2), Cer-
atopogonidae midge larvae (218 55 m 2), Polycentropus flavomaculatus (Pictet)
caddisfly larvae (196 65 m 2), Tanypodinae midge larvae (178 48 m 2),
Caenis luctuosa (Bürmister) mayfly larvae (148 51 m 2), Oulimnius sp. beetles
(132 31 m 2), Asellus aquaticus (L.) isopods (116 49 m 2) and Tinodes
waeneri (L.) caddisfly larvae (115 51 m 2) (Fig. 5, Appendix A).
The shape of the rank-abundance curve for LF disturbed communities
was similar to controls (16 core taxa accounted for 92% total numbers)
but the upper portion for HF disturbance was elevated, indicating that fre-
quently disturbed communities were less even, being dominated by relatively
10,000
Control
LF
Abundance (number m-2)

1000
HF
100
10
1
1 10 100
Taxon rank
Figure 4 Mean abundance (number m 2) of macroinvertebrates in undisturbed con-
trols (C) and treatments disturbed at high (HF) and low (LF) frequency. For each treat-
ment, taxa were ranked from left to right in order of decreasing abundance.
few taxa (11 core taxa accounted for 93% total numbers), most notably worms
and chironomids (Fig. 4, Appendix A). Partial redundancy analyses based on
both the numerical (analyses 1–3, Table 2) and relative abundance (analyses
4–6) of constituent taxa showed that community structure varied significantly
(P < 0.001) with drought treatment, time and their interaction. Ordination
revealed that some mayflies (Caenis luctuosa, Ephemera danica Müller), snails
(Ancylus fluviatilis Müller, Potamopyrgus antipodarum, Valvata piscinalis Müller),
caddisflies (Sericostoma personatum (Spense), Hydropsyche contubernalis
McLachlan) and beetles (Limnius volckmari (Panzer)) were highly susceptible
to drought, being significantly less abundant in drought treatments,
irrespective of frequency, than in undisturbed controls (Fig. 6A).
Resilience varied with disturbance frequency for many other taxa; densities
of amphipods (Gammarus pulex) and leeches (Erpobdella octoculata L.), together
with several caddisflies (Athripsodes cinereus Curtis, Lepidostoma hirtum
(Fabricius), Polycentropus flavomaculatus, Tinodes weaneri L.) and beetles
(Oulimnius tuberculatus Müller, Elmis aenea (Müller)), were sustained under
LF disturbance but markedly reduced under HF drought (Fig. 6A).
Control LF HF
Tubificidae Tanytarsini Orthocladiinae

10,000 100,000 100,000
10,000 10,000
1000 1000 1000
100 100
100 10 10
Naididae Chironomini Gammarus

10,000 10,000 10,000
1000 1000 1000

Abundance (numbers m-2)
100 100 100
10 10 10
Potamopyrgus Radix Pisidium

10,000 10,000 10,000
1000 1000 1000
100 100 100
10 10 10
1 1 1
Diamesinae Ceratopogonidae Polycentropus

10,000 10,000 10,000
1000 1000 1000
100 100 100
10 10 10
1 1 1
1.5.00 10.12.00 21.7.01 1.3.02 1.5.00 10.12.00 21.7.01 1.3.02 1.5.00 10.12.00 21.7.01 1.3.02
Date
Figure 5 Mean ( 1 SE) densities of 12 core taxa in mesocosms disturbed at high fre-
quency (HF), low frequency (LF) and in undisturbed controls (C) over 21 months. Note y-
axes are scaled to data.
Chironomini midges exploited drying irrespective of frequency, whereas

Oligochaeta (Eiseniella tetredra (Savigny), Lumbriculidae, Naididae)
worms only increased in HF disturbance treatments. Repeated-measures
ANOVA revealed that effects on the majority of common taxa depended
on the time of sampling (significant treatment time effect, Table 3). One-
way ANOVA with multiple comparisons revealed that for Pisidium sp., R.
Tin LF
Erp
Pol Pis
Oul Chi
Gam
Ath
Elm Lep Nai
Hyd
Pot Ser Lum
Cae Lim HF
Dug
Anc
C
Eis
Ase
Val
Erp LF
Pol Tip
Oul
Ort
Dia Chi
Nai
Tan
Cae Lum
Eph HF Tub
Anc C
Pro Eis
Val Hem
Figure 6 Partial redundancy analysis (RDA) diagram illustrating overall differences in

macroinvertebrate community structure among patches disturbed at low (LF) and high
(HF) frequency, and undisturbed controls (C). Ordinations were based on either relative
(A) or numerical abundance (B) of component species. The direction, and length, of taxa
vectors relative to the origin is indicated by abbreviated taxa labels, and reflects the
peregra and P. flavomaculatus, densities were lower in HF treatments than in

LF treatments or controls at most endpoints (Tukey HSD, P < 0.05; Fig. 5).
Contrasts in the numerical responses of component species to distur-
bance led to marked shifts in relative abundance, as revealed by RDA
(analyses 4–6, Table 2; Fig. 6B). Thus, LF treatments contained proportion-
ally more fly larvae (some chironomid midges and tipulid craneflies) and
fewer mayflies and gastropods than controls, but were otherwise similar
to controls in taxonomic composition, whereas HF treatments deviated
markedly from controls, being dominated by fly larvae (especially chirono-
mids) and most notably oligochaetes (Naididae, Lumbriculidae Tubificidae)
and heavily depleted of mayflies, snails and caddisflies (Fig. 6B).
3.3. Disturbance effects on temporal dynamics

Macroinvertebrate community structure differed markedly among sampling
endpoints and seasons (RDA analyses 2 and 5, Table 2) but the occurrence
and extent of statistically significant directional change (community
development) depended on disturbance frequency (RDA analyses 1–15,
Table 4). Linear time-trends reflecting strong turnover in community com-
position during the experiment were statistically significant (P ¼ 0.001) for
controls and LF disturbance treatments (RDA analyses 1–10, Table 4),
where densities of gastropods (Potamopyrgus antipodarum), bivalves
(Pisidium sp.) and oligochaetes (Lumbriculidae, Tubificidae) increased with
time as amphipods (Gammarus pulex), isopods (Asellus aquaticus L.), mayflies
(Caenis luctuosa) and caddisflies (Polycentropus flavomaculatus) declined (Figs. 5
and 7A, B). The percentage of variation attributable to a linear time trend
in the two treatments (mean C ¼ 28.6%, LF ¼ 20.7%) was similar (t-test,
P > 0.05). By contrast, RDAs were not statistically significant for HF
trend, and extent of increase in, (relative or numerical) abundance among treatments.
Taxa in diagrams were those in which > 15% species variance was explained by the
RDA model. Abbreviations as follows: Anc, Ancylus fluviatilis; Ase, Asellus aquaticus;
Ath, Athripsodes cinereus; Cae, Caenis luctuosa; Chi, Chironomini; Dia, Diamesinae;
Dug, Dugesia polychroa; Eis, Eiseniella tetradra; Elm, Elmis aenea; Eph, Ephemera
danica; Erp, Erpobdella octoculata; Gam, Gammarus pulex; Hem, Hemerodromia; Hyd c,
Hydropsyche contubernalis; Lep, Lepidostoma hirtum; Lim, Limnius sp.; Lum,
Lumbriculidae; Nai, Naididae; Ort, Orthocladiinae; Oul, Oulimnius sp.; Pis, Pisidium sp.;
Pol, Polycentropus flavomaculatus; Pot, Potamopyrgus antipodarum; Pro, Procleon
bifidum; Ser, Sericostoma personatum; Tan, Tanytarsini; Tin, Tinodes waeneri; Tip, Tipula
montium; Tub, Tubificidae; Val, Valvata piscinalis.
Table 4 Results of partial redundancy analyses (1–15) examining linear time trends in
macroinvertebrate community structure in stream mesocosms, based on the relative
abundance of component taxa
Analysis Treatment Block % Var r F P
1 Control 1 34.1 0.90 8.27 0.001
2 2 21.7 0.82 4.44 0.001
3 3 22.7 0.88 4.70 0.001
4 4 35.6 0.85 8.85 0.001
5 1-4 21.8 0.82 21.21 0.001
6 LF 1 23.6 0.84 4.94 0.001
7 2 17.2 0.87 3.33 0.001
8 3 21.8 0.86 4.45 0.001
9 4 20.0 0.83 3.91 0.001
10 1-4 14.6 0.76 13.01 0.001
11 HF 1 8.0 0.56 1.39 0.225
12 2 4.2 0.42 0.70 0.553
13 3 7.3 0.48 1.26 0.271
14 4 5.4 0.37 0.91 0.426
15 1–4 4.2 0.37 3.37 0.016
% Var, percentage of species variability explained by the first ordination axis; r, species-environment cor-
relation of the first axis; F, P, F-ratio and corresponding probability value of each Monte Carlo permu-
tation test.
disturbance communities (P > 0.05, RDA analyses 11–14), indicating that

monthly substratum drying arrested community development (Fig. 7C),
and the percentage of variation attributable to a linear time trend in HF
channels (mean HF ¼ 6.2%) was significantly lower than in controls or LF
treatments (t-test, P > 0.05).
4. DISCUSSION
Climate change is expected to increase the occurrence of extreme
events and change the nature of disturbance regimes across a variety of eco-
systems, but direct evidence as to how these effects might be manifested re-
mains scarce (Durance and Ormerod, 2007; Woodward et al., 2010). In the
present study, we simulated supraseasonal drought by repeatedly dewatering
stream sediments. Such droughts occur across the globe (e.g. Lake, 2008;
Lind et al., 2006; Schlief and Mutz, 2011) and are expected to increase in
frequency and intensity with climate change in many areas (IPCC, 2007).
The results of our mesocosm experiment reveal how disturbance regimes
A
Tanyt
Leu f Ort
Glo Sia
Val Eph
Pis Anc Gam
Erp Hyd c
TQ Pot Hyd p
Pol
Tub
Cae Ase
Lym Chi
B Tanyt
Gam
Erp
Hel
Bra sub Ase
TQ
Pis Bae m
Ant
Glo
Tub
Eph
Nai
C Tanyt
TQ
Cer
Tub
Nai
Figure 7 Partial RDA diagram illustrating directional change in macroinvertebrate com-

munity structure in undisturbed controls (A) and in patches disturbed at low (B) and
high (C) frequency. Axis 1 was constrained by experimental time (days) as a linear trend.
The direction, and length, of taxa vectors relative to the origin is indicated by
abbreviated taxa labels, and reflects the trend, and extent of increase in, (relative or
numerical) abundance through time. Abbreviations as in Figure 6 plus: Ant, Antocha
vitripennis; Bae m, Baetis muticus; Bra sub, Brachycentrus subnubilis; Cer, Cer-
atopogonidae; Glo, Glossiphonia complanata; Hel, Helobdella stagnalis; Hyd p,
Hydropsyche pellucidula; Leu, Leuctra fusca; Rad, Radix balthica; Sia, Sialis lutaria.
associated with drought shape ecological assemblages. Macroinvertebrates

were relatively resilient to drying disturbances occurring at low frequency
(quarterly), sustaining abundant and diverse assemblages which developed
over time despite repeated dewatering. These data provide further
evidence of the strong capacity for biotic recovery in streams following
modest levels of disturbance (Feld et al., 2011; Hladyz et al., 2011;
Townsend and Hildrew, 1994), including drought (e.g. Lake, 2003;
Ledger and Hildrew, 2001). However, more frequent (monthly) drying
eroded this innate resilience and generated relatively impoverished,
compositionally static assemblages dominated by a few opportunistic
species. Such severe impacts on community structure are likely to alter
process rates (e.g. decomposition, herbivory, primary and secondary
production), with wider effects on the amenity and conservation value of
streams, and their provision of ecological goods (production of fisheries)
and services (water quality) (Ledger et al., 2011), but much research
remains to be done to elucidate many of these effects (Feld et al., 2011;
Friberg et al., 2011).
4.1. Disturbance and diversity

Drying disturbances reduced macroinvertebrate taxon richness at high, but
not low, frequency. Our results are thus broadly consistent with the prev-
ailing view that disturbance in streams can reduce diversity (e.g. Death,
2002; Death and Winterbourn, 1995; Matthaei et al., 1996), but that
macroinvertebrate taxon richness is rapidly restored by recolonisation
(e.g. McCabe and Gotelli, 2000; Townsend and Hildrew, 1994).
Although our study tested only two levels of disturbance, the results were
not consistent with the unimodal diversity–disturbance relationship
predicted by the IDH (Connell, 1978). The most-often cited explanation
for deviation from IDH predictions is a lack of trade-off between
competitive ability and disturbance sensitivity among the biota (Chesson
and Huntly, 1997; dos Santos et al., 2011). Consistent with this, whilst
we observed that HF disturbance excluded large rare species and favoured
good colonists, the latter were still were present in undisturbed controls
and LF disturbance habitats, albeit at lower density.
4.2. Resilience and disturbance frequency

Flow cessation led to patchy dewatering of mesocosm habitats, and resis-
tance to drying among the biota was generally low, with high mortality
of macroinvertebrates stranded on desiccating sediments (Harris, 2006).
However, wet interstices and small pools provided refugia for suitably
adapted species (Harris, 2006; Ledger et al., 2011), and high resilience
to LF disturbance restored endpoint community structure. Although
some fauna exploited LF disturbance, especially some chironomids,
overall increases were less marked than in HF treatments. Chironomid
proliferations may have been constrained by the high resilience of
algae to infrequent drought (Ledger et al., 2006): crustose green algae
recovered from dewatering, displacing diatoms mats that provide
favourable habitat and food (Ledger et al., 2006, 2008). The
re-establishment of the community occurred via several routes, including
in-channel reproduction by survivors in interstitial sediments (see Burrell
and Ledger, 2003), immigration by drift from upstream (Mill Stream)
and oviposition by winged adults (Harris, 2006). The year-round
presence of colonists above and below the surface water in the channel is
thought to buffer stream communities against disturbance (Townsend and
Hildrew, 1994). In our experiment, undisturbed upstream source
communities (i.e. the parent river) provided a ready supply of recolonists
as may be the case in many natural droughts. However, our results could
be considered conservative, since drought typically causes extensive
drying across the riverscape and recolonist sources are more remote
(Ledger et al., 2011).
HF disturbance led to a marked shift in faunal composition, with substan-
tial irruptions in the abundance of chironomid midges and oligochaete
worms and declines in amphipods, mayflies and caddisflies, among
others. Chironomids are characterised by r-selected traits (relative to the more
K-selected larger macroinvertebrates), including high fecundity, small
size and short generation times, which enable rapid exploitation of food,
habitat or enemy-free space created by disturbances (Pinder, 1992;
Townsend and Hildrew, 1994). Post-disturbance irruptions of chironomid
larvae are often observed in streams (e.g. Power et al., 2008) and can be
particularly marked in the warm nutrient-rich waters of chalk streams
after drought (Wright et al., 2004). Many chironomids live in soft
sediments that provide refuge from high temperatures and low oxygen
concentrations associated with drought (Armitage et al., 1995), and
the proliferation of diatoms under HF drying may have triggered
irruptions of these primary consumers (Ledger et al., 2008). Together
with chironomids, oligochaetes dominated communities subject to HF
disturbance. Faced with disturbance, many oligochaetes increase their
reproductive output, some by adopting semelparity to maximize resources
invested in reproduction (Bird, 1982). For naidid worms, an immediate

(within a day) increase in numbers following disturbances was often
observed that we attribute to asexual reproduction, consistent with
observations elsewhere (Brinkhurst and Jamieson, 1971), although it is not
clear whether this is a response to favourable (e.g. warm temperature,
abundant resources) or deleterious (e.g. dessication, low oxygen)
environmental cues.
4.3. Resilience and ecosystem functioning

Our study revealed significant variation in species responses to drying, rang-
ing from irruption to extirpation, including those within the same functional
groups (Fig. 8), attributable to body size and life-history traits (Ledger et al.,
2011). Such variability in responses to environmental change among
species that contribute to the same processes is recognised as a key determi-
nant of ecosystem resilience (Elmqvist et al., 2003). Theoretically, where
assemblages contain species with a diversity of responses to specific local
conditions, as shown here, turnover in species composition when faced
with environmental stress may lead to maintenance of ecosystem processes,
and in such communities high taxonomic biodiversity can be viewed as
conferring a degree of ecological insurance against change (Elmqvist
et al., 2003; Mulder et al., 2012). On the other hand, widespread
uniformity in responses to change among species that perform the
same ecological roles should curtail redundancy, leading to potentially
dramatic shifts in key processes as the environment changes (Folke et al.,
2004). To date, however, drought research in streams has centred on
impacts on community structure, with uncertain consequences for
functioning (but see Chadwick and Huryn, 2007; Dewson et al., 2007).
As part of the present study, however, Ledger et al. (2011) showed how
drought affected the process of macroinvertebrate secondary production
and discovered that, while there was clear evidence of contrasting
responses in production to drought among biota within some functional
groups (grazers and collectors), substantial reductions were far more
frequent than no change or increased production, both within and
among functional groups, and overall secondary production was more
than halved (58% reduction) by frequent (monthly) drying (Ledger et al.,
2011). This substantial erosion of macroinvertebrate biomass in the face
of drought stress is likely to have wider effects on ecosystem processes
such as leaf litter decomposition and herbivory.
Collectors Filterers
1 1
0.5 0.5
0 0
Grazers Shredders
1 1
Proportion
0.5 0.5
0 0
Engulfers Piercers
1
1
0.5 0.5
0 0
- 0 + - 0 +
Drought response class
Figure 8 Distribution of high-frequency (monthly) dewatering effects on secondary
production of macroinvertebrate taxa in six functional feeding groups (figure redrawn
after Ledger et al., 2011). Taxa were classified according to their statistically significant
positive (þ) negative () or lack of (0) response to HF drought, as revealed by one-
sample t-tests.
Our mesoscosm experiment revealed strong reductions among core taxa

known to perform functionally important roles in stream communities. The
suppression of potent shredders, most notably amphipods (Gammarus pulex)
and caddis larvae (Sericostoma personatum, Limnephilidae) (see Jonsson and
Malmqvist, 2000; Woodward et al., 2008), could reduce leaf litter
decomposition rates and increase the accumulation of detritus in drought
affected streams (Lake, 2003), potentially causing wider indirect effects
on secondary production and the dynamic stability of food webs under

donor control (Rooney et al., 2006; Walters and Post, 2011). Many of
the most effective grazers, particularly gastropods, declined under
drought (e.g. P. antipodarum), raising the possibility that diatom
proliferations in HF disturbed treatments (see Ledger et al., 2008) was
caused by herbivore release, notwithstanding irruptions in herbivorous
chironomids. Drought also reduced populations of macroinvertebrate
predators, especially those of large size with limited access to refugia such
as caddis (e.g. P. flavomaculatus), alderflies (S. lutaria) and leeches (e.g.
E. octoculata), and we speculate this may lessen top-down pressure on
prey assemblages, such as chironomids, with unknown indirect effects.
However, further experiments are needed to establish the wider effects
of drought on ecosystem functioning.
4.4. Disturbance and community development

The experiment revealed dynamic, progressive change in community struc-
ture in the absence of disturbance. Theoretically, turnover in community
composition can be driven by a range of biotic processes including compe-
tition and ecosystem engineering, and/or by abiotic processes, such as shifts
in climate, flow or habitat (Milner, 1994). In the mesocosms, benthic hab-
itats changed subtly with time, with patches of sand and fine organic
sediment developing among coarse gravels and macrophytes (Harris,
2006). Changes in substratum particle size distributions may therefore
account for some of the observed turnover, with taxa including caddis
(P. flavomaculatus) and crustaceans (G. pulex, A. aquaticus) associated with
gravels replaced gradually by those tolerant of finer sediments, such as mol-
luscs (P. antipodarum, Pisidium sp.), worms (Lumbriculidae, Tubificidae) and
burrowing mayflies (E. danica) (Harris, 2006). However, there was also a
gradual fall in diatom biomass in the absence of disturbance (Ledger et al.,
2008) which we suggest could explain declines in herbivorous mayflies
(C. luctuosa).
The extent of community development under LF disturbance was sim-
ilar to that in undisturbed controls, indicating, first, that component taxa
were largely resilient to infrequent dewatering, and second, that key habitat
features were not permanently changed by the disturbance. By contrast,
HF disturbance arrested community development completely by recur-
rently eroding population abundances and/or by constraining habitat
development itself. HF disturbances acted to tightly constrain communities
to relatively few tolerant taxa, with traits which enable survival in harsh
conditions, as has been reported elsewhere (e.g. Chase, 2007; Lepori
and Malmqvist, 2009). However, we found no evidence of progressive
erosion of biodiversity or numerical abundance as experimental time
elapsed, consistent with the notion that immigration and extinction rates
either reached equilibrium or declined to zero, during the experiment
(see Death, 2002).
4.5. Drought as an environmental filter

Much debate has centred upon the extent to which community compo-
sition is determined by stochastic processes of colonisation and extinc-
tion (neutral theory) or by deterministic processes in which species
associate with specific ecological conditions (niche theory) (see e.g.
Chase, 2007; Thompson and Townsend, 2006). Our data suggest that
drought acted as a harsh environmental filter that stripped species
lacking resistance and/or resilience traits from the regional pool,
consistent with the notion of niche selection in communities (see
Chase, 2007; Poff, 1997). We also observed high compositional
similarity among the disturbed channels—similar habitats hosted similar
communities—with species–habitat associations shaped by traits (Chase,
2007). These largely predictable drought-adapted assemblages consisted
of small short-lived taxa (>1 life cycle per year, e.g. chironomids), or
those with refuge-seeking or interstitial habits (e.g. ceratopogonids,
oligochaetes), whereas many larger taxa with longer life cycles (1 life
cycle per year), including some caddis, mayflies and beetles, were
eliminated by frequent dewatering (Ledger et al., 2011; Fig. 9).
Community development was also canalised, with turnover in controls
corresponding closely to changes in the physical nature of the substrate,
and we observed little evidence of stochastic ecological drift at the scale
of the channel (Harris, 2006). However, we have shown that stochastic
arrival in a colonisation sequence can shape community composition at
smaller (patch) spatial scales (Ledger et al., 2006), and it seems likely
that both deterministic and stochastic processes influence community
development in stream habitats, with species composition shaped by
the physical nature of the environment and dispersal (Lepori and
Malmqvist, 2009).
A
60
Drought production (% of control)

40
20
0
-20
-40
-60
-80
-100
>1 1 <1
Number of generations per year
B
80
Drought production (% of control)
60
40
20
0
-20
-40
-60
-80
-100
0.011–0.1 0.11–1 1.1–10 11–100
Body Mass (mg)
Figure 9 Mean ( 1 SE) effect of high-frequency drought on secondary production of
macroinvertebrate taxa in relation to (A) the potential number of life cycles per year and
(B) mean individual body mass (figure redrawn after Ledger et al., 2011).
5. CONCLUSIONS
Hydrologic drought is a natural phenomenon and an important com-
ponent of the flow regime in many riverine ecosystems (Boulton, 2003;
Lake, 2003). Future shifts in climate are expected to increase the frequency,
intensity and extent of drought events in river systems, with potentially
devastating effects on benthic ecosystems (Sponseller et al., 2010).
The ecological effects of drought are still relatively poorly understood when
compared with other environmental stressors such as flooding or acid
episodicity, despite a recent intensification of research effort (e.g. James
et al., 2008). In our view, controlled manipulative field experiments are
needed to develop a strong mechanistic understanding of the many
structural and functional impacts of drought, particularly in relation to
biogeochemical processes and dynamics at higher levels of biological
organisation (Ledger et al., 2011). In this study, we simulated prolonged
drought conditions that caused repeated patchy dewatering of benthic
habitat and found that the effects of the stress depend on the frequency
with which benthic habitats are exposed to stream bed dewatering. The
effects of these harsh low-flow disturbances are likely to be very different
from those that do not lead to dewatering, and research is needed to
explore the relationships between drought regimes and ecological impacts
in rivers to identify resilience thresholds, non-linear responses (i.e. tipping
points) and the potential for system recovery, before a more predictive
science can emerge (Friberg et al., 2011).
ACKNOWLEDGMENTS
The Freshwater Biological Association (FBA) and the Centre for Ecology and Hydrology
Dorset generously supported this research. The project was funded by a FBA/Natural
Environmental Research Council (NERC) postdoctoral fellowship to MEL, a tied
studentship to RMLH, and NERC grant NER/B/S/2002/00215. Dr Iwan Jones kindly
supplied the photograph for Fig. 1. We are grateful to the many people who kindly
assisted in the field, with special thanks to Mr Brian Godfrey, Dr Bethan Ledger and
Dr John Murphy.
APPENDIX A
Summary (experimental mean and standard error [SE]) of benthic macroinvertebrate numerical (numbers m 2) and relative (% total
numbers) abundance in mesocosm patches disturbed at high (LF) and low (HF) frequency, and in undisturbed controls. Taxa within orders are
ranked alphabetically.
Taxon Control LF drought HF drought

m 2 % m 2 % m 2 %
Mean SE Mean SE Mean SE Mean SE Mean SE Mean SE
Tricladida
Dendrocoelum lacteum 2.8 1.8 < 0.1 < 0.1 3.2 1.9 < 0.1 < 0.1 0.5 0.8 < 0.1 < 0.1
(Müller)
Dugesia polychroa 10.0 5.9 < 0.1 < 0.1 3.5 2.5 < 0.1 < 0.1 0.2 0.4 < 0.1 < 0.1
Schmidt
Dugesia tigrina (Girard) 1.9 1.4 < 0.1 < 0.1 0.5 0.6 < 0.1 < 0.1 0 0 0 0
Glossoscolecidae 0 0 0 0 0 0 0 0 0.2 0.4 < 0.1 < 0.1
Planaria torva (Müller) 1.6 1.2 < 0.1 < 0.1 0.7 0.9 < 0.1 < 0.1 0.4 0.5 < 0.1 < 0.1
Polycelis nigra Müller 6.2 3.8 < 0.1 < 0.1 6.2 3.3 < 0.1 < 0.1 2.1 1.8 < 0.1 < 0.1
Oligochaeta
Eiseniella tetraedra 0.9 0.8 < 0.1 < 0.1 0.9 0.9 < 0.1 < 0.1 4.9 2.1 < 0.1 < 0.1
(Savigny)
Lumbriculidae 24.7 13.4 0.3 0.2 27.5 8.1 0.3 0.1 60.8 14.2 0.9 0.3
Naididae 975.9 429.1 6.8 2.4 1318.3 653.3 9.0 2.9 2034.1 680.1 15.8 4.2
Tubificidae 1843.5 378.3 17.6 3.2 1492.5 269.9 15.5 2.5 1505.3 203.3 18.2 2.6
Gastropoda
Acroloxus lacustris (L.) 0.2 0.4 < 0.1 < 0.1 0 0 0 0 0 0 0 0
Continued
ranked alphabetically.—cont'd
m 2 % m 2 % m 2 %
Ancylus fluviatilis 43.0 25.6 0.4 0.2 12.2 8.8 0.1 < 0.1 0.5 0.8 < 0.1 < 0.1
(Müller)
Bithynia leachii 0.5 0.6 < 0.1 < 0.1 0 0 0 0 0 0 0 0
(Sheppard)
Bithynia tentaculata (L.) 0.4 0.5 < 0.1 < 0.1 0.4 0.7 < 0.1 < 0.1 0 0 0 0
Physa fontinalis (L.) 3.7 3.0 < 0.1 < 0.1 4.2 2.9 < 0.1 < 0.1 0.2 0.4 < 0.1 < 0.1
Potamopyrgus 561.5 154.6 5.6 1.4 329.7 117.7 4.0 1.4 127.3 40.6 2.0 0.8
antipodarum (J.E. Grey)
Radix balthica (L.) 362.8 154.7 2.9 1.0 254.1 72.8 2.6 0.7 150.9 48.1 2.4 0.9
Theodoxus fluviatilis (L.) 3.9 2.8 < 0.1 < 0.1 0.7 0.9 < 0.1 < 0.1 0.2 0.4 < 0.1 < 0.1
Valvata piscinalis 47.6 17.2 0.5 0.2 11.6 8.7 0.1 < 0.1 0.9 0.9 < 0.1 < 0.1
(Müller)
Bivalvia
Pisidium sp. 360.2 116.3 3.3 1.0 257.1 70.2 2.7 0.8 63.8 17.0 0.8 0.3
Sphaerium sp. 1.9 1.8 < 0.1 < 0.1 0.4 0.7 < 0.1 < 0.1 0 0 0 0
Hirudinea
Erpobdella octoculata (L.) 44.6 13.3 0.4 0.1 31.6 8.6 0.3 < 0.1 6.5 2.8 0.1 < 0.1
Glossiphonia complanata 7.4 3.3 < 0.1 < 0.1 4.6 2.4 < 0.1 < 0.1 1.9 1.3 < 0.1 < 0.1
(L.)
Helobdella stagnalis (L.) 2.8 2.4 < 0.1 < 0.1 2.6 2.1 < 0.1 < 0.1 1.4 1.4 < 0.1 < 0.1
Piscicola geometra (L.) 0.4 0.7 < 0.1 < 0.1 0.4 0.5 < 0.1 < 0.1 0.2 0.4 < 0.1 < 0.1
Trocheta subviridis 0 0 0 0 0.2 0.4 < 0.1 < 0.1 0 0 0 0
(Dutrochet)
Isopoda
Asellus aquaticus (L.) 115.7 49.0 1.1 0.3 85.5 35.4 1.1 0.5 39.1 11.5 0.5 0.2
Amphipoda
Crangonyx pseudogracilis 15.0 8.1 0.2 < 0.1 15.0 6.1 0.3 0.1 16.9 8.5 0.3 0.2
Bousfield
Gammarus pulex (L.) 1165.1 318.9 10.2 2.3 1076.0 268.5 9.7 1.9 406.0 133.9 4.5 1.3
Ephemeroptera
Alainites muticus (L.) 14.5 7.3 0.1 < 0.1 30.3 13.1 0.3 0.2 10.4 4.1 0.2 < 0.1
Baetis buceratus Eaton 21.0 13.7 0.1 < 0.1 22.9 11.8 0.2 < 0.1 25.6 26.3 0.2 0.1
Baetis rhodani (Pictet) 10.4 7.1 < 0.1 < 0.1 4.6 3.2 < 0.1 < 0.1 4.2 2.7 < 0.1 < 0.1
Baetis scambus Eaton 47.3 28.3 0.3 0.2 64.7 28.2 0.4 0.2 50.6 26.3 0.2 0.1
Brachycercus harrisellus 6.7 5.2 < 0.1 < 0.1 2.5 2.7 < 0.1 < 0.1 1.4 1.3 < 0.1 < 0.1
Curtis
Caenis horaria (L.) 0.7 0.7 < 0.1 < 0.1 0 0 0 0 0 0 0 0
Caenis luctuosa 147.9 50.6 1.6 0.5 45.0 13.9 0.5 0.1 21.2 9.0 0.2 < 0.1
Bürmeister
Caenis rivulorum Eaton 1.4 1.3 < 0.1 < 0.1 0.2 0.4 < 0.1 < 0.1 0 0 0 0
Centroptilum luteolum 15.0 7.3 0.2 < 0.1 10.4 6.6 0.1 < 0.1 5.3 3.6 < 0.1 < 0.1
(Müller)
Ecdyonurus sp. 0.2 0.4 < 0.1 < 0.1 0 0 0 0 0 0 0 0
Ephemera danica Müller 92.6 21.5 0.9 0.2 28.7 7.4 0.3 < 0.1 5.6 2.3 < 0.1 < 0.1
Heptagenia sulphurea 6.3 3.3 < 0.1 < 0.1 2.6 1.7 < 0.1 < 0.1 0.5 0.6 < 0.1 < 0.1
(Müller)
Lasiobaetis atrebatinus 0.4 0.7 < 0.1 < 0.1 0.4 0.7 < 0.1 < 0.1 0 0 0 0
Eaton
Nigrobaetis niger (L.) 0.5 0.8 < 0.1 < 0.1 0.4 0.5 < 0.1 < 0.1 0.5 0.6 < 0.1 < 0.1
Paraleptophlebia 1.9 1.5 < 0.1 < 0.1 0.7 0.7 < 0.1 < 0.1 0.2 0.4 < 0.1 < 0.1
submarginata (Stephens)
Continued
m 2 % m 2 % m 2 %
Procloeon bifidum 1.4 1.2 < 0.1 < 0.1 0.5 0.6 < 0.1 < 0.1 2.3 1.6 < 0.1 < 0.1
Bengtsson
Procloeon pennulatum 0.2 0.4 < 0.1 < 0.1 1.1 1.8 < 0.1 < 0.1 0.7 0.7 < 0.1 < 0.1
Eaton
Serratella ignita (Poda) 76.5 52.0 0.3 0.2 80.4 58.1 0.3 0.2 62.2 50.8 0.2 0.2
Plecoptera
Isoperla grammatica 2.1 1.6 < 0.1 < 0.1 0.5 0.8 < 0.1 < 0.1 0.7 0.7 < 0.1 < 0.1
(Poda)
Leuctra fusca (L.) 9.9 5.7 < 0.1 < 0.1 7.6 4.5 < 0.1 < 0.1 0.5 0.6 < 0.1 < 0.1
Leuctra geniculata 21.0 9.9 0.2 0.1 13.4 5.7 0.2 < 0.1 4.8 3.4 < 0.1 < 0.1
(Stephens)
Perlodes microcephalus 0 0 0 0 0.5 0.8 < 0.1 < 0.1 0 0 0 0
(Pictet)
Odonata
Calopteryx splendens 0.2 0.4 < 0.1 < 0.1 0.2 0.4 < 0.1 < 0.1 0 0 0 0
(Harris)
Cordulegaster boltonii 0.5 0.6 < 0.1 < 0.1 0.2 0.4 < 0.1 < 0.1 0.2 0.4 < 0.1 <0.1
(Donovan)
Hemiptera
Aphelocheirus aestivalis 6.9 3.8 < 0.1 < 0.1 6.3 3.6 < 0.1 < 0.1 2.3 1.4 < 0.1 < 0.1
(Fabricius)
Coleoptera
Brychius elevatus (Panzer) 13.0 9.9 < 0.1 < 0.1 4.8 3.4 < 0.1 < 0.1 3.7 3.4 < 0.1 < 0.1
Deronectes sp. 0.2 0.4 < 0.1 < 0.1 0 0 0 0 0.4 0.7 < 0.1 < 0.1
Elmis aenea (Müller) 33.5 14.8 0.3 0.1 18.9 5.6 0.2 < 0.1 6.2 2.4 0.1 < 0.1
Haliplus haliplus sp. 0.4 0.5 < 0.1 < 0.1 0.2 0.4 < 0.1 < 0.1 0 0 0 0
Haliplus lineatocollis 78.8 43.3 0.6 0.3 23.3 9.9 0.2 < 0.1 20.3 12.0 0.1 < 0.1
(Marsham)
Hydraena riparia 0.2 0.4 < 0.1 < 0.1 0 0 0 0 0 0 0 0
Kugelann
Hydroporinae 0.7 1.4 < 0.1 < 0.1 0 0 0 0 0 0 0 0
Laccobius sp. 15.9 16.2 < 0.1 < 0.1 2.1 2.6 < 0.1 < 0.1 3.2 3.1 < 0.1 < 0.1
Limnius sp. 40.4 17.8 0.5 0.2 16.7 5.7 0.2 < 0.1 6.0 2.6 < 0.1 < 0.1
Limnius volckmari 4.4 2.5 < 0.1 < 0.1 5.8 3.7 < 0.1 < 0.1 1.2 0.9 < 0.1 < 0.1
(Panzer)
Nebrioporus depressus 6.0 4.9 < 0.1 < 0.1 4.1 2.9 < 0.1 < 0.1 9.2 6.0 < 0.1 < 0.1
elegans (Fabricius)
Orectochilus villosus 3.9 1.8 < 0.1 < 0.1 2.3 2.0 < 0.1 < 0.1 1.1 1.2 < 0.1 < 0.1
(Müller)
Oulimnius sp. 132.2 31.4 1.3 0.4 82.3 19.1 0.9 0.2 20.8 6.8 0.3 < 0.1
Oulimnius troglodytes 0.4 0.7 < 0.1 < 0.1 0 0 0 0 0 0 0 0
(Gyllenhal)
Oulimnius tuberculatus 1.4 1.2 < 0.1 < 0.1 0.9 0.9 < 0.1 < 0.1 0.2 0.4 < 0.1 < 0.1
(Müller)
Platambus maculatus (L.) 11.1 6.0 < 0.1 < 0.1 6.0 2.8 < 0.1 < 0.1 5.8 3.2 < 0.1 < 0.1
Potamonectes d. elegans 9.5 6.8 < 0.1 < 0.1 3.3 2.3 < 0.1 < 0.1 6.9 3.7 0.1 < 0.1
(Fabricius)
Riolus cupreus (Müller) 0 0 0 0 0.2 0.4 < 0.1 < 0.1 0 0 0 0
Megaloptera
Sialis lutaria (L.) 10.0 3.9 < 0.1 < 0.1 7.6 3.3 < 0.1 < 0.1 3.0 1.9 < 0.1 < 0.1
Continued
m 2 % m 2 % m 2 %
Trichoptera
Athripsodes albifrons (L.) 0.4 0.5 < 0.1 < 0.1 0.7 0.7 < 0.1 < 0.1 0.2 0.4 < 0.1 < 0.1
Athripsodes cinereus 11.1 4.5 0.1 < 0.1 8.5 3.9 < 0.1 < 0.1 1.2 1.0 < 0.1 < 0.1
(Curtis)
Brachycentrus subnubilus 3.0 2.0 < 0.1 < 0.1 5.8 3.5 < 0.1 < 0.1 5.6 4.6 < 0.1 < 0.1
Curtis
Ceraclea dissimilis 0 0 0 0 0.2 0.4 < 0.1 < 0.1 0.5 0.8 < 0.1 < 0.1
(Stephens)
Drusus annulatus 0.2 0.4 < 0.1 < 0.1 0 0 0 0 0 0 0 0
(Stephens)
Goera pilosa (Fabricius) 1.6 1.6 < 0.1 < 0.1 0.4 0.5 < 0.1 < 0.1 0.5 0.6 < 0.1 < 0.1
Holocentropus sp. 0 0 0 0 0 0 0 0 0.4 0.7 < 0.1 < 0.1
Hydropsyche contubernalis 32.6 13.8 0.3 0.1 37.6 25.2 0.2 < 0.1 12.3 8.1 < 0.1 < 0.1
Mclachlan
Hydropsyche pellucidula 25.4 9.6 0.3 0.1 18.0 6.6 0.2 < 0.1 5.1 2.6 < 0.1 < 0.1
(Curtis)
Hydropsyche siltalai 0.5 0.6 < 0.1 < 0.1 1.2 1.1 < 0.1 < 0.1 0.4 0.5 < 0.1 < 0.1
Dohler
Hydroptila sp. 8.8 6.1 < 0.1 < 0.1 15.9 10.8 0.1 < 0.1 13.8 10.4 < 0.1 < 0.1
Ithytrichia sp. 12.3 6.3 0.1 < 0.1 15.0 6.4 0.2 < 0.1 13.6 7.4 0.2 0.1
Lepidostoma hirtum 18.7 9.6 0.2 0.1 21.3 21.4 0.2 0.1 1.6 1.1 < 0.1 < 0.1
(Fabricius)
Limnephilus lunatus 0 0 0 0 0.2 0.4 < 0.1 < 0.1 0 0 0 0
Curtis
Lype sp. 0.9 1.4 < 0.1 < 0.1 0 0 0 0 0 0 0 0
Molanna angustata Curtis 0.2 0.4 < 0.1 < 0.1 0 0 0 0 0.2 0.4 < 0.1 < 0.1
Mystacides azurea (L.) 0.5 0.8 < 0.1 < 0.1 0.2 0.4 < 0.1 < 0.1 0 0 0 0
Oecetis testacea (Curtis) 0.2 0.4 < 0.1 < 0.1 0 0 0 0 0 0 0 0
Plectrocnemia sp. 1.8 2.9 < 0.1 < 0.1 0 0 0 0 2.1 3.6 < 0.1 < 0.1
Polycentropus 196.1 64.7 2.1 0.7 135.2 46.3 1.5 0.4 39.7 19.0 0.3 0.1
flavomaculatus (Pictet)
Potamophylax latipennis 0.5 0.6 < 0.1 < 0.1 0.4 0.5 < 0.1 < 0.1 0.5 0.6 < 0.1 < 0.1
(Curtis)
Psychomyia pusilla 4.2 2.7 < 0.1 < 0.1 6.2 3.7 < 0.1 < 0.1 1.4 1.1 < 0.1 < 0.1
(Fabricius)
Rhyacophila dorsalis 3.2 2.9 < 0.1 < 0.1 0.9 0.9 < 0.1 < 0.1 0 0 0 0
(Curtis)
Sericostoma personatum 14.8 6.7 0.2 < 0.1 10.9 8.0 0.1 < 0.1 1.9 1.4 < 0.1 < 0.1
(Spence)
Tinodes waeneri (L.) 115.1 51.0 1.3 0.6 128.2 58.7 1.4 0.6 13.9 6.0 0.2 < 0.1
Ylodes conspersus 0.2 0.4 < 0.1 < 0.1 0 0 0 0 0.2 0.4 < 0.1 < 0.1
(Rambur)
Diptera
Antocha vitripennis 6.7 3.7 < 0.1 < 0.1 11.3 5.4 0.1 < 0.1 1.4 1.9 < 0.1 < 0.1
(Meigen)
Atrichopogon sp. 0 0 0 0 0.2 0.4 < 0.1 < 0.1 0 0 0 0
Ceratopogonidae 218.4 54.5 3.1 1.0 187.9 47.5 2.9 1.0 135.4 39.7 2.1 0.6
Chelifera sp. 0.5 0.6 < 0.1 < 0.1 0 0 0 0 1.2 1.2 < 0.1 < 0.1
Chironomini 677.2 120.4 6.4 1.0 971.5 207.4 9.0 1.3 1209.0 316.1 10.1 1.6
Chrysops sp. 0 0 0 0 0.4 0.5 < 0.1 < 0.1 0 0 0 0
Clinocera sp. 3.7 3.6 < 0.1 < 0.1 4.4 2.5 < 0.1 < 0.1 4.2 2.6 < 0.1 < 0.1
Diamesinae (Potthastia) 253.2 152.4 1.6 0.7 493.8 272.2 2.3 0.9 550.8 234.2 2.9 0.9
Dicranota sp. 1.8 1.5 < 0.1 < 0.1 0.9 0.8 < 0.1 < 0.1 0.5 0.6 < 0.1 < 0.1
Continued
m 2 % m 2 % m 2 %
Dolichopodidae 0.2 0.4 < 0.1 < 0.1 0.2 0.4 < 0.1 < 0.1 0.5 0.8 < 0.1 < 0.1
Elaeophila sp. 12.2 5.9 0.1 < 0.1 15.3 6.8 0.1 < 0.1 5.3 2.9 < 0.1 < 0.1
Ephydridae 0 0 0 0 0.4 0.7 < 0.1 < 0.1 0 0 0 0
Gonomyia sp. 0 0 0 0 0 0 0 0 0.2 0.4 < 0.1 < 0.1
Hemerodromia sp. 2.5 1.7 < 0.1 < 0.1 1.4 1.3 < 0.1 < 0.1 4.2 2.0 < 0.1 < 0.1
Ibrisia marginata 0.2 0.4 < 0.1 < 0.1 0.2 0.4 < 0.1 < 0.1 0.5 0.6 < 0.1 < 0.1
(Fabricius)
Limnophora sp. 1.6 1.3 < 0.1 < 0.1 0.7 0.9 < 0.1 < 0.1 0.9 0.9 < 0.1 < 0.1
Limonia sp. 0.2 0.4 < 0.1 < 0.1 0 0 0 0 0 0 0 0
Orthocladiinae 1435.0 746.0 7.8 2.0 2069.3 815.4 11.7 2.3 2206.0 821.2 12.9 2.4
Oxycera trilineata 0 0 0 0 0 0 0 0 0.2 0.4 < 0.1 < 0.1
(Fabricius)
Pericoma trivialis Eaton 1.2 1.1 < 0.1 < 0.1 0.7 0.9 < 0.1 < 0.1 0.7 0.9 < 0.1 <0.1
Pilaria sp. 0 0 0 0 0.2 0.4 < 0.1 < 0.1 1.1 1.0 < 0.1 < 0.1
Prodiamesinae 39.3 22.5 0.3 0.1 34.9 17.0 0.2 < 0.1 41.4 16.3 0.3 0.1
Simuliidae 31.4 15.0 0.3 0.2 26.8 8.3 0.4 0.2 21.0 7.2 0.4 0.3
Tabanus sp. 5.3 2.2 < 0.1 < 0.1 3.7 2.7 < 0.1 < 0.1 4.6 3.3 < 0.1 < 0.1
Tanypodinae 177.9 47.6 1.5 0.4 155.9 43.7 1.3 0.3 199.1 59.7 1.5 0.3
Tanytarsini 1917.4 545.2 13.0 2.7 2212.2 796.7 15.4 3.3 3639.2 1422.1 19.0 4.3
Tipula montium Egger 6.2 2.7 < 0.1 < 0.1 23.8 9.6 0.2 < 0.1 39.5 19.5 0.4 0.2
Tipula sp. 0.5 1.1 < 0.1 < 0.1 0 0 0 0 0.5 0.8 < 0.1 < 0.1
Total abundance (m 2) 12,093 1618 100 12,235 1972 100 12,958 2434 100
APPENDIX B
Tables for repeated-measures ANOVA testing the main effects of drought treatment,
experimental block (between-subject factors) and time (within-subject factor), and their
interactions, on numerical abundance (m 2) of the most numerically abundant core
taxa (a–l).
(a) Gammarus pulex
SS df MS F P Post hoc
Within-subjects
Time 433.30 16 27.27 21.07 < 0.0005
Time drought 65.64 32 2.07 1.60 0.043
Time block 89.71 48 1.88 1.45 0.061
Error (time) 123.38 96 1.29
Between-subjects
Drought 64.21 2 32.10 17.01 0.003 C, LF > HF
Block 85.83 3 28.61 15.16 0.003
Error 11.33 6 1.89
(b) Tubificidae
SS df MS F P
Within-subjects
Time 159.12 20 7.96 37.97 < 0.0005
Time drought 21.68 40 0.54 2.59 < 0.0005
Time block 18.76 60 0.31 1.49 0.195
Error (time) 25.15 120 0.21
Between-subjects
Drought 1.18 2 0.59 0.54 0.608
Block 12.91 3 4.30 3.96 0.072
Error 6.53 6 1.09
(c) Chironomini
SS df MS F P
Within-subjects
Time 186.38 20 9.32 44.94 < 0.0005
Time drought 22.97 40 0.57 2.77 < 0.0005
Time block 18.30 60 0.31 1.47 0.038
Error (time) 24.88 120 0.21
Continued
taxa (a–l).—cont'd
Between-subjects
Drought 4.56 2 2.28 8.54 0.018
Block 3.98 3 1.33 4.97 0.046
Error 6
(d) Tanytarsini
SS df MS F P
Within-subjects
Time 551.51 20 27.58 52.04 < 0.0005
Time drought 43.85 40 1.10 2.07 0.001
Time block 27.30 60 0.46 0.86 0.742
Error (time) 63.59 120 0.53
Between-subjects
Drought 1.08 2 0.54 0.62 0.571
Block 5.46 3 1.82 2.08 0.204
Error
(e) Orthocladiinae
SS df MS F P
Within-subjects
Time 859.70 12 71.64 30.72 < 0.0005
Time drought 113.16 24 4.72 2.02 0.012
Time block 115.51 36 3.21 1.38 0.125
Error (time) 167.92 72 2.33
Between-subjects
Drought 21.68 2 10.84 6.60 0.031
Block 19.64 3 6.55 3.98 0.071
Error
(f) Naididae
SS df MS F P
Within-subjects
Time 743.91 20 37.20 27.15 < 0.0005
Time drought 82.73 40 2.07 1.51 0.046
Time block 159.69 60 2.66 1.94 0.001
Error (time) 164.41 120 1.37
Between-subjects
Drought 77.23 2 38.61 6.48 0.032
Block 12.87 3 4.29 0.72 0.575
Error
(g) Potamopyrgus antipodarum

SS df MS F P
Within-subjects
Time 430.30 19 22.78 15.49 < 0.0005
Time drought 98.19 38 2.60 1.77 0.011
Time block 120.62 57 2.13 1.45 0.049
Error (time) 166.65 113 1.47
Between-subjects
Drought 112.18 2 56.09 1.81 0.243
Block 16.06 3 5.35 0.17 0.911
Error 185.89 6 30.98
(h) Radix balthica

SS df MS F P
Within-subjects
Time 728.65 20 36.43 27.27 < 0.0005
Time drought 122.06 40 3.05 2.28 < 0.0005
Time block 138.34 60 2.31 1.73 0.006
Error (time) 160.32 120 1.34
Between-subjects
Drought 41.60 2 20.80 10.96 0.010
Block 101.96 3 33.99 17.90 0.002
Error 11.39 6 1.90
(i) Pisidium sp.

SS df MS F P
Within-subjects
Time 483.63 20 24.18 16.86 < 0.0005
Time drought 127.09 40 3.18 2.22 < 0.0005
Continued
Time block 83.06 60 1.38 0.97 0.553

Error (time) 172.13 120 1.43
Between-subjects
Drought 117.38 2 58.67 6.19 0.035
Block 105.01 3 35.00 3.69 0.081
Error 6
(j) Diamesinae
SS df MS F P
Within-subjects
Time 1367.90 20 68.40 40.67 < 0.0005
Time drought 141.94 40 3.55 2.11 0.001
Time block 182.58 60 3.04 1.81 0.003
Error (time) 201.83 120 1.68
Between-subjects
Drought 73.84 2 36.92 14.73 0.005
Block 27.47 3 9.16 3.65 0.083
Error 15.04 6 2.51
(k) Ceratopogonidae
SS df MS F P Post hoc
Within-subjects
Time 639.25 20 31.96 23.40 < 0.0005
Time drought 67.21 40 1.68 1.23 0.196
Time block 144.76 60 2.41 1.77 0.004
Error (time) 163.92 120 1.37
Between-subjects
Drought 21.33 2 10.67 41.81 < 0.0005 C > LF, HF
Block 7.76 3 2.59 10.14 0.009
Error 1.53 6 0.26
(l) Polycentropus flavomaculatus

SS df MS F P
Within-subjects
Time 651.44 20 32.57 17.03 < 0.0005
Time drought 171.88 40 4.30 2.25 < 0.0005
Time block 113.82 60 1.90 0.99 0.504
Error (time) 229.49 120 1.91

Between-subjects
Drought 178.33 2 89.17 19.01 0.003
Block 11.69 3 3.90 0.83 0.524
Error 28.14 6 4.69
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Environmental Warming in
Shallow Lakes: A Review of
Potential Changes in Community
Structure as Evidenced from
Space-for-Time Substitution
Approaches
Mariana Meerhoff*,{,{,1, Franco Teixeira-de Mello*, Carla Kruk},},
Cecilia Alonso||, Iván González-Bergonzoni*,{, Juan Pablo Pacheco*,
Gissell Lacerot||, Matías Arim*,#,**, Meryem Beklioğlu{{,
Sandra Brucet{{, Guillermo Goyenola*, Carlos Iglesias*,
Néstor Mazzeo*,{, Sarian Kosten}},}}, Erik Jeppesen{,||||,##
*Departamento de Ecologı́a y Evolución, Centro Universitario Regional Este (CURE), Facultad de Ciencias,
Universidad de la República, Burnett s/n, Maldonado, Uruguay
{
Department of Bioscience, Aarhus University, Vejlsvej, Silkeborg, Denmark
{
South American Institute for Resilience and Sustainability Studies (SARAS), Maldonado, Uruguay
}
Laboratory of Ethology, Ecology and Evolution, Instituto de Investigaciones Biológicas Clemente Estable,
Italia, CP 11600, Montevideo, Uruguay
}
Ecologı́a Funcional de Sistemas Acuáticos, Limnologı́a, IECA, Facultad de Ciencias, Universidad de la
República, Iguá, CP 11400, Montevideo, Uruguay
‖
Ecologı́a Funcional de Sistemas Acuáticos, Centro Universitario Regional Este (CURE), Universidad de la
República, Ruta 9, km 204, Rocha, Uruguay
#
Facultad de Ciencias, Universidad de la República, Iguá, CP 11400, Montevideo, Uruguay
**Center for Advanced Studies in Ecology and Biodiversity (CASEB), Depto. de Ecologı́a, Facultad de Ciencias
Biológicas, Pontificia Universidad Católica, CP 6513677, Santiago, Chile
{{
Department of Biology, Limnology Laboratory, Middle East Technical University, Üniversiteliler Mahallesi,
Dumlupınar Bulvarı, Çankaya, Ankara, Turkey
{{
European Commission, Joint Research Centre, Institute for Environment and Sustainability, Ispra, Italy
}}
Department of Aquatic Ecology and Water Quality Management, Wageningen University, Wageningen,
The Netherlands
}}
Leibniz-Institute of Freshwater Ecology and Inland Fisheries (IGB), Berlin/Neuglobsow, Germany
‖‖
Greenland Climate Research Centre (GCRC), Greenland Institute of Natural Resources, Kivioq, P.O. Box
570 3900, Nuuk, Greenland
##
Sino-Danish Centre for Education and Research (SDC), Beijing, China
1
Corresponding author: e-mail address: mm@dmu.dk; merluz@fcien.edu.uy

http://dx.doi.org/10.1016/B978-0-12-396992-7.00004-6
260 Mariana Meerhoff et al.
Contents
1. Introduction 261
1.1 Global change and freshwater communities 261
1.2 Shallow lakes and ecosystem responses to changes in temperature 262
1.3 Indirect effects of climate on community structure through availability of
nutrients 265
1.4 Theoretical predictions 266
1.5 Space-for-time substitution approach 273
2. Findings in Space-for-Time Studies 278
2.1 Richness changes with climate 278
2.2 Climate effects on biomass 283
2.3 Climate effects on density 290
2.4 Climate effects on body size and size structure 295
2.5 Climate effects on reproduction and growth 299
2.6 Climate effects on intensity of trophic interactions 303
3. Discussion 306
3.1 Can we predict changes in community traits with warming? 306
3.2 Advantages and disadvantages of the SFTS approach 316
3.3 Topics for further research 319
Appendix A. Periphyton Latitudinal Gradient 322
Appendix B. Bacterioplankton Latitudinal Gradient 325
Appendix C. Phytoplankton Unpublished Data and Latitudinal Gradient 327
C.1 Previously unpublished data: The Netherlands–Uruguay comparison 327
C.2 Latitudinal gradient meta-analysis 328
References 330
Abstract
Shallow lakes, one of the most widespread water bodies in the world landscape, are very
sensitive to climate change. Several theories predict changes in community traits, rel-
evant for ecosystem functioning, with higher temperature. The space-for-time substi-
tution approach (SFTS) provides one of the most plausible empirical evaluations for
these theories, helping to elucidate the long-term consequences of changes in climate.
Here, we reviewed the changes at the community level for the main freshwater taxa
and assemblages (i.e. fishes, macroinvertebrates, zooplankton, macrophytes, phyto-
plankton, periphyton and bacterioplankton), under different climates. We analyzed data
obtained from latitudinal and altitudinal gradients and cross-comparison (i.e. SFTS) stud-
ies, supplemented by an analysis of published geographically dispersed data for those
communities or traits not covered in the SFTS literature.
We found only partial empirical evidence supporting the theoretical predictions.
The prediction of higher richness at warmer locations was supported for fishes, phyto-
plankton and periphyton, while the opposite was true for macroinvertebrates and zoo-
plankton. With decreasing latitude, the biomass of cladoceran zooplankton and
periphyton and the density of zooplankton and macroinvertebrates declined (opposite
for fishes for both biomass and density variables). Fishes and cladoceran zooplankton
Space-for-Time Approach and Warming in Shallow Lake Communities 261
showed the expected reduction in body size with higher temperature. Life history
changes in fish and zooplankton and stronger trophic interactions at intermediate po-
sitions in the food web (fish predation on zooplankton and macroinvertebrates) were
evident, but also a weaker grazing pressure of zooplankton on phytoplankton occurred
with increasing temperatures. The potential impacts of lake productivity, fish predation
and other factors, such as salinity, were often stronger than those of temperature itself.
Additionally, shallow lakes may shift between alternative states, complicating theoretical
predictions of warming effects. SFTS and meta-analyses approaches have their shortcom-
ings, but in combination with experimental and model studies that help reveal mecha-
nisms, the “field situation” is indispensable to understand the potential effects of warming.
1. INTRODUCTION
1.1. Global change and freshwater communities
Anthropogenic impacts on natural ecosystems are increasing apace in both the
terrestrial and aquatic (both freshwater and marine) realms, and environmental
stressors, such as climate change, threaten to alter community structure and eco-
system functioning from local to global scales (Hagen et al., 2012; Ledger et al.,
2012; Mintenbeck et al., 2012; Mulder et al., 2012). The Millennium Ecosystem
Assessment (2005) has quantified existing and projected deterioration or loss of
natural ecosystems through the intensification of agriculture, urbanization and
other anthropogenic impacts that are likely to have significant impacts on
most of the terrestrial ecosystems on Earth by the year 2070. The key global
drivers include climate warming, changes in precipitation patterns, land
use changes (Vitousek, 1994), increasing atmospheric CO2 concentrations
(Rockström et al., 2009), and alterations in the global nitrogen cycle and
global fertilization of ecosystems (Galloway et al., 2008; Gruber and
Galloway, 2008). Invasive species (Walther et al., 2009) and decreasing
biodiversity due to habitat loss and rising water demands (Vörösmarty et al.,
2000) are among the most widely reported biological responses to these
changes (Parmesan and Yohe, 2003).
The impacts of environmental warming, although increasingly recognized
as a key component of climate change following the recent reports from the
Intergovernmental Panel on Climate Change (IPCC, 2007), and a growing
number of ecological studies, are still poorly understood at the higher (mul-
tispecies) levels of biological organization. It is recognized, however, that its
impacts are expected to be strongest at high altitude and high latitudes
(Phoenix and Lee, 2004; Rouse et al., 1997; Smol et al., 2005; Woodward
et al., 2010a,b). Large parts of the polar regions, particularly the Arctic, are
expected to show a much faster increase in the mean annual temperature
than lower latitudes (Howard-Williams et al., 2006).
Temperature affects a myriad of biological processes, including individual

growth and respiration rates (potentially affecting primary production and com-
munity respiration, e.g. Yvon-Durocher et al., 2010), changes in life history
traits, changes in phenology and trophic dynamics, with potential temporal
or spatial mismatches arising between prey availability and consumer demands
(e.g. Winder and Schindler, 2004). Species may not respond with the same
strength or synchronously in time, since they are affected not only by changes
in temperature but also by other environmental factors, such as changes in pho-
toperiod (Winder and Schindler, 2004). However, after accounting for size de-
pendence, temperature explains the largest amount of variation in almost all
biological rates (Brown et al., 2004; Peters, 1983). Given sufficient resource
availability, increasing temperatures generally accelerate growth and
development rates of individual organisms (Forster et al., 2011b), although
changes in absolute abundances may be species specific or ecosystem specific
(Adrian et al., 2006; Blenckner et al., 2007; Reist et al., 2006).
Warming may also contribute to changes in the latitudinal or altitudinal
distributional range of some species, thus likely affecting diversity and com-
munity structure. Stenothermal species (narrow thermal range) will most
probably shift range or become locally extinct, whereas eurythermal species
(wide thermal range) will likely be able to adapt to new thermal regimes
(Lappalainen and Lehtonen, 1997; Woodward et al., 2010a,b). The
already observed and the predicted changes in global and regional
temperatures make understanding warming effects on ecological
communities a priority (Moss et al., 2009; Petchey et al., 2010).
However, the effects of temperature on many aspects of community
structure, such as the distribution of diversity and biomass across trophic
levels, or the extent and distribution of specialism and generalism across
species, are still poorly understood (Petchey et al., 2010; Woodward
et al., 2010b).
1.2. Shallow lakes and ecosystem responses to changes in

temperature
Shallow lakes (typically polymictic, maximum depth ca. <5 m) are partic-
ularly strongly affected by human activity, as they are key providers of critical
ecosystem services that underpin aquaculture, crop irrigation and drinking
water supply. Besides being one of the most common and widespread inland
water bodies in the world landscape (Downing et al., 2006), these lakes rep-
resent one of the ecosystem types most rapidly affected by external pertur-
bations, including climate change (Jeppesen et al., 2009; Moss et al., 2009).
Shallow lakes are typically isolated and fragmented in the landscape and are
extremely sensitive to climate variability such as evaporation and
precipitation balances, since they have a very large surface:volume ratio
(Coops et al., 2003), which affects the persistence of climatic signatures.
Lake depth and hydrologic residence time, together with stratification
and mixing regime, are also physical features that interact to control the
duration and strength of climate signals, for instance, in water
temperature (Blenckner, 2005). In deep lakes, the winter climate signal
(as described, for instance, by the winter North Atlantic Oscillation
index, NAO, in the Northern Hemisphere) can persist until late summer,
whereas in shallow lakes, the winter temperature signal lasts for much
shorter time (Gerten and Adrian, 2001). Identification of climate signals
in current measurements may thus be difficult due to time-lags arising
from the action of other processes at different scales.
Most lakes are also commonly affected by multiple interacting stressors
(Christensen et al., 2006; Yan et al., 2008), potentially confounding the
detection of signals due to climate change. Freshwater systems, not least
shallow lakes, are subject to increasing deterioration processes in many parts
of the world (Feld et al., 2011; Friberg et al., 2011; Hladyz et al., 2011;
Moss, 1998; Moss et al., 2011). These include wetland area loss, local
extinction of native species and introduction of exotic species, acidification,
water level changes due to water extraction or canalization and, especially,
eutrophication (nutrient enrichment in the water bodies), among the major
drivers of global change that aquatic ecosystems are currently facing
(reviewed in, e.g. Carpenter et al., 1998; Dodds, 2007; Friberg et al., 2011;
Schindler, 2006; Smith, 2003). While some shallow lakes and ponds might
simply dry out (Beklioğlu et al., 2007), the lower water level will often
concentrate pollutants, enhance resuspension and, together with the higher
temperature, amplify the sediment release of nutrients, especially of
phosphorus (McKee et al., 2003; Özen et al., 2010). Under increasing
precipitation, in contrast, the runoff of nutrients from the catchments may
increase (Jeppesen et al., 2009, 2011; Özen et al., 2010). An amplification
of eutrophication symptoms by climate warming seems to occur also by
changes in trophic dynamics and interactions (Meerhoff et al., 2007a) and
shifts in fish community structure (Jeppesen et al., 2010a) and population
size structure (Daufresne et al., 2009). As a consequence, the likelihood of
dominance of nuisance phytoplankton taxa, such as cyanobacteria and
filamentous algae, may rise (Jeppesen et al., 2009; Kosten et al., 2011a;
Mooij et al., 2005; Paerl and Huisman, 2009; Trochine et al., 2011).
The interaction of climate signals with nutrient enrichment symptoms

has been addressed by several studies based on palaeolimnological records
(Bjerring et al., 2009), mesocosm experiments (e.g. Moss et al., 2004 and
references herein), latitudinal gradient analysis (Kosten et al., 2009b and ref-
erences herein) and synthesis papers (Jeppesen et al., 2010a, 2011; Moss,
2010; Moss et al., 2011). However, disentangling the specific effects of
environmental warming from nutrient enrichment (as well as from other
global changes) is crucial if we are to further our understanding of the
responses of freshwater ecosystems to a changing climate and contribute
to their conservation with adequate mitigation measures. The interactive
effects of warming and other global changes and the indirect impacts on
community structure, food web functioning and ecosystem processes are
even far less well known (Montoya and Raffaelli, 2010; Woodward et al.,
2010b).
The influence of the catchment on within-lake processes can vary
depending on land use, the regional climate and geographical location.
However, shallow lakes are especially complex due to their numerous inter-
nal feedbacks. Shallow lakes may respond differently from other aquatic sys-
tems to external perturbations or stressors, given the recognized potential for
them to shift between alternative states over an intermediate range of nutri-
ent concentrations, in a typical hysteresis process (Moss et al., 1996; Scheffer
et al., 1993, 2001): such extreme regime shifts seem far less prevalent in many
running waters, which appear to be far more stable in the face of
perturbations or stressors in general (Layer et al., 2010, 2011; Ledger
et al., 2012). Biological and physicochemical mechanisms related to the
presence or absence of macrophytes and water turbidity maintain either
state via a range of positive feedbacks. The stability of such alternative
states has been challenged by recent studies conducted in other regions of
the globe than the temperate zone (Jeppesen et al., 2007; Kosten et al.,
2011a; Meerhoff et al., 2007a), which was the birth place of this
theoretical framework, suggesting that they might be modulated by
climatic influences. Similar to enhanced nutrient loading, changes in
water level, enhanced temperature and longer growing season have been
identified as potential weakening factors that may trigger a change from a
clear water, macrophyte-dominated state to undesirable states (Beklioğlu
et al., 2006) involving the dominance by free-floating plants (Scheffer
et al., 2003) or filamentous green algae (Trochine et al., 2011). The
hysteresis phenomenon complicates our ability to make predictions for
the response of a specific community, not least at ecosystem level, to
changing temperatures, as several community and food web configurations

may occur under similar environmental conditions.
1.3. Indirect effects of climate on community structure through

availability of nutrients
Trends extracted from latitudinal gradient or cross-comparison analyses are
based on correlative data. This may render it difficult to disentangle strict
climate signals from potential indirect effects of climate and human-related
impacts (such as nutrient enrichment and salinization through cultivation,
e.g. Bjerring et al., 2009). An increase in nutrient loading may determine
a series of important changes in community traits in shallow lake commu-
nities. For instance, changes in fish community composition, biomass and
body size structure, with non-random loss of predatory species (due to in-
creased turbidity and lower concentrations or larger variations in dissolved
oxygen), occur worldwide with eutrophication (Jeppesen et al., 2005).
Large increases in nutrient concentrations due to eutrophication thus affect
lake trophic webs, from the basal resources to the top predators.
Both the absolute and relative concentrations of nutrients in the water
column are essential for the development of phytoplankton communities,
as they affect both total biomass and composition. A warmer climate can af-
fect the identity of the limiting nutrient and the availability of nutrients to
primary producers: for instance, higher denitrification under warmer con-
ditions could lead to nitrogen limitation (Lewis, 1996, 2000). There are
conflicting observations as to which is the main limiting nutrient across
different climates. In cross-comparison mesocosm experiments on
nutrient and fish addition under different temperatures, the nature of the
limiting nutrient varied between temperate and tropical systems (Danger
et al., 2009). Addition of phosphorus (P) favoured phytoplankton in
temperate lakes, while nitrogen (N) had positive effects in tropical
mesocosms, and water N:P ratios tended to be higher in the tropical than
in the temperate experiment. However, several latitudinal gradient studies
show no clear consistent differences in N or P limitation across large
spatial scales in terms of nutrient ratios and chlorophyll-a:nutrient
relationships, among other indicators (Huszar et al., 2006; Kosten et al.,
2009b; Mazumder and Havens, 1998). Kosten et al. (2011b) showed that
while total phosphorus (TP) explained most of the variance in
phytoplankton chlorophyll-a (Chl-a) in the cool region of South
America, total nitrogen (TN) explained most of the variance in the
intermediate and warm regions. A recent work based on an extensive
meta-analysis of various ecosystems has shown equivalence in N and P

limitation in freshwater ecosystems and synergistic effects of N and P
enrichment (i.e. co-limitation) (Elser et al., 2007). These authors found
only a weak negative correlation between latitude and the positive
response of primary producers to enrichment in N, but not in P. In
summary, our review of nutrient limitation among different climates in
the space-for-time substitution (SFTS) approach literature shows no clear
or consistent pattern.
1.4. Theoretical predictions

Changes in temperature, due to both anthropogenic activities and natural
temperature variations, are a main determinant of community structure
and ecosystem processes, via the direct effects on the metabolic demands
of individuals and the attendant changes in the distribution of body sizes
of organisms (Arim et al., 2007; Charnov and Gillooly, 2004; Forster
et al., 2011a,b; Gillooly, 2000; Yvon-Durocher et al., 2011a). The
metabolic theory of ecology (hereafter, MTE) considers the effects of
both body size and environmental temperature on relevant ecological
rates and patterns (Brown et al., 2004). MTE, and other physiologically
based theories relating environmental temperature with organisms’
performance and community function, provides the basis for predictive
analysis of the effect of climate warming on ecosystems (e.g. Angilletta,
2009; Karasov and Martı́nez del Rio, 2007; McNab, 2002; Perkins et al.,
2010; Yvon-Durocher et al., 2010). The MTE is based on a set of
empirical generalizations about scaling of biological rates with body size
(Brown et al., 2004; Peters, 1983), a mechanistic explanation for this
scaling (West et al., 1997) and its response to changes in temperature
(Dell et al., 2011; Gillooly et al., 2001; Huey and Kingsolver, 2011). This
theory remains at the centre of a heated debate (Brown et al., 2005;
Etienne et al., 2006; Forster et al., 2011b; Kozlowski and Konarzewski,
2004; Reiss et al., 2010). Nonetheless, despite some deviations from
general expectations (e.g. Algar et al., 2007; Caruso et al., 2010), the
predictive potential of this ecological theory, which is based on basic
principles of biology and kinetics, is notable (e.g. Weber et al., 2011).
MTE quantitatively predicts changes in species (or higher taxa) richness
due to changes in environmental temperature and in the mean body size of
the individuals composing local communities (Allen et al., 2002; Brown
et al., 2004). This theory predicts an increase in richness with temperature
(specifically, a linear relationship between the logarithm of species richness

and the inverse of temperature, Allen et al., 2002) (Fig. 1, Table 1). The
detection of some degree of curvilinear association between these
variables in invertebrate and vertebrate ectotherms could be considered as
a limitation of the theory or as an area in which further theoretical
advances are needed (Algar et al., 2007). Considering the possible change
in species body size and in metabolic rates due to changes in temperature,
several predictions can be made.
From a population perspective, the carrying capacity, the growth rates,
the incidence among local populations, and the geographic range of species
could be potentially affected by temperature. A basic determinant of a
population’s carrying capacity is the relationship between the demands of
individuals and the availability of resources (Damuth, 1981). The effect
of temperature on the demands of an individual predicts a displacement
of the density–mass relationship, as well as of the biomass distribution
(e.g. Brown et al., 2004). These displacements take place because the rise
in energetic demands with increasing temperature determines that the same
amount of resources is divided among individuals that require more from the
environment; consequently, fewer individuals can satisfy their demands
and a decrease in density and total biomass is expected (Fig. 1, Table 1).
However, if the amounts of available resources and/or predation strength
depend on body size and temperature, changes in the slope and modes of
the size distribution could also be expected (see Arim et al., 2011; Brown
et al., 2004). In addition to these changes in the carrying capacity of
species, population dynamics could also be affected since the maximum
growth rate is expected to increase with temperature (Brown et al.,
2004). In this sense, the rise in temperature could lead to less abundant
and more variable populations (e.g. Beisner et al., 1997) with more
frequent local extinction, affecting metapopulation dynamics and the
fraction of local habitats occupied by the species (Hanski, 1999).
A causal connection between temperature and body size has long been
recognized (reviewed by Angilletta, 2009; Kingsolver and Huey, 2008),
and Bergmann’s rule, now more than 160 years old, is one of the first
empirical generalizations about ecological patterns (Gaston and Blackburn,
2000) and still plays a central role in biogeography (Olalla-Tárraga, 2011).
It states that organisms from higher latitudes have large body sizes in
comparison with individuals of the same species, related species or
assemblages inhabiting lower latitudes (Olalla-Tárraga et al., 2010) (Fig. 1,
solid line). This trend was conceived for endotherms that obtain a
Theory pred. Fish Invertebrates Zooplankton Phytoplankton Periphyton Bacteria
25 A 25 B 30 C 100 D 350 E 35 F
Cyclopoidea
Calanoidea
Richness
Cladocera
10
FW
n = 69 Bk n = 23 n = 43
1
8 G H 1600 I 300 J 2 K 16,000 L

a
a
Biomass
No latitudinal
gradient data n = 290
b
n = 41 b n = 101 n = 33
c
250 M 35,000 N 3 O P Q 1e+9 R

Density
Typically not shown Typically not measured
FW FW
Bk Bk n = 25 1e+4 n =133
5 S T 1.6 U V W 0.12 X
Body size
Not enough data Typically not shown Typically not shown
FW North
Bk 0.4 South n =48
High Low
Temperature Latitude gradient (0–90)
Figure 1 Theoretical expectations and most representative empirical trends in main traits of different communities of shallow lakes along a
latitude gradient, as found in space-for-time substitution studies or built on meta-analysis. See Table 1 for a summary of the respective units
and references from which data were extracted, and respective Appendixes for the meta-analyses. From right to left: theoretically predicted
relationships (solid lines: most supported trend, dashed line: alternative expected trend, see Section 1), fish, macroinvertebrates, zooplankton,
phytoplankton, periphyton and bacterioplankton, and from top to bottom: richness, biomass, density and body size, indicating the maximum
scale value on each y-axis, the significant relationships (indicated by a line or an * where appropriate) and the reasons for empty panels.
Macrophytes were excluded due to lack of data on all traits. Data on proximate latitudes were averaged and shown as mean value for that
latitude range, in the case of fish biomass data (extracted from Gyllström et al., 2005) after removing the lowest phosphorus values from the
analysis in order to have a comparable range among climate zones. To calculate zooplankton dry weight, we used a conversion factor of 48%
to transform mg C L 1 to mg DW L 1 (Hessen, 1989). Phytoplankton biomass box-plots show mean, mean 1 SE, mean 1 SD and extreme
values. The letters in the right corner of the panels are used for identification in the main text. When shown, error bars correspond to 1 stan-
dard error. Codes: Bk ¼ brackish lakes, FW ¼ freshwater lakes.
Table 1 Summary of the data (variables and units) and respective references describing patterns of changes in main community traits along a
latitudinal gradient, shown in Fig. 1
Richness Biomass Density Body size
Theoretical log(s) ¼ ( E/1000k) W [R] M1/4eE/kT K [R] M3/4 eE/kT See text for explanation
predictions (1000/T ) þ C1 [R]: Supply rate of limiting
C1: constant, k: resource
Boltzmann’s
constant, E:
activation energy
Allen et al. (2002) Brown et al. (2004) Brown et al. (2004) Gardner et al. (2011),
Marquet and Taper
(1998), and Olalla-
Tárraga and Rodrı́guez
(2007)
Fish Species number CPUE (kg net 1 night 1) ind m 2 cm (standard length)
González- Gyllström et al. (2005) Brucet et al. (2010) and Brucet et al. (2010) and
Bergonzoni et al. Teixeira-de Mello et al. Teixeira-de Mello et al.
(2012) (2009) (2009)
Macroinvertebrates Taxa number No data ind m 2 No data
Brucet et al. (2012) Brucet et al. (2012) and
and Meerhoff et al. Meerhoff et al. (2007a)
(2007a)
Continued
Table 1 Summary of the data (variables and units) and respective references describing patterns of changes in main community traits along
a latitudinal gradient, shown in Fig. 1—cont'd
Richness Biomass Density Body size
Zooplankton Genera number mg dry weight L- 1 ind L 1 (cladocerans) mm (cladocerans)
(cladocerans and (total zooplankton)
copepods)
Brucet et al. (2010), Gyllström et al. (2005), Havens Hansson et al. (2007), Gillooly and Dodson
Meerhoff et al. et al. (2007), Jackson et al. (2007), Meerhoff et al. (2007a), (2000)
(2007b), and Pinto- Pinto-Coelho et al. (2005), and Meerhoff et al. (2007b), and
Coelho et al. (2005) Vakkilainen et al. (2004) Pinto-Coelho et al. (2005)
Phytoplankton Species number mg Chl-a L 1 No data No data
Stomp et al. (2011) Meta-analysis: Danger et al. (2009),
Ganf (1974), Kalff and Watson
(1986), Kruk et al. (2011), and
Melack (1976, 1979) plus all
references in Table 3
Periphyton Species number log mg Chl-a cm 2 No data No data
Analysis of metadata. Analysis of metadata. Appendix A
Appendix A
Bacterioplankton DGGE bands mg C L 1 cells ml- 1 mm3
Analysis of metadata. Analysis of metadata. Appendix B Analysis of metadata. Analysis of metadata.
Appendix B Appendix B Appendix B
The equations for the theoretical predictions and their respective references are also shown, while the references used to extract data for meta-analyses are presented in
Appendixes. Most data were recalculated or redrawn from the original literature, except the figure from Gillooly and Dodson (2000), republished with kind permission
from the Association for the Sciences of Limnology and Oceanography (copyright 2000) and the figure from Stomp et al. (2011), republished with kind permission from
the authors (copyright 2011). Abbreviation DGGE, denaturing gradient gel electrophoresis
thermoregulatory benefit by the reduction in the area:volume ratio at larger

masses (at high latitudes and thus cold conditions). However, several
mechanisms were proposed to account for latitudinal trends in the body
size of endo and ectothermic species, focusing on the effects of resource
availability and thermoregulation (reviewed by Watt et al., 2010).
The “heat balance hypothesis” predicts either an increase or a reduction in
body size depending on the original size and thermal biology of a given species
(Olalla-Tárraga, 2011). Individuals are typically active at a range of body temper-
atures that could be achieved by different mechanisms (McNab, 2002).
Thermoconformers, for instance, are those animals that match to their environ-
mental temperature, in contrast to thermoregulators that maintain a nearly con-
stant body temperature via behavioural (ectotherms) or physiological
(endotherms) mechanisms (see Angilletta, 2009; McNab, 2002). Among
thermoconformers, a reverse Bergmann’s pattern is expected to reduce
heating times in smaller organisms (Olalla-Tárraga and Rodrı́guez, 2007).
The body temperature of thermoconformers closely fluctuates with ambient
temperature with a heating time proportional to body size, being unable to
accelerate the heating process. As consequence, large individuals in colder
environments have a short activity window (e.g. to forage) while the reduced
available energy compromises their viability and, therefore, small individuals
might be favoured (see Olalla-Tárraga and Rodrı́guez, 2007). Small
ectothermic thermoregulators, however, would become larger at lower
temperatures to increase heat conservation (from Olalla-Tárraga, 2011)
(Fig. 1, dashed vs. solid lines, respectively). The existence of size thresholds
and potential range limits of body size for these processes to occur are not yet
defined. While originally focused on amphibians, this hypothesis has the
potential to explain observed patterns in fishes (Belk and Houston, 2002;
Blanck and Lamouroux, 2007), invertebrates (Blanckenhorn and Demont,
2004) and ectotherms in general (Olalla-Tárraga and Rodrı́guez, 2007), all of
which dominate the fauna of shallow lakes and freshwaters in general.
A common empirical generalization is the “temperature-size rule”, a
widely recognized phenomenon, according to which ectothermic individ-
uals growing at lower temperature reach larger body sizes (Angilletta, 2009;
Forster et al., 2011a,b; Kingsolver and Huey, 2008). This process prevails
independently of thermoregulatory behaviour and has been reported for
unicellular and multicellular organisms, and may arise due to differential
thermal responses of development and growth rates, which are not
addressed by the MTE (Forster et al., 2011a,b). From Bergmann’s rule,
MTE and the “temperature-size rule”, it is thus expected that for several,
not necessarily exclusive reasons, warming will promote changes in body

size (Gardner et al., 2011) although the direction of change will vary
depending, among other factors, on the thermal biology of the organisms.
Some macroecological approaches also support a change in body size not
only within, but also among, species with global warming. Individual fitness
may be summarized, from an energetic perspective, by two processes
(Brown et al., 1993), namely, the acquisition of energy from the environ-
ment and the transformation of this energy into progeny. While energy ac-
quisition increases with an increase in body size, the individual potential to
produce offspring decreases. From the balance between these two processes,
an optimum body size requiring less energy to survive in a given environ-
ment is expected (Marquet and Taper, 1998; Marquet et al., 2008). In this
sense, population viability is determined by the balance between individual
energetic demands and the availability of energy in the environment,
determining constraints to the maximum and minimum body sizes in local
communities (see Marquet and Taper, 1998; Marquet et al., 2008). Based
on this energetic context, small species could experience a selection for
larger sizes under a relative reduction in the supply–demand balance,
whereas the opposite is true for large-bodied species (Marquet and Taper,
1998; Marquet et al., 2008). Specifically, when the resource availability:
demands ratio is reduced (e.g. after an increase in temperature), the
maximum and minimum size constraints become stronger and the smaller
species experience a selection pressure towards larger sizes, while the
opposite occurs for larger species (Brown et al., 1993; Marquet and Taper,
1998; Marquet et al., 2008). Within this framework, the optimum body
sizes represent a threshold between positive and negative trends in response
to changes in environmental conditions (Brown, 1995; Brown et al., 1993;
Marquet and Taper, 1998; Marquet et al., 2008). The body size
distributions expected from this theory have been evaluated in mammals,
birds (e.g. Marquet and Taper, 1998) and fishes (Fu et al., 2004; Knouft,
2004; Knouft and Page, 2003; Rosenfield, 2002).
Trophic interactions may also be affected by temperature in several other
ways. The rise in energetic demands with temperature could involve more
consumption events (McNab, 2002), an increase in the range of prey con-
sumed and an increase in spatial movements to capture the prey (Petchey
et al., 2010; Pike, 1984; Schoener, 1974). In addition, it has been
proposed that community food chain length and species trophic position
can be negatively associated with environmental temperature (Arim et al.,
2007). Temperature might also indirectly affect biotic interactions by
altering the final body size of adults and the time elapsed to achieve this size
(Forster et al., 2011a,b). Size refugia from predation is a common
phenomenon in aquatic environments (Chase, 1999), where gape-limited
predation is prevalent (Gilljam et al., 2011; Woodward et al., 2010c).
Smaller prey will likely be more frequently preyed upon at higher
temperatures, while smaller predators might face a reduction in the total
amount of available resources (Arim et al., 2010, 2011). The relative rate
of variation in predator and prey sizes will determine the strength of this
effect. These changes in species richness, food chain length, frequency
and intensity of trophic interactions, and consequently in connectivity,
have a significant potential to alter food webs and create changes in
community structure and stability, and ecosystem functioning (Dunne
et al., 2002; Fox and McGrady-Steed, 2002; May, 1972; McCann, 2000;
Petchey et al., 2010). Contradictory results of models on the responses of
community traits and food web metrics to increasing temperatures (such
as connectance, Petchey et al., 2010) highlight the need for more and
better empirical data to parameterize models, test predictions and produce
models of mechanistic effects of temperature change on interspecific
interactions, especially in freshwater ecosystems.
1.5. Space-for-time substitution approach

Various methods have been used to investigate the potential effects of global
change in natural systems. In particular, a large battery of approaches is used to
study the effects of climate warming on shallow lakes, including warming ex-
periments at different scales, from individual-species responses to increased
temperature to larger field scale experiments where temperature and associated
climate factors are drivers (e.g. Feuchtmayr et al., 2009; Liboriussen et al.,
2005; McKee et al., 2002a,b; Netten et al., 2010; Yvon-Durocher et al.,
2011a), palaeolimnological surveys (e.g. Smol et al., 2005), long-term
contemporary surveys (e.g. Adrian et al., 2006; Winder and Schindler,
2004) and mathematical models (e.g. Mooij et al., 2007; Trolle et al., 2011).
Another research approach to study the potential impacts of climate
warming on ecosystems is the so-called SFTS (Pickett, 1989). The origins
of this approach, although not meant to analyze biological responses to
climate change, can be traced back to the end of the XVIII century with
the studies of von Humboldt and Bonpland, who after latitudinal and alti-
tudinal gradient studies in South America suggested that temperature and
precipitation played a key role in the spatial distribution of vegetation
(Von Humboldt and Bonpland, 1805, 1807). It has been widely used to
gauge community and ecosystem level responses to major environmental
gradients in freshwaters, including pH (Layer et al., 2010) and nutrients
(Rawcliffe et al., 2010), and many other systems (Olesen et al., 2010).
Within the current context of climate change, this approach is now used to
identify key differences between systems located in different climates (slightly
warmer or cooler) but otherwise similar (such as in area, trophic state or pro-
ductivity level, etc.). Comparable ecosystems under different natural climatic
conditions showing different ecosystem processes help elucidate the potential
long-term consequences of changes in climate, as long-term data are often not
available beyond a few years of sampling in most systems (but see Durance and
Ormerod, 2007; Jeppesen et al., submitted for publication; Layer et al., 2011).
Thus, this approach highlights the structure and interactions of communities
arguably at, or close to, equilibrium conditions rather than the responses to
short-term perturbations (i.e. experimental increase in temperature)
(Woodward et al., 2010a,b). SFTS is a common method used in the
attempt to understand change when it is not possible or desirable to wait
for years or decades to detect changes (Jackson, 2011). The SFTS approach
includes cross-comparison studies, latitudinal gradients (with mean
temperature generally increasing towards lower latitudes) and altitudinal
(with temperature generally increasing towards lowlands) gradients and has
been applied to a series of environments, such as marine and inland
ecosystems in Antarctica (e.g. Howard-Williams et al., 2006), Icelandic
geothermal streams (Friberg et al., 2009; Woodward et al., 2010a),
temperate and subtropical streams (Teixeira-de Mello et al., 2012) and
shallow lakes in Europe (Gyllström et al., 2005; Moss et al., 2004; Stephen
et al., 2004; and references herein) and South America (Kosten et al.,
2009c, 2011a and references herein). SFTS represents one of the most
widely used approaches in ecological climate change research, although its
potentially weak aspects should be considered before application, including
the need for a trait- or size-based approach so as to avoid the potentially
confounding effects of geology, biogeography and land use, and the
findings should be analyzed carefully since equilibrial or non-equilibrial
conditions may be hard to distinguish (Woodward et al., 2010b). We
argue that the SFTS approach provides one of the most plausible empirical
evaluations for these theories using real-world data and, by the
generalization of these theories, provides the potential for inductive
advances and the proposition of new mechanisms.
Our aim with this work is primarily to review and summarize the
changes in community traits (richness, biomass, density, body size) and in
growth, reproduction and strength of trophic interactions in shallow lakes
in relation to climate regimes, as shown by studies applying the SFTS ap-
proach, either in the form of cross-comparisons studies or investigations
along latitudinal and altitudinal gradients and as shown by analyses of pub-
lished metadata. Extraction of spatial trends that can be associated with cli-
mate signals may be done confidently when the sites chosen for comparison
are similar as to trophic state, area and other relevant limnological character-
istic (e.g. Brucet et al., 2010, 2012, submitted for publication; Meerhoff
et al., 2007a,b; Teixeira-de Mello et al., 2009), or when many sites are
sampled with a random distribution of trophic states (e.g. Kosten et al.,
2011b and references herein), so that physicochemical gradients are
nested within climate regions (e.g. Declerck et al., 2005). Thereby, we
aimed to detect patterns of change that can be associated with differences
in ambient temperature and thus to elucidate changes with warming.
We also analyzed metadata generated in different parts of the world in
order to construct gradients for the traits or communities not covered by
the current SFTS literature. We searched for shallow lake systems (maxi-
mum depth < 5 m, polymictic, or identified by the authors as such) and
checked for records on characteristics such as area, trophic state, pH, salinity,
turbidity and the presence of exotic species (if identified in the work). The
introduction or extraction of species, particularly invertebrates and fish
(Villéger et al., 2011), could blur latitudinal patterns of native fauna and
should thus be considered in the analysis. We analyzed trends at different
levels of organization, mostly focusing on community structure parameters
and compared these findings with theoretical expectations basically from
MTE (sensu Brown et al., 2004) and with findings from other research ap-
proaches. A significant challenge is to predict the effects of climate warming
on lake community structure, since the effects of temperature on a particular
community depend on the feedbacks with other communities that are also
affected by warming and other aspects of global change (Moss et al., 2011). It
is beyond the scope of this chapter to address all observed or potential
climate-driven changes in freshwaters, as many have been reviewed recently
for lakes (e.g. Adrian et al., 2009; Moss, 2010, 2011; Moss et al., 2009) or
freshwaters in general (Perkins et al., 2010; Woodward et al., 2010b).
Instead, our target is to highlight the trends in climate-associated changes
for community traits that may have profound implications for the
functioning of these ecosystems and to identify areas that require further
research and experimental testing of mechanisms, while stressing the

limitations and advantages of this research approach.
Being a comprehensive work, this chapter can be read either as a single
monograph or in part by considering the self-contained sections, following
the axis of community traits (e.g. richness, biomass, density, body size) or the
axis of specific shallow lake assemblages (i.e. fishes, macroinvertebrates, zoo-
plankton, macrophytes, phytoplankton, periphyton and bacterioplankton).
The articles most frequently cited in the following subsections are briefly
described when first mentioned and thereafter referred to for a summary
of their main characteristics (Table 2).
Table 2 Summary of the most frequently quoted articles used in the Results section
References Approach Type of study Latitude range n lakes Climate
Bécares et al. LG Mesocosm- 39–61 N 6 Med–
(2008) exp Temp–Cold
Brucet et al. CC Semi exp lit. 38–56 N 8 Med–Temp
(2010)
Brucet et al. LG Whole lake 28–69 N 1632 Med–
(submitted for Temp–Cold
publication)
Brucet et al. CC Semi exp lit. 38–56 N 8 Med–Temp
(2012)
Danger et al. CC Mesocosm- 14–48 N 2 Trop–Temp
(2009) exp
Declerck et al. LG Whole lake 36–56 N 98 Med–
(2005) Temp–Cold
Griffiths (1997) LG Whole lake 29–-74 N 474 Subtrop–Cold

Gyllström et al. LG Whole lake 38–68 N 81 Warm–
(2005) Temp–Cold
Havens et al. CC Whole lake 29–49 N 2 Subtrop–
(2009) Temp
Heino (2009) Review World wide
Table 2 Summary of the most frequently quoted articles used in the Results section—
cont'd
References Approach Type of study Latitude range n lakes Climate
Jackson et al. CC Whole lake 51–56 N 252 Temp–Cold
(2007)
Kosten et al. LG Whole lake 5–55 S 83 Trop–
(2009c) Subtrop–Cold
Kosten et al. LG Whole lake 5–55 S, 143 Trop–Cold
(2011a) 38–68 N
Kosten et al. LG Whole lake 5–55 S 83 Trop–
(2011b) Subtrop–Cold
Lacerot (2010) LG Whole lake 5–55 S 83 Trop–
Subtrop–Cold
Lewis (1996) CC Whole lake 0–70 N 26 Trop–Temp
Meerhoff et al. CC Semi exp lit. 32.5 S–56 N 10 Subtrop–
(2007a) Temp
Meerhoff et al. CC Semi exp lit. 32.5 S–56 N 10 Subtrop–
(2007b) Temp
Muylaert et al. LG Whole lake 36–56 N 98 Med–
(2010) Temp–Cold
Moss et al. LG Mesocosm- 36–56 N 6 Med–
Pinto-Coelho LG Whole lake 19–20 S, 64 Temp–Trop
et al. (2005) 27–55 N
Schiaffino et al. LG Whole lake 45–63 S 45 Cold–
(2011) SubPolar
Stephen et al. LG Mesocosm- 36–56 N 6 Med–
Teixeira-de CC Semi exp lit. 32.5 S–56 N 19 Subtrop–
Mello et al. Temp
(2009)
Abbreviations indicate the approach and type of study: LG, latitudinal gradient; CC, cross-comparison;
exp, experimental; lit, littoral (i.e. artificial plants were introduced). Broad climate regimes were assigned
based on the information given by authors or based on geographic locations, abbreviations: Med, med-
iterranean; Subtrop, subtropical; Temp, temperate. References are ordered alphabetically.
2. FINDINGS IN SPACE-FOR-TIME STUDIES

2.1. Richness changes with climate
The strong latitudinal relationship of increasing diversity towards low lati-
tudes is one of the most familiar and widespread patterns in ecology and has
puzzled many generations of scientists, since Darwin and von Humboldt
(e.g. Allen and Gillooly, 2006; Hillebrand, 2004). Lakes are good model
systems for the study of taxon richness in relation to environmental
gradients, because they are well-delineated ecological entities in the
landscape (Dodson et al., 2000), yet compared with terrestrial systems
studies on diversity patterns in lakes are underrepresented (Waide et al.,
1999), especially in shallow lakes (e.g. Declerck et al., 2005; Jeppesen
et al., 2000; Kruk et al., 2009; Scheffer et al., 2006). In this section, we
will briefly cover the findings for shallow lakes, stressing that we do not
attempt to explain the patterns in taxonomic richness solely (or mostly)
by climate factors, due to the fundamental effects of evolutionary history
and biogeography on this particular variable.
2.1.1 Fishes
At a global scale, a meta-analysis detected a decreasing latitudinal pattern
in fish assemblage species richness in shallow lakes (linear regression,
n ¼ 69, r2 ¼ 0.88, p < 0.0001) (from González-Bergonzoni et al., 2012)
(Fig. 1A). Greater fish biodiversity in warm climates has also been found
in a worldwide latitudinal gradient investigation and in lowland versus high
altitude lakes (Amarasinghe and Welcomme, 2002). This recurrent pattern is
also consistent at latitudinal continental scales in Europe (Brucet et al., sub-
mitted for publication) and North America (Griffiths, 1997; Mandrak, 1995)
(Table 2). Particularly, the broad-scale patterns of fish species richness and
diversity in European lakes were mainly explained by environmental
temperature together with morphometric variables (Brucet et al.,
submitted for publication; based on n ¼ 1632 lakes), while in a wide
spatial range of Chinese lakes (n ¼ 109 lakes, Zhao et al., 2006), climatic
variables (temperature and potential evapotranspiration) were among the
most important explanatory variables. Specifically in shallow lakes, cross-
comparison studies of littoral communities have found higher fish
richness at the warmer locations in a subtropical–temperate investigation
(Meerhoff et al., 2007a; Teixeira-de Mello et al., 2009) and in a
temperate versus cold climate comparison (Jackson et al., 2007).
In brackish lakes, the higher richness of fish at warmer locations seems,

however, less pronounced, as found in a similar cross-comparison study
of temperate and Mediterranean shallow lakes (Brucet et al., 2010).
Overall, there is an increase in fish richness from cold to warm climates,
modulated by hydrology-related factors (such as drought intensity and
salinity) that may promote lower relative richness in warm lakes with
high hydrological stress (Jeppesen et al., 2010a; M. Beklioğlu et al.,
unpublished data).
The functional diversity of fish seems also to increase with decreasing lat-
itude, as found in a review of North American freshwaters (Moss, 2010) and
in cross-comparison studies (Teixeira-de Mello et al., 2009). In particular,
the richness of omnivorous fish species follows a strong and negative world-
wide latitudinal gradient in all aquatic ecosystem types, this being associated
with the same pattern followed by taxonomic richness (González-
Bergonzoni et al., 2012), not least in shallow lakes (Jeppesen et al., 2010a).
2.1.2 Macroinvertebrates
Studies on invertebrate diversity patterns in freshwaters are clearly unbal-
anced in that they mainly focus on aquatic insects and primarily in running
waters. Overall, the few available studies suggest that differences in
macroinvertebrate richness between climate regions are ambiguous and de-
pend on taxonomic groups (Heino, 2009). At a global scale, the diversity of
some invertebrate groups, such as the orders Ephemeroptera and
Trichoptera, seems to show a negative relationship with latitude (Barber-
James et al., 2008; de Moor and Ivanov, 2008; data not available for our
meta-analysis), while other groups (e.g. Plecoptera, Decapoda, Simulidae
dipterans) do not show any clear trend (e.g. Plecoptera species richness,
linear regression r2 ¼ 0.001, p > 0.05; with data from Heino, 2009 and
Palma and Figueroa, 2008) or seem to increase their diversity towards
high latitudes, as in some studies in large biogeographic areas (Crandall
and Buhay, 2008; McCreadie et al., 2005). At family level, a latitudinal
gradient in assemblage composition of chironomids has revealed the
important role of ambient temperature as a key factor for the distribution
and relative abundance of different taxa (Larocque et al., 2006).
Unfortunately, in most studies, the original data are not shown, the
taxonomic resolution achieved differs from paper to paper, or data on
lakes and streams are pooled, preventing us from conducting a formal
meta-analysis of all published works.
In the few SFTS studies including only shallow lakes, plant-associated

macroinvertebrates had much lower richness (at different taxonomic reso-
lution, mostly order level) in the subtropics than in comparable temperate
lakes (Meerhoff et al., 2007a), a climate pattern also found in brackish lakes
in a similar cross-comparison study between Mediterranean and temperate
regions (Brucet et al., 2012) (Fig. 1B, Table 2). Similarly, in a study com-
paring 16 tropical and 10 temperate lakes, Lewis (1996) found lower diver-
sity and abundance of benthic invertebrates in the tropics, especially among
Nematoda and Chironomidae (although data are not available for our meta-
analysis). Higher risk of drought and large variations in salinity at the south-
ernmost locations may reduce the species richness in arid or Mediterranean
shallow lakes (Boix et al., 2008).
2.1.3 Zooplankton
In contrast to theoretical predictions, the literature shows evidence for a
negative or no relationship between mesozooplankton (i.e. cladocerans
and copepoda) richness and increasing temperature (in our review, decreas-
ing latitude) (Fig. 1C). Cladoceran species richness exhibited no significant
relationship with latitude (from 58.1 to 70.7 N) and altitude (from 0 to
1000 m) over a set of 336 Norwegian lakes, although high latitude and high
altitude lakes had relatively low richness (Hessen et al., 2006): these differ-
ences were attributed to constraints imposed during colonization and to
temperature, although the main explanatory factor was, in fact, productivity.
Lewis (1996) reported a similar number of zooplankton species (in total and
for cladocerans, copepods and rotifers), with slightly more cladoceran spe-
cies in temperate than in tropical lakes. A decline in cladoceran and copepod
species richness, in this case with increasing surface water temperature, was
also observed with a data set of 1042 lake-years collected from 53 lakes in the
northern hemisphere (Shurin et al., 2010; showing no latitudinal data and
thus unavailable for our meta-analysis). Temperate shallow lakes often host
a richer local assemblage of cladocerans (at genus level) than warm shallow
lakes (Fig. 1C) as found in different studies (LSmeans p < 0.001 in Meerhoff
et al., 2007b; no statistics reported in Pinto-Coelho et al., 2005; see details
in Table 2). Typically, larger-bodied genera, such as Daphnia, Sida,
Eurycercus, Leptodora and Polyphemus, were missing from both pelagic and
littoral habitats in warm shallow lakes (Meerhoff et al., 2007b), which is
in accordance with previous studies showing that large zooplankters were
rare in tropical lakes (Fernando, 2002; Fernando et al., 1987; Lewis,
1996). In brackish lakes, however, cladoceran species richness was similar
in temperate and Mediterranean regions and salinity emerged as the key

controlling factor (Brucet et al., 2009). Overall, local factors such as
productivity, salinity and fish predation pressure, despite being factors
likely ultimately related to climate often seem better proximate predictors
of cladoceran richness than temperature itself.
2.1.4 Macrophytes
The few latitudinal gradient studies on macrophytes diversity are not specific
to shallow lakes; they refer to freshwaters in general and often show contra-
sting results and unclear or no latitudinal pattern. A comparison between
temperate and tropical freshwaters revealed higher macrophytes richness
in temperate regions, a pattern attributed to the frequent dominance of a
particular species within a given water body in the tropics (Crow, 1993).
A Finnish study, however, reported a general decline in macrophyte richness
in lakes towards the north (Linkola, 1933; reported in Rorslett, 1991), re-
lated to the duration of the ice-free period since short growing seasons may
not only limit macrophyte growth but their distribution as well (Heino,
2001). Latitudinal changes in macrophyte richness have been recorded in
the Great Lakes basin (Canada, USA), largely associated with latitudinal
changes in geology and related factors such as sediment composition
(Lougheed et al., 2001) rather than climate. Yet another study in North
European lakes demonstrated no or only marginal latitudinal changes in
macrophyte diversity (Rorslett, 1991), coinciding with the lack of latitudinal
pattern in submerged macrophyte species richness in 83 South American
shallow lakes (S. Kosten et al., unpublished data). Although regional and
continental studies seemed to be inconclusive, a global analysis of the num-
bers and distribution of vascular macrophytes in freshwaters (not discrimi-
nating shallow lakes) showed that their diversity is highest in the tropics
(Afrotropics, Neotropics and Orient) and lowest in the Nearctic,
Palaeoarctic and Australasia (Chambers et al., 2008), suggesting a marked
divergence between alpha and gamma diversity.
2.1.5 Phytoplankton
Reports about phytoplankton composition and richness across latitudes, es-
pecially those including warm shallow lakes, are very scarce. Altitudinal gra-
dient studies of phytoplankton richness are also limited (but see Wang et al.,
2011). However, Stomp et al. (2011) analyzed patterns of species richness of
freshwater phytoplankton in 540 lakes and reservoirs across the United States
and found strong latitudinal (range: 26–51 N; linear regression: r2 ¼ 0.16,
p < 0.001; Fig. 1D), longitudinal and altitudinal gradients, overall showing
an increase in richness with rising water temperature. A comparison be-
tween temperate and subtropical climates reported a higher richness of spe-
cies comprising at least 5% of total biovolume in the subtropical lakes
(Kruskal–Wallis test H ¼ 14.31, p < 0.002, see Appendix C).
In terms of composition, warmer phytoplankton communities are often
described as overlapping with temperate communities and little endemism
(Lewis, 1996). Phytoplankton composition (considering both phylogenetic
groups and dominant species) seemed to be affected more by local condi-
tions and nutrient concentrations than by factors associated with latitude
per se, as found in 27 lakes situated at cold-temperate (56–60 N) and sub-
arctic (67–68 N) latitudes (Trifonova, 1998). Local factors such as the
presence of submerged vegetation cover may also override latitudinal differ-
ences, as described in a European study revealing a negative association
between phytoplankton richness and macrophyte cover in 98 shallow lakes
(Declerck et al., 2005), although the opposite pattern was traced in subtrop-
ical shallow lakes (Kruk et al., 2009).
2.1.6 Periphyton
That periphyton, including all substrata-attached microalgae and associated
bacteria and fungi, plays a fundamental role in shallow lake food webs has
been demonstrated by several studies during the past decade (Liboriussen
and Jeppesen, 2003; Vadeboncoeur et al., 2003, and references herein).
However, we did not find any studies on the latitudinal variation on
periphytic algae richness. To remedy this, we conducted a meta-analysis
of patterns in species richness and biomass (the only community traits
measured or shown for this assemblage, as far as we are aware) of
periphyton algae over a latitudinal gradient ranging from 68 S to 83 N,
including data from a total of 23 publications and 14 countries (see
Appendix A for further information). In our meta-analysis, we detected a
strong and significant linear decrease in periphyton algae richness with
increasing latitude (linear regression: r2 ¼ 0.755, p < 0.001, Fig. 1E).
2.1.7 Bacterioplankton
Inclusion of bacteria in the SFTS literature is restricted to a few papers on
investigations carried out along gradients in Europe (Declerck et al.,
2005; Van der Gutch et al., 2006), Argentina and Antarctica (Schiaffino
et al., 2011), and China (Wu et al., 2006). We therefore reviewed the lit-
erature and extracted crude data on community traits whenever available
from both gradient and single site studies (n ¼ 140 lakes in 17 publications,
see Appendix B for further information). We could not detect significant
trends in bacterioplankton richness (usually estimated through molecular
fingerprinting methods) along a latitudinal (or temperature) gradient from
our dataset (linear regression n ¼ 43, r2 ¼ 0.008, p ¼ 0.58; Fig. 1F). Bacter-
ioplankton richness is described in just a few studies, mostly conducted in
temperate regions, potentially biasing our results. However, there is increas-
ing evidence for the existence of an inverse relationship of richness with lat-
itude for both continental (Schiaffino et al., 2011) and marine (Fuhrman
et al., 2008; Pommier et al., 2007) water bodies. Despite the underlying
mechanisms still being under debate (e.g. species sorting, history), there
are indications that the bacterial community composition in the water
column (including shallow systems) changes along latitudinal gradients
(Schiaffino et al., 2011; Sommaruga and Casamayor, 2009; Van der
Gucht et al., 2007; Yannarell and Triplett, 2005).
2.2. Climate effects on biomass

2.2.1 Fishes
Fish biomass seems to increase with decreasing latitude, or increasing ambi-
ent temperature (Fig. 1G). Pelagic fishes increased significantly in biomass in
warm climates (as CPUE; g net 1 night 1) in a series of shallow lakes of
varying nutrient concentrations along a climate gradient in Europe
(ANOVA p < 0.04, for log-transformed biomass, recalculated from
Gyllström et al., 2005) (Fig. 1G). Also, cross-comparison studies have found
a significantly higher fish biomass (as g m 2) in warmer climates, both in
freshwater (ANOVA F1,100 ¼ 40.7, p < 0.0001, Teixeira-de Mello et al.,
2009) and in brackish shallow lakes (Brucet et al., 2010) at similar TP con-
centrations in each set under comparison (although brackish lakes seem to
have a lower biomass than freshwaters). In a European-scale study
(Brucet et al., submitted for publication), fish biomass was mainly related
to lake productivity, but when differences in productivity were taken into
account in the analysis, altitude was negatively correlated with biomass.
Information on changes in the biomass of macroinvertebrates along a climate
gradient is extremely scarce in general and almost absent in shallow lake
studies: most research records abundance and identity at local scales, rather
than biomass. Therefore, we were not able to identify or test a trend of
change in macroinvertebrate biomass under different climates or latitudes.
2.2.3 Zooplankton
Although our analysis of published metadata (Table 1) showed no significant
relationship, zooplankton biomass exhibits an apparent increase towards
colder regions of the globe (Fig. 1I). A latitudinal gradient analysis of 81
lakes in Europe (38–68 N) documented lower zooplankton biomass levels
in the warmer lakes of Mediterranean Spain, with climate being the second
most important predictor of zooplankton biomass after TP (F ¼ 19.7,
r2 ¼ 0.49, p < 0.001, n ¼ 65) (Gyllström et al., 2005). Lower zooplankton
biomass at lower latitudes was also evident in an outdoor experimental study
where nutrient enrichment and fish predation were analyzed in six European
lakes (Vakkilainen et al., 2004). A comparison of zooplankton biomass
between two eutrophic lakes, one in temperate Italy and the other in sub-
tropical Florida (USA), documented higher biomass in the temperate lake
(Havens et al., 2009). The small eutrophic tropical reservoirs in the study
by Pinto-Coelho et al. (2005) were the exception to this pattern, with
higher zooplankton biomass, particularly of Cladocera, in the warm region.
However, the subtropical Florida lakes included in this same study had a
lower cladoceran total biomass compared to the colder lakes. Mediterranean
brackish lakes also exhibited a remarkably lower biomass of large zooplank-
ton than similar temperate lakes (Brucet et al., 2010). In all cases, colder lakes
had a significantly higher proportion of Daphnia than similar warmer systems
(Brucet et al., 2010; Gyllström et al., 2005; Jackson et al., 2007; Meerhoff
et al., 2007b). Trends of change in zooplankton biomass with altitude appear
to be less clear than along latitudinal gradients, according to a study of
subarctic ponds (Karlsson et al., 2005).
The majority of the articles analyzed address the effect of lake trophic state
(i.e. nutrient concentrations) on zooplankton biomass, showing ambiguous re-
lationships between both variables and climate. TP seems the most important
predictor of zooplankton biomass and the biomass of large pelagic crustaceans,
irrespective of the climatic region considered, as found along a European lat-
itudinal gradient (Gyllström et al., 2005), a latitudinal gradient in Turkey
(Beklioğlu et al., in prep.) and in cross-comparisons (Jackson et al., 2007): all
these studies indicated that increases in TP concentration have a positive effect
on zooplankton biomass. However, the response of zooplankton, and partic-
ularly that of cladocerans, to increases in TP was more intense in tropical regions
(measured as the slope in the regressions) (Pinto-Coelho et al., 2005). Interest-
ingly, intermediate (subtropical) lakes in this study had the flattest slope in the
relationship between zooplankton biomass and TP (Pinto-Coelho et al., 2005),
as also found in subtropical Lake Apopka (Florida, USA) (Havens et al., 2009).
2.2.4 Macrophytes
Most evidence of effects of warming on macrophyte biomass comes from
interannual comparisons rather than from SFTS studies, preventing us from
assessing potential latitudinal trends. Early season warm temperatures seem
to favour a strong increase in whole-lake submerged macrophyte biomass, as
recorded in five lakes in the Eastern Townships of Quebec, Canada, despite
increased turbidity in such period (Rooney and Kalff, 2000). However, this
temperature effect seems to be overruled by the strong influence of under-
water irradiance, which in turn is most often impacted by lake trophic state.
In an analysis of data from 139 lakes between latitudes 46 and 69 , under-
water irradiance and not latitude explained a large part of the variance in
submerged macrophyte biomass (Duarte et al., 1986). For emergent macro-
phytes, however, lake morphometry is an important factor determining
plant biomass; however, no significant positive relationship between the
biomass per area colonized and latitude has been found (Duarte et al., 1986).
2.2.5 Phytoplankton
Most studies deal with biomass of phytoplankton in terms of chlorophyll-a
(Chl-a) concentrations (indirect estimate of biomass), and, to a lower extent,
biovolume (directly related to biomass). We analyzed published data from a
large amount of shallow lakes in different climate zones (Tables 1 and 3)
and discovered neither linear trends with latitude nor clear differences
between climatic regions, except for higher total biomass (as Chl-a) in
the tropics and temperate systems, followed by subtropical and subpolar
regions (Fig. 1J; n ¼ 90 lakes, Kruskal–Wallis: H ¼ 205, p < 0.001). Larger
biomass of phytoplankton in the tropics has been reported before
(Danger et al., 2009; Huszar et al., 2006; Lewis, 1996, 2000). Kruk et al.
(2010) found that the largest values of Chl-a occurred in subtropical lakes
(n ¼ 40) and the lowest in tropical lakes (n ¼ 42, over a total of 210
shallow lakes), while Kosten et al. (2011b) recorded a decrease in
phytoplankton Chl-a from subpolar regions towards the tropics in South
America (83 lakes in total). On the other hand, in a study of 143 shallow
lakes along a latitudinal transect ranging from subarctic Europe to
southern South America, lakes in warmer climates did not exhibit an
overall higher phytoplankton biomass, although cyanobacteria biomass
seemed favoured (Kosten et al., 2011a). Along a latitudinal gradient in
Europe, both high and low Chl-a concentrations were found in southern
and northern lakes (Nõges et al., 2003), while higher Chl-a
Table 3 Relationship between phytoplankton biomass (as chlorophyll-a, Chl-a, mg L 1) and total phosphorus (TP, mg L 1) in shallow lakes
under different climate regimes, as described in published studies
References Location Climate n Model R2 Slope
Antoniades et al. (2003a)* Canadian Arctic: Ellesmere Island Polar 31 y ¼ 0.16x 0.22 0.36 0.16
Antoniades et al. (2003a)* Canadian Arctic: Prince Patrick Polar 29 y ¼ 0.007x 0.40 0.00 0.01
Island
Antoniades et al. (2003b)* Canadian Arctic: Ellef Ringnes Polar 24 y ¼ 0.75x 1.58 0.36 0.75
Island
Flanagan et al. (2003) Canada Cold 113 y ¼ 0.33x 0.42 0.07 0.33
Kosten et al. (2011b) Argentina Cold 11 0.94
Mazumder and Havens North America, Europe Cold 126 y ¼ (0.87 0.05) 0.73 0.87
(1998) x þ 0.60 0.07
Ogbebeo et al. (2009)* Canada Cold (flooded 10 y ¼ 0.22x þ 0.25 0.38 0.22
Arctic-tundra)
Ogbebeo et al. (2009)* Canada Cold 6 y ¼ 0.94x 0.19 0.84 0.94
(forest-tundra)
Ogbebeo et al. (2009)* Canada Cold (non- 9 y ¼ 0.50x þ 0.07 0.39 0.50
flooded
Arctic tundra)
Flanagan et al. (2003) Canada Temperate 316 y ¼ 0.92x 0.38 0.28 0.92
Jackson et al. (2007) Canadian prairie Cold 30 y ¼ 0.86x þ 1.72 0.86
Jackson et al. (2007) Denmark Temperate 222 y ¼ 0.82x þ 2.35 0.82
Kruk et al. (2011)** The Netherlands Temperate 95 y ¼ 0.91x 0.33 0.34 0.91
Meerhoff et al. (2007a,b)** Denmark Temperate 9 y ¼ 1.64x 1.50 0.70 1.64
Prairie et al. (1989) North America, Europe Temperate 133 0.69 0.87
Mazumder (1994) North America, Europe Temperate LH 126 y ¼ (0.87 0.05) 0.73 0.87
x þ 0.60 0.07
Mazumder and Havens North America, Europe Temperate SH 235 y ¼ (0.97 0.02) 0.87 0.97
(1998) x þ 0.21 0.03
Mazumder and Havens Florida, USA Temperate 361 y ¼ (0.94 0.03) 0.71 0.94
(1998) SH and LH x þ 0.35 0.05
Kosten et al. (2011b) Brazil, Uruguay, Argentina Temperate– 34 0.62
subtropical
Brown et al. (2000) Subtropical 359 0.67 0.42
Wang et al. (2008) China Subtropical 45 y ¼ 1.04x 0.97 0.80 1.04
Kruk et al. (2009)** Uruguay Subtropical 18 y ¼ 0.25x þ 0.28 0.05 0.25
Kruk et al. (2011)** Uruguay Subtropical 12 y ¼ 0.12x þ 0.99 0.00 0.12
Meerhoff et al. (2007a,b)** Uruguay Subtropical 10 y ¼ 0.71x 0.59 0.34 0.71
Mazumder and Havens Florida, USA Subtropical SH 59 y ¼ (1.06 0.07) 0.79 1.06
(1998) x þ 0.36 0.09
Huszar et al. (2006) South America, Africa Tropical– 192 y ¼ 0.70x 0.15 0.42 0.70
subtropical
Kosten et al. (2011b) Brazil Tropical 38 0.20
Parinet et al. (2004) Ivory Coast Tropical 9 y ¼ 0.93x þ 1.66 0.32 0.93
2
The explained variance (R ), slope and linear models of the relationship between log10 Chl-a (y) and log10 TP (x) in the water column of polar, cold, temperate, sub-
tropical and tropical shallow lakes, indicating the respective references, location, and number of cases (n) are displayed. LH, lakes with large herbivorous zooplankton; SH,
lakes with small herbivorous zooplankton, as classified by the authors. * calculated from data available, ** data obtained in the cited references provided by authors.
References are ordered by increasing temperature of the region of the data.
concentrations were found in the southern lakes along a latitudinal gradient

in Turkey (M. Beklioğlu et al., unpublished data).
Interestingly, the other proxy for total phytoplankton biomass, that is,
biovolume, often shows a different pattern to that of Chl-a. In a comparison
of a large data set from subtropical and temperate regions, greater total
biovolume values appeared in the subtropics than in similar temperate lakes
over the same wide gradient in nutrient concentration (Kruskal–Wallis test
H ¼ 11.34, p < 0.001, n ¼ 650, see Appendix C). Some works argue the tro-
pics to have a higher frequency of cyanobacteria (Paerl and Huisman, 2009).
In the subtropical–temperate lakes comparison (see Appendix C for analysis
information), cyanobacteria and Dinophyceae had a significantly higher rel-
ative biovolume in the subtropics, whereas Chlorophyceae, Cryptophyceae,
Euglenophyceae, Zygnematophyceae, Chrysophyceae and Xantophyceae
had a higher relative biovolume in the temperate lakes (Kruskal–Wallis tests,
Fig. 2). Mesocosm experiments conducted in different European climate re-
gions have also suggested that warmer climates may increase the relative
contribution of cyanobacteria to total phytoplankton biovolume in shallow
lakes (Stephen et al., 2004; Van de Bund et al., 2004; Table 2) as also found
in a recent mesocosm warming experiment in southern England (Yvon-
Durocher et al., 2011a,b). In contrast, other mesocosm experiments
Temperate Subtropical
100 100
n = 540 n = 110
80 80
% Biovolume (m3 L–1)
60 60 *
40 * * 40
*
*
20 20
* *
*
0 0
Chl
Din
Cry
Zyg
Bac
Cya
Chl
Bac
Din
Cry
Eug
Zyg
Xan
Cya
Eug
Xan
Chr
Chr
Figure 2 Relative biovolume (%) of phylogenetic classes of phytoplankton in shallow

lakes located in temperate (n ¼ 540) and subtropical (n ¼ 110) climates. Abbreviations:
Cyanobacteria (Cya), Chlorophyceae (Chl), Bacillariophyceae (Bac), Dinophyceae (Din),
Cryptophyceae (Cry), Euglenophyceae (Eug), Zygnematophyceae (Zyg), Chrysophyceae
(Chr) and Xanthophyceae (Xan). Error bars correspond to 1 standard error and * indi-
cates classes with significantly higher biovolume according to the Kruskal–Wallis test
(p < 0.05). Data were extracted from Kruk et al. (2011), see Appendix C for a description
of methodology.
conducted in tropical and temperate shallow lakes have not revealed any
effect on cyanobacteria or any drastic changes in phytoplankton
community structure (Danger et al., 2009).
As the relationship between Chl-a and nutrients is directly associated
with the predictability of phytoplankton biomass, it is important to analyze
its variability and strength under different climatic conditions. The relation-
ship between phytoplankton Chl-a concentrations and nutrients (typically
TP) along latitudinal gradients is one of the most commonly reported in
the literature of gradients (Table 3). An increase in phytoplankton biomass
with increases in TP occurs across climates (positive slope in the regressions)
(Fig. 3). However, we found no clear patterns of change in the slope or
intercepts across climates (Table 3), even with opposite results being
evident in studies at the same latitudinal location (Brown et al., 2000;
Gyllström et al., 2005; Huszar et al., 2006; Jeppesen et al., 2007;
Muylaert et al., 2010). Although differences were not significant, high
variability in the importance of nutrients for phytoplankton biomass
(indicated by a wide range of r2 values in the regressions) emerges in
subtropical and also in cold regions (Huszar et al., 2006; Kosten et al.,
2009b,c) (Fig. 3), likely suggesting that factors other than TP (or
0.9 1.8
0.7 1.4
Chl-a-TP slope
Chl-a-TP R2
0.5 1.0
0.3 0.6
0.1 0.2
0 0
-0.1 -0.2
Tropical
Subtropical
Temperate
Cold
Polar
Tropical
Subtropical
Temperate
Cold
Polar
Figure 3 Relationship between phytoplankton biomass and nutrients along a climate

gradient, showing the explained variance (R2) and slope in the linear regressions
between total phosphorus (TP) and phytoplankton chlorophyll-a (Chl-a) in shallow lakes
from tropical (n ¼ 3), subtropical (n ¼ 8), temperate (n ¼ 9), cold (n ¼ 7) and polar (n ¼ 3)
regions, according to published works applying the space-for-time approach. Box-plots
show mean, mean SE, mean SD and extreme values. Respective references and full
regression models are shown in Tables 1 and 3.
nutrients) explain a large proportion of the phytoplankton biomass variation.

Besides, the amount of Chl-a per unit of TP may be higher in temperate and
tropical lakes than in other climatic regions (marginally significant
differences, Kruskal–Wallis test, p ¼ 0.07; Fig. 3).
2.2.6 Periphyton
Only a few published works applying the SFTS approach have included
periphyton in their target communities, and those that have, exclusively focus
on biomass (Bécares et al., 2008; Brucet et al., 2010, 2012; Meerhoff et al.,
2007a). In our meta-analysis, we found a significant and positive linear
response of periphyton algae biomass with increasing latitude (n ¼ 16
publications, r2 ¼ 0.378, p < 0.01) (Fig. 1K). This pattern is consistent with
findings in other studies based on both field sampling campaigns in temperate,
subarctic and Antarctic regions (Hansson, 1992), mesocosm experiments
along a latitudinal gradient (Bécares et al., 2008) and cross-comparisons
(Brucet et al., 2012; Meerhoff et al., 2007a). Nonetheless, the effects of
latitude or temperature might be very complex, because the periphyton
response curve to increasing nutrients shows saturation at different points
depending on climate regions and is clearly higher in the colder regions of
northern Europe than in the Mediterranean zone (Bécares et al., 2008).
In our constructed database, we could not detect any significant relationship
between bacterioplankton biomass and latitude, possibly due to the rela-
tively few geographic locations included (despite the fairly high number
of systems, n ¼ 33 lakes, Fig. 1L).
2.3. Climate effects on density

Abundance of individuals is typically measured, but not always reported, for
several communities in shallow lakes, particularly animal or single-cell com-
munities. Bacterioplankton represent an exception here, since most works
provide numerical counts of abundance rather than estimations of biomass.
2.3.1 Fishes
Published SFTS literature reporting absolute fish density data is rare, and,
typically, density and biomass proxies such as CPUE are shown. However,
the scarce findings support the trend of higher fish densities towards warmer
climates, over a wide range in nutrient concentrations and system area. The
evidence comes from cross-comparison studies in warm and temperate

climates, both in freshwater (Teixeira-de Mello et al., 2009) and in brackish
(Brucet et al., 2010) shallow lakes (Fig. 1), and from an extensive study in-
cluding both latitudinal and altitudinal gradients (Brucet et al., submitted for
publication). A comparison of fish abundance in cold Canadian lakes to
comparatively warmer Danish shallow lakes showed greater abundances
in Denmark, as a likely consequence of greater winter mortality in Canada
(Jackson et al., 2007). On the other hand, drought-induced fish mortality
can also explain the lower fish densities found in southern Mediterranean
lakes (M. Beklioğlu et al., unpublished data). All these works, despite show-
ing opposite results to general theoretical expectations based primarily on
metabolism (Brown et al., 2004; Fig. 1M), discard potential effects of trophic
state on the observed patterns, as the cross-comparison studies included lakes
paired in terms of nutrient levels and the large spatial gradient study also
covered the same gradient in TP for the different locations.
We found no latitudinal gradient study in shallow lakes including
macroinvertebrates, and thus our climate-related data come only from
cross-comparison studies. In contrast to fishes, but fitting predictions, the
relatively few available data indicate greater densities at colder locations
(Fig. 1N). Cross-comparison studies, both in freshwater (Meerhoff et al.,
2007a) and in brackish (Brucet et al., 2012) shallow lakes, traced up to eight
times lower densities of plant-associated macroinvertebrates in the warmer
systems.
2.3.3 Zooplankton
Our meta-analysis of the SFTS studies showed a significant trend of lower
microcrustacean abundance towards lower latitudes (linear regression:
r2 ¼ 0.16, p < 0.05, n ¼ 25, Fig. 1O), although variability in density
patterns was high. The cross-comparison studies detected overall higher
cladoceran densities in colder climates, both in freshwater (Meerhoff et al.,
2007b) and in brackish shallow lakes (Brucet et al., 2010). However, temper-
ature per se did not explain the low abundances of zooplankton in warm lakes
in the latter, since low abundances also occurred in cold lakes with high fish
densities (Brucet et al., 2010), suggesting a top-down food web effect. In
contrast, both cladocerans and copepods were more abundant in the warmer
lakes in a comparative study of diel migration patterns of microcrustaceans in
similar shallow lakes between latitudes 39 and 61 N in Europe (Hansson
et al., 2007). Both the highest and lowest crustacean densities occurred in the
warmer lakes in a study comparing several lakes and reservoirs of different
depth in temperate, subtropical and tropical countries (Pinto-Coelho
et al., 2005). Reservoirs might exhibit different patterns than true lakes, since
deeper sections are common, which might offer a hypolimnion refuge to
large zooplankton, thereby masking the otherwise typical patterns in warm
shallow lakes. Calanoid copepods, however, were more abundant in the col-
der lakes (Pinto-Coelho et al., 2005). The patterns followed by other zoo-
plankton groups, such as rotifers, remain unexplained due to the scarce
number of works including this fraction. Typically, however, rotifers seem
the dominant group in warm lakes (Brucet et al., 2010; Fernando, 2002).
2.3.4 Macrophytes
Different variables that may be used as proxies for density are regularly reported
in shallow lakes, such as the percent area covered and the volume of the lake
taken up by submerged macrophytes. All these variables are strongly influenced
by the underwater light conditions and therefore by lake trophic state but are
influenced by temperature as well. High coverage of submerged macrophytes
has been related to high spring temperatures in temperate systems (Rooney and
Kalff, 2000; Scheffer et al., 1992). In contrast, both space-for-time (Duarte
et al., 1986; Kosten et al., 2009a) and inter-annual comparative studies
(Hargeby et al., 2004) found that cold winters—typically quantified by the
cumulative number of frost—days generally lead to a higher coverage of
submerged macrophytes. Even after accounting for the effect of underwater
light conditions, however, the variance in coverage among lakes located at
similar latitudes remains high (Kosten et al., 2009a), again suggesting action
of different processes at a local scale. This likely explains why no latitudinal
gradient in submerged macrophyte coverage emerged from the literature,
even when variations in lake nutrient status were taken into account, as
done for 83 shallow lakes along a latitudinal study in South America
(S. Kosten et al., unpublished data) (Fig. 4). The great subjectivity and
variety associated with plant cover estimation methods (typically visual, for a
brief overview of different methods, see Kosten et al., 2009a) may also
prevent the identification of clear patterns.
2.3.5 Phytoplankton
We found only one study reporting microalgal density values in connection
to environmental gradients and particularly with latitude (Sballe and
Kimmel, 1987). These authors found a negative relationship between algal
3.0
Cover/TP (%/µg TP L-1)

2.5
2.0
1.5
1.0
0.5
0
0 10 20 30 40 50 60
Latitude
Figure 4 Coverage (%) of submerged macrophytes corrected by the lake total phos-
phorus concentration in 83 shallow lakes along a latitudinal gradient in South America.
S. Kosten et al. (unpublished data), see Kosten et al. (2009a) for details on methodology.
counts (log-transformed) and latitude (correlation r ¼ 0.45, p < 0.01) for

natural lakes all over United Sates. Due to the lack of raw data and the deeper
nature of the lakes including in this study (ca. 8 m versus ca. 5 m in our
review), we could not include this finding in our analysis (Fig. 1P).
In our constructed database (Appendix B), we found a significant increase in
bacterial abundance in the water column with decreasing latitude (linear re-
gression: n ¼ 133, r2 ¼ 0.08, p ¼ 0.001; Fig. 1R), which is in agreement with
a previous latitudinal gradient study specifically including shallow lakes
(Schiaffino et al., 2011). This correlation was also clear when we grouped
the lakes according to climatic zones (which do not necessarily overlap with
latitude), following the revision by Leemans and Cramer (1991) of the
Köppen climate system (1936) (Fig. 5). We attempted to identify the main
factors behind the emerging pattern by applying Spearman’s correlations and
stepwise multiple regressions with the following parameters: latitude, alti-
tude, lake area, water temperature, conductivity, TP, TN, phytoplankton
Chl-a, and dissolved organic carbon (DOC) (see Appendix B for a summary
of results). In particular, the concentration of DOC is a major controlling
factor of bacterial production in shallow polar lakes (Karlsson et al.,
2001). Increasing temperatures may stimulate photosynthate extracellular
release, thus indirectly contributing to increase DOC concentrations
(Morán et al., 2006). However, in our analysis, temperature and, secondly,
Chl-a were the two factors explaining most of the latitudinal variation in
109
p < 0.0001
R2 = 0.21
Bacterial abundance
108
(cells ml–1)
107
106
105
104
Tropical Temperate Polar 0 10 20 30 40
Sub- Cold Temperature (°C)
tropical
109
P = 0.004
R2 = 0.08
Bacterial abundance
108
(cells ml–1)
107
106
105
104
−1 0 1 2
Log Chl-a (µg L–1)
Figure 5 Density of bacterioplankton in lakes along a climate gradient as found in a
meta-analysis, showing densities in different climate regions and the relationship be-
tween bacterioplankton and temperature and bacterioplankton and phytoplankton
biomass (measured as Chl-a). Box-plots show median values (lines), while lower and
upper boundaries depict the 25th and 75th percentiles, respectively; whiskers indicate
the 10th and 90th percentiles and dots represent outliers. For both regressions,
explained variance (R2) and probability (p) are shown. Respective references are shown
in Appendix B.
bacterioplankton abundance (adj. r2 ¼ 0.66, p ¼ 0.005) (Fig. 5). Latitude and

DOC, however, co-varied strongly with temperature (r ¼ 0.83,
p < 0.0001, n ¼ 112; and r ¼ 0.94, p < 0.0001, n ¼ 26, respectively)
and were, therefore, not included in the regression model due to
multicollinearity.
Our regression model agrees with results obtained by White et al. (1991),
who found strong dependence of bacterial growth rate on temperature and
also that a substantial portion of the residual variation was explained by phy-
toplankton biomass in a broad range of aquatic systems, although no shallow
lakes were included in their investigation.
2.4. Climate effects on body size and size structure

The reduction in body size of aquatic organisms seems to be one of the
clearest responses to environmental warming, and it has even been described
as the third universal response to warming together with changes in phenol-
ogy and distribution (Daufresne et al., 2009; Gardner et al., 2011). In this
review, we sought to test for general trends in body size and community
size structure across the different trophic levels that typically constitute
shallow lake food webs.
2.4.1 Fishes
Mean body size of fish at the assemblage level tends to decrease with increas-
ing temperature (Fig. 1S), as shown in several latitudinal and cross-
comparison studies of lake fish assemblages (e.g. Griffiths, 1997; Meerhoff
et al., 2007a; Teixeira-de Mello et al., 2009). Littoral subtropical fishes
were significantly smaller than their temperate counterparts in cross-
comparison studies (LSmeans p < 0.0001 in Meerhoff et al., 2007a;
ANOVA F1,94 ¼ 32.5 p < 0.0001 in Teixeira-de Mello et al., 2009). A
similar climate pattern occurred in the brackish shallow lakes, although
the differences were not statistically significant, most likely due to an
overriding effect of salinity over temperature (Brucet et al., 2010). An
extensive fish analysis of North American lake fish showed that the
proportion of large fish species (> 20 cm TL) within the assemblage
increased with latitude and that small fish species (<20 cm TL) were
more common at lower latitudes (Griffiths, 1997). The same trends of an
increase in the relative proportion of small fishes (< 10 cm standard
length) at lower latitudes occurred along a latitudinal gradient in South
America (Lacerot, 2010), and in a review of lake studies from 11
European countries (Brucet et al., submitted for publication). Fish size
has been mainly related to altitude, air temperature and amplitude of
temperature, whereas trophic state was of little importance in a large
study of European lakes (Brucet et al., submitted for publication). Lack of
crude data on body sizes (instead of proportions of size classes) prevents
us from incorporating several of these studies in our analysis, but the
findings support the pattern of a reduction in the mean body size of fish
communities with decreasing latitude and increasing temperature.
The body size difference associated with latitude seems clear at the as-
semblage or community level, whereas the pattern at population level is
more ambiguous (Jeppesen et al., 2010a), probably as a result of contingent
effects of species-specific biology and biotic interactions. Typical temperate

fish species, such as roach (Rutilus rutilus) and perch (Perca fluviatilis), show
different responses with latitude; perch having the strongest decrease in
mean body size with decreasing latitude or increasing temperature, while
the mean body size of roach does not exhibit any such changes (Jeppesen
et al., 2010a).
Overall, data on changes in the body size of macroinvertebrates along spatial
gradients or changing temperatures are still too scarce and fragmented to
permit the drawing of firm conclusions (Fig. 1T), highlighting another im-
portant research gap that merits further work.
Using species lists and occurrence data on diving beetles (Coleoptera,
Dysticidae) in more than 400 Canadian lakes and ponds, Vamosi et al.
(2007) found that the proportion of large species tended to increase at higher
latitudes (along a narrow gradient: 49–55oN). Along an elevation gradient,
both the proportion of large species and total species richness peaked at
mid-altitudes, being exceptionally low at high altitudes (above 2000 m).
The authors attributed this to oxygen limitation and low productivity at high
altitude locations, overriding the expected temperature effect for body sizes
and species richness. In the cross-comparison study of subtropical and tem-
perate shallow lakes, the taxa occurring in the former were characterized by
either very small or very large body sizes (such as shrimps, applesnails, cray-
fish, etc.), whereas the taxa in the set of temperate lakes covered a far wider
range in body sizes (Meerhoff et al., 2007a).
2.4.3 Zooplankton
A comprehensive review has shown that cladoceran mean body size de-
creases towards lower latitudes (n ¼ 1100 water bodies, latitudinal gradient
between 81 N and 77 S, Gillooly and Dodson, 2000) (Fig. 1U), a pattern
mostly driven by differences in body size of individual species of three large
and dominant pelagic genera (Daphnia, Ceriodaphnia and Diaphanosoma). In
South America, zooplankton mean body size (length), as well as the body
size of different taxonomic and functional groups, decreased from temperate
to tropical lakes (Lacerot, 2010). This pattern was generated by large differ-
ences in the body length of pelagic cladocerans, particularly Ceriodaphnia,
Moina, Daphnia and Diaphanosoma genera (Lacerot, 2010). Along a latitudi-
nal gradient in Turkey, the mean body size of Cladocera was larger in the
higher latitude lakes (M.Beklioğlu et al., unpublished data). In contrast,

despite large differences in biomass, cladoceran zooplankton body size did
not vary along climate regions in the European latitudinal gradient analysis
by Gyllström et al. (2005), although the large-bodied Daphnia spp. were
scarce in the warmer lakes. Lack of large pelagic or littoral genera occurred
in freshwater subtropical lakes, whereas these taxa were common in similar
temperate lakes (Meerhoff et al., 2007b). Similarly, in European brackish
shallow lakes, the normalized biomass size spectra of zooplankton exhibited
a unimodal pattern with dominance of rotifers in the Mediterranean lakes,
whereas cold Danish lakes showed a bimodal distribution, with the second
dome corresponding to cladoceran and copepod species (Brucet et al., 2010)
(Fig. 6).
2.4.4 Macrophytes
Being a variable most often ignored in the plant community, we found no
data reporting changes in plant body size or data allowing us to indirectly
estimate body size (e.g. ratio biomass:cover) in the SFTS or in geographically
isolated literature.
2.4.5 Phytoplankton
Phytoplankton body size variation with latitude is seldom reported in em-
pirical literature, despite the fact that cells and colonies are routinely mea-
sured to estimate biovolume, one of the most typical proxies for
phytoplankton biomass (Kruk et al., 2010). Although individual sizes are
not available in the literature to construct a latitudinal gradient (Fig. 1V),
we compared the biovolume distribution of different size classes of phyto-
plankton species in shallow lakes in two contrasting climates (subtropical
Uruguay and temperate The Netherlands, see Appendix C for a description
of the methodology). We found no significant differences in the biovolume
of the different size classes, despite a higher total biovolume of phytoplank-
ton in the subtropical lakes (see Biomass). In mesocosm experiments study-
ing the effects of fish addition and nutrient loading on shallow lakes
distributed from Finland to southern Spain (Moss et al., 2004), fish shifted
the phytoplankton assemblage composition towards smaller phytoplankton,
especially chlorophytes and cyanobacteria, presumably by removing large-
bodied grazers; however, this effect was not affected by latitude (Moss
et al., 2004; Stephen et al., 2004).
Temperate Mediterranean
400 200
Lund Fjord (0.3 ‰) Nauplii Salins (0.4 ‰)
F = 6.2 Rotifera F = 20.0
m = 2.3 Copepoda m = 1.3
300 150
Cladocera
200 100
100 50
0 0
200 50
Selbjerg (0.5 ‰) Sirvent (0.8 ‰)
F = 42.5 F = 10.1
m = 0.5 40 m = 1.7
150
30
100
Zooplankton abundance (ind L–1)
20
50
10
0 0
400 40
Glombak (1.2 ‰) Bassa Coll (1.6 ‰)
F = 5.4 F = 5.9
m = 2.3 m = 1.6
300 30
200 20
100 10
0 0
12,000 500
Østerild (3.8 ‰) Ter Vell (2.2 ‰)
6000 F = 2.0 F = 40.0
800
m = 1.0 400 m = 0.9
600 300
400 200
200 100
0 0
-7.5
-6.5
-5.5
-4.5
-3.5
-2.5
-1.5
-0.5
0.5
1.5
2.5
3.5
-7.5
-6.5
-5.5
-4.5
-3.5
-2.5
-1.5
-0.5
0.5
1.5
2.5
3.5
Zooplankton size class (log2 µg DW)
Figure 6 Zooplankton size distribution in temperate (left column) and Mediterranean

(right column) brackish shallow lakes, showing the abundance contribution of nauplii,
Rotifera, Copepoda and Cladocera (each group shown with a different grey tone). Each
panel represents a lake, indicating the respective salinity (%), mean zooplankton size
diversity (m) and mean fish density (F, ind m 2). Modified from Brucet et al. (2010).
2.4.6 Periphyton
Neither in the SFTS studies nor in the geographically isolated studies used in
our previous meta-analysis have we found published data on periphyton size
structure in shallow lakes, preventing us from constructing our own gradient.
We found a relatively large number of lakes with data available on body size
(cell biovolume) of bacterioplankton (n ¼ 48), allowing us to construct a da-
tabase for the meta-analysis. However, all are derived from two extreme
geographic locations and showed strong variability, and no trend in body
size could be associated with latitude (Fig. 1X). Nevertheless, a wide range
of variation for the tropical locations was observed, indicating either that this
trait in bacterioplankton may be more linked to local conditions than to lat-
itude or that variations in this trait are constrained along latitudinal gradients.
2.5. Climate effects on reproduction and growth

2.5.1 Fishes
Animals with indeterminate growth experience a life history trade-off in re-
source allocation between onset and duration of reproduction, fecundity,
growth and survival (Gunderson and Dygert, 1988; Heino and Kaitala,
1999). Three primary life history strategies representing essential trade-offs
among those demographic parameters, namely, opportunistic, equilibrium
and periodic, have been proposed for freshwater fishes (see Winemiller and
Rose, 1992) and interpreted as being adaptive to the relative predictability
and variability of the environment (Winemiller, 2005).
Most of the large-scale studies of intraspecific variation in the life history
traits of fishes focus on single species, grouping populations from lentic and lo-
tic habitats (e.g. Heibo et al., 2005; Lappalainen and Tarkan, 2007; Lappalainen
et al., 2003, 2008), with very few studies on life history traits of whole fish
assemblages at a continental level (Mims et al., 2010). Different hydrological
characteristics of rivers and lakes could potentially influence life history traits
in a variety of ways (Lytle and Poff, 2003); however, the work by Blanck
and Lamouroux (2007) noted only a slight effect of habitat type on life
history traits within European freshwater fishes. In shallow lakes, responses
of life history traits of fishes to warming, among other responses, have been
reviewed by Jeppesen et al. (2010a). With variations among communities
and species-specific responses, empirical evidence indicates that higher-
latitude populations grow more slowly, mature later and have longer life
and reproductive spans and a greater maximal size than populations at lower
latitudes or higher temperatures (Jeppesen et al., 2010a). Reproductive seasons

are limited to periods of the year when limiting physical factors, typically
temperature, permit the survival of offspring (Conover, 1992). In temperate
systems, most freshwater fish species have seasonal reproduction, with peaks
in spring or summer (Wootton, 1984). Breeding and growing seasons,
growth rate, number of reproductive events per year and annual
reproductive investment are often negatively related to latitude (Fig. 7,
Table 4). Smaller, short-lived species with generally opportunistic strategies
are more abundant at low latitudes, whereas large, longer-lived species with
generally periodic or equilibrium strategies predominate at high latitudes,
according to a very comprehensive study of North American fishes (Mims
et al., 2010). The general pattern of variation in life history traits with
latitude (Fig. 7, Table 4) seems to be common for fishes of inland waters
(Conover, 1992; Gotelli and Pyron, 1991; Hubbs, 1985; Morin et al., 1982;
Length breeding and growing seasons

Annual reproductive investment
Reproductive events per year
Opportunistic
Reproductive lifespan
Age and size at maturity
Longevity
Periodic-equilibrium
Latitude
Temperature
Figure 7 Expected changes in the main life history traits of fish along a temperature and
latitudinal gradient based on our review of literature from inland water systems. With
increases in temperature, longer breeding and growing seasons, annual reproductive
investment and more reproduction events are predicted; a longer reproductive lifespan,
greater age and size at maturity and longevity being negatively related with tempera-
ture. See text for details and supporting literature.
Table 4 Evidence of variation in reproductive life history traits of fishes with latitude,
indicating example species and respective publications
Life history traits Example species Respective reference
Length of breeding and Jenynsia multidentata Goyenola et al. (2011),
growing seasons Sander lucioperca Lappalainen et al. (2003), and
Micropterus salmoides Rogers and Allen (2009)
Annual reproductive Jenynsia multidentata Goyenola et al. (2011) and Heibo
investment Perca fluviatilis et al. (2005)
Reproductive life span Rutilus rutilus Lappalainen and Tarkan (2007)
and Lappalainen et al. (2008)
Age and size at maturity Salvelinus alpinus Malmquist (2004) and Venne and
Magnan (1989)
Longevity Perca fluviatilis Heibo et al. (2005)
Please see conceptual Fig. 7 for the expected changes.
Paine, 1990; Reznick et al., 2006) as well as marine habitats (Vila-Gispert et al.,
2002).
Patterns on latitudinal changes in reproduction traits of invertebrates in di-
verse water bodies along a latitudinal gradient (12 N to 30 S) show that life
history traits are highly variable and very likely influenced by regional and
local factors (Hart, 1985). Despite this, recruitment seems to be more con-
nected with seasonality in temperate climates, as evidenced by the greater
timing flexibility in reproduction observed at low latitudes. Most of the
evidence for this pattern comes from lotic environments and supports
the same general trends as observed for fish, where larger body sizes,
later maturity, fewer broods and larger embryos of some macroinver-
tebrates seem more common towards higher latitudes (reviewed by
Sainte-Marie, 1991).
2.5.3 Zooplankton
We found few works on changes in zooplankton reproduction associated
with a latitude or altitude gradient. An increase in autumn temperatures,
as projected by different climate models, can switch the reproduction of
zooplankton from sexual to asexual, resulting in a lower genetic diversity
of these organisms (Chen and Folt, 1996). Likewise, studies of sediments
from shallow lakes from Greenland to Spain have shown a 100-times decline
in the ratio of resting eggs to carapaces of the pelagic microcrustacean
Bosmina spp., strongly correlated with changes in summer air temperature,
while Chl-a (food resources) and fish density (predation) explained a com-
paratively minor proportion of the variation (Jeppesen et al., 2003). Studies
of chydorids have also shown higher egg:carapace ratios in cold lakes than in
warmer waters (Sarmaja-Korjonen, 2003).
2.5.4 Macrophytes
Macrophytes display a range of overwintering strategies (e.g. either in the water
column or as seeds, tubers or turions in the sediments), which are differently
affected by changes in ambient temperature, particularly in winter. In compar-
ison to other lake communities, there is relatively little information published
on phenological changes in macrophytes as a consequence of warming. Both
longer (Jeppesen et al., 2010b) and shorter growing seasons (Barko and Smart,
1981) have been reported. At higher temperatures, an enhanced growth rate of
submerged macrophytes allows a quick access to the water surface (Barko and
Smart, 1981), leading to deeper colonization depths and higher biomass
(Rooney and Kalff, 2000). Various studies have indeed found deeper
colonization depths towards the equator (Duarte and Kalff, 1987; Kosten
et al., 2011b). Duarte and Kalff (1987) attributed the difference in
colonization depth to higher irradiance in the tropics. Maximum daily
irradiance (which is a combination of light intensity and day length),
however, does not vary substantially between lower and higher latitudes
(Lewis, 1986). Another factor in favour of the temperature effect is the
finding in Canadian lakes where colonization depth increased during a
relatively warm year, in spite of increased turbidity (Rooney and Kalff,
2000). Mesocosm investigations have also shown enhanced macrophyte
growth as a result of high temperature-mediated reduction in water level
(Bucak et al., 2012). Nevertheless, changes in periphyton densities, likely
affected by alternate trophic web configurations under different climates
(Meerhoff et al., 2007a), may also partially explain changes in colonization
depth (Kosten et al., 2011b and references therein).
2.5.5 Phytoplankton, periphyton and bacterioplankton

Life history traits of other assemblages, such as of phytoplankton, periph-
yton and bacterioplankton, appear less frequently in the SFTS literature.
For instance, studies on phytoplankton growth rates along latitudinal
transects mainly belong to the marine realm (e.g. Marañón et al.,
2000). One of the reasons lies in the microscopic and unicellular type of
life of these organisms, in which sexual reproduction is typically absent or
rare. Most of the studies on phytoplankton reproduction deal with par-
ticular species (e.g. Hickel, 1988; Jewson, 1992), without covering many
species or their change in different regions, despite the circumstance that
this might be important for understanding some community processes
(Eilertsen and Wyatt, 2000). Furthermore, it is relatively easy to
develop laboratory experiments to evaluate the effects of temperature
on microorganism growth (e.g. Butterwick et al., 2005), thus making
perturbation experiments a more common approach than the SFTS.
2.6. Climate effects on intensity of trophic interactions

Climate warming may affect not only species performances and community
traits but also species interactions. Interspecific interactions within food
webs or other multi-species networks are highly underrepresented within
the context of climate change research (Woodward et al., 2010b), not least
in shallow lakes (but see Meerhoff et al., 2007a). Indication of changes in the
intensity of trophic interactions may be obtained from certain indexes that
typically include ratios of biomass or densities between predator–prey pairs
relevant to shallow lake functioning (e.g. piscivorous fish:planktivorous fish,
zooplankton:phytoplankton biomass ratio) (e.g. Jeppesen et al., 2000), or
between groups of known different sensitivity to predation (such as motile
organisms) and the total amount of potential prey (e.g. Meerhoff et al.,
2007a). Also, the changes in size distribution of potential prey are used as
indicators of predation pressure (e.g. Brucet et al., 2010).
Evidence from SFTS studies indicates a clear difference in the strength of
trophic interactions with increasing temperature in shallow lakes. A stronger
predation pressure by fish under warm conditions was supported by cross-
comparison studies where littoral trophic interactions in subtropical and
temperate lakes were compared (Meerhoff et al., 2007a). Several predation
indexes constructed based on different sensitivities to predation by several
groups, such as the proportion of small fish, the proportion of small snails,
the proportion of chironomids, and the proportion of Daphnia relative to
small cladocerans (Meerhoff et al., 2007a), suggest stronger effects of fish
predation in warm lakes than in similar temperate lakes. The predation pres-
sure exerted by planktivorous fish, particularly on zooplankton (and also on
macroinvertebrates), increases with increasing temperature, as also found in
European (Gyllström et al., 2005) and South American (Lacerot, 2010) lat-
itudinal gradient analyses, and in cross-comparison studies (Brucet et al.,
2010, 2012; Meerhoff et al., 2007a, b) (Fig. 8). Mesocosm experiments

conducted from Finland to southern Spain (Moss et al., 2004) have
revealed significant effects of fish on the community structure of
zooplankton and phytoplankton (leading towards dominance of smaller
algae) along this latitudinal gradient. However, this effect of fish was not
influenced by latitude (Moss et al., 2004; Stephen et al., 2004), possibly
due to the similar density of fish stocked in all experimental locations.
Cross-comparison studies on Daphnia ephippia in sediments of subtrop-
ical and temperate shallow lakes indicated that they are also present in warm
lakes despite being almost absent from contemporary water samples (Iglesias
et al., 2011). These findings support the hypothesis that the typical lack of
Daphnia in warm climates is more a consequence of high predation rather
than of metabolic constraints (Havens and Beaver, 2011; Iglesias et al.,
2011; Meerhoff et al., 2007a). Anti-predator behavioural responses by
zooplankton also change with climate and the differential associated risk
of predation by fish (Brucet et al., 2010; Meerhoff et al., 2007b;
Tavsanoğlu et al., 2012).
Most likely as a consequence of increased predation by fish, the size dis-
tribution and composition of zooplankton in warm lakes typically change
towards dominance of smaller taxa and individuals (Brucet et al., 2010;
Gillooly and Dodson, 2000; Iglesias et al., 2011; Lacerot, 2010; Meerhoff
et al., 2007b); consequently, the capacity of zooplankton to control
phytoplankton crops (estimated as the zooplankton:phytoplankton
biomass ratio) may decrease with increasing temperature or decreasing
latitude (Gyllström et al., 2005) (Fig. 8). This last pattern occurred in all
freshwater studies we examined, regardless of approach (i.e. latitudinal
gradient, cross-comparisons), geographic areas, and use of different
biomass estimators (Fig. 8). In brackish lakes, the zooplankton:
phytoplankton biomass ratio remained low throughout the year in the
temperate regions, whereas the ratio was markedly higher in winter than
in summer in the Mediterranean lakes, likely reflecting shifts in
zooplankton and fish structure related to a fluctuating hydrology (Brucet
et al., 2009). The occurrence of macrophytes in the lakes seems to
enhance the grazing pressure of zooplankton in intermediate and cold
regions (most likely indirectly via the provision of refugia from fish
predation), while no or negligible effect of plants appears at low latitudes
(Meerhoff et al., 2006, 2007b; Muylaert et al., 2010; Tavsanoğlu et al.,
2012). Similar patterns were found in the gradient analysis in South
Fish:zooplankton biomass (CPUE: mg L–1)

60 1800
A
50 1500
Fish:zooplankton biomass
40 1200
30 900
20 600
10 300
0 0
4
Uruguay–Denmark (2007) B
South America (2009)
Zoo:phytoplankton biomass
Europe (2005)
3 Europe (2010)
Denmark–Canada (2007)
Spain–Denmark (2009)
0.03 0.06
0
Tropical Warm Temperate Cold
Figure 8 Variation in consumption pressure along a climate gradient, estimated as bio-
mass ratios. (A) predation pressure of planktivorous fish on zooplankton (fish:zooplank-
ton biomass) and (B) grazing pressure of zooplankton on phytoplankton (zoo:
phytoplankton biomass). The latitudinal gradient corresponds to ranges from 5 to
55 S and from 38 to 64 N in Europe and America. Data were grouped in wide climate
types: Tropical (Brazil), Warm (intermediate Argentina, Uruguay and Spain), Temperate
(Denmark, Belgium, The Netherlands, UK and Poland) and Cold (Estonia, Sweden,
Finland, Canada and southern Argentina). Zooplankton (either densities or biomass)
median values were extracted from the literature and converted into biomass when
necessary, according to Jeppesen et al. (1994). Full lines connect the points belonging
to the same paper (see symbols). Values were extracted from (A) Fig. 6 in Gyllström et al.
(2005) and Table 2 and Fig. 2 in Meerhoff et al. (2007a) and (B) Fig. 6 in Gyllström
et al. (2005), Fig. 6 in Brucet et al. (2009), Fig. 2B in Jackson et al. (2007), Fig. 4 in Muylaert
et al. (2010) and Fig. 7A in Kosten et al. (2009a). Error bars are 1 SE.
America (Kosten et al., 2009c), where the zooplankton grazing pressure

decreased from cold to warm regions; the patterns were, however,
influenced by macrophytes and the abundance of fish.
Despite lower total abundances, the relative abundance of herbivorous
plant-associated macroinvertebrates was higher in the subtropical climate
than in the temperate communities (Meerhoff et al., 2007a). This could im-
ply that a larger proportion of the macroinvertebrates, besides the large num-
bers of small omnivorous fish, is feeding on periphyton and macrophytes
under warmer conditions. On an evolutionary timescale, this could explain
the increase in chemical defences of macrophytes at low latitudes, as
suggested by Morrison and Hay (2011). On the other hand, grazing can af-
fect periphyton by diminishing its biomass and changing taxonomic or
group composition: grazing-mediated changes in composition have been
revealed in a study showing a shift to dominance of fast-growing or resistant
species (Sumner and McIntire, 1982).
Fully controlled experiments testing fish-mediated trophic cascading ef-
fects in shallow lakes under different climates are limited to a few meso-
cosm investigations. Trophic cascades seem to be weaker in tropical
mesocosms, with stronger fish effects on nutrient cycling promoting a more
pronounced bottom-up effect than in temperate mesocosms (Danger et al.,
2009). Another conclusion of the cross-comparison of littoral food webs
was that trophic cascades (concomitant with stronger fish predation pres-
sure) from fish to the bottom of the webs were weaker and with relatively
direct effects (perhaps reflecting shorter path lengths through the more re-
ticulate food webs) on most prey communities (Meerhoff et al., 2007a)
(Fig. 9).
3. DISCUSSION
3.1. Can we predict changes in community traits with
warming?
So far, we have attempted to detect whether common patterns of change in
community traits as a response to changes in temperature emerge from the
empirical SFTS literature: some traits of a few communities changed in
accordance to theoretical predictions, but for most organizational levels,
responses were often unclear or non-linear, and only partly supported pre-
dictions. Below, we contrast our findings with theoretical expectations and
compare them with findings from other research approaches.
Temperate Subtropical
Piscivorous fish
Other fish
Shrimps
Lit. invertebrates (c.) (×10)
Pel. invertebrates (c.) (×10)
Lit. invertebrates (h.) (×102)
Cladocerans (×103)
Periphyton
250 200 150 100 50 0 50 100 150 200 250
Density (ind m–2 / mg Chl-a m–2)
Piscivorous fish
Piscivorous fish
Other fish
Other fish Shrimps (omnivorous)
Lit. invert. (c.) Pel. invert. (c.)
Lit. invert. (h.)

Cladocerans Lit. invert. (c.)
Lit. invert. (h.) Pel. invert. (c.)

Phyto
Periphyton Cladocerans
Phyto
Periphyton
Figure 9 Structure of main communities in temperate (left) and subtropical (right) shal-
low lakes. (Above) Density of potentially piscivorous fish, all other fish, shrimps, littoral
carnivorous invertebrates (Lit. invert. (c)), pelagic carnivorous invertebrates (Pel. Invert
(c)), littoral herbivorous macroinvertebrates (Lit. invert. (h)), cladocerans and biomass of
periphyton. (Below) Simplified scheme of trophic interactions among the same trophic
groups. The densities in the subtropics are expressed relative to those in the temperate
lakes (considered as the unit). Except fish, the same taxa share the same trophic clas-
sification in both climate zones. Shrimp relative density is dashed due to shrimp ab-
sence in the temperate lakes. Phytoplankton (Phyto) box has the same size as it was
fixed in the study (surrogate of turbidity) by pairing the lakes in both climates. Data
are sample means of five selected lakes and error bars (above) show the standard error.
Modified from Meerhoff et al. (2007a).
3.1.1 Congruence of SFTS findings and theoretical expectations

Some of the shallow lake communities surveyed here clearly followed the
predictions of an increase in richness with an increase in ambient tempera-
ture (Allen et al., 2002), namely, fish, phytoplankton, and periphyton;
whereas macroinvertebrates and cladoceran zooplankton (at genera level)
typically showed the opposite trend, and no clear response could be iden-
tified for macrophytes and bacterioplankton. Fish taxonomic richness
exhibited the clearest pattern (meta-analysis by González-Bergonzoni
et al., 2012; Fig. 1A), with a significant positive relationship with decreasing
latitude. Macroinvertebrate richness data are often not available at species
level and latitudinal studies show ambiguous trends, besides being

commonly based on pooled data from lakes and streams (e.g. Heino,
2009). In studies including only shallow lakes, however, we found an oppo-
site trend to the expected response (at genus and family levels) (Fig. 1B), with
lower local taxon richness in warm lakes (e.g. Brucet et al., 2012; Lewis,
1996; Meerhoff et al., 2007a). Most of the reviewed articles also described
a decrease in local cladoceran zooplankton richness (at genus level) at
warmer locations (e.g. Brucet et al., 2010; Meerhoff et al., 2007b, Pinto-
Coelho et al., 2005) (Fig. 1C). Whether similar or contrasting latitudinal
richness patterns occur at species level remains unresolved for these
groups. However, richness at different taxonomic resolutions (e.g. species
and genera) tends to be highly correlated, as found for, for example,
terrestrial vegetation (Enquist et al., 2002), macroinvertebrates (Heino and
Soininen, 2007) and phytoplankton (Gallego et al., 2012) and as predicted
by theoretical models (Allen et al., 2002).
Microorganisms, ranging from phytoplankton to bacteria, however, are
usually considered to either lack or display only weak latitudinal gradients in
richness, because of their high abundances and small sizes, enabling them to
disperse easily over few geographical barriers and over large distances
(Fenchel and Finlay, 2004; Finlay, 2002; Hillebrand and Azovsky, 2001,
but see Van der Gucht et al., 2007). The distribution of these groups is
suggested to be more strongly driven by local environmental factors
(Baas-Becking, 1934; Beisner et al., 2006; Kruk et al., 2009; Ptacnik
et al., 2010a,b) than by latitudinal gradients. In our review, however,
phytoplankton and periphyton richness increased with decreasing latitude
(or rising temperature) (Fig. 1D and E). It has been suggested that most
microbial biodiversity is hidden from our observation, because most
species will occur at densities below current limits of detection (de Wit
and Bouvier, 2006); a limitation increasingly overcome by the application
of massive tag-sequencing, which allows for the detection of the
microbial components of the so-called rare biosphere (Purdy et al., 2010;
Sogin et al., 2006). In our analysis, bacterioplankton richness did not
show any clear trend, maybe reflecting the narrow geographic range of
the available data (i.e. temperate regions) or, alternatively, the suggested
stronger effect of local factors on this diverse group.
MTE predicts a decrease in community biomass and density with an
increase in ambient temperature, due to the enhanced metabolic demands
and consequent limitation of resources for individuals (Brown et al.,
2004; Fig. 1, Table 1). In our review, only periphyton biomass and
macroinvertebrate and zooplankton densities showed a significant decline

with decreasing latitudes (Fig. 1K, N and R).
Fish biomass and density showed the opposite pattern (Fig. 1G and M),
with a clear increase towards low latitude locations as found in several studies
applying different approaches (e.g. Brucet et al., 2010; Gyllström et al.,
2005; Meerhoff et al., 2007a; Teixeira-de Mello et al., 2009; see Table 2
for a summary). This is an intriguing phenomenon, since the potential
co-variation of lake productivity with latitude was considered in the
respective studies (i.e. comparing lakes with similar TP ranges in Brucet
et al., 2010; Gyllström et al., 2005, Teixeira-de Mello et al., 2009) and in
the data we extracted from the literature. Besides, we found no evidence
for limitations of specific nutrients or productivity gradients associated
with latitude (reviewed in Section 1.3). Increases in fish biomass and
abundance with temperature have also been reported recently from
Icelandic geothermal streams, which span a broad thermal gradient within
a single catchment (Woodward et al., 2010a).
The meta-analyses of zooplankton (in this case, cladocerans and cope-
pods), however, yielded no significant relationship between biomass and
latitude despite that the expected trend of reduction occurred in most
reviewed studies (e.g. Gyllström et al., 2005; Havens et al., 2007;
Jackson et al., 2007; Meerhoff et al., 2007b; Pinto-Coelho et al., 2005;
Vakkilainen et al., 2004).
Contrary to the predictions by MTE, warmer conditions have been ar-
gued to lead to higher phytoplankton biomass and yield (Lewis, 1996), not
least in shallow lakes. This has been explained by longer growing seasons
(Lewis, 1996, 2000), increased availability of phosphorus from internal
loading (Jeppesen et al., 2009; Sndergaard et al., 2003) and smaller size
of zooplankton grazers (Meerhoff et al., 2007b), resulting in lower
grazing pressure as suggested in our review (e.g. Gyllström et al., 2005;
Kosten et al., 2009c; Meerhoff et al., 2007a; Fig. 8). In our analysis of
large databases from two contrasting climates, we did find higher total
phytoplankton biovolume and higher total biovolume of cyanobacteria in
subtropical climates than in similar temperate lakes (Fig. 2), as reported in
studies following other approaches (Paerl and Huisman, 2009). The
general pattern was, however, not maintained for other phytoplankton
biomass proxies, such as Chl-a concentration (Fig. 1J), as also reported by
Kosten et al. (2012). The typical absence of counts of phytoplankton and
periphyton in the shallow lake literature prevented us from testing
density predictions on these communities.
The estimation of bacterial biomass relies on the application of conver-

sion factors to translate the volume assessments into carbon values, and these
factors are not yet fully established, leading to widely varying estimations
when applying the different proposed values to the same dataset (e.g. Posch
et al., 2001). Therefore, bacterioplankton does not seem to be the most ap-
propriate portion of the community with to test predictions of changes in
biomass with warming at present, at least not with the information found
in this review. Nonetheless, bacterioplankton still showed a significant in-
crease in density with decreasing latitudes (i.e. increasing temperature)
(Fig. 1R). According to our findings, higher temperatures could promote
higher bacterioplankton density both through a direct effect (via accelera-
tion of metabolic rates leading to enhanced multiplication) and indirect
effects (e.g. via increasing substrate availability, DOC) (Fig. 5). Higher
temperatures could also promote competitive advantages for bacteria over
algae (Carey et al., 2012; Yvon-Durocher et al., 2011a). The fact that
temperature and Chl-a appeared in our regression model as separate
factors supports the hypothesis that the effects of temperature and
resource availability on bacterial biomass production are independent
(Lopez-Urrutia et al., 2006).
Freshwater communities, and particularly shallow lake communities,
seem to be strongly size structured (Hildrew et al., 2007), as recognized
in the pioneering works on the effect of fish predation on the size structure
of zooplankton in ponds (Brooks and Dodson, 1965; Hrbacek et al.,
1961). Different trends of changes in body size with temperature could
be expected according to several theories, which are not necessarily
mutually exclusive (see Section 1, Fig. 1, Table 1 and Daufresne et al.,
2009). In our review, fish and zooplankton communities showed a
reduction in mean body size with increasing temperatures (Fig. 1S
and U, for fish and zooplankton, respectively), supporting the
predictions by MTE (Brown et al., 2004) and the “temperature-size”
rule (Angilletta, 2009). Bacterioplankton body size, however, revealed
no relationship with latitude or temperature, but the data were
geographically too restricted and the variability too large to allow
detection of latitudinal gradients. The lack of sufficient data for four of
our target communities (i.e. macroinvertebrates, macrophytes,
phytoplankton and periphyton) prevented us from generalizing a trend
for real lake communities. Moreover, at the population level, different
mechanisms may occur across latitudinal gradients as predicted by
several theories, leading to a decrease in the mean body size of
populations with a concomitant reduction of mean body size across the

community as a whole (Daufresne et al., 2009). At the community
level, a decrease in average body size with increasing temperature may
also reflect competitive exclusion of larger species, size-selective
predation (e.g. Brooks and Dodson, 1965) or a reduction of the density
of larger species due to inefficient energy transfer along the food web
with increasing temperatures (Arim et al., 2007). These mechanisms,
however, would not necessarily appear across latitudinal gradients due
to local variations in the amount of resources available and the thermal
setting in which the communities develop. The trends we found in the
SFTS literature mostly refer to changes at assemblage or community
level and may thus reflect the effect of temperature through a variety of
mechanisms or likely the combined effect of temperature and inter-
specific interactions.
3.1.2 Evidence of warming effects obtained by other approaches

Other approaches (e.g. perturbation experiments) to study the potential
effects of climate change have shown no effects of increased temperature
on richness of some freshwater communities. In outdoor heated mesocosms,
cladoceran diversity (McKee et al., 2002a) and phytoplankton richness (Moss
et al., 2003) were not significantly affected by experimental warming, al-
though measures of community evenness increased (McKee et al., 2002a).
Warming, rather than affecting macrophyte richness, may promote a switch
from submerged to free-floating macrophyte dominance in shallow eutro-
phic lakes, as reported mainly from perturbation experiments (Feuchtmayr
et al., 2009; Netten et al., 2010) and previously suggested by models
(Scheffer et al., 2003). Warming may thus promote a polewards expansion
of the geographical distribution of this type of plants (Scheffer et al., 2003),
with potential strong and negative consequences for local biodiversity.
In passively warmed mesocosms in alpine regions, zooplankton biomass was
suppressed due to the decline in large cladocerans, even in the absence of fish
(Strecker et al., 2004). At the same time, warming did not affect total phyto-
plankton biomass but significantly altered the assemblage composition by
favouring fast-growing phytoflagellates over larger filamentous green algae,
supporting the hypothesis that moderate warming can destabilize plankton dy-
namics in shallow cold-water ecosystems (Strecker et al., 2004). An experimen-
tal increase in temperature in mesocosms had also very minor effects on
phytoplankton Chl-a and total biovolume, although it significantly decreased
the biovolume of Cryptophyceae and Dinophyceae and did not affect the
abundance of cyanobacteria as might be expected (Moss et al., 2003). No

obvious effects on the densities of zooplankton (McKee et al., 2002a) and
macroinvertebrates (Feuchtmayr et al., 2007; McKee et al., 2003) were
observed, suggesting that the overall abundances of most invertebrate taxa
will not be severely affected by the predicted temperature rise (Feuchtmayr
et al., 2007; but see Dossena et al., 2012). In contrast, in another series of
outdoor heating experiments, warming shifted the composition and
distribution of phytoplankton size and biomass from assemblages of large
individuals with high standing biomass to assemblages with low standing
biomass and many smaller-bodied species, including small cyanobacteria
(Yvon-Durocher et al., 2011a). In this case, however, such an effect did not
occur in the distribution of size and biomass of zooplankton. Warming thus
seems to lead to reorganization of the biomass structure in both the benthic
and planktonic assemblages (Dossena et al., 2012; Yvon-Durocher et al.,
2011a), at least in experimental, relatively simple, food webs with fixed
fish densities.
In contrast to our findings (Fig. 1R), in experimental outdoor meso-
cosms, the abundances of picoalgae, bacteria and heterotrophic
nanoflagellates changed in a similar manner over time, with no direct effect
of experimental warming (Christoffersen et al., 2006). However, experi-
mental warming modified the effects of nutrient additions (Christoffersen
et al., 2006; Özen et al., 2012), indicating that interactive effects may be
significant in the future given the current and expected increase in
nutrient loading to many shallow lakes worldwide (Jeppesen et al., 2009,
2010b; Moss et al., 2011). The difference between our findings and these
experimental studies may reflect the co-variation in nutrient availability
(i.e. DOC) and temperature found in our data (Appendix B) rather than
different direct effects of temperature on bacterioplankton populations.
A meta-analysis of the effects of warming on body size of ectothermic
aquatic organisms, from the individual to the community level, revealed a
significant increase in the proportion of small species and organisms at
warmer temperatures (Daufresne et al., 2009), as we have found for fish
and cladoceran zooplankton (Fig. 1S and U). A study of Cladocera subfossil
distribution in 54 European lakes located in different climates showed that
small species dominated warm water lakes with high conductivity, macro-
phyte coverage and fish abundance. In contrast, large pelagic species were
more common in low-conductivity high-latitude lakes (Bjerring et al.,
2009). Higher summer temperatures have promoted a reduction in the
mean body size of temperate zooplankton (Moore et al., 1996), as also found
in heating experiments for phytoplankton communities (e.g. Sommer and
Lewandowska, 2011; Yvon-Durocher et al., 2011a). This effect was not
found in otherwise similar outdoor experiments, however (Moss et al.,
2003). The pieces of evidence showing a reduction in the body size of
organisms with increasing temperature suggest that the underlying size
structure of aquatic ecosystems might not be robust to global warming
(Yvon-Durocher et al., 2011a). The magnitude and sometimes direction
of change, however, seem to vary with taxonomic groups and
environmental conditions (Gardner et al., 2011). It should be also noted
that the spatial scale and range of body sizes under analysis may also affect
the generation and testing of congruent predictions (Tilman et al., 2004).
Our review of the SFTS literature revealed trends of a reduction in size at
maturity, life-span and the occurrence of more reproductive events in fish
towards warmer locations, and although the information on other commu-
nities is more scarce, it also suggests comparable changes in the reproduction
mode of zooplankton and macroinvertebrates (Section 2.5). In line with
these findings, experimental warming can influence the reproduction of fish
by affecting embryonic development time and offspring numbers
(unimodally linked to temperature) (e.g. Garcı́a-Ulloa et al., 2011). It can
also lead to a reduction in the body size at maturity, as reported for the cla-
doceran Simocephalus vetulus in heated mesocosms (McKee et al., 2002a).
Differential effects of temperature on life history traits such as fecundity, de-
velopment and survivorship will affect the overall fitness of organisms.
Mathematical models suggest, for instance, that warming will cause ecto-
thermic species with a high temperature sensitivity of development to reach
the age at first reproduction earlier in the year, potentially leading to mis-
matches between consumers and resources if the latter have a lower temper-
ature sensitivity of development (Amarasekare and Savage, 2012). Studies in
other heating experiments (outdoor tanks, Liboriussen et al., 2005) have
demonstrated the occurrence of a rapid microevolutionary response of
the cladoceran S. vetulus, in both survival and subcomponents of individual
performance (i.e. age at reproduction and number of offspring), suggesting
that populations may persist locally under the predicted scenarios of global
warming (Van Doorslaer et al., 2007). According to those results, such
microevolutionary responses may buffer changes in community structure
under climate warming and help explain the apparent lack of effects in some
experiments and field data.
3.1.3 The importance of local factors and trophic interactions

Local characteristics have a large potential of blurring latitudinal gradients in
traits of, at least, several communities. Some basic relationships, such as the
density–mass relationship, might be robust at the level of biomes or at a very
large range of body sizes but could exhibit large variations among local com-
munities (e.g. Arim et al., 2011; Hechinger et al., 2011; White et al., 2007;
but see, Brown et al., 2011; Layer et al., 2010; McLaughlin et al., 2010;
O’Gorman and Emmerson, 2010).
In particular, the strong imprint of biogeography and local factors may
override temperature-related effects on richness and could alter the
predicted trends. In many ecosystems, including shallow lakes, explanatory
variables that are potentially important as main drivers of local diversity tend
to be highly inter-correlated, such as productivity level and the abundance of
key structuring organisms, such as aquatic plants (Declerck et al., 2005) and
fish. Besides the potential influence of climatic factors such as the length of
the growing season, the annual input of solar radiation and the length of the
hydroperiod (Della Bella et al., 2008), local factors such as lake area (e.g.
Rorslett, 1991), sediment characteristics (Barko et al., 1991), maximum
depth, TP (Jeppesen et al., 2000) and nitrate concentration (James et al.,
2005) also have strong influences on plant species richness at local scales.
Trophic interactions may also indirectly affect submerged macrophytes
along latitudinal gradients: the positive effect of long ice cover on macro-
phyte coverage (e.g. Kosten et al., 2009a) may thus be due to a cascading
effect through anoxia causing fish kills (Jackson et al., 2007) and subsequent
stronger zooplankton and snail control on phytoplankton and periphyton
competitors (Jones and Sayer, 2003). The effect of warming on phytoplank-
ton and periphyton densities, however, also depends on the relative impor-
tance of trophic cascading effects, nutrient status and water residence time
(Sballe and Kimmel, 1987).
Our review highlights that several properties of the potential prey
communities, from richness to biomass and body size, indicate enhanced
predation pressure with increased temperatures. Temperature influences
the predator–prey interactions both directly and indirectly, either via
the alteration of predator feeding rates and feeding modes (Beisner et al.,
1996) or through changes in both prey and predator body size (Moore
et al., 1996; Woodward et al., 2010b). Experimental warming studies
measuring feeding intake rates at different temperatures have
demonstrated higher consumption of macroinvertebrates, both on other
invertebrates and on periphyton in warmer scenarios (Kishi et al., 2005).
Warming experiments have also shown that trophic cascade effects may vary
with temperature, due to physiological depression of predators (Kishi et al.,
2005).
Higher consumption by vertebrate and invertebrate grazers (Lazzaro,
1997; Meerhoff et al., 2007a) could thus also explain our observed local
patterns of richness of prey communities in warmer regions, the lower
macroinvertebrate densities and lower zooplankton density and mean
body size of zooplankton (Meerhoff et al., 2007a) as also suggested by
mathematical models (van Leeuwen et al., 2007) and confirmed in our
review (Fig. 8). The grazing pressure by zooplankton on phytoplankton
showed the opposite trend, being weaker at lower latitudes (Fig. 8).
The lack of a relationship or relatively weak latitude effect on
phytoplankton biomass could reflect local variations in contrasting
mechanisms. The final outcome may be the result at local scales of the
balance between temperature effects on metabolism, which should reduce
phytoplankton biomass, and the effects of longer growing seasons and
lower zooplankton grazing pressure, which would increase it. Ultimately,
our results indicate that overall the link between zooplankton and
phytoplankton weakens with increasing water temperature. Weak
interactions may dampen biomass oscillations between consumers and
resources (McCann et al., 1998), implying that not all responses at a
specific trophic level are propagated to lower trophic levels or have
significant impacts on ecosystem processes (Pace et al., 1999). An increase
in the duration of climatic variability effects due to food web interactions
seems possible, as the signal of winter climate can be detected in the clear
water phase (i.e. a reduction in phytoplankton biomass) in early summer
(Straile and Adrian, 2000) or in summer phytoplankton composition and
biomass (Blenckner et al., 2002; Weyhenmeyer, 2001) in temperate lakes.
Species higher in the food web are often especially sensitive to changes
in ambient temperature (Petchey et al., 1999; Woodward et al., 2010a,b).
The decline and maybe the extinction of a top predator, as a potential
consequence of warming, may significantly influence the effects of size-
structured interactions in food webs and ecosystem functioning. Other
temperature-related changes in fish structure and predation pressure
might also be expected. After conducting feeding experiments with the
omnivore fish species opalaye (Girella nigricans) at different ambient
temperatures, Behrens and Lafferty (2007) suggested that warming may
lead to changes in the diet of fish towards greater consumption and
assimilation of plant material. An increase in the relative proportion of
herbivorous and omnivorous species within the fish assemblage with

decreasing latitude has been found in meta-analyses of aquatic systems
worldwide, not least shallow lakes (González-Bergonzoni et al., 2012;
Jeppesen et al., 2010a), giving further support to the previous
hypothesis. This change in diet would result in food webs being more
truncated, as predicted both theoretically (Arim et al., 2007) and
empirically (Meerhoff et al., 2007a). Altogether, the evidence suggests
that food webs in temperate or cold shallow lakes will be affected by
warming, also due to the current lower number of feeding links (Fig. 9;
Meerhoff et al., 2007a) and the lower richness of top species (typically
fish) (Fig. 1A). As found in our review, however, the direction of
changes seems difficult to predict for the specific communities given the
different relative importance of direct or indirect effects of higher
temperature under specific local scenarios and the interactions with
other environmental stressors.
3.2. Advantages and disadvantages of the SFTS approach

The actual test of theoretical predictions with empirical data from shallow
lake literature represents a practical challenge relative to the heterogeneous
nature of currently available data. The description of different entities (e.g.
populations, communities) and the differences in taxonomic resolution (e.g.
species, genera, classes) make comparisons, in our case across studies and dif-
ferent communities, a challenging task (Yvon-Durocher et al., 2011b). Like
all other approaches, the SFTS approach has a series of advantages and dis-
advantages (many already summarized in Woodward et al., 2010b), as it
studies communities that have long been exposed to different temperatures,
rather than in a transient state in response to warming per se. Latitude is prob-
ably a better predictor of long-term regimes of climatic variables than cur-
rent climate values registered by local weather stations (Naya et al., 2008).
However, latitude may be correlated with other climatic (e.g. wind speed,
seasonality), ecological (e.g. day length and length of growing season), and
potentially also historical factors (e.g. biogeographical boundaries) that may
affect organisms’ physiology (Naya et al., 2008) and, with it, the observed
latitudinal patterns. Furthermore, climate is much more than temperature
alone, and other potential confounding processes interact with climate to
shape communities in lakes. Lake trophic state, as reflected by nutrient levels
(more commonly TP), affects community structure by augmenting the fish
densities and biomass in increasingly productive systems around the world
(Brucet et al., submitted for publication; Jeppesen et al., 2000, 2005; Mehner
et al, 2007; Teixeira-de Mello et al., 2009). Lake productivity thus often
overrides the effects of temperature on fish assemblage densities (e.g.
Brucet et al., submitted for publication; Mehner et al., 2007).
Experimental warming in outdoor mesocosms promoted an increase in
TP, total alkalinity, and conductivity, decreased pH and oxygen
saturation and increased the frequency of severe deoxygenation (McKee
et al., 2003). Several pieces of evidence also support the idea that
increasing temperature acts synergistically with eutrophication (e.g.
Feuchtmayr et al., 2007; Jeppesen et al., 2010b; McKee et al., 2003;
Moss et al., 2011), so these two key drivers could produce outcomes that
are not predictable from studying either in isolation.
Climate warming may lead to a higher frequency of dramatic changes in
water level, transforming permanent water bodies into temporary systems
(Beklioğlu et al., 2007) and leading to changes for the whole food web.
For example, strong differences in zooplankton assemblage structure
appeared between permanent and temporary shallow lakes of the same
wetland system, with higher diversity and lower density of large zooplank-
ton in permanent shallow lakes, which was attributed to a higher fish
predation pressure compared to temporary lakes (Brucet et al., 2005).
Warming may also promote an increase in salinity in shallow lakes due to
enhanced evaporation, especially in arid and semi arid climates (Beklioğlu
et al., 2007), saltwater intrusions into freshwater bodies (Schallenberg
et al., 2003) and enhanced use of freshwater for irrigation and industry under
a likely increased consumption pressure (Williams, 2001). Trophic structure
in shallow lakes typically changes along a salinity gradient (Brucet et al.,
2009, 2010; Jeppesen et al., 1994, 2007), as also shown in this review.
Indirect effects of climate warming, such as changes in salinity and
hydrology, could thus have larger consequences for the diversity, size
distribution and abundance of grazers of shallow lake ecosystems than
an increase in nutrients or temperature per se (Brucet et al., 2009, 2010).
Such shifts with increasing salinity and the subsequent decrease in
the top-down control on phytoplankton may negatively affect the
resilience of brackish lakes to the enhanced nutrient loading (Brucet
et al., 2010, 2012).
A further factor that potentially masks natural responses of aquatic com-
munities to temperature variations is the accidental or purposeful introduc-
tion of alien species (mostly fishes in freshwaters) by humans. The SFTS
approach has clear limitations as to predicting the impact of invasive species
associated with climate warming because a native species may become in-
vasive when expanded beyond its natural distributional range (as expected
for large free-floating plants, Scheffer et al., 2003), and we cannot presume
that ecological interactions among species will necessarily be similar in the
native and the foreign ecosystem. Climate warming also has the potential to
modify the impacts of invasive alien species by affecting the whole process
of invasion and further increasing ecosystem vulnerability (Rahel and
Olden, 2008). For instance, climate change may affect aquatic invasive spe-
cies by altering thermal regimes, reducing ice cover duration, altering
stream flow regimes, increasing salinity, and augmenting the demand for
water storage and conveyance structures (Rahel and Olden, 2008). Further-
more, potentially synergistic effects of climate warming and non-native spe-
cies make forecasting even more difficult (Woodward et al., 2010b). For
example, as pointed out by Rahel and Olden (2008), global climate change
will lead to an increase in water temperatures in northern-latitude lakes,
which may result in seasonally stressful conditions for coldwater-adapted
fish species. On the other hand, however, it may provide suitable thermal
conditions for non-native warm water fish species (Sharma et al., 2007).
Such species could prey on or compete with native fishes and this compe-
tition may result in a decline or loss of native populations (Jackson and
Mandrak, 2002).
However, potentially confounding factors such as eutrophication, acid-
ification, and the equivalent reverse phenomena generally fluctuate less rap-
idly than climatic variables. This difference in behaviour and signal-response
times can be used to distinguish between climatic forcing and confounding
factors, by removing trends and low-frequency fluctuations from relevant
time-series by detrending or high-pass filtering, and analyzing only the
remaining, higher-frequency fluctuations that are driven mainly by external
physical forcing (Adrian et al., 2009).
Notwithstanding the current shortage of empirical data on all relevant
communities or traits in the literature at a truly global scale, a clearer picture
of what we should expect with climate warming is starting to emerge, espe-
cially when we combine trends from SFTS studies with modelling studies,
in situ warming experiments and long-term empirical studies (e.g. Jeppesen
et al., 2010a; Jeppesen et al., submitted for publication; Sarmento et al.,
2010). In some cases, however, apparently contradictory patterns emerge,
as highlighted here. Experimental warming studies are often of short-term
duration, thus showing transient phenomena (i.e. warming as a stressor),
whereas SFTS studies in natural systems are more likely to reveal equilibrial
conditions with respect to temperature rather than responses to changing

conditions per se. Moreover, warming experiments most often simplify
food webs and, in particular, the role of predators by using fixed densities
of a single predatory fish species (e.g. Liboriussen et al., 2005; McKee
et al., 2002a; Yvon-Durocher et al., 2011a), thereby not allowing for the
assessment of temperature-driven effects on prey communities through
temperature impacts on the assemblage of predators. For instance, the
majority of the reviewed SFTS studies suggest that fish predation, rather
than temperature alone, is also responsible for the changes in the structure
of several communities, mainly as a result of cascading effects of the
temperature-driven decrease in fish size (Lacerot, 2010; Meerhoff et al.,
2007a) leading to a stronger predation pressure on macroinvertebrates and
zooplankton (Gyllström et al., 2005; Meerhoff et al., 2007a,b).
The SFTS approach thus highlights empirical trends that allow re-
searchers to generate hypotheses regarding climate-driven future changes
in community and ecosystem processes, thus potentially stimulating further
research and the design of appropriate experiments to disentangle effects of
potential drivers and to test mechanisms (e.g. Friberg et al., 2009;
Liboriussen et al., 2005 and other references mentioned along the text).
The combination of empirical data, mechanistic approaches and the
framework given by food web and metabolic theories to climate change
research in shallow lakes seems also fundamental, as suggested for other
ecosystems or in theoretical works (e.g. Montoya and Raffaelli, 2010;
Van der Putten et al., 2010; Woodward et al., 2010b).
3.3. Topics for further research

The occurrence of processes acting at different scales renders it difficult to
disentangle their specific effects and the relative importance of local and re-
gional characteristics on multispecies richness. In particular, both the exper-
imental evidence and our review of whole lake data might suggest that the
effects of nutrient enrichment and predation by fish on zooplankton and
macroinvertebrate communities might be stronger than the direct effects
of warming. It is thus open for further analysis whether some of our seem-
ingly contradictory findings are a result of temperature-enhanced fish pre-
dation in warm locations, and therefore with consequences for a climate
warming context, or a result of biogeographic processes or of geographically
restricted databases. SFTS studies analyzing changes in community traits in
fishless systems could provide some answers to these questions.
Our target community traits (i.e. richness, biomass, density and body
size) are very seldom combined in the literature within a given study, and
information on the responses of key communities to warming is therefore
fragmentary. The common use of proxies for some traits (such CPUE, with
different units in different works, as a proxy of fish density and biomass per
unit area) also renders it difficult to compare results from different publica-
tions and to estimate predation pressure indexes. The lack of reports in the
literature of traits typically measured (such as the body size and density of
phytoplankton and periphyton) represents information gaps that should
be relatively easy to solve. On the other hand, some traits are typically
not measured, such as the body size and density of macrophytes or traits
of macroinvertebrates at low levels of aggregation (i.e. species and genera),
while some assemblages are typically underrepresented in shallow lake re-
search. In particular, and despite the importance of bacteria for geochemical
cycles, biomass and nutrient and energy transport within aquatic trophic
webs (Azam, 1998), data on microbial communities in shallow lakes are
scarce. When present, bacterioplankton community traits are typically not
described, reflecting the very different methodological skills and facilities re-
quired to evaluate all community traits, which will hopefully become less of
a hindrance in the future with the advent of more sophisticated molecular
approaches (Purdy et al., 2010). Besides, microbial ecologists have modified
their focus, from evaluating bacterioplankton communities in terms of taxa-
independent approaches (e.g. measurements of biomass) to elucidating fac-
tors controlling the community composition with the aim to understand the
role and fate of specific populations (Pernthaler and Amann, 2005), and a
move towards more in situ characterizations of multispecies systems
(Purdy et al., 2010).
Possibly, more serious, though, than the scarcity of data on bacter-
ioplankton is the lack of data on their predators (i.e. heterotrophic
nanoflagellates, or HNF). The absence of this link from the literature
prevents us from estimating potential changes in energy and nutrient
fluxes within the food web of shallow lakes under warming, since these or-
ganisms link the microbial loop with the classic food web (i.e.
phytoplankton–zooplankton–fish) (Reiss et al., 2010). Changes in lake tro-
phic state could promote a decoupling between bacterioplankton and their
potential predators (Gasol, 1994), potentially leading to changes in the effi-
ciency of energy transfer and the occurrence and strength of trophic links
(Zingel et al., 2007) in the whole system. The scarcity or lack of data
(and large uncertainties associated with laboratory techniques) on the
microscopic components of shallow lakes also renders it very difficult to sea-

rch for body size thresholds on which to test the predictions of the different
theories that relate temperature with body size.
More data on changes in trophic position, diet breadth and feeding rates
are needed to test the predicted trends of a reduction in food web length with
increasing temperature (Arim et al., 2007) and of changes in key measures of
interaction density, such as connectance (Petchey et al., 2010). Climate ef-
fects on life history traits other than reproductive characteristics, and seasonal
dynamics of lake communities other than plankton (Adrian et al., 2006), are
areas that could be usefully investigated applying the space-for-time
framework. Another important caveat that deserves further investigation is
the effects of climate on host–parasite interactions: several studies suggest
that climate strongly influences parasite infection in lake communities (e.-
g. phytoplankton, Ibelings et al., 2011; fish, Macnab and Barber, 2012),
yet this field of trophic ecology is still surprisingly poorly understood
(Thompson, Dunne and Woodward, in press). Despite the fact that the over-
all effects still have yet to be fully elucidated, temperature-mediated changes
in parasite infection can potentially alter the expected outcomes of trophic
cascades or predator–prey dynamics between the main lake communities.
The likely important effects of changes in temperature on the production
and action of allelopathic substances represent another research area of great
potential.
Arguably, the most familiar characteristic of shallow lake ecosystems is
their capacity to shift between alternative, relatively stable, states (Moss,
1990; Scheffer et al., 1993, 2001). This implies path dependency or
hysteresis, in which a return to the environmental condition (e.g. a
particular nutrient concentration) before the shift is not sufficient to
recover the previous ecosystem state. Several pieces of evidence suggest
that the differences in the biotic interactions between cold and warmer
regions (Meerhoff et al., 2007a) might result in a weaker clearing effect of
submerged plants under warmer conditions (Jeppesen et al., 2007), and
thus in a weaker stability of the clear water state. Kosten et al. (2009b)
assessed whether the effect of submerged plants changes with climate in
South America and found that the competitive balance between
submerged macrophytes and phytoplankton is not straightforward.
However, the effect of submerged macrophytes on water clarity in the
lakes (outside the plants beds) was generally lower in South America
(Kosten et al., 2009b) than in temperate Northern Hemisphere lakes (e.g.
Jeppesen et al., 2007), suggesting that other processes may have been
overlooked. How global changes, including here the changes in C and N

cycles and land use, besides climate warming, affect the critical thresholds
over which the ecosystems experience such dramatic shifts is thus one of
the most relevant questions for ecosystem management in the future,
particularly for shallow lakes.
ACKNOWLEDGEMENTS
We are very grateful to Anne Mette Poulsen for chapter editing and to Juana Jacobsen and
Tinna Christensen for superb graphical assistance. We thank R. Schiaffino for kindly sharing
data on bacteria for our analysis, J. Huisman and M. Stomp for kindly permitting
reproduction of the panel of phytoplankton richness in Fig. 1D; J. Gorga for the nice
drawings of fish in Fig. 8. We thank two anonymous reviewers and Editor G. Woodward
for constructive comments that greatly improved the chapter. C. A., C. K., C. I., F. T.
M., G. G., G. L., M. A., M. M. and N. M. receive support from the S. N. I. (Agencia
Nacional de Investigación e Innovación, ANII, Uruguay). C. A., C. K., M. A., M. M.
and N. M. are supported by PEDECIBA, M. M. also by ANII-FCE (2009–2749) and the
national award by L’Oréal-UNESCO 2011 for Women in Science (Uruguay, with
support of DICyT). C. A., C. K. and G. L. are also supported by CSIC (Programa
Grupos IþD—1037, Ecologı́a Funcional de Sistemas Acuáticos), C. K. and G. L. by
Wetenschappelijk Onderzoek van de Tropen en Ontwikkelingslanden (WOTRO,
Foundation for the Advance of Tropical Research), The Netherlands, and C. A. also by
the Max Planck Society. F. T. M. and I. G. B. are supported by SNB-ANII and IGB also
by ANII-FCE (2009–2530). E. J., M. B. and S. B. are supported by FP7/ENV-2009-1
under grant agreement 244121 (REFRESH Project), and E. J. also by the Research
Council for Nature and Universe (272-08-0406), the STF project CRES, CIRCE,
CLEAR2 and FNU (16-7745). M. B. is also supported by TUBİTAK ÇAYDAĞ 105Y332.
APPENDIX A. PERIPHYTON LATITUDINAL GRADIENT

We analyzed papers covering a latitudinal gradient range from 68ºS
to 83ºN. All the data come from field sampling campaigns of periphyton
on different substrates, either natural or artificial, in freshwater shallow
lakes along a nutrient concentration range of 8.0–4050 mg TN L 1,
0.4–2750 mg TP L 1, and a planktonic chlorophyll-a concentration gradi-
ent from 0.4 to 400 mg Chl-a L 1. We performed linear regressions between
periphyton data and latitude using the statistical package STATISTICA.
Literature analyzed:
Ács, E., Borsodi, A.K., Makk, J., Molnár, P., Mózes, A., Rusznyak, A.,
Reskone, M.N., and Kiss, K.T. (2003). Algological and bacteriological
investigations on reed periphyton in Lake Velencei, Hungary.
Hydrobiologia 506/509, 549–557.
Bonaventura, S.M., Vinocur, A., Allende, L., and Pizarro H. (2006).

Algal structure of the littoral epilithon in lentic water bodies at Hope
Bay, Antarctic Peninsula. Polar Biol. 29, 668–680.
Bonilla, S., Villeneuve, V., and Vincent, W.F. (2005). Benthic and
planktonic algal communities in a high arctic lake: pigment structure
and contrasting responses to nutrient enrichment. J. Phycol. 41,
1120–1130.
Conde, D., Bonilla, S., Aubriot, L., de León, R., and Pintos, W. (1999).
Comparison of the areal amount of chlorophyll a of planktonic and at-
tached microalgae in a shallow coastal lagoon. Hydrobiologia 408/409,
285–291.
Fermino, F.S., Bicudo, C.E.M., and Bicudo, D.C. (2011). Seasonal in-
fluence of nitrogen and phosphorus enrichment on the floristic compo-
sition of the algal periphytic community in a shallow tropical,
mesotrophic reservoir (São Paulo, Brazil). Oecol. Aust. 15, 476–493.
Ferragut, C., Rodello, A.F., and Bicudo, C.E.M. (2010). Seasonal var-
iability of periphyton nutrient status and biomass on artificial and natural
substrates in a tropical mesotrophic reservoir. Acta Limnol. Brasil. 22,
397–409.
Franca, R.C.S., Lopes, M.R.M., and Ferragut, C. (2009). Temporal var-
iation of biomass and status nutrient of periphyton in shallow Amazonian
Lake (Rio Branco, Brazil). Acta Limnol. Bras. 21, 175–183.
Hansson, L.-A. (1992). The role of food chain composition and nutrient
availability in shaping algal biomass development. Ecology 73, 241–247.
Harrison, S.S.C., and Hildrew, A.G. (1998). Patterns in the epilithic
community of a lake littoral. Freshwater Biol. 39, 477–492.
Havens, K.E., East, T.L., Rodusky, A.J., and Sharfstein, B. (1999). Lit-
toral periphyton responses to nitrogen and phosphorus: an experimental
study in a subtropical lake. Aquat. Bot. 63, 267–290.
Kiss, M.K., Lakatos, G., Borics, G., Gido, Z., and Deak, C. (2003). Lit-
toral macrophyte-periphyton complexes in two Hungarian shallow wa-
ters. Hydrobiologia 506/509, 541–548.
Lambert, D., Cattaneo, A., and Carignan, R. (2008). Periphyton as an
early indicator of perturbation in recreational lakes. Can. J. Fish Aquat.
Sci. 65, 258–265.
Liboriussen, L., and Jeppesen, E. (2003). Temporal dynamics in epipelic,
pelagic and epiphytic algal production in a clear and a turbid shallow
lake. Freshwater Biol. 48, 418–431.
Liboriussen, L., and Jeppesen, E. (2006). Structure, biomass, production

and depth distribution of periphyton on artificial substratum in shallow
lakes with contrasting nutrient concentrations. Freshwater Biol. 51,
95–109.
Luttenton, M.R., and Lowe, R.L. (2006). Response of a lentic periph-
yton community to nutrient enrichment at low N:P ratios. J. Phycol. 42,
1007–1015.
Moschini-Carlos, V., Henry, R., and Pompêo, M.L.M. (2000). Seasonal
variation of biomass and productivity of the periphytic community on
artificial substrata in the Jurumirim Reservoir (São Paulo, Brazil).
Hydrobiologia 434, 35–40.
Murakami, E.A., Bicudo, D.C., and Rodrigues, L. (2009). Periphytic
algae of the Garças Lake, Upper Paraná River floodplain: comparing
the years 1994 and 2004. Braz. J. Biol. 69, 459–468.
Ortega, M.R., Alvarado, R., Hernández, R., Israde, I., Sánchez, J.D.,
Arredondo, M., and Martı́nez, I. (2009). El perifiton de un lago
hiposalino hipereutrófico en Michoacán, México. Biológicas 11, 56–63.
Pizarro, H., Allende, L., and Bonaventura, S.M. (2004). Littoral
epilithon of lentic water bodies at Hope Bay, Antarctic Peninsula: bio-
mass variables in relation to environmental conditions. Hydrobiologia 529,
237–250.
Rautio, M., and Vincent, W.F. (2006). Benthic and pelagic food re-
sources for zooplankton in shallow high-latitude lakes and ponds. Fresh-
water Biol. 51, 1038–1052.
Roberts, E., Kroker, J., Körner, S., and Nicklisch, A. (2003). The role of
periphyton during the re-colonization of a shallow lake with submerged
macrophytes. Hydrobiologia 506/509, 525–530.
Rodrı́guez, P., Tell, G., and Pizarro, H. (2011). Epiphytic algal biodi-
versity in humic shallow lakes from the lower Paraná River basin (Ar-
gentina). Wetlands 31, 53–63.
Rodusky, A.J., Steinman, A.D., East, T.L., Sharfstein, B., and Meeker,
R.H. (2001). Periphyton nutrient limitation and other potential growth-
controlling factors in Lake Okeechobee, U.S.A. Hydrobiologia 448,
27–39.
Rouf, A.J.M., Ambak, M.A., Lokman, S., Siew-Moi, P., and Sinn, C.H.
(2008). Temporal changes in the periphytic algal communities in a
drowned tropical forest reservoir in Malaysia: Lake Kenyir. Lakes Reser-
voirs: Res. Manage. 13, 271–287.
Sánchez, M.L., Pizarro, H., Tell, G., and Izaguirre, I. (2010). Relative
importance of periphyton and phytoplankton in turbid and clear vege-
tated shallow lakes from the Pampa Plain (Argentina): a comparative ex-
perimental study. Hydrobiologia 646, 271–280.
APPENDIX B. BACTERIOPLANKTON LATITUDINAL

GRADIENT
We analyzed 17 publications including information on 140 lakes
along a latitudinal gradient from 7o to 64oS and from 29.1o to 68.5oN.
The lakes covered a gradient in trophic status from 1.1 to 506 mg TP L 1
and 0.29 to 221 mg phytoplankton Chl-a L 1. We grouped the lakes
according to climatic zones following the revision by Leemans and
Cramer (1991) of the Köppen climate system (1936). We performed
Spearman’s correlations and stepwise multiple linear regressions (after
log-transforming relevant data) between bacterioplankton data and rele-
vant environmental variables, latitude, altitude, lake area, water tempera-
ture, conductivity, nutrients, such as phytoplankton Chl-a, dissolved
organic carbon concentration, etc. We used the statistical packages
STATISTICA and SigmaPlot.
The Spearman’s correlations indicated that bacterioplankton abundance
significantly declined with increasing latitude (r ¼ 0.55, p < 0.0001, n ¼ 133)
and increased with DOC (r ¼ 0.90, p < 0.0001, n ¼ 34), temperature
(r ¼ 0.67, p < 0.0001, n ¼ 112), conductivity (r ¼ 0.58, p < 0.0001, n ¼ 98)
and Chl-a (r ¼ 0.46, p < 0.0001, n ¼ 95). No significant relationships were
found for nutrients (TP and TN).
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APPENDIX C. PHYTOPLANKTON UNPUBLISHED DATA

AND LATITUDINAL GRADIENT
C.1. Previously unpublished data: The
Netherlands–Uruguay comparison
We compiled a database from 650 shallow lakes located within two climate
zones in the Netherlands (temperate) and Uruguay (subtropical), covering a
wide range of environmental characteristics (Kruk et al., 2011). The sam-
pling and sample analyses protocols were similar in both locations. Lakes
were sampled at random points integrating the water column and covering
the whole lake area. Water samples for nutrients and plankton were taken
integrating the water column with a plastic tube (20-cm diameter) and com-
bining from 3 to 20 random replicates in each lake. Phytoplankton samples
were fixed in Lugol’s solution and total phosphorus (TP, mg L 1) was es-
timated. Details on sample analysis are provided in Kruk et al. (2009).
Phytoplankton populations were counted in random fields from fixed
Lugol samples using the settling technique (Utermöhl, 1958). We examined
the samples at multiple magnifications and counted until we reached at least
100 individuals of the most frequent species (Lund et al., 1958). Organisms
between 5 and 100 mm were counted at 400, larger organisms were counted
at 200, and organisms between 5 and 2 mm were counted at 1000. We did
not include picoplanktonic species (<2 mm) or species strongly associated
with periphytic communities. For all lakes, we considered the organism as the
unit (unicell, colony or filament). Cell numbers per colony as well as organism
dimensions, including maximum linear dimension (MLD, mm) were
estimated. Individual volume (V, mm3) and surface (S, mm3) were calculated
according to geometric equations (Hillebrand et al., 1999). For colonial
organisms with mucilage, V and S calculations were made for whole colonies
including mucilage. Population biovolume was estimated (mm3 L 1) and
calculated as the individual volume of the species multiplied by the abundance
of individuals. Most of the samples were analyzed by the same group of
scientists using the same identification keys and a common protocol.
However, to diminish the potential taxonomical discrepancies between
different data sets, we did not include the organisms that were not identified
at least at the class level. Also, organisms from the same genus but not iden-
tified to species level were grouped together. We also excluded the species
with a contribution of less than 5% to the total community biomass in any
individual lake. Richness was estimated as the sum of species per lake.
We classified species into phylogenetic classes following Van Den Hoeck
et al. (1997), except cyanobacteria (Pérez et al., 1999; Komárek and
Anagnostidis, 2005) and Bacillariophyceae (Round, 1992). We also classified
the species into size classes, selected to represent the main growing strategies of
phytoplankton. Following Reynolds (1988), we plotted the mean values per
species of all lakes of log S/V versus log MLD and selected five MLD classes
corresponding to <3, 3–10, 10–30, 30–100 and >100 mm that have a more
homogeneous distribution of the species. For each class and each size class, the
biovolumes were summed per sample. In the case of classes, the biovolume
was transformed into percentage to compare the relative contribution in each
climatic region.
Total richness of 5% species, total biovolume and the percentage of each
phylogenetic group biovolume were tested for differences in their median
value between subtropical and temperate regions using Kruskal–Wallis tests.
C.2. Latitudinal gradient meta-analysis

A meta-analysis of data was done searching in published and un-published
sources for total chlorophyll-a (Chl-a) and its relationship with total
phosphorus (TP), determined using simple linear regression with log10-
transformed data in all studies. The considered studies had comparable
sampling procedure and sample analysis. A total of 290 cases were obtained
for Chl-a including tropical, subtropical, temperate, cold and polar lakes.
A total of 28 models were calculated from the data available with Statistica
software or obtained from the cited references (see Table 3).
Chlorophyll concentration as well as the slope and r2 of the relation be-
tween (log10-transformed) chl-a and TP were tested for differences in their
median value among climatic regions (tropical, subtropical, temperate, cold
and polar lakes) using Kruskal–Wallis tests and post hoc multiple comparisons
(Z value). We used this type of analysis due to its widespread use in the rel-
evant literature, thus allowing us to increase the power of our comparison.
KW test was selected due to the uneven number of cases in each climate
region for all categorical variables.
Data on phytoplankton species richness and latitude from Stomp et al.
(2011) (Ecological Archives E092-183-S1 in http://esapubs.org/archive/
ecol/E092/183/suppl-1.htm) were used to estimate the r2 of the linear
relation between richness and latitude.
Literature cited:
Komárek, J., and Anagnostidis, K. (2005). Cyanoprokaryota II. Teil
Oscillatoriales. Spektrum Akademischer Verlag, München.
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S., and Scheffer, M. (2011). Phytoplankton community composition can
be predicted best in terms of morphological groups. Limnol. Oceanogr. 56,
110–118.
Kruk, C., Rodrı́guez-Gallego, L., Meerhoff, M., Quintans, F., Lacerot,
G., Mazzeo, N., Scasso, F., Paggi, J., Peeters, E.T.H.M. and Scheffer, M.
(2009). Determinants of biodiversity in subtropical shallow lakes (Atlan-
tic coast, Uruguay). Freshwater Biol. 54, 2628–2641.
Lund, J.W.G., Kipling, C., and Le Cren, E.D. (1958). The inverted mi-
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estimations by counting. Hydrobiologia 11, 143–170.
Pérez, M.C., Bonilla, S., De León, L., Smarda, J., and Komárek, J. (1999).
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Impact of Climate Change on
Fishes in Complex Antarctic
Ecosystems
Katja Mintenbeck*,1, Esteban R. Barrera-Oro{,{, Thomas Brey*,
Ute Jacob}, Rainer Knust*, Felix C. Mark*, Eugenia Moreira{,
Anneli Strobel*, Wolf E. Arntz*
*Alfred Wegener Institute for Polar and Marine Research, Bremerhaven, Germany
{
Instituto Antártico Argentino and CONICET, Buenos Aires, Argentina
{
Museo Argentino de Ciencias Naturales ‘Bernardino Rivadavia’, Buenos Aires, Argentina
}
Institute for Hydrobiology and Fisheries Science, University of Hamburg, Hamburg, Germany
1
Corresponding author: e-mail address: kmintenbeck@hotmail.com
Contents
1. Introduction 352
2. The Antarctic Marine Ecosystem 357
2.1 Geographical and physical conditions 357
2.2 Biological characteristics 359
3. Antarctic Fish Communities 362
3.1 Composition of the modern fauna 362
3.2 Evolution and adaptive radiation 365
3.3 Adaptations and characteristics of notothenioid fishes 366
3.4 Threats to the fish community 370
4. Physiological Vulnerability of Antarctic Fishes 371
4.1 Sensitivity to changes in temperature and salinity 371
4.2 Sensitivity to increasing pCO2 375
5. Trophic Vulnerability of Antarctic Fishes 376
5.1 Vulnerability to general changes in trophic structure and dynamics 376
5.2 Vulnerability to changes in size structure and prey quality 381
6. Vulnerability of Antarctic Fishes to Habitat Destruction 386
6.1 The impact of sea ice reduction 386
6.2 The impact of increased iceberg scouring 387
7. Discussion 394
7.1 The impact of climate change on Antarctic fish species 394
7.2 Effects of climate change in other marine systems 395
7.3 Antarctic fish community persistence—Winners and losers 398
7.4 Consequences of fish species loss for the marine Antarctic ecosystem 400
7.5 Final thoughts—Is climate change exclusively to blame? 404

http://dx.doi.org/10.1016/B978-0-12-396992-7.00006-X
352 Katja Mintenbeck et al.
Appendix 406
References 407
Abstract
Antarctic marine ecosystems are increasingly threatened by climate change and are
considered to be particularly sensitive because of the adaptation of most organisms
to cold and stable environmental conditions. Fishes play a central role in the Antarctic
marine food web and might be affected by climate change in different ways: (i) directly
by increasing water temperatures, decreasing seawater salinity and/or increasing con-
centrations of CO2; (ii) indirectly by alterations in the food web, in particular by changes
in prey composition, and (iii) by alterations and loss of habitat due to sea ice retreat and
increased ice scouring on the sea floor. Based on new data and data collected from the
literature, we analyzed the vulnerability of the fish community to these threats.
The potential vulnerability and acting mechanisms differ among species, develop-
mental stages and habitats. The icefishes (family Channichthyidae) are one group that
are especially vulnerable to a changing South Polar Sea, as are the pelagic shoal fish
species Pleuragramma antarcticum. Both will almost certainly be negatively affected by
abiotic alterations and changes in food web structure associated with climate change,
the latter additionally by habitat loss. The major bottleneck for the persistence of the
majority of populations appears to be the survival of early developmental stages, which
are apparently highly sensitive to many types of alterations. In the long term, if climate
projections are realized, species loss seems inevitable: within the demersal fish commu-
nity, the loss or decline of one species might be compensated by others, whereas the
pelagic fish community in contrast is extremely poor in species and dominated by
P. antarcticum. The loss of this key species could therefore have especially severe conse-
quences for food web structure and the functioning of the entire ecosystem.
1. INTRODUCTION
Climate change in the Antarctic is not simply a future scenario but al-
ready a well-established fact (e.g. Curran et al., 2003; Gille, 2002; Jacob
et al., 2011; Murphy et al., 2007, Rignot et al., 2008). Its impacts are
most evident in the Antarctic Peninsula region (including the southern
Bellingshausen and Amundsen seas), where average temperatures at the
sea surface have increased by nearly 3 C within just the past 50 years
( 0.56 C increase decade 1; e.g. Domack et al., 2003; Turner et al.,
2005), and winter temperatures have increased by 5–6 C (Vaughan
et al., 2003). This represents a dramatic increase in air temperature in this
region far above the global mean and exceeds any other warming rate
observed on Earth at comparable spatial scales; the causes, however, are
still under discussion (Gille, 2008; Vaughan et al., 2003).
Impact of Climate Change on Fishes in Complex Antarctic Ecosystems 353
The corresponding warming of the seawater is less pronounced, though

again highly significant: the upper water layers (down to about 50 m water
depth) west off the Antarctic Peninsula have warmed by 1 C since 1955
(Meredith and King, 2005) and are predicted to rise by another 2 C over
the next century (Murphy and Mitchel, 1995). In Palmer Deep, West Ant-
arctic Peninsula, bottom water temperature has been increasing at a rate of
about 0.01 C year 1 since the 1980s (Smith et al., 2012). Moreover, there
is some indication of a warming trend emerging in the deep waters of the
Ross and Weddell seas (Ozaki et al., 2009; Robertson et al., 2002).
Increasing temperatures significantly affect ice dynamics: the warming has
already resulted in a significant reduction in extent and duration of sea ice in
the Antarctic Peninsula region, the Amundsen and Bellingshausen seas (Jacobs
and Comiso, 1997; Loeb et al., 1997; Stammerjohn et al., 2008a,b) and has
also contributed to disintegration and collapses of large ice shelves, such as
the northern part of the Larsen ice shelf in the northwestern Weddell Sea
(Domack et al., 2005; Marshall et al., 2006). In some shelf regions at the
Antarctic Peninsula and in the Ross Sea, melting ice shelves, increased
glacial meltwater runoff and reduced sea ice production have led to
reduced seawater salinity, particularly in surface water layers (Jacobs et al.,
2002; Moline et al., 2004). In Potter Cove, King George Island (South
Shetland Islands, west Antarctic Peninsula), a glacier retreat of hundreds of
metres and significant freshening of the upper water column have been
observed within the past 15 years alone (Schloss et al., 2008).
Ocean acidification is considered a major threat for marine ecosystems
that is concomitant with warming and atmospheric change (IPCC, 2007).
Anthropogenic CO2 emissions have increased atmospheric CO2 concentra-
tions since the industrialization in the 1850s, and about one-third of anthro-
pogenic CO2 from the atmosphere is absorbed by the world’s oceans (Sabine
et al., 2004). CO2 is physically dissolved in seawater and this leads to pro-
gressive ocean acidification: several models predict a drop of seawater pH by
0.3–0.5 units by the year 2100 (atmospheric pCO2 of 1000 matm) and up to
0.77 units until the year 2300 (atmospheric pCO2 of 1900–2300 matm;
Caldeira and Wickett, 2003, 2005; Feely et al., 2004; IPCC, 2007). So
far, information on CO2 changes in the Antarctic marine ecosystem is
scarce, but local measurements of atmospheric CO2 concentrations
recorded at the permanent Argentinian station ‘Carlini1’, at the shoreline
of Potter Cove, revealed a trend of increasing concentrations over a
1
Formerly known as ‘Jubany’ (renamed in March 2012).
relatively short time (from 356 matm in 1994 to 379 matm in 2006; Ciattaglia
et al., 2008).
Though all the mechanisms involved and their interactions are not yet
fully understood, there is little doubt that many of these observed changes
are beyond that associated with natural variability but caused at least in part
by anthropogenic climate change. In the light of ongoing global climate
change, it is most likely that those regions of the Antarctic where alterations
are not yet evident will also be affected in the near future.
Extant Antarctic marine communities have already been significantly af-
fected by these environmental changes. In Potter Cove, clear shifts in ben-
thic community composition have been observed that appear to be related to
increased sediment load in the water column and ice impact due to melting
and disintegration of the glacier (Sahade et al., 2008). Changes in salinity
alter seawater density and thus can affect stratification of the water column
and the depth of the mixed layer: salinity and surface water stratification are
two main factors determining phytoplankton composition (Arrigo et al.,
1998; Moline et al., 2004). Off the west Antarctic Peninsula, Moline
et al. (2004) observed a recurrent change in phytoplankton community
structure, with a spatiotemporal shift from large diatoms towards small
cryptophytes as salinity declined. Alterations in community structure are
also evident in consumers higher in the food chain: since the 1970s, the
abundance of krill (Euphausia superba) has declined in the southwestern
Atlantic and salps have become more abundant (Atkinson et al., 2004).
As life cycle and overwintering strategy of Antarctic krill are closely
coupled to the sea ice, its accelerating retreat will suppress krill
abundance (Atkinson et al., 2004; Loeb et al., 1997). Other factors
contributing to krill decline might be water temperature itself, as krill
prefers cooler water compared to salps (e.g. Pakhomov et al., 2002), and
indirect (trophodynamic) effects, including predation of early krill stages
by salps (Huntley et al., 1989) and the inability of krill to efficiently graze
on small cryptophytes (see Moline et al., 2004 and references therein).
Moreover, salps feed efficiently on a wide range of particles even when
phytoplankton concentrations are low (Hopkins, 1985; Kremer and
Madin, 1992; Madin, 1974) and are able to attain large population sizes
and biomass rapidly (e.g. Mianzan et al., 2001). Under favourable
environmental conditions, their efficient grazing and high ingestion rates
(e.g. Perissinotto and Pakhomov, 1998a,b) could result in the competitive
exclusion of other grazers, such as copepods.
Though there are no immediately obvious visible effects reported so far,

Antarctic marine communities could be vulnerable to ocean acidification in
the future. Recent experimental studies have shown that survival and devel-
opment of early stages of calcifying invertebrates and Antarctic krill are sig-
nificantly negatively affected by levels of predicted future CO2
concentrations (Kawaguchi et al., 2011; Kurihara, 2008).
Increasing warming of the Southern Ocean will facilitate the invasion
and/or introduction and colonization by species from adjacent oceans. Inva-
sion by invertebrates via warming deep waters appears to be already under-
way. Lithodid crabs have been absent from Antarctic waters for millions of
years (see e.g. Thatje et al., 2005), but reports of sightings in Antarctic waters
have been accumulating in recent years (e.g. Garcı́a Raso et al., 2005; Thatje
et al., 2008). Recently, a large and reproductive population of king crabs
(Neolithodes yaldwyni) was discovered in Palmer Deep, west of the
Antarctic Peninsula (Smith et al., 2012). So far, the distribution of lithodids
seems to be restricted to the deeper slope, but assuming a persistent
warming of waters of the Antarctic Peninsula region, Smith et al. (2012)
speculated that lithodids might migrate upwards and invade the shelf
communities within the next 20 years. Invasion of such hitherto absent
durophagous (i.e. shell- or skeleton-crushing) predators strongly affects
benthic communities (Aronson et al., 2007). The presence of the king
crabs in Palmer Deep has been associated with a decrease in diversity of
the megabenthos, including an absence of echinoderms (Smith et al., 2012).
Another more direct impact of human activity is in the form of the increas-
ing ship traffic by tourist cruise ships and research vessels, which further en-
hance the risk of introduction of exotic species to the South Polar Sea (Lee and
Chown, 2007; Lewis et al., 2005, 2006). The North Atlantic spider crab Hyas
araneus, for example, was found in benthic samples from the Antarctic
Peninsula: a species usually only found in the North Atlantic and Arctic
Ocean that was most likely introduced into the Southern Ocean via ships’
sea chest or ballast water (Tavares and De Melo, 2004). Another passive,
man-made pathway for invasion is the increasing amount of litter in the
world’s oceans. Non-indigenous species may be introduced into the
Southern Ocean by transport on drifting plastic debris (Barnes, 2002; Lewis
et al., 2005 and citations therein).
Invasion/introduction of alien species will most likely lead to strong
alterations in food web structure owing to removal of prey for indigenous
species, competition and predation (Woodward et al., 2010a). So far, only
invasion by crustaceans has been detected, but if the warming trend con-
tinues, it is inevitable that further species, both benthic and pelagic, will in-
vade the Antarctic marine ecosystem. As long as conditions in the South
Polar Sea are appropriate for survival but still limit growth and in particular
reproduction capacity of invasive species, the threat for indigenous species
will remain low. However, once alien species become able to successfully
reproduce and to build up populations (as it seems to be the case in the
lithodids found in Palmer Deep; Smith et al., 2012), the threat for native
Antarctic species significantly increases.
The direction and strength of ecosystem response to environmental
change depend strongly upon responses of individual species and their inter-
actions among each other. Fishes are an integral part of marine ecosystems
and have been proposed to serve as useful bio-indicators of climate change
(Dulvy et al., 2008; McFarlane et al., 2000). As organisms within an
ecosystem are linked to each other directly or indirectly via
trophodynamics, any kind of change affecting fishes will indirectly affect
other members of the food web, with a huge range of potential indirect
effects being triggered. For many decades, scientists retained a view that
Antarctic food chains were relatively short and simple: essentially a
connection from diatoms to krill to consumers. Krill, E. superba, in
particular was regarded as an inexhaustible resource that underpinned the
whole Antarctic food web, supporting fishes, penguins, seabirds, seals and
whales (e.g. Murphy, 1962; Tranter, 1982). However, this paradigm has
been challenged as being overly simplistic. Although krill does indeed
seem to be a key species over large areas, many food chains are
independent of it (e.g. Rodhouse and White, 1995), and high species
numbers in the South Polar Sea (e.g. Gutt et al., 2004) suggest that the
diatom–krill–consumer chain is only one component of a highly complex
food web (Clarke, 1985; Jarre-Teichmann et al., 1995). Fishes take a
central position in this ecological network: they occupy a variety of
trophic niches, are the main consumers of benthos and plankton, and are
an important food source for a multitude of species, including
cephalopods, piscivorous fishes, penguins, flying birds, seals and whales
(for review, see Barrera-Oro, 2002; Hureau, 1994; Kock, 1992; La Mesa
et al., 2004). Fishes thus represent an important trophic link that connects
small invertebrates and top predators of the Antarctic marine ecosystem,
making their potential vulnerability to systemic shifts of particular interest.
In this chapter, we provide an overview of the potential effects of climate
change on Antarctic fish species and communities. Based on our own data
collected during several expeditions and data that were taken from the lit-
erature, we summarize the characteristics of the Antarctic marine ecosystem
and the fish communities, and we evaluate the threats to fishes, the degree of
endangerment of particular species and the potential consequences for over-
all ecosystem functioning.
2. THE ANTARCTIC MARINE ECOSYSTEM

2.1. Geographical and physical conditions
The ocean surrounding the Antarctic continent represents one of the most
unique marine environments on Earth, an appreciation of which requires a
brief review of the geological and climatological history and settings of the
Antarctic and its adjacent waters and land masses (summarized in Clarke and
Johnston, 1996; Eastman, 1991). In the Jurassic, Antarctica was still part of
the supercontinent Gondwana, which subsequently broke up, leaving
Antarctica connected to South America and Australia throughout the
Cretaceous (about 65 Ma2 ago), when the climate was temperate, with
water temperatures above 10 C. Between late Eocene and early
Oligocene (about 38 Ma), separation of Antarctica from Australia was
most likely completed, and seawater temperatures began to decrease
sharply. The separation from South America and the formation of sea ice
and the continental ice sheet began between 37 and 34 Ma (e.g.
Ehrmann and Mackensen, 1992; Ivany et al., 2008; Pearson et al., 2009).
The final separation from South America and the opening of the Drake
Passage allowed for the development of the strongest current system in
the world, the Antarctic Circumpolar Current (ACC), driven by strong
westerly winds. The ACC encircles the whole continent and acts as a
thermal barrier by effectively separating lower latitude warmer and higher
latitude colder waters (see e.g. Orsi et al., 1995).
The Antarctic continent and shelf areas are now geographically isolated
from other continents and shelves by great distances and the large abyssal
basins of more than 4000 m water depths that surround it (Fig. 1): the only
connection to other continents with water depths less than 2000 m is via the
Scotia Ridge composed of numerous islands linking South America to the
Antarctic Peninsula (Arntz et al., 2005; Tomczak and Godfrey, 1994). In
addition, the continent and the surrounding ocean are thermally isolated
by the ACC, which flows eastwards and connects the Atlantic, Indian
2
Millions of years before present (Ma).
Figure 1 Map of Antarctica and the Southern Ocean (Source: Centenary edition of the
GEBCO Digital Atlas).
and Pacific basins. This strong current system includes the Antarctic Polar
Front, a region of downwelling and sharp temperature change of 3–4 C
(Knox, 1970). As a result, water temperatures in the South Polar Sea are
consistently low (ranging from þ1 to 1.86 C close to the continent)
with little seasonal variation (Deacon, 1984; Olbers et al., 1992). Close to
the continent, the Antarctic Coastal Current (East Wind Drift) flows in
the opposite direction and forms clockwise gyres in the Weddell Sea,
Ross Sea and Bellingshausen Sea (Gordon and Goldberg, 1970). The
region between both current systems is an area of wind- and density-
driven upwelling of nutrient-rich circumpolar deep water (Antarctic
Divergence), overlaid by Antarctic surface water in the upper layers (e.g.
Eastman, 1993).
Beside the unique current system, the most important physical feature
structuring the Antarctic marine ecosystem is the ice. The whole Antarctic
shelf is narrow and depressed by the large continental ice sheet to depths of
about 200 to >600 m. Shallow benthic habitats are thus extremely rare in
the South Polar Sea and mostly restricted to the Islands of the Scotia Arc and
along the Antarctic Peninsula. The continental ice sheet extends far beyond
the coastline, forming large, floating ice shelves and a major source of calving
icebergs (Nicol and Allison, 1997), which significantly affect vast areas of the
shelf by grounding and seabed scouring (Gutt, 2001).
Sea ice is present year round but the overall coverage varies strongly with
season, ranging from 4 106 km2 in the austral summer to 20 106 km2 in
winter (Nicol and Allison, 1997; Zwally et al., 1983). Three major zones are
distinguished based on prevailing sea ice conditions (Eicken, 1992): (i) the
high Antarctic zone is almost permanently covered by ice and includes most
areas close to the continent; (ii) the seasonal sea ice zone is characterized by
open water in summer and ice coverage in winter; (iii) the marginal ice
zone represents the transition from sea ice to the ice-free open ocean and
is a region of enhanced ice drift, fragmentation and deformation. Sea ice
dynamics significantly affect stratification of the underlying water column.
During autumn, the depth of the mixed layer in the ice-free zone is
mainly determined by the wind regime. During ice formation and
growth, cold and highly saline (and thereby highly dense) seawater is
ejected from the ice into the water below, resulting in thermohaline
convection and a deepening of the mixed layer (and the pycnocline) to a
depth of 50–200 m. In spring during sea ice melt, the entry of freshwater
with low density lowers and stabilizes the pycnocline (Eicken, 1995;
Gordon et al., 1984).
Light conditions in the Antarctic and in the upper layer of the South Po-
lar Sea also undergo strong seasonal changes, ranging from 24 h of light in
summer to complete darkness during the winter months.
Notwithstanding these strong seasonal fluctuations in ice coverage and
light regime, the general physical conditions and cold climate in the South
Polar Sea have been stable for more than 15 Ma (Dayton, 1990; Dayton
et al., 1994).
2.2. Biological characteristics

The Antarctic marine biota are well adapted to the physical conditions in
their environment, particularly in the high Antarctic where primary produc-
tion, life cycles and strategies are closely coupled to seasonal sea ice dynam-
ics. During winter, autotrophic primary production is low and mostly
restricted to the sea ice (Arrigo et al., 1997; Lizotte, 2001). During spring
and summer, when the sea ice is melting, the released ice algae fuel
subsequent phytoplankton blooms in the shallow and stable mixed layer
of the marginal ice edge (Lizotte, 2001; Smith and Nelson, 1986); these
blooms are mainly formed by diatoms and Phaeocystis (Estrada and
Delgado, 1990; Nöthig et al., 1991). In autumn, sea ice extends again
and remaining algae are incorporated into newly formed ice (e.g.
Melnikov, 1998). The large microphytoplankton (>20 mm) blooms
account for most of the annual primary production (e.g. Scharek and
Nöthig, 1995; Smith and Sakshaug, 1990) but their occurrence is limited
in time and space. Pico- (0.2 to < 2.0 mm) and nanoplankton (2.0 to
<20 mm) are present in the water column throughout the whole year but
these small size classes achieve much lower biomass and productivity
compared with the bloom system (Detmer and Bathmann, 1997; Scharek
and Nöthig, 1995).
Primary and secondary consumers in the water column are mainly repre-
sented by copepods, hyperiid amphipods, salps, fish larvae, chaetognaths and
euphausiids; larger pelagic predators include squids and fishes (Hempel, 1985;
Siegel et al., 1992). Antarctic krill, E. superba, is a dominate member of the
community in the seasonal sea ice zone and the life history pattern of this
species is closely linked to the seasonal sea ice cycle (Smetacek et al.,
1990). In the high Antarctic zone, E. superba is replaced by a smaller
congener Euphausia crystallorophias, the so-called ice krill (e.g. Hempel,
1985). Most zooplankton species are present and feeding in the upper
water column or at the ice underside the whole year round (Bathmann
et al., 1991; Marshall, 1988; resland, 1995; Smetacek et al., 1990).
Benthic shelf communities in the high Antarctic are characterized by ex-
traordinarily high biomass and diversity (Brey and Gerdes, 1997; Dayton
et al., 1994; Gutt et al., 2004) and are characterized by the dominance of
suspension and deposit-feeding species such as sponges, ascidians and
echinoderms (Dayton et al., 1974; Gutt and Starmans, 1998; Voss, 1988).
In many regions, from shallow water coastal zones to deeper high
Antarctic shelf areas, benthic community structure is shaped by physical
disturbance, in particular by ice (Gutt, 2000, 2001; Sahade et al., 1998;
Smale et al., 2008). In the eastern Weddell Sea, for example, the
disturbance of the seafloor by grounding icebergs results in a patchy
distribution of various successional stages, which increases between-
habitat diversity (Gutt, 2000, 2001; Gutt and Piepenburg, 2003; Knust
et al., 2003) which adds a spatiotemporal component to changes in the
structure of the benthic food webs (Hagen et al., 2012).
In vast areas of the high Antarctic shelf, large sponges form a typical
3-dimensional habitat for a diverse invertebrate and fish community
(Arntz et al., 1994; Gutt and Starmans, 1998). Sponges are often used
by invertebrates and fishes as a refuge and/or nursery as well as an upper
level substrate to benefit from enhanced access to the water column
(Fig. 2A,B). In shallow, inshore areas (e.g. Potter Cove in King George
Island), benthic macroalgae such as Desmarestia spp., Himantothallus
grandifolius and Palmaria decipiens contribute significantly to primary
production (Quartino and Boraso de Zaixso, 2008). As with the sponges
on the deeper shelf, benthic macroalgae in shallow waters provide an
analogously complex habitat and shelter for a multitude of species
including fishes in coastal communities (e.g. Barrera-Oro and Casaux,
1990; Gambi et al., 1994; Moreno et al., 1982; Tada et al., 1996;
Takeuchi and Watanabe, 2002) and are a major food source for
secondary producers (Iken, 1996; Tatián et al., 2004). Below the depth
zone of macroalgal presence, benthic consumers depend on pelagic
production (e.g. Mincks et al., 2008). On the high Antarctic continental
shelf, where benthic macroalgae are absent over vast areas, tight bentho-
pelagic coupling plays an important role in the food web. The high
benthic biomass found on the shelf indicates a highly efficient transfer of
organic matter from surface waters towards the seafloor (Smith et al.,
2006). The vertical export of energy is driven either passively, via sinking
particulate organic matter (POM), or actively by migrating organisms.
POM flux on the shelves is dominated by faecal pellets and strings, and
large diatoms (Bathmann et al., 1991; Bodungen et al., 1988; Fischer, 1989;
Nöthig and Bodungen, 1989). Mass sedimentations of ice algae, Phaeocystis
Figure 2 (A) Trematomus cf. nicolai hiding inside a sponge; (B) Pogonophryne sp. on top
of a sponge (ANT XXVII-3 in 2011, western Weddell Sea). Photos: ©Tomas Lundälv, Uni-
versity of Gothenburg.
or diatoms after ice melt and termination of blooms are seasonally important
export mechanisms (DiTullio et al., 2000; Riebesell et al., 1991; Scharek
et al., 1999). Several zooplankton species including Antarctic krill,
copepods and salps were observed to undertake extensive vertical
migrations within the water column (Atkinson et al., 1992; Gili et al.,
2006; Zhou and Dorland, 2004), thereby significantly contributing to the
energy export from the euphotic zone towards the seafloor.
The marine living communities of the South Polar Sea are exploited by a
multitude of endothermic animals. Whales and seabirds are seasonal visitors
that forage in the seasonal sea ice zone and under the pack ice during summer
(Boyd, 2002; Murase et al., 2002; Van Franeker et al., 1997). Penguins
(mainly Emperor penguin, Aptenodytes forsteri, and Adélie penguin,
Pygoscelis adeliae) and seals (Weddell seal, Leptonychotes weddellii; Ross seal,
Ommatophoca rossii; Crabeater seal, Lobodon carcinophagus; Fur seal,
Arctocephalus gazella; Elephant seal, Mirounga leonina) are permanent
inhabitants of Antarctic coastal areas. Extensive cracks in the ice shelf
covered by sea ice, such as the Drescher Inlet in the Riiser-Larsen Shelf
ice (eastern Weddell Sea), represent particularly important breeding and
foraging grounds for Weddell Seals and large Emperor Penguin colonies
(Plötz et al., 1987).
3. ANTARCTIC FISH COMMUNITIES

3.1. Composition of the modern fauna
Despite the large area covered by the South Polar Sea (>20 million km2),
the modern fish fauna is composed of only about 320 species, belonging
to 50 families (Eastman, 2005). This Antarctic ichthyofauna is unique for
two reasons: (i) the modern fish fauna is highly endemic, with 88% of all
species being confined to the South Polar Sea (Andriashev, 1987), and
(ii) the communities are dominated by a single taxonomic group, the
perciform suborder Notothenioidei, which accounts for about 35%
of all Antarctic fish species (Eastman, 1993). In high Antarctic shelf
areas, such as those of the eastern Weddell Sea, notothenioids form up
to 98% of the total fish abundance and biomass (R. Knust and
K. Mintenbeck, unpublished data). Groups typical of fish communities
in temperate or boreal regions, such as clupeids, are absent. Non-
notothenioid fish species inhabiting the South Polar Sea mostly belong
to typical deep-sea groups such as zoarcids, liparids, macrourids and
myctophids. The occurrence of these groups is largely restricted to the
lower slope and the deep sea where notothenioid fishes, except for the
two Dissostichus spp. (Dissostichus eleginoides and Dissostichus mawsoni),
are absent (Boysen-Ennen and Piatkowski, 1988; Donnelly et al.,
2004; Gon and Heemstra, 1990; Kock, 1992).
Close to 100 notothenioid fish species have been described from the
South Polar Sea (Eastman and Eakin, 2000) but new species are still being
discovered (see e.g. Eakin and Balushkin, 1998, 2000; Eakin and
Eastman, 1998; Eakin et al., 2008). Most species belong to just five
families: Nototheniidae (notothens), Channichthyidae (icefish),
Artedidraconidae (plunderfish), Bathydraconidae (dragonfish) and
Harpagiferidae (spiny plunderfish). Endemism within the suborder is
extremely high, with 97% of notothenioid species being found only in
the Antarctic (Andriashev, 1987).
The diversity of the demersal fish community differs regionally, with a
latitudinal shift in species composition (Hureau, 1994; Kock, 1992;
Mintenbeck et al., 2003, 2012; Permitin, 1977). In the ice-free zone,
on the Sub-Antarctic island shelves, typical members of the demersal
fish communities are the channichthyids Chaenocephalus aceratus and
Champsocephalus gunnari, the nototheniids Patagonotothen guntheri, Gobionotothen
gibberifrons, Lepidonotothen spp., Notothenia spp. and D. eleginoides (Patagonian
toothfish).
At higher latitudes, in the seasonal sea ice zone, communities are dominated
by Lepidonotothen spp., Notothenia spp., Chionodraco rastrospinosus (Chan-
nichthyidae) and some species of the genus Trematomus (see also Barrera-
Oro, 2002). In inshore shallow waters, the harpagiferid Harpagifer antarcticus
is also abundant (Barrera-Oro, 2002; Barrera-Oro and Casaux, 1998).
The demersal fish fauna in the high Antarctic zone is characterized by
several Trematomus (Nototheniidae), artedidraconid and bathydraconid spe-
cies, and the channichthyids Chionodraco spp. and Cryodraco antarcticus
(Donnelly et al., 2004; Eastman and Hubold, 1999; Hubold, 1992;
Schwarzbach, 1988). In high Antarctic shelf regions, such as the eastern
Weddell Sea shelf, species diversity is much higher than on the Sub-
Antarctic island shelves or west of the Antarctic Peninsula (Mintenbeck
et al., 2012; Schröder et al., 2001). The major reasons for this high
species diversity are the 3-dimensionality of the benthic habitat and the
high between-habitat diversity shaped by grounding icebergs, both
allowing for small-scale niche separation (horizontally and vertically) and
thus for the coexistence of trophically similar species (Brenner et al.,
2001; Gerdes et al., 2008; Knust et al., 2003).
Figure 3 Composition of the pelagic and demersal fish communities on the eastern
Weddell Sea shelf between 200 and 600 m water depth (samples from 26 otter trawl
hauls and 10 hauls with a bentho-pelagic net taken between 1996 and 2004). Only
the 28 out of 49 species contributing > 0.15% to overall individuals and biomass are
shown for the demersal community. Species number, species richness, diversity and
evenness are given for the two communities using different scales.
The pelagic ichthyofauna of the South Polar Sea includes an oceanic and
a neritic fish community. The oceanic pelagic communities off the shelves
are mainly composed of several myctophid fish species (Barrera-Oro, 2002;
Pusch et al., 2004). The neritic pelagic community differs significantly from
the oceanic community and is extremely species poor compared with the
demersal community on the shelf. In Fig. 3, this difference is exemplified
by comparing the pelagic and the demersal fish communities on the
eastern Weddell Sea shelf between 200 and 600 m water depth. The
neritic pelagic fish community is composed of very few species, and most
of them (e.g. the channichthyids Chionodraco spp., Dacodraco hunteri,
Neopagetopsis ionah and the bathydraconid Gymnodraco acuticeps) are in fact
demersal fishes that only occasionally move into the water column. The
cryopelagic nototheniid Pagothenia borchgrevinki is closely associated with
the underside of ice (e.g. Janssen et al., 1991) and is rarely found in open
waters. Both the demersal and pelagic fish communities are distinctly
dominated by a single nototheniid species, the Antarctic silverfish
P. antarcticum. The only other species that attains higher biomass in the
demersal community is the large icefish Chionodraco myersi (Fig. 3).
P. antarcticum is an endemic species with circum-Antarctic distribution
and is one of the few truly pelagic representatives of the entire suborder
Notothenioidei. It is a shoaling species (Eastman, 1985a) and adults
undertake diel vertical migrations from the sea floor towards the surface
waters (Fuiman et al., 2002; K. Mintenbeck and R. Knust unpublished
data; Plötz et al., 2001). This species dominates the pelagic fish biomass
in coastal waters of the South Polar Sea by >90% (see also DeWitt,
1970; Donnelly et al., 2004; Hubold and Ekau, 1987). In the southern
Weddell Sea, P. antarcticum accounts for most of the overall fish
production, and stock density was estimated to amount at least
1 ton km 2 (Hubold, 1992). Though usually found in the free water
column, its life cycle strategy, including its feeding dynamics, seems to be
closely associated with the sea ice (Daniels, 1982; La Mesa and Eastman,
2012; Vacchi et al., 2004). Besides adult P. antarcticum, larvae and early
juveniles of several notothenioid species dominate the neritic pelagic fish
community numerically. The notothenioid ichthyoplankton community
is also dominated by early life stages of P. antarcticum. Notothenioid larvae
are mainly concentrated in the upper 50 m in well-stratified surface
waters, while juveniles occur in slightly deeper waters (Granata et al.,
2002; Hubold, 1984, 1985; Hubold and Ekau, 1987; Kellermann, 1986a,
b; Morales-Nin et al., 1998). Due to their dominate role in Antarctic fish
communities, this chapter largely focuses on notothenioids.
3.2. Evolution and adaptive radiation

The uniqueness of the Antarctic fish fauna with its high degree of endemism
and a single dominant group is the result of a long evolutionary history of
adaptive radiation in isolation at sub-zero temperatures. Though fossil re-
cords are scarce, there is some evidence that the fish fauna in the Antarctic
during the Eocene differed substantially from the modern fauna and that the
community was composed of species from many, and more cosmopolitan,
families (Eastman, 1993, 2005; Eastman and Grande, 1989). Following the
complete separation of Antarctica and the progressive cooling of the region’s
waters, most components of the Eocene fish fauna vanished from shelf areas.
Local extinctions likely occurred due to habitat loss associated with the
massive expansion of the ice sheet and changes in trophic structure (Eastman,
2005). After this period of extinctions, a multitude of niches were available
for other species. These niches were filled by species of the suborder
Notothenioidei, which have undergone a remarkable diversification by
adaptive radiation on the isolated shelf of the Antarctic continent. The
lack of competition from other fish groups allowed increased
morphological and ecological diversification of notothenioid fish and
expansion into various niches (e.g. Eastman and McCune, 2000; Ekau,
1988; Ptacnik et al., 2010). Accordingly, notothenioid fish species
now occupy benthic, bentho-pelagic, pelagic as well as cryopelagic
habitats. However, due to the lack of a swimbladder in their common
ancestor, the majority of recent notothenioid species are demersal
(Clarke and Johnston, 1996). Adaptive radiation of notothenioids also
included trophic diversification (Ekau, 1988; Schwarzbach, 1988), and
notothenioid fishes now occupy a multitude of trophic niches. Kock
(1992) distinguished five main feeding types according to their principal
prey: benthos feeders, fish and benthos feeders, plankton and fish feeders,
plankton and benthos feeders, and plankton feeders. As some species,
such as the channichthyid D. hunteri, rely almost exclusively on piscivory
(Eastman, 1999; Schwarzbach, 1988), a sixth group of pure ‘fish feeders’
also exists.
The point at which the characteristic modern fauna became established
exactly is unknown (Clarke and Johnston, 1996; Eastman, 2005). The few
existing fossil records indicate first appearance of this group in the early
Tertiary (38 Ma; Balushkin, 1994), and according to a recent phylogenetic
study, radiation of notothenioids began near the Oligocene–Miocene
transition (24 Ma), coinciding with the enhanced formation of sea ice
(Matschiner et al., 2011).
3.3. Adaptations and characteristics of notothenioid fishes

3.3.1 Physiological and morphological adaptations
Notothenioid fishes are characterized by a multitude of physiological ad-
aptations to life within cold waters, but the key innovation enabling species
to survive and diversify was most likely the evolution of antifreeze glyco-
proteins (AFGPs; Matschiner et al., 2011). AFGPs provide a highly effi-
cient protection from freezing of hypoosmotic (compared to seawater)
body fluids by adhering to and blocking the growth of ice crystals
(DeVries, 1971; Fletcher et al., 2001). Concentrations of AFGP differ
between species and depend on ambient water temperature, depth
distribution, life cycle, activity and phylogeny (Wöhrmann, 1996, 1997).

AFGP synthesis is most likely regulated by ambient water temperature
(Wöhrmann, 1997).
Beside the risk of freezing, another problem of life at sub-zero tempera-
tures is the temperature dependence of viscosity of body fluids in ectotherms.
Viscosity and temperature are strongly, negatively correlated, that is, body liq-
uids become more viscous when cold, which affects membrane fluidity, blood
circulation, enzyme kinetics and gas diffusion (e.g. Hochachka and Somero,
2002). Cell membrane fluidity is maintained in the cold by homeoviscous ad-
aptation (see Sinensky, 1974), which involves an increased content of unsat-
urated fatty acids and specific membrane phospholipids (e.g. Eastman, 1993;
Hazel, 1995). An increased blood viscosity is offset by reduced haematocrit
and haemoglobin concentrations in notothenioid fishes (Egginton, 1996,
1997a,b; Kunzmann, 1991). The only known exceptions of fish with a
relatively high haematocrit are Notothenia coriiceps and N. rossii from the
Antarctic Peninsula (Beers and Sidell, 2011; Mark et al., 2012; Ralph and
Everson, 1968). Owing to the low metabolic demands of notothenioids
(e.g. Clarke, 1983; Clarke and Johnston, 1996) and the increased physical
oxygen solubility in seawater, blood and cytosol at cold temperatures, the
reduction in haematocrit and respiratory pigment is not detrimental to
aerobic performance. In species of the family Channichthyidae, the so-
called icefishes or white-blood fishes, functional red blood cells are
completely absent: these fishes do not possess any oxygen-binding pigment
(haemoglobin) in their blood and some species also lack intracellular
myoglobin (Montgomery and Clements, 2000; Sidell and O’Brien, 2006).
The limited oxygen-carrying capacity of the blood is compensated by a
multitude of secondary adaptive body modifications in icefishes, for example,
a larger ventricle, increased blood volume and cardiac output, and increased
skin vascularity (Kock, 2005a; O’Brien and Sidell, 2000; O’Brien et al., 2003;
Sidell, 1991). Molecular adaptations also include the absence of heat-shock
protein expression in some notothenioids (Carpenter and Hofmann, 2000)
and a rearrangement of the mitochondrial genome that may have
supported cold adaptation of mitochondrial properties (Mark et al., 2012;
Mueller et al., 2011; Papetti et al., 2007; Zhuang and Cheng, 2010).
The increased viscosity of body fluids, together with cold temperatures,
affect enzyme kinetics and cytosolic diffusion processes (Sidell, 1991).
Both gas diffusion and enzyme kinetics are temperature dependent and
decelerate rapidly at cold temperatures. Mitochondrial oxidative capacity
of notothenioid fishes is low compared with warm water species
(Johnston et al., 1994), and reduced diffusion of gas and metabolites to and
from mitochondria entails an additional reduction of available energy and
oxygen. The negative effects of temperature and viscosity on enzymes
and diffusion are counterbalanced in Antarctic fishes by two metabolic ad-
aptations. First, these fishes have increased quantities and capacities of intra-
cellular enzymes (Crockett and Sidell, 1990), which reduce diffusion
distance and increase efficiency (Pörtner et al., 2000). Second, they display
mitochondrial proliferation, an increase in mitochondrial abundance and
ultra-structural density (Guderley and Johnston, 1996). Up to 60% of muscle
fibre volume of the slow-swimming, pelagic notothenioid P. antarcticum is
occupied by mitochondria (Clarke and Johnston, 1996). Additionally, many
species have relatively high intracellular concentrations of lipids which may
be used as energy stores (Crockett and Sidell, 1990; Eastman and DeVries,
1981) and aid gas diffusion (Kamler et al., 2001). These intracellular lipids
also play a role in buoyancy (see below).
Notothenioid fishes are thus well adapted to cold waters. Nevertheless,
these adaptations apparently involve an extreme stenothermy of physiolog-
ical functions and seem to result in narrow thermal tolerance windows of this
group (Johnston, 2003; Mueller et al., 2011; Pörtner and Peck, 2010;
Somero and DeVries, 1967).
However, the success of notothenioid species in the South Polar Sea eco-
system is not only based on physiological adaptations, but also on morpho-
logical modifications related to buoyancy (Eastman, 2005; Eastman et al.,
2011). Notothenioids lack a swim bladder and, without this organ, the
exploitation of bentho-pelagic or pelagic food sources is extremely
energy consuming. To compensate for the lack of a swim bladder, some
notothenioid species developed modifications in body structure, which
allow them to inhabit and to exploit the pelagic realm without an
energetic disadvantage. In these species, mineralization of skeleton and
scales is reduced, and the skeleton contains a high proportion of cartilage,
which is less dense than bone (DeVries and Eastman, 1978; Eastman and
DeVries, 1981, 1982; Eastman et al., 2011). P. antarcticum has a persistent
notochord and large amounts of lipids (accounting for 39% of muscle
dry mass) are stored in subcutaneous and intramuscular lipid sacs which
provide static lift (DeVries and Eastman, 1978). D. mawsoni possess
extensive lipid deposits in adipose cells, which account for 23% white
muscle dry weight (Eastman and DeVries, 1981). The lipid deposits in
these species mainly consist of triglycerols (Eastman and DeVries, 1981,
1982; Hubold and Hagen, 1997). However, neutral buoyancy is rare in
notothenioids and limited to very few species, for example, P. antarcticum,

D. mawsoni and Aethotaxis mitopteryx (Eastman, 2005).
3.3.2 Growth, reproduction and development

Most notothenioids are characterized by a rather sluggish mode of life and
high longevity. High Antarctic fish species typically reach ages of
15–21 years (see Kock, 1992; La Mesa and Vacchi, 2001 for review). The
pelagic P. antarcticum was estimated to live more than 30 years (Radtke
et al., 1993). Growth performance of most species is similar to species
from boreal or temperate regions (Kock and Everson, 1998; La Mesa and
Vacchi, 2001) but there seems to be a trend towards lower growth
performance in the high Antarctic notothenioids, relative to their
congeners from the seasonal sea ice zone (Kock, 1992). However, in
adult fish, growth performance is apparently related to lifestyle and tends
to increase from pelagic towards benthic lifestyles (La Mesa and Vacchi,
2001). Pelagic fishes such as P. antarcticum are thus characterized by slow
growth (e.g. Hubold and Tomo, 1989). Many notothenioids show a
distinct seasonal growth pattern with high growth rates in summer and
low growth rates in winter (Hureau, 1970; North et al., 1980; White,
1991). The interspecific latitudinal and intraspecific seasonal differences in
growth rates of notothenioids most likely (primarily) stem from variations
in food supply and/or prey composition, and feeding intensity (Kock,
1992). For example, N. coriiceps undergoes winter metabolic suppression
and enters a dormant stage with periodic arousals lasting only a few
hours, resulting in a net loss of growth rate during the winter months
(Campbell et al., 2008). However, most notothenioids seem to feed year
round (e.g. Casaux et al., 1990; Hubold, 1992).
Sexual maturity is delayed in most Antarctic fishes. With a few excep-
tions, species reach maturity at 50–80% of their maximum age and size
(Kock and Everson, 1998; La Mesa and Vacchi, 2001). The spawning
season is species- and location specific: in the seasonal sea ice zone, most
species spawn in autumn/winter and in the high Antarctic zone, most
species are summer and autumn spawners (Kock and Kellermann, 1991).
Some species have demersal eggs, which are often laid on rocks or in the
cavity of sponges. Nest-guarding and other parental care behaviours have
been reported increasingly in notothenioids (e.g. Barrera-Oro and
Lagger, 2010; Detrich et al., 2005; Kock et al., 2006; Moreno, 1980).
Others species, for example, P. antarcticum, have pelagic eggs (Faleyeva
and Gerasimchuk, 1990; Vacchi et al., 2004). The eggs are usually large
and yolky, so relative fecundity is low in most species, particularly in high

Antarctic notothenioids (Hubold, 1992; Kock, 1992; Kock and Kellermann,
1991). The incubation period of eggs is long and usually takes several months
(Hubold, 1992; Kock and Kellermann, 1991; North and White, 1987).
Larvae of many species apparently hatch in spring and summer
(Efremenko, 1983) when food conditions are best; however, some
species also hatch in winter (Ekau, 1989; North and White, 1987).
Larvae are large at hatching (Kellermann, 1990; North and White, 1987)
and the mouth is well-developed, so that even early yolk-sac larvae are
able to feed (Kellermann, 1986b). Most, if not all, notothenioid larvae are
pelagic.
3.4. Threats to the fish community

Antarctic fish communities are threatened by climate change in multiple
ways. On the one hand, fishes might be affected at the physiological level
directly by increasing water temperatures and pCO2, and reduced water sa-
linity. Due to the numerous adaptations to life in the South Polar Sea, fishes
are likely to be affected on different organizational levels, from the cellular
level up to the population level and beyond. In particular, an increase of wa-
ter temperatures might pose a major threat to stenothermal species (see e.g.
Somero, 2010), whereas increasing concentrations of CO2 might have more
general detrimental effects across many fish species (e.g. Ishimatsu et al.,
2005). Whether and to what extent fitness and survival are affected by such
changes depends on individual or species-specific physiological plasticity.
Climate change can additionally affect fishes indirectly by secondary ef-
fects, such as those due to changes in the abiotic environment that will entail
alterations in the food web, as also reported for instance in many freshwaters
(Meerhoff et al., 2012). Unfavourable abiotic conditions as well as invasion
of Antarctic waters by non-indigenous species may result in changes in tro-
phic structure and dynamics by alterations in composition and population
density of prey and predator communities (Woodward et al., 2010a).
Changes in prey species composition will involve alterations in the type
of prey available to fishes, particularly in size structure and energy content: a
shift from diatoms to cryptophytes is accompanied by a strong shift in size
structure of primary producers, and ultimately with a potential size shift
in secondary producers; a shift from a krill dominated zooplankton commu-
nity towards a community dominated by salps involves a drastic decrease in
nutritional value of potential prey for higher trophic level consumers (but
see also Gili et al., 2006). In the marine Antarctic, where life cycles are
closely coupled to seasonal sea ice dynamics, changes in water temperature
itself but also reduced sea ice extent and duration might entail phenological
shifts and a trophic mismatch between prey and consumer species (Hagen
et al., 2012). Secondary effects of climate change may also involve a reduc-
tion of habitat, which could lead to fragmentation of the food web (Hagen
et al., 2012): sea ice reduction means a loss of habitat for ice-associated pe-
lagic species, but demersal fish are threatened by habitat reduction as well, as
warmer temperatures will most likely result in enhanced disintegration of
glaciers and ice shelves. An increased iceberg calving and breakup will lead
to a higher frequency of iceberg scouring events and thus to increased sea-
floor and habitat destruction.
From other ecosystems, it is well-known that many fish species are sen-
sitive to these types of threats, via mechanisms operating directly at the eco-
physiological level (e.g. McFarlane et al., 2000; Pörtner and Peck, 2010;
Pörtner et al., 2008) but also indirectly at the trophic level (Beaugrand
et al., 2003; Benson and Trites, 2002; Drinkwater et al., 2010), as well as
by alterations in habitat structure and heterogeneity (Hughes et al., 2002;
Yeager et al., 2011).
4. PHYSIOLOGICAL VULNERABILITY OF ANTARCTIC

FISHES
4.1. Sensitivity to changes in temperature and salinity
Antarctic fishes have very narrow thermal windows due to cold adaptation
(Clarke, 1991; Somero et al., 1968; Wohlschlag, 1963), resulting in high
stenothermy in this group (Gonzalez-Cabrera et al., 1995; Podrabsky and
Somero, 2006; Robinson et al., 2011; Somero and DeVries, 1967). Most
species, for example, the bottom-dwelling Trematomus bernacchii, Trematomus
hansoni and Trematomus pennellii, have an upper lethal temperature between
just 4 and 6 C (Robinson, 2008; Somero and DeVries, 1967). Fish
performance is already affected well below the lethal limit. However, the
paradigm that all notothenioid species are extremely stenothermal without
exceptions has recently been revised.
Some species such as H. antarcticus and young N. coriiceps are frequently
found in tide pools in King George Island (South Shetland Islands), where
during sunny days individuals are exposed to warm temperatures for many
hours (E.R. Barrera-Oro and E. Moreira, personal observation). Thus, these
species can at least cope with acute, relatively short-term temperature
increases. A few species are apparently also able to compensate for chronic
exposure to higher temperatures, for example, the cryopelagic P. borchgrevinki
shows some metabolic plasticity: long-term warm acclimation of P. borchgrevinki
to 4 C results in a shift of the thermal tolerance window towards warmer
temperatures (Bilyk and DeVries, 2011; Franklin et al., 2007; Robinson and
Davison, 2008) owing to metabolic compensation (Seebacher et al., 2005)
which leads to a reduced performance at low temperatures (Franklin
et al., 2007). Recent measurements of routine metabolic rate of Notothenia
rossii and Lepidonotothen squamifrons from the Scotia Arc shelf revealed a
partial compensation after long-term acclimation to elevated temperatures
(A. Strobel and F.C. Mark, unpublished data). Similarly, long-term
warm acclimation of the Antarctic eelpout Pachycara brachycephalum
involves metabolic rearrangements (Lannig et al., 2005) and indicates an
improvement of hepatic metabolism accompanied by a shift of energy
sources from lipids to carbohydrates (Brodte et al., 2006, Windisch et al., 2011).
However, these metabolic acclimations apparently do not result in a full
compensation and cannot be generalized across all species (c.f. the deepwater
zoarcid Lycodichthys dearborni; Podrabsky and Somero, 2006), but seem
rather dependent on the physical capacities of the circulatory system: studies
of energy allocation in isolated cells of Antarctic notothenioids and
P. brachycephalum suggest that within a thermal range of about 1 to 12 C,
thermal tolerance limits are defined at the whole organism level (Fig. 4), for
Figure 4 Temperature dependence of whole animal metabolic rate (filled symbols, left
axis) and respiration rate of hepatocytes (open symbols, right axis) of the Antarctic eel-
pout Pachycara brachycephalum. Due to organismal complexity, acute whole animal
critical temperatures (Tcrit) that mark the onset of anaerobic metabolism are reached
at lower temperatures (13 C, black arrow) than in isolated cells (>21 C, grey arrow;
redrawn from Mark et al., 2002, 2005; with permission from Springer).
example, by capacity limitations of the circulatory system rather than by

a general failure of cellular energy metabolism (Mark et al., 2002, 2005).
Due to their lower level of organizational complexity, thermal tolerance
windows of organelles generally span a wider temperature range than those
of the whole organism (Mark et al., 2005). Thus, acclimatory capacities
are mainly defined by the degree of changes in cellular energy metabolism
and depend strongly on the mitochondrial oxidative capacities. The acute
thermal tolerance of oxidative capacity varies between species and tissues
(Mark et al., 2012; Urschel and O’Brien, 2009). However, these acclimatory
capacities are always constrained within the frame of the thermal window
set by the whole organism’s physiological plasticity.
Fishes possess the flexibility to respond to chronically elevated temper-
atures via mitochondrial proliferation—modifications of the amount and
volume of mitochondria to adjust aerobic capacity (Tyler and Sidell,
1984; Urschel and O’Brien, 2008). Mitochondrial oxygen demand rises
with increasing temperature and aerobic capacities need to be adjusted
accordingly. Only a few studies have demonstrated a full compensation of
the increased oxygen demand at the mitochondrial level after warm
acclimation, and these studies were exclusively performed on non-
Antarctic organisms (e.g. Dahlhoff and Somero, 1993; Sloman et al.,
2008). This indicates that there are limitations to mitochondrial
acclimation, ultimately co-defining the rather narrow bandwidth of
thermal acclimation, especially in Antarctic fishes (Mark et al., 2006).
Increased mitochondrial oxygen demand in warmer conditions may be
met by altering haemoglobin affinities (Tetens et al., 1984) and raising
the haematocrit to optimize the oxygen-carrying capacity of the blood.
Yet, haematocrit levels are correlated with haemoglobin expression
(Beers and Sidell, 2011). Thus, species with low or no haemoglobin
levels have less capacity to adjust haematocrit. This is further exacerbated
by the fact that rising temperatures result in lower levels of physically
dissolved oxygen in the blood. Therefore, icefishes that lack haemoglobin
will be more vulnerable to warming than red-blooded species, because
they cannot increase the oxygen-carrying capacity of the blood.
According to Beers and Sidell (2011), Antarctic fishes with higher
haematocrit levels thus possess higher temperature acclimatory capacities
than species with lower haematocrit.
Studies on the impact of salinity changes on notothenioid fishes are ex-
tremely scarce. O’Grady and DeVries (1982) investigated the capacity for
osmoregulation of adult P. borchgrevinki and Trematomus spp. at a wide range
of salinities (25–200% of the salinity in their natural habitat, 35 psu) and found
these species to be rather tolerant towards even large fluctuations from 50%
to 175% normal salinity. Blood serum osmolarities in Antarctic fishes are
among the highest in marine teleosts, which has been interpreted as an addi-
tional antifreezing protection (O’Grady and DeVries, 1982). After warm
acclimation, serum osmolarities reduced to the levels found in temperate
teleosts were measured in T. bernacchii, T. newnesi and P. borchgrevinki
(Gonzalez-Cabrera et al., 1995; Hudson et al., 2008; Lowe and Davison,
2005), and also in N. rossii and L. squamifrons (A. Strobel and F.C. Mark,
unpublished data). Thus, adult notothenioids are apparently capable of
efficient osmoregulation and seem able to adapt blood osmolarity to
ambient environmental conditions.
Almost all studies on physiological sensitivity of notothenioid fishes to
changing abiotic parameters have been conducted on adults. Data from non-
Antarctic fish species suggest an ontogenetic shift in temperature tolerance,
with narrow thermal tolerance windows in eggs and larvae (e.g. Pörtner and
Farrell, 2008; Pörtner and Peck, 2010). Most teleost fishes are able to
osmoregulate at hatch, but the efficiency seems to be higher in more
advanced developmental stages (Varsamos et al., 2005). To our knowledge,
there are no experimental data for early developmental stages of
notothenioid fishes, but indirect evidence from abundance and distribution
of P. antarcticum larvae and juveniles indicate that these early stages likely
have limited ability to tolerate changes in temperature and salinity. Larvae
and juveniles of this species are mostly found within water masses of
particular temperature and salinity (e.g. Granata et al., 2002; Guglielmo
et al., 1998; Hubold, 1984; Kellermann, 1986a). West of the Antarctic
Peninsula, P. antarcticum larvae and juveniles were clearly confined to cold
and high salinity water masses originating from the Weddell Sea (Slósarczyk,
1986). Based on combined datasets of fish abundances in waters of Weddell
Sea and Bellinghausen Sea origin, Slósarczyk (1986) calculated the range of
approximate optimum conditions for larvae and juveniles in the Bransfield
Strait: Abundances suggested optimal ranges in temperature and salinity of
0.50 to þ0.45 C and 34.10–34.62 psu, respectively.
Though changes in salinity induced by climate change might be a locally
restricted phenomenon, dense aggregations of larvae and juveniles that
are concentrated close to the coast/shelf ice in the upper water layers
might be significantly affected. Moline et al. (2004) found vast areas west
of the Antarctic Peninsula covered by low salinity water (33.4–33.6 psu),
and the meltwater plume extended to depths as great as 50 m (Dierssen
et al., 2002). It still needs to be verified whether and to what degree tem-
peratures and salinities outside the narrow ranges given by Slósarczyk
(1986) limit physiological performance and survival of larvae and juveniles,
but tolerance indeed seems to be low: P. antarcticum larvae acclimated to
cold Weddell Sea water were observed to shrink and to die immediately
at water temperatures >0 C (Hubold, 1990). Whether or not this limited
tolerance holds true for early stages of other species needs further investiga-
tion, but at least P. antarcticum larvae seem to be highly vulnerable to changes
in the abiotic environment.
4.2. Sensitivity to increasing pCO2

Ocean acidification, as an additional stressor in parallel to ongoing
climate warming (Woodward et al., 2010a), may prove to be particularly
threatening to polar ecosystems owing to enhanced CO2 solubility in
cold waters and body fluids. Thermal tolerance windows are narrow in
most species and, thus, sensitivities to combined stressor effects are likely
to be higher in cold-adapted polar compared to temperate species.
Many notothenioids will eventually find themselves at the upper end
of their thermal tolerance range, implying that they are energetically
limited and their physiological performance is highly susceptible to
further stressors, such as the increasing concentration of carbon dioxide
(Pörtner and Peck, 2010).
Previous research on the effects of elevated CO2 levels on marine fishes
led to the general notion that fishes are not particularly vulnerable to the di-
rect effects of ocean acidification alone, due to their powerful mechanisms of
ion regulation (Fivelstad et al., 2003). Most adult fishes are able to compen-
sate for acid–base disturbances (Larsen et al., 1997) and show only minimal
effects of hypercapnia on physiological performance (Melzner et al., 2009)
including an incomplete compensation of extracellular pH (Michaelidis
et al., 2007).
However, several studies on different non-Antarctic fish species demon-
strated chronic effects of environmental hypercapnia, with early develop-
mental stages being particularly affected: exposure to elevated CO2
concentrations impairs embryonic metabolism (Franke and Clemmesen,
2011), survival and growth of eggs and larvae (Baumann et al., 2012),
and growth of juveniles (Moran and Stttrup, 2010), and causes severe to
lethal tissue damage in many internal organs of larvae (Frommel et al.,
2012). The sensitivity to ocean acidification may generally be enhanced
by ocean warming, which has been confirmed in tropical fishes (Nilsson

et al., 2009; Pörtner and Farrell, 2008). Still very little is known about
how the physiology and distribution of Antarctic fishes and their various
life stages may be altered by the additional effects of hypercapnia, but
several current projects are dealing with this topic, and initial results
indicate that chronic hypercapnia leads to significant reductions of
mitochondrial capacities in N. rossii (A. Strobel and F.C. Mark,
unpublished data), on top of the thermal sensitivity of its mitochondrial
metabolism (see Section 4.1 above; Mark et al., 2012). Hypercapnia-
induced regulatory shifts in intracellular metabolic pathways and
capacities therefore may exacerbate the effects of increased temperature
on cellular and whole animal metabolism.
We currently lack sufficient data on Antarctic fishes to be able to gener-
alize as to whether all life stages respond similarly or whether early develop-
mental stages represent potential bottlenecks for population survival.
Another topic that needs to be addressed is how hypercapnia will modify
interactions between species already affected by the warming trend. Recent
findings in tropical coral reef fish demonstrated behavioural disturbances by
moderate levels of ocean acidification (1050 ppm CO2, pH 7.8, year 2100
scenario), presumably elicited by hypercapnia effects on the central nervous
system (Munday et al., 2009). Hypercapnia therefore may also alter trop-
hodynamic interactions in a particular ecosystem (cf. Ferrari et al., 2011),
beyond those of the direct lethal effects on interacting organisms. These as-
pects have never been studied in Antarctic fishes and clearly need further
research.
5. TROPHIC VULNERABILITY OF ANTARCTIC FISHES

5.1. Vulnerability to general changes in trophic structure
and dynamics
The vulnerability of a particular species to changes in food web structure and
dynamics depends on its ability to cope with both ‘bottom-up’ and ‘top-
down’ effects (Jacob et al., 2011; Melian et al., 2011; O’Gorman and
Emmerson, 2010). Trophic plasticity, that is, the capability to cope with
fluctuations in resource availability, is positively related to prey diversity
(specialist vs. generalist consumers; Johnson, 2000; Mihuc and Minshall,
1995). Predator-induced mortality is the principal ‘top-down’ effect, and
suppression of a particular species strongly increases with increasing
predator diversity (Snyder et al., 2006). Vulnerability to ‘top-down’
effects and resilience capability are thus related to the number of predator
species. Accordingly, species vulnerability to food web-mediated
alterations is expected to decrease with prey diversity and to increase
with predator diversity. Whether and how the complete loss of one
species will affect overall food web structure and ecosystem functioning
depends on the community’s capacity for functional compensation, that
is, species trophic redundancy (Johnson, 2000; Naeem, 1998).
Here, the relative trophic vulnerability of the adult notothenioid fish
community inhabiting the eastern Weddell Sea shelf (between 200 and
600 m water depth) to alterations in the food web was estimated. A simple,
quantitative measure based on the number of feeding links to prey and pred-
ator species was used to assess vulnerability. Information on trophic linkages
was extracted from the extensive trophic database published in Jacob et al.
(2011) that includes information on feeding relations of 489 consumer and
resource species from the Antarctic Weddell Sea (for detailed information
and sources, see Jacob, 2005; Jacob et al., 2011). For seven more fish
species, additional information on prey composition was collected from
Foster et al. (1987), Gon and Heemstra (1990), La Mesa et al. (2004) and
Schwarzbach (1988). All in all, information on prey composition and
links to predators was available for 37 of the 42 notothenioid species
inhabiting the shelf. P
For each fish species i, the total number of prey species Pi, the number
of prey Pspecies belonging
P Pto the functional groups ‘Benthos’, ‘Plankton’
P and
‘Fish’, PB,i, PP,i, PF,i, andPthe number
P of predators Ci were
extracted from the database. Both P and C are common descriptors
inPtheoretical food web ecologyP and usually referred to as ‘generality’
( P) and ‘vulnerability’ ( C; see e.g. Memmot et al., 2000; Schoener,
1989). Here, both variables were combined to calculate consumers’
relative trophic vulnerability,
P a comparative index with values located
between 0 and 1.P C was taken as a measure of vulnerability to top-
down effects, and P as an (inverse) measure of vulnerability to bottom-
up effects.
The relative trophic vulnerability VIi of fish species i can thus be com-
puted by
P
m
Ci
i¼1
VIi ¼ P
n P
m ½1
Pi þ Ci
i1 i¼1
where m is the total number of consumer PspeciesPand n is the total number

of preyP speciesPof fishPspecies i.
P Pi þ Ci 1 and 0 VIi 1;
Pi ¼ PB,i þ PP,i þ PF,i. In this basic equation (Eq. 1), each Ci
and Pi count 1.
However, there is a difference in relative top-down and bottom-up ef-
fects depending on (i) whether a particular consumer is a generalist feeder or
specialized on fish species i and (ii) whether a particular prey species is ex-
clusively consumed by fish species i or exploited by a multitude of predators.
To account for these differences, each consumer of fish species i, Ci,
was weighted by the number of its own prey species (Pj) and each prey spe-
cies of fish species i, Pi, was weighted by the number of its own consumer
species (Ck). These weighted consumer and prey values of fish species i are
referred to as WCi and WPi, respectively. Accordingly, the calculation of the
relative trophic vulnerability index VIi of fish species i was adapted by
P
m
WCi
i¼1
VIi ¼ P
n P
m ½2
WPi þ WCi
i¼1 i¼1
with
0 1 0 1
B 1 C B 1 CX X
WPi, k ¼ B Cand WCi, j ¼ B
B
C
C; WP þ WCi > 0
@Pm A @Pn
A
i
Ck Pj
k¼1 j¼1
P P P P
and 0 VIi 1; WPi ¼ WPB,i þ WPP,i þ WPF,i. Here, m is the
total number of weighted consumer species and n is the total number of
weighted prey species of fish species i. This index was used as an indicator
of species’ risk to be negatively affected by changes in the food web. Spe-
arman’s rank correlation was usedP to analyze
P relationships
P between
P all pa-
rameters
P with the aim to rank WC, WP, WP B, WP P and
WPF according to their effectPon VI.
The number of prey items P ranged from 5 in some planktivorous
P
fishes to >100 in benthos feeders. The number of predators C ranged
from 12 to 47 (Table A1). The majority of notothenioid fish species are
benthos feeders and mixed feeders, consuming varying proportions of ben-
thos and plankton (Fig. 5). The number of pure plankton feeders and
mixed feeders of plankton and fish is comparatively low and pure pisciv-
orous species are extremely scarce. Relative vulnerability VI is related to
P P P
Figure 5 Relative proportions [%] of benthos ( PB), plankton ( PP) and fish ( PF) in
the diet of notothenioid fish species. Each circle represents one species; circle diameter
indicates relative trophic vulnerability (VI). For species code numbers, see Table A1.
the distribution of prey species among the functional groups ‘Benthos’,

‘Plankton’ and ‘Fish’. VI is lowest in benthos feeders (VI 0.02–0.11, mea-
n SD 0.07 0.03), fish feeders (VI 0.1, mean SD 0.1 0) and benthos
and fish feeders (VI 0.03–0.07, mean SD 0.05 0.02), intermediate in
mixed feeders of benthos and plankton (VI 0.02–0.28, mean SD
0.16 0.07) and highest in species feeding almost exclusively on plank-
tonic prey (VI 0.15–0.96, mean SD 0.56 0.34) or on a mixture of
plankton and fish (VI 0.28–0.77, mean SD 0.69 0.20). The highest
VI of 0.96 is found in the plankton-feeding P. antarcticum, followed by
some channichthyid species such as C. myersi and C. antarcticus with VIs
of 0.77 (see Table A1; Fig. 5). It appears that there is a certain accumulation
of risk in the P
trophic group of plankton feeders. VI is correlated more
strongly
P with WP (Spearman’s r ¼ 0.980, p < 0.0001; Table 1) than
to WC (r ¼ 0.614, p < 0.0001). In notothenioid fishes, differences in rel-
ative vulnerability VI between species are thus mainly determined by the
number of prey items, that is, by the degree of generalism (see Table 1).
The effect of predator diversity is of less significance, as most fish species
share a similar number of potential predators that feed non-selectively.
Table 1 Spearman's rank correlations between

P relative trophic vulnerability index VI,
weighted
P number of consumer species WC and
P weighted number P of prey species
P
WP, with the functional prey
P groups benthos
P WP B, plankton
P WPP and
P fish WPF
VI WC WP WPB WPP
P
WC r ¼ 0.614 – – – –
p < 0.0001
P
WP r ¼ 0.980 r ¼ 0.505 – – –
p < 0.0001 p ¼ 0.0014
P
WPB r ¼ 0.861 r ¼ 0.648 r ¼ 0.817 – –
p < 0.0001 p < 0.0001 p < 0.0001
P
WPP r ¼ 0.389 r ¼ 0.469 r ¼ 0.347 r ¼ 0.490 –
p ¼ 0.0174 p ¼ 0.0034 p ¼ 0.0357 p ¼ 0.0021
P
WPF r ¼ 0.186 r ¼ 0.500 r ¼ 0.101 r ¼ 0.436 r ¼ 0.449
ns p ¼ 0.0016 ns p ¼ 0.0070 p ¼ 0.0053
For each parameter combination, correlation coefficient r and level of significance (p value) are given (ns,
not significant, that is, p > 0.05). With respect to VI, r and p are interpreted as indicators of effect strength
with signs indicating the direction of the effect.
P
Among functional prey groups, the number of benthic prey items WPB
P effect on VI (r ¼ 0.861, p < 0.0001), followed by
exerts the strongest
planktonic preyP WPP (r ¼ 0.389, p ¼ 0.0174). The number of fish spe-
cies in the diet WPF is not significantly related to VI (p > 0.05). The pat-
tern of high benthic biomass and diversity on the high Antarctic shelf (see
Section 2.2) is obviously reflected in notothenioid prey diversity
P and thus
in trophic vulnerability: the number of benthic prey species WPB exerts
by far the strongest effect on VI; the higher the share of benthic species in
the diet, the lower is VI (Table 1; Fig. 5).
The resilience of the entire system, that is, to what extent the extinction
of particular consumer species from the system impacts overall food web sta-
bility and ecosystem functioning, strongly depends on the systems’ ability to
compensate for the loss by co-occurring species (Johnson, 2000; Naeem,
1998). As the majority of species include a certain proportion of benthic
prey in their diet, functional redundancy seems to be high among
benthos feeders (see Fig. 5). Feeding on the benthos is associated with a
high degree of trophic generalism and functional redundancy, and hence
with a certain capability to adapt food choice to prey availability and to
dampen bottom-up effects. Plankton consumers tend to have higher
vulnerability: specializing on a comparatively narrow prey spectrum
makes them more sensitive to changes in prey availability. As there are
fewer plankton-feeding species in the system, the potential for functional

compensability is lower, too, making this part of the food web
particularly sensitive to change.
Larvae and juveniles were not considered in this analysis because infor-
mation on diet composition of early stages is not as complete as that of the
adults for most species (except for P. antarcticum; see e.g. Granata et al., 2009;
Kellermann, 1987; Vallet et al., 2011). However, as early stages of most
notothenioids are pelagic, it is most likely that the relative trophic
vulnerability is high Pcompared with adult benthic stages. The number of
potential predators ( C) is presumably size- (see Section 5.2) and/or
density-dependent (e.g. Woodward et al., 2010b). Early stages of
P. antarcticum, for example, occur in dense aggregations and are heavily
preyed upon by other notothenioids (Eastman, 1985b; Hubold and Ekau, P
1990; La Mesa et al., 2011). The degree of trophic generalism ( P)
seems to differ strongly among families. Nototheniid larvae (including
P. antarcticum) feed mainly on early copepod stages and eggs, whereas
early juveniles feed on small copepod species. Compared with
nototheniids, larvae and juveniles of the family Channichthyidae (e.g.
C. myersi, C. antarcticus) are trophic specialists, with a narrow food
spectrum that is exclusively composed of early developmental stages of
krill and fish fry (Hubold and Ekau, 1990; Kellermann, 1986b, 1987,
1989). Accordingly, relative trophic vulnerability of larval and juvenile
channichthyids is expected to be very high.
5.2. Vulnerability to changes in size structure and prey quality

5.2.1 Prey size
Body size is one of the major factors determining who eats whom in aquatic
food webs (e.g. Brose et al., 2006; Castle et al., 2011; Woodward et al., 2005,
2010a,b). In particular for early developmental stages of fishes, the size of
their prey seems to play an important role as the upper limit of
consumable prey size is strongly limited by mouth width (Kellermann,
1986b, 1987). Accordingly, early stages always feed on a relatively narrow
prey size range (Hubold and Ekau, 1990; Kellermann, 1986b). However,
size of ingested prey is not only determined by morphological constraints
but may also be the result of selective feeding behaviour. In postlarval
and juvenile P. antarcticum, prey selection was found to be a function of
prey density: at low food density conditions, larger prey species were
selectively chosen, but when food density was high, size-selective feeding
behaviour was distinctly less pronounced (Kellermann, 1986b, 1987).
There is also some evidence of size-selective feeding in adult P. antarcticum,

with a negative selection of highly abundant small prey (K. Mintenbeck,
unpublished data). However, whether this is the result of density-
dependent selection (as observed in early stages) or due to other
restrictions still needs to be verified.
In adult fish, mouth gape is less restrictive for prey handling than in larvae
and juveniles, but sensory capabilities might be a limiting factor for efficient
detection of small-sized prey. Depending on species’ sensory capabilities,
detection, capture success and feeding efficiency are likely to vary with prey
size. To test for the impact of prey size on fish detection capability and feed-
ing efficiency, feeding experiments with two nototheniid species were car-
ried out during the expedition ANT/XXVII-3 with RV Polarstern in 2011.
N. coriiceps and N. rossii were caught by means of baited traps in Feb-
ruary 2011 in Potter Cove. Both species belong to the family Not-
otheniidae and are common components of the inshore demersal fish
fauna in waters of the northwestern Antarctic Penı́nsula region (Barrera-
Oro, 2003). Fishes were held unfed in large tanks at a water temperature
of 0 C for about 2 months prior to the experiments. Ten individuals were
selected of each species (size ranges: N. coriiceps 24.2–33.6 cm standard
length (SL), N. rossii 24.0–35.1 cm SL) and transferred into individual
85-l aquaria (0 C water temperature, dim light conditions) 24 h before
the feeding experiment started. Five different prey size classes were offered
to each fish (prey size categories 1 (small) to 5 (large); see Table 2), starting
with the smallest size category. Prey density was constant with 30 prey in-
dividuals per fish in all feeding trials. Times of first reaction, and each
Table 2 Food used in the feeding experiments to test for the impact of prey size on fish
detection capability and feeding efficiency included five different prey size categories
Size category Type Size range [cm] (min–max)
1 Cyclopoid copepods 0.8–1.3
2 Daphnia 2.2–3.0
3 Mysids 9.2–14.5
4 Juvenile euphausiids 12.2–18.9
5 Adult euphausiids 27.9–33.5
Categories 1–4 were commercial frozen fish food (Erdmann Frostfutter, Germany) and category 5 was
adult ice krill (Euphausia crystallorophias) caught during the RV Polarstern expedition. The food was def-
rosted prior to experiments.
Table 3 Number (N) of feeding individuals (N. coriiceps and N. rossii), and mean times
(min:s; standard deviation) until first reaction to prey addition (movement of head
towards prey), first detection of a prey item that was followed by an attack and first
consumption are given for each prey size class (categories 1–5)
Prey N of feeding First First prey First
category fish reaction detection consumption
Notothenia coriiceps
1 0 – – –
2 0 – – –
3 6 2:12 2:53 3:34 3:50 3:36 3:50
4 10 1:27 3:21 1:47 3:18 1:48 3:17
5 10 0:10 0:16 0:10 0:16 0:12 0:15
Notothenia rossii
1 0 – – –
2 1 0:37 0:37 0:40
3 5 4:12 6:04 4:12 6:04 4:13 6:04
4 9 1:18 3:19 1:31 3:16 1:34 3:15
5 10 0:10 0:08 0:10 0:08 0:12 0:07
particular prey detection and consumption were registered; overall exper-

imental duration was 15 min. Depending on the amount of food con-
sumed, the time lag between particular experiments was up to 3 days to
avoid an effect of satiation on feeding behaviour. The offered food was
not alive, but prey items were in motion in the tanks all the time owing
to aeration and steady inflow of fresh seawater.
None of the fish fed on the smallest prey (category 1) and only one small
N. rossii consumed a single prey item of category 2 (Table 3). Except for this
single individual, no reaction to prey of categories 1 or 2 was observed.
Both N. coriiceps and N. rossii started to react when prey of size category
3 was offered: a total of six N. coriiceps and five N. rossi detected and con-
sumed prey of this category. All but one fish fed on size categories 4 and 5.
Time until first reaction to prey addition (movement of the head towards
prey), time of first prey detection that was followed by an attack and time of
first consumption were all inversely related to prey size in both species
(Table 3).
Figure 6 Mean consumption rate (number of consumptions time 1) in N. coriiceps (A)

and N. rossii (B) depending on prey size category (2–5; 2: daphnia, 3: mysids, 4: juvenile
euphausiids, 5: adult euphausiids). For the number (N) of feeding individuals, see
Table 3.
The mean consumption rate (number of consumptions time 1)

depended upon prey size category in both species (Fig. 6; Kruskal–Wallis
ANOVA, N. coriiceps: H ¼ 29.45, p < 0.0001; N. rossii: H ¼ 46.99,
p < 0.0001). The feeding rates were low when fish were offered size catego-
ries 2 and 3, and high for the two largest prey size categories. The feeding
rates of fish offered the two small size categories (2 and 3) were significantly
lower than the feeding rates of fish offered large prey (4 and 5; Dunn’s post
hoc test, p < 0.01), while no differences were found among the two small
nor the two large categories (Dunn’s post hoc test, p > 0.05). The mean time
between detection and consumption was independent of prey size in both
species (Kruskal–Wallis ANOVA, p > 0.05). Neither the total sum of con-
sumed prey nor time until first reaction and mean time between detection
and consumption were significantly correlated with fish size for any prey size
category (Spearman’s rank correlation, p > 0.05). However, the fish used in
these experiments did not differ much in size, hence, further experiments
using a broader range of fish sizes will be needed to verify the relationship
between fish size and these parameters.
Nevertheless, these data clearly show that feeding rates depend strongly
on prey size. Both species are obviously not capable (and/or willing) to at-
tack small prey items and feeding efficiency is low below a certain prey size
limit. This prey size-dependent detection and consumption rate are most
likely not only found in these two species, but might be a limitation in many
other Antarctic species (if not all).
5.2.2 Prey quality

The importance of prey quality for consumers is widely accepted, but only a
few studies have dealt with this issue in fishes. Malzahn et al. (2007) found
nutrient limitation of primary producers to propagate along the food chain,
finally affecting condition of fish (larval herring Clupea harengus; condition
assessed based on RNA/DNA ratios) feeding on herbivorous zooplankton.
Based on the histology of the digestive organs, Koubbi et al. (2007) inves-
tigated the condition of larval P. antarcticum off Terre Adélie in relation to
prey composition and found that larvae feeding on copepods were in better
condition than those feeding on diatoms.
The energy contents of Antarctic and Sub-Antarctic species from various
taxonomic groups are well studied (Ainley et al., 2003; Barrera-Oro, 2002;
Clarke et al., 1992; Croxall and Prince, 1982; Donnelly et al., 1990, 1994;
Eder and Lewis, 2005; Lea et al., 2002; Tierney et al., 2002; Torres et al.,
1994) and are summarized in Fig. 7. Fishes and decapods have the highest
energy contents; squid and crustaceans such as mysids, euphausiids and
copepods have moderate energy contents. By far, the lowest energy
content is found in gelatinous zooplankters such as salps, chaetognaths
and cnidarians. Shifts in the zooplankton community with crustaceans
being replaced by salps (see Section 1) thus involve a drastic decrease in
energy density and nutritive value of prey for consumers such as fish.
Figure 7 Energetic value (kJ g 1 wet weight; means SE) of Antarctic and Sub-
Antarctic species belonging to several taxonomic groups (for details and data sources
for each group, see Mintenbeck, 2008 and references therein).
Some species, such as N. coriiceps, feed on crustaceans (mainly krill and

amphipods) and even on macroalgae (Iken, 1996; Iken et al., 1997).
However, in feeding experiments, algae are only ingested in the absence
of alternative animal prey (e.g. crustaceans; Fanta, 1999; K. Mintenbeck,
unpublished data), providing evidence that macroalgae are not a favoured
food source (see also Fanta et al., 2003). If krill is not available due to a
shift in zooplankton composition, omnivorous fish species such as
N. coriiceps might, however, be increasingly forced to feed on such low
energy macroalgae.
Low energy food might affect survival, growth, body condition and repro-
ductive output of consumers and ultimately might make fish species itself a low
quality prey for its endothermic predators (see Österblom et al., 2006, 2008).
6. VULNERABILITY OF ANTARCTIC FISHES TO HABITAT

DESTRUCTION
6.1. The impact of sea ice reduction
There is no doubt that a reduction in sea ice extent and duration of coverage
due to climate-driven warming will affect the sympagic community living
within the ice and invertebrates such as Antarctic krill, E. superba, whose life
cycle is coupled to seasonal sea ice dynamics (see Moline et al., 2008 for
review). However, there are also fish species whose life cycles and life styles
are closely associated to the sea ice, namely P. borchgrevinki and P. antarcticum.
P. borchgrevinki is morphologically well adapted for a cryopelagic life
(Eastman and DeVries, 1985) and is usually found closely associated with
the underside of ice, where it frequently hides in crevices (e.g. Davis
et al., 1999). Main prey items of this species include sympagic copepods
(Hoshiai et al., 1989): sea ice thus provides the consumer with a habitat, ref-
uge and feeding ground. Though P. antarcticum is usually found in the free
water column, sea ice seems to be an important feeding ground for this spe-
cies as well. Huge shoals of several thousand individuals have been observed
feeding under the fast ice west off the Antarctic Peninsula (Daniels, 1982).
The sea ice region is apparently also the spawning ground (La Mesa and East-
man, 2012) as the pelagic eggs were found floating under the sea ice (Vacchi
et al., 2004). The reproductive cycle of P. antarcticum seems to be closely
coupled to seasonal sea ice dynamics, and early stages depend on the tem-
poral and spatial match with the seasonal zooplankton production (La
Mesa and Eastman, 2012; La Mesa et al., 2010). The hatching period of
P. borchgrevinki seems to be less strongly coupled to production peaks
(Pankhurst, 1990), but both species are expected to be significantly
affected by alterations in seasonal sea ice dynamics by loss of habitat/
refuge and spawning ground and alterations at the base of the food web.
6.2. The impact of increased iceberg scouring

6.2.1 The role of habitat structure and disturbance events for species
richness
For freshwater habitats (lakes and rivers) as well as for marine habitats, such as
coral reefs and hard-substrate environments in the Mediterranean, a high di-
versity in habitat structures often promotes high species richness in the as-
sociated fish communities (Feld et al., 2011; Garcia and Ruzafa, 1998;
Gratwicke and Speight, 2005; Guégan et al., 1998; Öhman and
Rajasuriya, 1998). The benthic communities of the eastern Weddell Sea
shelf in water depths between 200 and 450 m are characterized by a
patchwork of structurally different successional stages; the two extremes
are areas with a diverse epifauna forming the rich 3-dimensional habitat
(Fig. 8A) on the one hand and desert-like areas with nearly no epibenthic
fauna (Fig. 8B) on the other. This patchwork is the result of mechanical
disturbance events by grounding icebergs, calving from the shelf ice and
grounding at water depths between 200 and 500 m. This kind of
Figure 8 (A) Typical undisturbed site with a rich 3-dimensional habitat and Trematomus
cf. eulepidotus hiding inside a large sponge; (B) Fresh iceberg scour habitat without any
3-dimensional megafauna species, only with a pycnogonid, some ophiuroids and Pri-
onodraco evansii. Photos: ©Julian Gutt, AWI Bremerhaven.
disturbance by ice is a common phenomenon in polar regions and affects the

sea floor up to a maximum water depth of 550 m (Conlan and Kvitek, 2005;
Conlan et al., 1998; Gutt, 2001). Beside forest fires and hurricanes, iceberg
scouring is one of the most significant natural physical perturbations imposed
on ecosystems (Garwood et al., 1979; Gutt and Starmans, 2001; Peck et al.,
1999) and is considered to be one of the strongest physical forces structuring
the benthic environment in polar regions (Gutt and Piepenburg, 2003).
In the area of Austasen and Kapp Norvegia (eastern Weddell Sea), about
7% of the coastal zone (<400 m) is covered by iceberg aggregations (Fig. 9;
Knust et al., 2003). Gutt and Starmans (2001) analyzed video and photo ma-
terial from this area and calculated that 42–70% of the sea bed is affected by
iceberg scouring (Fig. 10). Depending on sea floor morphology, nearly
10–40% of the area showed young scour marks or early recolonization
stages. On a smaller (local) scale, these iceberg disturbances completely de-
stroy most of the in- and epifauna. However, on a regional scale, the sea floor
destruction by icebergs creates new space for pioneer species that are special-
ized in recolonization (Gerdes et al., 2008; Teixidó et al., 2004), and the
patchwork of structurally different successional stages increases the overall
gamma diversity (Gray, 2000). Following the Intermediate Disturbance
Hypothesis, which predicts a high diversity caused by intermediate levels
of disturbance (Huston, 1979), Gutt and Piepenburg (2003) calculated an
increased species diversity for the epibenthic megafauna on a regional
scale (1–100 km) due to iceberg disturbances.
However, iceberg scouring not only affects benthic organisms, but also
the demersal fish fauna, the composition of which differs significantly
-70°20¢
2000 m
2500 m
1500 m
1 -70°40¢
Antarctica 1000 m
400 m
Weddell Sea
200 m
2 -71°00¢
Austasen
-71°20¢S
5 Kapp Norvegia
4
7 6 Shelf ice
-14° -13° -12° -11° -10° W
Iceberg aggregation
1 : 29.0 ⫻ 11.5 km = 334 km2

2 : 10.4 ⫻ 4.6 km = 48 km2
3 : 12.3 ⫻ 3.9 km = 48 km2
4 : 41.8 ⫻ 14.4 km = 602 km2
5 : 12.5 ⫻ 4.2 km = 53 km2
6 : 7.2 ⫻ 5.9 km = 43 km2
7 : 16.0 ⫻ 10.1 km = 162 km2
Figure 9 Iceberg aggregations on the high Antarctic shelf off Austasen and Kapp
Norvegia (eastern Weddell Sea) in March 2000 (redrawn from Knust et al., 2003; with per-
mission from Backhuys Publishers).
between undisturbed and recently disturbed sites, with higher species rich-
ness and a higher diversity (Shannon’s diversity) in undisturbed areas, and
in species identity (Fig. 11; Knust et al., 2003). Some species, such as
Trematomus scotti, C. antarcticus, Pagetopsis maculatus and Artedidraco
loennbergi, are typical members of the fish community in undisturbed areas,
while T. pennellii, Trematomus nicolai and Prionodraco evansii are specialized
to live at disturbed sites. Iceberg disturbance events play a key role in small-
scale niche separation of fishes, as the structurally different habitats allow
for the coexistence of trophically similar species (Brenner et al., 2001;
Hagen et al., 2012; Ptacnik et al., 2010).
Level Small Large

plateau iceberg iceberg
banks bank
100
Undisturbed
80
Uncertain status
Area %
60 Intermediate recolonization
40 Early recolonization
Young scour mark

20
Areas analyzed
130 322 88 No.
12.3 21.2 16.5 Transect length (km)
Figure 10 Proportions of different recolonization stages at different morphological

condition in the shelf area off Austasen and Kapp Norvegia (eastern Weddell Sea) (red-
rawn from Knust et al., 2003, based on data from Gutt and Starmans, 2001; with permission
from Backhuys).
In view of climate change, the major questions are (i) whether the pat-
tern of increased diversity at intermediate disturbance levels found for ben-
thic megafauna (e.g. Gutt and Piepenburg, 2003; see above) does also hold
true for the demersal fish community and (ii) how diversity and commu-
nity structure will respond to increased disturbance events. To answer
these questions, we analyzed the relationship between the level of distur-
bance events and the gamma diversity of the demersal fish fauna on the
eastern Weddell Sea shelf using a simple simulation model.
6.2.2 The disturbance simulation model

The calculations of the model are based on abundance data from several
bottom trawls (standard otter trawl, 20-mm mesh in codend) taken in
undisturbed and disturbed areas off Austasen and Kapp Norvegia (eastern
Weddell Sea) during four expeditions between 1996 and 2004. The posi-
tion of iceberg scours was identified by side scan sonar, ROV underwater
video and underwater photography. The composition of invertebrate by-
catches of the otter trawls was used as an indicator for the degree of dis-
turbance. In particular, the presence/absence of large, old hexactinellid
sponges indicated the disturbance level of the sea floor (Gerdes et al.,
Figure 11 Mean abundance (N/1000 m2) of the dominating fish species in undisturbed
areas and on young iceberg scours (recalculated with data from Knust et al., 2003;
R. Knust and K. Mintenbeck, unpublished data). For both communities, average number
of species (S), average Shannon diversity (H0 ) and average evenness (E) are given.
2008; Knust et al., 2003). Overall 30 stations were sampled, 22 in

undisturbed areas and 8 in disturbed areas. Fish abundance data were
calculated based on 1000 m2 swept area.
To simulate different disturbance levels, the abundance data of each catch
from disturbed and undisturbed areas were randomly combined in a 200 sta-
tion matrix by a Monte Carlo simulation. To simulate a completely
undisturbed situation (disturbance level 0.0), data from exclusively
undisturbed stations were randomly combined. The disturbance level 1.0
(the entire shelf is disturbed) was simulated by a random combination of
catches from exclusively disturbed areas. For a disturbance level of 0.05
(5% of the shelf area is disturbed by iceberg scouring), 5% of the 200 stations
in the matrix were filled with abundance data from disturbed stations and 95%
were filled with abundance data from undisturbed station. The stations were
randomly selected. The disturbance level was increased in 0.05 steps. For each
disturbance level, 100 iterations of random combination were computed.
For each disturbance level, the averages of total number of species (S),
gamma diversity (Shannon’s diversity, H0 ) and evenness (Pielou, E) were
calculated:
X
S
H0 ¼ pi
lnðpi Þ ½3
i¼1
where pi ¼ ni/N, with ni is the abundance of species i and N the sum of all
individuals;
H0
E¼ 0
½4
H max
where H0 max ¼ log2(S). To avoid an oversized effect of very rare species
on the total number of species, only species with an abundance of
>0.001 individuals per 1000 m2 were taken into account for each
combination.
The results of the Monte Carlo simulation are shown in Fig. 12. The
results of the different catch combinations were fitted to a univariate,
second-order polynomial (solid line), the dots represent the particular results
of each combination. All three parameters increased with increasing distur-
bance level up to a maximum between disturbance values of 0.25–0.40, rep-
resenting 25–40% of the shelf area disturbed by icebergs. Average species
richness was highest (57.9 species) at a disturbance level of 0.25, average
gamma diversity was highest (H0 ¼ 2.80) at a level of 0.34 and average even-
ness (0.69) was highest at a disturbance level of 0.40.
The comparison of these results with the estimated disturbance level on
the shelf of the eastern Weddell Sea (Gutt and Starmans, 2001; see above)
shows that the fish fauna on the eastern Weddell Sea shelf is obviously well
adapted to this kind of mechanical disturbances and to the average level of
disturbance occurrence there. The gamma diversity (and evenness) of the
fish fauna is highest at the disturbance level we find nowadays, but rapidly
decreases at higher levels according to the model predictions. Future climate
scenarios suggest an increasing rate of iceberg calving in the shelf ice areas of
Antarctica, with an enhanced risk of iceberg groundings and an increasing
disturbance level in the benthic communities.
Such a reduction in habitat structure and heterogeneity means on the one
hand a reduction of habitat and refuge for demersal fishes (e.g. Moreno et al.,
Figure 12 Results of the Monte Carlo simulation: total number of species, gamma
diversity (H0 ) and evenness (E) of the demersal fish community depending on distur-
bance rates. The calculations are based on fish abundance data from disturbed and
undisturbed areas on the eastern Weddell Sea shelf (R. Knust and K. Mintenbeck
unpublished data).
1982), with an increased predation risk for all developmental stages. On the
other hand, a reduction in habitat diversity will result in an increased com-
petition among species with overlapping trophic niches, which at the pre-
sent disturbance level perfectly avoid competition by small-scale niche
separation (Brenner et al., 2001). If the disturbance level increases in the fu-
ture, a loss in species diversity seems to be inevitable.
7. DISCUSSION
7.1. The impact of climate change on Antarctic fish
species
Notothenioid fishes are well adapted to their habitat, and alterations in the
abiotic environment directly affect physiological functions. Increasing water
temperatures, particularly in combination with ocean acidification, pose a
major thread to the persistence of notothenioid fishes. Some species such
as P. borchgrevinki and Notothenia spp. show some physiological plasticity
and are able to compensate for increasing oxygen demand, for example,
by mitochondrial proliferation and/or increased haematocrit. However,
these compensatory mechanisms are limited and most notothenioid species
are in fact stenothermal and are not capable to adjust metabolic functioning.
Channichthyids are highly vulnerable to changes in the abiotic environment
as they lack any capacity to adjust blood parameters to an increasing oxygen
demand. Early developmental stages as well seem to be highly vulnerable to
all kinds of abiotic alterations, including salinity.
General vulnerability to changes in food web structure and dynamics was
analyzed using a conceptual approach, with a quantitative measure (VI) that
served as an indicator of the risk of consumer species to be negatively affected
by such changes. Relative trophic vulnerability was found to be low in all fish
species that include a certain proportion of benthic organisms in their diet.
Obviously, feeding on benthos goes along with a high degree of trophic gene-
ralism and, hence, with a certain capability to adapt food choice to prey avail-
ability and to dampen bottom-up effects. Plankton consumers displayed a
distinctly higher vulnerability, as these species tend to specialize on a compar-
atively narrow prey spectrum, which makes them more sensitive to changes in
prey availability. Thus, there exists an accumulation of risk in the trophic
group of plankton feeders, making this part of the food web particularly sen-
sitive to change. Highest trophic vulnerability was found in channichthyids,
such as C. myersi, C. antarcticus and P. maculatus, which are all specialized on
very few prey items, and in the nototheniid P. antarcticum, which not only has a
narrow food spectrum but is additionally exploited by a multitude of preda-

tors. Relative trophic vulnerability of plankton-feeding larvae and early juve-
niles is expected to be very high, as well.
Trophic vulnerability to shifts in prey size was investigated in two fish spe-
cies, N. coriiceps and N. rossii. In the two species studied, feeding efficiency and
prey detection capability were found to strongly depend upon prey size, with a
complete detection failure (or ignorance) of smallest prey. However, the gen-
eral susceptibility to prey size shifts might differ among species and age/size
classes. As large fish species/individuals usually have a larger size range of avail-
able prey than small species/specimens, large fish are expected to be less sus-
ceptible to shifts in prey size compared with small fish. Trophic vulnerability
to shifts in energy content is likely similar for most fish species. Nutritive value
varies strongly among taxonomic groups, with lowest energy contents found
in gelatinous zooplankton. Salps with their guts filled with fresh phytoplank-
ton are a valuable food source for some Antarctic benthic suspension feeders,
which usually depend on more or less degraded POM (Gili et al., 2006). Nev-
ertheless, in comparison with other zooplankton species such as decapods,
euphausiaceans and copepods, their nutritive value for fishes is extremely
low. Prey of inappropriate size and/or quality affects the nutritional status
and condition of fishes (see also Beaugrand et al., 2003; Koubbi et al.,
2007; Malzahn et al., 2007), and in the worst case even survival.
The loss of habitat poses a threat to the majority of Antarctic fish species.
There is no doubt that a reduction in sea ice extent and duration due to
climate-driven warming will particular affect the life stages of those fish
species that are strongly associated with sea ice, namely P. borchgrevinki
and P. antarcticum. Habitat structure and heterogeneity are of particular im-
portance for the demersal fish community because their loss would imply a
loss of refuge and shelter for juveniles, adults and eggs (see Barrera-Oro and
Casaux, 1990; Moreno, 1980; Moreno et al., 1982), with the consequent
increase in competition among trophically similar species (e.g. Brenner
et al., 2001). Model simulations based on abundance data indicated that
an increase in ice scouring will lead to a steep decrease in diversity and
evenness, and to the loss of species.
7.2. Effects of climate change in other marine systems

In general, the changes detected so far in the South Polar Sea resemble many
of those observed on a worldwide scale. The world’s oceans are warming,
atmospherical pCO2 is rising, leading to potential ocean acidification
(IPCC, 2007), and seawater salinity is decreasing in the vicinity of melting

ice and glaciers (e.g. Curry and Mauritzen, 2005). Fishes, for example, in
temperate regions, have been shown to be significantly affected at the phys-
iological level, in particular by increasing water temperatures, resulting in
reduced growth performance, recruitment and abundance (e.g. Pörtner
and Knust, 2007; Pörtner et al., 2008; Sirabella et al., 2001). In response
to such environmental alterations, several fish species have already shifted
their distributional ranges and have migrated into waters with more
favourable conditions (Dulvy et al., 2008; Perry et al., 2005).
The risk of habitat loss and alteration of habitat structure and heteroge-
neity due to sea ice retreat (Stroeve et al., 2007) and increasing occurrence of
iceberg scouring events (Conlan et al., 1998; Gutt et al., 1996) is comparable
in the Arctic Ocean. Invasion by lithodids as observed west of the Antarctic
Peninsula is also found in the northern hemisphere. The most popular
example is the red king crab (Paralithodes camtschaticus), which was
introduced into the Barents Sea and subsequently invaded Norwegian
waters. In the presence of these invaders, benthic biomass and diversity is
drastically reduced; these crabs thus remove potential prey for benthos
feeding fish species and even prey upon fish eggs (reviewed in Falk-
Petersen et al., 2011).
Alterations in plankton community composition due to climate forcing
are common in many ecosystems and often include a shift from larger to
smaller phytoplankton (Yvon-Durocher et al., 2011) and zooplankton spe-
cies, in particular in copepods (e.g. in the North Sea, Beaugrand et al., 2003;
Helaouët and Beaugrand, 2007; and in the Humboldt Current ecosystem
reviewed in Alheit and Niquen, 2004). Substantial increases in gelatinous
zooplankton have been observed in different marine systems in recent
years (e.g. Attril et al., 2007; Brodeur et al., 1999; Purcell, 2005). High
abundances of gelatinous zooplankton are often related to water
temperature and salinity, suggesting that population density of gelatinous
zooplankton will further increase under future climate change scenarios
(reviewed in Purcell, 2005). In the central North Sea, the occurrence of
jellyfish was also negatively correlated with seawater pH, thus, future
levels of CO2 may synergistically promote the presence of gelatinous
zooplankton (Attril et al., 2007). Gelatinous zooplankton prey upon fish
eggs and larvae (Doyle et al., 2008; Purcell, 1985) and also represent
strong competitors for plankton-feeding fish by efficiently removing
potential prey, such as copepods (Purcell and Decker, 2005) or
euphausiids (Suchman et al., 2008). Some gelatinous zooplankton such as
salps or ctenophores are occasionally consumed by fishes (including

notothenioids), but appear to be a form of ‘survival food’ when preferred
zooplankton prey are not abundant (Kashkina, 1986; Mianzan et al., 2001).
Taking a closer look at the effects of climatic shifts in the world’s oceans,
an intriguing pattern seems to emerge: the most severe (or most rapid) effects
of climate forcing on marine biota appear to be found within pelagic com-
munities (Alheit, 2009; Alheit and Niquen, 2004; Alheit et al., 2005; Arntz,
1986; Beaugrand et al., 2003; Benson and Trites, 2002). These observed
changes in the pelagic realm are not restricted to one or two trophic
levels, or to specific species, but usually involve strong alterations in food
web structure and ecosystem functioning and dynamics. In the central
Baltic and the North Sea (Alheit et al., 2005; Beaugrand et al., 2003), in
the Bering Sea and the North Pacific (Benson and Trites, 2002) as well as
in the Humboldt Current ecosystem (Alheit and Niquen, 2004; Arntz,
1986; Arntz and Fahrbach, 1991), all trophic levels in the pelagial, from
primary producers to apex predators, were affected by direct and/or
indirect climate forcing. In particular, pelagic fishes with short plankton-
based food chains, such as clupeids, may undergo strong fluctuations in
stock density (Alheit and Niquen, 2004), with severe consequences
for their endothermic consumers (e.g. Alheit, 2009; Arntz, 1986; Cury
et al., 2000).
To our knowledge, there are no reports on such extensive severe effects
of climatic shifts on benthic biota, suggesting that they are less affected, but
whether this is really a common pattern or just due to a greater focus on the
pelagic realm still needs to be verified.
Overall, the general effects of climate forcing and the potential direct and
indirect impact on marine living communities thus appear to be similar in
the South Polar Sea compared with marine systems worldwide. Neverthe-
less, there are some significant differences: (i) fishes inhabiting temperate and
tropical regions often have the opportunity to emigrate into waters with
more favourable abiotic and biotic (prey) conditions (see Arntz, 1986;
Dulvy et al., 2008; Perry et al., 2005). For notothenioid fishes,
particularly for high Antarctic species, emigration is strongly limited by
stenothermy and the lack of alternative habitats, as they are already living
at the highest latitudes. (ii) Fish species such as clupeids in upwelling
systems are evolutionarily adapted to strong environmental fluctuations
by possessing traits associated with fast growth (Cubillos et al., 2002) and
high fecundity (Alheit and Alegre, 1986), both facilitating population
recovery after stock decline. In tropical reef fish, a rapid transgenerational
acclimation to increasing water temperatures has also been observed

(Donelsen et al., 2012). In contrast, notothenioid fish species are
characterized by slow development rates and low fecundity, and their
recovery potential is thus strongly limited. Due to the low recovery
capacity, even a modest increase in the amplitude of interannual climate
fluctuations could affect long-term population dynamics of notothenioid
fish, with ramifications that would ripple through the wider food web.
Given the rate of alterations due to climate change observed off the
Antarctic Peninsula and fish species’ life history characteristics, an
evolutionary adaptation of notothenioid fishes that keeps pace with the
rate of change in conditions is unlikely, if not impossible (see Somero, 2010).
7.3. Antarctic fish community persistence—Winners and losers

Given the current state of knowledge, it is unlikely that there will be any true
‘winners’ of climate change among notothenioid fish species. There will be
only ‘survivors’ and many ‘losers’. P. borchgrevinki, for example, might be
among the survivors in a changing South Polar Sea as this species is charac-
terized by relatively high metabolic plasticity and a wide thermal tolerance
window (Robinson and Davison, 2008), and low trophic vulnerability. But
still, P. borchgrevinki is threatened by habitat reduction owing to retreat of sea
ice and so far it is unknown whether this species can cope with loss of its ice
habitat. Demersal fish species (except for plankton-feeding channichthyids)
show low relative trophic vulnerability, but will be significantly affected by
the loss of habitat structure and diversity. Which species will ultimately sur-
vive and which will not in the long run depends on a combination of
species-specific physiological and trophical plasticity, and population dy-
namics, in addition to higher-level food web effects. Trophic plasticity is ap-
parently high in benthos feeders, but acclimation capacity seems to differ
strongly among species: some, such as N. rossii, possess partially compensa-
tory mechanisms (A. Strobel and F.C. Mark, unpublished data), whereas
the potential for acclimation is apparently low for many others (e.g. high
Antarctic Trematomus spp.; Robinson, 2008). However, which demersal
species exactly will be lost due to habitat loss on the high Antarctic shelf
remains unknown for now. Population dynamic parameters such as relative
fecundity and growth rate are rather similar among most demersal high
Antarctic notothenioids (e.g. Kock and Kellermann, 1991; La Mesa and
Vacchi, 2001), but much more work is needed on the effects that
changes in the abiotic environment exert on population dynamics.
Icefishes, however, are one group that will almost certainly be on the
losing side in a warming South Polar Sea with increasing levels of CO2,
as the oxygen-carrying capacity of their blood is limited, and there is no po-
tential for physiological acclimation to satisfy the increasing tissue oxygen
demand. Moreover, many channichtyids, such as C. myersi, are specialist
consumers with a high relative trophic vulnerability, making this group ad-
ditionally susceptible to changes in food web structure and dynamics. An-
other potential ‘loser’ which is affected by direct and indirect effects of
climate change is the currently dominant pelagic species, P. antarcticum,
which will be most likely affected by sea ice reduction. It also seems to
be highly vulnerable to alterations in the food web, and indirect evidence
suggests that at least larvae and juveniles are highly vulnerable to abiotic
changes. Theoretically, all fish species are threatened by a shift in prey size
structure and a decrease in prey nutritive value. However, the pelagic realm
in the South Polar Sea (and elsewhere) will likely be among the first to react
to climate fluctuations, and the shifts in question have thus so far only been
observed in the plankton community. Plankton consumers are, therefore,
especially vulnerable. Shifts in size distribution from large to small phyto-
plankton organisms in the marine Antarctic (as observed west off the Ant-
arctic Peninsula; Moline et al., 2004) will thus most likely favour the
prevalence of small zooplankton species, such as cyclopoid copepods (as ob-
served in other marine systems). Given the size dependency of prey detec-
tion and feeding efficiency in notothenioid fish, it is questionable whether
plankton consumers such as P. antarcticum but also icefish can cope with such
a prey size shift. Feeding on low quality ‘survival food’ such as salps is not a
suitable alternative to energy-rich crustaceous zooplankton in the long run.
In particular, at the edge of their thermal tolerance window, fish species will
be highly sensitive to such additional stressors.
However, the major bottleneck for the persistence of most (if not all)
species’ populations is most likely the survival of early developmental stages.
Eggs and larvae appear particularly sensitive to alterations in the abiotic en-
vironment, some might be affected by sea ice reduction (e.g. early stages of
P. antarcticum), and larvae and juveniles are apparently vulnerable to indirect
food-web-mediated effects of climate change. For non-Antarctic pelagic
larval fish, three key parameters were identified: prey abundance, prey type
and seasonal timing (Beaugrand et al., 2003). Shifts in any of these three pa-
rameters might significantly compromise larval condition and survival. Most
notothenioid larvae depend on seasonal timing as well (Efremenko, 1983; La
Mesa and Eastman, 2012; La Mesa et al., 2010), and the capacity to avoid a
mismatch depends on species’ plasticity in their reproductive cycle. In some

species, a certain plasticity to adapt the reproductive cycle might exist, as
indicated by differences in spawning time among populations in different
locations (see Kock and Kellermann, 1991), but it is unknown whether
all species are able to adapt their reproductive cycle and by which factors
the timing is triggered. Without offspring sustaining the stocks,
populations will progressively age and density will inexorably decline.
So far, our knowledge on species-specific vulnerability, potential plastic-
ity, and acclimation and/or adaptation potential is still limited. However,
based on what we already know from the Antarctic and from what we
can observe in other systems, we can at least identify some potential bottle-
necks. Nevertheless, there is an urgent need for more experimental studies
on a broad range of species to gain a cause-and-effect understanding of the
consequences of the potentially complex interactions between abiotic and
biotic mechanisms (Woodward et al., 2010a).
7.4. Consequences of fish species loss for the marine Antarctic

ecosystem
Fishes of the South Polar Sea will be affected by climate change in multiple
ways, with the potential vulnerability and mechanisms differing among spe-
cies, developmental stages and habitats. What we know about the effects of
climate change and the vulnerability of Antarctic fish species leaves little
doubt that the population density of many species will decline and some spe-
cies will go extinct in the long run. The resilience of the entire system, that
is, to what extent the decline or extinction of particular notothenioid fish
species from the system impacts overall food web stability and ecosystem
functioning, depends strongly on the species’ functional role and the sys-
tems’ ability to absorb for the loss by compensatory mechanisms among
co-occurring species (Johnson, 2000; Naeem, 1998).
In the South Polar Sea, demersal fish communities are characterized by
relatively high species richness in comparison with the very limited diversity
of the pelagic ichthyofauna. The majority of demersal fish species are oppor-
tunistic generalist consumers with high trophic niche overlap, indicating a
high functional redundancy. It is therefore likely that within the demersal
community, the decline or loss of some species can be compensated for
by others. However, the model on the impact of disturbance events on de-
mersal fish communities indicated not only a future decrease in species num-
ber but also in evenness. Thus, one or a few species might become extremely
dominant, and the impact of such an alteration in community composition
on overall ecosystem functioning ultimately depends on a species’ identity,

its specific traits and its potential to serve as valuable prey for top predators.
As the role of demersal fish as a food source for endothermic predators is
more important in inshore compared to offshore areas (Barrera-Oro,
2002), the effects of alterations in the demersal community on fish con-
sumers might be stronger in shallow coastal zones. In inshore waters of
the South Shetland Islands, for example, N. coriiceps proliferated and became
the dominant demersal fish species after the stocks of the demersal N. rossii
and G. gibberifrons were drastically diminished in the early 1980s due to an-
thropogenic actions (Barrera-Oro et al., 2000; see Section 7.5 below). Si-
multaneously, the breeding populations of one of their most important
consumers in this area, the Antarctic shag Phalacrocorax bransfieldensis, now
mainly preying upon N. coriiceps, steadily declined. Thus, though N. coriiceps
is similar to N. rossii and G. gibberifrons in terms of ecology and body size, it
could apparently not fully compensate for the reduction of the two fish spe-
cies within the food web (Casaux and Barrera-Oro, 2006).
The extent to which the loss of channichthyids such as C. myersi or
C. antarcticus can be compensated by other fish species is not clear.
Channichthyids feed almost exclusively on krill and fish (reviewed in
Hureau, 1994; Kock, 2005a; La Mesa et al., 2004). While a multitude of
other fish species also feed on krill, true piscivores are rare among other
notothenioids (e.g. Hureau, 1994). Some species occasionally feed on fish
(see Fig. 5; La Mesa et al., 2004) but to a much lesser extent compared to
channichthyids. Hence, the loss of channichthyids from the system might
release some fish populations from top-down control. Though icefish are
an abundant component in Antarctic fish communities, they seem to be
of minor importance in the diet of endothermic predators, but their
importance increases regionally when other prey, such as krill, is scarce
(Kock, 2005a,b and references therein). Compared with most other
notothenioids, adult channichthyid fishes are large and show only weak
escape responses (authors’ personal observation from ROV videos),
making them an easy-to-catch prey for large consumers. At our current
state of knowledge, we can only speculate, but it is likely that the loss of
channichthyids will have detrimental effects on many components of the
Antarctic marine food web.
The pelagic fish community is composed of very few species only, and
the whole community is dominated by a single fish species, P. antarcticum (see
above), which on the high Antarctic shelf seems to occupy a similar ecolog-
ical key role in the food web as Antarctic krill in the seasonal sea ice zone
(Hubold, 1992; Hureau, 1994; La Mesa et al., 2004; Takahashi and Nemoto,
1984). It is one of the principal consumers of zooplankton, and all
developmental stages are among the most important food sources for a
multitude of predators, in particular for endotherms inhabiting Antarctic
shelf areas (e.g. Daneri and Carlini, 2002; Hureau, 1994; La Mesa et al.,
2004; Plötz, 1986). This pelagic fish species occurs in loose shoals
(Eastman, 1985a; Fuiman et al., 2002) and undertakes nocturnal
migrations into upper water layers (K. Mintenbeck and R. Knust,
unpublished data; Plötz et al., 2001), where it provides a rich and easily
accessible food source. It is thus of critical importance in the Antarctic
marine food web. No other species, neither other pelagic notothenioids
nor invertebrates (e.g. squid or krill), may be able to provide full
functional compensation in the case of its extinction or reduction of the
stock, in particular because none combines a pelagic shoaling life style
and vertical migration with a comparable size spectrum and energy
content (see e.g. Ainley et al., 2003). In its appearance (Fig. 13) and life
style, as well as in its central role in a relatively simply structured and
highly productive pelagic system, P. antarcticum strongly resembles
shoaling clupeid fishes in upwelling systems (see Section 7.2 above).
Figure 13 Catch of Pleuragramma antarcticum in the eastern Weddell Sea (Photo by

J. Plötz, AWI Bremerhaven).
In the eastern South Pacific, for example, El Niño events involve strong
reductions in stocks of anchovy and sardine (owing to direct and indirect
climate forcing in combination with fisheries effects), causing starvation
and mortality in the very top predators, birds and seals (e.g. Arntz, 1986).
But life history traits of clupeids and the nototheniid P. antarcticum (see
Table 4) and recovery potential differ significantly: population doubling
time was estimated to be often less than 15 months in clupeid fish
species and 5–14 years in P. antarcticum (Froese et al., 2002), making
populations of the latter extremely vulnerable to any kind of disturbance
or systemic shifts.
Nevertheless, seals and penguins do not depend exclusively on pelagic
prey but also prey upon demersal fishes (e.g. Casaux et al., 2006; Coria
et al., 2000; Plötz et al., 1991). In many high Antarctic shelf areas,
exploitation of this resource requires deep diving. Though Weddell seal
and Emperor penguin are both excellent divers (Burns and Kooyman,
2001; Wienecke et al., 2007), exploitation of fishes at great depth is
energetically disadvantageous for these air-breathing endothermic
predators as it involves an increased swimming effort, shorter times at
feeding depth, and/or longer dives followed by longer recovery phases
(Kooyman, 1989; Kooyman and Kooyman, 1995; Wilson and Quintana,
2004). Moreover, foraging efficiency is higher in shallow dives (Croxall
et al., 1985), while encounter rates are probably lower in light-depleted
deep waters, as indicated by a lower number of feeding events at depth
(see Liebsch et al., 2007; Plötz et al., 2005). Hence, declining stocks or
complete loss of P. antarcticum will in either case severely affect the top
predators in the Antarctic marine ecosystem.
Table 4 Life history traits of clupeid fishes (sardines and anchovies) and the nototheniid
P. antarcticum
Clupeids Pleuragramma antarcticum
Von Bertalanffy growth constant K 0.5–0.83 0.05–0.075
Age at first spawning (years) 1–1.52,8 7–97
Relative fecundity (eggs g 1 wet weight) 550–6001 70–1604
Duration of larval phase (days) 37–746 180–3655
Data sources are indicated by superscripts: 1Alheit and Alegre (1986), 2Cubillos and Claramunt (2009),
3
Cubillos et al. (2002), 4Gerasimchuk (1988), 5Hubold and Tomo (1989), 6Houde and Zastrow (1993),
7
Kock and Kellermann (1991) and 8Whitehead (1985).
What are the future perspectives for Antarctic fish communities? There is
no doubt that fishes still will be an important and abundant component of
the Antarctic marine ecosystem in the future, but the composition of com-
munities will change significantly in the long run. It is likely that, with an
ongoing warming trend, Sub-Antarctic demersal fish species such as
Notothenia spp. (but also non-notothenioids) will move southwards into high
Antarctic shelf areas, taking over the role of extinct or declining species in
the present-day food web. Possible future scenarios for the pelagic commu-
nity are the occupation of the ‘small pelagic zooplankton feeder’ niche by
myctophid fishes or by clupeids such as the Falkland sprat, Sprattus fuegensis.
Whether myctophids or clupeids can effectively replace P. antarcticum in its
functional role in the food web, however, remains to be seen.
7.5. Final thoughts—Is climate change exclusively to blame?

Though our knowledge is steadily improving, we are in fact just starting to
comprehend the structure, dynamics and functioning of the Antarctic ma-
rine ecosystem, while the system apparently has already started to respond to
climate change. This, however, is not the only threat to marine living
communities in the South Polar Sea, and human activities have already
caused significant alterations in the past and still affect Antarctic communities
today. Commercial fisheries in the Antarctic started in the late 1960s/early
1970s (see Kock et al., 2007 for review), and the destructive impact of bot-
tom trawling on benthic communities is comparable to the impact of iceberg
scouring (discussed in Barnes and Conlan, 2007). Commercial sealing and
whaling activities in the South Polar Sea in the nineteenth and twentieth
centuries (see Kock, 2007; Laws, 1977) resulted in large-scale and long-
term alterations of food web structure and population dynamics of prey
and competitors (Ainley et al., 2007, 2010; Laws, 1985). Industrial
exploitation of Antarctic fish species (and krill) between the 1970s and
1990s resulted in dramatic stock decreases and rapid overexploitation of
some species (reviewed in Ainley and Blight, 2008; Kock, 1992, 2007).
Since 1982, the fisheries are regulated by CCAMLR (Commission for
the Conservation of Antarctic Marine Living Resources), and many were
closed between 1985 and 1990 due to overexploitation (Ainley and
Blight, 2008; Kock et al., 2007). Nevertheless (to provide some examples
only), regular monitoring of the stocks of many commercially exploited fish

species, such as N. rossii and G. gibberifrons, around the South Shetland
Islands, indicates a lack of recovery more than three decades after the end
of fisheries (Barrera-Oro and Marschoff, 2007; Barrera-Oro et al., 2000).
Similarly, stocks of the channichthyid C. gunnari in the Indian Ocean did
not recover to pre-exploitation levels after the fishery had ceased for
many years (Kock, 2005b). One reason for the slow stock recovery may
be the low fecundity and slow development (see Section 3.3.2 above) of
many species. However, two additional factors that may adversely affect
stock recovery of C. gunnari were proposed (Kock, 2005b and references
therein): (i) an increase in top-down pressure, that is, increased predation
by seals owing to fluctuations in alternative prey (krill) and (ii) possible
direct effects of climate change, in particular increasing water
temperature. Owing to strict regulation, the numbers of some whale
species seem to be increasing again in the South Polar Sea (Branch, 2006,
2007), which is on the one hand desirable, but on the other hand might
entail an additional increased top-down pressure on zooplankton and fish
communities.
These examples emphasize the complexity of relationships among hu-
man activities (historic and current), abiotic climate forcing and altered
trophic structure, and how these factors can interact to control fish
populations in the South Polar Sea. Thus, multiple drivers act synergisti-
cally to affect a particularly sensitive ecosystem, and projecting the future
trajectories of fish stocks is particularly challenging, but we are better
placed than ever before to start to anticipate and respond to likely scenarios
of future change.
ACKNOWLEDGEMENTS
We thank the crew and officers of RV Polarstern for professional support in fisheries during
several expeditions, and Tomas Lundälv and Julian Gutt for providing the underwater
photographs. We are deeply grateful to Carlos Bellisio, Lena Rath, Luis Vila, Nils
Koschnick, Oscar González, Timo Hirse and Tina Sandersfeld for their help in field
activities, in the lab and in experimental work. We appreciate the reviewers’ efforts and
comments that helped to improve the manuscript. The work of K. M. and A. S. was
funded by the German Research Foundation (DFG, SSP 1158; projects MI 1391/1-1 and
PO 273/13-1).
APPENDIX
Table A1 Species names, family and code no. (see Fig. 5) of the species used for the
analysis and comparison of the trophic vulnerability to general changes in food web
structure and dynamics
No. Species name Family SP SC VI TG
1 Aethotaxis mitopteryx Nototheniidae 53 14 0.20 BP
2 Akarotaxis nudiceps Bathydraconidae 79 13 0.09 B
3 Artedidraco loennbergi Artedidraconidae 108 14 0.06 B
4 Artedidraco orianae Artedidraconidae 27 14 0.21 BP
5 Artedidraco shackletoni Artedidraconidae 110 14 0.07 B
6 Artedidraco skottsbergi Artedidraconidae 86 13 0.09 BP
7 Bathydraco marri Bathydraconidae 47 13 0.17 BP
8 Chaenodraco wilsoni Channichthyidae 16 15 0.28 PF
9 Chionobathyscus dewitti Channichthyidae 5 14 0.77 PF
10 Chionodraco hamatus Channichthyidae 10 15 0.67 P
11 Chionodraco myersi Channichthyidae 5 15 0.77 PF
12 Cryodraco antarcticus Channichthyidae 5 15 0.77 PF
13 Cygnodraco mawsoni Bathydraconidae 55 14 0.14 BP
14 Dacodraco hunteri Channichthyidae 37 15 0.10 F
15 Dissostichus mawsoni Nototheniidae 52 21 0.28 BP
16 Dolloidraco longedorsalis Artedidraconidae 142 14 0.04 B
17 Gerlachea australis Bathydraconidae 14 14 0.46 P
18 Gymnodraco acuticeps Bathydraconidae 33 14 0.15 P
19 Histiodraco velifer Artedidraconidae 85 13 0.07 BF
20 Neopagetopsis ionah Channichthyidae 5 14 0.77 PF
21 Pagetopsis macropterus Channichthyidae 43 15 0.10 F
22 Pagetopsis maculatus Channichthyidae 5 15 0.77 PF
23 Pagothenia borchgrevinki Nototheniidae 17 12 0.27 BP
24 Pleuragramma antarcticum Nototheniidae 12 47 0.96 P
25 Pogonophryne marmorata Artedidraconidae 45 14 0.13 BP
Table A1 Species names, family and code no. (see Fig. 5) of the species used for the
analysis and comparison of the trophic vulnerability to general changes in food web
structure and dynamics—cont'd
No. Species name Family SP SC VI TG
26 Pogonophryne permitini Artedidraconidae 79 14 0.10 B
27 Pogonophryne scotti Artedidraconidae 78 14 0.11 B
28 Prionodraco evansii Bathydraconidae 88 14 0.08 BP
29 Racovitzia glacialis Bathydraconidae 89 14 0.08 BP
30 Trematomus bernacchii Nototheniidae 93 14 0.02 B
31 Trematomus eulepidotus Nototheniidae 45 14 0.12 BP
32 Trematomus hansoni Nototheniidae 81 14 0.06 BF
33 Trematomus lepidorhinus Nototheniidae 71 14 0.10 BP
34 Trematomus loennbergii Nototheniidae 105 14 0.05 BF
35 Trematomus nicolai Nototheniidae 88 14 0.09 B
36 Trematomus pennellii Nototheniidae 164 14 0.03 BF
37 Trematomus scotti Nototheniidae 121 14 0.06 B
All species are members of the fish community on the eastern Weddell Sea shelf. Species are listed in
alphabetical order; for authorities,
P please consult Gon and
P Heemstra (1990). For each notothenioid spe-
cies, the number of prey ( P) and consumer species ( C), the relative trophic vulnerability (VI) and
trophic group (TG) are P given. The index of relative vulnerability VI was calculated
P from the weighted
number of prey species ( WP) and weighted number of consumer species ( WC) (see Eq. 2). Data on
trophic links are part of the database published in Jacob et al. (2011). Trophic groups were assigned
according to main food components as shown in Fig. 5, with B, benthos; P, plankton; F, fish.
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A Complete Analytic Theory for
Structure and Dynamics of
Populations and Communities
Spanning Wide Ranges in
Body Size
Axel G. Rossberg*,{,1
*Centre for Environment, Fisheries and Aquaculture Science (Cefas), Lowestoft Laboratory, Suffolk, United
Kingdom
{
Medical Biology Centre, School of Biological Sciences, Queen’s University Belfast, Belfast, United Kingdom
1
Corresponding author: e-mail address: axel.rossberg@cefas.co.uk
Contents
1. Introduction 429
1.1 Orientation on a changing planet 429
1.2 Size spectra 430
1.3 Mathematical size-spectrum models 433
1.4 Approximations 435
1.5 Structure of the paper 437
2. Some Aspects of the Analytic Theory Explained in Non-mathematical Language 437
2.1 Two different scenarios generate power-law community size spectra 437
2.2 Feeding alone couples size classes 440
2.3 Population-level predator–prey size-ratio windows are wide 440
2.4 Simple mass-balance models explain only equilibrium 441
2.5 Both upward and downward cascades form in response to size-specific
perturbations 441
2.6 Trophic cascades form slowly 443
2.7 Depletion of species higher up in the food chain is fast 444
2.8 Food-web structure essentially affects size-spectrum structure and
dynamics 444
2.9 Body mass approximates reproductive value 445
2.10 Physiological mortality is constrained by population dynamic equilibrium 445
2.11 Solutions of “size-spectrum” equations follow general characteristics 446
3. Methods 447
4. Model 448
5. Properties of the Scale-invariant Community Steady State 454
5.1 Discussion of the underlying approximations 454
5.2 Scale-invariant demographics 456

http://dx.doi.org/10.1016/B978-0-12-396992-7.00008-3
428 Axel G. Rossberg
5.3 Scale-free size distribution 458

5.4 Implications of the boundary condition (part I) 459
5.5 Total biomass per size class 461
5.6 Total metabolic loss rate per size class 461
5.7 Implications of the boundary condition (part II) 462
6. Derivation of the Species Size-Spectrum Model 465
6.1 General framework 465
6.2 Operators and eigenfunctions 466
6.3 Reduced dynamics 469
6.4 Food-web effects 477
7. Solution of the Species Size-Spectrum Model 478
7.1 Approximation for times shortly after onset of fishing 478
7.2 Tentative steady-state solution 479
^
7.3 The roles of complex poles and zeros of KðÞ 479
7.4 Analytic approximation of time-dependent size-spectrum dynamics 480
^
7.5 Extension of the method to all zeros of KðÞ 486
8. Comparison of Analytic Theory and Simulations 487
8.1 A specific parametrisation 487
8.2 Simulation technique 490
8.3 Numerical evaluation of the analytic approximation 491
8.4 Case studies 491
9. Implications, Discussion, and Outlook 500
9.1 The final steady state of a perturbed species size spectrum 500
9.2 Distribution of individual sizes in the final steady state 501
9.3 The population-level predator–prey size-ratio window 503
9.4 Slow and fast responses to size-selective fishing 505
9.5 Neutrality and the validity of the QNA 506
9.6 How do power-law size spectra arise? 508
9.7 Comparison with the theory of Andersen and Beyer (2006) 510
9.8 Outlook 511
Appendix. Numerical Study of the Spectrum of the McKendrick–von Foerster
Operator 513
References 515
Abstract
The prediction and management of ecosystem responses to global environmental
change would profit from a clearer understanding of the mechanisms determining
the structure and dynamics of ecological communities. The analytic theory presented
here develops a causally closed picture for the mechanisms controlling community and
population size structure, in particular community size spectra, and their dynamic re-
sponses to perturbations, with emphasis on marine ecosystems. Important implications
are summarised in non-technical form. These include the identification of three different
responses of community size spectra to size-specific pressures (of which one is the
Complete Analytic Theory for Size-Structure and Dynamics 429
classical trophic cascade), an explanation for the observed slow recovery of fish com-
munities from exploitation, and clarification of the mechanism controlling predation
mortality rates. The theory builds on a community model that describes trophic inter-
actions among size-structured populations and explicitly represents the full life cycles of
species. An approximate time-dependent analytic solution of the model is obtained by
coarse graining over maturation body sizes to obtain a simple description of the model
steady state, linearising near the steady state, and then eliminating intraspecific size
structure by means of the quasi-neutral approximation. The result is a convolution equa-
tion for trophic interactions among species of different maturation body sizes, which is
solved analytically using a novel technique based on a multiscale expansion.
1. INTRODUCTION
1.1. Orientation on a changing planet
We have entered a period of rapid, global environmental change, in which
anthropogenic climate change is one important factor (Solomon et al.,
2007), which is complicated by additional drivers such as elevated nutrient
discharge and the direct impacts of overexploitation on natural resources
(Millennium Ecosystem Assessment, 2005). The planet’s ecosystems may
never before have experienced this type of environmental change. Knowing
how they will respond could help us prepare for and, if possible, manage the
consequences of these developments (Woodward et al., 2010a).
Experimental and comparative methods, the dominant modes of scientific
enquiries in ecological research, have obvious limitations when addressing
scenarios of unprecedented environmental change at global or even regional
scales. The relevant temporal and spacial scales are too large to conduct
experiments (O’Gorman et al., 2012), and the data required for direct com-
parative analyses are often simply not yet available (Twomey et al., 2012).
The natural response, therefore, is to resort to models. These models can,
for example, be (i) experimental systems such as microcosms (Reiss et al., 2010)
or mesocosms (Yvon-Durocher et al., 2011), (ii) statistical models to extrap-
olate ecological data to the environmental conditions expected in future,
(iii) numerical models aimed at simulating the relevant aspects of
future scenarios directly, or (iv) analytic models that seek to isolate the impli-
cations of general ecological and biological principles that are sufficiently
fundamental not to be overruled by global change. Common to any such
modelling is the expectation that some aspect of the scenarios one seeks to
predict are sufficiently insensitive to ecological detail that such detail need
not be reproduced in the models (Rossberg, 2007). These robust aspects are
those one can be predicted, for which one can prepare, and which one might
attempt to manage. Those aspects of future system states that do depend on
many details (Friberg et al., 2011), however, might simply be beyond control.
Common to all modelling is the problem of knowing which aspects of future
system states can be predicted and which system details are relevant for this.
A common approach to identifying aspects of complex systems amenable
to modelling is to search for coherent patterns in data. Obviously, if clear pat-
terns arise similarly in data from different systems, the mechanisms generating
these patterns are unlikely to depend on many details (Riede et al., 2010). It
is, therefore, natural for research addressing the large-scale ecological impacts
of global change to concentrate on the major known macroecological
patterns. The patterns at the focus of the present work are those found in
the distributions of the biomasses of individuals or species over wide ranges
in body size. The first step, before addressing specific problems in the face
of global change, is to ask which ecological details are important for generating
these patterns in reality and what the underlying mechanisms are; these will be
the details that any type of model, for example (i)–(iv), would need to capture
to be reliable. Answering these questions is the central aim of the present work.
Technically, this is done by deriving an approximate analytic solution
of a detailed community model. In doing so, determining which approxi-
mations are feasible without much affecting the predicted body-size distri-
butions means understanding which ecological details are unimportant for
the outcome. The resulting, approximate descriptions of community struc-
ture and dynamics encapsulate the mechanisms by which those details that
do matter bring about the dominating patterns and their responses to pres-
sures. Therefore, judiciously applied approximations, rather than meaning
loss of information, actually reveal what is important. This is why the route
along which the approximate solution of the community model is derived is
as important as the outcome. The step-by-step derivation, therefore, forms
the main body of this chapter.
1.2. Size spectra

Much of the early empirical and theoretical work on size distributions related
to plant communities (see Koyama and Kira, 1956). Regularities in size
spectra have now been investigated, for example, for benthic communities
(Duplisea, 2000; Gerlach et al., 1985), terrestrial soil (Mulder and Elser,
2009; Mulder et al., 2008; Reuman et al., 2008), and birds (Thibault
et al., 2011). The most striking form of the phenomenon, however, is
found in pelagic communities. Sheldon et al. (1972) suggested, based on

measurements and literature data, that pelagic biomass is approximately
evenly distributed over the logarithmic body-size axis “from bacteria to
whales”, spanning up to 20 orders of magnitude in body mass. The core
of this conclusion has remained unchallenged, although intensive human
harvesting makes its validation for the largest size classes difficult (Gaedke,
1992b; Jennings and Blanchard, 2004; Sheldon et al., 1977). Over shorter
size ranges, similar phenomena are observed for benthic communities
(Duplisea, 2000; Gerlach et al., 1985) or in terrestrial soil ecosystems
(Mulder and Elser, 2009; Mulder et al., 2008, 2011; Reuman et al., 2008).
The work of Sheldon et al. (1972) drew attention to the usefulness of
characterising community structure through size spectra. In the form they
used, size structure is represented irrespective of species identity, trophic
level, or life-history stage. In a common, though by no means exclusive,
protocol to determine size spectra in aquatic communities, individuals are
assigned to logarithmic size classes by carbon content, for example, . . .,
1–2 pgC, 2–4 pgC, . . . using various optical and mechanical techniques.
The density of biomass in each size class is then determined, for example,
as a value averaged over a full year and a specific range of the water column.
Subsequent investigations revealed deviations from the hypothesis for-
mulated by Sheldon et al. (1972) in the detail (Kerr and Dickie, 2001).
As illustrated in Fig. 1, one often finds approximate power-law relationships
between abundance and body mass as the basic pattern, that is, straight lines
on double-logarithmic plots, with “slopes” (actually exponents) close to but
different from the one corresponding to the Sheldon hypothesis (which is
2, 1, or 0, depending on the specific choices of dependent and indepen-
dent variables; see Blanco et al., 1994). On top of this, size spectra often de-
viate from power laws by exhibiting several maxima (or “domes”) spaced
more or less evenly along the logarithmic body-size axis (see, e.g. Fig. 1,
or Kerr and Dickie, 2001).
The idea that the size distribution of individuals can indicate the “health”
of an ecological community (e.g. Castle et al., 2011; Jennings and Blanchard,
2004; Kerr and Dickie, 2001; Rice et al., 2011; Sheldon et al., 1977) has
recently been inscribed in legal documents. Arguably, the simplest way of
characterising a size distribution is to compare the relative proportions of
biomass in two wide body-size classes. In a series of reports, reviewed by
Greenstreet et al. (2011), the International Council for the Exploration of
the Sea developed, as an indicator for community state, the Large Fish
Indicator (LFI), defined as the proportion among all fish in a community of
100
Biomass dB/dlnm
(gC/m3)
10-3
10-6 -15
10 10-12 10-9 10-6 10-3 100 103
Body mass m (gC)
Figure 1 Five typical planktonic size spectra. Triangles represent data for the highly
eutrophic lake Müggelsee averaged over 3 years, after Gaedke et al. (2004); stairs
represent a seasonal average for Überlingersee, a division of the meso-eutrophic Lake
Constance (Bodensee), after Gaedke (1992b), including an estimate for the contribution
by fish (shaded area); crosses represent yearly averages for Lake Ontario, after Sprules
and Goyke (1994), using a nominal depth of 50 m to convert to volume density; circles with
1 SD error bars represent the oligotrophic waters of the North Pacific Central Gyre averaged
over 3 years of sampling by Rodriguez and Mullin (1986a), where measurements are com-
patible with a perfect power law; squares represent the oligotrophic open waters at a sta-
tion near the Yakutat Seamount in the Northwest Atlantic, after Quiñones et al. (2003). For
further examples, see Boudreau and Dickie (1992), among many others. The density of bio-
mass along the logarithmic size axis dB/d ln m was estimated from the published data as
Bimi /(Dmi), where Bi is the biomass of individuals in body-mass interval i (actually, their
biomass per unit volume), mi the midpoint of this body-mass interval on a logarithmic axis,
and Dmi is the linear width of the interval. This representation combines the advantage of
Sheldon size spectra (Sheldon et al., 1972) of visualising structural details with the advan-
tage of high intercomparability between empirical datasets (often highlighted for
normalised spectra Bi /Dmi), because Bi mi /(Dmi) approximates the protocol-independent
quantity dB/d ln m up to a relative error declining as fast as (Dmi /mi)2 for small Dmi /mi. Axes
are isometric to ease visual appreciation of the varying degrees of uniformity of the spectra.
individuals longer than a given length threshold. The Convention for

the Protection of the Marine Environment of the North-East Atlantic
proposed the LFI as a means to set an Ecological Quality Objective
(OSPAR, 2006). EU legislation (European Commission, 2010) includes
the LFI in a list of “Criteria to be used by the Member States to assess the
extent to which good environmental status is being achieved”. Among the
important open issues in this context is, for example, the question of how
fast the LFI will return to natural levels when fishing pressure is relaxed
(OSPAR, 2006). Predictions appear to depend sensitively on the way
communities are modelled (ICES, 2010; Shephard et al., 2012), and
observed recovery is slower than was previously thought (Fung et al.,
2012a). A better understanding of the underlying fundamental processes is
thus required (Arim et al., 2011; Castle et al., 2011; Gilljam et al., 2011;
Jacob et al., 2011; Melian et al., 2011).
In view of such current, practical questions regarding marine size spectra

and their dynamics in response to anthropogenic pressures, the theory pres-
ented here is phrased with reference to marine communities and their per-
turbations by fishing. However, it should apply similarly to other cases of
size-structured communities, for example, soil ecosystems, and partially also
to communities of competing plants.
1.3. Mathematical size-spectrum models

As its starting point, any mathematical modelling requires a basic formal descrip-
tion of the system. This should be sufficiently detailed to contain or imply de-
scriptions of the main phenomena of interest. Deciding how much detail one
needs to start with is often a matter of trial and error. Typically, one will start
with very simple basic descriptions and add model ingredients only upon the
suspicion that this might lead to different conclusions. However, the implica-
tions of these more complete models can easily become difficult to understand.
In particular, the application of formal analytic tools may become impossible.
The history of the theory of community size spectra is no exception.
The earliest models developed to understand size spectra distinguished spe-
cies by their trophic levels and considered the balance of energy flow through
food chains (Kerr, 1974; Sheldon et al., 1977). Later theories, however, tended
to follow the empirically successful paradigm of simplifying the description of
community structure by disregarding species identity. This led to models in
which individuals enter the community at a fixed lower cut-off size at
constant rate, grow, consume other individuals, and eventually die through
predation, fishing, or other causes (e.g. Benoı̂t and Rochet, 2004;
Blanchard et al., 2009; Camacho and Solé, 2001; Datta et al., 2010; Law
et al., 2009; Platt and Denman, 1978; Silvert and Platt, 1978, 1980; Zhou
and Huntley, 1997). In reality, the growth of individuals slows when they
reach maturation, at a size dependent on their species identity, after which a
large proportion of food intake is invested into reproductive efforts. To
take interspecific variability in life histories into account, recent size-
spectrum models often go back to distinguishing individuals by species
(Hall et al., 2006) or maturation size class (Andersen and Beyer, 2006). To
overcome another limitation of earlier theories, Arino et al. (2004) and
Maury et al. (2007a,b) made the production of offspring dependent on
available resources. Models such as those of Andersen and Ursin (1977),
Shin and Cury (2004), Pope et al. (2006), and Hartvig et al. (2011)
combine these lines of thought by resolving individuals by both body size
(or age) and species, and accounting for the full life cycle of each species
separately. The complexity of these models, however, renders their
mathematical analysis challenging (Hartvig et al., 2011).
The model analysed here was developed by Hartvig et al. (2011), building on
the ideas of Andersen and Beyer (2006). The structure of the model is illustrated
in Fig. 2: populations of different species (not necessarily fish) are coupled
through feeding interactions. Some of the energy intake by feeding is used to
cover maintenance costs, the rest invested into growth. After body mass reaches
a maturation threshold, which depends on the species, increasingly larger pro-
portions of surplus energy are invested into reproduction so that growth ulti-
mately comes to a halt. Fecundity, therefore, depends on food availability, but
not on the density of reproducing adults, as some models in fisheries science as-
sume. Feeding interactions are particularly strong for predator individuals that are
by a certain factor larger than their prey, but interaction strengths may in addition
depend on species identities. Predation is the dominating cause of mortality. Each
of these model components is represented by fairly simple submodels designed to
keep the number of model parameters low. Where applicable, the size-
dependence of biological and ecological rates is represented through allometric
scaling laws. For a mathematical description of the model, see Section 4.
The model of Hartvig et al. (2011) represents, in simplified form,
processes operating on a number of different levels of organisation: the
short-term energy balance of individuals, the full life cycle including growth,
maturation, and reproduction, the dynamics of intraspecific population
structures, population dynamics driven by trophic interactions, and the
resulting structure and dynamics of the community as a whole. The model
is complete in that it contains, except for the energy input at the bottom of
Figure 2 Schematic illustration of the model structure. Shown are three populations of
species with different maturation body sizes that feed on and are fed on by other spe-
cies and themselves. Dashed lines indicate growth of individuals, dotted lines reproduc-
tion, and thick arrows feeding interactions.
the food chain, no “loose ends;” the balance of biologically available energy
within the system and the balance of individuals within each population are
fully accounted for.
1.4. Approximations
Legitimate approximations of community models, here those that do not
much affect predicted structure and dynamics of the size spectrum, inform
one of those details of community dynamics of which community structure
is largely independent. The approximation techniques used here will be dis-
cussed in detail when they are applied in the formal analysis. The following
provides a non-technical overview.
The basic structure of the mathematical analysis follows from a standard
technique used throughout the scientific literature: system dynamics is con-
sidered in a linearised form valid for small deviations from an equilibrium
state. As a result, the analysis technically separates into three steps: (i) the der-
ivation of the equilibrium state, (ii) linearization of system dynamics near this
equilibrium state, and (iii) evaluation of this linearised description. Of
course, approximations employed in one of the earlier steps remain in place
at the later steps. The premise implied when applying this technique is that,
although there will be corrections to system dynamics through non-linear
effects, its semi-quantitative nature is captured already at the linear level.
Whether this is indeed the case is not analysed here, although preliminary
comparisons of results with empirical data such as in Fig. 1 are encouraging.
What will be discussed in Section 9.6 is the question of whether the linear-
ization is self-consistent in the sense that small deviations from equilibrium
remain small in the future (and eventually die out).
An approximate analytic description of the model’s equilibrium state be-
comes possible mainly by combining two standard techniques: coarse graining
(Perry and Enright, 2006) along the maturation body-size axis and a mean-
field approximation (Keitt, 1997; Wilson et al., 2003) of trophic interaction
strengths. As explained in Section 5.1, these two approximations
combined lead to a picture in which species are distinguished only by
their characteristic size, for example, maturation body size, and
individuals by body size and maturation size, where the community is
described by a continuum of species of different maturation sizes, and
where trophic interaction strengths depend only on the body sizes of
predator and prey individuals. The validity of these approximations
supports studies of model systems that focus on the body sizes of species
and individuals (Belgrano and Reiss, 2011). Although formal derivation of

these approximations for the present model is conceivable, their justification
here comes only from their frequent successful application in other contexts.
One must therefore be mindful of possible artefacts. Indeed, as discussed in
Sections 2.8 and 6.4, while the intricacies of real community food webs
appear negligible for size-spectrum dynamics, the stabilising effect
resulting from their structure with distinct species linked through a sparse
network of feeding interactions cannot be ignored entirely.
Even with these two approximations, the direct mathematical analysis of
linearised system dynamics would still be challenging. To simplify the problem
further, the Quasi-Neutral Approximation (QNA; Rossberg and Farnsworth,
2011) of population dynamics is employed. The QNA assumes that variations
through time in density-dependent life-history parameters, and the resulting
modifications of intraspecific population structures, are rather small. Common
mathematical techniques exploiting small parameters can then be applied. This
allows direct calculation of the effective growth (or decay) rates of entire
populations, which result from interactions between individuals of different
populations at different life stages, without having to take the changes in pop-
ulation structures involved in these processes explicitly into account. When
the QNA is valid, it justifies the use of community models that do not resolve
different life stages within populations. The common concern that broad in-
traspecific size structure complicates community dynamics (Gilljam et al.,
2011) should therefore not lead to outright dismissal of such models.
A last step required to bring linearised community dynamics into a form sim-
ple enough to derive analytic time-dependent solutions is to recognise that,
when the offspring of a species are much smaller than the adults, its actual body
size has little influence on dynamics under the approximations used here. Off-
spring may just as well be considered “infinitely small”. The resulting, highly
simplified description of community dynamics is called the Species Size-
Spectrum Model. The approximation is verified by performing QNA and
model linearization initially in a formulation where offspring size does depend
on maturation body size and carefully analysing the implications of letting the
ratio of offspring to adult size go to zero. Incompatibility of unicellular organ-
isms with this condition is one of the reasons why microcosm experiments using
such taxa (Reiss et al., 2010) are unsuitable for modelling marine size spectra.
An approximate analytic description of the response of the Species
Size-Spectrum Model to external pressures (e.g. fishing) is then derived
using a novel technique, related to a singular perturbation expansion
(Kevorkian and Cole, 1996) of special solutions of the model. These
special solutions correspond to the trophic cascades and the bending of size
spectra described in Section 2. The validity of the approximation (verified

numerically) highlights the centrality of these phenomena for community
dynamics.
This analytic theory for size spectrum structure and dynamics is complete
to the degree that the underlying model of Hartvig et al. (2011) is complete. It
explicitly specifies conditions for jointly attaining and maintaining equilibrium
of all essential feedback loops that link individual physiology with community
structure. These are the metabolic equilibrium of individuals, the demo-
graphic equilibrium of population structures, population-dynamical equilib-
rium, and the ecological balance of community size spectra.
1.5. Structure of the paper

After briefly reviewing relevant mathematical methods (Section 3) and provid-
ing a formal description of the model (Section 4), the approximate steady-state
solution of the model is derived in Section 5. Using this solution, the QNA is
applied to the model and linearised near the equilibrium in Section 6, leading
to the Species Size-Spectrum Model. Novel mathematical techniques are then
used to find approximate analytic solutions of that model (Section 7) and ver-
ified by comparison with simulations of the same model (Section 8). Section 9
provides technical discussion of further implications of the results and points to
questions and research problems arising. Non-technical summaries of a num-
ber of noteworthy aspects of the theory are provided in Section 2.
2. SOME ASPECTS OF THE ANALYTIC THEORY

EXPLAINED IN NON-MATHEMATICAL LANGUAGE
The formal mathematical analysis of the model by Hartvig et al. (2011)
leads to several novel insights into structure and dynamics of size-structured
communities and the underlying mechanisms. This section summarises and
discusses some of these findings in a non-mathematical language. To avert
the risk of misunderstanding inherent in such undertakings, consultation of
the referenced parts of the theory for details and specifics is encouraged.
Table 1 summarises the crucial mechanisms succinctly.
2.1. Two different scenarios generate power-law community

size spectra
The analysis reveals two different scenarios that lead to formation of power-
law size spectra (Section 5.2). In the first scenario, primary producers are suf-
ficiently abundant for all grazers and all species higher up in the food chain to
feed ad libitum. The second scenario corresponds to communities in which
Table 1 Summary of major regulating constraints controlling the model community's

steady state
Regulating constraint
Phenomenon Eutrophic regime Oligotrophic regime
Size-spectrum exponent (slope) Physiological Constant satiation
mortality rate
Mortality Growth and physiological mortality rates
Individual growth rate Satiation
Satiation Maximal Size-spectrum
coefficient and
search/attack rate
Size-spectrum coefficient Producer abundance Physiological mortality
(intercept) rate
Physiological mortality rate Intraspecific size structure
Intraspecific size structure Population-dynamic equilibrium
Search/attack rate Unknown (see Section 9.6)
typical individuals at all sizes find enough food so as not to die of starvation
but if more food was available they could grow faster and generate more off-
spring. (The crossover between the two scenarios is not considered.)
Figure 1 illustrates that biomass densities of individuals in all size classes
can be much higher in eutrophic systems than they are in oligotrophic sys-
tems, so situations in which consumers effectively feed ad libitum are more
likely. The first scenario is therefore here called the eutrophic regime here and
the second the oligotrophic regime. Of course, this nomenclature is not meant
to imply that trophic status is defined by consumer satiation. The labelling
just hints at the fact that, the more eutrophic a system is, the more likely the
regime with ad libitum feeding will be encountered.1
Perfect oligotrophic power-law size spectra require the “right” abun-
dance of primary producers or a corresponding tuning of other biological
or ecological parameters. One conceivable mechanism for this is the evolu-
tionary adaptation of attack (or search) rates to avoid overexploitation of
resources (Rossberg et al., 2008). The size-spectrum is determined solely
1
Bolt labelling of mathematically distinct regimes is common scientific practice. Solid-state physicists,
for example, refer to scenarios unfolding at the temperature of liquid nitrogen (-196 C) as the “high-
temperature regime” Pratap et al., 1999).
by the allometric exponents for metabolic and attack rates (Andersen and
Beyer, 2006 and Section 5.2), typically leading to slopes close to the value
suggested by Sheldon et al. (1972). With somewhat over-abundant pro-
ducers, size spectra will bend upward on double-logarithmic scales, and vice
versa (Section 9.6).
Eutrophic power-law size spectra appear to impose fewer constraints on
parameters. In the eutrophic regime, the size-spectrum slope depends on the
efficiency of energy transfer from smaller to larger species. Depending on
ecological parameters, the slope can become larger or smaller than in the ol-
igotrophic case, and for real systems, it can vary along the size axis. Absolute
abundances scale with the abundances of primary producers.
As the oligotrophic regime is characterised by ad libitum, and therefore
density-independent, feeding, model populations in this regime are regu-
lated entirely through density-dependent mortality, so it might be a surprise
that, despite this pure “top-down control”, the abundance of primary pro-
ducers can determine population abundances at higher trophic levels.
This becomes possible because overabundance of species in any given size
class releases the early life stages of larger species from predation mortality.
As a result, the populations of larger species grow and deplete smaller
species through increased mortality—until a new equilibrium is reached
(Section 8.4.5).
This new, differentiated picture of the controlling mechanisms might help
to understand the role of trophic status in shaping observed size spectra.
A general empirical pattern seems to be (Marquet et al., 2005) that in
oligotrophic systems, size spectra closely follow power laws with slopes
(i.e. exponents) in line with Sheldon’s hypothesis Sprules and Munawar
(1986), Rodriguez and Mullin (1986a), Gaedke (1992b), Quiñones et al.
(2003), and that with increasing nutrient load, size spectra become more ir-
regular, exhibiting weak trends in the best-fitting slopes, which vary between
studies (Ahrens and Peters, 1991; Bays and Crisman, 1983; Bourassa and
Morin, 1995; Dortch and Packard, 1989; Gaedke et al., 2004; Jeppesen
et al., 2000; Pace, 1986; Sprules and Munawar, 1986), with some
tendency to favouring higher relative abundance of larger individuals at
high nutrient loads (Ahrens and Peters, 1991; Sprules and Munawar, 1986,
see also Fig. 1) as expected from the present theory. Mulder and Elser
(2009) and Mulder et al. (2009) found the same trend in soil communities.
Indeed, such patterns are suggested already by comparisons of the size
spectra recorded by Sheldon et al. (1972) around the American continent
with corresponding maps of nutrient loading (Garcia et al., 2006). Related
to this may be the observation by Yvon-Durocher et al. (2011) that warming

increases size-spectrum slopes in aquatic mesocosms.
2.2. Feeding alone couples size classes

An intermediate result of the analytic calculations is the Species Size-
Spectrum Model, Eq. (78), a balance equation for the biomasses pertaining
to species in different size classes, which are coupled through feeding interac-
tions. The Species Size-Spectrum Model only accounts implicitly for intraspe-
cific size structure. By showing that such a model can describe community
dynamics and, by extension, the dynamics of the classical individual size spec-
trum, the present analysis differs from some earlier approaches. It implies that
somatic growth does not essentially contribute to the ecological coupling
along the size axis, notwithstanding its important contributions in controlling
biomasses and population structures of species. This result provides firm foun-
dations to related criticism by Kerr and Dickie (2001), who argue that the
“characteristics [of size spectra] form an inexorable consequence of mathematical relations
between size-dependent allometries of the acquisition and transmission of energy through
predation processes and the attendant metabolic dissipation.” (p. 138). They consider
that “mechanisms operating at the physiological level” enter just by determin-
ing the “scaling of the efficiency coefficients” (p. 139) in this process. Indeed,
the observed deep gaps between domes that Kerr and Dickie (2001) highlight
would become tight bottlenecks were size classes primarily coupled through
somatic growth. This insight parallels a corresponding observation that, de-
spite the wide body-size ranges species span during growth, the individual size
spectrum is highly correlated with the species size spectrum (Shephard et al.,
2012).
2.3. Population-level predator–prey size-ratio windows

are wide
Most verbal models and qualitative models of trophic interactions in aquatic
communities2 operate at the population or species level, as do many quan-
titative models. Understanding the general size-dependence of trophic
interactions at the population level is therefore important not only for
size-spectrum theory.
2
Such models abound in the literature. Two randomly chosen examples are the statement “Norway lob-
ster, while not quite as an important part of the cod diet as whiting, is a slow-growing species and consequently more
sensitive to the predation release produced by the removal of cod” made by Speirs et al. (2010) or the graphs of
food-web topologies by Yodzis (1998).
Under the simplifying assumption that the size-dependence of trophic

interactions is controlled, apart from allometric scaling laws, only by relative
sizes, it can be characterised by a predator–prey size-ratio window. This
gives, for each ratio of predator to prey size, the probability or intensity
of trophic interactions. The window can be defined either for interactions
between individuals, with the relative sizes given, for example, in terms of
the individuals’ body masses, or for interactions between populations of
species, with size then measured, for example, in terms of maturation
body mass.
It is shown in Section 9.3 that the structure of (average) population-level
predator–prey size-ratio windows is mostly determined by the intraspecific
size structures of prey and predator. The individual-level predator–prey
size-ratio window plays only a minor role. The predicted population-level
predator–prey size-ratio window (Fig. 9) is wide, in line with empirical an-
alyses by Neubert et al. (2000) and Woodward and Warren (2007). Under
the idealisations invoked in the analytic theory, it decays with an exponent
near zero (0.05) with increasing maturation body mass ratio (Fig. 9). In
reality, the windows will, of course, be truncated above maturation size
ratios where the newborns or hatchlings of one species are so large that they
feed on the adults of the other.
2.4. Simple mass-balance models explain only equilibrium

It turns out (Section 9.2) that predicted equilibrium size spectra of commu-
nities perturbed by size-selective fishing can consistently be interpreted by
verbal arguments or simplified, static mass-balance models (Christensen and
Pauly, 1992) where “large species eat small species” without regard to the
broad population-level predator–prey size-ratio windows resulting from
somatic growth. However, when such simplified models would be used
to predict dynamics (akin to the Ecopath with Ecosim approach; Pauly
et al., 2000), this would lead to very different results from when size
structure was, at least implicitly, included (Section 9.2, Fig. 10).
2.5. Both upward and downward cascades form in response to

size-specific perturbations
The dynamics of complex systems can often efficiently be analysed and de-
scribed in terms of their responses to controlled perturbations of system
states. Adapting this idea to the ecological context, Bender et al. (1984) dis-
tinguish between short pulse perturbations and long-lasting press perturbations of
constant intensity. Here, press perturbations will be considered, if not stated

otherwise. An example of such a perturbation is sustained fishing with a con-
stant effort.
Trophic cascades, in which a perturbation of abundance at a higher tro-
phic level leads through trophic top-down effects to alternating increases and
decreases of abundances towards lower trophic levels, are a well understood
phenomenon. They naturally arise in size-spectrum models (Benoı̂t and
Rochet, 2004). Andersen and Pedersen (2010) demonstrated in simulations
of a size spectrum perturbed by fishing that, together with these “down-
ward” cascades, another type of cascade can emerge, with alternating abun-
dance increase and decrease towards higher trophic levels. The cascades
found by Andersen and Pedersen (2010) were always damped, that is, the
relative change in abundances became smaller with increasing distance from
the externally perturbed size class. Periodic maxima (“domes”) in size spec-
tra, as observed, for example, by Schwinghammer (1981), Sprules et al.
(1983), and Sprules and Goyke (1994), and documented in Fig. 1, are likely
to correspond either to upward or to downward trophic cascades.
The Species Size-Spectrum Model accounts for both types of cascades
(Section 8.4.1). Its analysis reveals that upward and downward cascades
are mathematically independent phenomena (Section 7.4), and that both
can be damped or not (i.e. amplifying), sensitively depending on model pa-
rameters (Sections 8.4.4 and 8.4.5). The intuitive mechanism underlying
upward cascades is the more-or-less pronounced formation of a trophic
ladder, with the steps corresponding to the cascade’s local maxima and
the space between steps to the minima. In simple variants of the Species
Size-Spectrum Model with narrow individual-level predator–prey
size-ratio windows (not analysed here), therefore one finds that in
upward cascades subsequent abundance maxima are separated by the
predator–prey size ratio, whereas for downward cascades subsequent
maxima are separated by the square of the predator–prey size ratio (two
steps down ladder). In the more realistic model variants considered in
Section 8.4, this situation is realised for some parameter choices (e.g.
Fig. 7A and B). However, for the standard parameter set used here
(Section 8.1), which builds on that proposed by Hartvig et al. (2011), the
distinction of upward and downward cascades by characteristic size ratios
is blurred (Figs. 4 and 6).
The separation of subsequent local maxima for standard parameters cor-
responds in both directions to a factor 105 in body mass (Fig. 4). Perhaps
fortuitously, this agrees well with the separation of subsequent “domes” or
maxima in empirical size spectra (Fig. 1; Sprules and Goyke, 1994; Sprules
et al., 1983). To classify cascades empirically, it might therefore be necessary
to determine the direction of motion of perturbation responses in temporally
resolved size spectra (Rodriguez and Mullin, 1986b; Rodriguez et al., 1987;
Vasseur and Gaedke, 2007).
In the light of the observations in Section 2.4, it is conceivable, though
by no means established, that the theoretical interpretation of “domes” in
size spectra by Thiebaux and Dickie (1993) through equilibrium
mass–balance equations is compatible with formation of these structures
by one of the two mechanisms leading to periodic modulations in the pre-
sent theory. The difference would be that, whereas Thiebaux and Dickie
(1993) address the fully developed non-linear form of the domes, the present
theory describes their dynamic emergence in the linear response to pertur-
bations. The relationship between the two theories would then be similar to
that encountered for water waves (Johnson, 1997), where linear and weakly
non-linear theories describe low-amplitude waves, which are necessarily
sinusoidal, whereas high-amplitude waves, which, as we know from expe-
rience, can assume entirely different shapes, are described by a different,
non-linear theory.
The observation that different phyla are often associated with different
domes (Gaedke, 1992a) does not necessarily stand in opposition to explana-
tions of these structures in terms of general principles. In fact, evolution
might naturally lead to this kind of specialisation within uneven size spectra.
2.6. Trophic cascades form slowly

Upward and downward trophic cascades in communities with broad intra-
population size distributions will emerge slower than would be expected
from models that do not account for intrapopulation size structure
(Section 9.4). The reason is that pairs of species for which the adults are in
a clear predator–prey relation to each other might interact as prey–predator
or as competitors at other life-history stages. Figure 4, for example, docu-
ments formation of a downward cascade in the model with a delay
corresponding to the threefold maturation age of the main size class targeted
by fishing. Lags of 6–12 years between time-series of size-spectrum charac-
teristics and of exploitation rates, which Daan et al. (2005) observed in the
North Sea but found “hard to account for”, might be explained by this
observation. The slow recovery of the LFI shown by Fung et al. (2012a,b)
in data and simulations is likely to reflect this phenomenon too.
2.7. Depletion of species higher up in the food chain is fast

For the scenario labelled as the oligotrophic regime, the Species Size-
Spectrum Model predicts that upward trophic cascades are superimposed
with an overall decline of species larger than the size class targeted by
size-selective harvesting (Sections 8.4.1 and 8.4.4) and that this effect is
the stronger the larger species are relative to the targeted size class
(Section 9.4). The underlying mechanism is the same as that operating in
simple food-chain models: insufficient supply of energy. However, with
broad intrapopulation size distributions, the effect can propagate faster to
larger species than it would in simpler models, because the indirect
responses of larger species propagating through the food chain are
combined with direct responses of similar magnitude attributable to
harvesting or starvation of their juveniles. The timescale for the population
response of large species to size-selective harvesting of smaller species or
individuals is therefore of the order of magnitude of their maturation times.
2.8. Food-web structure essentially affects size-spectrum

structure and dynamics
The derivation of the Species Size-Spectrum Model depicts communities as if
there was a continuum of interacting species of all sizes and assumes that life-
history traitsand feeding interactions are determined by maturation sizesand body
sizes alone. An immediate consequence is that species of comparable size are also
similar in all their ecological traits and therefore compete with each other. With-
out appropriate regularisation of the model, the resulting competitive exclusion
dynamics lead to instabilities of size spectra in which increases in the abundances of
some species are compensated by decreases in the abundances of other species of
very similar size (when coarsening the resolution of size classes, the spectra are
generally stable). In reality, stable size-structured communities can form because
ecological traits differ even between species of equal maturation size (Jacob et al.,
2011), and, perhaps most importantly, in general, feeding interactions do not de-
pend only on the sizes of prey and predator (Naisbit et al., 2012). Species coexist
by forming rather sparse food webs: for example, Rossberg et al. (2011) show that
only about 10 species contribute more than 1% to the diet of the average fish spe-
cies, independent of local species richness. This, it is argued in Section 6.4, mod-
ifies continuum size-spectrum dynamics at size resolutions corresponding to the
maturation body-size ratios among species in the diets of typical predators.
Because, as a result of strongly overlapping intraspecific size distribu-
tions, size-spectrum dynamics rather slow, these food-web effects are
likely to be sufficiently strong to modify dynamics substantially, even on

coarser scales. In the present analysis, food-web effects are derived, para-
metrised, and included in the model based on heuristic arguments rather
than on first principles. The theory, while allowing many other insights,
is therefore unsuitable for reliable quantitative predictions of community
dynamics. This would require models that quantitatively account for food-
web topology.
2.9. Body mass approximates reproductive value

Fisher (1930) defined the reproductive value of an individual as its expected
contribution “to the ancestry of future generations”. Recently, Rossberg and
Farnsworth (2011) developed a method to extend this empirically useful
concept from the density-independent (linear) dynamics of a single popula-
tion to complex communities of interacting populations. They argued, with
fisheries management in mind, that a quantification of the size of a popula-
tion by the summed reproductive values of its members should allow better
predictions of future population (or “stock”) sizes than other measures of
population size, for example, the commonly used spawning-stock biomass.
Remarkably, under a certain set of approximations, the present theory
evaluates the reproductive value of individuals to be exactly equal to their body
mass (Section 6.2). This result holds for both mature and immature individuals.
The summed reproductive value of a population would then simply be its total
biomass. Tests of this prediction by computing reproductive values from em-
pirically determined life-history parameters of a population might lead to more
reliable characterisations of stock sizes and help to resolve the question whether
the smaller or the larger individuals of a stock should be harvested preferentially
to maximise economic output under given constraints on ecological impact.
2.10. Physiological mortality is constrained by population

dynamic equilibrium
Beyer (1989) recognised the importance of the specific physiological mortality
rate, a dimensionless parameter defined as a cohort’s mortality rate divided by
its specific growth rate (i.e. the relative body mass increase per unit time).
Physiological mortality as a function of body size determines a population’s
internal size structure. Here, it is shown that, under a certain set of approxi-
mations, specific physiological mortality must be exactly 1 for immature co-
horts in population-dynamic equilibrium (Section 5.4). Greater mortality
leads to the decline, less mortality to the growth of populations. Even under
relaxed assumptions, a value close to one can still be expected (Section 5.7).
Indeed, the density dependence of physiological mortality alone essentially
controls population dynamics (Section 6.3, Eqs. (61) and (63)). Real-world
complications will modify these results, especially for species with rather
small ratios of adult to newborn (or hatchling) body sizes, but overall a
close relation between population-dynamic equilibrium and specific
physiological mortality is expected. This insight might help fisheries
managers interpreting the outcomes of virtual population analyses (Lassen
and Medley, 2001) and relating them to stock dynamics.
To the extent that the specific physiological mortality of immature in-
dividuals attains a universal value, the results of Beyer (1989) imply that
the size structure of the immature component of populations is universal,
except for a truncation below the size of newborns or hatchlings
(Section 6.2). An empirical test of this approximate universality of size dis-
tributions and a better understanding of the magnitude and the causes for
deviations from it might lead to other generalisations regarding structure
and dynamics of interacting size-structured populations (Houde, 2009).
2.11. Solutions of “size-spectrum” equations follow general

characteristics
In Section 7, this chapter develops a general method to approximate the
solutions of a wide class of equations that describe the dynamics of
size-structure communities, subject to two general principles that are often
invoked in ecological theory. The first principle is allometric scaling of eco-
logical rates with a fixed power n of body size (n ¼ 3/4 is often used), and the
second principle posits that, apart from the allometric scaling of rates, inter-
action strengths between individuals depend only on their relative, but not
their absolute, sizes.
The approximate general solution of this class of equations implies that,
in response to press perturbations targeting a narrow range of size classes,
fronts are emitted from the perturbed size range that travel at constant speed
on a scale given by body mass raised to the power (1 n), either towards
larger or towards smaller size classes. The fronts leave behind themselves
either a static, modulated structure with a wavelength that is constant on
the logarithm body mass axis (e.g. trophic cascades) or regions of either con-
sistently raised or reduced abundances. The amplitude of the modulation or
of the rise/decline can either increase away from the perturbed size class,
or decrease. The effects of a pulse perturbation can be described by linear
combinations of press perturbations (Section 9.6). A graphic method to
decide for a given system which of the various conceivable scenarios will be
realised is introduced in Section 8.4.3.
3. METHODS
This section briefly recalls some standard concepts of functional
analysis used in developments of the theory below. The text by Boccara
(1990) covers most of these topics in mathematically rigorous yet accessible
form.
For a real- or complex-valued function f(x), define its Fourier transform
f^ðxÞ such that
Z 1 Z 1 ixx
^ ixx e ^
f ðxÞ ¼ e f ðxÞdx, f ðxÞ ¼ f ðxÞdx, ½1
1 1 2p
where i is the imaginary unit (i2 ¼ 1). The convolution f ∗ g of two func-
tions is defined as the function h given by
Z 1
hðxÞ ¼ ½ f ∗gðxÞ ¼ f ðy xÞgðyÞdy: ½2
1
With normalisations as in Eq. (1), Fourier transformations directly carry

convolutions over into multiplication, that is, for any two functions f, g, one
has fc ^
∗g ¼ f ^g. This relation implies that f ∗ g ¼ g ∗ f, ( f ∗ g) ∗ h ¼ f ∗ (g ∗ h), and
f ∗ ( g þ h) ¼ f ∗ g þ f ∗ h.
Depending on the convergence of the defining integral, the value of a Fou-
rier transform f^ðxÞ can be computed via Eq. (1) not only for any real x but also
for some complex-valued x. Consider, for example, the Gaussian window

y2
Ws ðyÞ ¼ exp 2 : ½3
2s
Its Fourier integral evaluates for arbitrary complex x to
pffiffiffiffiffi
W^ s ðxÞ ¼ 2psexpðx2 s2 =2Þ: ½4
As another example, the function defined by f(x) ¼ 0 for x < 0 and
f(x) ¼ e 2x for x 0 has, by Eq. (1), the Fourier transform
f^ðxÞ ¼ ð2 þ ixÞ1 for any complex x such that Im{x} < 2. (Real and
imaginary parts of complex numbers x are denoted by Re{x} and Im
{x}, respectively.) When Im{x} 2, the integral in Eq. (1) does not con-
verge. However, the definition of f^ðxÞ is naturally extended to any
complex x 6¼ 2i by analytic continuation. Then, the formula

f^ðxÞ ¼ ð2 þ ixÞ1 is valid for all complex x except x ¼ 2i. Such analytic
continuations of Fourier transforms will play an important role below.
Dirac’s delta function d(x) symbolises the idealised case of a function
Ra that
is zero for all x except x ¼ 0, and so (infinitely) large atRx ¼ 0 that a d(x)dx
a
¼ 1 for any a > 0. It follows, for example, that a f(x)d(x)dx ¼ f(0)
for any a > 0.
A functional derivative dF[g]/dg(y) is the generalisation of the notion of a
gradient to vectors with continuous-valued indices y, that is, functions g(y).
Standard rules of differential calculus translate straightforwardly to functional
derivatives, except that, because the dependence of an expression F[g] in g(x)
on the single point of g(x) where x ¼ y is generally tiny, functional deriva-
tives contain
R1 an additional factor d(y). For example, dg(x)/dg(y) ¼ d(x y),
and d 1 f(g(z))dz/dg(y) ¼ df(u)/du evaluated at u ¼ g(y).
Define a scalar product for real-valued functions as
Z 1
h f jgi ¼ f ðxÞgðxÞdx: ½5
0
The adjoint of a linear operator L (a linear mapping from functions g(x)

onto functions [Lg](x)) can then be defined as the linear operator Lþ that
satisfies for all functions f and g (with some mathematical constraints):
hL þ f jgi ¼ h f jLgi: ½6
It can be computed as
dh f jLgi
L þ f ðxÞ ¼ : ½7
dgðxÞ
4. MODEL
The model underlying this theory has been motivated and derived by
Hartvig et al. (2011). Its major strengths are a consistent synthesis of dynamic
descriptions of size-structured communities, populations, individual
growth, and bioenergetics based on general biological principles; the
model’s small set of parameters, all of which are estimated from empirical
data; and its demonstrated structural stability. This section provides only a
technical summary and highlights minor deviations from the formulation
of Hartvig et al. (2011). Table 2 lists symbols used throughout this work
and their interpretation.
Table 2 List of important symbols

Symbol Defined near equation Interpretation
a (11) Assimilation efficiency
b Preferred predator–prey size ratio
b~ ðwÞ (71) Equilibrium population structure on log-
scale
b~ ðwÞ (73) b~ ðwÞ

b~ ðwÞ
n (126) enwb~ ðwÞ
g (10) Coefficient of search/attack rate
E (12) Efficiency of reproduction
(11) Maturation- over asymptotic mass
k0(w) (70) Individual-level interaction kernel on
log-scale
l (16) Exponent of community size spectrum
mp(m) (13) Predation mortality
m0 (14) Coefficient of natural mortality
~
m (26) Coefficient of predation mortality
n (73) 3–l–n
sF (77) Width of harvested size range
f(m) (19) Density of prey available
~
f (19) Coefficient of f(m)
F(u) (79) Fishing pressure on log-scale
c(x) (11) Reproduction selection function
aj(u, t) (93) Delocalised response to fishing pressure
a(m, m∗) (60) Specific physiological mortality
a~ (35) Scale-free juvenile specific physiological
mortality
b(u) (75) Perturbation of equilibrium biomass
distribution over log-scale
b0(u) (89) Fourier solution of Species Size-
Spectrum model
bc(u) (93) Core response to fishing pressure
Continued
Table 2 List of important symbols—cont'd

B(m∗) (56) Reduced dynamic variables of QNA
Btot(m∗) (40) Scale-invariant equilibrium biomass per
maturation size class
B~tot (40) Coefficient of Btot(m∗)
Bm∗ (49) Equilibrium biomass per maturation size
class
Cm∗ (53) Normalisation constant of reproductive
value
F (77) Maximal fishing mortality
f(m) (10) Degree of satiation
~gðxÞ (24) Scale-free growth rate
~gr ðxÞ (24) Scale-free fecundity
g(m, m∗) (11) Growth rate
gr(m, m∗) (11) Fecundity
~g0 (24) Coefficient of growth rate/fecundity
h (11) Coefficient of maximal food intake
J ðmÞ (52) Equilibrium flow of reproductive value
m
∗
k (11) Coefficient of metabolic loss rate
Ktot(m∗) (42) Metabolic losses per maturation size class
K~ tot (42) Coefficient of Ktot(m∗)
K(m∗, m∗0 ) (62) Population-level interaction kernel on
linear scales
~
KðwÞ (74) Population-level interaction kernel on
log-scales
Lm (47) McKendrick–von Foerster operator
∗
Lþm (51) Adjoint McKendrick–von Foerster
∗
operator
m Body size
M (75) Arbitrary unit mass
m∗ Body size at maturation
m0, m0(m∗) (16) Size of offspring
Table 2 List of important symbols—cont'd

mF (79) Size class targeted by fishing
n (10) Exponent for physiological rates
N(m, m∗) (16) Distribution of individuals by body and
maturation size
Ni(m) (9) Intraspecific size distribution
~
N(x) (16) Scale-free intraspecific size distribution
N ðmÞ (17) Community size spectrum
~
N (17) Coefficient of community size spectrum
q (10) Exponent for search/attack rate
s(x) (8) Predator–prey size-ratio window
uF (108) Logarithmic size class targeted by fishing
Vm∗(m) (51) Reproductive value
Ws(y) (3) Gaussian window
Wm∗(m) (48) Equilibrium population structure
x0 (29) Relative size of offspring
The model describes trophic interactions between reproductively iso-

lated populations of heterotrophic species in large, size-structured aquatic
communities. It distinguishes between individuals of different body mass
m within each population j, and assumes all individuals of the same size and
the same population to be equivalent. Each population is therefore
characterised by a size distribution Nj(m) of individuals. Specifically, following
Hartvig et al. (2011), the number of individuals of population j within the
infinitesimally small body mass interval [m; m þ dm] is given by VNj ðmÞdm,
where V is the volume of the system considered (a formulation in terms of
areal density would equally be possible). In general, Nj(m) will be time-
dependent.
Energy and biomass are thought to flow overwhelmingly from smaller to
larger individuals (Gilljam et al., 2011; Woodward et al., 2010b). The
demographics of the smallest species in the community are not modelled
explicitly. Rather, the idealisation is invoked that all species are much
larger than the smallest individuals in the community, so that the relevant
(log m)-axis stretches infinitely into both directions. This admits a description
in which the prey species of every consumer are again consumers, and all
species are consumed by some other, larger species so that, mathematically,
there is an infinite hierarchy of species sizes in the community. The
original model of Hartvig et al. (2011) instead summarises the density of
individuals of small species by a resource spectrum NR(m).
The biomass density of food available to an individual of species j with
body mass m is given by
Z 1
m
fj ðmÞ ¼ mp N j ðmp Þs ln dmp , ½8
0 mp
where N j ðmp Þ is the density of prey of size mp available to j, and the function
s() characterises the individual-level predator–prey size-ratio window on a
logarithmic scale.
The theory admits essentially arbitrary predator–prey size-ratio windows,
but the following plausible constraints shall be imposed: s(u) is non-negative
and decays faster than exponentially as u ! 1. The Fourier transform ^sðxÞ
of s(u) is then an entire function (i.e. it is finite for any complex x). An example
satisfying this condition is given by Eqs. (109) and (110).
The density of prey entering Eq. (8) is given by
X
N j ðmÞ ¼ yj, k Nk ðmÞ, ½9
k
with the weights yj,k 2 [0; 1] characterising dietary preferences, that is, the
food web. Dependence of yj,k on life stages could be incorporated into
the formalism but is not considered here. On the contrary, the analysis will
largely be based on a mean-field approximation, that is, the ecosystem mean
of yj,k is absorbed into the search rate (see below), and all yj,k are set to 1.
Then N j ðmÞ ¼ N ðmÞ is the same for all predators j, and so the density of
available food fj(m) ¼ f(m).
Food intake is determined by the density of prey f(m), the effective
search rate, assumed to be of the form gmq (with constants g, q > 0), and
the physiological maximum food-intake rate of individuals. The latter is as-
sumed to scale as hmn, with constants h > 0 and 0 < n < q. For simplicity, n is
identified with the allometric exponent for metabolic rates. Typically,
n 0.75 (Peters, 1983), but here only n < 1 is required. Specifically,
individuals of size m feed at a rate f(m)hmn, where the degree of satiation
f(m) 2 [0; 1] is given by
gmq fðmÞ
f ðmÞ ¼ : ½10
gmq fðmÞ þ hmn
This corresponds to an individual-level Type II functional response with
handling time (hmn) 1 (dimensions: Time/Mass). In the limit h ! 1, the
special case of a linear functional response f(m)hmn ! gmqf(m) is recovered.
Food intake is discounted by the assimilation efficiency 0 < a < 1 and
metabolic losses at a rate kmn (with constant k > 0), leaving a net uptake
of energy af(m)hmn kmn available for somatic growth and reproduction.
It is apportioned between these two uses according to a reproduction-
selection function c(m/m∗j) 2 [0, 1], with m∗j characterising the size of spe-
cies j at maturation. That is, individuals grow at a rate g(m, m∗j) (dimension
Mass/Time) and invest into offspring at a rate gr(m, m∗j), with
gðm, m∗j Þ ¼ ½1 cðm=m∗j Þ½af ðmÞh kmn ,
½11
gr ðm, m∗j Þ ¼ cðm=m∗j Þ½af ðmÞh kmn :
Individuals produce offspring, assumed to be of size m0j, at a rate
(E/2m0j)gr (m, m∗j) (dimension 1/Time), with the factor 1/2 representing
the assumed proportion of females in a population and the reproduction
efficiency E discounting for all additional losses from production of eggs
to birth or hatching. With the case of fish in mind, Hartvig et al. (2011)
assumed the size of hatchlings m0j ¼ m0 to be effectively the same for all
species, independent of maturation size m0j. Here, m0j values that vary
between species will be admitted. Integrating over spawners of all sizes,
species j produces offspring at a rate
Z 1
E
Rj ¼ Nj ðmÞgr ðm, m∗j Þdm: ½12
2m0j 0
Many analytic results derived here are independent of the specific form of
the reproduction-selection function c(x), but the following general charac-
teristics will be used below: whereas maturation is a gradual process, it is
sufficiently well defined that, as x ! 0, c(x) goes to zero, with most of
the transition taking place near x 1. In order for individuals to have
well-defined growth trajectories, c(x) should be Lipschitz continuous.3
Further, it is assumed that c( 1) ¼ 1 for some constant 0 < < 1, and that
0 c(x) < 1 for 0 < x < 1.
3
A function f(x) is called Lipschitz continuous if there is a positive constant K such that |f(x)– f(y)| <
K |x –y| for all x, y in the domain of f.
These conditions ensure that individuals cannot reach the size m∗/, which
therefore becomes a sharp upper bound on body size.
The predation mortality of individuals of size mp follows from the model
of food intake above. It is given by
Z 1
m
mp ðmp Þ ¼ s ln ½1 f ðmÞgmq N ðmÞdm: ½13
0 mp
Mortality from all other causes is summarised in a species-dependent back-

ground mortality
mj ¼ m0 mn1
∗j
, ½14
chosen such as to be proportional to inverse generation time. It is assumed
here that, as Hartvig et al. (2011) suggested, the parameter m0 0 is suffi-
ciently small that mj becomes relevant only for adults. Hartvig et al.
(2011) also included starvation mortality in their model, but the situations
where this becomes relevant lie beyond the scope of the current theory.
Combining the effects of growth, mortality, and reproduction, one ob-
tains a balance equation for the distribution Nj(m) of the individuals forming
a population over body sizes (McKendrick, 1926; von Foerster, 1959):
@Nj ðmÞ @ h i h i
þ gðm, m∗j ÞNj ðmÞ ¼ mp ðmÞ þ m0 mn1 Nj ðmÞ: ½15
@t @m ∗j
The boundary condition Rj ¼ g(m0j, m∗j)Nj(m0j), equating offspring produc-

tion with outgrowth, closes the model.
5. PROPERTIES OF THE SCALE-INVARIANT

COMMUNITY STEADY STATE
5.1. Discussion of the underlying approximations
To obtain an analytic characterisation of the solution of this model, two ad-
ditional approximations are made. Both are motivated by the empirical fact
that the community size spectrum N ðmÞ often follows a power law
N ðmÞ/ ml over a wide range of body sizes m. (Sheldon’s hypothesis cor-
responds to l 2.) The first approximation is to coarse-grain over species
with similar maturation size m∗j, giving a smooth distribution N(m, m∗) of
individuals over body sizes m and maturation sizes m∗ (Andersen and Beyer,
2006). In this coarse-grained description, the number of individuals in the
infinitesimal body size interval [m; m þ dm] belonging to species with
maturation body sizes in the infinitesimal interval [m∗; m∗ þ dm∗] is given by

VN (m,m∗) dmdm∗ with V again denoting system volume. It is assumed that
the size of hatchlings or newborns m0 is determined largely by maturation
size m∗, so that the former becomes a function of the latter. This can be a
linear relationship, a functional relationship where m0 is constant over some
range in m∗, or any other type of non-linear functional relationship. With
this and the foregoing mean-field approximation in place, species with sim-
ilar m∗ will typically be similar in all their ecological characteristics. The
competitive exclusion dynamics resulting from this approximation is dis-
cussed in Section 6.4.
The second approximation is motivated by the scale-invariance of the
community size spectrum, highlighted by Camacho and Solé (2001) and
Capitán and Delius (2010).4 It suggests that the underlying intraspecific size
distributions Nj(m) are, to some approximation, also scale-invariant when fac-
toring out the dependence on maturation body size m∗j. Specifically, condi-
tions will be derived for which Nj(xm∗j) / Nk(xm∗k) to a good approximation
over a wide range in dimensionless body masses x for most pairs of species
( j, k). The obvious truncation of intraspecific size structure below the size
def
of hatchlings m0j, that is, for5 x < x0j ¼ m0j =m∗j , violates this approximation
and will therefore receive special attention below. It turns out that the limit
x0j ! 0 is often non-singular and taking it yields ecologically consistent results.
The combination of these two approximations leads to an ansatz
(
ml1 N~ ðm=m Þ for m m0 ,
N ðm, m∗ Þ ¼ ∗ ∗ ½16
0 for m < m0
for the coarse-grained, scale-invariant distribution of individuals, where m0
~ remains to be
is a function of m∗ and the scale-free size distribution N(x)
determined.6
In the small-hatchling limit m0/m∗ ! 0, the coarse-grained community
size spectrum Eq. (9) can be evaluated, by using first Eq. (16) and then
substituting m∗ ¼ m/x, as
4
Recall that scale invariance in the simple form N ðcmÞ ¼ c -l N (m) is equivalent to the power-law con-
dition N (m) 1 m -l: The power law obviously implies scale invariance. The converse can be seen by
differentiating the scaling laws with respect to the scale factor c at c ¼1 and solving the resulting
differential equation. As both conditions imply each other, they are equivalent.
def
5
The notation A ¼ B indicates the definition of A as B.
6
To streamline notation, a tilde (
) is used throughout this work to indicate the “scale-invariant part” of
some mass-dependent function. This leads to the following modification of the notation used by
Andersen and Beyer (2006) and Hartvig et al. (2011): a ! ~a,Nc ðmÞ ! N ðmÞ,kc ! N ~ , ℏ ! ~g , ap ! m
~:
0
Z 1
N ðmÞ ¼ Nðm,m∗ Þdm∗
Z0 1
¼ ~ ðm=m Þdm
m∗ l1 N ∗ ∗
½17
Z0 1
¼ ~ ðxÞdx
xl1 ml N
0
~,
¼ ml N
with a constant
Z 1
~ ¼
N ~ ðxÞdx:
xl1 N ½18
0
Equation (17) confirms the supposed relation between ansatz (16) and
power-law size spectra, Eq. (17). Consistency of this result requires that
the integral in Eq. (18) converges, which will be verified after
~ and l in Section 5.4.
computing N(x)
5.2. Scale-invariant demographics

The steady-state demographic rates are now evaluated assuming
scale-invariance (Eq. (17)) and making use of the mean-field approximation
N j(m) ¼ N (m). Prey availability, Eq. (8), then becomes
Z 1 !
m
fðmÞ ¼ mp N mp s ln dmp
0 mp ½19
~
¼ m2l f,
where the constant
Z 1
f ~
~ ¼N yl3 sðlnyÞdy ½20
0
is obtained from Eq. (19) using the substitution mp ¼ m/y. Doing another
substitution, y ¼ ex, then noting the formal similarity with a Fourier integral,
the integral in the last equation above can be expressed in terms of the
Fourier transform ~sðxÞ of s(x):
Z 1 Z 1
y sð lnyÞdy ¼
l3
eðl2Þx sðxÞdx
0 1
¼ ~sðiðl 2ÞÞ: ½21
Below, similar transformations will be applied to evaluate other integrals.
The consumer satiation resulting from the prey availability f(m) com-
puted above is
gm2þql f~
f ðmÞ ¼ : ½22
~ þ hmn
gm2þql f
According to Eq. (11), consumers neither grow nor reproduce when
satiation f(m) < k/ah. Exclusion of this situation leaves two scenarios for
~ hmn over the body-size
scale-invariance of f(m). In the first case, gm2þql f
(m) range of interest, so f(m) 1. This regime breaks down at body sizes
~ 1=ð2þqlnÞ , where a crossover to a non-scale-invariant regimes
m ½h=ðfgÞ
occurs. However, this point can be moved mathematically to arbitrarily large
or small m, respectively, by an appropriate choice of g. In the second case,
def ~ ~ þ hÞ. This fixes
2 þ q l ¼ n, so that f ðmÞ ¼ f~ with constant f~ ¼ gf=ðg f
the size-spectrum exponent as l ¼ 2 þ q – n (Andersen and Beyer, 2006).
Mindful of the caveats discussed in Section 2.1, the first case is called the
eutrophic regime and the second the oligotrophic regime.7
Both cases lead to scale-invariant somatic and reproductive growth rates:
gðm, m Þ ¼ ~gðm=m∗ Þmn , gr ðm=m∗ Þ ¼ ~gr ðm=mr ∗ Þmn , ½23
where
~gðxÞ ¼ ½1 cðxÞ~g0 , ~gr ðxÞ ¼ cðxÞ~g0 ½24
with
~g0 ¼ af0 h k, ½25
and f0 ¼ 1 or f0 ¼ f~, depending on the case considered.
To evaluate predation mortality, Eq. (13), in the eutrophic regime, the
lowest-order correction to satiation, f ðmÞ ¼ 1 hmnþl2q g1 f~ 1 þ ,
needs to be taken into account, giving
Z !
1
m ~ 1 N
~ dm
mp ðmp Þ ¼ s ln hmn2 f
0 mp ½26
~mn1
¼m p ,
with a constant
7
Maury et al. (2007b) investigated a size-spectrum model in which the allometric exponent for maximal
ingestion / m2/3 is smaller than the exponent for metabolic losses / m, so that ingestion limits are
relevant only for the largest organisms. Then other scaling regimes become possible, e.g. such that in-
gestion balances maintenance cost by having feeding levels/ m1-2/3 ¼ m1/3. Their Fig. 5e might rep-
resent this scenario for body lengths <0.1 m. It is not considered here.
~
hN
~¼
m ^sðiðn 1ÞÞ, ½27
~
f
expressed in terms of the Fourier transform of s(x).
In the oligotrophic regime, predation mortality evaluates to a power law
of the same form as Eq. (26), but now with coefficient
~
m ~ ^sðiðn 1ÞÞ ¼ ghN ^sðiðn 1ÞÞ:
~ ¼ ð1 f~ÞgN ½28
~ þh
gf
It is worth noting that, although the demographic parameters derived in this
section depend on the exponent l and coefficient N ~ characterising the com-
munity size spectrum, Eq. (17), the scale-free size distribution N(x) itself does
not enter the results. Hence, the results hold also when the community size spec-
trum follows a power law but is not apportioned to scale-free intrapopulation
size distributions. With such a situation in mind, it is instructive to consider
the boundary condition gj(m0j)Nj(m0j) ¼ Rj of the McKendrick–von Foerster
Equation, while making use of the scale-invariant expressions for the demo-
graphic parameters derived above but allowing arbitrary population structures
Nj(m0j). With m0j ¼ x0m∗j, this yields by Eqs. (12), (23), and (24):
E~g0 mnj Z 1
∗
½1 cðx0 Þ~g0 x0 m j Nj ðx0 m∗j Þ ¼
n n
Nj ðxm∗j ÞcðxÞxn dx: ½29
∗ 2x0 0
Observing that the maturation selection function for hatchlings c(x0) is
generally zero, and cancelling common factors on both sides of the equation,
this reduces to
Z
Ex1n 1
Nj ðx0 m∗j Þ ¼ 0 Nj ðxm∗j ÞcðxÞxn dx: ½30
2 0
The exponent 1 n of x0 decomposes into a contribution -1, arising

from simple book-keeping, and a contribution -n for the ratio of the rates of
metabolic activity of adults and hatchlings. Little more ecology enters this
power law, Eq. (30), for the scaling of the ratio of hatchling and adult abun-
dance with x0. It should therefore be robust with respect to variations in the
structure of the model and its solutions.
5.3. Scale-free size distribution

~ can now be obtained as the equilibrium
The scale-free size distribution N(x)
solution of the McKendrick–von Foerster Equation (15). Taking above re-
sults for growth and mortality into account,
@ h i
~ ðm=m Þ ¼ ð~ ~ ðm=m Þ,
~gðm=m∗ Þmn N mmn1 þ m0 mn1 ÞN ½31
@m ∗ ∗ ∗
or, substituting m ¼ m∗x and cancelling a factor m∗n 1,

@
~ ðxÞ ¼ ð~ ~ ðxÞ:
~gðxÞxn N mxn1 þ m0 ÞN ½32
@x
The equation is solved by
Z x
~0
N ~
m m0
~
N ðxÞ ¼ exp þ dx 0
½33
~gðxÞxn 1 ~gðx0 Þx0 ~gðx0 Þx0 n
for x < 1 and N(x)
~ ¼ 0 for x 1. The normalisation factor N ~0 is re-
~ ~ requires the integral in
lated to N via Eq. (18). Differentiability of N(x)
Eq. (33) to diverge at x ¼ 1, which is the case when the function c(x)
is Lipschitz continuous at the point c( 1) ¼ 1, as demanded above.
To understand the structure of solution (33), recall that for body sizes
much smaller than maturation size (x 1), all available energy is used for
growth (c(x) ¼ 0), so ~gðxÞ reduces to ~g0 by Eq. (24). The integral in
Eq. (33) can then be evaluated, giving

1 ~
m
~ ðxÞ / x ~g0 exp m ðx 1n
1Þ
N 0
ðforx 1Þ:
xn ~g0 ð1 nÞ
With n < 1, and therefore x1 n ! 0 as x ! 0
~ ðxÞ / xn~a ðforx 1Þ,
N ½34
where the constant
~
m
~a ¼ , ½35
~g0
is the specific physiological mortality (Beyer, 1989) of immature individuals.
5.4. Implications of the boundary condition (part I)

To assure demographic equilibrium, the boundary condition, Eq. (30), still
needs to be evaluated. Putting Nj(m) / N(m/m~ ∗ j) into this equation and
substituting Eq. (34) for the left-hand side, one obtains
xn~
0
a
/ x1n
0 : ½36
As x0 takes different values for different maturation size classes, existence
~ requires that
of a scale-free intrapopulation size distribution N(x)
~a ¼ 1: ½37
The mechanism by which this condition can be satisfied depends on the

size-spectrum regime. In the oligotrophic case, the results of Section 5.2
combine with a~¼ 1 to the condition
~ ¼ k
N , ½38
g½ða kh1 ÞI1 I2
def def
where I1 ¼^sðiðl 2ÞÞ and I2 ¼^sðiðn 1ÞÞ. Therefore, a~¼ 1 implies a con-
straint on physiological parameters or on the coefficient of the commu-
nity size spectrum N~ . For the eutrophic regime, Section 5.2 with a~¼ 1
implies
ða kh1 ÞI1 I2 ¼ 0: ½39
By varying the size-spectrum slope l, the value of I1 can be adjusted to satisfy

this condition. Hence, power-law size spectra impose a condition on the
size-spectrum slope in the eutrophic regime, and on absolute abundances
(with a slope fixed at l ¼ 2 þ q n) in the oligotrophic regime.
To interpret Eqs. (38) and (39) ecologically, observe first that a kh 1 is
the conversion efficiency at ad libitum feeding (assimilation minus metabolic
losses). Now, consider the special case of a sharply defined predator–prey size
ratio b, that is, s(x) ¼ d(x ln b), ^sðxÞ ¼ bix . Equation (39) is then
equivalent to a kh 1 ¼ bn 1b2 l, which has the form of an energy-
balance equation as encountered in early size-spectrum theory (e.g. Platt
and Denman, 1978): losses through conversion a kh 1 are matched by
a corresponding reduction of metabolic activity at the next trophic level
bn 1, corrected by the ratio of predator to prey biomass abundance
b2 l. In the oligotrophic regime, where hypothetical ad libitum feeding
leads to an energy surplus (a positive denominator in Eq. (38)), a power-
law size spectrum is attained with less-efficient feeding at lower
abundances. Remarkably, despite the fact that reproduction played a
crucial role in deriving Eqs. (38) and (39), the result could have been
obtained similarly when disregarding species identity and reproduction.
It is also noteworthy that, to the degree that (i) natural death is negligible
so that conversion efficiency equals the Lindeman’s trophic transfer effi-
ciency (commonly found to be 0.1) and (ii) Sheldon’s hypothesis l ¼ 2
holds, the energy balance discussed above necessarily leads to a predator–
prey size ratio b ¼ 0.11/(n 1) 1000, which is similar to observed values,
without any reference to mechanical constraints on feeding interactions.
One might therefore wonder whether the size of a fish’s gape is determined
by community-level constraints, rather than vice versa.
We can now ask under which conditions the integral in Eq. (18) converges
for small x, in other words, under which conditions the contribution of large
species to the abundance of small individuals in a community is small. By
Eqs. (34) and (37), this requires l > 1 þ n. Therefore, there is with n 3/4
little scope for size-spectrum slopes much smaller than the Sheldon slope l ¼ 2.
5.5. Total biomass per size class

From Eq. (16), the total biomass of species belonging to a small maturation
size interval [m∗; m∗þDm∗] can be computed for the scale-invariant solution
as VBtot ðm∗ ÞDm∗ , with
Z 1
Btot ðm∗ Þ ¼ mN ðm, m∗ Þdm
Zm01
¼ m ml1 ~ ðm=m Þdm
N ½40
∗ ∗
m0
¼ mlþ1
∗
B~tot ðm0 =m∗ Þ
and
Z 1
B~tot ðx0 Þ ¼ ~
xNðxÞdx: ½41
x0
~
From the asymptotic form of N(x), Eq. (34), it follows that the integrand
above scales as x n for small x, implying that the contribution from small
individuals to the total biomass is small as long as n < 1. The biomass of a
maturation size class or species is dominated by its adults.
5.6. Total metabolic loss rate per size class

Contrasting with population biomass, the rate of metabolic losses of a
maturation size class or species contains a large contribution from small in-
dividuals and diverges in the limit x0 ! 0. Specifically, the total losses kmn of
individuals belonging to a small maturation size interval [m∗; m∗þDm∗]
evaluates to VKtot ðm∗ ÞDm∗ , with
Z 1
Ktot ðm∗ Þ ¼ kmn N ðm, m∗ Þdm
Z 01
m
~ ðm=m Þdm ½42

¼ kmn ml1
∗
N ∗
m0
¼ mlþn
∗
K~ tot ðm0 =m∗ Þ
and
Z 1
K~ tot ðx0 Þ ¼ k ~ ðxÞdx:
xn N ½43
x0
By Eqs. (34) and (37), the integrand above is proportional to x 1 for

small x, implying a logarithmic divergence of the integral as x0 ! 0. It is
easily verified that a similar logarithmic divergence arises for biomass loss
by predation mortality and biomass gain by somatic growth. Consistency
of model solutions in the limit x0 ! 0 requires that these contributions
cancel each other out.
5.7. Implications of the boundary condition (part II)

The conditions derived in the foregoing section leave no free parameter that
could be adjusted to ensure that boundary condition Eq. (29) is satisfied not
only by order of magnitude but also exactly. Below, it is shown that exact
satisfaction is possible only under special, artificial assumptions, so deviations
of the population structure N(m, m∗) from the ideal scale-invariant form
m∗ l 1N(m/m∗) must be expected. Then, the qualitative nature of the
expected deviations is discussed.
Consider first the case of vanishing background mortality m0 ¼ 0 and as-
sume a~¼ 1 (i.e. m ~ ¼ ~g0 ) and scale-invariance: N0(m) / N(m/m~ ∗ j) for
1
m0 m m∗ and Nj(m) ¼ 0 otherwise. Define the function
Z x
1 0
EðxÞ ¼ exp 0 0
dx , ½44
1 ½1 cðx Þx
which satisfies the identify

Z Z " #
1 1
cðxÞ 1
EðxÞdx ¼ 1 EðxÞdx
x0 1 cðxÞ x0 1 cðxÞ
Z 1
dEðxÞ
¼ x EðxÞdx ½45
x0 dx
Z 1
d
¼ ½xEðxÞdx ¼ x0 Eðx0 Þ:
x0 dx
Using Eqs. (24), (33), (44), and (45), one can re-evaluate the general
boundary condition (29) as
~ 0 xn Z 1
N Ex1n
~ ðx0 Þ ¼
½1 cðx0 ÞN 0
Eðx0 Þ ¼ 0 N ~ ðxÞcðxÞxn dx
~g0 2 x0
~ 0 x0
1n Z 1
EN cðxÞ
¼ EðxÞdx
2~g0 x0 1 cðxÞ
EN~ 0 xn
¼ 0
Eðx0 Þ:
2~g0
½46
Hence, boundary condition (46) will be satisfied for scale-invariant so-

lutions only when E/2 ¼ 1. This requires an energetically impossible repro-
duction efficiency E > 1. When natural mortality (m0) is taken into account,
the value of the left-hand side in Eq. (46) would reduce further, requiring
even larger values of E. Perfect scale-invariant solutions are ecologically
infeasible, so what happens instead?
Losses caused by reproduction efficiencies E < 2 need to be compensated
by accelerated growth or reduced mortality, that is, reduced physiological
mortality over some phase of life history, typically in the immature
phase. In the current model, specific physiological mortality before maturation
depends only on body size, not on species identity. Therefore, if specific phys-
iological mortality is reduced for one species over a given body-size range, so
as to increase abundances by 2/E compared with the unmodified case, it will
lead to an increase of abundances by 2/E for all other species covering this
range too, effectively compensating their inefficiency in reproduction. Species
covering a larger body-size range can therefore exploit conditions generated
by other species contained within this range (this may be one of the reasons
why large body-size ranges are encountered in nature).
The resulting picture for the case of fish is illustrated in Fig. 3: as hatch-
ling size, m0, is approximately the same for all fish (Cury and Pauly, 2000),
independent of maturation size, specific physiological mortality will be re-
duced only within a size range covered by the smallest species. Larger species
are affected only in early life history. For most fish species, setting E ¼ 2 and
assuming the universal population structure given by Eq. (33) will therefore
yield legitimate approximations of the true population structure, provided it
can be shown that the effects of deviations from this structure at small body
sizes are negligible.
Hatchlings
Biomass density
1-n
10-12 10-10 10-8 10-6 10-4 10-2 100

Body mass (a.u.)
Figure 3 Schematic representation of intrapopulation size distributions. Body-mass
ranges are exaggerated. Curves show the density of a population's biomass along
the logarithmic size axis, given by m2Nj(m) up to a constant factor. Solid lines correspond
to scale-invariant distributions, which have a small-size tail scaling as m1–n (dash-dotted
line) by Eqs. (16), (34), and (37). Dashed lines represent conceivable corrections due to
reproductive losses. Because juvenile specific physiological mortality, which controls
the local slope of the curves, does not depend on species identity, corrections for all
species occur in the same size range.
This picture explains the observed discrepancies between the simulation

results of Hartvig et al. (2011) and their analytic equilibrium theory, which
predicts another value for a~. Specifically, the scenario sketched in Fig. 3
agrees with simulations by Hartvig et al. (2011) (i) in the predicted defor-
mation of population structures for the smallest individuals, (ii) in its predic-
tion for the scaling of offspring abundance with maturation size
(corresponding to a~¼ 1), (iii) in its prediction of power-law scaling of sur-
vival to a given size corresponding to a~¼ 1, after a short phase of lower mor-
tality. See Hartvig et al. (2011) for details.
Outside the range covered by fish, one can expect other regions on the
logarithmic body-size axis where a~ is depleted relative to 1, so as to compen-
sate for inefficient reproduction of the species overlapping these regions, and
values of a~ near 1 in between. The locations and relative proportions of these
regions on the body-size axis are currently unclear. On the condition that
most species in a community cover wide ranges in body size, few regions
of depleted a~ will be necessary to compensate for E < 2, and these will, for
most maturation size classes, fall outside their adult size ranges.
This completes the characterisation of the model’s steady state. In
what follows, the response of this steady state to perturbations will be eval-
uated in a linear approximation. To understand the impact of short regions
of depleted a~ on the logarithmic body-size axis, some critical calculations

below will be carried out along two tracks: first for the general case of arbi-
trary E 2, m0(m∗) and resulting forms for g(m, m∗), mp(m), and N(m, m∗), tak-
ing the considerations above into account, and then for the scale-invariant
case of E ¼ 2, m0(m∗) m∗, with scale-invariant N(m, m∗) and life-history pa-
rameters. It will be argued that, as far as regions of depleted specific physi-
ological mortality fall outside the adult body-size ranges of species, the
scale-invariant case is a reasonable approximation of the general case. To aid
orientation of the reader, the terms general and scale-invariant are italicised
in the subsequent Section 6 when used with these particular meanings.
Later, an additional simplification m0 ¼ 0 is introduced for the scale-invariant
case, which is then explicitly stated.
6. DERIVATION OF THE SPECIES SIZE-SPECTRUM MODEL
6.1. General framework

As an effective and accurate method to reduce models for the dynamics of
interacting structured populations to models in which each population is de-
scribed by a single variable only (e.g. population biomass), Rossberg and
Farnsworth (2011) introduce the QNA. The QNA for a system of S struc-
tured populations, described by vectors nj ¼ nj(t) of abundances by stage
(1 j S), satisfying dnj/dt ¼ Aj(n1, . . ., nS)nj with a density-dependent
population matrix Aj(n1, . . ., nS), can be carried out by following a simple
recipe. (1) Obtain an approximate description of the community steady state
and use it to construct for each species j an approximation of its steady-state
population matrix Aj , that is, a constant matrix of transition rates between dif-
ferent population stages in the community steady state. Ensure that, because
the system is in steady state and populations neither grow nor decay on
average, all matrices Aj have an eigenvalue zero. (2) Compute the eigenvector
wj and adjoint eigenvector vj corresponding to eigenvalue zero for each Aj ,
choosing normalisations such that the equilibrium population structure wj
corresponds to a population of unit size (e.g. 1 kg of biomass), and
that vTj wj ¼ 1. (3) Approximate the dynamics of population sizes, defined
by Bj(t) ¼ vTj nj(t), as dBj/dt ¼ vTj A(w1B1, ..., wSBS)wjBj, which is an ordinary
differential equation in the variables Bj. Using this result, approximate the full
community dynamics as nj(t) wjBj(t). The components of the vectors vj are
interpreted as the reproductive values of the corresponding population stage.
6.2. Operators and eigenfunctions

Applying the QNA to obtain a simplified description of the dynamics of the
density of individuals, N(m, m∗), requires adapting it to a continuum of life-
history stages indexed by body mass m and a continuum of populations
characterised by maturation size m∗. Functional analysis (Section 3) provides
the necessary formal tools. The first step of the recipe (approximation of the
steady state) has been completed in the Section 5. To obtain a description of
dynamics in a form appropriate for the second step, the McKendrick–von
Foerster Equation (15) is written as dN(m, m∗)/dt ¼ Lm∗N(m, m∗), where
the linear operator Lm , parametrised by m∗, is modified such as to include
∗
the production of hatchlings explicitly:
@ h i h i
Lm N ðm,m∗ Þ ¼ gðm,m∗ ÞN ðm, m∗ Þ mp ðmÞ þ m0 mn1 N ðm,m∗ Þ
∗ @m ∗
Z 1
E
þ dðm m0 Þ N ðm0 ,m∗ Þgr ðm0 , m∗ Þdm0 :
2m0 0
½47
Here, m0 is again understood to be a function of m∗. The boundary condi-
tion for N(m, m∗) then becomes N(m, m∗) ¼ 0 for any m < m0. The facts that
the last term correctly enforces the original boundary condition g(m, m∗)
N(m, m∗) ¼ Rm (with Rm given after obvious adjustments by Eq. (12)) is
∗ ∗
readily verified by integrating Eq. (47) over a small interval [m0 Dm/2;
m0 þ Dm/2].
The general steady-state McKendrick-von Foerster operator Lm∗ is
obtained from Lm∗ by replacing the functions g(m, m∗), gr(m, m∗), and
mp(m) with the results gðm, m∗ Þ, g ðm, m∗ Þ, and mðmÞ for a particular
r
general steady-state community size spectrum N ðmÞ ¼ N ðmÞ. The null-
eigenvectors required by the QNA, that is, the equilibrium population
structures Wm∗(m) satisfying Lm Wm∗ ðmÞ ¼ 0, can be obtained as
∗
Wm∗ ðmÞ ¼ B1

m Nðm, m∗ Þ, ½48
∗
where Nðm,m∗ Þ is N(m, m∗) evaluated at a general steady state (which may or
may not be scale-invariant), and a normalisation to unit biomass (actually
biomass density) is obtained by setting
Z 1
Bm∗ ¼ mNðm,m∗ Þdm: ½49
0
As for the scale-invariant case in Section 5.5, this integral is dominated by

adult individuals in the general case as well. Therefore, for maturation size clas-
ses m∗ where the general population structures Nðm, m∗ Þ do not differ much
from the scale-invariant case in the adult range of m, the scale-invariant form
of Wm∗ is a good approximation of general Wm∗ in the adult range. In the
scale-invariant case, Wm∗ is obtained from Eqs. (48), (16), (49), and (40) as
1
Wm ðmÞ ¼ m∗2 B~tot Nðm=m
~
∗
Þ for m m0 ½50
∗ 0 for m < m0 ,
~
with N(m/m ~
∗) given by Eq. (33) and Btot standing as shorthand for
~
Btot ðm0 =m∗ Þ.
For populations described by a finite number of stages (Section 6.1), the
steady-state population matrices Aj only have a finite number of eigenvalues.
The eigenvalue 0, assumed to be the one with the largest real part and to
have multiplicity one, is therefore always separated by a gap from the real
parts of the other eigenvalues. This leads to a separation between the time-
scales of intra- and interspecific population dynamics that is exploited in the
QNA. However, when populations are described by a continuum of life-
history stages, as is the case here, the corresponding linear operator Lm
∗
has an infinite number of eigenvalues. Thus, the existence of a spectral
gap between 0 and the other eigenvalues is not guaranteed. In Appendix,
the spectrum of operator Lm is studied for a numerical example of the
∗
scale-invariant case. It is concluded that indeed 0 is the unique eigenvalue
of Lm with largest real part, and that all other eigenvalues have real parts
∗
smaller than 1 (mortality of the largest individuals of the population).
These observations can plausibly be expected to generalise to the general class
of operators Lm considered here, so the eigenvalue zero will be separated
∗
from the subdominant eigenvalues by a gap of size mðm∗ =Þ þ m0 mn1 ∗
.
The resulting separation of timescales is estimated in Section 9.5.
To obtain the adjoint eigenvectors (here eigenfunctions), the adjoint lin-
ear operator Lþ m of Lm needs to be computed. Application of the method
∗ ∗
described in Section 3 yields
@V ðmÞ h i
Lþ
m V ðmÞ ¼ gðm,m∗ Þ mðmÞ þ m0 mn1 V ðmÞ
∗ @m ∗
EV ðm0 Þ
þ g ðm, m∗ Þ : ½51
r 2m0
Following the general prescription (Section 6.1), the reproductive value of

an individual of size m and maturation size m∗ is given by the solution Vm∗(m) of
Lþ
m V ðmÞ ¼ 0, subject to the normalisation condition hVm |Wm i ¼ 1. As, for
∗ ∗ ∗
any species of maturation size class m∗, the equilibrium density of individuals
along the m axis for a population of unit biomass is given by Wm∗(m), the equi-
librium density of reproductive value for a unit population along the m axis is
given by the product Vm∗(m)Wm∗(m). Multiplying this with the equilibrium
growth rate, gðm, m∗ Þ gives the equilibrium flow of reproductive value along
def
the size axis for a unit population, J ðmÞ¼ gðm,m∗ ÞVm∗ ðmÞWm∗ ðmÞ. It is
m
∗
readily verified using Lm∗Wm∗ ¼ Lmþ∗Vm ¼ 0 and Eqs. (47) and (51) that for
∗
m > m0
d h i
dJ EVm∗ ðm0 Þ
m∗
¼ gðm, m∗ ÞVm∗ ðmÞWm∗ ðmÞ ¼ g ðm,m∗ ÞWm∗ ðmÞ:
dm dm 2m0 r
½52
That is, until maturation J ðmÞ is constant and then it declines. Obviously,
m
∗
J ðmÞ ¼ 0 for m < m0 and m m∗/. Therefore, one can compute general re-
m
∗
productive values from a given general population structure Wm (m) by
∗
integrating Eq. (52) as
Z m =
1 ∗
Vm∗ ðmÞ ¼ g ðm0 , m∗ ÞWm∗ ðm0 Þdm0 , ½53
Cm∗ gðm, m∗ ÞWm∗ ðmÞ m r
where the correct normalisation hVm |Wm i ¼ 1 is assured by setting

∗ ∗
Z m = Z m =
2m0 ∗ 1 ∗
¼ Cm∗ ¼ g ðm0 ,m∗ ÞWm∗ ðm0 Þdm0 dm: ½54
EVm∗ ðm0 Þ m0 gðm, m ∗
Þ m r
An important observation now is that, because gðm, m∗ Þ scales as mn

with n < 1 for m m∗, and g ðm, m∗ Þ is localised near m∗, the integral
r
over m in Eq. (54) is dominated by contributions from large m. The value of
Cm therefore depends only on Wm (m) and the size spectrum near m∗, and
∗ ∗
these will often be well approximated by the scale-invariant forms.
If natural mortality (m0) is negligible in the scale-invariant case, Eq. (53)
evaluates by manipulations similar to Eq. (45) to the simple form
Vm∗ ðmÞ ¼ m: ½55
In this approximation, reproductive value therefore exactly equals body

mass. This result is most easily verified by directly confirming Lþ
m V ðmÞ ¼ 0
∗
and hVm |Wm i ¼ 1. The simplicity of this result allows carrying out the
∗ ∗
QNA analytically, which is done in the next section.
A generalisation of Eq. (55) to the case with natural mortality gives an
enhancement of reproductive value by an amount of the order of magnitude
mm0 = ~g0 for old individuals, and a corresponding proportional reduction for
all others. As this does not much affect the overall structure of Vm (m), nat-
∗
ural mortality is not considered further in detail below.
6.3. Reduced dynamics

Following the recipe of the QNA, define a reduced description B(m∗) of the
community state as
D E Z 1
Bðm∗ Þ ¼ Vm∗ jN ð,m∗ Þ ¼ Vm ðmÞN ðm, m∗ Þdm ½56
∗
0
for an arbitrary, time-dependent distribution of individuals N(m, m∗). In the

approximation that reproductive value equals body mass, the function B(m∗)
approximates the time-dependent distribution of biomass over maturation
body sizes. To the accuracy of the QNA, the dynamics of B(m∗) follow
1 @Bðm∗ Þ D E
¼ Vm∗ jLm∗ Wm∗
Bðm∗ Þ @t
Z 1 ( )
@ h i
¼ Vm∗ ðmÞ gðm,m∗ ÞWm∗ ðmÞ ½mp ðmÞ þ m0 m∗ Wm∗ ðmÞ dm ,
n1
0 @m
Z 1
EVm∗ ðm0 Þ
þ Wm∗ ðmÞgr ðm, m∗ Þdm
2m0 0
½57
where g(m, m∗), gr(m, m∗), and mp(m) are evaluated for a variable size spectrum
given by
Z 1
N ðmÞ ¼ Bðm∗ ÞWm∗ ðmÞdm∗ : ½58
0
By Eq. (57), one can read hVm |Lm Wm i as the momentary growth rate of
∗ ∗ ∗
biomass in maturation size class m∗.
In the scale-invariant case without natural mortality (m0 ¼ 0), the simple
results (50) and (55) for the null-eigenfunctions hold and the right-hand
side of Eq. (57) simplifies through integration by parts to
D E Z 1h iN~ ðm=m Þ
∗
Vm∗ jLm∗ Wm∗ ¼ gðm, m∗ Þ þ gr ðm,m∗ Þ mmp ðmÞ dm
m0 m 2B~tot
∗
Z 1h iN ~ ðm=m Þ
∗
¼ ðaf ðmÞh kÞmn mmp ðmÞ dm:
m0 m2 B~tot
∗
½59
The second step implies that the density-dependencies of investments into
somatic and reproductive growth are here equivalent in their population-
dynamic effects. This is remarkable when recalling that the causal chains
through which these effects are achieved are fundamentally different.
Careful inspection reveals that Eq. (59) holds to a good degree also in the
general case. To see this, observe first that, using Lþm∗ Vm∗ ðmÞ ¼ 0, Eqs. (51),
and (54),
" #
@Vm∗ ðmÞ aðm,m∗ Þ g ðm, m∗ Þ
¼ Vm∗ ðmÞ r
, ½60
@m m Cm gðm,m∗ ÞVm∗ ðmÞ
∗
h i
def
where aðm, m∗ Þ ¼ m m ðmÞ þ m0 mn1 ∗
=gðm,m∗ Þ is the steady-state specific
p
physiological mortality. Then integrate the somatic growth term in
Eq. (57) by parts, eliminate @ Vm /@ m through Eq. (60), and, finally, elim-
∗
inate E using Eq. (54), to obtain
D E Z 1 aðm,m∗ Þ aðm,m∗ Þ
Vm jLm Wm ¼ gðm, m∗ ÞVm ðmÞWm ðmÞ dm
∗ ∗ ∗
0
∗ ∗ m
Z 1 W ðmÞ "g ðm,m Þgðm, m Þ g ðm, m Þgðm,m Þ#
m r ∗ ∗ ∗ ∗
þ ∗ r
dm
0 C m gðm,m ∗
Þ
Z 1 ∗
aðm, m∗ Þ aðm, m∗ Þ
¼ gðm,m∗ ÞVm∗ ðmÞWm∗ ðmÞ dm
0 m
Z 1
aðm, m∗ Þ aðm, m∗ Þ
¼ J m ðmÞ dm þ h:o:t:
0 ∗ m
½61
h i
def
with aðm,m∗ Þ¼ m mp ðmÞ þ m0 mn1∗
=gðm, m∗ Þ. In the second step the sec-
ond integral vanishes because the term in brackets becomes zero when
inserting the definitions of g(m, m∗) and gr(m, m∗) from Eqs. (23) and (24).
Below, only effects linear in deviations of growth, reproduction and
mortality from the steady-state rates will be investigated, and to linear
order one can substitute g(m, m∗) by gðm, m∗ Þ in the remaining integral, so
g(m, m∗)Vm (m)Wm (m) reduces to J ðmÞ in the last line, up to higher-
∗ ∗ m
order contributions indicated by h.o.t.∗
Denote by Bðm∗ Þ the equilibrium values of the reduced dynamic vari-
ables B(m∗) defined in Eq. (56). To investigate the community response
to perturbations of this equilibrium state, the linearization of hVm |Lm Wm i
∗ ∗ ∗
for small deviations DBðm∗ Þ ¼ Bðm∗ Þ Bðm∗ Þ from this state is now con-
structed. Specifically, an integral kernel K(m∗, m∗0 ) is sought such that
D E Z 1
Vm∗ jLm∗ Wm∗ ¼ Kðm∗ ,m∗0 ÞDBðm∗0 Þdm0∗ þ h:o:t:, ½62
0
with h.o.t. denoting higher-order terms in DB. As hVm |Lm Wm i depends

∗ ∗ ∗
on B(m∗) only through the size spectrum N ðmÞ, the chain rule for functional
derivatives can be applied before using Eqs. (58) and (61) to obtain
D E
d Vm jLm Wm
∗ ∗ ∗
K m∗ ,m0 ∗ ¼
dBðm∗0 Þ
D E
Z 1 d Vm jLm Wm
∗ ∗ ∗ dN ðm0 Þ 0
¼ dm
0 dN ðm0 Þ dBðm∗0 Þ
Z 1Z 1 J
m ðmÞ daðm,m∗ Þ
¼ ∗ Wm0∗ ðm0 Þdmdm0
0 0 m dN ðm0 Þ
h i
Z 1Z 1 J ðmÞ d 1 c m=m∗ a m,m∗
m
¼ h ∗ i Wm∗0 ðm0 Þdm0 dm:
0 0 m 1 cðm=m Þ dN ðm0 Þ
∗
½63
This expression needs to be evaluated at the equilibrium state. By

multiplying a(m, m∗) with [1 c(m/m∗)] in the last step, a divergence of
a(m, m∗) at the size of the largest adults caused by cessation of growth,
Eq. (24), is suppressed. This effectively removes the distinction between so-
matic and reproductive growth. The division by [1 c(m/m∗)] in the first
factor of the integrand cancels with a corresponding factor entering J ðmÞ ¼
m∗
gðm,m∗ ÞVm∗ ðmÞWm∗ ðmÞ through gðm, m∗ Þ and, therefore, does not cause a
divergence for large adults. Equations (57), (62), and (63) together specify
the QNA for the general case.
To understand to what extent deviations from scale-invariance affect
Eq. (63), it is useful to investigate how the value of the integrand scales
for small m and m0 while m > m0(m∗), m0 > m0(m∗0 ). As J ðmÞ is constant for
m∗
small m, the first factor scales as m 1. The second factor describes

the dependence of the specific physiological mortality of individuals of
size m on the density of individuals of size m0 . The body-size ratios of
interacting individuals are constrained by the predator–prey size-ratio win-
dow s(x). The second factor will therefore be significantly different from
zero only when m and m0 are of roughly similar magnitude. For such a sit-
uation, the functional derivative operator d=dN ðm0 Þ shows the same scaling
behaviour as dðm m0 Þ=N ðm0 Þ, with d(m m0 ) denoting Dirac’s delta func-
tional (as can be verified by evaluating the derivative). The operand
[1 c(m/m∗)]a(m, m∗) will be of the order of magnitude of one, even
in the general case. In the scale-invariant case, the last factor grows for
small m0 as (m0 ) n 1 by Eqs. (50), (34), and (37). In the general case, it
may grow slower to accommodate inefficient reproduction (Section 5.7),
but it will never grow faster. After performing the integration over m0 ,
the integrand does therefore not increase faster than
m 1 ml m n 1 ¼ ml n 2 for small m. Small m dominates the
integral if the integrand increases faster than m 1, implying that l < 1 þ n.
This is unlikely to be the case, because it violates a condition for the
existence of a scale-invariant steady state (Section 5.4). Therefore, the
integrand is generally dominated by contributions where m and m0 are of
similar order of magnitude as m∗0 .
These considerations have two important implications. As explained in
Section 6.2, general J ðmÞ and Wm (m) can be approximated by their scale-
m ∗
invariant forms in the∗ adult range, at least as long as m∗ is not in a size
range of depleted specific physiological mortality. Further, J ðmÞ attains
m
in the juvenile range a constant value that depends only on the∗ life-history
parameter in the adult range. The first implication is therefore that, except
for cases where m∗ or m0∗ are in or near one of the regions of depleted specific
physiological mortality described in Section 5.7, the right-hand side of (63)
can be approximated by the corresponding scale-invariant form. Because
contributions from small m and m0 do not dominate the integral, a second
consequence is that the mathematical limit m0(m∗), m0(m∗0 ) ! 0 of infinitely
small offspring is regular and approximates the case of general but small
m0(m∗)/m∗. The calculations are therefore continued from here on using
the simplifying approximations of scale-invariant population structures with
m0(m∗) ! 0 for any m∗. To simplify matters further, natural mortality is not
taken into consideration (m0 ¼ 0), as it has only minor effects on dynamics
(see also Hartvig et al., 2011).
Therefore, starting from Eq. (59) and making use of Eq. (50) for scale-in-
variant population structures,
D E
d Vm∗ jLm∗ Wm∗
K m∗ , m0∗ ¼
dB m0∗
D E
Z 1 d Vm jLm Wm
∗ ∗ ∗ dN ðm0 Þ 0
¼ 0
dm
0 dN ðm Þ dB m∗0
8
Z 1 <Z 1 " # ~ 9
~ m0 =m0

df ðmÞ dm ðmÞ N m=m = N
∗ ∗
dm0 :
p
¼ ahmn m dm
0 : 0 dN ðm0 Þ dN ðm0 Þ m2∗ B~tot ; m0 2 B~tot
∗
½64
The functional derivatives of f(m) and mp(m) can be evaluated based on
results of Section 5.2. For the eutrophic regime, one obtains
df ðmÞ h 0 2lþnq4 m
¼ mm s ln 0 ½65
dN ðm0 Þ gf ~2 m
and

dmp ðmÞ h m0 1 m0
S ln ,l 4 þ n m0
lþn2
¼ s ln , ½66
~
dN ðm0 Þ f m I1 m
using I1 ¼ ^sðiðl 2ÞÞ as above and the abbreviation
Z 1
Sðy, cÞ ¼ xc sð ln xÞsðy þ lnxÞdx
Z 1
0 ½67
¼ eðcþ1Þu sðuÞsðy þ uÞdu:
1
In Eq. (66), the first term in brackets describes direct predation mortality,
the second term a release from predation pressure in the presence of other prey
of similar size. It follows from the condition gm2þql f ~ hmn , which defines
the eutrophic regime, that the functional derivative of f(m0 ) in Eq. (64) will
generally be negligible compared with that of mp(m0 ). It is discarded hereafter.
In the oligotrophic regime,
df ðmÞ gh m
0 qn
¼ m m s ln 0 ½68
dN ðm0 Þ ~ þh
2
m
gf
and, using Eq. (38),


dmp ðmÞ gh m0 k m0
S ln , q 2 m0 :
q
¼ s ln ½69
~ þh
dN ðm0 Þ gf m hðaI1 I2 Þ m
To simplify Eq. (64), define first the individual-level interaction kernel
m m0 lnþ2 dmp ðmÞ

n df ðmÞ
k0 ln 0 ¼ ahm m : ½70
m m dN ðm0 Þ dN ðm0 Þ
It follows from Eqs. (66) to (69) that the right-hand side of Eq. (70) does
indeed depend only on the ratio m/m0 . Further, let
~ 1
bðwÞ ~ ðew Þ
¼ B~tot e2w N ½71
describe the scale-free distribution of a species’
R 1biomass over the logarithmic
~
body mass axis for m0, x0 ! 0, normalised to 1 bðwÞdw ¼ 1. Equation (64)
can then be rewritten in terms of convolution integrals by performing the
substitutions m ¼ e wm∗ and m0 ¼ e um∗, which yield, after some
calculation,
Z 1Z 1 !
m∗
0
K m∗ , m ∗ ¼ m ∗ v ~ðw Þb
e k0 ðu w Þb
nu ~ u þ ln dw du
1 1 m0∗
!
h i m
¼ mv k∗b ~ ln ∗ ,
∗ m0 ∗
½72
with the abbreviations n ¼ 3 l n and
h i
~ ðuÞ,
kðuÞ ¼ enu k0 ∗ b ½73
where b~ ðuÞ¼def ~

bðuÞ:
In order to fully go over to logarithmic scales, introduce the scale-
invariant interaction kernel
h i
~
KðwÞ ~ ðwÞ,
¼ B~tot k ∗ b ½74
and a logarithmic mass axis u ¼ ln(m∗/M), where M denotes a unit mass

(e.g. M ¼ 1 g). Deviations b(u) of the distribution of biomass on the u-axis
from the power-law steady state are given by
bðuÞ ¼ Meu DBðMeu Þ: ½75
The density-dependent growth rate, given by Eq. (62), then becomes,

up to higher-order terms,
!
D E
1 v m∗
Vm∗ jLm∗ Wm∗ ¼ B~tot m∗ K~ ∗b ln
M
! ½76
mn2 m∗
¼ ∗
K~ b ln
B ðm Þ ∗
,
tot M ∗
where Eq. (40) was applied in the second step.

The response of size spectra to external perturbations is of great practical
interest: here, we concentrate on the effects of fishing. Assume a size-selective
fishing regime that enhances mortality of individuals by up to F over a range
centred at mF with logarithmic width sF; that is, next to predation and natural
mortality, there is additional mortality mF(m) ¼ FWsF(ln m/mF) with the
Gaussian window WsF(x) defined in Section 3. Putting this into Eq. (57)
and using Eqs. (50) and (71) leads, in the limit m0 ! 0, in addition to
natural community dynamics, to a pressure on populations with maturation
size m∗, corresponding to a rate of decline (dimension 1/Time):
Z 1 Z 1 !
m∗ ~
mmF ðmÞWm ðmÞdm ¼ F WsF u þ ln bðuÞdu
0
∗
1 mF
Z 1 !
m∗ ~
¼F WsF u þ ln b ðuÞdu ½77
1 mF
!
h
i m
¼ F WsF ∗b ~ ln ∗ :
mF
One can then, by applying Eqs. (76), (75), and B(m∗) ¼ DB(m∗) þ
Btot(m∗) to Eq. (57) and including of the effect of fishing, Eq. (77),
express system dynamics in response to fishing pressure that sets in at t ¼ 0
by the integro-differential equation
@bðuÞ
¼ ðMeu Þn1 K~ ∗b ðuÞ ðMeu Þ2l FðuÞYðtÞ, ½78
@t
where
h
i mF
~ ~
FðuÞ ¼ Btot F WsF ∗b u ln ½79
M
describes the fishing pressure, and Y(t) denotes the unit step function:
Y(t) ¼ 0 for t < 0 and Y(t) ¼ 1 for t 1. If fishing was specific to the matu-
ration size of species rather than to the size of individuals, Eqs. (79) would be
modified to
mF
FðuÞ ¼ B~tot FWsF u ln : ½80
M
Equation (78) represents the Species Size-Spectrum Model. It describes
the dynamics of deviations of the size spectrum from the steady state in the
linearised QNA. Linearised versions of other size-spectrum models pro-
posed in the literature would assume similar forms. The main difference be-
h theyi contain. In practice,
tween these models lies in the interaction kernels
~
the interaction kernel derived here, KðwÞ ¼ B~tot k∗b~ ðwÞ, is best evaluated
via its Fourier transform
^
KðxÞ ¼ B~tot k ^ ¼ B~tot k
^ðxÞbðxÞ ^
^0 ðx þ viÞbðx ^
viÞbðxÞ, ½81
which follows from Eqs. (73) and (74) and some manipulations of
convolution integrals.
Making use of Eq. (70), the preceding explicit formulae (65) to (69) for
the functional derivatives, and the observation that the Fourier transform of
Sðy,cÞ with respect to y is
^ cÞ ¼ ^sðx þ ðc þ 1ÞiÞ^sðxÞ
Sðx, ½82
give the Fourier transform of the individual-level interaction kernel

h ^sðx viÞ½^sðx∗ Þ∗

^0 ðxÞ ¼ ½^sðx Þ þ
k ∗ ∗ ½83
f~ ^sððl 2ÞiÞ
in the eutrophic regime and

ah2 g gh
^0 ðxÞ ¼
k ^sðx viÞ ½^sðx∗ Þ∗
~
ðgf þ hÞ 2 ~
gf þ h
½84
~h
g2 N
þ ^sðx viÞ½^sðx∗ Þ∗
~ þ hÞ2
ðgf
in the oligotrophic regime. The last expression can be brought into alterna-
tive forms by using the identity
gN~ k
¼ , ½85
~ þ h hðaI1 I2 Þ
gf
which follows from results in Section 5.
6.4. Food-web effects

Simulations show that Eq. (78) with the kernel given by (74) is structurally
unstable, as indicated in Section 5.1. As a result of combining coarse graining
with the mean-field approximation, the equation effectively describes com-
petition among a continuum of species along the species-size axis. This
destabilises the system by mechanisms similar to those involved in the scenar-
ios described by Pigolotti et al. (2007), leading ultimately to a breakup of the
continuum into a set of distinct species (isolated spikes on the size axis). In real
communities, this distinct set of species is already established and, as a result,
dynamics will be modified. Deriving these modifications of dynamics from
first principles would require a better understanding of food-web structure
and dynamics than we currently have. But the following heuristic arguments
suggest the general pattern that can be expected.
Consider perturbations of b(u) of the form i sin(xu þ c) with small ampli-
tude i and arbitrary phase c. For species randomly distributed along the u-axis
and sufficiently small wavelengths 2p/x, the perturbations received by each
species become uncorrelated. Such short-wavelength perturbations of the
size spectrum are therefore effectively equivalent to random perturbations
with a distribution independent of the wave number x and, relative to species
biomass, independent and identical among species. The relaxation of the
system from such perturbations to the equilibrium state (or the attractor)
can be expected to be rather complicated in detail and involves a range of
timescales (Rossberg and Farnsworth, 2011), but, as a simple model, linear
relaxation at a constant rate proportional with m∗n and independent of x
(if large enough) should provide an appropriate picture. Unfortunately, these
heuristic considerations do not provide a value for the relaxation rate, except
for the general principle that rates become larger for larger B~tot . Because the
community effect of perturbations of food-web nodes is typically diffuse
(Yodzis, 1998) and decays swiftly with the degree of separation from the
perturbed node (Berlowa et al., 2009), a periodic perturbation has effectively
a random effect when the wavelength 2p/x is small compared to the typical
distance in u among the main prey and predators of a species. As wavelengths
become larger—and wave numbers x smaller—these food-web effects will
gradually subside. Food-web effects
might therefore be modelled by adding
~
a correction of the form r Btot 1 expðsr x =2Þ to the Fourier transform
2 2
of the interaction kernel KðxÞ.^ The constant sr controls the cut-off-

wavelength for food-web effects. The relaxation-rate constant r has the same
dimensions as the search-rate coefficient g, and it may therefore be assumed to
be of comparable magnitude, presumably somewhat smaller (Rossberg and
Farnsworth, 2011).
Back-transforming, this leads to a corrected interaction kernel

nh i o
~
KðwÞ ¼ B~tot k∗b ~ ðwÞ þ XðwÞ ½86
with food-web effects being given by

1 w2
XðwÞ ¼ r pffiffiffiffiffi exp 2 dðwÞ : ½87
2psr 2sr
7. SOLUTION OF THE SPECIES SIZE-SPECTRUM MODEL

The factor (Meu)n 1 in Eq. (78) expresses the slowing-down of effec-
tive ecological activity of larger species attributable to allometric scaling of
metabolic rates. This factor makes the solution of Eq. (78), either numeri-
cally or analytically, difficult. Datta et al. (2010) and Capitán and Delius
(2010) avoided this problem by imposing conditions equivalent to n ¼ 1,
i.e. absence of allometric scaling of metabolism. Three analytical approaches
that do not require this constraint will be explored here.
7.1. Approximation for times shortly after onset of fishing

For the time before the onset of fishing, assume an unperturbed power-law
size spectrum, b(u) ¼ 0. Shortly after the onset at t ¼ 0, when b(u) is still close
to zero, the first term on the right-hand side of Eq. (78) will be small
compared with the second term. Disregarding the first term, the solution
of Eq. (78) can be approximated as b(u) (Meu)2 l F(u)t. This corre-
sponds to a depletion of populations in response to fishing without consid-
eration of density-dependent effects. Early density-dependent responses by
prey and predators can be obtained by putting this first-order approximation
into Eq. (78) and integrating in time, which leads to the second-order
approximation
u 2l 1 nþ1l ðn1Þu n

h
ð2lÞu
io
bðuÞ ¼ ðMe Þ FðuÞt M e K ðuÞ∗ e FðuÞ t2
2
þ h:o:t: ½88
Here, h.o.t. stands for higher-order terms in t, which could be computed
by iterating this procedure. However, it is quite likely that a series expansion
in t would not converge for any value of t. Inclusion of higher-order terms
would then not generally improve the approximation. It is valid only
asymptotically, as t ! 0. To describe the system’s long-term response to fish-

ing, other approaches are required.
7.2. Tentative steady-state solution

An idea that comes to mind for understanding the long-term dynamics of
Eq. (78) is to consider its steady-state (@b/@t ¼ 0). A formal steady-state so-
lution b(u) ¼ b0(u) is easily derived. Dividing the right-hand side of Eq. (78)
by (Meu)n 1 and Fourier transforming, it becomes
0 ¼ KðxÞ ^ þ viÞ,
^ b^0 ðxÞ M v Fðx ½89
^
with KðxÞ denoting the Fourier transform of KðuÞ ~ and

^ ~ ^ ^
FðxÞ ¼ Btot F W sF ðxÞbðxÞ exp ixln M the Fourier transform of F(u).
mF
^
As KðxÞ generally has no zeros on the real x axis, we can solve for
^ þ viÞ
M v Fðx
b^0 ðxÞ ¼ , ½90
^
KðxÞ
from which b0(u) is obtained by back-transforming. However, care must be
taken, because not all steady-state solutions b(u) necessarily have a Fourier
transform. To understand why, the analytic properties of KðxÞ ^ need to
be discussed.
^
7.3. The roles of complex poles and zeros of KðjÞ
Consider, for some complex x 2 C, the convolution integral
Z 1 Z 1
~
KðuÞ∗e ¼ixu ~
KðuÞe iðuuÞx
du ¼ e iux ~
KðuÞe ixu
du: ½91
1 1

The integral exists if and essentially only if KðuÞ ~ decays faster than
|eixu| ¼ e u Im{x} as u ! 1, with given by the sign of Im{x}. If the
integral exists, it equals eiux times the analytic continuation of the Fourier
^
transform KðxÞ into the complex plane. The range of Im {x} values over
which Eq. (91) converges determines a stripe in the complex plane, parallel
to and covering the real axis. Typically, as is the case here, the stripe is limited
^
by poles of KðxÞ, which correspond to exponentially decaying “tails” of
~
KðuÞ as u ! 1. To find these poles, recall that

^
KðxÞ ¼ B~tot k ^
^0 ðx þ viÞbðx ^ r B~tot 1 exp s2 x2 =2 , ½92
viÞbðxÞ r
^ has a pole at x ¼ (1 n)i because of the hatchling tail of N(x),

and that bðxÞ ~
Eq. (34), and possibly more poles farther from the real axis. This is the only
^
source of poles of KðxÞ. The Fourier transform k^0 ðxÞ of k0(w) is an entire
function by Eqs. (83) and (84) and the assumption that ^sðxÞ is an entire
function. In the oligotrophic regime KðxÞ ^ therefore has poles at
x ¼ (1 n)i and x ¼ (q n)i, corresponding to decays of KðuÞ ~ as e(1 n)u
(q n)u
for u ! 1 and as e for u ! þ1, and these two poles generally
limit the range over which the integral (91) exists. In the eutrophic
^
regime the pole x ¼ (1 n v)i of bðx viÞ coincides with a zero of k^0 ðx þ
^
viÞ by Eq. (83), eliminating the corresponding pole of KðxÞ, but other poles
^
of bðx viÞ may persist. Denote by X the maximal (open) stripe in the
complex plane parallel to the real axis for which KðxÞ ^ is analytic
(X ¼ {x : (1 n) < Im{x} < q n}in the oligotrophic regime).
^
Now, if x0 2 X is a complex zero of KðxÞ, and A0 is any complex num-
ber, then with every solution b0(u) of Eq. (78), b(u) ¼ b0(u) þ A0 exp(ix0u) is,
by Eq. (91), a solution of Eq. (78), too. Such additional exponential terms do
not have finite Fourier integrals for any x and therefore cannot be found
using Eq. (90). The correct choice of these corrections to the Fourier trans-
form solution b0(u) of (78) follows, as for corresponding problems in physics
(Jackson, 1962), from causality considerations: the corrections should be
added if localised perturbations trigger waves or fronts that increase in mag-
nitude as they propagate towards |u| ! 1. However, because of the factor
(Meu)n 1 in Eq. (78), standard methods for deciding when to make these
corrections cannot be applied directly. Instead, this problem will here be
(partially) solved by first investigating explicitly time-dependent solutions
of Eq. (78).
7.4. Analytic approximation of time-dependent

size-spectrum dynamics
Above, it was explained how complex zeros of KðxÞ ^ lead to complications
when solving Eq. (78). The idea of the approach described in this section is
that, under certain conditions, the dynamics of b(u) can indeed be dominated
by the effects of these zeros. For example, it is evident from Eq. (90) that the
Fourier transform b^0 ðxÞ of the steady-state solution b0(u) derived there gen-
erally has poles wherever KðxÞ^ has zeros. These poles are likely to have
strong effects when the inhomogeneity (the fishing term) in Eq. (78) is
not too broadly spread out on the logarithmic species size axis, that is, if
its Fourier transform is not too localised along the real x axis. Specifically,
the spread sF should be smaller than the typical logarithmic predator–prey
size ratio, that is, fishing should not target more than about two trophic
levels. This is often the case in practice.
^
Firstly, only zeros of KðxÞ within the stripe X are considered. Denote by
x1, x2, .. . an enumeration of these zeros (which may be finite or infinite in
number). To isolate the effect of these zeros on the time-dependent solution
of Eq. (78), we seek a representation of the solution in the form
X
bðu, tÞ ¼ bc ðu,tÞ þ aj ðu, tÞ expðixj uÞ, ½93
j
with the functions bc(u, t) and aj(u, t) to be specified below. The condition
that b(u, t) is real-valued requires that aj(u, t) ¼ (ak(u, t))∗ when xj ¼ xk∗
(the asterisk ∗ denotes complex conjugation).
Eliminating b in Eq. (78) by Eq. (93), one obtains an equation for bc,
@bc ðu, tÞ
¼ ðMeu Þn1 K~ ∗ bc ðu, tÞ þ ðMeu Þn1 Cðu, tÞ, ½94
@t
with
XZ 1
u n
Cðu, tÞ ¼ ðMe Þ FðuÞYðtÞ þ ~ uÞaj ðu, tÞeixj u du
Kðu
j 1
X ½95
u 1n @aj ðu, tÞ ixj u
ðMe Þ e :
j
@t
The condition for choosing the functions aj(u, t) is now that they should
vary slowly in u and t in a sense explained below, and that, even in the limit
t ! 1, the Fourier transform b^c ðx,tÞ of bc(u, t) exists and can be continued
analytically into X. This implies that, even in the limit t ! 1, bc(u, t) decays
~
at least as fast as KðuÞ for u ! þ 1 and –1, that is, bc(u, t) is at least as
~
localised as KðuÞ. The impacts of fishing on species much smaller or larger
than the target species should then be completely captured by the functions
aj(u, t).
The strategy to achieve this goal is to assure that the Fourier transform
^ tÞ of C(u, t) has zeros at the points xk 2 X at all times, so as not to excite
Cðx,
these modes in bc(u, t). This gives the condition
^ k , tÞ,
0 ¼ Cðx ½96
^ tÞ to be small also in the vicinity of these points. An
and one can require Cðx,
interesting implication of this condition stems from the Fourier transform of the
convolution integral in Eq. (95). Let z be an arbitrary complex number in X.
~
Using information aboutR 1the exponential decay of KðuÞ as u ! 1 derived
~ ^
above and the fact that 1 KðuÞ expðixj uÞdu ¼ Kðxj Þ ¼ 0, one finds that
Z 1 Z 1
e izu ~ uÞaj ðu, tÞeixj u du du
Kðu
1 1
becomes, after multiplying and dividing by eixju

Z 1 Z 1
¼ eiðxj zÞu ~ uÞaj ðu, tÞeixj ðuuÞ dudu,
Kðu
1 1
after integrating by parts in u

Z 1 Z 1Z uu
@aj ðu, tÞ
¼ e iðxj zÞu ~
KðwÞe ixj u
dw du du,
1 1 1 @u
after changing order of integration and substituting u ! u þ u
Z 1Z 1 Z u
@aj ðu, tÞ
eiðxj zÞðuþuÞ ~
KðwÞeixj w
dw du du,
1 1 1 @u
and after factoring out a constant
Z 1 Z u Z 1
iðxj zÞu ~ ixj w iðxj zÞu @aj ðu,tÞ
¼ e KðwÞe dw du e du :
1 1 1 @u
If xj 6¼ z, the first factor evaluates, integrating by parts in u, to

Z 1 Z 1
1 iðxj zÞu ~ ix 1 ~
e KðuÞe j u
du ¼ eizu KðuÞdu
i z xj 1 i z xj 1
½97
K^ ðzÞ
¼ ,
i z xj
whereas for xj ¼ z, it becomes, again integrating by parts,

Z 1 Z
~ d 1 ixu ~ 0
ueixj u KðuÞdu ¼ i e KðuÞdujx¼xj ¼ iK^ ðxj Þ, ½98
1 dx 1
with the prime denoting the derivative with respect to the argument. There-
fore, in the vicinity of the points z ¼ xk, the Fourier transform of the con-
volution integrals is either zero (or small) by Eq. (97) or approximated by
Eq. (98) when xk ¼ xj.
For reasons to become clear later, define
0
vk ¼ ið1 nÞM n1 K^ ðxk Þ: ½99
With respect to a Fourier transform near xk, the sum over convol-
ution integrals in Eq. (95) is then equivalent to a term
(1 n) 1vkeixkuM1 n @ak(u, t)/@u. One can now attempt to choose the
functions ak(u, t) such that, with this substitution, the right-hand side of
Eq. (95) for C(u) vanishes identically for all u. This leads, for each k, to
the condition
@ak ðu, tÞ vk euðn1Þ @ak ðu, tÞ

¼ ðMeu Þ2l eixk u FðuÞYðtÞ
@t 1n @u
X
iðxj xk Þu @aj ðu,tÞ
e : ½100
j6¼k
@t
An alternative route to Eq. (100), currently under development, employs

a multiple-scale singular perturbation formalism (Kevorkian and Cole,
1996). In this approach, the functions ak(u, t) vary formally on slow spatial
and temporal scales, admitting a gradient expansion of the convolution,
of which the derivative in u above is the lowest-order contribution.
Now, a new independent variable z ¼ eu(1 n) is introduced, so, because dz/
du ¼ (1 n)eu(1 n) ¼ (1 n)z, one gets @ f/@ u ¼ (@ f/@ z)(dz/du) ¼ (1
n)z @ f/@ z for any function f(u). Writing Ak(z, t) ¼ ak(u, t), Eq. (100) then
becomes

@Ak ðz,tÞ @Ak ðz, tÞ 2lixk lnz
¼ vk M z
2l 1n F YðtÞ
@t @z 1n
X iðxj xk Þ @Aj ðz,tÞ
z : ½101
j6¼k
1n @t
When reading this equation as

@Ak ðz, tÞ @Ak ðz,tÞ
¼ vk þ Hk ðz,tÞ, ½102
@t @z
it formally describes fronts that are generated by the inhomogeneity Hk (z, t)
and move away from it at a velocity vk. However, complicating matters, the
velocity vk can here be a complex numbers. Yet, for Hk(z, t) analytic in z,
one can write a formal solution of Eq. (102),
Z 1
Ak ðz, tÞ ¼ Hk ðz vk t, t tÞdt, ½103
0
which is easily verified. The solution is causal: A (z, t) depends on Hk(z0 , t0 )

only for times t0 t. To understand this result better, consider first p
the hy-
ffiffiffiffiffiffiffiffiffiffi
pothetical special case that Hk ðz, tÞ ¼ expððz z0 Þ2 =2s2 ÞYðtÞ= 2ps2 ,
with arbitrary s, z0 > 0. Then

YðtÞ z z0 z z0 vk t
Ak ðz, tÞ ¼ erf pffiffiffi erf pffiffiffi : ½104
2vk 2s 2s
The error function erf(x) for complex arguments x approaches 1 ¼ signRe

{x} for large |x| when |Re{x}| > |Im{x}|, but for |Re{x}| < |Im{x}|,
it oscillates heavily. It follows that, as Hk(z, t) converges to d(z z0)Y(t) for
small s, one can approximate
1
8Ak ðz, tÞ vk YðtÞ½Yðz z0 Þ Yðz z0 Refvk gt Þ
< þvk1 for Refvk g > 0,t > 0 and z0 < z < z0 þ Refvk gt,
½105
¼ vk1 for Refvk g < 0,t > 0 and z0 þ Refvk gt < z < z0 ,
:
0 otherwise
when |Re{vk}| > |Im{vk}| 0. This describes a sharp front moving at ve-
locity Re{vk} away from z ¼ z0. The heavy oscillations in z and t arising
when |Re{vk}| < |Im{vk}| violate the assumptions that Ak(z, t) varies
slowly along z and bring Ak(z, t) outside the range of validity of
Eq. (102). Generally, one would assume such oscillations to be suppressed
by higher-order derivative terms not included in Eq. (102), resulting, again,
in a front moving at velocity Re{vk}. Below, Eq. (105) will be used to
approximate the response of Ak(z, t) to any sharply localised perturbation d-
(z z0)Y(t) “switched on” at t ¼ 0, as long as Re{vk} 6¼ 0. The case Re
{vk} ¼ 0 does not generally arise and is not considered here. The approxi-
mate response of Ak(z, t) to general Hk(z, t) can be obtained as a linear com-
bination of solutions of the form (105).
According to Eq. (105), @ Ak/@ t is localised at the tip of the travelling
fronts generated by inhomogeneities elsewhere on the z-axis. The last term
in Eq. (101) describes secondary excitations of fronts/waves by fronts per-
taining to other zeros xj. In the singular perturbation formalism, it arises as
a higher-order correction. Its effect can be observed in simulations of the
system (see Section 8.4.1) but are disregarded in the following analytic
calculations, for simplicity. The term containing the fishing pressure F(˙)
in Eq. (100) is then the only contribution to Hk(z, t) and, using approxima-
tion (101), one obtains
Z
M 2l YðtÞ z 2lixk ln y
Ak ðz, tÞ y 1n F dy ½106
vk z1 1n
where z1 ¼ max(0, z Re{vk}t).
On the logarithmic maturation size scale, this becomes
Z
M 2l YðtÞð1 nÞ u
ak ðu, tÞ eðvixk Þw FðwÞdw, ½107
vk u1
with u1 ¼ u1(u, t) ¼ (1 n) 1 ln[e(1 n)u Re{vk}t] if the expression in

brackets is positive, and u1 ¼ 1 otherwise. For fishing pressure specific
to maturation size rather than individual size (i.e. using Eq. (80)), the integral
can be evaluated analytically, leading to
pffiffiffi " #
pB~tot M 2l FsF YðtÞð1 nÞ ðv ixk Þ2 s2F
ak ðu,tÞ pffiffiffi exp ðv ixk ÞuF þ
2vk 2
8 2 3 2 39
< ðv ixk Þs2F þ uF u1 5 ðv ixk Þs2F þ uF u5=
erf 4 pffiffiffi erf 4 pffiffiffi ,
: 2sF 2sF ;
½108
where uF ¼ ln(mF/M) and u1 is as defined above. Once the front generated by

the onset of fishing has run over a given point u on the logarithmic species-
size axis, which happens at time t (e(1 n)u e(1 n)uF)/Re{vk}, the
expression in braces evaluates to 2 sign Re{vk}, and the amplitude of the
community response to fishing is controlled by the constant of dimension
Mass/Volume given by the first two factors in Eq. (108). The first factor ac-
counts for the available biomass (BtotM2 l of dimensions Mass/Volume),
the fishing pressure applied to it (FsF dimension 1/Time), and the rate at
which this pressure is diverted to other size classes (vk, dimension 1/Time).
The exponential function in the second factor combines the allometric scal-
ing laws of response rates (1 n) and available biomass (2 – l, recall
v ¼ 3 l n), a weight and phase factor exp(ixkuF) attributable the mod-
ulation of the kth mode, and a correction factor relevant when fishing is
spread out over a broad body mass range.
The time-dependent community response to size-selective fishing can
be approximated analytically by inserting Eq. (108) into Eq. (93) and setting
the localised core contribution bc(u, t) to zero. According to this approxima-
tion, fronts travelling towards smaller body sizes (Re{vk} < 0) accelerate and
reach u ¼ –1, that is, z, m∗ ¼ 0, after the finite time t ¼ e(1 n)uF/|Re
{vk}| ¼ (mF/M)(1 n)/|Re{vk}|. Fronts travelling towards larger body sizes
(Re{vk} > 0) decelerate logarithmically on the u-axis. All fronts travel at
constant speed on the z ¼ (m∗/M)(1 n) axis. If Re{vk} and Im{xk} have
the same sign, the front described by ak(u, t)exp(ixku) travels into the di-
rection in which | exp(ixku)| decreases. The contribution from ak(u, t)exp
( ixku) is then bounded and its Fourier transform exists. In the opposite case
(sign Re{vk} 6¼ sign Im{xk}), the contribution by ak(u, t)exp(ixku) grows
beyond all bounds as time proceeds. These contributions are of the ampli-
fying type not captured by the Fourier transform steady-state solution
Eq. (90). This phenomenon is closely related to what the physics and engi-
neering literature calls a convective instability. It is characterised by the fact that,
although the system response to a pulse perturbation remains finite at any
fixed point on the u-axis, it grows beyond all bounds applicable uniformly
for the entire infinite u-axis.8 In reality, logarithmic size u is limited from
both above and below, and the community response to perturbations re-
mains finite. Convective instabilities are distinguished from absolute instabil-
ities, where perturbation responses grow beyond all bounds for some given
value of u. Such instabilities are conceivable also for size spectra and can be
observed in simulations for specific parameter values, but the analysis de-
scribed here is unable to capture them. An adaptation of standard methods
for identifying absolute instabilities (e.g. Akhiezer and Polovin, 1971) to the
particular form of Eq. (78) is therefore highly desirable.
^
7.5. Extension of the method to all zeros of KðjÞ
It turns out that the approximation constructed above can be improved fur-
ther by including also the zeros of KðxÞ ^ outside the stripe X, although some
care needs to be taken. For zeros xk outside the strip, the exponentially
^
decaying tails of KðuÞ are “flat” compared with the rate of increase or de-
ixk
crease of e . The tails can therefore mediate long-range interactions and
delocalise the dynamics of the modes ak(u, t). An analysis of the special case
^
where KðxÞ is the ratio of two linear polynomials (not discussed here) reveals
that this can lead to the suppression of convective instabilities even when
sign Re{vk} 6¼ sign Im{xk}: the response of ak(u, t) is then in the direction
on the u-axis opposite to Re{vk}. To take this into account, the following
heuristics suppressing convective instabilities are employed. In the rare cases
8
As here press perturbations are considered here rather than pulse perturbation, not all unbounded re-
sponses necessarily correspond to convective instabilities.
where Re{vk} and Im{xk} have opposite signs for zeros xk 2 = X, the value of
u1 in Eq. (107) or (108) is, for all times t > 0, set to þ1 for Re{vk} > 0 and to
–1 for Re{vk} < 0. Because of the rapid decay of these modes along u, the
discontinuity of b(u) in t resulting from this approximation is hardly
noticeable. If Re{vk} and Im{xk} have the same signs, ak(u, t) is
computed according to Eq. (107) or (108) without modifications.
Although convective instabilities for zeros outside X have not been
observed in simulations, there is some risk that exceptions to these
heuristics exist.
Provided the extension of this method to all zeros xk of KðxÞ~ is successful
^
so that limt!1 Cðxk , tÞ ¼ 0, one can expect that, by Eq. (94), the Fourier
transform of the residual bc(u, t) converges to an entire function as t ! 1.
That is, | lim t ! 1bc(u, t)| decays faster than exponentially for u ! 1.
The steady-state residual lim t ! 1bc(u, t) unaccounted for by the approxima-
tion developed above is then, in this sense, strongly localised near the size
class targeted by fishing. When using the approximation method below,
the contribution by bc(u, t) is not included.
8. COMPARISON OF ANALYTIC THEORY AND

SIMULATIONS
8.1. A specific parametrisation

To visualise typical responses of size spectra to fishing and to test the analytic
predictions of Section 7.4 by comparison with simulations, specific choices
for the free model parameters need to be made. This includes, in particular,
choices for the predator–prey size-ratio window s(x) and the maturation se-
lection function c(x). Standard values used for the scalar parameters are listed
in Table 3. The choices follow Hartvig et al. (2011), and the reader is re-
ferred to their work for detailed motivations. All body masses are measured
in units of the body mass class targeted by fishing (M ¼ mF). To report sim-
ulation results independent of the specific choice of mF, time is measured in
units of the approximate age of the targeted size class at maturation (i.e. the
age when m ¼ m∗ ¼ mF), computed for c(x) ¼ 0 and m0 ! 0 for simplicity.
The growth trajectories of individuals then follow dm=dt ¼ ~g0 mn and time
1
to maturation is Tmat ¼ m1n
F ~g1
0 ð1 nÞ . For mF ¼ 1 kg, this equals 3.0 years
with standard parameters. Fishing pressure F was fixed so that, in response to
the onset of fishing, species of size mF initially decline at a rate
F ¼ 0.1 Tmat 1.
Table 3 Standard parameters used in simulations

Symbol Value Unit Description
n 3/4 Exponent of physiological activity
h 85 g1–n yr–1 Coefficient of maximal food intake
1–n –1
k 10 g yr Coefficient of metabolic loss rate
q 0.8 Exponent of search/attack rate
g Cancels out g1–q m–3 yr–1 Coefficient search/attack rate
a 0.6 Conversion efficiency
b 100 Preferred predator–prey mass ratio
ss 1 Width of predator–prey size-ratio window
–1
F See text yr Fishing mortality
sF ln 10 Width of harvested size range
0.25 Maturation over asymptotic mass
sr 0.5 Cut-off length for food-web effects
r 0.5g g1–q m–3 yr–1 Strength of food-web effects
The parameters values r ¼ 0.5g and sr ¼ 0.5 of the heuristic submodel for
food-web effects where chosen, following the reasoning of Section 6.4,
according to the observation that g is the only other model parameter of the same
dimension as r, so that both might be of similar magnitude, and that exp(sr)
corresponds to the typical mass ratio between prey in the diet of a consumer.
8.1.1 Choice of the predator–prey size-ratio window

With b standing for the preferred predator–prey mass ratio (not to be
~
confused with the size distribution bðwÞ) and x for the actual logarithmic
predator–prey mass ratio, the predator–prey size-ratio window is chosen
following Hartvig et al. (2011) as a Gaussian window:
" #
ðx lnbÞ2
sðxÞ ¼ exp : ½109
2s2s
Its Fourier transform is

2 2
1=2 s x ix
^sðxÞ ¼ ð2pÞ ss exp s b : ½110
2
8.1.2 Choice of the reproduction-selection function and its implications

Hartvig et al. (2011) showed that with a reproduction-selection function of
the form
cðxÞ ¼ ðxÞ1n , ½111

growth of individuals follows a von Bertalanffy trajectory. The coefficient
stands for the ratio of maturation size to asymptotic size. Hartvig et al. (2011)
multiplied this form with a smoothed step function to describe the onset of
maturation at x ¼ 1, but here I stick with Eq. (111) for the sake of analytic
tractability. In fact, population structures resulting from c(x) with or with-
out this additional factor do not differ much.
For the special case that the allometric exponent for the metabolic loss
rate is exactly n ¼ 3/4, and that background mortality is negligible
(m0 ¼ 0), the scale-free population size structure N(x) ~ (Eqs. 33 and 24)
with c(x) given by Eq. (111), and m ~ ¼ ~g0 (i.e. a~¼ 1) evaluates to
h i3
N~ 0 1 ðxÞ1=4
N~ ðxÞ ¼ ½112
4
~g0 ½1 1=4 x7=4
for x 1 and N(x)
~ ¼ 0 otherwise. This result follows after verifying that
E(x), defined by Eq. (44), is given by E(x) ¼ [1 (x)1/4]4[1 1/4] 4x
(compute E0 (x)/E(x) to see this).
From Eq. (112) one gets, according to Eq. (41),
Z 1
~ ~
Btot ¼ Btot ð0Þ ¼ ~ ðxÞdx
xN
0
~0
N ½113
¼ 4 :
~g0 ½1 1=4 1=4
Consequently, the distribution of a species’ biomass over the logarithmic size

axis is given, following Eq. (71), by
h i3
~
bðwÞ ¼ ðew Þ1=4 1 ðew Þ1=4 ½114
~
for w ln and bðwÞ ¼ 0 otherwise. This function has the Fourier
transform
^ ¼ ix
bðxÞ : ½115
ði þ xÞði þ 4x=3Þði þ 2xÞði þ 4xÞ
Next to the pole at x ¼ i/4, expected from the general asymptotic form
~ ^
of N(x) for small x, Eq. (34), the analytic continuation of bðxÞ has poles also
at x ¼ i/2, x ¼ 3i/4, and x ¼ i. Interestingly, all poles are located at
multiples of i(1 n).
As Eq. (113) contains the unknown N ~0, it does not give a numerical
value for B~tot . To compute B~tot , use Eq. (71) to express N(x) ~
~ by bðwÞ in
~
Eq. (18). The resulting equation can be solved for Btot , to obtain
N~
B~tot ¼ : ½116
^
bðiðl 2ÞÞ
~ ¼ 1 by normalisation, the two coefficients B~tot and N~ are there-
As bð0Þ
fore nearly identical when l 2.
8.2. Simulation technique

Simulation of the Species Size-Spectrum Model, Eq. (78), over a large range
in u is difficult because, by the factor (Meu)n 1, a broad range of timescales
has to be covered. The u-axis was discretized to 256 points at distance 0.5,
ranging from u ¼ umin ¼ 128/3 to u ¼ 254.5/3. This corresponds to a range
from about 10 19M to 1037M in maturation size, which is much larger than
the size range covered in real size spectra. The reason for choosing this broad
range is to isolate the effects of scale-invariant dynamics, which can be
approximated analytically, from conceivable complications due to boundary
effects. To gain some qualitative understanding of the modifications of
dynamics that could result from boundary effects, a variant of the model
(constrained-domain variant) was simulated where Eq. (78) was applied
only over the interval euM ¼ 10 15M to 103M, and b(u) ¼ 0 held fixed
otherwise.
The right-hand-side of Eq. (78) was evaluated using a pseudospectral
method: the convolution was evaluated in Fourier space by multiplication
^ with the result for KðxÞ,
of bðxÞ ^ Eq. (92), with either Eq. (83) or (84). To
reduce aliasing, the u-axis was extended by another 256 points for
this operation. To suppress numerical instabilities developing at the lower
edge of the u-axis, a stabilising extra term 8(Meu)n 1b(u)/{1 þ exp
[0.6(u umin ln b)]} was added to Eq. (78). Over most of the u-axis, this
term has no effect. The discretized system was then solved using the implicit
ODE solver CVODE included in the SUNDIALS package (Hindmarsh
et al., 2005). This solver automatically adjusts the approximation order and
the step size to achieve a prescribed accuracy (here 10 4 per step). In
addition, upper limits on step size, scaling as the square-root of time since the
start of simulations, were imposed to suppress numerical instabilities.
8.3. Numerical evaluation of the analytic approximation

The analytic formula for the Fourier transform of the interaction kernel,
~
KðxÞ, was converted into a subroutine which takes arbitrary complex x
as arguments and outputs KðxÞ. ~ ~
The zeros of KðxÞ in the vicinity of
x ¼ 0 were then determined using a simple secant search algorithm, initiated
at all points on a grid with resolution p/(8 ln b) spanning the range
0 Rex 8p/ln b, |Im x| 4p/b. It was verified that enlarging this
range did not change the results markedly. Zeros found repeatedly were dis-
~
carded. The derivatives of KðxÞ at the zeros, required to evaluate the analytic
approximation of dynamics, are most easily computed numerically.
The programming language used (Cþþ) did not include an implemen-
tation of the error function for complex arguments in its mathematical library.
This function is required when computing the analytic approximation of size-
spectrum dynamics using Eq. (108). The function was therefore implemented
using the method proposed by Hui et al. (1978). Alternatively, the integrals in
Eq. (107) could have been evaluated numerically. This second approach has
the advantage of being applicable for arbitrary external perturbations F(w) but
is slightly more computation-intensive.
8.4. Case studies

8.4.1 Standard parameters
Equation (78) for the oligotrophic case was solved with standard parameters
both numerically and in the analytic approximation described in Section 8.1.
The evolution of the system state is shown in Fig. 4. One observes the
formation of two trophic cascades, one downwards from mF to smaller spe-
cies, the other one upwards, towards larger species. In a later phase, an
upward-moving front emerges that bends the size spectrum downward
and carries an additional downward cascade in its wake.
The initial dynamics are not reproduced well by the analytic result in
Eqs. (93) and (108). The theory overestimates the initial decay of the
targeted size class (which is well described by the small-t approximation,
Eq. (88)) and is late in predicting the formation of a weak downward
trophic cascade. The analytic solution predicts the timing of the
saturation of the downward cascade around 3.3–10 Tmat reasonably well.
It makes an excellent prediction of its final, saturated state.
0.2
0
0.1
-0.2
0 -0.4
t = 0.01Tmat -0.6 4
t = 10 Tmat
-0.1
-0.8
-0.2 -1
0.2
0
0.1
-0.2
0 -0.4
t = 0.1Tmat -0.6 4.5
t = 10 Tmat
-0.1
-0.8
-0.2 -1
0.2
Relative change in biomass or abundance
0
0.1 -0.2
0 -0.4
t =Tmat -0.6 5
t = 10 Tmat
-0.1
-0.8
-0.2 -1
0.2
0
0.1
-0.2
0 -0.4
t = 3.3Tmat -0.6 5.5
t = 10 Tmat
-0.1
-0.8
-0.2 -1
0.2
0
0.1
-0.2
0 -0.4
t = 10Tmat -0.6 6
t = 10 Tmat
-0.1
-0.8
-0.2 -1
0.2
0
0.1
-0.2
0 -0.4
t = 33Tmat -0.6 6.5
t = 10 Tmat
-0.1
-0.8
-0.2 -1
0.2
0
0.1
-0.2
0 -0.4
t = 100Tmat -0.6 7
t = 10 Tmat
-0.1
-0.8
-0.2 -1
0.2
0
0.1
-0.2
0 -0.4
t = 333Tmat -0.6 7.5
t = 10 Tmat
-0.1
-0.8
-0.2 -1
-20 -10 -20 -10
10 10 100 1010 1020 1030 1040 10 10 100 1010 1020 1030 1040
Relative species size m* /mF Relative species size m* /mF
Figure 4 Time-dependent response of a size spectrum to size-specific exploitation

targeting maturation sizes around mF, for the oligotrophic regime in the standard par-
ametrisation described in Section 8.1. Solid lines: simulations. Dashed lines: analytic the-
ory. Tmat is the approximate age at which individuals maturing at mF reach this size. In
the second column, corresponding to later stages, the vertical axis is expanded.
The upward cascade evolves much slower than the downward cascade.
This is mostly a consequence of the allometric scaling of biological rates, en-
capsulated in the factor (Meu)n 1 in Eq. (78). The analytic approximation
captures reasonably well the timing of the formation of the first maximum
of the upward cascade around 10–33 Tmat, the formation of the second min-
imum around 100 Tmat, and the full emergence of the second maximum
around 333 Tmat. Thereafter (second column in Fig. 4), the two trophic cas-
cades have mostly stabilised.
What follows is the propagation of a downward-bending front to larger

species sizes. Continuation of the simulation until t ¼ 107.5Tmat and over an
(unrealistically) large body-size range demonstrates three general facts.
Firstly, the analytic theory makes a good prediction of the velocity of the
downward-bending front on the u-axis. Secondly, the modulations behind
the front travel in its wake, and, after sufficient waiting time, subside (com-
pare, e.g. the simulation results at the point m/mF ¼ 1010 for t ¼ 105Tmat and
t ¼ 107.5Tmat). Presumably, these secondary excitations of the size spectrum
would be captured when including the neglected sum over j in Eq. (100) as
an additional inhomogeneity contributing to Hk(z, t). Thirdly, whereas in
the analytic approximation the front quickly becomes sharp as it moves
to larger u (as does the front of the upward trophic cascade), it is blurred
in simulations. This indicates the presence of additional diffusive effects
along the u-axis that were not captured in the present approximation.
The case displayed in Fig. 4 is a typical example for the degree of agree-
ment between simulations and analytic approximations. Despite many dif-
ferences in detail, the analytic approximation captures the main features and
the times of their emergence.
8.4.2 The constrained-domain variant

In Fig. 5, it is shown how the response of the size spectrum changes in sim-
ulations when dynamics are constrained to a narrower domain. The dynamic
domain was chosen so that with mF ¼ 1 kg it corresponds approximately to
the realised range of species sizes in marine communities. The resulting
modification of dynamics evident in Fig. 5 can be interpreted as a minimal
adaptation (a reflection on the upper boundary?) required to keep b(u) con-
tinuous at the domain boundaries. Otherwise, the effect on dynamics is
small, at least for the case considered here. Small dynamic effects of the
boundaries do not imply that their effects on the steady-state size spectrum
will be small.9 The latter are discussed briefly in Section 9.6.
9
The correct form of the boundary conditions that represent the upper and lower size limits of real com-
munities in the Species Size-Spectrum Model is unknown. In an approximation consistent with the
model, one can expect them to take the form of a set of inhomogeneous linear conditions on b(u)
(Cross and Hohenberg, 1993). A particular, stationary solution of the model compatible with these
inhomogeneous boundary conditions represents the effect of “press perturbations by the boundaries”
discussed in Sec. IX.F below. These perturbations will be stronger the larger the inhomogeneities in the
boundary conditions. After subtracting this particular solution from b(u), the reminder is constrained by
a set of homogeneous boundary conditions. Of these, the condition applied here (b(u) ¼ 0 for u outside
the domain) is one example. As it is independent of the magnitude of the inhomogeneities, its effect on
the dynamics inside the domain can be small even when boundary perturbations are strong.
0.2
0.1
0

-0.1 t = 0.1Tmat
-0.2
0.2
0.1
0
-0.1 t =Tmat
-0.2
0.2
0.1
0
-0.1 t = 10Tmat
-0.2
0.2
0.1
0
-0.1 t = 100Tmat
-0.2
-18
10 10-12 10-6 100 106
Relative species size m* /mF
Figure 5 Effect of constraining the domain of the dynamic response of the size spec-
trum to the size range indicated by the bar above. Simulations with standard parame-
ters in the oligotrophic regime as in Fig. 4, at four points in time t. Solid lines:
constrained-domain variant. Dashed line: unconstrained variant for comparison.
8.4.3 Characterisation of size-spectrum dynamics by the zeros of KðjÞ ^

^
The solution of Eq. (78) is controlled by the Fourier transform KðxÞ of the
interaction kernel KðuÞ~ entering Eq. (78), specifically by its complex zeros
and its first derivatives at these points. A good qualitative understanding of
the solution of Eq. (78) can therefore be gained already by studying the
geometry of these zeros in the complex plane. For the standard parameter
set used here, the zeros of KðxÞ ^ and its analytic continuation are marked
as open circles in Fig. 6. The arrow attached to each open circle indicates
the argument of the first derivative of KðxÞ^ at this point (an arrow pointing
straight right would mean a real, positive first derivative). The filled circles
represent poles of KðxÞ. ^ Figure 6B offers a broader view of the same
configuration.
Results derived in Section 7.4 translate into the following geometric pic-
^
ture: zeros of KðxÞ located below the real axis (Im{x} ¼ 0) correspond to
modulations or bending of b(u) that increases towards larger u (larger body
sizes), and vice versa for zeros above the real axis. A non-modulated (bending)
contribution corresponds to a zero on the imaginary axis (Re{x} ¼ 0).
A 1 B
3
2
0.5
Cascade up Cascade up 1
l-2
Im{x}
Im{x}
0 Bending 0
Cascade down Cascade down
-1
-0.5
-2
-1 -3
-1 -0.5 0 0.5 1 -3 -2 -1 0 1 2 3
Re{x} Re{x}
0
^
Figure 6 (A) Locations of zero (open circles) and poles (closed circles) of KðxÞ in the complex plane as well as the argument of K^ ðxÞ at the
zeros (arrows), annotated with the corresponding perturbation responses. Standard parameters. (B) gives a wider perspective.
All other zeros always come in pairs (x ¼ xr þ ixi), guaranteeing that the
sum of all contributions approximating b(u) by Eq. (93) is real-valued. When
expressing deviations from the unperturbed equilibrium state in terms of rel-
ative changes in biomass or abundance (rather than by absolute differences in
biomass density), modulations and bending increase towards positive u if the
corresponding zero is located below the line Im{x} ¼ l 2, and vice versa.
The direction into which the front corresponding to each of these
contributions propagates is determined by the vertical component of the ori-
entation of the attached arrows. Arrows pointing downwards correspond to
fronts propagating into the direction of positive u (upward cascades), that is,
towards larger body size. Arrows pointing upwards correspond to fronts
propagating in the direction of smaller body size (downward cascades).
Combining the positions of zeros with the orientations of arrows, it follows
that for zeros with arrows pointing towards the line Im{x} ¼ l 2 the
corresponding modulations of relative abundance (or non-modulated bend-
ing) become smaller away from the size class targeted by fishing, or any other
press perturbation. Effects on relative abundance corresponding to zeros
with arrows pointing away from the line Im{x} ¼ l 2 increase as they
propagate along the size axis. Such contributions correspond to the ampli-
fying contributions mentioned at the end of Section 7.4. For the standard
parameter set, the only contribution of this type is the upward-moving front
of size-spectrum bent.10
Among zeros with attached arrows pointing towards the line Im{x} ¼
l 2, their contributions decay the faster along the u-axis the farther they
are from the line Im{x} ¼ l 2. Further, zeros at some distance from Im
{x} ¼ l 2 generally appear to be of the convectively stable type (see
Figs. 6B, 7B, and 8B). Often, good qualitative images of the system
response to press perturbations can be obtained from considering just a
few zeros close to the line Im{x} ¼ l 2. In Fig. 6A, the five zeros of
^
KðxÞ closest to this line have been annotated.
10
The fact that in the oligotrophic regime there is always a purely imaginary zero corresponding to an
amplifying, upward-moving front follows from the observation that KðxÞ ^ is real along the imaginary
^
axis, the existence of the two poles of KðxÞ at x ¼ (1 n)i and x ¼ (q n)i, their respective sign struc-
tures, and continuity considerations. The sign structure follows heuristically from the fact that KðuÞ ~
describes feeding on smaller species and predation by larger species. The corresponding analytic ar-
gument makes use of the observation that the denominator in Eq. (46) is positive, so aI1 I2 > kh 1I1,
a comparison of Eqs. (83) and (84), and the observation that Eq. (83) has a zero coinciding with the
pole at x ¼ (q n)i.
Relative change
0.4
0.2
0
-0.2
-0.4 t = 103.5Tmat
-0.6
10-20 10-10 100 1010 1020 1030 1040
Relative species size m* / mF
B
1.5
0.5
Im{x}
-0.5
-1
-1.5
-1.5 -1 -0.5 0 0.5 1 1.5
Re{x}
Figure 7 Perturbation response of the size spectrum (A) and graphic characterisation of
^
KðxÞ (B) for the case discussed in Section 8.4.4, which leads to an amplifying upward
trophic cascade. As in Fig. 4, solid and dashed lines in panel (A) correspond to simulation
and analytic approximation, respectively. As in Fig. 6, open and closed circles in (B) cor-
0
^
respond to zeros and poles of KðxÞ respectively, and arrows to the argument of K^ ðxÞ at
the zeros.
8.4.4 An amplifying upward trophic cascade

When changing model parameters, other types of dynamics can be found.
Figure 7A displays simulation and analytic results when, compared with the
previous case, the preferred predator–prey mass ratio is increased from
b ¼ 102 to b ¼ 105. The upward cascade now becomes amplifying, which
means that the modulated system response becomes stronger towards species
sizes larger than mF (Fig. 7). Figure 7B displays the configuration of zeros and
^
poles of KðxÞ in the complex plane. The amplifying upward cascade is gen-
erated by the pair of zeros near 0.5 with attached arrows pointing away from
the line Im{x} ¼ l 2.
Relative change
5
-5
10-20 10-10 100 1010 10

20
1030 1040
Relative species size m* / mF
B
1.5
0.5
Im{x}
-0.5
-1
-1.5
-1.5 -1 -0.5 0 0.5 1 1.5
Re{x}
Figure 8 Perturbation response of the size spectrum (A) and graphic characterisation of
^
KðxÞ (B) for the case discussed in Section 8.4.5, which leads to an amplifying downward
trophic cascade. Symbols as in Figs. 4 and 6. As in Fig. 6, solid and dashed lines in
(A) correspond to simulation and analytic approximation, respectively. As in Fig. 6,
open and closed circles in (B) correspond to zeros and poles of KðxÞ, ^ respectively,
0
and arrows to the argument of K^ ðxÞ at the zeros.
8.4.5 An amplifying downward trophic cascade

Finally, an example for the eutrophic regime is considered. In addition to
setting b ¼ 105 as in the previous example, standard parameters are modified
by increasing the width of the predator–prey size-ratio window (Eq. 109)
from s ¼ 1 to s ¼ 3. The coefficient of the allometric scaling law for respi-
ration is increased from k ¼ 10 g1 n year 1 to k ¼ 49.09 g1 n year 1, giving
a size-spectrum slope of l ¼ 2.1 via the constraint Eq. (39). For ecological
consistency, all biomasses and abundances must be sufficiently large to fully
satiate all consumers. For the system response to the fishing regime used
here, this is clearly not the case. As can be seen in Fig. 8A, the predicted
linear response grossly exceeds changes by 100% in biomass. Realistically,
one should therefore apply less fishing pressure. Reducing fishing pressure
by, say, one-tenth would yield exactly the same response as shown in Fig. 8,
only with a ten times lower amplitude. Fishing pressure was retained at the
standard value in Fig. 8A to allow easy comparison with the previous
examples.
Now, the downward cascade becomes amplifying: abundance modu-
lations increase towards lower species sizes. As the downward cascade
propagates at constant speed on the m∗1 n-axis, it reaches the lower
end of the simulated range after finite time (about 100 Tmat). The simula-
tion results differ from the analytic predictions for very low species sizes
because of the numerical stabilisation applied near the lower boundary
(see Section 8.2). The occurrence of a convectively unstable downward
cascade can be predicted from the fact that in Fig. 8B there is one pair
of zeros above the line Im{x} ¼ l 2 with attached arrows pointing away
from it. The observation that the amplitude of the system response here is
considerably larger than in the previous cases might be related to the fact
that these two zeros are both close to other zeros, which could lead to small
0
^
derivatives of KðxÞ at these zeros (when KðxÞ ^ has a double zero, K^ ðxÞ
vanishes), small values of |vk|, and hence large modulation amplitudes
by Eq. (108).
Comparing Figs. 7A and 8A, one can see that in the eutrophic regime the
^
pole of bðx viÞ at x ¼ (l 2)i has disappeared. It has been cancelled in
^
KðxÞ by the zero of k^0 ðx þ viÞ, Eq. (83), at the same position. This zero re-
sults from the interplay between predation mortality (first term in Eq. (83))
and release from predation (second term in Eq. (83)) under ad libitum
feeding. The pole of bðx^ viÞ is a result of taking the limit m0, x0 ! 0
in Section 6.3. When regularising bðxÞ, ^ for example, by fixing x0 at some
^
small but positive value, bðx viÞ would instead attain a large, but finite,
0
^
value at x ¼ (l 2)i. Then KðxÞ at this point would be zero and K^ ðxÞ large,
corresponding to perturbation responses in the form of small amplitude, rap-
idly upward-moving fronts, by Eqs. (99) and (108). These fronts represent the
mechanism by which the overall abundances of larger species are adjusted to
match those of smaller species in the eutrophic regime. In the limit m0, x0 ! 0,
this mechanism degenerates to an immediate, rigid regulation, concealing the
regulating dynamics.
9. IMPLICATIONS, DISCUSSION, AND OUTLOOK
9.1. The final steady state of a perturbed species size

spectrum
The theory of size-spectrum dynamics developed in Section 8 now allows
the problem of computing the steady-state solution reached long after ini-
tiating a size-specific press perturbation to be revisited. As argued in Sec-
tion 7.2, this solution must be of the form
X
bðuÞ ¼ b0 ðuÞ þ Aj eixj u , ½117
j
where b0(u) is given by its Fourier transform in Eq. (90) and Aj are constants
to be determined. By comparing with the related decomposition Eq. (93) of
the time-dependent solution and taking the limit t ! þ 1, one obtains
X
lim bc ðu, tÞ ¼ b0 ðuÞ þ Aj lim aj ðu, tÞ eixj u : ½118

t!þ1 t!þ1
j
The fact that b0(u) has a Fourier transform and the conjecture that
lim t ! þ 1bc(u, t) is strongly localised (Section 7.5) and can now be used
to compute the coefficients Aj. Consider first those cases where | exp(ixju)|
diverges as u ! þ 1 (i.e. where Im{xj} < 0). The conditions on bc(u) and
b0(u) require that
Aj ¼ lim aj ðu, tÞ: ½119
t, u!þ1
For fronts propagating to negative u, that is, Re{vj} < 0, this implies
Aj ¼ 0. In the opposite case, Re{vj} > 0, application of Eqs. (107) and
(99) gives
M 2l ð1 nÞ ^
Aj ¼ Fðxj þ viÞ
vj
^ j þ viÞ ½120
iM v Fðx
¼ 0 :
K^ ðxj Þ
The corresponding results in the case Im{x} > 0 has the opposite sign
for Aj. The close similarity between this expression for Aj and Eq. (90)
for b^0 ðxÞ has the interesting consequence that the final steady state b(u) ¼
lim t ! þ 1b(u, t) can be computed by formally evaluating the inverse Fourier
transformation, Eq. (1), of b^0 ðxÞ,
Z
1
bðuÞ ¼ b^0 ðxÞeixu dx: ½121
2p C
However, the path of integration C in the complex plane must be chosen
such that, in the geometric picture introduced in Fig. 6A, it remains above
all zeros xj (open circles) with attached arrows pointing upwards, and be-
low all zeros with attached arrows pointing downwards. Using Eq. (120)
and the residue theorem of functional analysis, it is easily verified that the
additional terms resulting form deviations of this path C from the real axis
are exactly the non-zero contributions Ajeixju in Eq. (117).
9.2. Distribution of individual sizes in the final steady state

From b(u), the final deviations of the distribution of biomass over logarith-
mic species sizes from the unperturbed distribution, one can compute the
corresponding deviations c(u) of the distribution of biomass over logarithmic
individual sizes by a convolution with the intraspecific mass distribution
h i
cðuÞ ¼ b ~ b ðuÞ. For simplicity, only those situations are considered here
∗
where Im{xk} > (1 n) for all k for which Ak 6¼ 0. Graphically, this means
that all zeros (open circles) with attached arrows pointing away form the
dash-dotted line must lie above the highest pole (filled circle) in the lower
half plane. In all scenarios considered above (Figs. 6–8), this is the case.
Using Eq. (117) and again invoking the residue theorem, one can then
evaluate
h i X
cðuÞ ¼ b ~ b0 ðuÞ þ ^ j ÞAj eixj u
bðx
∗
Z j
½122
1
¼ ^c 0 ðxÞe dx,
ixu
2p C
^ b^0 ðxÞ and the path C taken identical to that in Eq. (121).
with ^c 0 ðxÞ ¼ bðxÞ
Interestingly, when considering the case of fishing specific to the size of in-
dividuals (rather than species) and ignoring food-web effects, Eqs. (90), (79),
and (92) evaluate ^c 0 ðxÞ to the simple expression
^
bðxÞM v^
Fðx þ viÞ
^c 0 ðxÞ ¼
^
KðxÞ
^
bðxÞM v~
Btot F W ^
^ sF ðx þ viÞbðx viÞðM=mF Þixv
¼ ½123
B~tot k ^
^0 ðx þ viÞbðx ^
viÞbðxÞ
!ixv
^ sF ðx þ viÞ M
FM v W
¼ :
^0 ðx þ viÞ
k mF
This result depends on ecological detail only through the feeding inter-
actions described through k ^0 , not through the life-history characteristics
of species. These enter c(u) only through path C determined by KðxÞ. ^
Formally, c(u) is a steady-state solution of the balance equation
@cðuÞ mF
¼ ðMeu Þn1 K~ 1 ∗c ðuÞ B~tot FðMeu Þ2l WsF u ln , ½124
@t M
with K~ 1 ðuÞ ¼ B~tot evu k0 ðuÞ (so that K^ 1 ðxÞ ¼ B~tot k
^0 ðx þ viÞ). Making use of
~
the definition of k0(u), Eq. (70), K 1 ðuÞ can be expressed as
m
df ðmÞ dmp ðmÞ

K~ 1 ln 0 ¼ B~tot m 2l
ah m 1n
, ½125
m dBðm0 Þ dBðm0 Þ
were BðmÞ ¼ mN ðmÞ denotes the density of biomass on the (linear) body-
size scale. The two terms in brackets describe effects on individuals of size m
by trophic interactions with individual of size m0 . The leading factor
B~tot m2l scales as the size-dependence of the biomass of affected individuals.
Oddly, Eq. (124) therefore describes the mass balance in a size-structured
community of individuals that feed upon each other but, akin to microor-
ganisms, essentially only to multiply their numbers rather than to grow in
size—despite the fact that the equation was obtained from a model for
interacting highly size-structured populations. The fact that the true
steady-state c(u) solves Eq. (124) justifies the use of simplifying pictures
where “large species eat small species” in verbal arguments. However,
over-interpretation of such pictures or corresponding numerical models
can be fatal: the dynamic response of c(u) to fishing pressure predicted by
h i via the
the Eq. (124) will generally be very different from that predicted
Species Size-Spectrum Model, Eq. (78), by setting cðuÞ ¼ b ~ b ðuÞ. There
∗
can be differences in the timing of events, as demonstrated in Section 9.4,
when the propagation velocities Re{vk} of perturbation responses (see
Eq. (105)) have different magnitudes but the same signs in both cases, and
the dynamic selection of entirely different steady states when some velocities
Re{vk} have different signs.
9.3. The population-level predator–prey size-ratio window

Models of interacting size-structured populations often invoke an
individual-level predator–prey size-ratio window such as the function
s(w) entering the model of Hartvig et al. (2011). On the other hand, models
of unstructured populations differentiating species by size (e.g. Brännström
et al., 2010) often depend on a population-level predator–prey size-ratio
window S(w) that describes the size-dependence of the amount consumed
of a species of size m∗ by another species of size m0∗ ¼ ewm∗. The QNA in the
form developed in Section 6 allows the derivation of S(w) from s(w).
The computation is analogous to the derivation of the interaction kernel
~
KðuÞ from individual-level interactions, but now contributions related to
active and passive feeding are handled separately. Consider the special case
of a linear functional response (h ! 1) in the oligotrophic regime. The con-
tribution of predation mortality to k0(w), Eq. (70), then simplifies to gs(w).
Verifying that K(m∗, m0 ∗) specifies, according to Eqs. (57) and (62), a rate of
change (dimension 1/Time) normalised to the biomass density of
the affecting species, and replacing k0(w) by gs(w) in the formula for
K(m∗, m0 ∗), Eq. (72), one obtains—in the mean-field approximation
underlying this calculation—the rate of population decay of a species of
size m∗ resulting from consumption by a species of size m0 ∗ with biomass
density B0 as gm0∗q 1S(ln(m0∗/m∗))B0 , where
h i
SðwÞ ¼ s∗b ~ ðwÞ, with b
~ b ~ def vw ~ ð1qÞw ~
∗ v v ¼ e bðwÞ ¼ e bðwÞ: ½126
The quantity gm0∗q 1 was factored out to make this result comparable with
the corresponding formula for s(w), that is, Eq. (13) with N ðmÞ expressed in
terms of biomass density BðmÞ ¼ mN ðmÞ.
Conversely, the rate of population growth of a species of size m0∗ resulting
from consumption of a species of size m∗ with biomass density B evaluates
to agm0∗q 1S(ln(m0∗/m∗))B. Therefore, surprisingly, the population-level
assimilation efficiency is here identical to the individual-level assimilation
efficiency a.
The convolutions in Eq. (126) generally need to be evaluated numeri-
cally, for example using Fourier techniques. The resulting form of S(w)
for standard parameters is shown in Fig. 9. However, some general charac-
teristics of S(w) can be derived directly from Eq. (126). Recalling the
Prey = predator
Individual level
0.8 Population level
Preference (a.u.)
0.6 Small prey Large prey
0.4
~r -0.05
0.2
~r 0.25
0
1012 1010 108 106 104 102 100 10-2 10-4
Predator–prey mass ratio r
25 20 15 10 5 0 -5 -10
w = In(r)
Figure 9 Comparison between the predator–prey size-ratio windows at individual level
s(w) and at population level S(w). The mass ratio r ¼ ew is the body-size ratio m0 /m for
s(w) and the species-size m0∗ /m∗ for S(w), with the prime denoting the predator. To dis-
play the curves from the predator's perspective, the horizontal axis is inverted. Curves
correspond to standard parameters with x0 ! 0. For finite parent-offspring size ratios,
the tails of S(w) will be truncated.
assumption that s(w) decays faster than exponentially for w ! 1 (Section 4)

~
and the observation that bðwÞ / eð1nÞw as w ! 1 (see Eqs. (34), (37), and
(71)), it follows immediately that (i) S(ln(m0∗/m∗)) / (m0∗/m∗)1 n for
predator species smaller than their prey, (ii) S(ln(m0∗/m∗)) / (m∗/m0∗)q n
for prey species much smaller than their predators, and (iii) typical s(w),
~
localised much sharper than intraspecific size structures bðwÞ, have little
influence on the structure of S(w) apart from determining a preferred
predator–prey size ratio.
The conclusion that the population-level predator–prey size-ratio win-
dow is wide appears at odds with the conclusion reached analytically by
Nakazawa et al. (2011), consistent with empirical analyses by Woodward
and Warren (2007) (see also Gilljam et al., 2011; Woodward et al.,
2010b), that the mean predator–prey size ratio at population level must
be smaller than that at individual level. However, the paradox is easily
resolved by noting that Nakazawa et al. (2011) and Woodward and
Warren (2007) weighted all individuals equally when averaging over
populations, whereas here each individual is weighted by its body mass as
a proxy for reproductive value. With this modification, the analysis by
Nakazawa et al. (2011) does indeed lead to the opposite conclusions: the
mean population-level predator–prey size ratio is larger than that at

individual level. This is the more adequate choice. As demonstrated by
Rossberg and Farnsworth (2011) analytically and through simulations,
weighting individuals within populations by reproductive value leads to
better predictions of community dynamics than equal weighting.
9.4. Slow and fast responses to size-selective fishing

The timescale for the long-term community responses to fishing is deter-
mined by the constants vk entering Eq. (107), which are defined as
0
vk ¼ ið1 nÞM n1 K^ ðxk Þ. These depend on ecological details through the
0
factor K^ ðxk Þ, given by Eq. (92).
If intraspecific biomass distributions over the logarithmic mass scale bðwÞ~
^
are wide and smooth, then their Fourier transforms bðxÞ are narrow on the
Re{x}-axis, as exemplified by Eq. (115). As a result, all xk (except for the
purely imaginary zero) are likely to lie outside the region where bðxÞ^ is large.
Typically, this is the case when the logarithmic predator–prey mass ratio ln b
~
is small compared with the width of bðwÞ, evidenced by cannibalistic feed-
0
ing. This leads, by Eq. (92), to small K^ ðxk Þ and a sluggish formation of tro-
phic cascades compared, for example, with expectations from the naive
0
picture of Eq. (124)—at least as long as K^ ðxk Þ is not dominated by food-
web effects through the second term in Eq. (92). Expressed in ecological
terms, trophic cascades form slowly because population-level predator–prey
size-ratio windows are broad: even species differing in maturation sizes by
exactly the predator–prey mass ratio b do not form a simple predator–prey
pair, rather they interact through a mixture of predator–prey, prey–predator,
and competitive relationships resulting from the tremendous ontogenetic
growth of fish and other aquatic organisms.
For the purely imaginary zero corresponding to size-spectrum bending,
the situation is opposite. As shown in Figs. 6 and 7, this zero of KðxÞ^ is typ-
ically located near the pole of KðxÞ^ that corresponds to the first pole of
^
bðx ^
viÞ. Because of the resulting rapid transition of KðxÞ from zero to
0
^
infinity, K ðxk Þ is generally large for this zero. The downward bending of
the size spectrum for large species is therefore fast, at least when compared
with the biological rates of these species (despite being slow in absolute
terms, see Fig. 4). The underlying ecological mechanism, which follows im-
mediately from back-tracing how bðx ^ viÞ enters this result, is that larger
species are being depleted directly through fishing mortality of
their juveniles, even if the proportion of these in the catch—which scales
as (mF/m∗)1 n—is relatively low. The mechanism is further amplified by a

depletion of the food resources of juveniles of large species.
The effects of intraspecific size structure on response times can be
demonstrated by a comparison of simulations of the Species Size-Spectrum
Model with simulations of Eq. (124), which does not account for intraspe-
cific size structure. To stabilise solutions of Eq. (124), some technical
adjustments are required (caption of Fig. 10). As seen in Fig. 10, the initial
response of the two systems to exploitation targeting a narrow range of body
sizes is very different. Formation of the downward cascade is by a factor 3–10
slower in the full model than in Eq. (124). Depletion of larger organisms,
however, proceeds by about a factor 3 faster for the reasons explained above.
Yet, the equilibrium states approached by both systems are very similar:
indeed, by the arguments of Section 9.2, they are possibly the same.
9.5. Neutrality and the validity of the QNA

Perfect ecological neutrality in the sense of Hubbell (2001) is a situation of per-
fectly even competition. Apart from drift driven by stochastic processes (which
are not modelled here), communities of neutrally competing species are demo-
graphically stable for any combination of their relative abundances. In situa-
tions of approximate neutrality, populations approach particular equilibrium
values, but only slowly in comparison with typical life-history time scales.
The QNA, invoked in Section 6, exploits the resulting separation of the time-
scales of intraspecific and interspecific population dynamics to simplify descrip-
tions of community dynamics (Rossberg and Farnsworth, 2011). Approximate
neutrality among species with similar maturation sizes in a size-structured
community is a likely phenomenon (O’Dwyer et al., 2009). Indeed, in the
Species Size-Spectrum Model, the contribution from food-web effects had
to be included in the interaction kernel KðuÞ ~ exactly to regularise model
artefacts arising from perfect neutrality within size classes (Section 6.4).
The QNA as applied in the Species Size-Spectrum Model, however, in-
vokes approximate neutrality not only within size classes, but, to a certain
degree, also across size classes. This is justified a posteriori by the substantial
competitive components in the interactions between species of different
size, which arise from broad population-level predator–prey size-ratio win-
dows, leading to slow dynamics. To quantify the resulting degree of time-
scale separation, and hence to gauge the reliability of the QNA, one can
compare typical intra- and interspecific relaxation times in the model. In
the simulation with standard parameters, shown in Fig. 4, population sizes
near the targeted size class m∗ ¼ mF relax on a timescale of 4–10 Tmat, with
0.05
0
-0.05 t = 0.03Tmat
0.05
0
-0.05 t = 0.1Tmat
0.05
0
-0.05 t = 0.3Tmat
0.05
0
-0.05 t =Tmat
0.05
0
-0.05 t = 3Tmat
0.05
0
-0.05 t = 10Tmat
0.05
0
-0.05 t = 33Tmat
10-12 10-
6
100 106 1012
Relative individual size m/mF
Figure 10 Comparison of the response of individual (i.e. Sheldon-type) size spectra to size-
specific feeding as predicted by the Species Size-Spectrum Model (Eqs. (78) and (79), solid
lines) and a corresponding model that disregards intraspecific size structure (Eq. (124),
dashed lines). Simulations with standard parameters for the oligotrophic regime,
~tot ½en k0 ðuÞ þ XðuÞ in Eq. (124)
however, with 10-fold fishing mortality F, with K~ 1 ðuÞ ¼ B h i
to stabilise short-wavelength instabilities, X(w) in Eq. (86) replaced by X b b ~ ðwÞ
n
for consistency, and the parameter r in X(w) set to 20g to suppress amplifying cascades
that would otherwise arise.
1
Tmat ¼ m1n
F ~ g1
0 ð1 nÞ . The intraspecific relaxation timescale is given by
the inverse size of the spectral gap of the McKendrick–von Foerster operator
Lm , which is estimated in Appendix as m ~ðm∗ =Þn1 . As m
~ ¼ ~g0 by Eqs. (35)
and (37), the ratio between the two timescales is 4–10 times (1 n) 1n 1,
∗
which is 20 to 60. These are fairly large values, from which at least a semi-
quantitative validity of the QNA can be expected. Indeed, Hartvig et al.
(2011) find for their closely related model, using simulations that
explicitly account for both intra- and interspecific population dynamics in
small communities, that dynamical details are generally much more
complex than the Species Size-Spectrum Model predicts. Yet, the
structures emerging when averaging across time and communities
(Hartvig et al., 2011) are similar to those derived here.
9.6. How do power-law size spectra arise?

Just as in the paper of Andersen and Beyer (2006), the current analysis began
with the assumption of a power-law size spectrum and then investigated its
consequences, for example, constraints on the power-law exponent. This
does not immediately answer the question of why power laws emerge in
the first place. In addressing this question, the oligotrophic and eutrophic
regimes have to be distinguished.
In the oligotrophic regime, where l ¼ 2 þ q n, conditions on overall abun-
dance, Eq. (38) for N ~ or Eq. (116) for B~tot , must be satisfied for steady-state
power-law size spectra. Press perturbations of the size spectrum lead to modifi-
cations of the power law that spread on the m∗-axis away from the point of per-
turbation. Pulse perturbations can be described as two press perturbations of
opposite sign initiated with a short delay. These are therefore predicted to lead
to pulses travelling along the m∗-axis away from the point of perturbation.
Assuming that any deviation of the size spectrum from the ideal form can be gen-
erated by applying appropriate pulse perturbations, one can conclude that any
such deviations will eventually travel towards the upper and lower ends of the
m∗ range realised in a community, and there, depending on the effective bound-
ary conditions, either be reflected back or disappear. When reflection is suffi-
ciently weak and/or all modes are sufficiently damped, all deviations will
eventually disappear when no further perturbations are applied. What remains
is a power-law size spectrum.
Complications of this scenario can arise only when the boundaries of the
ecologically realised m∗ range effectively impose press perturbations on the
size spectrum, which will then lead to persistent upward or downward cas-
cades or bends originating at the upper or lower end of the realised range. In
particular, insufficient biomass at the lower end acts as a press perturbation
which will generate an upward-travelling front of reduced abundance
corresponding to the purely imaginary zero of KðxÞ ^ (Fig. 6A), and
eventually to a bent-down steady-state size spectrum. This has, after

back-translating result of Section 7 to the linear m∗-axis and disregarding tro-
phic cascades, the form

Bðm∗ Þ ¼ mlþ1 ~tot 1 þ Qml2Imfx1 g þ h:o:t: ,
B ½127
∗ ∗
with a scale parameter Q < 0, rather than following a power law.

Overabundance of biomass at the lower end corresponds to Q > 0.
Higher-order terms in Q, not captured by the linearised QNA, are indicated
by h.o.t. However, the exponent l 2 Im{x1} can be numerically quite
small (Fig. 6A), so the deviations from a perfect power law described
by Eq. (127) might remain undetected in empirical data. Possibly, all that
can be seen is a change in the best-fitting power-law exponent (“slope”).
Besides, mechanisms not considered here could help satisfying Eq. (38) at
least approximately, to keep deviations from a power law in Eq. (127) small.
For example, temporal modulations of abundances, as observed by Hartvig
et al. (2011), can modify the effective value of the interaction coefficient g in
Eq. (38). An effect observed in simulations of size-structured food webs may
also be important (Rossberg et al., 2008): evolutionary forces can lead to
adjustments of attack rates at community level such that effective food
availability becomes of similar magnitude as physiological food demand. In
the present case, this would mean that gN/k ~ becomes approximately of
the order of magnitude of one, which is indeed what Eq. (38) requires.
In the eutrophic regime, a power-law spectrum can form at any abun-
dance level N ~ , provided N ~ is sufficiently large to guarantee ad libitum feed-
ing. Perturbations of the size spectrum will, over time, subside as in the
oligotrophic case, leaving a power-law size spectrum, possibly overlaid with
boundary-induced trophic cascades. Therefore, power-law size spectra form
naturally in the eutrophic regime.
In size-spectrum theories pre-dating Benoı̂t and Rochet (2004), an individ-
ual’s rate of food uptake is generally thought to be density independent, as here
in the eutrophic regime (e.g. Brown et al., 2004; Platt and Denman, 1977,
1978), leading to perfect power laws over a wide range of conditions. A
similar situation arises in the models investigated analytically by Benoı̂t and
Rochet (2004) and Law et al. (2009), where all growth and mortality terms
scale linearly with abundance, so that abundance can be factored out.
Contrary to a statement by Capitán and Delius (2010), the two cases (no
density dependence or uniform linear density dependence) are neither
ecologically nor mathematically the same. Yet, it is characteristic for both
that power-law size spectra can form at any abundance level, and that the size-
spectrum slope l depends on several physiological parameters (in the present
case, according to Eq. (39), on a, h, k, n, and the predator–prey size-ratio
window s(˙)).
9.7. Comparison with the theory of Andersen and Beyer (2006)

An important result of the present work is that in size-structured commu-
nities of populations covering wide size distributions the boundary condi-
tion of the McKendrick–von Foerster Equation (which balances
production and outgrowth of newborns) implies that the specific physiolog-
ical mortality of immature individuals is constrained to a~¼ 1 over most of
their life history. This finding differs from the analytic results of Andersen
and Beyer (2006), which Hartvig et al. (2011), similar to Andersen et al.
(2008), evaluate to a~ 0.42 for parameters as in Table 3. The theory of
(Andersen and Beyer, 2006) does not consider the boundary condition
and is therefore not “complete” in the sense used here. As a result, it predicts
“equilibrium” population structures that violate the condition that mean
lifetime reproductive output per individual (known as R0) should equal
one (Andersen et al., 2008). Resolution of the discrepancy between the
two approaches requires understanding how Andersen and Beyer (2006) ar-
rive at their constraint on a~.
The case considered by Andersen and Beyer (2006) corresponds to the
oligotrophic regime, because the feeding level is assumed fixed at an interme-
diate value 0 < f0 < 1. They were the first to observe that this alone determines
the size-spectrum slope as l ¼ 2 þ p – n (Capitán and Delius, 2010, make a
similar observation). The crucial difference from the model of Hartvig
et al. (2011)—investigated here—seems to be that Andersen and Beyer
(2006) assume the rate of food intake to follow a different allometric scaling
law than metabolic loss so that the loss becomes relevant only as individuals
approach their maximal attainable size. For younger individuals, both growth
g(m, m∗) and predation mortality mp(m) are proportional to what Andersen and
Beyer (2006) call the metabolic requirement for food. This leads to a value
a~¼ lim m/m∗ ! 0mmp(m)/g(m, m∗) that is fully determined by basic physiological
parameters. By contrast, the density-dependent bioenergy available for
growth in the model of Hartvig et al. (2011) is always discounted by substantial
density-independent metabolic loss so that a~ (mortality over growth) be-
comes density dependent. This leaves room for a~to be adjusted at community
level by the mechanisms explored in Sections 5 and 9.6.
9.8. Outlook
Although providing answers and clarifications to many questions related to
community dynamics, the present analysis also led to a number of new ques-
tions and challenges. In closing, some of these are discussed briefly.
The distinction between the mechanisms shaping size spectra in oligo-
trophic and eutrophic regime made throughout the analysis immediately
raises the question as to which empirical systems are best described by which
regime, or whether either of these exclusively describes the situation in the
field. An easy approach to this question would be to measure how close so-
matic growth and reproduction rates in a given community are to those
found in laboratory experiments with ad libitum feeding. By the definition
of the eutrophic regime, they should be identical in this case, whereas for
the oligotrophic regime, growth and reproduction would be slower in
the field than in the laboratory.
Based on such identifications of the relevant regimes, further progress
may be possible in relating size-spectrum slopes to trophic status (Ahrens
and Peters, 1991; Sprules and Munawar, 1986), temperature (Yvon-
Durocher et al., 2011), and other environmental conditions. Obviously,
changes in the slope resulting from environmental change can have great
impacts on the production at higher trophic levels available to human
consumption.
Another question that deserves further study is the distinction between
damped and amplifying upward and downward cascades in field data. As
mentioned in Section 2.5, this will probably require analysis of temporally
resolved size-spectrum data. Clearly, the distinction between upward and
downward cascades has implications for approaches to management of
size-structured communities. Provided that amplifying cascades can be iden-
tified, the theoretical problem arises of extending the linear theory for
size-spectrum dynamics to include non-linear corrections, because these
could limit the amplification. Perturbative approaches developed in other
contexts (Newell and Whitehead, 1969) might be employed usefully here.
Important in the context of fisheries management are the three related
questions of what determines the upper cut-off of the size spectrum (i.e.
the natural size of the largest species), how the boundary condition resulting
from this cut-off is best incorporated into size-spectrum models, and how
large the expected perturbation of the size spectrum resulting from this
boundary conditions is. A way forward on these questions might be to study
them first in corresponding species-resolved models of size-structured
communities (Hartvig et al., 2011; Rossberg et al., 2008; Shephard et al.,

2012), where the upper cut-off naturally emerges.
Finally, the observations of Section 9.4 highlight that care must be taken
to incorporate population size structure and trophic interactions at all life
stages adequately into management models, because this may drastically
modify dynamics. Consistency of model steady states with observed condi-
tions is an insufficient criterion for model validation: this insight might allow
improvements of some models currently in use.
As exemplified throughout this work, the language of mathematics has its
use in science not only for reasons of numerical precision. Often, the outcome
is just precision of thought: the definition of a quantity through a formula
allows investigation of logical relations to other quantities; equations stating
mechanistic relations between quantities allow tracking down their implica-
tions; a description of a system by combinations of such equations (rather than
verbal models) allows evaluation of its logical consistency, its descriptive com-
pleteness, its mechanical consistency, and at least the qualitative consistency of
its predictions with observations. Verbal descriptions and analyses of complex
systems are more prone to the risks of being incomplete, overlooking essential
feedback loops, or incorporating hidden inconsistencies. Ecology as a field
might be underestimating the benefits inherent to the mathematical idiom.
Especially in a context of rapid, global change leading into a world with
environmental conditions not experienced before, there is need for good
understanding of the general mechanisms controlling high-level ecosystem
states (Mintenbeck et al., 2012; Möllmann and Diekmann, 2012). This
understanding should ideally derive not solely from syntheses of past
observations but be anchored in systematic analyses of the consequences
of fundamental principles.
Formal reasoning using mathematical language can help to navigate the
complexities of such analyses. The present work hopefully, therefore, does
not only provide insights into the workings of size-structured communities
but also encourages researchers to make greater use of formal reasoning in
order to advance our understanding of complex ecological patterns and
processes.
ACKNOWLEDGEMENTS
Discussion and comments on this work by Eric Benoı̂t, Martin Hartvig, Ken Haste Andersen,
Linus Carlsson, Åke Brännström, Christian Mulder, Andy Payne, and three anonymous
reviewers, as well as editorial input by Julia Reiss, Gabriel Yvon-Durocher, Ute Jacob,
and Guy Woodward are gratefully acknowledged. This Beaufort Marine Research Award
is carried out under the Sea Change Strategy and the Strategy for Science Technology
and Innovation (2006–2013), with the support of the Marine Institute, funded under the
Marine Research Sub-Programme of the Irish National Development Plan 2007–2013.
APPENDIX. NUMERICAL STUDY OF THE SPECTRUM OF

THE MCKENDRICK–VON FOERSTER
OPERATOR
This appendix reports results of a numerical study of the spectrum of
the linear operator Lm , as defined by Eq. (47). Parameters were chosen as in
∗
Section 8.1. To avoid numerical difficulties at small body size, the eigen-
value problem Lm W ðmÞ ¼ lW ðmÞ for the density of individuals along the
∗
linear mass axis was transformed into the corresponding eigenvalue problem
for the density of biomass along the logarithmic mass axis f(u) ¼ e2uW(eu),
with u ¼ ln(m/m∗). The equivalent eigenvalue problem is then Hm f(u) ¼
∗
lf(u), with
df ðuÞ
1 u=4
Hm f ðuÞ ¼ m~mn1 e 1=4 f ðuÞ eu=4 1=4 ½128
∗ ∗ 4 du
Z ln
þ1=4 dðu u0 Þ f ðuÞdu

u0
def
conditional to f(u) ¼ 0 for u < u0, where u0 ¼ lnðm0 =m∗ Þ ¼ lnðx0 Þ. As in
Sec. VIII.A, the maximum attainable relative body mass was set to
1 ¼ 4. Results reported here are for x0 ¼ 10 5. Results depend only
weakly on this particular choice. The last term in Eq. (128) enforces the
condition
Z ln
1=4 1=4 1=4 1
f ðu0 Þ ¼ ðx0 Þ f ðuÞdu ½129
u0
on eigenfunctions f(u).
The problem was discretized on a grid with G points, spaced equally on
the u-axis from u0 þ Du to – ln , where Du ¼ (ln u0)/G. The deriv-
ative of f(u) in Eq. (128) was approximated by backward differences. To
compute this difference for the first point, u ¼ u0 þ Du, that is,
f 0 (u0 þ Du) (Du) 1[f(u0 þ Du) f(u0)], Eq. (129) (trivially approximated
by a sum) was used for f(u0). The factor m ~mn1
∗
in Eq. (128) can be eliminated
by rescaling all eigenvalues. The eigenvalue problem for Hm∗ is then approx-
imated by a corresponding numerical eigenvalue problem for a G G ma-
trix Hjk.
A B C
3 3 3
2 2 2
1 1 1
Im{l}
0 0 0
-1 -1 -1
-2 -2 -2
-3 -3 -3
-2 -1 0 1 -2 -1 0 1 -2 -1 0 1
Re{l}
Figure 11 Eigenvalues l of the matrix Hij, a discretization of the McKendrick–von
Foerster operator, Eq. (47). (A) Naive implementation, exhibiting discretization artefacts.
(B) Regularised version, obtained by removing the last two rows and columns of Hij. (C)
After removal of yet another row and column. All eigenvalues are given in units of
~mn1
m .
Figure 11A shows the eigenvalues of Hjk for G ¼ 2000. All eigenvalues
have multiplicity one. The largest eigenvalue found, l ¼ 0:00018~ mmn1
∗
, is
close to zero. Further, one can distinguish 5–6 negative real eigenvalues, and
a family of complex eigenvalues.11 The negative real eigenvalues are numer-
ical artefacts. They arise from the fact that, because g(eum∗, m∗) approaches
0 linearly as u ! –ln (the largest adults do not grow), the matrix Hjk has
for large G in its lower right corner the approximate structure
0 1
.. ..
B . . C
B 4A B 0 0 0 0 C
B C
B 3A B 0 C
B 3A 0 0 C, ½130
B .. . 2A C
B 0 2A B 0 0 C
@ 0 0 A A B 0 A
0 0 0 0 B
with positive constants A and B that are independent of G. This leads to one
eigenvector with eigenvalue –B, localised on the last lattice point with small
contributions in all other components, and a series of eigenvectors of the
approximate forms (. . ., 0, 0, –1, 1, 0)T, (. . ., 0, 1, –2, 1, 0)T, (. . ., –1, 3,
–3, 1, 0)T, . . . and corresponding eigenvalues –(2A þ B), –(3A þ B),
–(4A þ B), . . . The strong localisation of these eigenvectors on the u-axis
in the limit G ! 1 and their alternating sign structures exclude them from
the set of possible eigenvectors of the exact problem.
These artefacts can be suppressed by removing the last two points of the dis-
cretization lattice. The spectrum of the regularised (G – 2) (G – 2) matrix is
shown in Fig. 11B. When removing instead the last three lattice point, reducing
Hjk to a (G – 3) (G – 3) matrix, the structure of the spectrum remains
unchanged (Fig. 11C), indicating that the regularisation was successful. The
leading eigenvalue l ¼ 0:00018~ mmn1
∗
remains essentially unchanged close
to zero. The corresponding eigenvector, appropriately normalised,
differs by no more than 0.5 10–5 at any lattice point from the exact solution
~
of Hm f(u) ¼ 0, given for u0 < u < – In by f ðuÞ ¼ bðuÞ (as in Eq. (114)) and
∗
f(u)¼ 0 otherwise. This result confirms the numerical method used.
All eigenvalues but the leading one are complex. They are separated from
the leading eigenvalue by a gap of about 0:7 m ~mn1 . The size of the gap
∗
approximately equals m ~ðm∗ =Þ , the mortality of the largest adults, and
n1
it was verified to exhibit the corresponding dependence on . The density

of the subdominant eigenvalues along a line in the complex plane (Fig. 11B)
was verified to increase approximately as G1/2. The results suggest that these
subdominant eigenvalues becomes a continuous family of eigenvalues in the
limit G ! 1, separated from zero by gap of a size given by the mortality of
the largest adults of the m∗ size class considered.
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INDEX
Note: Page numbers followed by “f ” indicate figures, “t” indicate tables, and “b” indicate
boxes.
A numerical evaluation, 491

Analytic theory offspring production rate, 453
biomass density, 452 orientation, changing planet
characterisation, size-spectrum dynamics, body-size distributions, 430
494–496 elevated nutrient discharge, 429
coarse graining and mean-field models, ecological research, 429–430
approximation, 435–436 paper structure, 437
constrained-domain variant, 493 parametrisation
density-dependent life-history heuristic submodel, 488
parameters, 436 predator–prey size-ratio window, 488
distribution, individual sizes reproduction-selection function,
fisheries management, 511–512 489–490
food-web effects, 501–502 simulations, 487, 488t
intraspecific mass, 501–502 predation mortality, 454
mass balance, 502–503 predicted structure and dynamics, 435
oligotrophic and eutrophic regime, 511 pseudospectral method, 490–491
population-level predator–prey size- scale-invariant community steady state,
ratio, 503–505 454–465
population size structure and trophic singular perturbation expansion, 436–437
interactions, 512 size spectra
power-law size spectra, 508–510 anthropogenic pressures, 433
QNA, 506–508 LFI, 431–432
size-structured communities, 512 planktonic, 431, 432f
slow and fast, fishing, 505–506 regularities, 430–431
steady-state solution, 502 species size-spectrum model (see Species
theory of Andersen and Beyer, 510 size-spectrum model)
verbal descriptions, 512 standard parameters, 491–493
downward trophic cascade, 498–499 system dynamics, 435
energy and biomass, 451–452 time-dependent solutions, 436
final steady state, perturbed size spectrum, trophic interactions, 451
500–501 upward trophic cascade, 497
food-intake, 452–453 Antagonistic and mutualistic network
lists symbols, 448, 449t models, 168–169
mathematical size-spectrum models, Antagonistic host–parasitoid interactions
433–435 description, 135–136
Mckendrick–von Foerster operator, mosaic, variable-quality patches, 135–136
513–515 species-specific extent, 136
methods, 447–448 survival, 136
non-mathematical language within-patch effects, 136
(see Non-mathematical language, Antagonistic host–parasitoid networks,
analytic theory) 160–162
523
524 Index
Antagonistic interactions, food webs ice dynamics, 353

biomass interactions, 156–158 invasion, crustaceans, 355–356
body-mass-driven extinctions, 158–159 life cycle, 354
Caribbean coral reefs, 159–160, 161f marine communities, 354
coral bleaching, 159–160 marine ecosystem
ecological network structure, 155–156, biological characteristics, 359–362
156f geographical and physical conditions,
fragmentation, 159–160 357–359
habitat fragmentation, 134–135 model simulations, 395
handling time, 135 notothenioid fishes, 394
higher trophic levels, 156–158 ocean acidification, 353–354
higher trophic rank hypothesis, 159 physiological vulnerability, 371–376
impacts, habitat fragmentation, 159, 160f regular monitoring, stocks, 404–405
model system, 159 Southern Ocean, warming, 355
mountainous aquatic fragmentation, species loss, ecosystem
155–156, 157b anchovy and sardines, 403, 403t
mutualistic networks, 135 channichthyids, 401
predator–prey, 134 demersal communities, 400–401
riverine network, Gearagh forest, pelagic community, 401–402
154–155, 155f Pleuragramma antarcticum, 401–402, 402f
short-term patch-scale, 135 population density, 400
stream benthic, 155–156, 158f recovery phases, 403
terrestrial systems and channels, 154–155 stages, calcifying invertebrates, 355
Antarctic ecosystems, climate change trophic vulnerability, 376–386
impacts vulnerability (see Habitat destruction)
abiotic climate forcing, 405 warming, seawater, 353
adaptations and characteristics, 366–370 Antarctic fish communities
bio-indicators, 356 adaptations and characteristics, 366–370
commercial sealing, 404–405 composition, modern fauna
community persistence benthic habitat, 363
abiotic and biotic mechanisms, 400 diversity, demersal fish community,
demersal fish species, 398 363
icefishes, 399 notothenioids, 362–363
population dynamic parameters, 398 pelagic and demersal fish, 364f,
sea ice reduction, 399–400 364–365
composition, modern fauna, 362–365 pelagic ichthyofauna, 364–365
effects, marine systems evolution and adaptive radiation
marine biota, 397 endemism, 365–366
plankton community composition, Oligocene–Miocene transition, 366
396–397 trophic diversification, 365–366
seawater salinity, 395–396 physiological and morphological
transgenerational, 397–398 adaptations
evolution and adaptive radiation, body fluids, ectotherms, 367
365–366 cytosolic diffusion processes, 367–368
food web structure and dynamics, notothenioid, 368
394–395 oxygen-carrying capacity, blood, 367
global mean, 352 sexual maturity, 369
human activity, 355 prey species, 370–371
Index 525
trophic structure and dynamics, 370 contrasting dichotomies, 5–9

Antarctic marine ecosystem monophyletic ecological assemblages, 9
biological characteristics operational classification, 10, 10f
benthic food webs, 360 predicting (see Predicting B–EF)
phytoplankton blooms, 359–360 scaling (see Scaling B–EF)
POM, 361 system-driven, 48–54
primary and secondary consumers, 360 taxocenes, 10
seasonal sea ice zone, 362 terrestrial ecosystems, 44–46
geographical and physical conditions vexing drivers (see Vexing drivers)
geological and climatological Biotic interactions
history, 357 antagonistic, food webs, 134–135
light conditions, 359 antagonistic host–parasitoid, 135–136
map, Antarctica and Southern Ocean, mutualistic plant–ant, 132–134
357–358, 358f mutualistic plant–frugivore, 131–132
physical feature structuring, 358–359 mutualistic plant–pollinator, 129–131
sea ice, 359 Boundary
Aquatic ecosystems aquatic–terrestrial, 112, 119
eutrophication, 46–48 fragment–matrix, 116–117
framework articulating functional, 45f, 46 layer, 118–120
trophic effect and response traits, marine–freshwater, 115f
46–48, 47f
Articulating B–EF in aquatic ecosystems, C
46–48 Caribbean coral reefs, 159–160, 161f
Articulating B–EF in terrestrial ecosystems, Community resilience, climate change
44–46 impacts on
benthic macroinvertebrate, 241–248
B biogeochemical processes, 239–240
Bacterioplankton descriptors, disturbance effects
body size and structure, 299 macroinvertebrate, 223–224, 225f
climate effects, biomass, 290 mean taxon richness, 223, 224f
density, climate effects, 293–294 stability, rank abundance, 223–224
latitudinal gradient, 325–327 disturbance and development, 237–238
reproduction and growth, 302–303 disturbance and diversity
B–EF. See Biodiversity–ecosystem dynamics, 213–214
functioning (B–EF) recolonisation, 233
Bimodal networks, 97, 98, 101 theoretical models, 213–214
Biodiversity and disturbance frequency
interacting species, 91–92 chironomid midges, 234–235
planet’s ecosystems, 91 flow cessation, 233–234
types, 94 drought disturbance, streams
Biodiversity–ecosystem functioning (B–EF) biodiversity and ecosystem
aquatic ecosystems, 46–48 functioning, 214
biotic resources, 10–11 freshwater organisms, 215
coda pressure, populations, 214–215
allometric metrics, 54–55 thermal envelope, 214–215
large-scale macroecology, 54 and ecosystem functioning
predictors, 55 distribution, dewatering effects,
constraining (see Constraining B–EF) 235, 236f
526 Index
Community resilience, climate change Monte Carlo simulation, 392, 393f

impacts on (Continued ) side scan sonar, 390–391
environmental change, 235 Weddell Sea shelf, 392
herbivore release, 236–237
effects, drought treatment, 249–253 E
environmental filter, drought, 238 Ecological networks
experimental design and application, bimodal/bipartite, 97
219–220 biotic interactions, 94, 95f
hydrologic drought, 239–240 body size, 98–99
linear time trends, 230–231, 231t food webs, 96–97
mesocosms, 217–218 functional groups, 100
sampling and processing, 220 habitat fragmentation and selection
statistical analysis mosaics
community structure, 220–221 antagonistic predator–prey and
Monte Carlo permutation test, 222 mutualistic seed dispersal
partial RDA, 221–222, 221t interactions, 171–172
RM-ANOVA, 220 explorations, 171
structure, disturbance GMTC, 171
ecosystem, 212–213 hypothesised effects, 171
life cycles, organisms, 213 species shape, 171
mean abundance, macroinvertebrates, tiny and semi-autonomous
226–230, 227f networks, 172
mean densities, mesocosms, 226–230, two-species models, 172
228f links, 94–96
natural systems, 212 mutualistic and antagonistic
RDA, 226–230, 229f measurement, structure, 97
RM-ANOVA, 225–226, 226t nestedness and modularity, 98
temporal dynamics, disturbance effects, substructures, 97–98
230–231 traditional food webs, 96
Constraining B–EF nodes, 94
body size, 18 selection mosaics, 171–172
microbial taxa, 17–18 species abundance, 99–100
pollinating insects, 18, 19f Elemental-affected net primary production
sensitivities and traits, species, 16–17 (eNPP), 8t, 24
taxocene (see Taxocene) eNPP. See Elemental-affected net primary
Contrasting dichotomies production (eNPP)
biomass/production and biodiversity, Environmental warming, shallow lakes
5–6, 6f bacterioplankton latitudinal gradient,
body size, 9 325–327
dynamics relationships, 5–6 changes, community traits
eNPP, 7–9, 8t bacterial biomass, 310
fishes, 6f, 7 biomass and density, 308–309
metabolic capacity, 7–9 ectothermic aquatic organisms,
312–313
D factors and trophic interactions,
Dianthus deltoides, 123 314–316
Disturbance simulation model fish taxonomic richness, 307–308
habitat structure, 392–394 freshwater communities, 310–311
Index 527
lake productivity, 309 food webs, 44

mathematical models, 313 scale manipulation, 44
mesocosms, 311–312 total biomass, 42, 43f
meta-analyses, zooplankton, 309 Fishes
microorganisms, 308 body size and structure, 295–296
organizational levels, 306 climate effects, biomass, 283
perturbation experiments, 311 climate effects, density, 290–291
and ecosystem responses, temperature reproduction and growth
deterioration processes, 263 breeding and growing seasons,
hysteresis process, 264–265 299–301, 300f
nutrient enrichment symptoms, 264 hydrological characteristics, 299–301
polymictic, 262–263 primary life history strategies, 299
global change and freshwater variation, reproductive life history
communities traits, 299–301, 301t
anthropogenic impacts, 261 richness changes with climate, 278–279
Stenothermal species, 262 Food webs, antagonistic. See Antagonistic
temperature, 262 interactions, food webs
indirect effects, community structure
latitudinal gradient, 265 G
nitrogen limitation, 265–266 Geographic mosaic theory of coevolution
periphyton latitudinal gradient, 322–325 (GMTC)
phytoplankton data and latitudinal description, 169
gradient effects, basic components
meta-analysis, 328–330 contrasting selection and stochastic
Netherlands–Uruguay comparison, genetic variation, 170
327–328 ecosystem via trophic cascades, 170
research mathematical models, 170
biogeographic processes, 319 open-habitat species, 170
ecosystem management, 321–322 reduction, gene flow, 170
fish density, 320 two-species interactions, 170
HNF, 320–321 gene flow, 169–170
trophic ecology, 321 space, 169–170
SFTS approach (see Space-for-time GMTC. See Geographic mosaic theory of
substitution (SFTS) approach) coevolution (GMTC)
temperature, 262
theoretical predictions H
data, community traits, 267, 269t Habitat destruction
empirical generalizations, 267–271 iceberg scouring
heat balance hypothesis, 271 climate change, 390
macroecological approaches, 272 disturbance simulation model, 390–394
MTE, 266 mechanical disturbance events,
population dynamics, 267 387–388
temperature-size rule, 271–272 recolonization, 388
trophic interactions, 272–273 sea ice reduction
food web, 387
F sympagic community, 386–387
Fish biodiversity Habitat edges
cascade effects, 42 emigration rates, 114
528 Index
Habitat edges (Continued ) spatial and temporal turnover, species

frequency distribution, pairwise distances, high turnover rates, 117
114, 115f mismatches, 118
hard/soft, 114 role, 117
natural/anthropogenic, 111 soft edge, 117
phenological response, trees, 112–114, 113f tree, edge effects, 113f, 117–118
physical and biological effects, 111–112 species, 176
species, 112 species traits, 121–129
swarm-markers, 112 super-networks, 176
taxonomical/functional groups, 112 ubiquitous, 92–94, 93f
Habitat fragmentation Heterotrophic nanoflagellates (HNF),
abiotic environment and biotic 320–321
complexity, 92 HNF. See Heterotrophic nanoflagellates
applications, conservation and agriculture (HNF)
conceptual challenge, 173
connectance/link density, 174 I
key components, 173–174 Invasive species, 116–117, 170
link-focused management, 174–175 Island biogeography theory, 168
physical structure and network
architecture, 174–175 M
practical hurdles, 173 Macroinvertebrates
presence/absence, apex consumers, 174 body size and structure, 296
species-centric measurements, 173 climate effects, biomass, 283
aquatic ecosystems, 103, 105b density, climate effects, 291
ashdown forest, 177–178 reproduction and growth, 301
biodiversity (see Biodiversity) richness, climate, 279–280
biotic interactions, 129–138 Macrophytes
Brazilian Atlantic Rainforest Trees, 103, body size and structure, 297
106b climate effects, biomass, 285
characteristics climate effects, density, 292
animal and plant traits, 107, 108t reproduction and growth, 302
biodiversity effect, 107 richness, climate, 281
isolation and connectivity, 111 Mass-balance models, 441
landscape elements, 111 Mathematical models, 170
species richness, 107 Mathematical size-spectrum models
coevolutionary dynamics, 169–172 feeding interactions, 434
data analytical tools, 92 formal analytic tools, 433
definition, 103 short-term energy balance, 434–435
edges, 111–114 structure, 434, 434f
landscape changes, 92 trophic levels, 433–434
link-based management, 176 Matrix
matrix (see Matrix) agroecosystems, 116
meta-network, 164–169 anthropogenic, 116
natural and anthropogenic processes, 93f, food webs, 116–117
103, 104f invasions, 116–117
networks (see Networks) pollinator rescue, 116
quantitative measurement, 103 quality, 114–117
scales, 118–121 structure and dynamics, 114–116
Index 529
Mckendrick–von Foerster operator antagonistic host–parasitoid, 160–162

body mass, 513 coevolutionary dynamics, 169–172
eigenvalues, 514–515, 514f ecological, 94–100
linear operator, 513 GMTC (see Geographic mosaic theory of
subdominant eigenvalues, 515 coevolution (GMTC))
Mesocosms mutualistic plant–ant, 153–154
disturbance treatments, 219–220, 219t mutualistic plant–frugivore, 150–153
mean densities, 226–230, 228f mutualistic plant–pollinator, 138–149
natural systems, 215–216 properties
research, 217 fragment size and isolation, 163
stream facility, 212, 217 habitat fragmentation, 163
Metabolic theory of ecology (MTE) in silico communities, 162
availability, resources, 267 matrix quality, 163
changes, species, 266–267 modular structure, 163
community biomass and density, 308–309 nestedness and structure parameters, 163
warmer conditions, 309 species and link richness, 162
Meta-networks spatial, 100–101
colonisation Non-mathematical language, analytic theory
abundant and diverse, 167–168 body mass, 445
bipartite ecological networks, 168–169 depletion, food chain, 444
isolation and quality, 167–168 feeding, size classes, 440
pairwise mutualistic interactions, 168 food-web structure, 444–445
residents and fragment characteristics, mass-balance models, 441
167–168 physiological mortality, dynamic
seminal work, island biogeography equilibrium, 445–446
theory, 168 population-level predator–prey size-ratio
definition, 164 windows, 440–441
description, 164 power-law community size spectra,
dispersal, 166 437–440
ecological networks, 164, 165f regulating constraints, 437, 438t
extinction, 166–167 size-spectrum, 446–447
single-species meta-population trophic cascades, 443
models, 164 upward and downward cascades,
Meta-population theory, 166 perturbations, 441–443
Monte Carlo permutation test, 222
MTE. See Metabolic theory of ecology P
(MTE) Particulate organic matter (POM), 361
Mutualistic and antagonistic interactions Periphyton
animal behaviour role, 138 body size and structure, 299
body size and trophic rank effects, 137 climate effects, biomass, 290
fruit sizes, 137 latitudinal gradient, 322–325
habitat and dietary specialisation, 137 reproduction and growth, 302–303
species trait, 137 richness, climate, 282
Physiological vulnerability, Antarctic fishes
N changes, abiotic environment, 374–375
Network contraction, 139–140 circulatory system, 372–373
Networks. See also Meta-networks metabolic plasticity, 371–372
antagonistic food webs, 154–160 salinity changes, 373–374
530 Index
Physiological vulnerability, Antarctic fishes Cynorkis uniflora, 130–131

(Continued ) effective movement, 130
sensitivity, increasing CO2, 371–375 habitat loss and fragmentation, 129–130
temperature dependence, 372–373, 372f Hawaiian tree, 130–131
Phytoplankton Plant–pollinator networks, mutualistic
biomass body size
climate regimes, 285–288, 286t landscape configuration, 147–148
cyanobacteria, 285–288 and linkage level, 144–146, 148f
linear regressions, 289–290, 289f mobility and reproduction, 147–148
phylogenetic classes, 288–289, 288f modes, attraction, 148
body size and structure, 297–298 morphological and behavioural
climate effects, density, 292–293 traits, 148
reproduction and growth, 302–303 nectar-holder depth and tongue length,
richness, climate, 281–282 146–147
Pistacia chinensi, 123 seed set, 148–149
Plant–ant interactions, mutualistic triangular relationship, 144–146, 147f
description, 133–134 wind-pollinated plants, 148–149
ecological and evolutionary dynamics, complexity–stability relationship, 140
133–134 contraction, 139–140, 141f
extrafloral nectary, 132–133 description, 138–139
mutualisms, 132 diversity and mobility, 138–139, 139b
mutualist systems, 132, 133b four fragmentation scenarios, 149
Plant–ant networks, mutualistic linkage level, 140, 141f
body size, 153–154 link switching, 143
nestedness, 154 modularity, 143–144, 145f
phylogeny and structure, 154 nestedness, 142
symbiotic and free-living, 153 single fragments, 142
Plant–frugivore interactions, mutualistic species and link richness, 139–140
dispersal distance, endozoochorously, switch/rewire, 142
131–132 POM. See Particulate organic matter (POM)
primate diets, 131 Population-level predator–prey size-ratio
small-to–medium-size, 131 window
traits, 131 biomass density, 503
vertebrates, 131 computation, 503
Plant–frugivore networks, mutualistic interacting size-structured, 503
array, species traits, 151–152 standard parameters, 503–504, 504f
complex landscape, 151–152 Power law/lognormal (POLO) rank
depauperation, 151–152, 151f abundance distributions, 142
diversity, taxa, 150–151 Power-law size spectra, 508–510
fleshy fruits and rely, 150–151 Predicting B–EF
flocking behaviour and seasonally fish biodiversity (see Fish biodiversity)
altitudinal migrants, 152–153 functional redundancy
fragmentation and habitat loss, 153 abiotic predictors, 26, 27t
functional losses, 153 food webs, 27–29
nested assemblages, 152–153 freshwater fishes, 27–28, 28t, 62t
species and link diversity, 152–153 interactions, 26, 28–29
Plant–pollinator interactions, mutualistic link density, 26–27
bumblebees, 130 pair-wise interactions, 26
Index 531
predator-prey matrix, 26, 28t RM-ANOVA. See Repeated-measures

population fluctuations analysis of variance (RM-ANOVA)
allometric scaling, 39–40
biomass-size spectrum, 40 S
body mass scaling, 41–42 Scale
fish size spectra, 41 complexity and spatiotemporal, 121
log-transformed biomass, 40 extinction debts, 120–121
mass-abundance scatter-plots, 40 flow habitats, 118–120
sampling methods, 26, 41–42 forest fragmentation, 120
water biodiversity (see Water biodiversity) phytotelmata, 118–120, 119b
Prey quality single spatial scale, 120
Antarctic and Sub-Antarctic species, 385 time, 120–121
digestive organs, 385 time-lagged, 120–121
low energy food, 386 Scale-invariant community steady state
omnivorous fish species, 386 ansatz, 455
Prey size boundary condition (part I), 459–461
aquatic food webs, 381–382 boundary condition (part II), 462–465
fish detection capability and feeding coarse-grain, 454–456
efficiency, 382–383, 382t demographics, 456–458
mean consumption rate, 384–385, 384f metabolic loss rate per size class, 461–462
mouth gape, 382 power-law size spectra, 456
prey detection and consumption, scale-free size distribution, 458–459
382–383 total biomass per size class, 461
Scaling B–EF
green world allometry
Q
metabolic rate, 15
QNA. See Quasi-neutral approximation
nitrogen, 13
(QNA)
plant physiology, 12f, 13, 14f
Quasi-neutral approximation (QNA)
protozoan metabolism, 13–15
ecological neutrality, 506
management and allometry
intraspecific relaxation timescale,
angiosperms and gymnosperms, 12f,
506–508
14f, 15–16
Species Size-Spectrum Model, 506–508,
conservation and sequestration
507f
management, 16
domestic population management, 16
R taxocene, 15
Redundancy analysis (RDA) Seed dispersal networks
disturbance regimes, community antagonistic predator–prey and
structure, 221–222 mutualistic, 171–172
drought disturbance, 225–226 avian frugivores, 128b
macroinvertebrate community structure, pollination, 150f
230–231 Single-site models, 169–170
Monte Carlo permutation test, 222 Single-species meta-population models, 164
Repeated-measures analysis of variance Soft edge, 117
(RM-ANOVA) Space-for-time substitution (SFTS)
drought treatment, 225–226, 226t approach
effect, disturbance frequency, 220 advantages and disadvantages
stability, rank abundance, 223–224 aquatic communities, 317–318
532 Index
Space-for-time substitution (SFTS) natural mortality, 469

approach (Continued ) normalisation condition, 468
biogeographical boundaries, 316–317 scale-invariant, 467, 468
community and ecosystem processes, steady-state population, 467
319 steady-state transition, 466
eutrophication, 318 reduced dynamics
taxonomic resolution, 316–317 density-dependencies, 470
body size and structure, 295–299 equilibrium values, 471
climate effects, biomass, 283–290 fishing pressure, 475–476
climate warming, 275–276 Fourier transform, 476
comparable ecosystem, 274 functional derivatives, 473
density, climate effects, 290–294 growth rate, 475
global change, 273 individual-level interaction, 474
intensity, trophic interactions integrand scales, 471–472
consumption pressure, 304–306, 305f oligotrophic regime, 473–474
cross-comparison, 304 power-law steady state, 474
lake functioning, 303 predation mortality, 473
nutrient cycling, 306 QNA, 469
predation pressure, 303–304 scale-invariant, 469–470, 473
monograph, 276 size spectra, 475
reproduction and growth, 299–303 somatic growth, 470–471
richness, climate, 278–283 species’ biomass, 474
spatial distribution, vegetation, 273–274 tentative steady-state solution, 479
Spatial networks time-dependent
analysis, 101 convective instability, 485–486
and ecological error function, 484
description, 101 fishing pressure, 485
dispersal and interactions links, Fourier transform, 481–482
101–102 inhomogeneity, 480–481
graph of graphs, 101–102 logarithmic maturation size scale, 485
three-species food chains, 102 multiple-scale singular perturbation
turing patterns, 102–103 formation, 483
habitat fragmentation framework, 101 singular perturbation formalism,
landscape ecology, 100–101 484–485
measurement, species-specific times, onset of fishing, 478–479
landscape, 101 zeros of K^(x), 486–487
nodes and links, 100–101 Species traits
topological role and position, 101 animal
Species size-spectrum model Amazonia, 124–126
complex poles and zeros of K^(x), 479–480 bees, 126, 127b
density-dependent population body size, 124–126
matrix, 465 genetic differentiation, 123, 125f
food-web effects, 477–478 trophic rank, 123–124
operators and eigenfunctions wider dietary/habitat niche, 123–124
boundary condition, 466 winged adult phases, 123, 124f
eigenvectors, 467 combinations
general population structure, 468 Amazonian forest, 126–129
hatchlings explicitly, 466 avian frugivores, 126, 128b
Index 533
Barro Colorado Island (Panama), framework articulating, 44, 45f

126–129 predators / fungivores, 45–46
bees, 126, 127b trophic effect traits, 45
interacting plants and animals, 129 Trivariate webs, 98–99
network analysis, 129 Trophic vulnerability, Antarctic fishes
description, 121–122 changes, trophic structure and dynamics
plant degree, trophic generalism, 381
Dianthus deltoides, 123 food web structure, 376–377
flower morphology, 122–123 planktivorous fishes, 378–380
fruit, 122 predators, 378
Pistacia chinensi, 123 resilience, entire system, 380–381
pollinators, 122 Spearman’s rank correlations, 378–380,
seed dispersal, pollination and breeding 380t
system, growth form and seed species trophic redundancy, 376–377
bank, 122 prey quality (see Prey quality)
System-driven B–EF size structure, prey (see Prey size)
abiotics, 48, 49f Turing patterns, 102–103
biomass, 48–50 Two-species models, 172
ecological stoichiometry and classical
prey-predator, 54 V
energy enrichment paradox, 48–50, 49f Vexing drivers
food web manipulation, 52–53 effects, dominant species, 5
free-living nematodes, 26, 48–50 forecasting global changes, 3–4
individual body-mass, 50–52 pragmatic approach, 4
mass-abundance slope, 50–52 response-effect hypothesis, 4–5
nutrient ratios, 50, 51f vascular plants, 4
omnivorous species, 53–54, 53f
predator-prey body-mass ratios, 50 W
soil mesofauna, 52–53, 53f Water biodiversity
stable states, 50 comparison, species diversity, 37–38, 38f
computational methods
T density implies, 36
Taxocene electrofishing, 30
agroecosystems, 18–20, 20f fish size distribution, 30
diversity and soil abiotics, 21, 26 food webs, 31, 33f, 34, 35t
enchytraeids, 25 freshwater ecosystems, 28t, 31–32
eNPP, 24 random and connectivity descending,
grazers, 24 33f, 34
invertebrates, 24 resource node, 34–36
macroarthropods, 22–24, 22f size spectra and power laws, 29–30
micro and mesofauna, 25 species diversity, 31, 32f
polar deserts, 20 static deletion sequences, 26, 30–31, 36
protozoa and microorganisms, 18–20 diversity-stability relationship, 39
scaling, 22–24, 23t food webs, 38–39
soil food webs, 25 intermediate connectances, 35t, 37–38
spatial scaling predicts, 21 Ohio fish data, 38–39
Terrestrial ecosystems primary and secondary deletions, 37
environmental response traits, 45 streams and ecoregions, 29
534 Index
Z biomass, 284
Zooplankton density, 291–292
body size and structure, 296–297 reproduction and growth, 301–302
climate effects richness, climate, 280–281
ADVANCES IN ECOLOGICAL RESEARCH
VOLUME 1–46
CUMULATIVE LIST OF TITLES
Aerial heavy metal pollution and terrestrial ecosystems, 11, 218

Age determination and growth of Baikal seals (Phoca sibirica), 31, 449
Age-related decline in forest productivity: pattern and process, 27, 213
Allometry of body size and abundance in 166 food webs, 41, 1
Analysis and interpretation of long-term studies investigating responses
to climate change, 35, 111
Analysis of processes involved in the natural control of insects, 2, 1
Ancient Lake Pennon and its endemic molluscan faun (Central Europe; Mio-
Pliocene), 31, 463
Ant-plant-homopteran interactions, 16, 53
Anthropogenic impacts on litter decomposition and soil organic matter, 38,
263
Arctic climate and climate change with a focus on Greenland, 40, 13
Arrival and departure dates, 35, 1
Assessing the contribution of micro-organisms and macrofauna to
biodiversity-ecosystem functioning relationships in freshwater micro-
cosms, 43, 151
A belowground perspective on dutch agroecosystems: how soil organisms
interact to support ecosystem services, 44, 277
The benthic invertebrates of Lake Khubsugul, Mongolia, 31, 97
Biodiversity, species interactions and ecological networks in a fragmented
world 46, 89
Biogeography and species diversity of diatoms in the northern basin of Lake
Tanganyika, 31, 115
Biological strategies of nutrient cycling in soil systems, 13, 1
Biomonitoring of human impacts in freshwater ecosystems: the good, the
bad and the ugly, 44, 1
Bray-Curtis ordination: an effective strategy for analysis of multivariate eco-
logical data, 14, 1
Body size, life history and the structure of host-parasitoid networks, 45, 135
Breeding dates and reproductive performance, 35, 69
535
536 Advances in Ecological Research Volume 1–46
Can a general hypothesis explain population cycles of forest lepidoptera? 18,

179
Carbon allocation in trees; a review of concepts for modeling, 25, 60
Catchment properties and the transport of major elements to estuaries, 29, 1
A century of evolution in Spartina anglica, 21, 1
Changes in substrate composition and rate-regulating factors during decom-
position, 38, 101
The challenge of future research on climate change and avian biology, 35,
237
Climate change impacts on community resilience: evidence from a drought
disturbance experiment 46, 211
Climate change influences on species interrelationships and distributions
in high-arctic Greenland, 40, 81
Climate influences on avian population dynamics, 35, 185
Climatic and geographic patterns in decomposition, 38, 227
Climatic background to past and future floods in Australia, 39, 13
The climatic response to greenhouse gases, 22, 1
Coevolution of mycorrhizal symbionts and their hosts to metal-contami-
nated environment, 30, 69
Communities of parasitoids associated with leafhoppers and planthoppers in
Europe, 17, 282
Community structure and interaction webs in shallow marine hardbottom
communities: tests of an environmental stress model, 19, 189
A complete analytic theory for structure and dynamics of populations and
communities spanning wide ranges in body size, 46, 427
Complexity, evolution, and persistence in host-parasitoid experimental sys-
tems with Callosobruchus beetles as the host, 37, 37
Conservation of the endemic cichlid fishes of Lake Tanganyika; implications
from population-level studies based on mitochondrial DNA, 31, 539
Constructing nature: laboratory models as necessary tools for investigating
complex ecological communities, 37, 333
The contribution of laboratory experiments on protists to understanding
population and metapopulation dynamics, 37, 245
The cost of living: field metabolic rates of small mammals, 30, 177
Decomposers: soil microorganisms and animals, 38, 73
The decomposition of emergent macrophytes in fresh water, 14, 115
Delays, demography and cycles; a forensic study, 28, 127
Dendroecology; a tool for evaluating variations in past and present forest
environments, 19, 111
Advances in Ecological Research Volume 1–46 537
Determinants of density-body size scaling within food webs and tools for
their detection, 45, 1
The development of regional climate scenarios and the ecological impact of
green-house gas warming, 22, 33
Developments in ecophysiological research on soil invertebrates, 16, 175
The direct effects of increase in the global atmospheric CO2 concentration
on natural and commercial temperate trees and forests, 19, 2; 34, 1
Distributional (In)congruence of biodiversity—ecosystem functioning,
46, 1
The distribution and abundance of lakedwelling Triclads-towards a hypoth-
esis, 3, 1
The dynamics of aquatic ecosystems, 6, 1
The dynamics of endemic diversification: molecular phylogeny suggests an
explosive origin of the Thiarid Gastropods of Lake Tanganyika, 31, 331
The dynamics of field population of the pine looper, Bupalis piniarius L. (Lep,
Geom.), 3, 207
Earthworm biotechnology and global biogeochemistry, 15, 369
Ecological aspects of fishery research, 7, 114
Eco-evolutionary dynamics of individual-based food webs, 45, 225
Ecological conditions affecting the production of wild herbivorous mam-
mals on grasslands, 6, 137
Ecological networks in a changing climate, 42, 71
Ecological and evolutionary dynamics of experimental plankton communi-
ties, 37, 221
Ecological implications of dividing plants into groups with distinct photo-
synthetic production capabilities, 7, 87
Ecological implications of specificity between plants and rhizosphere micro-
organisms, 31, 122
Ecological interactions among an Orestiid (Pisces: Cyprinodontidae) species
flock in the littoral zone of Lake Titicaca, 31, 399
Ecological studies at Lough Inc, 4, 198
Ecological studies at Lough Ryne, 17, 115
Ecology of mushroom-feeding Drosophilidae, 20, 225
The ecology of the Cinnabar moth, 12, 1
Ecology of coarse woody debris in temperate ecosystems, 15, 133; 34, 59
Ecology of estuarine macrobenthos, 29, 195
Ecology, evolution and energetics: a study in metabolic adaptation, 10, 1
Ecology of fire in grasslands, 5, 209
The ecology of pierid butterflies: dynamics and interactions, 15, 51
The ecology of root lifespan, 27, 1

The ecology of serpentine soils, 9, 225
Ecology, systematics and evolution of Australian frogs, 5, 37
Ecophysiology of trees of seasonally dry Tropics: comparison among pho-
nologies, 32, 113
Effect of flooding on the occurrence of infectious disease, 39, 107
Effects of food availability, snow, and predation on breeding performance of
waders at Zackenberg, 40, 325
Effect of hydrological cycles on planktonic primary production in Lake
Malawi Niassa, 31, 421
Effects of climatic change on the population dynamics of crop pests, 22, 117
Effects of floods on distribution and reproduction of aquatic birds, 39, 63
The effects of modern agriculture nest predation and game management
on the population ecology of partridges (Perdix perdix and Alectoris rufa),
11, 2
El Niño effects on Southern California kelp forest communities, 17, 243
Empirical evidences of density-dependence in populations of large herbi-
vores, 41, 313
Endemism in the Ponto-Caspian fauna, with special emphasis on the
Oncychopoda (Crustacea), 31, 179
Energetics, terrestrial field studies and animal productivity, 3, 73
Energy in animal ecology, 1, 69
Environmental warming in shallow lakes: a review of potential changes
in community structure as evidenced from space-for-time substitution
approaches, 46, 259
Environmental warming and biodiversity-ecosystem functioning in fresh-
water microcosms: partitioning the effects of species identity, richness
and metabolism, 43, 177
Estimates of the annual net carbon and water exchange of forests: the
EUROFLUX methodology, 30, 113
Estimating forest growth and efficiency in relation to canopy leaf area, 13,
327
Estimating relative energy fluxes using the food web, species abundance, and
body size, 36, 137
Evolution and endemism in Lake Biwa, with special reference to its gastro-
pod mollusc fauna, 31, 149
Evolutionary and ecophysiological responses of mountain plants to the
growing season environment, 20, 60
The evolutionary ecology of carnivorous plants, 33, 1
Evolutionary inferences from the scale morphology of Malawian Cichlid

fishes, 31, 377
Explosive speciation rates and unusual species richness in haplochromine
cichlid fishes: effects of sexual selection, 31, 235
The evolutionary consequences of interspecific competition, 12, 127
The exchange of ammonia between the atmosphere and plant communities,
26, 302
Faunal activities and processes: adaptive strategies that determine ecosystem
function, 27, 92
Fire frequency models, methods and interpretations, 25, 239
Floods down rivers: from damaging to replenishing forces, 39, 41
Food webs, body size, and species abundance in ecological community
description, 36, 1
Food webs: theory and reality, 26, 187
Food web structure and stability in 20 streams across a wide pH gradient, 42,
267
Forty years of genecology, 2, 159
Foraging in plants: the role of morphological plasticity in resource acquisi-
tions, 25, 160
Fossil pollen analysis and the reconstruction of plant invasions, 26, 67
Fractal properties of habitat and patch structure in benthic ecosystems, 30,
339
Free air carbon dioxide enrichment (FACE) in global change research: a
review, 28, 1
From Broadstone to Zackenberg: Space, time and hierarchies in ecological
networks, 42, 1
From natural to degraded rivers and back again: a test of restoration ecology
theory and practice, 44, 119
The general biology and thermal balance of penguins, 4, 131
General ecological principles which are illustrated by population studies of
Uropodid mites, 19, 304
Generalist predators, interactions strength and food web stability, 28, 93
Genetic and phenotypic aspects of lifehistory evolution in animals, 21, 63
Geochemical monitoring of atmospheric heavy metal pollution: theory and
applications, 18, 65
Global climate change leads to mistimed avian reproduction, 35, 89
Global persistence despite local extinction in acarine predator-prey systems:
lessons from experimental and mathematical exercises, 37, 183
Heavy metal tolerance in plants, 7, 2
Herbivores and plant tannins, 19, 263

High-arctic plant–herbivore interactions under climate influence, 40, 275
High-arctic soil CO2 and CH4 production controlled by temperature,
water, freezing, and snow, 40, 441
Historical changes in environment of Lake Titicaca: evidence from Ostra-
cod ecology and evolution, 31, 497
How well known is the ichthyodiversity of the large East African lakes? 31,
17
Human and environmental factors influence soil faunal abundance-mass
allometry and structure, 41, 45
Human ecology is an interdisciplinary concept: a critical inquiry, 8, 2
Hutchinson reversed, or why there need to be so many species, 43, 1
Hydrology and transport of sediment and solutes at Zackenberg, 40, 197
The Ichthyofauna of Lake Baikal, with special reference to its zoogeograph-
ical relations, 31, 81
Impact of climate change on fishes in complex antarctic ecosystems, 46, 351
Implications of phylogeny reconstruction for Ostracod speciation modes in
Lake Tanganyika, 31, 301
Importance of climate change for the ranges, communities and conservation
of birds, 35, 211
Individual-based food webs: species identity, body size and sampling effects,
43, 211
Industrial melanism and the urban environment, 11, 373
Inherent variation in growth rate between higher plants: a search for phys-
iological causes and ecological consequences, 23, 188; 34, 283
Insect herbivory below ground, 20, 1
Insights into the mechanism of speciation in Gammarid crustaceans of Lake
Baikal using a population-genetic approach, 31, 219
Integrated coastal management: sustaining estuarine natural resources, 29,
241
Integration, identity and stability in the plant association, 6, 84
Inter-annual variability and controls of plant phenology and productivity at
Zackenberg, 40, 249
Introduction, 38, 1
Introduction, 39, 1
Introduction, 40, 1
Isopods and their terrestrial environment, 17, 188
Lake Biwa as a topical ancient lake, 31, 571
Lake flora and fauna in relation to ice-melt, water temperature, and chem-
istry at Zackenberg, 40, 371
The landscape context of flooding in the Murray–Darling basin, 39, 85
Landscape ecology as an emerging branch of human ecosystem science, 12,
189
Late quaternary environmental and cultural changes in the Wollaston Forland
region, Northeast Greenland, 40, 45
Linking spatial and temporal change in the diversity structure of ancient
lakes: examples from the ecology and palaeoecology of the Tanganyikan
Ostracods, 31, 521
Litter fall, 38, 19
Litter production in forests of the world, 2, 101
Long-term changes in Lake Balaton and its fish populations, 31, 601
Long-term dynamics of a well-characterised food web: four decades of acid-
ification and recovery in the broadstone stream model system, 44, 69
Macrodistribution, swarming behaviour and production estimates of the
lakefly Chaoborus edulis (Diptera: Chaoboridae) in Lake Malawi, 31, 431
Making waves: the repeated colonization of fresh water by Copepod
crustaceans, 31, 61
Manipulating interaction strengths and the consequences for trivariate
patterns in a marine food web, 42, 303
Manipulative field experiments in animal ecology: do they promise more
than they can deliver? 30, 299
Mathematical model building with an application to determine the distribu-
tion of DurshanÒ insecticide added to a simulated ecosystem, 9, 133
Mechanisms of microthropod-microbial interactions in soil, 23, 1
Mechanisms of primary succession: insights resulting from the eruption of
Mount St Helens, 26, 1
Methods in studies of organic matter decay, 38, 291
The method of successive approximation in descriptive ecology, 1, 35
Meta-analysis in ecology, 32, 199
Microbial experimental systems in ecology, 37, 273
Microevolutionary response to climatic change, 35, 151
Migratory fuelling and global climate change, 35, 33
The mineral nutrition of wild plants revisited: a re-evaluation of processes
and patterns, 30, 1
Modelling terrestrial carbon exchange and storage: evidence and implica-
tions of functional convergence in light-use efficiency, 28, 57
Modelling the potential response of vegetation to global climate change, 22, 93

Module and metamer dynamics and virtual plants, 25, 105
Modeling individual animal histories with multistate capture–recapture
models, 41, 87
Mutualistic interactions in freshwater modular systems with molluscan com-
ponents, 20, 126
Mycorrhizal links between plants: their functioning and ecological signifi-
cances, 18, 243
Mycorrhizas in natural ecosystems, 21, 171
The nature of species in ancient lakes: perspectives from the fishes of Lake
Malawi, 31, 39
Nitrogen dynamics in decomposing litter, 38, 157
Nocturnal insect migration: effects of local winds, 27, 61
Nonlinear stochastic population dynamics: the flour beetle Tribolium as an
effective tool of discovery, 37, 101
Nutrient cycles and Hþ budgets of forest ecosystems, 16, 1
Nutrients in estuaries, 29, 43
On the evolutionary pathways resulting in C4 photosynthesis and cra-
ssulacean acid metabolism (CAM), 19, 58
Origin and structure of secondary organic matter and sequestration of C and
N, 38, 185
Oxygen availability as an ecological limit to plant distribution, 23, 93
Parasitism between co-infecting bacteriophages, 37, 309
Temporal variability in predator–prey relationships of a forest floor food web,
42, 173
The past as a key to the future: the use of palaeoenvironmental understand-
ing to predict the effects of man on the biosphere, 22, 257
Pattern and process of competition, 4, 11
Permafrost and periglacial geomorphology at Zackenberg, 40, 151
Phenetic analysis, tropic specialization and habitat partitioning in the Baikal
Amphipod genus Eulimnogammarus (Crustacea), 31, 355
Photoperiodic response and the adaptability of avian life cycles to environ-
mental change, 35, 131
Phylogeny of a gastropod species flock: exploring speciation in Lake
Tanganyika in a molecular framework, 31, 273
Phenology of high-arctic arthropods: effects of climate on spatial, seasonal,
and inter-annual variation, 40, 299
Phytophages of xylem and phloem: a comparison of animal and plant sapfeeders,
13, 135
The population biology and turbellaria with special reference to the fresh-
water triclads of the British Isles, 13, 235
Population cycles in birds of the Grouse family (Tetraonidae), 32, 53
Population cycles in small mammals, 8, 268
Population dynamical responses to climate change, 40, 391
Population dynamics, life history, and demography: lessons from Drosophila,
37, 77
Population dynamics in a noisy world: lessons from a mite experimental
system, 37, 143
Population regulation in animals with complex lifehistories: formulation and
analysis of damselfly model, 17, 1
Positive-feedback switches in plant communities, 23, 264
The potential effect of climatic changes on agriculture and land use, 22, 63
Predation and population stability, 9, 1
Predicted effects of behavioural movement and passive transport on individ-
ual growth and community size structure in marine ecosystems, 45, 41
Predicting the responses of the coastal zone to global change, 22, 212
Present-day climate at Zackenberg, 40, 111
The pressure chamber as an instrument for ecological research, 9, 165
Primary production by phytoplankton and microphytobenthos in estuaries,
29, 93
Principles of predator-prey interaction in theoretical experimental and nat-
ural population systems, 16, 249
The production of marine plankton, 3, 117
Production, turnover, and nutrient dynamics of above and below ground
detritus of world forests, 15, 303
Quantification and resolution of a complex, size-structured food web, 36,
85
Quantitative ecology and the woodland ecosystem concept, 1, 103
Realistic models in population ecology, 8, 200
References, 38, 377
The relationship between animal abundance and body size: a review of the
mechanisms, 28, 181
Relative risks of microbial rot for fleshy fruits: significance with respect to
dispersal and selection for secondary defence, 23, 35
Renewable energy from plants: bypassing fossilization, 14, 57
Responses of soils to climate change, 22, 163
Rodent long distance orientation (“homing”), 10, 63
The role of body size in complex food webs: a cold case, 45, 181
Scale effects and extrapolation in ecological experiments, 33, 161

Scale dependence of predator-prey mass ratio: determinants and applica-
tions, 45, 269
Scaling of food-web properties with diversity and complexity across ecosys-
tems, 42, 141
Secondary production in inland waters, 10, 91
Seeing double: size-based and taxonomic views of food web structure, 45,
67
The self-thinning rule, 14, 167
A simulation model of animal movement patterns, 6, 185
Snow and snow-cover in central Northeast Greenland, 40, 175
Soil and plant community characteristics and dynamics at Zackenberg, 40,
223
Soil arthropod sampling, 1, 1
Soil diversity in the Tropics, 21, 316
Soil fertility and nature conservation in Europe: theoretical considerations
and practical management solutions, 26, 242
Solar ultraviolet-b radiation at Zackenberg: the impact on higher plants and
soil microbial communities, 40, 421
Some economics of floods, 39, 125
Spatial and inter-annual variability of trace gas fluxes in a heterogeneous
high-arctic landscape, 40, 473
Spatial root segregation: are plants territorials? 28, 145
Species abundance patterns and community structure, 26, 112
Stochastic demography and conservation of an endangered perennial plant
(Lomatium bradshawii) in a dynamic fire regime, 32, 1
Stomatal control of transpiration: scaling up from leaf to regions, 15, 1
Stream ecosystem functioning in an agricultural landscape: the importance
of terrestrial–aquatic linkages, 44, 211
Structure and function of microphytic soil crusts in wildland ecosystems of
arid to semiarid regions, 20, 180
Studies on the cereal ecosystems, 8, 108
Studies on grassland leafhoppers (Auchenorrhbyncha, Homoptera) and their
natural enemies, 11, 82
Studies on the insect fauna on Scotch Broom Sarothamnus scoparius (L.)
Wimmer, 5, 88
Sustained research on stream communities: a model system and the compar-
ative approach, 41, 175
Systems biology for ecology: from molecules to ecosystems, 43, 87
The study area at Zackenberg, 40, 101

Sunflecks and their importance to forest understorey plants, 18, 1
A synopsis of the pesticide problem, 4, 75
The temperature dependence of the carbon cycle in aquatic ecosystems, 43,
267
Temperature and organism size – a biological law for ecotherms? 25, 1
Terrestrial plant ecology and 15N natural abundance: the present limits to
interpretation for uncultivated systems with original data from a Scottish
old field, 27, 133
Theories dealing with the ecology of landbirds on islands, 11, 329
A theory of gradient analysis, 18, 271; 34, 235
Throughfall and stemflow in the forest nutrient cycle, 13, 57
Tiddalik’s travels: the making and remaking of an aboriginal flood myth, 39,
139
Towards understanding ecosystems, 5, 1
Trends in the evolution of Baikal amphipods and evolutionary parallels with
some marine Malacostracan faunas, 31, 195
Trophic interactions in population cycles of voles and lemmings: a model-
based synthesis 33, 75
The use of perturbation as a natural experiment: effects of predator introduc-
tion on the community structure of zooplanktivorous fish in Lake Victoria,
31, 553
The use of statistics in phytosociology, 2, 59
Unanticipated diversity: the discovery and biological exploration of Africa’s
ancient lakes, 31, 1
Understanding ecological concepts: the role of laboratory systems, 37, 1
Understanding the social impacts of floods in Southeastern Australia, 39, 159
Using fish taphonomy to reconstruct the environment of ancient Lake
Shanwang, 31, 483
Using large-scale data from ringed birds for the investigation of effects of
climate change on migrating birds: pitfalls and prospects, 35, 49
Vegetation, fire and herbivore interactions in heathland, 16, 87
Vegetational distribution, tree growth and crop success in relation to recent
climate change, 7, 177
Vertebrate predator–prey interactions in a seasonal environment, 40, 345
Water flow, sediment dynamics and benthic biology, 29, 155
When microscopic organisms inform general ecological theory, 43, 45
Zackenberg in a circumpolar context, 40, 499
The zonation of plants in freshwater lakes, 12, 37.

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ADVANCES IN ECOLOGICAL

32 Jamestown Road, London NW1 7BY, UK

First edition 2012

Copyright © 2012 Elsevier Ltd. All rights reserved.

No part of this publication may be reproduced, stored in a retrieval system

For information on all Academic Press publications

Printed and bound in UK

Marcus A.M. De Aguiar

Evaluating the consequences of global change is a major challenge in current

although the latter focuses on the effects of warming on stream ecosystems.

ON THE WISHLIST: BETTER DATA AND PREDICTIVE

of body size and behaviour in determining the structure and dynamics of

A MATTER OF TIME AND SPACE: TEMPORAL AND

and contributions here (e.g. Hagen et al., 2012) and in recent or

based framework that can incorporate these different functional properties

THE NEXT STEPS FORWARD . . .

in concert (Walther et al., 2002; Woodward et al., 2010a). Predicting the

Advances in Ecological Research, Volume 46 # 2012 Elsevier Ltd 1

Our analysis allows us to assess consequences of the relocation or removal of fish

1.1. Vexing drivers and responses

different productivity (e.g. Hartnett and Wilson, 1999; Klironomos et al.,

1.2. Contrasting dichotomies

Linear response (%) Quadratic response (%)

Terrestrial invertebrates Terrestrial invertebrates

Aquatic invertebrates Aquatic invertebrates

Figure 1 Meta-analysis of the biomass/production and biodiversity relationships pub-

avoid competitive exclusion under low productivity, or species adapted to

investment have been hypothesized to be responsible for many observed

1.3. Aims of our study

Previous attempts to compare different monophyletic assemblages with

1. analyze biodiversity–productivity relationships in the framework of EF

2.2. Green world allometry

Log respiration mmol CO2 / shoot / s (20 °C)

0 0.0001 0.00011 0.00023 0.51

2.3. Allometry and management

individual metabolism in a community (e.g. roughly comparing angio-

the emergent characteristics of large data sets of organisms (Jonsson et al.,

This is in contrast to the nitrogen uptake by zooplankton, whose smaller

3.2. How local biodiversity determines individual abundances

Lepidoptera metabolic rate

productive sites of that study (physically isolated water-filled microhabitats such as

To test the MIH model of Srivastava and Lawton (1998), we analyzed

Invertebrate abundance (counts/m2)

Temperate soil microarthropods

(like nematodes, enchytraeids, mites and collembolans) clearly have a much

3.3. The extent to which scaling changes between taxocenes

S¼N 0:25 ¼M 0:75

Fish traits Predictors

Examples: pH; hardness; dissolved oxygen

omnivory and piscivory dominate) or a skew towards specialists (low Ct

species-related traits and size-related guilds within the Pisces monophyletic

4.2. Inland water biodiversity: Effects of landscape

4.2.2 Computational methods

4.2.3 Can a web be robust?

Connectance (C) Linkage density (L/S) Biodiversity (S)

0.0 *** * 0.0

0.0 *** ** 0.0

0.0 *** *** 0.0

One common measure of a food web’s vulnerability to extinctions is

S¼N 0:25 ¼M 0:75

0.0 * 0.0

0.0 * * 0.0