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Understanding the biodiversity consequences of habitat change: The value of

secondary and plantation forests for Neotropical dung beetles

Article in Journal of Applied Ecology · March 2008

DOI: 10.1111/j.1365-2664.2008.01454.x

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Journal of Applied Ecology 2008 doi: 10.1111/j.1365-2664.2008.01454.x

Understanding the biodiversity consequences of habitat

Blackwell Publishing Ltd

change: the value of secondary and plantation forests

for neotropical dung beetles
Toby A. Gardner1*, Malva I.M. Hernández2, Jos Barlow3,4 and Carlos A. Peres1
1
Centre for Ecology, Evolution and Conservation, School of Environmental Sciences, University of East Anglia, Norwich
NR4 7TJ, UK; 2Universidade Federal da Paraíba, Cidade Universitária-Campus I, CEP 58059–900 João Pessoa, Paraíba,
Brazil; 3Museu Paraense Emílio Goeldi (MPEG), Avenue, Perimetral 1901, Bairro Terra Firme, Belém-Pará, 66077–530,
Brazil; and 4Lancaster Environment Centre, Lancaster University, Lancaster LA1 4YQ, UK

Summary
1. Secondary and plantation forests are becoming increasingly widespread in the tropics. A recent
meta-analysis on the impacts of land-use change on tropical forest dung beetles concluded that
regenerating forests can be effective in helping to offset species loss following deforestation. How-
ever, our understanding of the extent to which these results can be generalized to new locations
remains very poor.
2. We attempted to overcome many of the design limitations that characterize previous studies by
collecting spatially independent dung beetle samples from primary, secondary and Eucalyptus
plantation forests in north-east Brazilian Amazonia across a large quasi-experimental landscape
that minimized confounding edge and fragmentation effects.
3. We recorded 9203 dung beetles, comprising 85 species. Species richness was significantly higher
in primary forest and the majority of species were more abundant there than elsewhere, whereas
secondary and plantation sites harboured an impoverished subset of primary forest species.
4. Our data illustrate the low value of tropical secondary and plantation forests for dung beetles in
our study area, and our conclusions are more pessimistic than those of earlier studies.
5. Because of differences in the order of species rank-abundance and rank-biomass patterns,
re-coding community data from abundance to biomass significantly altered the analytical weight of
individual species in determining community patterns. Larger bodied beetles were more prone to
local extinctions and abundance declines and this effect was consistent both within and between
genera.
6. Synthesis and applications. Our study demonstrates that secondary and plantation forests in a
large neotropical landscape host exceptionally impoverished dung beetle communities. Furthermore,
the depletion of beetle abundance combined with a reduction in average body mass in converted
forests is likely to have detrimental consequences for the maintenance of dung beetle-mediated
ecosystem services in these habitats. Differences in biogeographical and landscape context, and the
influence of common limitations in sampling design, may explain why many other studies have
painted a more optimistic picture of the conservation value of anthropogenic habitats. In the
absence of further evidence we caution strongly against the claim that forest regeneration schemes
on degraded land can effectively offset the loss of species following deforestation, and urge that
conservation strategies prioritize the protection of remaining areas of primary forest.
Key-words: Scarabaeinae, tropical forests, habitat change, habitat value, deforestation, Brazil,
sampling bias, biomass

*Correspondence author. E-mail: tobyagardner@gmail.com

© 2008 The Authors. Journal compilation © 2008 British Ecological Society

2 T. A. Gardner et al.

produce very different results, subject to potentially different

Introduction
ecological interpretations (Vulinec 2002).
The survival of many tropical forest species is dependent on The primary aim of this study was to contribute to our
conservation management in human-dominated landscapes understanding of the value of primary, secondary and plan-
as a consequence of the rapid rate of tropical deforestation tation forests for tropical dung beetles. Working within a large
and the inadequacy of existing protected areas (Daily 2001). quasi-experimental forestry landscape allowed us to over-
While the conversion of primary forest for intensive agri- come many design limitations, including access to extensive
culture inevitably leads to dramatic losses in biodiversity, primary forest controls, minimizing the confounding influ-
conservation biologists are far less certain about the conservation ence of edge effects and habitat fragmentation and maxi-
value of more structurally complex secondary and planted mizing the spatial independence among sites of each forest
forests (Dunn 2004; Wright & Muller-Landau 2006; Gardner type. We compared patterns of species richness, abundance
et al. 2007a; Laurance 2007). This lack of consensus is and diversity with the results of a recent meta-analysis on the
illustrated in a series of recent reviews on a variety of taxa, consequences of tropical forest modification for dung beetles
including birds (Barlow et al. 2007a), amphibians and reptiles (Nichols et al. 2007), and hypothesize that the conclusions
(Gardner, Barlow & Peres 2007) and butterflies (Barlow et al. reached by Nichols et al. (2007) paint an overly optimistic
2007b; Koh 2007). This uncertainty, coupled with the rapid picture of the conservation value of these habitats. Finally, we
expansion of secondary (Wright 2005) and plantation forests evaluated the potential implications of converting abundance
(FAO 2006) across the tropics, highlights the need for more data into biomass data when examining the structure of dung
biodiversity research in human-dominated landscapes. beetle communities in response to landscape change.
Dung beetles (Coleoptera: Scarabaeinae) form an impor-
tant component of the tropical forest insect fauna (Peck &
Methods
Forsyth 1982), contributing to several key functional roles,
such as secondary seed dispersal, nutrient recycling, soil STUDY AREA AND SITE SELECTION
aeration and control of vertebrate parasites (Andresen & Feer
The project was conducted within a 1·7-Mha landholding located in
2005). Dung beetles can also be sampled more cost-effectively
the state of Pará in north-eastern Brazilian Amazonia (00°27′00′–
than many other rainforest taxa, and have been proposed
01°30′00′ S, 51°40′00′–53°20′00′ W), containing 53 000 ha of Eucalyptus
as effective indicators of landscape change (Gardner et al.
plantations and a similar area of regenerating native vegetation,
2008). A recent meta-analysis on the consequences of land- embedded within a large and virtually undisturbed primary forest
scape change for tropical forest dung beetles showed that, matrix (> 500 000 ha). Fifteen study sites were established, with five
while clear-felling and intensive agriculture led to significant replicates each in primary rainforest, ‘mature’ Eucalyptus plantations
reductions in diversity, land uses that maintained a high (4–5 years old) and even-aged secondary forest (14 –19 years since
degree of forest cover and relatively high vegetation complex- abandonment) (for a map and more detailed habitat descriptions
ity (such as secondary forests) held species-rich dung beetle see Barlow et al. 2007a). The scale of the landscape allowed us to
communities similar to those found in intact areas (Nichols select sites that were both spatially independent [mean distance
et al. 2007; cf. Vulinec 2002; Quintero & Roslin 2005; Vulinec, between primary, secondary and Eucalyptus sites was 30 km (range
14–67), 9 km (4–44) and 11 km (7–50), respectively] and of sufficient
Lambert & Mellow 2006). Although these preliminary results
size [mean size of Eucalyptus and secondary forest blocks was 1687 ha
demonstrate the potential biodiversity value of forest regen-
(range 574 –3910) and 2682 ha (1079–3508), respectively] to minimize
eration following deforestation, there are some important
problems of spatial pseudoreplication and edge effects. Moreover,
reasons to cast doubt on these conclusions. Eucalyptus and secondary forest sites were located at similar mean
First, Nichols et al.’s (2007) meta-analysis is based upon a distances from the nearest areas of continuous primary forest [1124
relatively small number of studies. For example, only seven m (range 550–2300) and 1316 m (650–2800), respectively].
studies on late secondary forests (> 15 year) and six studies
on tree plantations were available for analysis across the tropics
DUNG BEETLE SAMPLING
(Nichols et al. 2007), and there were marked between-study
differences in the habitat types sampled (e.g. plantation forests Dung beetles (Coleoptera: Scarabaeinae) were sampled using pitfall
comprised of different tree species and different types of under- traps (20 cm diameter, 15 cm depth) buried flush with the ground
storey vegetation). Secondly, almost all of the studies were and baited with c. ~20 g of fresh human dung, the most effective bait
confounded by the methodological problems that are present for dung beetle studies in the neotropics (for a similar design see
in many tropical biodiversity studies (Barlow et al. 2007c; Larsen & Forsyth 2005). Five traps were placed at each site, sepa-
rated by 200 m along a linear 1-km transect.
Gardner et al. 2007a) and often result in a near best-case scenario
Trapping was conducted twice at each site, coinciding with the early
of the value of converted forest for biodiversity (Dunn 2004).
dry (July–August 2004) and mid-wet (April–May 2005) seasons. Traps
Finally, very few studies have evaluated patterns of biomass
were operated for 2 × 24-h periods at each site in both seasons, with
when detailing the response of dung beetle communities to the captured individuals removed and bait being replaced every 24 h.
habitat change (Nichols et al. 2007). However, species abundance All captures were later processed in a laboratory and separated to
often provides a poor predictor of biomass in arthropod com- species. Where species names were unknown a series of morphospecies
munity data (Saint-Germain et al. 2007), such that analyses numbers was assigned to each genus. To obtain body mass estimates
employing either abundance or biomass data alone may for each species, a sample of between 1 and 31 individuals (median

© 2008 The Authors. Journal compilation © 2008 British Ecological Society, Journal of Applied Ecology
 Land-use change and tropical forest dung beetles 3

= 12, mode = 30) was dried in a constant-temperature oven at 60 °C based separately on abundance and biomass data (Saint-Germain
for 1 week prior to weighing on a balance accurate to 0·0001 g (see et al. 2007). We used non-metric multidimensional scaling (MDS) to
Table S1 in the supplementary material). define the overall differences in community structure within and
between habitats based on each matrix type, implemented in
PRIMER v·5 (PRIMER-E, Plymouth Marine Laboratory, UK).
DATA ANALYSIS Ordinations were conducted using site-standardized and square-
root transformed data and the Bray–Curtis similarity index,
Patterns of species richness and abundance although patterns were qualitatively similar when using either
untransformed or presence–absence data. We used analysis of
Comparisons of species richness among habitat types were made by
similarities (; Clarke & Warwick 2001) to test for significant
visual assessment of overlapping 95% confidence intervals on indi-
differences in multivariate community structure between forests
vidual-based rarefaction curves (Gotelli & Colwell 2001) imple-
for each data type, and a non-parametric Mantel test (;
mented in EstimateS v·7.5 (Colwell 2005). Species richness, total
Clarke & Warwick 2001) to compare directly the abundance and
abundance and species-rank abundance distributions varied little
biomass-based similarity matrices.
between seasons (see Appendix S1 in the Supplementary material)
Finally, to detect differences in the analytical weight of individual
and data were therefore pooled across all samples for each analysis.
species in discriminating patterns of community turnover when
To describe patterns of beta diversity across the landscape, we
using abundance vs. biomass data, we calculated the similarity per-
calculated the average number of species absent in each site defined
centage contribution (; Clarke & Warwick 2001) of each spe-
as β = γ – α, where γ is the number of species sampled in the entire
cies, and plotted the percentage values for abundance vs. biomass
landscape (gamma diversity) and α is the average number of species
data for both pairwise habitat dissimilarities and within-habitat
present at a given site (alpha diversity). This approach is used as a
community similarities.
measure of additive partitioning of diversity and allows for a direct
comparison between alpha and beta diversities in terms of numbers
(or percentage) of species (Gardner et al. 2007b). Evaluating the effects of habitat change on dung beetle
We compared the relative abundance of ‘common’ (> 15 cap- body mass and biomass
tures) primary forest species in each of the three habitat types by
scaling species’ abundances in each site by the average abundance Overall differences between habitat types in the average body mass
for that species across all sites in the landscape. The average scaled per species (irrespective of individuals) and per individual (irre-
abundances for all species were then plotted for each habitat in turn. spective of species), as well total biomass (body mass × individuals
Deviation from the expected abundance (i.e. if all individuals of a summed across species), were compared using non-parametric
species were randomly distributed across all 15 sites of the three Kruskal–Wallis tests. To control for the impact of changes in the
habitats) was evaluated by comparing the mean and 95% bias- abundance of species of a particular size on observed habitat differ-
corrected bootstrap confidence interval (Efron 1987) for each species ences in body mass, we examined relationships within individual
with the scale factor of 1. If the confidence interval fell above or genera in cases where multiple representatives of a given genus
below 1 then the abundance of that species in a given habitat was occurred across different habitat types. As well as providing a proxy
significantly different from that expected by chance (P = 0·05). correction for phylogenetic differences (the true phylogeny for all
species being unknown), comparisons within genera also provide a
proxy for gross differences in beetle size and functional behaviour
Comparison with a recent meta-analysis (Vulinec 2002). Comparisons were only made in cases where there
were more than 10 individuals (and ≥ 2 species) of a given genus in
We compared our data with the results of the meta-analysis by
each between-habitat pairwise comparison. Average species body
Nichols et al. (2007) by visually comparing the 95% bootstrapped
sizes (and pooled biomass values) for each genus in secondary and
confidence intervals for standardized community parameters
plantation forest sites were scaled against the average values
reported in the meta-analysis with the single value for the same
obtained for primary forest sites.
parameters calculated using our data. The six parameter values
examined were: total number of species and individuals, total
number of primary forest species and individuals, community simi-
larity (Morista–Horn similarity index) and community evenness
Results
(Pielou’s evenness index). Parameter values in Nichols et al. (2007)
were standardized relative to values calculated for intact forest sites PATTERNS OF SPECIES RICHNESS AND ABUNDANCE
in each study (Dunn 2004).
We captured totals of 9203 individuals and 85 species of dung
beetle, with 5208 individuals and 72 species in primary forest,
Comparing dung beetle communities with both abundance 2077 individuals and 48 species in secondary forests, and 1918
and biomass data individuals and 43 species in Eucalyptus plantations (see
Table S1 in the supplementary material). Sample representa-
The biomass of each species in each site was calculated by multiply-
tion (of beetles attracted to human faeces) was estimated to
ing the mean body mass by the total abundance for that species,
such that the pooled species biomass was the sum of all species prod-
be ≥ 83% in each habitat type (see Table S2 in the supplemen-
ucts (Peck & Howden 1984). The interspecific relationship between tary material).
body mass and abundance was examined using linear regression on We captured significantly more species and individuals
log-transformed data (Saint-Germain et al. 2007). in primary forest than in secondary forests or Eucalyptus
We evaluated patterns of community turnover between the three plantations, which were indistinguishable from each other
forest types by constructing two separate community matrices, in terms of both species richness and abundance (Fig. 1).
© 2008 The Authors. Journal compilation © 2008 British Ecological Society, Journal of Applied Ecology
4 T. A. Gardner et al.

Fig. 1. Individual-based rarefaction curves for dung beetles in

primary, secondary and Eucalyptus plantation forests. Fitted dotted
lines indicate 95% confidence intervals.

Seventy-nine per cent of species were recorded in primary for-

est and 31% of all species were unique to this habitat (see
Table S2 in the supplementary material). In contrast, only
56% and 50% of all species were recorded in secondary and
Eucalyptus forest, respectively (see Table S2 in the supplemen-
tary material). Discounting occasional species whose distri-
bution may represent sampling artefacts (i.e. those that were
captured less than five times), 99% and 86% of species cap-
tured in secondary and plantation forests, respectively, were
also found in primary forest. The gamma diversity of the
entire landscape can be expressed in an additive form as: 85
[γ] = 28 [α] + 57 [β]. Beta diversity contributed 39%, 49% and
62% of the total gamma diversity for primary, secondary and
Eucalyptus forests, respectively.
Fig. 2. Scaled mean abundances (solid circles) for primary forest
Species-abundance distributions were also strongly nested dung beetle species in (a) primary, (b) secondary and (c) plantation
across the three habitats, and the majority of species recorded forests. Species that fall above the average value for the entire
in both primary and converted habitats had markedly higher landscape (scale parameter = 1) are more likely to occur in that forest
abundances in primary forest sites (Fig. 2). Eighty-three per type than would be expected by chance; (a) clearly demonstrates that
most individuals of more and less abundant species were found in
cent of these species had a greater average abundance in pri-
primary forest. Bias-corrected 95% bootstrap confidence intervals
mary forest than was expected by chance, and the difference are presented where data were sufficient. The secondary axis (shaded
was significant for 28%. This pattern was consistent irrespec- bars) complements the pattern of average abundances, and illustrates
tive of whether species were relatively common or rare in our the total number of captures of each species in each forest type,
samples (Fig. 2). compared with the rank abundance across all samples (the grey line
and dots). Darker bars identify species that were confined to a single
habitat.
COMPARISON WITH A RECENT META-ANALYSIS

Compared with primary forest controls, the total species rich- plantation studies (Fig. 3). The standardized difference in
ness and abundance of dung beetles in secondary forests was community composition of plantation samples from primary
significantly, or nearly significantly, lower than the conclu- forest controls was similar to that found for other studies,
sions from the recent meta-analysis by Nichols et al. (2007) while our secondary forest samples were more distinct from
(Fig. 3). This result was consistent when compared with the (but within the confidence intervals of ) the results of the
results of other studies that sampled both young (< 10 years) meta-analysis (Fig. 3).
and old (> 15 years) secondary forest sites. Although our
study was in broad agreement with the findings of Nichols
COMPARING ABUNDANCE AND BIOMASS DATA
et al. (2007) that plantation forests have greatly reduced spe-
cies richness, we found a large decrease rather than an There was no relationship between species body mass and
increase in dung beetle abundance. Community evenness in abundance (R2 = 0·001, P = 0·82, n = 76), and this pattern
our study was similar to that found in other studies of sec- was consistent when comparing among species for each
ondary forest, and greater than the evenness recorded in most genus in turn (n = 7 genera with > 3 species, mean R2 = 0·11,
© 2008 The Authors. Journal compilation © 2008 British Ecological Society, Journal of Applied Ecology
 Land-use change and tropical forest dung beetles 5

meant that individual species often contributed a very differ-

ent weight to each analysis (Fig. 6). In particular, when trans-
forming abundance to biomass data, the analytical weight of
larger bodied species invariably increased, while the weight of
smaller bodied species either decreased or remained similar
(Fig. 6). Consequently, in almost all cases less than half of the
top 10 weighted species were the same for abundance and bio-
mass-based analyses (see Tables S3 and S4 in the supplemen-
tary material).

EVALUATING THE EFFECTS OF HABITAT CHANGE ON

BODY MASS AND BIOMASS

A significantly greater mean site biomass of dung beetles was

recorded in primary forest sites (mean 102 g, SE 15·6) than
either secondary (mean 26·7 g, SE 8·5) or plantation (mean
20·2 g, SE 6·9) forests (Kruskal–Wallis; χ2 = 9·5, P = 0·009,
d.f. = 2). In addition to diminished abundances (Figs 1 and
2), this difference could be attributed to the fact that the aver-
age body mass of both species (mean 0·011 g, SE 0·0017, n =
5) and individuals, irrespective of species (mean 0·083 g,
SE 0·065) in primary forest, was greater than that in either
secondary (mean 0·0029 g and 0·045 g for species and indi-
viduals, respectively) or plantation forests (mean 0·0022 g
and 0·031 g) (Kruskal–Wallis; species body mass χ2 = 9·5, P
= 0·009, individual body mass χ2 = 6.7, P = 0·035, d.f. = 2).
Fig. 3. Comparison of standardized community parameters in (a) The community-level pattern of reduced species body size
secondary and (b) Eucalyptus forests (scaled by average values from and pooled biomass outside primary forest was consistent
intact forest; grey bar) between this study (circles) and similar studies within different genera, irrespective of the huge variation in
elsewhere, presented in a recent meta-analysis by Nichols et al. mean body size of species between the largest (Coprophaneus;
(2007), illustrated by bias-corrected 95% bootstrap confidence
intervals. For secondary forest, grey and black confidence intervals
0·96 g) and smallest genera (Uroxys; 0·003 g; Fig. 7). In some
describe the findings of studies in young (< 10 years) and old cases, primary forest species were larger because the largest
(> 15 years) secondary forests, respectively. Plantation forests in representatives of any given genus were wholly confined to
Nichols et al. (2007) included other timber and crop species. Values primary forest samples (e.g. Onthophagus onthochromus,
for species richness and abundance in our study are consistently lower Canthidium sp. 2, Ateuchus sp. 2 and Uroxys sp. 3), while in
than those reported in other studies.
others it was more simply a function of larger species being
more likely to occur in a primary forest site (e.g. Copropha-
SE = 0·069, P > 0·12 in all cases). In contrast, there was a naeus lancifer, Eurysternus hamaticollis and Oxysternon fes-
positive relationship between species abundance and total tivum; see Table S1 in the supplementary material).
biomass for all sites combined and for each individual forest
type (Fig. 4; with consistent within-genus patterns, mean
Discussion
R2 = 0·68, SE = 0·1 and P < 0·05 in all cases, except Delto-
chilum which showed no relationship). However, there was
VALUE OF PRIMARY, SECONDARY AND PLANTATION
considerable variance in the abundance–biomass relationship
FORESTS FOR DUNG BEETLES
across all species, with marked discrepancies in the rank-
abundance and rank-biomass of individual species (overall The overall conclusion from our study is that dung beetle
R2 < 0·40 in all forest types; Fig. 4). communities in both secondary forest and Eucalyptus plan-
Despite the relatively weak relationship between species tations in our study area are severely impoverished compared
abundance and biomass distributions, patterns of turnover in with neighbouring areas of primary forest. Although planta-
overall community structure among sites were similar when tion areas were not ‘green deserts’, both Eucalyptus and
analysed using either data type (Fig. 5; , Rho = 0·9, P secondary forests in Jari harbour a depleted subset of primary
< 0·001) and both the abundance and biomass matrices were forest species. The prediction that human impacts in managed
equally effective at discriminating among habitats (Fig. 5; landscapes can have a negative effect on site (alpha)-level pat-
; abundance data, global R = 0·56, P < 0·001, all pair- terns of species richness, but promote higher gamma diversity at
wise comparisons P < 0·032; biomass data, global R = 0·61, the landscape scale (Halffter, Favila & Halffter 1992; Arellano
P < 0·001, all pairwise comparisons P < 0·008). However, & Halffter 2003) was only very weakly supported as few
discrepancies in abundance–biomass relationships (Fig. 4) open-area species colonized areas outside primary forest.
© 2008 The Authors. Journal compilation © 2008 British Ecological Society, Journal of Applied Ecology
6 T. A. Gardner et al.

Fig. 4. Species rank-abundance curves (lines) for dung beetles sampled across the entire Jari landscape, and separately for primary, secondary
and plantation forests, with biomass values superimposed (bars). Linear regressions between species abundance and species biomass are
presented as insets. All data are log10 transformed.

Furthermore, we found no evidence of density compensation (Sowig 1995). Numerous observational and experimental
by habitat generalists or open-area specialists, and species- studies have demonstrated the strength of interspecific
poor habitats consistently held fewer individuals of both competition for ephemeral dung resources in dung beetles
relatively rare and relatively common species, highlighting the (reviewed in Horgan & Fuentes 2005). Three lines of indirect
fact that the relationship between rarity and local extinction evidence indicate that the availability of mammalian dung
risk remains poorly understood (Gaston 1994). resources is markedly lower outside primary forest in our
The restructuring of dung beetle communities following study landscape. (i) Primates are known to be keystone
habitat change is frequently explained by two non-exclusive resource providers for many dung beetles (Estrada, Anzures
hypotheses: changes in vegetation structure and changes in & Coates-Estrada 1999) and their biomass was reduced by an
the availability of mammalian dung resources. It is well order of magnitude in Eucalyptus sites and by about half in
known that dung beetle communities that are closely associ- secondary forest (C. A. Peres, unpublished data). (ii) High
ated with tropical forest habitats are greatly influenced by ambient temperatures outside primary forest can rapidly
differences in vegetation structure (Halffter & Matthews desiccate dung piles, making them inaccessible to many beetles
1966; Halffter, Favila & Halffter 1992; Halffter & Arellano (Peck & Forsyth 1982). (iii) Scavenger flies were more abun-
2002), with individual species often having specific affinities for dant in plantation and secondary forests than in primary
certain structural habitat properties (Davis et al. 2001). Fur- forest (Barlow et al. 2007c), potentially increasing competition
thermore, secondary forests and Eucalyptus plantations in Jari, within the wider dung insect community. Although it is diffi-
like elsewhere, are typically characterized by low, relatively cult to ascertain the relative importance of vegetation struc-
open canopies with hot and dry understorey environments. ture and resource availability for structuring dung beetle
These microclimatic differences could help explain the communities, we predict that the latter is likely to have a
observed impoverishment of dung beetle communities weaker influence in Jari, as few tropical forest dung beetles are
through a physiological intolerance to high temperatures resource specialists (Peck & Forsyth 1982; Larsen, Lopera &
(Chown 2001), the influence of solar radiation on adult activ- Forsyth 2006) and the biomass of small-bodied primates,
ity patterns (Lobo, Lumaret & Jay-Robert 1998) or the influ- large rodents and ungulates remains relatively high outside
ence of decreased soil moisture content on larval survival primary forest (C. A. Peres, unpublished data).
© 2008 The Authors. Journal compilation © 2008 British Ecological Society, Journal of Applied Ecology
 Land-use change and tropical forest dung beetles 7

cacao (Theobroma cacao) and oil palm (Elaeis guineensis).

Furthermore, while it is possible that conditions of relatively
poor soil quality and low productivity in the geologically
older (> 300 million years) central and eastern Amazon
region could lead to a more generally impoverished native
biota (including dung beetles; Radtke, da Fonseca & William-
son 2007), the fact that our primary forest sites contained
highly abundant and diverse samples suggests that this is
unlikely to explain the observed patterns.
Secondly, it is likely that community-level consequences
of habitat change are strongly influenced by differences in
biogeographical context and the available pool of regional
colonists (Nichols et al. 2007). The vast majority of neotropical
dung beetles are forest dwellers, unable to persist in artificially
open and more xeric environments (Howden & Nealis 1975;
Klein 1989). This situation may be exacerbated in lowland
areas, where species may have lower physiological tolerances
to microclimatic change (Janzen 1967). As a result, continu-
ally forested lowland sites often exhibit highly nested patterns
of species distribution, with few open-habitat specialists (this
study but see also Vulinec 2002; Escobar 2004). In contrast,
forested areas adjacent to open habitats (most notably large
natural savanna regions such as west Africa; Davis & Philips
2005; but also areas that have been heavily deforested histor-
ically, such as central America; Halffter, Favila & Halffter
1992; and the Andes; Medina, Escobar & Kattan 2002) are
characterized by a much stronger turnover in species compo-
Fig. 5. Multidimensional scaling (MDS) ordination of dung beetle sition, with open habitat specialists elevating the alpha diver-
community structure across primary, secondary and plantation sity of disturbed forests and increasing overall landscape
forests based on the abundance (a) and biomass (b) data. The three
diversity (Arellano & Halffter 2003).
habitats host largely distinct dung beetle communities and converting
abundance data into biomass data gives a superficially very similar Finally, many existing studies on habitat change suffer
pattern. Patterns were similar using both transformed (presented) from methodological limitations that can dilute the perceived
and untransformed data. effect of forest conversion on biodiversity (Gardner et al.
2007a). Such sampling problems are increasingly recognized
as widespread in biodiversity studies in general (Hamer &
Hill 2000; Hill & Hamer 2004; Barlow et al. 2007a, b, c; Gardner
COMPARISON WITH A RECENT META-ANALYSIS
et al. 2007b; Gardner, Barlow & Peres 2007; Koh 2007). Key
Our results contrast markedly with the consensus reported by issues include the following. (i) The size and matrix context
Nichols et al. (2007), which suggests that regenerating sec- of secondary and plantation sites. Many studies are subject
ondary forests may be effective in mitigating future losses in to edge and spill-over effects (of dung beetles and also the
dung beetle diversity following continued deforestation mammal species upon which they depend; Medina, Escobar
(Nichols et al. 2007; Shahabuddin, Schulze & Tscharntke & Kattan 2002; Vulinec 2002; Shahabuddin, Schulze &
2004; Quintero & Roslin 2005; Vulinec, Lambert & Mellow Tscharntke 2004; Avendaño-Mendoza et al. 2005; Quintero
2006). In further contrast, Nichols et al. (2007) concluded & Roslin 2005). Also, small modified forest patches that are
that dung beetle abundance was a poor metric for distinguish- surrounded by primary forest may have a more humid micro-
ing community responses across habitat modification gradi- climate than larger and more isolated areas of converted for-
ents because of the large numbers of beetles often found in est (Avendaño-Mendoza et al. 2005). (ii) The size and quality
degraded forests, whereas we found low levels of abundance of control sites. Many studies, particularly those in Mesoa-
in both secondary and plantation forests. merica (Avendaño-Mendoza et al. 2005), Andean countries
We have examined three potential explanations for these (Medina, Escobar & Kattan 2002; Escobar 2004) and parts of
significant discrepancies. First, it is possible that there is south-east Asia (Boonrotpong, Sotthibandhu & Pholpunthin
something unique about the types of habitats we sampled or 2004), have access only to relatively small and isolated frag-
the Jari landscape in general. However, our secondary forest ments of semi-degraded primary forest, which are unlikely to
sites were older than many in the meta-analysis by Nichols be representative of pre-disturbance conditions. (iii) The spa-
et al. (2007) and, although there are no previous studies of tial extent of study landscapes. Although it is often logistically
Eucalyptus plantations, other studies have encompassed a challenging (or impossible) to secure spatially independent
wide variety of perennial crops, including coffee (Coffea spp.), samples of both treatment and control forests, the fact that we
© 2008 The Authors. Journal compilation © 2008 British Ecological Society, Journal of Applied Ecology
8 T. A. Gardner et al.

Fig. 6. Percentage contributions, based

separately on abundance and biomass data,
of individual species towards patterns of
community structure between (a–c) and
within (d–f ) habitats. Species are represented
by black circles, which are scaled by
differences in average body mass. Both axes
are logged so the species in the top right
corner of each panel contribute the most
towards the patterns (see Tables S3 and S4 in
the supplementary material for identities of
top-ranked species). The diagonal dashed
line identifies the position of species that
contribute equal weights to analyses based on
both data sets, so that large-bodied species
clearly contributed the most to patterns
based on biomass data. Total percentage
dissimilarity and similarity values are
displayed next to each axis, and are almost
identical for each data type.

found a high (33–62%) turnover in species composition believe that our findings are therefore vital in moderating
across sites in all three habitats illustrates the importance of optimistic generalizations about the conservation value of
conducting studies at a landscape scale (Arellano & Halffter these habitats elsewhere (Wright & Muller-Landau 2006).
2003).
In conclusion, we believe that one of the most probable
COMMUNITY-WIDE EROSION OF DUNG BEETLE BODY
explanations for the differences between our results and those
MASS AND BIOMASS
of the studies reviewed by Nichols et al. (2007) relates to the
large spatial scale and experimental design of our study. Although community analyses based upon species abund-
While our study area may not be typical of a highly frag- ance and species biomass data may produce superficially
mented landscape, it does present an almost unique oppor- similar patterns, these may be driven by distinct sets of species
tunity for understanding the value of large secondary and (Fig. 6) that are potentially associated with distinct ecological
plantation forest blocks for tropical forest dung beetles. We mechanisms (Peck & Forsyth 1982; Saint-Germain et al.
© 2008 The Authors. Journal compilation © 2008 British Ecological Society, Journal of Applied Ecology
 Land-use change and tropical forest dung beetles 9

Cooling rates in dung beetles are inversely related to body

mass (Bartholomew & Heinrich 1978) and, while elevated
body temperatures provide a competitive advantage in the
cool, humid environment of tropical forests, an inability to
dissipate excess heat in more open environments may incur
severe physiological costs (Chown 2001). In addition, larger
beetles require higher soil humidity content for digging
deeper galleries (Anduaga 2004), and therefore these species
may be disadvantaged when exposed to drier conditions.
Larger dung beetles also use a disproportionately larger share
of resources (Doube 1990) and therefore may be negatively
affected by reductions in resource availability outside pri-
mary forest. Finally, there is some evidence to suggest that
larger beetles are attracted to larger dung piles (Peck &
Howden 1984) and that a reduction in the mean body size of
resident mammal species may deplete the resources available
to larger beetle species (Cambefort 1991). In support of this
hypothesis we observed a marked decrease in the mean body
size of all primate species encountered during standardized
line transect surveys in secondary forest (1·3 kg individual–1)
compared with that of primary forest (3·6 kg), and the largest
primate species in Jari (spider monkey, Ateles paniscus) was
Fig. 7. Standardized changes from primary forest in (a) average restricted to primary forest (C. A. Peres, unpublished data).
species body mass and (b) average pooled biomass for 11 dung beetle One of the most striking and novel results from this study is
genera sampled in secondary and plantation forest sites. Average that the decline of dung beetle body size observed across the
values with bias-corrected 95% bootstrap confidence intervals are whole community was largely consistent within individual
compared against the respective average for that genus in primary
genera. Similar results have been found in other analyses, con-
forest samples (horizontal line), demonstrating that genera in
secondary and plantation forest are consistently represented by trolling for higher level phylogenetic differences, on patterns
smaller species and lower levels of biomass than in intact habitat. of body size and extinction risk in birds (Gaston & Blackburn
Genera are arrayed left to right by rank-order of absolute size (the 1995) and beetles (Cunningham & Murray 2007). However, it
absolute body mass, shown by grey bars). All data are log10 is not immediately clear why this should be the case across a
transformed. Genus codes are: COPR, Coprophanaeus; OXYS,
much finer (i.e. genus level) taxonomic scale of functionally
Oxysternon; DICH, Dichotomius; DELT, Deltochilum; EURY,
Eurysternus; ONTH, Ontherus; CANT, Canthon; CANM, similar species. It seems unlikely that the same physiological
Canthidium; ATEU, Ateuchus; ONTG, Onthophagus; UROX, Uroxys. or resource-based mechanisms responsible for driving com-
munity-wide changes in body mass are also responsible for
driving patterns within genera that vary in mass by orders of
2007). Consequently, analyses based on both abundance and magnitude. Nevertheless, non-random species co-occurrence
biomass data can provide complementary information that is patterns are common in nature and, if our observation reflects
vital in achieving a robust understanding of the ecological a more general phenomenon, it is possible that a combination
consequences of habitat change for tropical forest dung beetles of internal species’ constraints (e.g. taxon-dependent com-
(Peck & Forsyth 1982). Our data suggest that larger bodied petitive advantages or dispersal ability) and external environ-
dung beetles are more susceptible than smaller bodied species mental filters (e.g. phylogenetically constrained thresholds of
to abundance declines, if not local extinctions, following physiological tolerance; Chown 2001) serve to determine a set
conversion of primary rainforest to secondary or plantation of assembly rules that selects against large bodied congeners
forest. Large body size is one of the most commonly cited traits outside primary forest. However, understanding the nature of
promoting extinction over ecological time scales, and has any such set of rules is hampered by our almost complete lack
been reported in both vertebrates and invertebrates, including of ecological information on most tropical forest dung beetles,
dung beetle studies on the effects of fragmentation (Klein especially small-bodied genera.
1989; Larsen, Williams & Kremen 2005) and forest clearance
(Scheffler 2005). Interpreting the ecological mechanisms
CONCLUSIONS
responsible for this reduction in mean body size in converted
forests is confounded by the fact that body size is often We have demonstrated that secondary and plantation forests
correlated with other variables that are themselves positively in a large neotropical landscape host exceptionally depauper-
and negatively associated with extinction risk (Gaston 1994). ate dung beetle communities. That secondary and plantation
Nevertheless, changes in the physiological tolerance to thermal forests harboured smaller populations of most primary forest
stress, and alterations in the supply of dung resources, indi- species and tended to lack larger bodied species has worrying
cate why size-dependent effects may be important. implications for the maintenance of dung beetle-mediated
© 2008 The Authors. Journal compilation © 2008 British Ecological Society, Journal of Applied Ecology
10 T. A. Gardner et al.

services outside primary forests, such as secondary seed dis- Bartholomew, G.A. & Heinrich, B. (1978) Endothermy in African dung beetles
during flight, ball making, and ball rolling. Journal of Experimental Biology,
persal and dung burial (Andresen & Feer 2005).
73, 65–83.
The discrepancy between our results and those of studies Boonrotpong, S., Sotthibandhu, S. & Pholpunthin, C. (2004) Species com-
elsewhere in the tropics is most probably explained by the position of dung beetles in the primary and secondary forests at Ton Nga
Chang Wildlife Sanctuary. Science Asia, 30, 59–65.
importance of differences in biogeographical and landscape
Cambefort, Y. (1991) Dung beetles in tropical savannas. Dung Beetle Ecology
context, together with the influence of systematic sampling (eds I. Hanski & Y. Cambefort), pp. 156–178. Princeton University Press,
biases. These factors confound our ability to draw general Princeton, NJ.
Chown, S.L. (2001) Physiological variation in insects: hierarchical levels and
patterns, and highlight the importance of developing quanti-
implications. Journal of Insect Physiology, 47, 649–660.
tative meta-analyses (Nichols et al. 2007) that can provide an Clarke, K.R. & Warwick, R.M. (2001) Change in Marine Communities: An
objective basis for evaluating future empirical studies. Approach to Statistical Analysis and Interpretation. Primer-E Ltd, Plymouth
Marine Laboratory, UK.
In accounting for many of these confounding factors, our
Colwell, R.K. (2005) Estimates: Statistical Estimation of Species Richness and
results indicate that we are in danger of understating the trop- Shared Species from Samples, Version 7·5. User’s GUIDE and Application.
ical forest biodiversity crisis (Laurance 2007). Specifically, we http://purl.oclc.org/estimates, accessed 01/08/06.
Cunningham, S.A. & Murray, W. (2007) Average body length of arboreal and
caution strongly against optimistic views that forest regener-
aerial beetle (Coleoptera) assemblages from remnant and plantation Euca-
ation schemes in highly degraded landscapes can effectively lyptus forests in southwestern Australia. Oecologia, 151, 303–312.
offset the loss of species following the loss of primary forest Daily, G.C. (2001) Ecological forecasts. Nature, 411, 245–245.
Davis, A.J., Holloway, J.D., Huijbregts, H., Krikken, J., Kirk-Spriggs, A.H. &
habitat (Wright & Muller-Landau 2006). To be effective,
Sutton, S.L. (2001) Dung beetles as indicators of change in the forests of
management strategies for production landscapes need to northern Borneo. Journal of Applied Ecology, 38, 593–616.
emphasize the importance of protecting remaining areas of Davis, A.L.V. & Philips, T.K. (2005) Effect of deforestation on a southwest
Ghana dung beetle assemblage (Coleoptera: Scarabaeidae) at the periphery
primary forest. In areas where this is not possible, it is vital
of Ankasa conservation area. Environmental Entomology, 34, 1081–1088.
that the key methodological and ecological considerations Doube, B.M. (1990) A functional classification for analysis of the structure of
highlighted in our study are given priority when assessing the dung beetle assemblages. Ecological Entomology, 15, 371–383.
Dunn, R.R. (2004) Recovery of faunal communities during tropical forest
conservation value of human-dominated forest lands.
regeneration. Conservation Biology, 18, 302–309.
Efron, B. (1987) Better bootstrap confidence intervals. Journal of the American
Statistical Association, 82, 171–185.
Acknowledgements Escobar, F. (2004) Diversity and composition of dung beetle (Scarabaeinae)
We thank the Brazilian Ministério de Ciências e Tecnologia (CNPq) and assemblages in a heterogeneous Andean landscape. Tropical Zoology, 17,
Ministério do Meio Ambiente (MMA-IBAMA) for permission to conduct 123–136.
this research. We thank Grupo Orsa and the staff of Orsa Florestal and Jari Estrada, A., Anzures, A. & Coates-Estrada, R. (1999) Tropical rain forest
Celulose at Jari for permissions and logistic support. We are very grateful to fragmentation, howler monkeys (Alouatta palliata), and dung beetles at Los
Fernando Z. Vaz-de-Mello for help in the identification of specimen material. Tuxtlas, Mexico. American Journal of Primatology, 48, 253–262.
The project was funded by a Natural Environment Research Council (NERC) FAO (2006) Global Forest Resources Assessment 2005: Progress Towards
Studentship to T. A. Gardner, the UK Government Darwin Initiative, National Sustainable Forest Management. Food and Agriculture Organisation (United
Geographic Society, Conservation Food and Health Foundation, and Conser- Nations), Rome, Italy.
vation International. We thank Liz Nichols and Sacha Spector for discussions, Gardner, T.A., Barlow, J., Araujo, I.S., Avila-Pires, T.C.S., Bonaldo, A.B.,
and Liz Nichols, Julio Louzada and three anonymous referees for valuable Costa, J.E., Esposito, M.C., Ferreira, L.V., Hawes, J., Hemández, M.I.M.,
comments on earlier versions of this manuscript. This is publication number Hoogmoed, M.S., Leite, R.N., Lo-Man-Hung, N.F., Malcolm, J.R., Mar-
15 of the Land-Use Change and Amazonian Biodiversity Project (see tins, M.B., Mestre, L.A.M., Miranda-Santas, R., Nunes-Gutjahr, A.L.,
www.tropicalforestresearch.org). Overal, W.L., Parry, L., Peters, S.L., Ribeiro-Gunior, M.A., da Silva,
M.N.F., da Silva Mottc, C. & Peres, C. (2008) The cost-effectiveness of bio-
diversity surveys in tropical forests. Ecology Letters, 11, 139–150.
References Gardner, T.A., Barlow, J., Parry, L.T.W. & Peres, C.A. (2007a) Predicting the
uncertain future of tropical forest species in a data vacuum. Biotropica, 39,
Andresen, E. & Feer, F. (2005) The role of dung beetles as secondary seed 25–30.
dispersers and their effect on plant regeneration in tropical rainforests. Gardner, T.A., Ribeiro, M.A. Jr, Barlow, J., Ávila-Pires, T.A.S., Hoogmoed,
Seed Fate: Predation, Dispersal and Seedling Establishment (eds P.M. Forget, M. & Peres, C.A. (2007b) The value of primary, secondary and plantation
J.E. Lambert, P.E. Hulme & S.B. Vander Wall), pp. 331–349. CABI Interna- forests for a neotropical herpetofauna. Conservation Biology, 21, 775–787.
tional, Wallingford, UK. Gardner, T.A., Barlow, J. & Peres, C.A. (2007) Paradox, presumption and
Anduaga, S. (2004) Impact of the activity of dung beetles (Coleoptera: Scara- pitfalls in conservation biology: consequences of habitat change for amphi-
baeidae: Scarabaeinae) inhabiting pasture land in Durango, Mexico. Envi- bians and reptiles. Biological Conservation, 138, 166–179.
ronmental Entomology, 33, 1306–1312. Gaston, K.J. (1994) Rarity. Chapman & Hall, London, UK.
Arellano, L. & Halffter, G. (2003) Gamma diversity: derived from and a deter- Gaston, K.J. & Blackburn, T.M. (1995) Birds, body size and the threat of
minant of alpha diversity and beta diversity. An analysis of three tropical extinction. Philosophical Transactions of the Royal Society of London B Bio-
landscapes. Acta Zoologica Mexicana (Nueva Serie), 90, 27–76. logical Sciences, 347, 205–212.
Avendaño-Mendoza, C., Moron-Rios, A., Cano, E. & Leon-Cortes, J. (2005) Gotelli, N.J. & Colwell, R.K. (2001) Quantifying biodiversity: procedures and
Dung beetle community (Coleoptera: Scarabaeidae: Scarabaeinae) in a pitfalls in the measurement and comparison of species richness. Ecology
tropical landscape at the Lachua Region, Guatemala. Biodiversity and Con- Letters, 4, 379–391.
servation, 14, 801–822. Halffter, G. & Arellano, L. (2002) Response of dung beetle diversity to human-
Barlow, J., Mestre, L.A.M., Gardner, T.A. & Peres, C.A. (2007a) The value of induced changes in a tropical landscape. Biotropica, 34, 144–154.
primary, secondary and plantation forests for Amazonian birds. Biological Halffter, G. & Matthews, E.G. (1966) The natural history of dung beetles in the
Conservation, 126, 212–231. subfamily Scarabaeidae (Coleoptera, Scarabaeidae). Folia Entomoliogica
Barlow, J., Overal, W.L., Araujo, I.S., Gardner, T.A. & Peres, C.A. (2007b) The Mexicana, 12–14, 1–312.
value of primary, secondary and plantation forests for fruit-feeding butter- Halffter, G., Favila, M.E. & Halffter, V. (1992) A comparative study on the
flies in the Brazilian Amazon. Journal of Applied Ecology, 44, 1001–1012. structure of scarab guilds in tropical rainforests and derived ecosystems.
Barlow, J., Gardner, T.A., Araujo, I.S. et al. (2007c) Quantifying the biodiver- Folia Entomoliogica Mexicana, 84, 131–156.
sity value of tropical primary, secondary and plantation forests. Proceedings Hamer, K.C. & Hill, J.K. (2000) Scale-dependent effects of habitat disturbance
of the National Academy of Sciences of the United States of America, 104, on species richness in tropical forests. Conservation Biology, 14, 1435 –
18555–18560. 1440.

© 2008 The Authors. Journal compilation © 2008 British Ecological Society, Journal of Applied Ecology
 Land-use change and tropical forest dung beetles 11

Hill, J.K. & Hamer, K.C. (2004) Determining impacts of habitat modification prid dung beetles: the influence of soil type and soil moisture. Ecograpahy,
on diversity of tropical forest fauna: the importance of spatial scale. Journal 18, 147–154.
of Applied Ecology, 41, 744–754. Vulinec, K. (2002) Dung beetle communities and seed dispersal in primary
Horgan, F.G. & Fuentes, R.C. (2005) Asymmetrical competition between forest and disturbed land in Amazonia. Biotropica, 34, 297–309.
neotropical dung beetles and its consequences for assemblage structure. Vulinec, K., Lambert, J.E. & Mellow, D.J. (2006) Primate and dung beetle
Ecological Entomology, 30, 182–193. communities in secondary growth rain forests: implications for conservation
Howden, H.F. & Nealis, V.G. (1975) Effects of clearing in a tropical rainforest of seed dispersal systems. International Journal of Primatology, 27, 855–879.
on the composition of the coprophagous scarab beetle fauna (Coleoptera). Wright, S.J. (2005) Tropical forests in a changing environment. Trends in
Biotropica, 7, 77–85. Ecology and Evolution, 20, 553–560.
Janzen, D.H. (1967) Why mountain passes are higher in tropics. American Wright, S.J. & Muller-Landau, H.C. (2006) The future of tropical forest species.
Naturalist, 101, 233–249. Biotropica, 38, 207–301.
Klein, B.C. (1989) Effects of forest fragmentation on dung and carrion beetle
communities in central Amazonia. Ecology, 70, 1715–1725. Received 5 August 2007; accepted 5 December 2007
Koh, L.P. (2007) Impacts of land use change on south-east Asian forest Handling Editor: Julia Jones
butterflies: a review. Journal of Applied Ecology, 44, 703–713.
Larsen, T.H. & Forsyth, A. (2005) Trap spacing and transect design for dung
beetle biodiversity studies. Biotropica, 37, 322–325.
Larsen, T.H., Lopera, A. & Forsyth, A. (2006) Extreme trophic and habitat Supplementary material
specialization by Peruvian dung beetles (Coleoptera: Scarabaeidae: Scara-
baeinae). Coleopterists’ Bulletin, 60, 315–324. The following supplementary material is available for this
Larsen, T.H., Williams, N.M. & Kremen, C. (2005) Extinction order and article.
altered community structure rapidly disrupt ecosystem functioning. Ecology
Letters, 8, 538–547. Appendix S1. The influence of seasonality on patterns of
Laurance, W.F. (2007) Have we overstated the tropical biodiversity crisis? observed species richness and relative abundance in primary,
Trends in Ecology and Evolution, 22, 65–70.
Lobo, J.M., Lumaret, J.P. & Jay-Robert, P. (1998) Sampling dung beetles in the secondary and Eucalyptus plantation forests in Jari, north-
French Mediterranean area: effects of abiotic factors and farm practices. east Brazilian Amazonia
Pedobiologia, 42, 252–266.
Medina, C.A., Escobar, F. & Kattan, G. (2002) Diversity and habitat use of Table S1. Species, numbers of captures and average body
dung beetles in a restored Andean landscape. Biotropica, 34, 181–187. masses of Scarabaeinae dung beetles sampled in primary,
Nichols, E., Larsen, T.B., Spector, S., Davis, A.L.V., Escobar, F. Favila, M.,
Vulinec, K. & the Scarabaeinae Research Network (2007) Global dung secondary and Eucalyptus plantation forests
beetle response to tropical forest modification and fragmentation: a quan-
titative literature review and meta-analysis. Biological Conservation, 137, 1– Table S2. Species richness, sample coverage and complete-
19. ness, and diversity of dung beetles sampled in primary,
Peck, S.B. & Forsyth, A. (1982) Composition, structure, and competitive secondary and Eucalyptus plantation forests
behavior in a guild of Ecuadorian rain-forest dung beetles (Coleoptera,
Scarabaeidae). Canadian Journal of Zoology–Revue Canadienne de Zoologie, Table S3. Species percentage contributions towards pairwise
60, 1624–1634.
Peck, S.B. & Howden, H.F. (1984) Response of a dung beetle guild to different dissimilarities in dung beetle community structure across pri-
sizes of dung bait in a Panamanian rainforest. Biotropica, 16, 235–238. mary, secondary and Eucalyptus plantation forests
Quintero, I. & Roslin, T. (2005) Rapid recovery of dung beetle communities
following habitat fragmentation in central Amazonia. Ecology, 12, 3303– Table S4. Species percentage contributions towards within
3311. habitat similarities in dung beetle community structure for
Radtke, M.G., da Fonseca, C.R.V. & Williamson, G.B. (2007) The old and
young Amazon: dung beetle biomass, abundance and species diversity. primary, secondary and Eucalyptus plantation forests
Biotropica, 39, 725–730.
Saint-Germain, M., Buddle, C.M., Larrivee, M., Mercado, A., Motchula, T., This material is available as part of the online article
Reichert, E., Sackett, T.E., Sylvain, Z. & Webb, A. (2007) Should biomass be from: http://www.blackwell-synergy.com/doi/full/10.1111/
considered more frequently as a currency in terrestrial arthropod community j.1365-2664.2008.01454.x
analyses? Journal of Applied Ecology, 44, 330–339.
Scheffler, P.Y. (2005) Dung beetle (Coleoptera: Scarabaeidae) diversity and (This link will take you to the article abstract.)
community structure across three disturbance regimes in eastern Amazonia.
Journal of Tropical Ecology, 21, 9–19. Please note: Blackwell Publishing is not responsible for the
Shahabuddin, G., Schulze, C.H. & Tscharntke, T. (2005) Changes of dung content or functionality of any supplementary materials
beetle communities from rainforests towards agroforestry systems and supplied by the authors. Any queries (other than missing
annual cultures in Sulawesi (Indonesia). Biodiversity and Conservation, 14,
863–877. material) should be directed to the corresponding author for
Sowig, P. (1995) Habitat selection and offspring survival rate in three paraco- the article.

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