Biodiversity and Ecosystem Services in Agroecosystems

K Garbach, Loyola University Chicago, Chicago, IL, USA

JC Milder, Rainforest Alliance, New York, NY, USA
M Montenegro and DS Karp, University of California-Berkeley, Berkeley, CA, USA
FAJ DeClerck, Bioversity International, Maccarese, Rome, Italy
r 2014 Elsevier Inc. All rights reserved.

Glossary services provide recreational, esthetic, spiritual, and other

Agroecology The application of ecological concepts and nonmaterial benefits.
principles to the design and management of sustainable Human well-being A context- and situation-dependent
agroecosystems. state that comprises basic material for a good life, freedom
Agroecosystems Agricultural ecosystems including and choice, health, good social relations, and security.
biophysical and human components and their interactions. Millennium Ecosystem Assessment An international
Biodiversity The variation of life in all forms from genes, synthesis released in 2005, created by more than 1000 of
to species, to communities, to whole ecosystems. the world's leading scientists, that analyzed the state of the
Ecosystem service providers Organisms, guilds, and Earth's ecosystems.
ecological communities that are biological mediators of Payment for ecosystem services Market-based
ecosystem services, providing services through their instruments used to channel investment in ecosystem
functions and interactions. services.
Ecosystem services Functions of ecosystems – including Resilience The capacity of a system to absorb disturbance
agroecosystems – that are useful to humans or support and retain structure and function; this includes the human
human well-being: (1) provisioning services include the capacity to anticipate and plan for the future (e.g., in
production of food, fuel, fiber, and other harvestable goods; managing agricultural systems).
(2) regulating services include climate regulation, flood Scale Geographical extent; relevant scales for
control, disease control, waste decomposition, and water agroecosystems often include units commonly used in
quality regulation; (3) supporting services include the management and decision making, such as field (local and
foundational processes necessary for production of other on-farm cultivated area), farm (including cultivated and
services, including soil formation, nutrient cycling, and noncultivated areas), landscape, regional, and global.
photosynthesis (primary production); and (4) cultural

Introduction Work on multifunctional ecosystems draws on the Millen-

nium Ecosystem Assessment (2005) and other recent evalu-
Historically, agricultural systems have been managed, above ations of ecosystem services (e.g., The Economics of Ecosystems
all, for the production of food and fiber; however, agricultural and Biodiversity and The Common International Classification
landscapes can provide a wide range of goods and services to of Ecosystem Services). The Millennium Ecosystem Assessment
society. ‘Ecosystem services’ are those functions of ecosystems provides a globally recognized classification that emphasizes
– including agroecosystems – that are useful to humans relationships between ecosystem services and human well-
or support human well-being (Daily, 1997; Kremen, 2005). being and describes four types of services (The authors draw
The ecosystem services concept is remarkably longstanding. on the classification of ecosystems services used in Millennium
Mooney and Ehrlich (1997) noted that in approximately 400 Ecosystem Assessment throughout the article (MEA, 2005),
BC, Plato observed how forests provided important services to recognizing that more recent classifications have minimized
Attica and forest loss resulted in drying springs and soil ero- or eliminated supporting services in favor of specific, oper-
sion. Plato's work highlights that people have been aware ational descriptions designed for environmental accounting
of these critical services long before the dawn of industrial (Haines-Young and Potschin, 2012) and economic valuation
agriculture (Rapidel et al., 2011). (TEEB, 2010)). Provisioning services include the production
In the past two decades, work at the interface of ecology of food, fuel, fiber, and other harvestable goods. Regulating
and economics to characterize, value, and manage ecosystem services include climate regulation, flood control, disease
services has supported a paradigm shift in how society thinks control, waste decomposition, and water quality regulation.
about ecosystems and human relationships to them. As both Supporting services include the foundational processes neces-
major providers and major beneficiaries of ecosystem services, sary for production of other services, including soil formation,
agricultural landscapes and the people within them are at the nutrient cycling, and photosynthesis (primary production).
center of this shift. Growing calls for agriculture landscapes to Cultural services provide recreational, esthetic, spiritual, and
be managed as ‘multifunctional’ systems create new mandates, other nonmaterial benefits. Most classifications, despite their
as well as opportunities, to maintain and enhance ecosystem variations, consider interdependence between ecosystem ser-
services as part of productive agroecosystems. vices and human well-being as well as variation in ecosystem

Encyclopedia of Agriculture and Food Systems, Volume 2 doi:10.1016/B978-0-444-52512-3.00013-9 21

22 Biodiversity and Ecosystem Services in Agroecosystems

services across spatial scales ranging from local to global control through the effects of large root and mycorrhizal net-
(Figure 1). works holding soil in place (Balvanera et al., 2006). It is also
Biodiversity – the variation of life in all forms from genes, to important to note that some ecosystem services are provided in
species, to communities, to whole ecosystems – is a significant part by the abiotic (nonliving) components of ecosystems, such
determinant of ecosystem function and provision of ecosystem as aquifers and inorganic portions of soils. Biodiversity can be
services. Although relationships between biodiversity and eco- considered a form of ‘biological insurance’ that helps to assure
system services are complex and vary widely across different ecosystem performance, including providing ecosystem ser-
types of ecosystems, at the broadest level, increased native vices, as diversity increases the chances that one or more species
biodiversity is generally associated with higher levels of eco- will be able to perform critical functions, even in the event of
system services within a given system (Balvanera et al., 2006; disturbance or species loss (e.g., natural disaster and human-
Cardinale et al., 2012). Plant diversity, for example, has been induced land use change) (Naeem and Li, 1997).
found to enhance belowground plant and microbial biomass, Agroecosystems both provide and rely on ecosystem
which is associated with the ecosystem service of erosion services to sustain production of food, fiber, and other

Global
Regional
Local

Human well-being
Basic materials and conditions necessary
for a good life

Human
activities
Ecosystem services
Services necessary for the production of other ecosystem services
Photosynthesis

Provisioning
Goods and products obtained from an ecosystem

Food, fuel, fiber

Biochemicals
Genetic resources
Biogeochemical cycling

Regulating
Benefits obtained from regulation of ecosystem
Supporting

processes

Carbon sequestration
Pollination, pest control
carbon sequestration climate regulation
water purification

Cultural
Soil formation

Nonmaterial benefits obtained from ecosystems

Spiritual and religious

Recreation, ecotourism
Esthetics, inspiration
Sense of place
Cultural heritage

Biodiversity

Figure 1 Typology of ecosystem services. This ecosystem service typology, adapted from the Millennium Ecosystem Assessment (MEA, 2005),
considers biodiversity as a foundation for all ecosystem services (represented with a dotted line framing ecosystem services). Ecosystem services
include provisioning, regulating, and cultural services (dark gray boxes, solid outline), as well as supporting services (light gray box, dashed
outline). Ecosystem services support human well-being (charcoal gray box, white text), and, in turn, are influenced by human activities and land-
use management decisions. Both ecosystem services and human well-being can be considered at nested spatial scales from local, to regional, to
global.
 Biodiversity and Ecosystem Services in Agroecosystems 23

harvestable goods. Many services have on-farm benefits (e.g., The evaluation and management of ecosystem services
for farmers, plantation managers, and other people on-site), in agricultural landscapes has emerged as a top priority for
whereas others have broader public benefits to off-farm users; several reasons. First, agricultural ecosystems – including
some benefit both groups (Table 1). croplands and pastures – are among the largest terrestrial

Table 1 Ecosystem service descriptions and related on-farm benefits and public, off-farm benefits

Ecosystem service Description On-farm benefits Public, off-farm benefits

Provision of food, fuel, fiber, Harvestable goods from Food and other goods for on- Goods for agricultural markets
and biochemicals agroecosystems farm consumption or sale
Soil structure and fertility Soil structure and processes of Support for crop growth; can May limit need to mine or
enhancement nutrient cycling and delivery limit need for chemical manufacture chemical
of nutrients to plants; fertilizers fertilizer
processing organic matter
and transforming detritus and
wastes
Erosion protection Soil retention; limiting soil loss Maintain soil, and the nutrients Potential reduction of sediment
through wind and water it contains, to support transfer to downstream
erosion production systems & users
Hydrologic services: Water flow Buffering and moderation of the Water in soils, aquifers, and Stabilize stream base flow and
regulation hydrologic cycle, including surface bodies available to mitigate flooding to
water infiltration into soils support plant growth downstream areas; recharge
and aquifers, moderation of into aquifers and bodies of
runoff, and plants water; plant transpiration may
transpiration support precipitation patterns
Hydrologic services: Water Filtration and absorption of Clean water available for human Clean water available to
purification particles and contaminants by consumption, irrigation, and downstream users
soil and living organisms in other on-farm uses
the water and soil
Pollination Transfer of pollen grains to Necessary for seed set and fruit Necessary for outcrossing in
fertilize flowers production in flowering plants noncultivated flowering plants
and crops
Pest control Control of animal and insect Minimize crop damage and limit May limit need for pesticides
pests by their natural enemies competition with crops that threaten environmental
– predators, parasites, and and human health
pathogens
Weed control Botanical component of pest Minimize weed competition May limit need for herbicides
control; suppressing weeds, with crops that threaten environmental
fungi, and other potential and human health
competitors through physical
and chemical properties of
cover crops, intercrops, and
other planted elements
Carbon sequestration Atmospheric carbon dioxide is Few demonstrable on-farm Regulation of the carbon cycle;
taken up by trees, grasses, benefitsa mitigation of greenhouse gas
and other plants through contributions to atmospheric
photosynthesis and stored as change
carbon in biomass and soils
Genetic resources Pool of genetic diversity needed Distinct genotypes (cultivars) Prevention against large-scale
to support both natural and allow fruit set in orchards and crop failure
artificial selection hybrid seed production; trait
diversity (from landraces and
wild relatives) supports
disease resistance, new
hybrids, and climate
adaptations
Cultural and esthetic services Maintaining landscapes that Esthetics and inspiration; Esthetics and inspiration;
support: esthetics and spiritual and religious values; spiritual and religious values;
inspiration; spiritual and sense of place; cultural sense of place; cultural
religious values; sense of heritage; recreation and heritage; recreation and
place; cultural heritage; ecotourism ecotourism
recreation and ecotourism
a
On-farm carbon sequestration can be associated with on-farm benefits in closely related ecosystem services, such as increased soil organic matter and microclimate regulation
(e.g., shade provided by trees).
24 Biodiversity and Ecosystem Services in Agroecosystems

biomes and account for approximately 40% of the Earth's function and diversity of the surrounding landscape (Kremen
surface (Foley et al., 2005). Second, increases in food and and Ostfeld, 2005; Tscharntke et al., 2005). Yet, there is an
fiber production have often been achieved at the cost of outstanding need for field studies that describe the mech-
other critical services. The Millennium Ecosystem Assessment anisms, which control how ecosystem services vary across both
(2005) reported that approximately 60% (15 out of 24) of space and time. Building understanding of the mechanisms
services measured in the assessment were being degraded underlying ecosystem services is also essential to developing
or unsustainably used as a consequence of agricultural man- the ability to predict how management activities will affect
agement and other human activities. Finally, evaluations of the single ecosystem services, and suites of services, needed
‘planetary boundaries,’ which describe the safe operating space to support both productive farmlands and human well-being.
for human activities with respect to the planet's biophysical
systems and processes, indicate that modern, industrial agri-
culture is among the activities that have most significantly
Ecosystem Services and Disservices in Agricultural
undermined the Earth's life-support systems (Rockström et al.,
Landscapes
2009). Major negative impacts have occurred through con-
verting natural habitat to agriculture and infrastructure, en-
Ecosystem Services and Disservices
vironmental pollution, and environmental change induced by
shifts in nitrogen and phosphorus use. Agroecosystems both provide and rely on ecosystem services.
Recent work highlights the need for better understanding Services that help to support production of harvestable goods
the ecological processes that underpin critical ecosystem ser- can be considered services to agriculture (Zhang et al., 2007).
vices (Kremen, 2005). Provision of ecosystem services in These services include soil structure and fertility enhancement,
farmlands is directly determined by their design and man- nutrient cycling, water provision, erosion control, pollination,
agement (Zhang et al., 2007) and strongly influenced by the and pest control, among others (Figure 2). Ecological

Services to agriculture
Services from agriculture
Genetic resources
Provisioning services:
Hydrologic services—
Food, fuel, fiber
Water flow regulation biochemicals
Water purification
Pest control
Agroecosystems Other ecosystem services:
Pollination Carbon sequestration
Soil structure and fertility Soil conservation
enhancement
Cultural and aesthetic services
Habitat provision

Disservices to agriculture Disservices from Agriculture

Pest damage (e.g., negative impacts that
diminish ecosystem services)
Pathogen outbreaks
Habitat degradation/loss
Competition for:
• Water Soil degradation/loss
• Nutrients Water quality degradation/loss
• Pollination
Other off-site, negative impacts

Feedback

Figure 2 Ecosystem services and disservices to and from agriculture Farming systems can be both producers and beneficiaries of ecosystem
services, and in many cases these relationships are deliberately managed by farmers. Such ecosystem services are represented by two gray boxes
in the diagram. Production systems can also suffer from various disservices or contribute to disservices or loss of services. These negative
relationships are usually the unintentional result of management action, represented by the two lower gray boxes and the dashed arrows.
Disservices from agriculture can also lead to agricultural inputs and result in detrimental on-farm impacts, such as when habitat for natural
enemies is removed and pest outbreaks increase, represented by the feedback arrow at the bottom of the diagram. Adapted from Zhang, W.,
Ricketts, T., Kremen C., et al., 2007. Ecosystem services and dis-services to agriculture. Ecological Economics 64, 253–260 and Swinton, S., Lupi,
F., Robertson, G., Hamilton, S., 2007. Ecosystem services and agriculture: Cultivating agricultural ecosystems for diverse benefits. Ecological
Economics 64, 245–252.
 Biodiversity and Ecosystem Services in Agroecosystems 25

processes that detract from agricultural production can be Nutrient losses in agroecosystems contrast with unmanaged,
considered disservices to agriculture (Zhang et al., 2007) and undisturbed ecosystems in which nutrient cycles tend to be
include pest damage, competition for water, and competition more nearly closed, with inputs approximately matching
for pollination. Management of agricultural ecosystems also outputs (Daily et al., 1997). Many high-intensity farming sys-
affects flows of ecosystem services and disservices (or dimin- tems do not retain soil structure and fertility through bio-
ution of naturally occurring services) from production land- logical processes, they are rather maintained through tillage
scape to surrounding areas. Services from agriculture include and additions of chemical and organic fertilizers (Daily et al.,
provisioning services (food, fuel, fiber, and biochemicals) as 1997; Matson et al., 1997).
well as carbon sequestration, soil conservation, cultural and
esthetic services, and habitat provision (e.g., providing habitat Pollination
for endemic organisms). Disservices from agriculture can in- Animal pollinators are essential for approximately 35% of
clude degradation or loss of habitat, soil, water quality, and global crop production, and 60–90% of all plant species are
other off-site, negative impacts. Both services and disservices pollinator-dependent (Klein et al., 2007). Bees are recognized
are typically a result of management practices within agri- as the taxon providing most pollination services, yet other
cultural fields and landscapes. The remainder of this section taxa – including birds, bats, thrips, butterflies and moths, flies,
describes some of the key ecosystem services that support wasps, and beetles – also pollinate some of the world's most
agricultural productivity (summarized in Table 1) and dis- important food crops (Nabhan and Buchmann, 1997). Pol-
services detract from it (see Swinton et al., 2007 for detailed lination is necessary for sexual reproduction in many crops,
discussion of services and disservices from agriculture). including fruits, vegetables, nuts, and seeds (Klein et al., 2007)
as well as many wild plants known to contribute calories and
micronutrients to human diets (Sundriyal and Sundriyal,
2004). There are also many globally important crops that are
Services to Agriculture Help to Sustain Agricultural
pollinated passively or by wind, including cereals, sugarcane,
Productivity
and grasses (Klein et al., 2007).
Soil structure and fertility enhancement services include the Overall, pollinators play a significant role in the world's
processes of soil formation, structural development (including food systems and agricultural economies. The estimated value
physical, chemical, and biological properties of soil), and of insect-pollinated crops in the United States ranged from US
nutrient cycling mediated by biotic and abiotic factors to $18–27 billion in 2003. If calculations include secondary
support plant growth. These soil characteristics are important products, such as beef and milk from cattle fed alfalfa, the
determinants of the quantity and quality of farming outputs estimated value more than doubles (Mader et al., 2011). Al-
(Zhang et al., 2007). As soil organisms process dead organic though honey bees (Apis spp.) are the most important com-
matter, and their waste replenishes nutrients required for pri- mercially managed pollinator, native and wild bee species
mary production, the fertility needed to support primary also make significant contributions. Approximately 15% of
production is maintained (Daily et al., 1997). the value associated with pollination services comes from
Soil structure is enhanced through the activities of macro- native bees and other animals living in farmlands and adjacent
fauna – such as earthworms, centipedes, millipedes, and iso- natural habitat (Mader et al., 2011). Both agricultural man-
pods – that aerate soil by creating pores as they burrow agement and landscape configuration are important in deter-
through the soil profile, mixing organic and mineral particles, mining availability and distribution of pollination services.
redistributing organic matter and microorganisms, and en- Some wild (native) pollinators nest within fields, including
riching soil with castings (Hendrix et al., 1990; Edwards, ground-nesting bees, or disperse from nearby unmanaged
2004). A host of microfauna also act as biological mediators of habitats to pollinate crops (Ricketts et al., 2004). Conserving
soil fertility and structure. Their activities support soil fertility wild pollinators in unmanaged or restored natural habitats
as they break down plant detritus and other organic matter, adjacent to agricultural fields can improve pollination levels
and incorporate nutrients into their biomass, which may and stability, which can support increases in agricultural yields
otherwise move through the system or be lost downstream (Klein et al., 2003).
(Paul and Clark, 1996). Micro- and macrofauna (e.g., acarina The potential contributions of native pollinators have
and collembola) influence nutrient cycling by regulating received a great deal of recent attention due to global declines
bacterial and fungal populations, release energy by breaking in managed honey bee colonies (National Academies, 2006).
down large molecules into smaller units (catabolizing organic Declines in honey bee abundance, driven by establishment of
matter), and mineralizing and immobilizing nutrients. Their parasitic mites (e.g., Varroa destructor), hive pests, and social
activities influence soil structure by producing organic com- factors such as aging beekeeper populations, have resulted in
pounds that bind soil aggregates. Bacteria and fungi are also pollination shortages in some areas (Klein et al., 2007). This
part of an important cadre of microflora that mediates nitro- has caused increased prices for honey bee rental and created
gen fixation from the atmosphere, transforming it into plant- concern about pollination shortfalls, such as those seen in
available forms (Hendrix et al., 1990). California almonds (National Academies, 2006). These factors
Soil processes in agroecosystems are subject to removal have heightened interest in the role of native pollinators to
of nutrient-rich biomass during harvest, plus elevated de- help assure availability and stability of crop pollination ser-
composition rates that increase with frequency of tillage and vices. Recommendations for managing pollinator-friendly
irrigation. In some systems, organic matter is also lost when landscapes include maintaining areas of natural and semi-
fields are burned (e.g., to clear biomass for the next planting). natural perennial habitat (e.g., grass and woodlands, forests,
26 Biodiversity and Ecosystem Services in Agroecosystems

old fields, and hedgerows) to provide ample floral and nesting Hydrologic services – water flow regulation and water
resources available throughout the year (Kremen et al., 2007; purification
Mader et al., 2011). Agricultural production relies on a host of water-related
ecosystem services, ranging from water supply (quantity), to
Pest control purification (quality), and flood protection (Brauman et al.,
Pest damage is a major limiting factor for global food pro- 2007). Globally, agroecosystems are a major consumer of
duction. Animal pests destroy 8–15% of global wheat, rice, groundwater and surface water, accounting for approximately
maize, potato, soybean, and cotton production (Oerke, 2005) 70% of freshwater use worldwide (UN Water, 2013). Agri-
and cause more than US$30 billion in damage in the United cultural water use may be as high as 90% of total withdraws in
States each year (Pimentel et al., 2005). However, despite fast-growing economies (UN Water, 2013) or arid environ-
dramatic increases in pesticide application, damage levels re- ments (USDA ERS, 2013). Irrigation is considered a con-
mained roughly unchanged during the four decades following sumptive water use, in that water is not directly returned to
the escalation of pesticide use after World War II (Pimentel rivers and streams. Much of this water eventually returns to the
et al., 1992; Oerke, 2005). Pesticides have even precipitated atmosphere through evaporation and plant transpiration (e.g.,
pest outbreaks. For instance, Southeast Asian rice fields were the process of water moving through plant tissues and evap-
devastated by the brown planthopper (Nilaparvata lugens) after orating through leaves, stems, and flowers), particularly in
excessive pesticide application caused the pest to evolve re- thirsty crops, such as alfalfa and cotton.
sistance while its predators continued to suffer high mortality The majority of prime land for rainfed cultivation is already
(Kenmore et al., 1984). In Indonesia, planthopper outbreaks in use and development of irrigated land has contributed
abated once many pesticides were banned (Naylor and substantially to production gains. A prime example is in India,
Ehrlich, 1997). Instead, farmers adopted an integrated pest where the growth of irrigated rice and wheat on the semiarid
management approach in which natural pest predators were plains of Punjab has substantially boosted food production
fostered, and pesticides were used only after damage exceeded over the past several decades (Matson et al., 1997). Globally,
critical economic thresholds. approximately 40% of crop production is supported by irri-
The idea that farmers can harness nature to provide pest gated agricultural lands, which account for 20% of all agri-
control benefits is not new. As early as AD 304, Chinese farmers cultural areas (UN Water, 2013). Scientists project that
created and maintained citrus ant (Oecophylla smaragdina) nests continued increases in agricultural production would require
in their orchards to control pest outbreaks (Huang and Pei, sustained or increased supply of irrigation water (Matson et al.,
1987). Centuries later, in 1888, the modern concept of classic 1997).
biological control emerged, again in citrus orchards, when Ecosystems do not create water; however, they can modify
introduced vedalia beetles (Rodolia cardinalis) caused the near the amount of water moving through the landscape. These
complete collapse of cottony-cushion scale (Icerya purchasi) modifications result from ecosystem influence on the hydro-
pests in California (Caltagirone and Doutt, 1989). Since then it logic cycle, including local climate, water use by plants, and
has become widely recognized that adjusting agricultural modification of ground surfaces that alter infiltration and flow
practices to benefit pest predators can provide a valuable pest patterns (Brauman et al., 2007). The amount of water stored
control strategy with significant benefit to farmers. in watersheds, or discharged above and below ground, influ-
Strategies for enhancing pest control services to agriculture ences water supply and availability to downstream users. The
may require understanding predator ecology to ensure that understanding of how water availability changes with land use
pest predators have suitable food and habitat resources and land cover change is elementary (Brauman et al., 2007).
throughout their life cycles (Landis et al., 2000). Plants that Planting of forests and trees – native or introduced – can either
provide floral or nectar resources can be used to sustain increase or decrease evapotranspiration and downstream water
predators and parasitoids. Sweet alyssum (Lobularia maritima) availability, depending on the context. In one study, analysis
has proven especially effective for bolstering syrphid fly of paired catchment experiments found that stream flows were
abundances in California (Tillman et al., 2012). Predator reduced 45% on an average when grasslands were converted to
populations can also be enhanced indirectly through agri- forests (Farley et al., 2005). Other studies from the Amazon
cultural practices that increase nonpest prey, for example, by basin illustrate that evapotranspiration from a pasture can be
applying mulch or intercropping (Riechert and Bishop, 1990; up to 24% less than a nearby forest (Von Randow et al., 2004).
Bugg et al., 1991). Small patches of native vegetation on Vegetation can also be selected to support management goals
and around farms can provide these species with food re- based on water requirements. For example, Australian studies
sources and overwintering habitat (Landis et al., 2000; Tillman describe use of plants such as lucerne (Medicago sativa), euca-
et al., 2012). Emerging evidence suggests that conservation lyptus trees (Eucalyptus spp.), and saltbush (Atriplex spp.),
activities at a landscape scale can also benefit farmers. For which are thought to mitigate potential crop damages in areas
example, conserving natural habitat surrounding farms in- where rising water tables bring saline water into root zones
creases predators and often enhances pest control services by lowering water tables through high transpiration rates
(Thies and Tscharntke, 1999; Bianchi et al., 2006; Chaplin- (Heuperman et al., 2002).
Kramer et al., 2011b; Karp et al., 2013). These examples rep- Water purification depends on filtration and absorption of
resent but a few of many techniques that have emerged for particles and contaminants by clay, silt, and sand particles in
controlling crop pests with native predators, many of which soil as well as living organisms in soil and water. Agricultural
are readily accessible to farmers through government, uni- production depends on water quality to maintain productive
versity, and agency extension programs. capacity, but there are a number of threats and challenges the
 Biodiversity and Ecosystem Services in Agroecosystems 27

continued provision of clean water. Irrigated farmlands in arid breeders, thereby increasing the vulnerability of crops to sud-
and semiarid regions are experiencing degradation due to den environmental changes (Esquinas-Alcázar, 2005).
salinization and waterlogging (Matson et al., 1997).
Maintaining water quality for agriculture and other uses is Disservices to Agriculture Detract from Agricultural
increasingly thought to require maintaining buffers of vege- Productivity
tation with intact groundcover and root systems throughout
the watershed. Vegetation, microbes, and stabilized soils can Disservices to agriculture result from the ecological processes
remove pollutants from overland flow and from groundwater or relationships that detract from agricultural productivity.
by physically trapping water and sediments, by adhering to Crop pests, including seed eaters, herbivores, frugivores, and
contaminants, by reducing water speed to enhance infiltration, pathogens (e.g., insects, fungi, bacteria, and viruses), can result
by biochemical transformation of nutrients and contaminants, in reduced productivity, or total crop loss in worst case scen-
and by absorbing water and nutrients from the root zone arios (Zhang et al., 2007). Weeds and other noncrop plants can
(Naiman and Décamps, 1997). Vegetated riparian buffer zones reduce agricultural productivity through competition for re-
in particular perform critical functions to support water quality. sources. At the field scale, weeds compete with crops for sun-
Genetic resources provide a pool of raw material necessary light, water, and soil nutrients and may limit crop growth and
to support the process of natural selection and produce evo- productivity by limiting access to these critical resources
lutionary adaptations in unmanaged ecosystems. In agroeco- (Welbank, 1963). Within fields, plants may exhibit allelopathy
systems, crop and animal breeders draw on genetic diversity (biochemical inhibition of competitors), such as the toxins
using traditional breeding and biotechnology to artificially exuded by some plant roots that can decrease crop growth
select and perpetuate desirable traits (Zhang et al., 2007). A (Weston and Duke, 2003).
broad portfolio of genetic resources increases the likelihood of Resource competition that potentially detracts from agri-
maintaining production, particularly as environmental pres- cultural yields can also take place at larger scales. Competition
sures such as climate, pests, and disease fluctuate. Production for pollination from flowering weeds and other noncrop
stability comes through an array of genotypes, each with plants beyond agricultural fields can reduce crop yields (Free,
different characteristics of disease resistance, tolerance for 1993). Water used by other plants, such as trees that reduce
environmental extremes, and nutrient use (Esquinas-Alcázar, aquifer recharge, can reduce water available to support agri-
2005). Different genotypes, or cultivars, are required for plants cultural production by diminishing an important source of
in orchard systems and hybrid seed production to set fruit or irrigation water (Zhang et al., 2007).
seed (Free, 1993; Delaplane and Mayer, 2000). The benefits of Food safety concerns related to pathogen outbreaks are
genetic variation at the species level include enhanced biomass other potential detractors from agricultural productivity. Since
production, reduced loss to pests and diseases, and more ef- the 1990s these concerns have gained some prominence
ficient use of available nutrients (Tilman, 1999). in highly productive regions, such as the Salinas Valley of
Crop production is supported by genetic resources from California (the ‘salad bowl of America’), which experienced
two important sources. First are ‘landraces,’ the varieties of Escherichia coli contamination of leafy greens. The unfortunate
crops and livestock that have been cultivated and selected by consequence has been broad-scale removal of riparian habitat
farmers over many generations practicing traditional agri- to minimize wildlife intrusion into crop fields. Wildlife was
culture (Shand, 1997). Second are closely related species that posited to spread harmful bacteria, although whether it con-
survive in the wild, known as crop ‘wild relatives.’ Areas with stitutes a significant food safety risk remains unclear. Never-
high concentrations of landraces and wild relatives are con- theless, over a 5-year period following an E. coli O157:H7
sidered centers of crop genetic diversity (Shand, 1997). These outbreak in spinach, 13.3% of remaining riparian habitat was
centers are critical, as many important crops could not main- removed from the Salinas Valley (Gennet et al., 2013). This
tain commercial production without periodic infusions of habitat removal may result in degradation or loss of the eco-
genetic resources from wild relatives (de Groot et al., 2002). system services typically provided by riparian areas.
The consequences of losing genetic resources in a crop It is important to note that disservices from agriculture can
system can be severe. The Irish potato famine in the 1830s is also affect the productivity and environmental impacts of
one such example. The crop failure can be attributed in part to farming systems through multiple feedbacks. For instance,
a very limited number of genetic strains of potatoes in Ireland, when habitat for natural enemies is removed, pest outbreaks
which made the crop particularly susceptible to potato blight can result in crop damage or loss, resulting in reduced prod-
fungus (Hawtin, 2000). Reintroducing disease-resistant var- uctivity and potentially increased use of pesticides, which may
ieties from Latin America, where the potato originated, helped be accompanied by further detrimental effects. Similarly, when
to resolve the problem. Recent reviews of crop genetic riparian habitat is degraded or removed, the hydrologic ser-
resources highlight that increases in human population size, vices of water flow regulation and water purification services
ecological degradation in farmlands, and globalization have can be diminished or lost (Figure 2).
contributed to a dramatic reduction of crop diversity world-
wide. Approximately 150 species now comprise the world's
most important food crops and most human diets are dom- Managing Ecosystem Services in Agricultural
inated by no more than 12 plant species (Esquinas-Alcázar, Landscapes
2005). Loss of crop genetic diversity is of great concern be-
cause it reduces the pool of genetic material available for Different ecosystem services are mediated and delivered at
natural selection and artificial selection by farmers and plant different scales, ranging from individual farm plots to entire
28 Biodiversity and Ecosystem Services in Agroecosystems

watersheds or regions (Zhang et al., 2007). Accordingly, efforts Considerations for Managing Ecosystem Services
to maintain or enhance ecosystem services in farming land-
Managing ecosystem services requires building an in-depth
scapes may require deliberate management of different areas
understanding of the species, functional groups, and eco-
and scales, including cultivated areas within farms, non-
logical processes through which services are provided
cultivated areas within farms, and broader landscapes (well
(Kremen, 2005). Table 2 highlights some of the key organ-
beyond farm boundaries) that comprise both cultivated and
isms, guilds, and communities that are the biological medi-
noncultivated areas.
ators of ecosystem services and disservices to agriculture. Their
Management of cultivated fields often focuses on eco-
biological activities affect the provision of ecosystem services
system services that have a direct influence on farm product-
at the field, farm, landscape, and regional-to-global scales. For
ivity; farmers have a direct interest in managing services,
example, at the field scale, services of soil structure and fertility
including pollination, pest control, soil fertility and nutrient
enhancement (including the processes of soil formation,
cycling, soil retention, water purification, and water flow
development of structure, and nutrient cycling) are provided
regulation. On-farm practices that target water conservation,
by microbes, invertebrates, and nitrogen-fixing plants. Thus,
including moisture from rainfall that is stored in the soil
field-scale management may focus on practices such as in-
profile, may help to offset water shortages during dry seasons
corporating nitrogen-fixing plants into crop rotations and
or droughts (Rost et al., 2009). Mulching or modification of
planning the timing and depth of tillage to minimize impacts
field tillage practices can reduce evaporation of soil water by
on beneficial invertebrates. At the farm scale, soil-related eco-
30–50%. In addition, farmers can harvest rainwater by in-
system services may also be influenced by levels and types of
stalling microtopographic features in their fields (e.g., small
vegetative cover; thus, farm-scale management may focus on
bunds or pits) as well as ponds, dykes, or other infrastructure,
the total area, type, and timing of harvest (if any) of vege-
enabling recovery of up to 50% of water normally lost in the
tation, including both cultivated and noncultivated areas
system (Rost et al., 2009; Power, 2010).
(Table 2).
Management of noncultivated areas of farms may support
both ecosystem services of benefit both to farmers themselves
and to the broader public. Studies of smallholder farms
have documented the benefits of planting trees in non- Measuring Ecosystem Services and Evaluating Service
cultivated areas, in both temperate and tropical regions, Providers
including Nepal (Carter and Gilmour, 1989) and Costa Rica
(Casasola et al., 2007). Increasing tree cover is associated There is a great deal of interest in methods used to measure
with enhanced diversity and richness of mobile organisms – provision of ecosystem services. One method is to evaluate the
such as birds, bats, and butterflies (Harvey et al., 2006) – soil presence or abundance of organisms believed to provide eco-
retention (Carter and Gilmour, 1989), and carbon seques- system services. A second method is to measure the delivery of
tration (Montagnini and Nair, 2004). In the case of man- the service themselves (Kremen and Ostfeld, 2005). For in-
agement that supports ecosystem services, which provide stance, in order to measure pollination in a California squash
public benefits but does not directly support farm product- field, the first method would focus on the abundance and
ivity (e.g., carbon sequestration needed to support climate distribution of key pollinators, such as native squash bees
regulation), farmers may have less incentive to implement (Peponapis pruinosa) and other insects. Alternatively, the second
management practices. To stimulate provision of public method would evaluate whether a squash crop was sufficiently
benefits, policies and programs may be needed to offset pollinated. These two methods are complementary and may
the costs of management investments or create financial be used together to build a comprehensive understanding
incentives for using new management practices (Garbach of ecosystem service delivery. Counting ecosystem service
et al., 2012). providers can provide insight into the likelihood of an eco-
Broader landscape management to support ecosystem ser- system service being available. In contrast, measuring the
vices requires to understand the ways in which ecosystem outcomes (e.g., pollination metrics, such as seed set or
processes take place across multiple parcels of land (including pollination deficit) can help to verify delivery of a service but
movement of biotic and abiotic components, such as organ- does not provide much information about the organisms
isms, water, and nutrients). Pollination illustrates the im- providing the service. A comprehensive approach to under-
portance of broader landscape management, highlighting that standing and measuring ecosystem services includes under-
mobile organisms respond to resources both within and be- standing key ecosystem service providers (e.g., organisms,
yond cultivated fields. Studies in California suggest that pol- guilds, and communities), factors influencing the ability of
lination by native bees was higher in farms near greater providers to deliver services of interest, and measuring spatial
proportions of natural habitat (no significant relationship was and temporal scales over which providers operate and eco-
found between pollination and farm type, insecticide usage, system services are available (Kremen and Ostfeld, 2005).
field size, or honeybee abundance) (Kremen et al., 2004). The relationships between biodiversity and ecosystem
There is some evidence that multiple farmers practicing di- function are also important for understanding provision of
versified farming – using practices focused on maintaining and ecosystem services (Altieri, 1995; Hooper et al., 2005;
enhancing biodiversity of flora and fauna within and across Tscharntke et al., 2005). In general, species richness – meas-
fields – across a region can result in greater provision of eco- ured as the number of species in a given area – is associated
system services than simply the sum of their individual man- with enhanced ecosystem services (Balvanera et al., 2006).
agement actions (Gabriel et al., 2010). Similarly, biodiversity loss is associated with diminished
 Biodiversity and Ecosystem Services in Agroecosystems 29

Table 2 Ecosystem services and disservices to agriculture, the scales over which they are typically provided, and organism, guilds, and
communities that provide them

Organisms, guilds, and communities that provide services at the following scales:

Field Farm Landscape Region/globe

Services to agriculture
Genetic resources Diversity within a single Diversity across multiple Landrace varieties, wild Landrace varieties, wild
crop; genotypes help to crops; rotations help to relatives of crops; can be relatives of crops; can be
provide pest and disease provide pest and disease used to infuse crops with used to infuse crops with
resistance resistance genetic diversity genetic diversity
Hydrologic services: Water Vegetation within cultivated Vegetation around water Vegetation cover in Vegetation cover in
flow regulation, water areas sources, drains, and watershed; riparian watersheds; riparian
purification ponds communities communities
Pest control Predators, parasites Predators, parasites Predators, parasites –
(animals and insects, (animals and insects, (animals and insects
including vertebrates, including vertebrates, including vertebrates,
invertebrates, and invertebrates, and invertebrates, and
parasitoids) parasitoids) parasitoids)
Weed control Predators, competitors Predators, competitors Predators, competitors –
(herbivores, seed (herbivores, seed (herbivores, seed
predators, and other predators, and other predators, and other
competitors that limit competitors that limit competitors that limit
plants and fungi) plants and fungi) plants and fungi)
Pollination Pollinators: primarily bees Pollinators: primarily bees Pollinators: primarily bees –
but also bats, thrips, but also bats, thrips, but also bats, thrips,
butterflies and moths, butterflies, and moths, butterflies and moths,
flies, wasps, beetles, and flies, wasps, beetles, and flies, wasps, beetles, and
birds (note: some crops birds (note: some crops birds (note: some crops
are wind-pollinated) are wind-pollinated) are wind-pollinated)
Soil structure and fertility Microbes, micro and macro Vegetative cover Vegetative cover –
(including processes of invertebrates, nitrogen-
soil formation, fixing plants
development of structure,
nutrient cycling
supporting fertility)
Erosion protection Cover crops and perennial Cover crops and perennial Riparian vegetation; Riparian vegetation;
crops crops vegetative cover on steep vegetative cover on steep
areas, thin soils; areas, thin soils;
floodplains floodplains
Disservices to agriculture
Pest damage and pathogen Insects, snails, birds, Insects, snails, birds, Insects, snails, birds, –
outbreaks mammals, fungi, mammals, fungi, mammals, fungi,
bacteria, viruses, and bacteria, viruses, and bacteria, viruses, and
weeds weeds rangeland weeds
Competition for water Weeds Vegetation near drainage Vegetation in watersheds Vegetation in watersheds
ditches
Competition for pollination Flowering weeds Flowering weeds Flowering plants in
watershed

Source: Adapted from Zhang, W., Ricketts, T., Kremen, C., et al., 2007. Ecosystem services and dis-services to agriculture. Ecological Economics 64, 253−260.

provision of ecosystem services, often due to reduced efficiency Many ecological studies aim to understand which popu-
of resource capture and use in ecological communities, di- lations, species, functional groups, guilds, food webs, and
minished biomass production, and diminished rates of nu- habitat types produce key services. One method to do so is
trient decomposition and recycling (Cardinale et al., 2012). a functional inventory, which includes identifying and de-
In addition to biodiversity, ecosystem function is influenced scribing the focal ecosystem service providers in a landscape
by the identity, density, biomass, and interactions of species and quantifying their contributions (Kremen and Ostfeld,
within a community (Kremen and Ostfeld, 2005). These at- 2005). A functional inventory is most relevant at the scale
tributes can aggregate at different levels (e.g., field, farm, and of the focal ecosystem service. Thus, evaluating disease re-
landscape scales). Thus, it is important to consider how eco- sistance in crops may require a functional inventory at
logical attributes may vary over space and time, as this can the genetic level, (Zhu et al., 2000) whereas evaluating
influence when and where ecosystem services are available. biological control of pests may require an inventory at the
30 Biodiversity and Ecosystem Services in Agroecosystems

level of a population or food web (Kruess and Tscharntke, from biodiversity-rich rainforests (Ramankutty and Rhemtulla,
1994). 2012). Therefore, existing farmlands are being called on
to simultaneously increase crop yields and provision of eco-
system services. This call for multifunctional agricultural
Functional Differences landscapes can be summarized as agroecosystems in which
A second method to build understanding of ecosystem service productivity and ecological integrity are complementary out-
providers is evaluating functional attribute diversity (Kremen comes, rather than opposing objectives.
and Ostfeld, 2005). This method describes differences within Agroecology is a scientific subdiscipline and farming ap-
the guild, functional group, or community that provides each proach intended to do precisely this by applying ecological
service. A commonly used metric is ecological distance, which concepts and principles to the design and management
describes differences in morphology, ecology, or behavior of of sustainable farming systems (Altieri, 1995). Agroecology
the organisms (Laliberté and Legendre, 2010; Walker et al., emphasizes understanding the ecology of crop, livestock, and
1999) that provide ecosystem services. Characteristics that other species in a farming system as well as the mechanisms
determine how an organism performs key functions are often that govern their functions. It highlights the role of human
used for measuring ecological distance, such as root depth of managers in maintaining and enhancing desirable functions
plants (potential determinant of water flow regulation), tim- and related ecosystem services to optimize use of water, en-
ing of emergence and senescence (primary production and ergy, nutrients, and genetic resources (Altieri, 1995; Gliessman
nutrient cycling), or pollinator's tongue length (pollination). et al., 1998). In doing so, the practice of agroecology often
seeks to intensify production systems – that is, to deliver
greater yields per unit of land, water, or other inputs used – in
Response to Disturbance a way that is based on and, in turn, maintains healthy systems
of soil, water, and biodiversity.
Comprehensive evaluation of the abundance of ecosystem There is considerable evidence that systems of agroecolo-
services providers, and broader patterns of ecosystem services gical intensification can increase yields relative to prevailing
availability, can build a solid foundation for investigating farmer practices in many parts of the world (e.g., Pretty et al.,
potential influence of disturbance. For example, what happens 2006). A recent quantitative review investigated whether
when species that provide key services are lost? Sometimes agroecological intensification systems tend to deliver yield and
ecosystem services are resilient to disturbance and loss. If re- ecosystem service benefits simultaneously (Garbach et al., in
maining species can compensate for the species that are re- press). Here the authors summarize results for two illustrative
moved or have become extinct, ecosystem services may also be systems of agroecological intensification: conservation agri-
maintained rather than diminished. This compensation effect culture and the system of rice intensification.
can happen in several ways. Conservation agriculture is an agroecological intensifi-
First, compensation can occur through response diversity, cation system that aims to increase productivity and sustain-
described as the diversity of responses to change shown among ability of soil resources through three main practices:
species contributing to the same ecosystem functions and (1) minimal soil disturbance, (2) permanent soil cover, and
services disturbance (Elmqvist et al., 2003). Second, it can (3) crop rotations (Kassam et al., 2009). Development agen-
occur through functional compensation, which occurs when cies, such as the Food and Agriculture Organization of the
efficiencies of individual ecosystem service providers shift in United Nations, have promoted this system due to its poten-
response to changing community composition. Third, com- tial applications in farms of diverse sizes and crop systems
pensation may also happen through the portfolio effect. Just as (FAO, 2011).
having a diverse investment portfolio may buffer an investor Field studies of conservation agriculture report benefits in
against fluctuations in individual investments, a diverse bio- soil structure, nutrient cycling, erosion protection, and animal
logical community is more likely to contain some species that biodiversity relative to conventional soil tillage (Milder et al.,
can persist through disturbances (Tilman et al., 1998). 2012). However, inconsistent results have been reported for
key services, such as pest control, which was found to be di-
minished in some field studies due to increased pests harbored
Promoting Synergies between Yield and Ecosystem by crop residues (Van den Putte et al., 2010). Other field
Services studies have reported increased pest control associated with
maintaining soil cover (e.g., mulching and retaining plant
Recent global estimates project the need to double world food residues on soil surfaces) and increased species richness and
production by 2050 (World Bank, 2008a; The Royal Society, population density of beneficial insects, such as predatory
2009; Godfray et al., 2010). At the same time, there is a crickets, beetles, bugs, ants, and spiders (Jaipal et al., 2005).
growing consensus that increased food production must not Synergistic outcomes in conservation agriculture –
come at the expense of diminishing key ecosystem services, enhanced yield and ecosystem services – were reported in
such as carbon sequestration, water flow regulation, and water approximately 40% of comparisons (17 of 43 total quantita-
purification. Additionally, the prospect of clearing additional tive comparisons with conventional cultivation, reported in 16
land for agriculture is unappealing, as most of the remaining studies, Garbach et al., in press) (Figure 3). However, conser-
potentially arable land on the Earth is covered by tropical vation agriculture studies have also reported trade-offs, such
rainforest; agricultural expansion in these areas would come as enhanced yield despite diminished weed control services
at a steep cost to biodiversity and the delivery of services (Haggblade and Tembo, 2003) and diminished yield but
 Biodiversity and Ecosystem Services in Agroecosystems 31

Conservation agriculture
+

Ecosystem services

− +

−
Yield

System of rice intensification Legend

+ Pest control
Weed control
Ecosystem services

>50% of
C sequestration comparisons

Habitat provision
− +
25−50% of
Soil fertility
comparisons
Erosion control

Water purification
>25% of
− Water flow regulation comparisons
Yield

Figure 3 Synergies and trade-offs between ecosystem services and yield in conservation agriculture and system of rice intensification. Bubble
location indicates the specific combination of outcomes for ecosystem services (Y-axis: enhanced, upper quadrants; diminished, lower quadrants)
and yield (X-axis: enhanced, right quadrants; diminished, left quadrants) relative to comparison systems. Bubbles located on the axis indicate no
significant difference from the comparison system. Bubble size indicates the percent of reviewed comparisons reporting each combination of yield
and AEI outcomes: large bubbles indicate 450% of comparisons; medium bubbles indicate 25–50% of comparisons; and small bubbles indicate
o25% of comparisons. The ecosystem services evaluated are represented by colored charts in each bubble and represented as the percentage of
comparisons in which the ecosystem service was measured. Adapted from Garbach, K., Milder, J.C., DeClerck, F., et al., in press. Closing yield
gaps and nature gaps: Multi-functionality in five systems of agroecological intensification. Proceedings of the National Academy of Sciences-Plus.

enhanced soil structure and erosion control (Araya et al., 2011) of both yield and ecosystem services were reported in 87% of
(7% of comparisons, Figure 3). A small number of studies comparisons (39 of 45 quantitative comparisons reported in
have reported both diminished yield and ecosystem service 15 studies, Garbach et al., in press) (Figure 3). Most studies
(6% of comparisons, Figure 3). Diminished yield in conser- compared the system of rice intensification to the predominant
vation agriculture was often associated with a decrease in weed unintensified farmer practices in the study area. Thus, the re-
control (Narain and Kumar, 2005) and pest control services sults suggest that the system of rice intensification can signifi-
(Van den Putte et al., 2010). cantly improve productivity and ecosystem service delivery
The system of rice intensification has received a great deal relative to current practices in many regions. However, the
of recent attention as an agroecological intensification system relative benefits of the system of rice intensification compared
developed specifically for a staple grain. This approach to with regionally specific best management practices in con-
irrigated rice cultivation includes six key practices: transplant- ventional rice farming are less clear (McDonald et al., 2006).
ing young seedlings; low seedling density with shallow root
placement; wide plant spacing; intermittent application of
water (vs. continuous flooding); frequent weeding; and in- Landscape Context
corporation of organic matter into the soil, possibly com-
plemented by synthetic fertilizer (Africare, Oxfam America, From above, agricultural landscapes often resemble a patch-
WWF-ICRISAT, 2010). work of rural villages, natural and seminatural habitat, and
Field studies report considerable evidence for synergies be- farms cultivating a diverse array of crops. ‘Natural habitat’
tween yield and ecosystem services in the system of rice in- in this context describes the full range of natural, seminatural,
tensification, particularly water flow regulation. Enhancement and weedy vegetation types that tend to be present in
32 Biodiversity and Ecosystem Services in Agroecosystems

agricultural areas. However, over the past decades in many Klein et al., 2012). As large fields of a single crop variety re-
parts of the world, remnants of natural habitat have begun place more diversified farms, the total length of time during
disappearing, replaced by vast fields of industrial agriculture which crop species are flowering becomes shorter. As a result,
(Perfecto et al., 2009). This physical restructuring of agri- pollinators may become increasingly dependent on the wild
cultural landscapes has resulted in dramatic changes in many plants that flower throughout the year in noncropped areas
critical ecosystem services. (Mandelik et al., 2012). Pollination services are thus not only
Ecological processes often occur at scales larger than indi- higher but also more stable at field edges than in the interior
vidual farms, making the composition of the broader agri- (Garibaldi et al., 2011).
cultural landscape an essential determinant of ecosystem Although pollination services may vary from crop to crop,
service provision. Natural habitat can provide many benefits to pollinator to pollinator, and region to region, the positive
farmers and the public (Kremen and Miles, 2012). Benefits influence of natural habitat on pollinator activity has proven
include harvestable goods, such as fuelwood, medicinal remarkably consistent across many studies (Ricketts et al.,
plants, and bushmeat, as well as genetic resources provided by 2008). This consistency has allowed researchers to create
crop wild relatives. Natural habitat can provide recreational spatial pollination models that estimate pollination provision
opportunities and has been found to support mental health on the farm based on the composition of the surrounding
in some case studies (Bratman et al., 2012). landscape (Lonsdorf et al., 2009). For instance, the InVEST, the
Ensuring that agricultural systems realize diverse benefits ecosystem service modeling platform operated by the Natural
requires looking beyond on-farm practices and managing the Capital Project, allows land managers to predict the pollin-
broader landscape. Here the authors focus on examples of ation consequences of their land-use decisions and manage
landscape management for two animal-mediated ecosystem land assets accordingly.
services: pollination and pest control. Many other ecosystem
services, including water purification, genetic resources, and
soil structure and fertility enhancement, also require landscape
Pest Control
management. Animal-mediated services, however, are among
the most severely affected by landscape simplification, and Not all crops are animal pollinated, but every crop suffers pest
landscape-level effects have been well documented. damage. The shift from diversified, agricultural landscapes
When natural habitat is removed for agriculture, beneficial with patches of natural habitat to large monocultures that lack
pollinators and predators of insect pests often decline in natural habitat has likely brought with it more severe pest
abundance, whereas pests increase, which may precipitate outbreaks. High vegetation diversity ensures that specialist
lower yields for farmers (Philpott et al., 2008; Karp et al., 2011; pests do not enjoy vast food resources (Matson et al., 1997).
Melo et al., 2013). The amount of natural habitat required to Further, because not all crops and vegetation in natural habitat
sustain pest control and pollination services is often a product is palatable to pests, complex landscapes may inhibit pest
of the home range sizes of the predator and pollinator species movements and cause more localized outbreaks (Avelino et al.,
that provide these services, an attribute that can vary con- 2012). However, natural habitat can sometimes provide pests
siderably among species. The relevant management scale for with resources vital for completing their lifecycles and thus
farmers depends on both the focal ecosystem service and on facilitate outbreaks (Chaplin-Kramer et al., 2011b). For ex-
the attributes of its animal providers. Fortunately, the past ample, because aphids sequester chemicals in wild mustards
decades have seen a surge of research documenting the role of (Brassica nigra) as antipredator defenses, the proximity of
landscape structure and composition in sustaining pollinators natural habitat with high mustard density may function to
and pest control providers. increase the density of aphids in nearby crop fields (Chaplin-
Kramer et al., 2011a).
Another critical consideration, however, is the predators
of crop pests. Predators rely on natural habitat for essential
Pollination
activities, including breeding, roosting, foraging, and hiber-
Although managed honey bees (Apis mellifera) provide most nating (Landis et al., 2000; Jirinec et al., 2011). Predator
pollination globally, native insects are often more effective abundance and diversity thus regularly decline as agricultural
pollinators and provide complementary pollination benefits landscapes shift from complex mosaics of natural habitat and
(Garibaldi et al., 2013). Further, native insects enhance pol- cropland to simplified monocultures (Bianchi et al., 2006;
lination resilience, especially as honey bee colonies continue Chaplin-Kramer et al., 2011b). Although diverse predator
to collapse (Winfree and Kremen, 2009). Retaining a diverse communities are not always more effective at providing pest
pollinator community is thus increasingly recognized as an control because predators sometimes consume each other
essential component of any sustainable food system. (Vance-Chalcraft et al., 2007), most studies report that more
Unsurprisingly, native pollinators rely on native habitat. predator diversity translates to more effective pest control
Many species center their foraging activity around the nest, (Bianchi et al., 2006; Letourneau et al., 2009; Chaplin-Kramer
often located in patches of habitat embedded in agricultural et al., 2011b).
landscapes (Lonsdorf et al., 2009; Jha and Kremen, 2013). An increasing number of studies have documented in-
Pollinator activity matches pollinator foraging ranges, and creased pest consumption in complex versus simple landscapes
pollination is thus consistently higher at the edges of crop (Thies and Tscharntke, 1999; Gardiner et al., 2009; Chaplin-
fields near native habitat than in the interior of large crop Kramer and Kremen, 2013; Karp et al., 2013). Fewer studies,
monocultures (Kremen et al., 2004; Ricketts et al., 2004, 2008; however, have traced the benefit of maintaining natural habitat
 Biodiversity and Ecosystem Services in Agroecosystems 33

all the way to crop yields and profits, but some have reported habitat, coffee plants located near rainforest enjoy significantly
positive effects (Thies and Tscharntke, 1999; Karp et al., higher pollination than sites in the middle of extensive plan-
2013). Like pollination, the relevant scale for pest manage- tations. Higher pollination translates to higher yields, better
ment can vary from predator to predator and from pest to coffee quality, and increased profits. One study found that
pest, such that distant areas may determine the abundance yields increased by 20% and misshaped ‘peaberries’ decreased
of highly mobile animals (Werling and Gratton, 2010). Sim- by 27% within 1 km distance of two forest patches (Ricketts
ply focusing on local agricultural practices may be ineffective. et al., 2004). These benefits translated into a significant eco-
Because predator communities often collapse after harvest, nomic gain, approximately US$60 000 per year for a single
a stream of colonizers from adjacent natural habitat may coffee plantation.
be required to replenish the predator community in the Costa Rican coffee plantations also enjoy pest control
following year. benefits from forest patches. The coffee berry borer beetle
(Hypothenemus hampeii), coffee's most damaging insect pest,
arrived in Costa Rica in 2000 and the canton of Coto Brus in
Landscape Effects on Agriculture: A Costa Rican Case Study 2005 (Staver et al., 2001). Not more than 5 years later, native
Tropical rainforest provides an array of ecosystem services, birds had already expanded their diets to include the pest and
including water purification, water flow regulation (e.g., sup- began reducing infestation severity by half (Karp et al., 2013).
porting hydropower production), carbon sequestration, and Like wild bees, many of the pest-eating birds rely on forest
cultural services such as ecotourism. Recognizing this, in the habitat, and pest control provision is higher on farms with
mid-1990s the Costa Rican government created the first na- more forest cover (Karp et al., 2013). Small, unprotected forest
tional payment for ecosystem services (PES) scheme, in which patches embedded in coffee plantations provided the most
landowners were paid to maintain rainforest on their private benefits. Forest patches smaller than 1 ha area secured ap-
lands (Sánchez-Azofeifa et al., 2007). For farmers, the program proximately 50% of the total pest control benefits across the
provided the dual benefit of monetary compensation for un- Coto Brus valley (Figure 4).
cultivated lands and continued provision of critical ecosystem
services.
The canton of Coto Brus in Southern Costa Rica has been Policies and Programs to Conserve and Enhance
studied as a model system for how strategic conservation ef- Ecosystem Services in Agricultural Landscapes
forts influence agricultural production. Unlike many other
parts of the country that now host vast expanses of pineapple, Growing interest in the management of ecosystem services has
oil palm, or banana, Coto Brus still exists as a patchwork of been matched, in recent years, by a proliferation of policy
coffee plantations, pasture, small rural villages, and tropical and programmatic strategies to promote the conservation or
wet forest, perhaps a result of its hilly terrain (Mendenhall enhancement of these services in agricultural landscapes.
et al., 2011). This complex configuration supports a remark- Traditionally, environmental management policies were often
able concentration of biodiversity, often at par with native described in terms of a dichotomy between regulatory instru-
forest (Daily et al., 2001; Mendenhall et al., 2013). Coffee, the ments (‘command and control’ requirements put forth by
most extensively cultivated crop in the region, benefits from governments) and market-based instruments focused on
this biodiversity. Although coffee can self-pollinate, animal shifting incentives and price signals for farmers, businesses,
pollination increases yields, sometimes by more than 50% and other market actors. However, this dichotomy is now
(Ricketts et al., 2004). Because wild bees rely on rainforest understood to be too simplistic: not only have the boundaries

0.25
km

2370 kg Berries saved

0 kg Berries saved
N

Coffee
1.5
km Pasture

Figure 4 Pest control value of forest patches to coffee plantations in Southern Costa Rica forest provides habitat for the insectivorous birds that
consume the coffee berry borer beetle (Hypothenemus hampei), coffee's most economically damaging insect pest. Maps show the estimated
kilograms of coffee berries saved from infestation by each patch of forest across the Coto Brus Valley. Integrated together, the small, unprotected
forest patches embedded within or adjacent to coffee plantations provided the majority of pest control value to coffee farmers.
34 Biodiversity and Ecosystem Services in Agroecosystems

between regulatory and market-based approaches blurred in forestry. Land-use regulations restrict or prohibit agriculture in
many cases, but the range of market-based approaches has also certain locales (e.g., protected areas, watershed conservation
proliferated to the point where further categorization is ne- areas, and multiuse management zones) and in some instances
cessary (Lemos and Agrawal, 2006). This situation reflects a aim to reduce the degree to which agriculture conflicts with the
broader shift from the primacy of state institutions in en- provision of important ecosystem services. On a broader scale,
vironmental governance to the inclusion – and sometimes both Brazil and Indonesia have enacted temporary moratoria
dominance – of other groups, including corporations, con- on deforestation for agricultural expansion, which have been
sumers, civil society organizations, and multinational organ- credited with reducing the loss of ecosystem services associated
izations (Liverman, 2004). with soybean and oil palm expansion, respectively (Macedo
Before describing the range of policy and programmatic et al., 2012). A limited number of regulation require on-farm
strategies used to conserve and manage ecosystem services protection of remaining natural ecosystems (e.g., remnant
from agricultural landscapes, it is worth noting some chal- forest patches), or riparian buffers, recognizing their capacity to
lenges endemic to the governance of agricultural systems, provide ecosystem services both within and beyond cultivated
which have limited the effectiveness of most if not all these areas. Nonetheless, these regulations are quite limited overall,
strategies to varying degrees. First, in contrast to other eco- and, in many places where they exist, have been poorly en-
system types that are major providers of ecosystem services forced and widely ignored. A notable example is Brazil's Forest
(e.g., forests, wetlands, and water bodies), agricultural lands Code, which on paper requires farmers to establish mosaics of
are predominately owned or managed by private individuals natural habitat within agricultural landscapes but in practice
and companies, or in some instances collectively by rural has been generally flaunted.
communities. This means that government authorities gener- Regulation of certain farm inputs – particularly pesticides –
ally cannot influence the use of these lands simply by ad- is robust in many countries and may help to mitigate certain
justing management plans and policies for lands and water negative impacts of agriculture, including the negative off-site
over which they have substantial control, as they might for a impacts on water quality. However, even where the most toxic
state-owned protected area or water body. Second, the his- pesticides are effectively regulated, use of other legal, but still
torically private nature of agricultural enterprises means that toxic, pesticides may contribute to large aggregate impacts that
there is little tradition of public sector regulation of agri- diminish both water quality and habitat provision (Schiesari
cultural activities, at least with regard to major agronomic et al., 2013). In particular, pesticide contamination can nega-
decisions affecting ecosystem services, such as rural land use, tively affect the ecological communities in waterways, resulting
tillage, planting, and soil fertility management. in degradation or loss of the important services these com-
Third, agricultural management systems are highly context- munities provide (e.g., pest control services provided by
dependent (based on climate, soils, hydrology, and other mosquito fish in small channels near populated areas; fishing
factors), making it inappropriate to devise ‘one size fits all’ and other cultural services supported by rivers and streams).
regulations and frequently inefficient to incentivize specific Agriculture (and the ecosystem services it provides) may
management practices, which may not be appropriate in all also be governed by broader regulations that apply across
contexts. Fourth, most of the major ecosystem services and many sectors. However, these laws are not always applied fully
disservices from agriculture are ‘nonpoint’ in nature, meaning in the context of farms and ranches. For instance, in the United
that they flow from the land itself, in heterogeneous patterns, States, agricultural operations enjoy a variety of statutory or de
and are, therefore, difficult to quantify, monitor, or regulate facto exemptions from otherwise strong environmental laws
(Ribaudo et al., 2010). In contrast, point source impacts, such including the federal Clean Water Act, federal Endangered
as water withdrawals and factory emissions from a smokestack Species Act, and certain state endangered species acts. These
or effluent pipe, are much easier to monitor and regulate exemptions highlight both the privileged political status that
and have been the subject of many effective environmental the agriculture sector enjoys in many countries and the dif-
regulations. Fifth, monitoring and enforcement in agricultural ficulty in enforcing these types of laws in an agricultural con-
settings is always a challenge, given the dispersed, private na- text. They also underscore the need for interventions focused
ture of agricultural activities and the nonpoint nature of key on ecosystem services that support rather than compromise
ecosystem service outcomes. This is particularly so on the production functions.
world's approximately 350 million small farms, where the
transaction and administrative costs of policies and programs
can become proportionately quite high.
Market-Based Instruments
Table 3 provides a basic typology of policies, programs,
and instruments that may be used to conserve and enhance In the context of policy options, the term ‘market-based’ is
ecosystem services from agricultural landscapes. Each of these used broadly to refer to strategies that seek to influence be-
is described further below. havior by adjusting the price signals to various market actors,
including farmers, corporations, and consumers. Such instru-
ments are often intended to remedy ‘market failures’ that can
occur when the providers of ecosystem services do not reap the
Government Regulation
full benefit of delivering these services, or when they avoid
Agriculture in most countries is a relatively lightly regulated bearing the full cost when they diminish these services. For
enterprise when compared with other land uses, such as instance, farmers usually receive little or no monetary benefit
industrial facilities, mines, urban development, and even from protecting wildlife habitat, although this is an important
 Biodiversity and Ecosystem Services in Agroecosystems 35

Table 3 Typology of policies, programs, and instruments that may be used to conserve and enhance ecosystem services from agricultural
landscapes

Type of policy, program, or Level of state involvement Role of farmers Examples

instrument

Government regulation (‘command and control’)

Land use regulations High (set and enforce Subject of regulations Land-use zoning; temporary
regulations) moratoria; riparian buffer zone
requirements
Regulation of agricultural Bans and restrictions on use of
inputs certain pesticides; prohibition on
planting genetically modified
organisms
Regulation of other Good agricultural practices
agricultural practices regulations focused on food safety
Other regulations affecting Regulations on water, wetlands, and
agricultural lands endangered species
Market-based instruments (influencing price signals or incentive structures)
Taxes and subsidies High (establish tax and Payer of taxes or recipient of Earning tax credits for best
subsidy policies) subsidies management practices (e.g.,
Resource Enhancement and
Protection Program in PA, USA)
subsidies for no-till planters
Markets formed through Moderate to high (set Buyers or sellers of ecosystem Water quality trading, regulated
regulation (e.g., cap-and- regulations and oversee services, where required or carbon markets
trade), leading to PES market) eligible to participate
Public sector PES High (deploy funds and Sellers of ecosystem services Agri-environment payments (Europe),
administer PES Farm Bill environmental programs
program) (USA)
Private and voluntary PES None or low Buyers or sellers of ecosystem Various watershed, biodiversity, and
services carbon PES involving farmers
Eco-standards and None to moderate Sellers of agricultural goods IFC Performance Standards,
certification produced in accordance with Rainforest Alliance, and
eco-standards Roundtable on Sustainable Palm Oil
Rural development and farmer assistance programs
Technical assistance and None to high (some Program participants and Farm Bill programs for conservation
cost-share programs programs are funded or beneficiaries measures on US farms
Education and training run by the public sector, Conservation Farming Unit (Zambia)
programs others by private or civil
Rural development projects society entities) Sustainable Land Management
and programs investments (Global Environmental
Facility/World Bank)

Note: Some of these instruments also serve additional aims or are not always used to manage ecosystem services in agricultural landscapes. The abbreviation PES stands for payment
for ecosystem services.

public benefit. Conversely, when fertilizer runoff from farms of ecosystem services. For instance, in Kazakhstan, the govern-
contributes to downstream eutrophication and its attendant ment in 2008 began subsidizing farmers to adopt conservation
environmental and economic harms, the farmers responsible agriculture technologies – including continuous soil cover, direct
for these harms usually bear no economic consequences. seeding, and no-till management – that are credited with helping
Market-based instruments can address such environmental to increase farmer yields and profitability while reducing soil
‘externalities,’ which would otherwise result in suboptimal erosion.
delivery of or investment in the provision of ecosystem PES are abroad set of market-based instruments that have
services. proliferated since the mid-1990s to channel new investment in
The most long-standing types of market-based instruments ecosystem services. Formally, PES has been defined as volun-
are various forms of taxes and subsidies, which are deployed tary transactions between ecosystem service seller(s) (such as
across many different economic sectors, including agriculture. farmers or other land managers) and ecosystem service buyer
Historically, agricultural subsidies (e.g., for fertilizer inputs) (s) (such as water users or conservation organizations) that
played a significant role in promoting both the expansion and provide cash or other payment in exchange for the provision
intensification of agriculture to the significant detriment of eco- of specific defined ecosystem services (Engel et al., 2008). In
system services. However, taxes and subsidies can also promote practice, however, many PES schemes do not conform to this
conservation-friendly agriculture that may deliver increased levels definition, for instance, because they do not target specific
36 Biodiversity and Ecosystem Services in Agroecosystems

ecosystem services or make payments contingent on actual (Southeast Asia), where levels of carbon payments supported
delivery of these services (Muradian et al., 2010). For instance, by ecosystem service markets may provide insufficient in-
many publicly administered PES schemes – including those in centive to prevent deforestation and the significant loss of
Costa Rica, Mexico, Europe, and the United States – function ecosystem services (Fisher et al., 2011).
more like environmentally focused farmer subsidy programs A final market-based instrument is the adoption and use
than true conditional payments targeted to deliver the largest of voluntary sustainability standards – often called ‘eco-
quantity of ecosystem services for the least cost. standards’ – and associated ‘eco-certification’ labels for agri-
Ecosystem service payments that involve the creation of cultural products and investments. Agricultural sustainability
open markets (as opposed to government payments) are likely standards are sets of social and environmental criteria put forth
to more closely resemble market-based instruments in the to define and encourage sustainable farming by providing
classic sense of the term. In the United States and other market recognition for sustainable producers. These include
countries, such markets have been established through regu- standards developed and managed by nonprofit organizations
lations that cap total levels of pollution or degradation to a (e.g., Fairtade, Rainforest Alliance, and UTZ Certified), multi-
given ecosystem or ecosystem type but enable landowners to stakeholder ‘roundtables’ for various commodities (e.g., for
trade the limited allocated rights to pollute or degrade. Such soybeans, palm oil, sugar, beef, and cotton), individual food
‘cap-and-trade’ mechanisms are intended to reduce the overall companies (e.g., Unilever, Nestlé, Mars, and others), and the
cost of achieving specific environmental goals and have re- finance sector (e.g., IFC Performance Standards and the Equator
sulted in robust markets for wetland mitigation, wildlife Principles). By participating in such schemes, farmers, traders,
habitat, and agricultural runoff, among other ecosystem ser- and food companies that produce and sell certified products
vices and disservices. Truly voluntary private markets for eco- may benefit from improved market access or market share, price
system services involving farmers as ecosystem service sellers premiums, or improved legitimacy and reputation in the eyes of
have also developed in places, although on a smaller scale. consumers and regulators. Most, if not all, agricultural sus-
These markets have formed around carbon sequestration, tainability standards include provisions intended to help con-
watershed conservation, and biodiversity protection, with serve biodiversity, including sensitive habitat that supports
buyers ranging from private companies (e.g., water bottling organisms of conservation concern, and ecosystem services
businesses), to individuals and corporations wishing to offset (e.g., water purification and water flow regulation and soil
their carbon emissions, to conservation organizations. fertility and erosion control) (UNEP-WCMC, 2011). Thus, e
On a global scale, PES makes only a modest contribution co-certification may provide monetary incentives for farmers to
to incentivizing increased ecosystem service delivery from maintain or enhance ecosystem services, although such in-
agricultural landscapes. However, this contribution is pro- centives are not necessarily explicit or direct with respect to
portionately much larger in the United States, Europe, and specific ecosystem services.
China, where large government PES programs – totaling per-
haps US$20 billion per year – exist to support watershed
Rural Development and Farmer Assistance Programs
protection, biodiversity conservation, and esthetic protection
(‘landscape beauty’) services (Milder et al., 2010). The future Governments, international donors, civil society organiza-
size of ecosystem service markets affecting farmers remains tions, and others have been involved for decades in supporting
uncertain: although it is clear that farmers deliver critical agricultural development around the world. In the past 10–15
ecosystem services to a wide range of stakeholders, it is not years, an increasing proportion of these efforts have begun
clear whether these beneficiaries will actually be willing to pay to orient program objectives and activities toward maintaining
for such services on a large scale, or whether markets will be or increasing flows of ecosystem services in concert with in-
formed that support the cost-effective procurement and man- creased yields and farmer profitability. Some initiatives, par-
agement of these services. The future regulation of greenhouse ticularly in developed countries, provide technical assistance,
gas emissions (or lack thereof) at national or global level is a farmer training, or cost sharing of on-farm investments to re-
critical factor, as farmers stand to participate heavily in carbon duce the negative environmental impacts of agriculture. For
markets if they coalesce at full scale. instance, a variety of programs funded under the US Farm Bill
Experience from a wide range of contexts suggests that PES provide technical assistance and cost sharing for practices such
in agricultural landscapes is likely to be most effective and as improved water management structures, erosion control
scalable where management practices that sustain or increase practices, integrated pest management, and transitioning to
ecosystem service delivery also support agricultural product- organic practices.
ivity or profitability. In these situations, PES can provide In the developing world, agricultural development efforts
farmers with supplemental revenue that helps them to over- that strongly integrate ecosystem management have been ad-
come initial investment barriers or other constraints to vanced under a variety of names and approaches. A 2006 re-
adopting more conservation-friendly management practices view surveyed 286 such interventions covering a total of 37
(FAO, 2007; Majanen et al., 2011). However, where there is a million hectares and found evidence of substantial increases in
high opportunity cost to manage agricultural landscapes for crop yields together with water-use efficiency gains and po-
increased levels of ecosystem services, PES schemes are un- tential gains for carbon sequestration and other ecosystem
likely to be able to compete with the profitability of en- services (Pretty et al., 2006). More recently, the World Bank
vironmentally destructive farming and will find few willing and other multilateral institutions have supported ‘sustainable
sellers of ecosystem services. A prime example is at the agri- land management’ programs in dryland regions of dozens of
cultural frontiers of major commodity crops, such as palm oil countries to enable farmers and pastoralists to increase
 Biodiversity and Ecosystem Services in Agroecosystems 37

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