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Biodiversity and Ecosystem Services in AgroecosystemsK Garbach, Loyola University Chicago, Chicago, IL, USAJC Milder, Rainforest Alliance, New York, NY, USAM Montenegro and DS Karp, University of California-Berkeley, Berkeley, CA, USAFAJ DeClerck, Bioversity International, Maccarese, Rome, Italy

r 2014 Elsevier Inc. All rights reserved.

GlossaryAgroecology The application of ecological concepts andprinciples to the design and management of sustainableagroecosystems.Agroecosystems Agricultural ecosystems includingbiophysical and human components and their interactions.Biodiversity The variation of life in all forms from genes,to species, to communities, to whole ecosystems.Ecosystem service providers Organisms, guilds, andecological communities that are biological mediators ofecosystem services, providing services through theirfunctions and interactions.Ecosystem services Functions of ecosystems – includingagroecosystems – that are useful to humans or supporthuman well-being: (1) provisioning services include theproduction of food, fuel, fiber, and other harvestable goods;(2) regulating services include climate regulation, floodcontrol, disease control, waste decomposition, and waterquality regulation; (3) supporting services include thefoundational processes necessary for production of otherservices, including soil formation, nutrient cycling, andphotosynthesis (primary production); and (4) cultural

cyclopedia of Agriculture and Food Systems, Volume 2 doi:10.1016/B978-0-444

services provide recreational, esthetic, spiritual, and othernonmaterial benefits.Human well-being A context- and situation-dependentstate that comprises basic material for a good life, freedomand choice, health, good social relations, and security.Millennium Ecosystem Assessment An internationalsynthesis released in 2005, created by more than 1000 ofthe world's leading scientists, that analyzed the state of theEarth's ecosystems.Payment for ecosystem services Market-basedinstruments used to channel investment in ecosystemservices.Resilience The capacity of a system to absorb disturbanceand retain structure and function; this includes the humancapacity to anticipate and plan for the future (e.g., inmanaging agricultural systems).Scale Geographical extent; relevant scales foragroecosystems often include units commonly used inmanagement and decision making, such as field (local andon-farm cultivated area), farm (including cultivated andnoncultivated areas), landscape, regional, and global.

Introduction

Historically, agricultural systems have been managed, aboveall, for the production of food and fiber; however, agriculturallandscapes can provide a wide range of goods and services tosociety. ‘Ecosystem services’ are those functions of ecosystems– including agroecosystems – that are useful to humansor support human well-being (Daily, 1997; Kremen, 2005).The ecosystem services concept is remarkably longstanding.Mooney and Ehrlich (1997) noted that in approximately 400BC, Plato observed how forests provided important services toAttica and forest loss resulted in drying springs and soil ero-sion. Plato's work highlights that people have been awareof these critical services long before the dawn of industrialagriculture (Rapidel et al., 2011).

In the past two decades, work at the interface of ecologyand economics to characterize, value, and manage ecosystemservices has supported a paradigm shift in how society thinksabout ecosystems and human relationships to them. As bothmajor providers and major beneficiaries of ecosystem services,agricultural landscapes and the people within them are at thecenter of this shift. Growing calls for agriculture landscapes tobe managed as ‘multifunctional’ systems create new mandates,as well as opportunities, to maintain and enhance ecosystemservices as part of productive agroecosystems.

Work on multifunctional ecosystems draws on the Millen-nium Ecosystem Assessment (2005) and other recent evalu-ations of ecosystem services (e.g., The Economics of Ecosystemsand Biodiversity and The Common International Classificationof Ecosystem Services). The Millennium Ecosystem Assessmentprovides a globally recognized classification that emphasizesrelationships between ecosystem services and human well-being and describes four types of services (The authors drawon the classification of ecosystems services used in MillenniumEcosystem Assessment throughout the article (MEA, 2005),recognizing that more recent classifications have minimizedor eliminated supporting services in favor of specific, oper-ational descriptions designed for environmental accounting(Haines-Young and Potschin, 2012) and economic valuation(TEEB, 2010)). Provisioning services include the productionof food, fuel, fiber, and other harvestable goods. Regulatingservices include climate regulation, flood control, diseasecontrol, waste decomposition, and water quality regulation.Supporting services include the foundational processes neces-sary for production of other services, including soil formation,nutrient cycling, and photosynthesis (primary production).Cultural services provide recreational, esthetic, spiritual, andother nonmaterial benefits. Most classifications, despite theirvariations, consider interdependence between ecosystem ser-vices and human well-being as well as variation in ecosystem

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22 Biodiversity and Ecosystem Services in Agroecosystems

services across spatial scales ranging from local to global(Figure 1).

Biodiversity – the variation of life in all forms from genes, tospecies, to communities, to whole ecosystems – is a significantdeterminant of ecosystem function and provision of ecosystemservices. Although relationships between biodiversity and eco-system services are complex and vary widely across differenttypes of ecosystems, at the broadest level, increased nativebiodiversity is generally associated with higher levels of eco-system services within a given system (Balvanera et al., 2006;Cardinale et al., 2012). Plant diversity, for example, has beenfound to enhance belowground plant and microbial biomass,which is associated with the ecosystem service of erosion

Human well-beinBasic materials and conditio

for a good life

Ecosystem services

ProvisionGoods and products obtaine

RegulatinBenefits obtained from regu

processe

CulturaNonmaterial benefits obtain

Biodiversity

Sup

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oth

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cosy

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ser

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Food, fuel, Biochemic

Genetic reso

Humanactivities

Carbon sequePollination, pes

carbon sequestration clwater purific

Spiritual and reRecreation, ecoEsthetics, insp

Sense of pCultural her

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Figure 1 Typology of ecosystem services. This ecosystem service typologyconsiders biodiversity as a foundation for all ecosystem services (representeinclude provisioning, regulating, and cultural services (dark gray boxes, solidoutline). Ecosystem services support human well-being (charcoal gray box, wuse management decisions. Both ecosystem services and human well-beingglobal.

control through the effects of large root and mycorrhizal net-works holding soil in place (Balvanera et al., 2006). It is alsoimportant to note that some ecosystem services are provided inpart by the abiotic (nonliving) components of ecosystems, suchas aquifers and inorganic portions of soils. Biodiversity can beconsidered a form of ‘biological insurance’ that helps to assureecosystem performance, including providing ecosystem ser-vices, as diversity increases the chances that one or more specieswill be able to perform critical functions, even in the event ofdisturbance or species loss (e.g., natural disaster and human-induced land use change) (Naeem and Li, 1997).

Agroecosystems both provide and rely on ecosystemservices to sustain production of food, fiber, and other

gns necessary

Local

ingd from an ecosystem

glation of ecosystems

led from ecosystems

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Global

Regional

, adapted from the Millennium Ecosystem Assessment (MEA, 2005),d with a dotted line framing ecosystem services). Ecosystem servicesoutline), as well as supporting services (light gray box, dashedhite text), and, in turn, are influenced by human activities and land-can be considered at nested spatial scales from local, to regional, to

MAC_ALT_TEXT Figure 1

Biodiversity and Ecosystem Services in Agroecosystems 23

harvestable goods. Many services have on-farm benefits (e.g.,for farmers, plantation managers, and other people on-site),whereas others have broader public benefits to off-farm users;some benefit both groups (Table 1).

Table 1 Ecosystem service descriptions and related on-farm benefits an

Ecosystem service Description

Provision of food, fuel, fiber,and biochemicals

Harvestable goods fromagroecosystems

Soil structure and fertilityenhancement

Soil structure and processes ofnutrient cycling and deliveryof nutrients to plants;processing organic matterand transforming detritus andwastes

Erosion protection Soil retention; limiting soil lossthrough wind and watererosion

Hydrologic services: Water flowregulation

Buffering and moderation of thehydrologic cycle, includingwater infiltration into soilsand aquifers, moderation ofrunoff, and plantstranspiration

Hydrologic services: Waterpurification

Filtration and absorption ofparticles and contaminants bysoil and living organisms inthe water and soil

Pollination Transfer of pollen grains tofertilize flowers

Pest control Control of animal and insectpests by their natural enemies– predators, parasites, andpathogens

Weed control Botanical component of pestcontrol; suppressing weeds,fungi, and other potentialcompetitors through physicaland chemical properties ofcover crops, intercrops, andother planted elements

Carbon sequestration Atmospheric carbon dioxide istaken up by trees, grasses,and other plants throughphotosynthesis and stored ascarbon in biomass and soils

Genetic resources Pool of genetic diversity neededto support both natural andartificial selection

Cultural and esthetic services Maintaining landscapes thatsupport: esthetics andinspiration; spiritual andreligious values; sense ofplace; cultural heritage;recreation and ecotourism

aOn-farm carbon sequestration can be associated with on-farm benefits in closely related e(e.g., shade provided by trees).

The evaluation and management of ecosystem servicesin agricultural landscapes has emerged as a top priority forseveral reasons. First, agricultural ecosystems – includingcroplands and pastures – are among the largest terrestrial

d public, off-farm benefits

On-farm benefits Public, off-farm benefits

Food and other goods for on-farm consumption or sale

Goods for agricultural markets

Support for crop growth; canlimit need for chemicalfertilizers

May limit need to mine ormanufacture chemicalfertilizer

Maintain soil, and the nutrientsit contains, to supportproduction

Potential reduction of sedimenttransfer to downstreamsystems & users

Water in soils, aquifers, andsurface bodies available tosupport plant growth

Stabilize stream base flow andmitigate flooding todownstream areas; rechargeinto aquifers and bodies ofwater; plant transpiration maysupport precipitation patterns

Clean water available for humanconsumption, irrigation, andother on-farm uses

Clean water available todownstream users

Necessary for seed set and fruitproduction in flowering plantsand crops

Necessary for outcrossing innoncultivated flowering plants

Minimize crop damage and limitcompetition with crops

May limit need for pesticidesthat threaten environmentaland human health

Minimize weed competitionwith crops

May limit need for herbicidesthat threaten environmentaland human health

Few demonstrable on-farmbenefitsa

Regulation of the carbon cycle;mitigation of greenhouse gascontributions to atmosphericchange

Distinct genotypes (cultivars)allow fruit set in orchards andhybrid seed production; traitdiversity (from landraces andwild relatives) supportsdisease resistance, newhybrids, and climateadaptations

Prevention against large-scalecrop failure

Esthetics and inspiration;spiritual and religious values;sense of place; culturalheritage; recreation andecotourism

Esthetics and inspiration;spiritual and religious values;sense of place; culturalheritage; recreation andecotourism

cosystem services, such as increased soil organic matter and microclimate regulation


biomes and account for approximately 40% of the Earth'ssurface (Foley et al., 2005). Second, increases in food andfiber production have often been achieved at the cost ofother critical services. The Millennium Ecosystem Assessment(2005) reported that approximately 60% (15 out of 24) ofservices measured in the assessment were being degradedor unsustainably used as a consequence of agricultural man-agement and other human activities. Finally, evaluations of‘planetary boundaries,’ which describe the safe operating spacefor human activities with respect to the planet's biophysicalsystems and processes, indicate that modern, industrial agri-culture is among the activities that have most significantlyundermined the Earth's life-support systems (Rockström et al.,2009). Major negative impacts have occurred through con-verting natural habitat to agriculture and infrastructure, en-vironmental pollution, and environmental change induced byshifts in nitrogen and phosphorus use.

Recent work highlights the need for better understandingthe ecological processes that underpin critical ecosystem ser-vices (Kremen, 2005). Provision of ecosystem services infarmlands is directly determined by their design and man-agement (Zhang et al., 2007) and strongly influenced by the

Services to agriculture

Disservices to agriculture

Genetic resources

Water flow regulationWater purification

Pest control

Pest damage

Competition for:• Water• Nutrients• Pollination

Pathogen outbreaks

Pollination

Soil structure and fertilityenhancement

Hydrologic services—

Feedba

Agroecosy

Figure 2 Ecosystem services and disservices to and from agriculture Farmservices, and in many cases these relationships are deliberately managed byin the diagram. Production systems can also suffer from various disservicesrelationships are usually the unintentional result of management action, reprDisservices from agriculture can also lead to agricultural inputs and result inenemies is removed and pest outbreaks increase, represented by the feedbacRicketts, T., Kremen C., et al., 2007. Ecosystem services and dis-services toF., Robertson, G., Hamilton, S., 2007. Ecosystem services and agriculture: CEconomics 64, 245–252.

function and diversity of the surrounding landscape (Kremenand Ostfeld, 2005; Tscharntke et al., 2005). Yet, there is anoutstanding need for field studies that describe the mech-anisms, which control how ecosystem services vary across bothspace and time. Building understanding of the mechanismsunderlying ecosystem services is also essential to developingthe ability to predict how management activities will affectthe single ecosystem services, and suites of services, neededto support both productive farmlands and human well-being.

Ecosystem Services and Disservices in AgriculturalLandscapes

Ecosystem Services and Disservices

Agroecosystems both provide and rely on ecosystem services.Services that help to support production of harvestable goodscan be considered services to agriculture (Zhang et al., 2007).These services include soil structure and fertility enhancement,nutrient cycling, water provision, erosion control, pollination,and pest control, among others (Figure 2). Ecological

Services from agriculture

Disservices from Agriculture

Provisioning services:

Other ecosystem services:

Carbon sequestration

Soil conservation

Habitat provision

Habitat degradation/loss

Soil degradation/loss

Water quality degradation/loss

Other off-site, negative impacts

ck

stems

(e.g., negative impacts thatdiminish ecosystem services)

Cultural and aesthetic services

Food, fuel, fiberbiochemicals

ing systems can be both producers and beneficiaries of ecosystemfarmers. Such ecosystem services are represented by two gray boxesor contribute to disservices or loss of services. These negativeesented by the two lower gray boxes and the dashed arrows.detrimental on-farm impacts, such as when habitat for naturalk arrow at the bottom of the diagram. Adapted from Zhang, W.,agriculture. Ecological Economics 64, 253–260 and Swinton, S., Lupi,ultivating agricultural ecosystems for diverse benefits. Ecological



processes that detract from agricultural production can beconsidered disservices to agriculture (Zhang et al., 2007) andinclude pest damage, competition for water, and competitionfor pollination. Management of agricultural ecosystems alsoaffects flows of ecosystem services and disservices (or dimin-ution of naturally occurring services) from production land-scape to surrounding areas. Services from agriculture includeprovisioning services (food, fuel, fiber, and biochemicals) aswell as carbon sequestration, soil conservation, cultural andesthetic services, and habitat provision (e.g., providing habitatfor endemic organisms). Disservices from agriculture can in-clude degradation or loss of habitat, soil, water quality, andother off-site, negative impacts. Both services and disservicesare typically a result of management practices within agri-cultural fields and landscapes. The remainder of this sectiondescribes some of the key ecosystem services that supportagricultural productivity (summarized in Table 1) and dis-services detract from it (see Swinton et al., 2007 for detaileddiscussion of services and disservices from agriculture).

Services to Agriculture Help to Sustain AgriculturalProductivity

Soil structure and fertility enhancement services include theprocesses of soil formation, structural development (includingphysical, chemical, and biological properties of soil), andnutrient cycling mediated by biotic and abiotic factors tosupport plant growth. These soil characteristics are importantdeterminants of the quantity and quality of farming outputs(Zhang et al., 2007). As soil organisms process dead organicmatter, and their waste replenishes nutrients required for pri-mary production, the fertility needed to support primaryproduction is maintained (Daily et al., 1997).

Soil structure is enhanced through the activities of macro-fauna – such as earthworms, centipedes, millipedes, and iso-pods – that aerate soil by creating pores as they burrowthrough the soil profile, mixing organic and mineral particles,redistributing organic matter and microorganisms, and en-riching soil with castings (Hendrix et al., 1990; Edwards,2004). A host of microfauna also act as biological mediators ofsoil fertility and structure. Their activities support soil fertilityas they break down plant detritus and other organic matter,and incorporate nutrients into their biomass, which mayotherwise move through the system or be lost downstream(Paul and Clark, 1996). Micro- and macrofauna (e.g., acarinaand collembola) influence nutrient cycling by regulatingbacterial and fungal populations, release energy by breakingdown large molecules into smaller units (catabolizing organicmatter), and mineralizing and immobilizing nutrients. Theiractivities influence soil structure by producing organic com-pounds that bind soil aggregates. Bacteria and fungi are alsopart of an important cadre of microflora that mediates nitro-gen fixation from the atmosphere, transforming it into plant-available forms (Hendrix et al., 1990).

Soil processes in agroecosystems are subject to removalof nutrient-rich biomass during harvest, plus elevated de-composition rates that increase with frequency of tillage andirrigation. In some systems, organic matter is also lost whenfields are burned (e.g., to clear biomass for the next planting).

Nutrient losses in agroecosystems contrast with unmanaged,undisturbed ecosystems in which nutrient cycles tend to bemore nearly closed, with inputs approximately matchingoutputs (Daily et al., 1997). Many high-intensity farming sys-tems do not retain soil structure and fertility through bio-logical processes, they are rather maintained through tillageand additions of chemical and organic fertilizers (Daily et al.,1997; Matson et al., 1997).

PollinationAnimal pollinators are essential for approximately 35% ofglobal crop production, and 60–90% of all plant species arepollinator-dependent (Klein et al., 2007). Bees are recognizedas the taxon providing most pollination services, yet othertaxa – including birds, bats, thrips, butterflies and moths, flies,wasps, and beetles – also pollinate some of the world's mostimportant food crops (Nabhan and Buchmann, 1997). Pol-lination is necessary for sexual reproduction in many crops,including fruits, vegetables, nuts, and seeds (Klein et al., 2007)as well as many wild plants known to contribute calories andmicronutrients to human diets (Sundriyal and Sundriyal,2004). There are also many globally important crops that arepollinated passively or by wind, including cereals, sugarcane,and grasses (Klein et al., 2007).

Overall, pollinators play a significant role in the world'sfood systems and agricultural economies. The estimated valueof insect-pollinated crops in the United States ranged from US$18–27 billion in 2003. If calculations include secondaryproducts, such as beef and milk from cattle fed alfalfa, theestimated value more than doubles (Mader et al., 2011). Al-though honey bees (Apis spp.) are the most important com-mercially managed pollinator, native and wild bee speciesalso make significant contributions. Approximately 15% ofthe value associated with pollination services comes fromnative bees and other animals living in farmlands and adjacentnatural habitat (Mader et al., 2011). Both agricultural man-agement and landscape configuration are important in deter-mining availability and distribution of pollination services.Some wild (native) pollinators nest within fields, includingground-nesting bees, or disperse from nearby unmanagedhabitats to pollinate crops (Ricketts et al., 2004). Conservingwild pollinators in unmanaged or restored natural habitatsadjacent to agricultural fields can improve pollination levelsand stability, which can support increases in agricultural yields(Klein et al., 2003).

The potential contributions of native pollinators havereceived a great deal of recent attention due to global declinesin managed honey bee colonies (National Academies, 2006).Declines in honey bee abundance, driven by establishment ofparasitic mites (e.g., Varroa destructor), hive pests, and socialfactors such as aging beekeeper populations, have resulted inpollination shortages in some areas (Klein et al., 2007). Thishas caused increased prices for honey bee rental and createdconcern about pollination shortfalls, such as those seen inCalifornia almonds (National Academies, 2006). These factorshave heightened interest in the role of native pollinators tohelp assure availability and stability of crop pollination ser-vices. Recommendations for managing pollinator-friendlylandscapes include maintaining areas of natural and semi-natural perennial habitat (e.g., grass and woodlands, forests,


old fields, and hedgerows) to provide ample floral and nestingresources available throughout the year (Kremen et al., 2007;Mader et al., 2011).

Pest controlPest damage is a major limiting factor for global food pro-duction. Animal pests destroy 8–15% of global wheat, rice,maize, potato, soybean, and cotton production (Oerke, 2005)and cause more than US$30 billion in damage in the UnitedStates each year (Pimentel et al., 2005). However, despitedramatic increases in pesticide application, damage levels re-mained roughly unchanged during the four decades followingthe escalation of pesticide use after World War II (Pimentelet al., 1992; Oerke, 2005). Pesticides have even precipitatedpest outbreaks. For instance, Southeast Asian rice fields weredevastated by the brown planthopper (Nilaparvata lugens) afterexcessive pesticide application caused the pest to evolve re-sistance while its predators continued to suffer high mortality(Kenmore et al., 1984). In Indonesia, planthopper outbreaksabated once many pesticides were banned (Naylor andEhrlich, 1997). Instead, farmers adopted an integrated pestmanagement approach in which natural pest predators werefostered, and pesticides were used only after damage exceededcritical economic thresholds.

The idea that farmers can harness nature to provide pestcontrol benefits is not new. As early as AD 304, Chinese farmerscreated and maintained citrus ant (Oecophylla smaragdina) nestsin their orchards to control pest outbreaks (Huang and Pei,1987). Centuries later, in 1888, the modern concept of classicbiological control emerged, again in citrus orchards, whenintroduced vedalia beetles (Rodolia cardinalis) caused the nearcomplete collapse of cottony-cushion scale (Icerya purchasi)pests in California (Caltagirone and Doutt, 1989). Since then ithas become widely recognized that adjusting agriculturalpractices to benefit pest predators can provide a valuable pestcontrol strategy with significant benefit to farmers.

Strategies for enhancing pest control services to agriculturemay require understanding predator ecology to ensure thatpest predators have suitable food and habitat resourcesthroughout their life cycles (Landis et al., 2000). Plants thatprovide floral or nectar resources can be used to sustainpredators and parasitoids. Sweet alyssum (Lobularia maritima)has proven especially effective for bolstering syrphid flyabundances in California (Tillman et al., 2012). Predatorpopulations can also be enhanced indirectly through agri-cultural practices that increase nonpest prey, for example, byapplying mulch or intercropping (Riechert and Bishop, 1990;Bugg et al., 1991). Small patches of native vegetation onand around farms can provide these species with food re-sources and overwintering habitat (Landis et al., 2000; Tillmanet al., 2012). Emerging evidence suggests that conservationactivities at a landscape scale can also benefit farmers. Forexample, conserving natural habitat surrounding farms in-creases predators and often enhances pest control services(Thies and Tscharntke, 1999; Bianchi et al., 2006; Chaplin-Kramer et al., 2011b; Karp et al., 2013). These examples rep-resent but a few of many techniques that have emerged forcontrolling crop pests with native predators, many of whichare readily accessible to farmers through government, uni-versity, and agency extension programs.

Hydrologic services – water flow regulation and waterpurificationAgricultural production relies on a host of water-relatedecosystem services, ranging from water supply (quantity), topurification (quality), and flood protection (Brauman et al.,2007). Globally, agroecosystems are a major consumer ofgroundwater and surface water, accounting for approximately70% of freshwater use worldwide (UN Water, 2013). Agri-cultural water use may be as high as 90% of total withdraws infast-growing economies (UN Water, 2013) or arid environ-ments (USDA ERS, 2013). Irrigation is considered a con-sumptive water use, in that water is not directly returned torivers and streams. Much of this water eventually returns to theatmosphere through evaporation and plant transpiration (e.g.,the process of water moving through plant tissues and evap-orating through leaves, stems, and flowers), particularly inthirsty crops, such as alfalfa and cotton.

The majority of prime land for rainfed cultivation is alreadyin use and development of irrigated land has contributedsubstantially to production gains. A prime example is in India,where the growth of irrigated rice and wheat on the semiaridplains of Punjab has substantially boosted food productionover the past several decades (Matson et al., 1997). Globally,approximately 40% of crop production is supported by irri-gated agricultural lands, which account for 20% of all agri-cultural areas (UN Water, 2013). Scientists project thatcontinued increases in agricultural production would requiresustained or increased supply of irrigation water (Matson et al.,1997).

Ecosystems do not create water; however, they can modifythe amount of water moving through the landscape. Thesemodifications result from ecosystem influence on the hydro-logic cycle, including local climate, water use by plants, andmodification of ground surfaces that alter infiltration and flowpatterns (Brauman et al., 2007). The amount of water storedin watersheds, or discharged above and below ground, influ-ences water supply and availability to downstream users. Theunderstanding of how water availability changes with land useand land cover change is elementary (Brauman et al., 2007).Planting of forests and trees – native or introduced – can eitherincrease or decrease evapotranspiration and downstream wateravailability, depending on the context. In one study, analysisof paired catchment experiments found that stream flows werereduced 45% on an average when grasslands were converted toforests (Farley et al., 2005). Other studies from the Amazonbasin illustrate that evapotranspiration from a pasture can beup to 24% less than a nearby forest (Von Randow et al., 2004).Vegetation can also be selected to support management goalsbased on water requirements. For example, Australian studiesdescribe use of plants such as lucerne (Medicago sativa), euca-lyptus trees (Eucalyptus spp.), and saltbush (Atriplex spp.),which are thought to mitigate potential crop damages in areaswhere rising water tables bring saline water into root zonesby lowering water tables through high transpiration rates(Heuperman et al., 2002).

Water purification depends on filtration and absorption ofparticles and contaminants by clay, silt, and sand particles insoil as well as living organisms in soil and water. Agriculturalproduction depends on water quality to maintain productivecapacity, but there are a number of threats and challenges the


continued provision of clean water. Irrigated farmlands in aridand semiarid regions are experiencing degradation due tosalinization and waterlogging (Matson et al., 1997).

Maintaining water quality for agriculture and other uses isincreasingly thought to require maintaining buffers of vege-tation with intact groundcover and root systems throughoutthe watershed. Vegetation, microbes, and stabilized soils canremove pollutants from overland flow and from groundwaterby physically trapping water and sediments, by adhering tocontaminants, by reducing water speed to enhance infiltration,by biochemical transformation of nutrients and contaminants,and by absorbing water and nutrients from the root zone(Naiman and Décamps, 1997). Vegetated riparian buffer zonesin particular perform critical functions to support water quality.

Genetic resources provide a pool of raw material necessaryto support the process of natural selection and produce evo-lutionary adaptations in unmanaged ecosystems. In agroeco-systems, crop and animal breeders draw on genetic diversityusing traditional breeding and biotechnology to artificiallyselect and perpetuate desirable traits (Zhang et al., 2007). Abroad portfolio of genetic resources increases the likelihood ofmaintaining production, particularly as environmental pres-sures such as climate, pests, and disease fluctuate. Productionstability comes through an array of genotypes, each withdifferent characteristics of disease resistance, tolerance forenvironmental extremes, and nutrient use (Esquinas-Alcázar,2005). Different genotypes, or cultivars, are required for plantsin orchard systems and hybrid seed production to set fruit orseed (Free, 1993; Delaplane and Mayer, 2000). The benefits ofgenetic variation at the species level include enhanced biomassproduction, reduced loss to pests and diseases, and more ef-ficient use of available nutrients (Tilman, 1999).

Crop production is supported by genetic resources fromtwo important sources. First are ‘landraces,’ the varieties ofcrops and livestock that have been cultivated and selected byfarmers over many generations practicing traditional agri-culture (Shand, 1997). Second are closely related species thatsurvive in the wild, known as crop ‘wild relatives.’ Areas withhigh concentrations of landraces and wild relatives are con-sidered centers of crop genetic diversity (Shand, 1997). Thesecenters are critical, as many important crops could not main-tain commercial production without periodic infusions ofgenetic resources from wild relatives (de Groot et al., 2002).

The consequences of losing genetic resources in a cropsystem can be severe. The Irish potato famine in the 1830s isone such example. The crop failure can be attributed in part toa very limited number of genetic strains of potatoes in Ireland,which made the crop particularly susceptible to potato blightfungus (Hawtin, 2000). Reintroducing disease-resistant var-ieties from Latin America, where the potato originated, helpedto resolve the problem. Recent reviews of crop geneticresources highlight that increases in human population size,ecological degradation in farmlands, and globalization havecontributed to a dramatic reduction of crop diversity world-wide. Approximately 150 species now comprise the world'smost important food crops and most human diets are dom-inated by no more than 12 plant species (Esquinas-Alcázar,2005). Loss of crop genetic diversity is of great concern be-cause it reduces the pool of genetic material available fornatural selection and artificial selection by farmers and plant

breeders, thereby increasing the vulnerability of crops to sud-den environmental changes (Esquinas-Alcázar, 2005).

Disservices to Agriculture Detract from AgriculturalProductivity

Disservices to agriculture result from the ecological processesor relationships that detract from agricultural productivity.Crop pests, including seed eaters, herbivores, frugivores, andpathogens (e.g., insects, fungi, bacteria, and viruses), can resultin reduced productivity, or total crop loss in worst case scen-arios (Zhang et al., 2007). Weeds and other noncrop plants canreduce agricultural productivity through competition for re-sources. At the field scale, weeds compete with crops for sun-light, water, and soil nutrients and may limit crop growth andproductivity by limiting access to these critical resources(Welbank, 1963). Within fields, plants may exhibit allelopathy(biochemical inhibition of competitors), such as the toxinsexuded by some plant roots that can decrease crop growth(Weston and Duke, 2003).

Resource competition that potentially detracts from agri-cultural yields can also take place at larger scales. Competitionfor pollination from flowering weeds and other noncropplants beyond agricultural fields can reduce crop yields (Free,1993). Water used by other plants, such as trees that reduceaquifer recharge, can reduce water available to support agri-cultural production by diminishing an important source ofirrigation water (Zhang et al., 2007).

Food safety concerns related to pathogen outbreaks areother potential detractors from agricultural productivity. Sincethe 1990s these concerns have gained some prominencein highly productive regions, such as the Salinas Valley ofCalifornia (the ‘salad bowl of America’), which experiencedEscherichia coli contamination of leafy greens. The unfortunateconsequence has been broad-scale removal of riparian habitatto minimize wildlife intrusion into crop fields. Wildlife wasposited to spread harmful bacteria, although whether it con-stitutes a significant food safety risk remains unclear. Never-theless, over a 5-year period following an E. coli O157:H7outbreak in spinach, 13.3% of remaining riparian habitat wasremoved from the Salinas Valley (Gennet et al., 2013). Thishabitat removal may result in degradation or loss of the eco-system services typically provided by riparian areas.

It is important to note that disservices from agriculture canalso affect the productivity and environmental impacts offarming systems through multiple feedbacks. For instance,when habitat for natural enemies is removed, pest outbreakscan result in crop damage or loss, resulting in reduced prod-uctivity and potentially increased use of pesticides, which maybe accompanied by further detrimental effects. Similarly, whenriparian habitat is degraded or removed, the hydrologic ser-vices of water flow regulation and water purification servicescan be diminished or lost (Figure 2).

Managing Ecosystem Services in AgriculturalLandscapes

Different ecosystem services are mediated and delivered atdifferent scales, ranging from individual farm plots to entire


watersheds or regions (Zhang et al., 2007). Accordingly, effortsto maintain or enhance ecosystem services in farming land-scapes may require deliberate management of different areasand scales, including cultivated areas within farms, non-cultivated areas within farms, and broader landscapes (wellbeyond farm boundaries) that comprise both cultivated andnoncultivated areas.

Management of cultivated fields often focuses on eco-system services that have a direct influence on farm product-ivity; farmers have a direct interest in managing services,including pollination, pest control, soil fertility and nutrientcycling, soil retention, water purification, and water flowregulation. On-farm practices that target water conservation,including moisture from rainfall that is stored in the soilprofile, may help to offset water shortages during dry seasonsor droughts (Rost et al., 2009). Mulching or modification offield tillage practices can reduce evaporation of soil water by30–50%. In addition, farmers can harvest rainwater by in-stalling microtopographic features in their fields (e.g., smallbunds or pits) as well as ponds, dykes, or other infrastructure,enabling recovery of up to 50% of water normally lost in thesystem (Rost et al., 2009; Power, 2010).

Management of noncultivated areas of farms may supportboth ecosystem services of benefit both to farmers themselvesand to the broader public. Studies of smallholder farmshave documented the benefits of planting trees in non-cultivated areas, in both temperate and tropical regions,including Nepal (Carter and Gilmour, 1989) and Costa Rica(Casasola et al., 2007). Increasing tree cover is associatedwith enhanced diversity and richness of mobile organisms –such as birds, bats, and butterflies (Harvey et al., 2006) – soilretention (Carter and Gilmour, 1989), and carbon seques-tration (Montagnini and Nair, 2004). In the case of man-agement that supports ecosystem services, which providepublic benefits but does not directly support farm product-ivity (e.g., carbon sequestration needed to support climateregulation), farmers may have less incentive to implementmanagement practices. To stimulate provision of publicbenefits, policies and programs may be needed to offsetthe costs of management investments or create financialincentives for using new management practices (Garbachet al., 2012).

Broader landscape management to support ecosystem ser-vices requires to understand the ways in which ecosystemprocesses take place across multiple parcels of land (includingmovement of biotic and abiotic components, such as organ-isms, water, and nutrients). Pollination illustrates the im-portance of broader landscape management, highlighting thatmobile organisms respond to resources both within and be-yond cultivated fields. Studies in California suggest that pol-lination by native bees was higher in farms near greaterproportions of natural habitat (no significant relationship wasfound between pollination and farm type, insecticide usage,field size, or honeybee abundance) (Kremen et al., 2004).There is some evidence that multiple farmers practicing di-versified farming – using practices focused on maintaining andenhancing biodiversity of flora and fauna within and acrossfields – across a region can result in greater provision of eco-system services than simply the sum of their individual man-agement actions (Gabriel et al., 2010).

Considerations for Managing Ecosystem Services

Managing ecosystem services requires building an in-depthunderstanding of the species, functional groups, and eco-logical processes through which services are provided(Kremen, 2005). Table 2 highlights some of the key organ-isms, guilds, and communities that are the biological medi-ators of ecosystem services and disservices to agriculture. Theirbiological activities affect the provision of ecosystem servicesat the field, farm, landscape, and regional-to-global scales. Forexample, at the field scale, services of soil structure and fertilityenhancement (including the processes of soil formation,development of structure, and nutrient cycling) are providedby microbes, invertebrates, and nitrogen-fixing plants. Thus,field-scale management may focus on practices such as in-corporating nitrogen-fixing plants into crop rotations andplanning the timing and depth of tillage to minimize impactson beneficial invertebrates. At the farm scale, soil-related eco-system services may also be influenced by levels and types ofvegetative cover; thus, farm-scale management may focus onthe total area, type, and timing of harvest (if any) of vege-tation, including both cultivated and noncultivated areas(Table 2).

Measuring Ecosystem Services and Evaluating ServiceProviders

There is a great deal of interest in methods used to measureprovision of ecosystem services. One method is to evaluate thepresence or abundance of organisms believed to provide eco-system services. A second method is to measure the delivery ofthe service themselves (Kremen and Ostfeld, 2005). For in-stance, in order to measure pollination in a California squashfield, the first method would focus on the abundance anddistribution of key pollinators, such as native squash bees(Peponapis pruinosa) and other insects. Alternatively, the secondmethod would evaluate whether a squash crop was sufficientlypollinated. These two methods are complementary and maybe used together to build a comprehensive understandingof ecosystem service delivery. Counting ecosystem serviceproviders can provide insight into the likelihood of an eco-system service being available. In contrast, measuring theoutcomes (e.g., pollination metrics, such as seed set orpollination deficit) can help to verify delivery of a service butdoes not provide much information about the organismsproviding the service. A comprehensive approach to under-standing and measuring ecosystem services includes under-standing key ecosystem service providers (e.g., organisms,guilds, and communities), factors influencing the ability ofproviders to deliver services of interest, and measuring spatialand temporal scales over which providers operate and eco-system services are available (Kremen and Ostfeld, 2005).

The relationships between biodiversity and ecosystemfunction are also important for understanding provision ofecosystem services (Altieri, 1995; Hooper et al., 2005;Tscharntke et al., 2005). In general, species richness – meas-ured as the number of species in a given area – is associatedwith enhanced ecosystem services (Balvanera et al., 2006).Similarly, biodiversity loss is associated with diminished

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

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

Field Farm Landscape Region/globe

Services to agricultureGenetic resources Diversity within a single

crop; genotypes help toprovide pest and diseaseresistance

Diversity across multiplecrops; rotations help toprovide pest and diseaseresistance

Landrace varieties, wildrelatives of crops; can beused to infuse crops withgenetic diversity

Landrace varieties, wildrelatives of crops; can beused to infuse crops withgenetic diversity

Hydrologic services: Waterflow regulation, waterpurification

Vegetation within cultivatedareas

Vegetation around watersources, drains, andponds

Vegetation cover inwatershed; ripariancommunities

Vegetation cover inwatersheds; ripariancommunities

Pest control Predators, parasites(animals and insects,including vertebrates,invertebrates, andparasitoids)

Predators, parasites(animals and insects,including vertebrates,invertebrates, andparasitoids)

Predators, parasites(animals and insectsincluding vertebrates,invertebrates, andparasitoids)

–

Weed control Predators, competitors(herbivores, seedpredators, and othercompetitors that limitplants and fungi)

Predators, competitors(herbivores, seedpredators, and othercompetitors that limitplants and fungi)

Predators, competitors(herbivores, seedpredators, and othercompetitors that limitplants and fungi)

–

Pollination Pollinators: primarily beesbut also bats, thrips,butterflies and moths,flies, wasps, beetles, andbirds (note: some cropsare wind-pollinated)

Pollinators: primarily beesbut also bats, thrips,butterflies, and moths,flies, wasps, beetles, andbirds (note: some cropsare wind-pollinated)

Pollinators: primarily beesbut also bats, thrips,butterflies and moths,flies, wasps, beetles, andbirds (note: some cropsare wind-pollinated)

–

Soil structure and fertility(including processes ofsoil formation,development of structure,nutrient cyclingsupporting fertility)

Microbes, micro and macroinvertebrates, nitrogen-fixing plants

Vegetative cover Vegetative cover –

Erosion protection Cover crops and perennialcrops

Cover crops and perennialcrops

Riparian vegetation;vegetative cover on steepareas, thin soils;floodplains

Riparian vegetation;vegetative cover on steepareas, thin soils;floodplains

Disservices to agriculturePest damage and pathogenoutbreaks

Insects, snails, birds,mammals, fungi,bacteria, viruses, andweeds

Insects, snails, birds,mammals, fungi,bacteria, viruses, andweeds

Insects, snails, birds,mammals, fungi,bacteria, viruses, andrangeland weeds

–

Competition for water Weeds Vegetation near drainageditches

Vegetation in watersheds Vegetation in watersheds

Competition for pollination Flowering weeds Flowering weeds Flowering plants inwatershed

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 efficiencyof resource capture and use in ecological communities, di-minished biomass production, and diminished rates of nu-trient decomposition and recycling (Cardinale et al., 2012).In addition to biodiversity, ecosystem function is influencedby the identity, density, biomass, and interactions of specieswithin a community (Kremen and Ostfeld, 2005). These at-tributes can aggregate at different levels (e.g., field, farm, andlandscape scales). Thus, it is important to consider how eco-logical attributes may vary over space and time, as this caninfluence when and where ecosystem services are available.

Many ecological studies aim to understand which popu-lations, species, functional groups, guilds, food webs, andhabitat types produce key services. One method to do so isa functional inventory, which includes identifying and de-scribing the focal ecosystem service providers in a landscapeand quantifying their contributions (Kremen and Ostfeld,2005). A functional inventory is most relevant at the scaleof the focal ecosystem service. Thus, evaluating disease re-sistance in crops may require a functional inventory atthe genetic level, (Zhu et al., 2000) whereas evaluatingbiological control of pests may require an inventory at the


level of a population or food web (Kruess and Tscharntke,1994).

Functional Differences

A second method to build understanding of ecosystem serviceproviders is evaluating functional attribute diversity (Kremenand Ostfeld, 2005). This method describes differences withinthe guild, functional group, or community that provides eachservice. A commonly used metric is ecological distance, whichdescribes differences in morphology, ecology, or behavior ofthe organisms (Laliberté and Legendre, 2010; Walker et al.,1999) that provide ecosystem services. Characteristics thatdetermine how an organism performs key functions are oftenused for measuring ecological distance, such as root depth ofplants (potential determinant of water flow regulation), tim-ing of emergence and senescence (primary production andnutrient cycling), or pollinator's tongue length (pollination).

Response to Disturbance

Comprehensive evaluation of the abundance of ecosystemservices providers, and broader patterns of ecosystem servicesavailability, can build a solid foundation for investigatingpotential influence of disturbance. For example, what happenswhen species that provide key services are lost? Sometimesecosystem services are resilient to disturbance and loss. If re-maining species can compensate for the species that are re-moved or have become extinct, ecosystem services may also bemaintained rather than diminished. This compensation effectcan happen in several ways.

First, compensation can occur through response diversity,described as the diversity of responses to change shown amongspecies contributing to the same ecosystem functions andservices disturbance (Elmqvist et al., 2003). Second, it canoccur through functional compensation, which occurs whenefficiencies of individual ecosystem service providers shift inresponse to changing community composition. Third, com-pensation may also happen through the portfolio effect. Just ashaving a diverse investment portfolio may buffer an investoragainst fluctuations in individual investments, a diverse bio-logical community is more likely to contain some species thatcan persist through disturbances (Tilman et al., 1998).

Promoting Synergies between Yield and EcosystemServices

Recent global estimates project the need to double world foodproduction by 2050 (World Bank, 2008a; The Royal Society,2009; Godfray et al., 2010). At the same time, there is agrowing consensus that increased food production must notcome at the expense of diminishing key ecosystem services,such as carbon sequestration, water flow regulation, and waterpurification. Additionally, the prospect of clearing additionalland for agriculture is unappealing, as most of the remainingpotentially arable land on the Earth is covered by tropicalrainforest; agricultural expansion in these areas would comeat a steep cost to biodiversity and the delivery of services

from biodiversity-rich rainforests (Ramankutty and Rhemtulla,2012). Therefore, existing farmlands are being called onto simultaneously increase crop yields and provision of eco-system services. This call for multifunctional agriculturallandscapes can be summarized as agroecosystems in whichproductivity and ecological integrity are complementary out-comes, rather than opposing objectives.

Agroecology is a scientific subdiscipline and farming ap-proach intended to do precisely this by applying ecologicalconcepts and principles to the design and managementof sustainable farming systems (Altieri, 1995). Agroecologyemphasizes understanding the ecology of crop, livestock, andother species in a farming system as well as the mechanismsthat govern their functions. It highlights the role of humanmanagers in maintaining and enhancing desirable functionsand related ecosystem services to optimize use of water, en-ergy, nutrients, and genetic resources (Altieri, 1995; Gliessmanet al., 1998). In doing so, the practice of agroecology oftenseeks to intensify production systems – that is, to delivergreater yields per unit of land, water, or other inputs used – ina way that is based on and, in turn, maintains healthy systemsof soil, water, and biodiversity.

There is considerable evidence that systems of agroecolo-gical intensification can increase yields relative to prevailingfarmer practices in many parts of the world (e.g., Pretty et al.,2006). A recent quantitative review investigated whetheragroecological intensification systems tend to deliver yield andecosystem service benefits simultaneously (Garbach et al., inpress). Here the authors summarize results for two illustrativesystems of agroecological intensification: conservation agri-culture and the system of rice intensification.

Conservation agriculture is an agroecological intensifi-cation system that aims to increase productivity and sustain-ability of soil resources through three main practices:(1) minimal soil disturbance, (2) permanent soil cover, and(3) crop rotations (Kassam et al., 2009). Development agen-cies, such as the Food and Agriculture Organization of theUnited Nations, have promoted this system due to its poten-tial applications in farms of diverse sizes and crop systems(FAO, 2011).

Field studies of conservation agriculture report benefits insoil structure, nutrient cycling, erosion protection, and animalbiodiversity relative to conventional soil tillage (Milder et al.,2012). However, inconsistent results have been reported forkey services, such as pest control, which was found to be di-minished in some field studies due to increased pests harboredby crop residues (Van den Putte et al., 2010). Other fieldstudies have reported increased pest control associated withmaintaining soil cover (e.g., mulching and retaining plantresidues on soil surfaces) and increased species richness andpopulation density of beneficial insects, such as predatorycrickets, beetles, bugs, ants, and spiders (Jaipal et al., 2005).

Synergistic outcomes in conservation agriculture –enhanced yield and ecosystem services – were reported inapproximately 40% of comparisons (17 of 43 total quantita-tive comparisons with conventional cultivation, reported in 16studies, Garbach et al., in press) (Figure 3). However, conser-vation agriculture studies have also reported trade-offs, suchas enhanced yield despite diminished weed control services(Haggblade and Tembo, 2003) and diminished yield but

Pest control

>50% ofcomparisons

>25% ofcomparisons

25−50% ofcomparisons

Weed control

Erosion control

Water purification

Water flow regulation

C sequestration

Habitat provision

Soil fertility

Conservation agriculture

Yield

Legend

−

−

−

−

+

+

+

+

Yield

System of rice intensification

Eco

syst

em s

ervi

ces

Eco

syst

em s

ervi

ces

Figure 3 Synergies and trade-offs between ecosystem services and yield in conservation agriculture and system of rice intensification. Bubblelocation 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 nosignificant difference from the comparison system. Bubble size indicates the percent of reviewed comparisons reporting each combination of yieldand AEI outcomes: large bubbles indicate 450% of comparisons; medium bubbles indicate 25–50% of comparisons; and small bubbles indicateo25% of comparisons. The ecosystem services evaluated are represented by colored charts in each bubble and represented as the percentage ofcomparisons in which the ecosystem service was measured. Adapted from Garbach, K., Milder, J.C., DeClerck, F., et al., in press. Closing yieldgaps 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)(7% of comparisons, Figure 3). A small number of studieshave reported both diminished yield and ecosystem service(6% of comparisons, Figure 3). Diminished yield in conser-vation agriculture was often associated with a decrease in weedcontrol (Narain and Kumar, 2005) and pest control services(Van den Putte et al., 2010).

The system of rice intensification has received a great dealof recent attention as an agroecological intensification systemdeveloped specifically for a staple grain. This approach toirrigated rice cultivation includes six key practices: transplant-ing young seedlings; low seedling density with shallow rootplacement; wide plant spacing; intermittent application ofwater (vs. continuous flooding); frequent weeding; and in-corporation of organic matter into the soil, possibly com-plemented by synthetic fertilizer (Africare, Oxfam America,WWF-ICRISAT, 2010).

Field studies report considerable evidence for synergies be-tween yield and ecosystem services in the system of rice in-tensification, particularly water flow regulation. Enhancement

of both yield and ecosystem services were reported in 87% ofcomparisons (39 of 45 quantitative comparisons reported in15 studies, Garbach et al., in press) (Figure 3). Most studiescompared the system of rice intensification to the predominantunintensified farmer practices in the study area. Thus, the re-sults suggest that the system of rice intensification can signifi-cantly improve productivity and ecosystem service deliveryrelative to current practices in many regions. However, therelative benefits of the system of rice intensification comparedwith regionally specific best management practices in con-ventional rice farming are less clear (McDonald et al., 2006).

Landscape Context

From above, agricultural landscapes often resemble a patch-work of rural villages, natural and seminatural habitat, andfarms cultivating a diverse array of crops. ‘Natural habitat’in this context describes the full range of natural, seminatural,and weedy vegetation types that tend to be present in



agricultural areas. However, over the past decades in manyparts of the world, remnants of natural habitat have begundisappearing, replaced by vast fields of industrial agriculture(Perfecto et al., 2009). This physical restructuring of agri-cultural landscapes has resulted in dramatic changes in manycritical ecosystem services.

Ecological processes often occur at scales larger than indi-vidual farms, making the composition of the broader agri-cultural landscape an essential determinant of ecosystemservice provision. Natural habitat can provide many benefits tofarmers and the public (Kremen and Miles, 2012). Benefitsinclude harvestable goods, such as fuelwood, medicinalplants, and bushmeat, as well as genetic resources provided bycrop wild relatives. Natural habitat can provide recreationalopportunities and has been found to support mental healthin some case studies (Bratman et al., 2012).

Ensuring that agricultural systems realize diverse benefitsrequires looking beyond on-farm practices and managing thebroader landscape. Here the authors focus on examples oflandscape management for two animal-mediated ecosystemservices: pollination and pest control. Many other ecosystemservices, including water purification, genetic resources, andsoil structure and fertility enhancement, also require landscapemanagement. Animal-mediated services, however, are amongthe most severely affected by landscape simplification, andlandscape-level effects have been well documented.

When natural habitat is removed for agriculture, beneficialpollinators and predators of insect pests often decline inabundance, whereas pests increase, which may precipitatelower yields for farmers (Philpott et al., 2008; Karp et al., 2011;Melo et al., 2013). The amount of natural habitat required tosustain pest control and pollination services is often a productof the home range sizes of the predator and pollinator speciesthat provide these services, an attribute that can vary con-siderably among species. The relevant management scale forfarmers depends on both the focal ecosystem service and onthe attributes of its animal providers. Fortunately, the pastdecades have seen a surge of research documenting the role oflandscape structure and composition in sustaining pollinatorsand pest control providers.

Pollination

Although managed honey bees (Apis mellifera) provide mostpollination globally, native insects are often more effectivepollinators and provide complementary pollination benefits(Garibaldi et al., 2013). Further, native insects enhance pol-lination resilience, especially as honey bee colonies continueto collapse (Winfree and Kremen, 2009). Retaining a diversepollinator community is thus increasingly recognized as anessential component of any sustainable food system.

Unsurprisingly, native pollinators rely on native habitat.Many species center their foraging activity around the nest,often located in patches of habitat embedded in agriculturallandscapes (Lonsdorf et al., 2009; Jha and Kremen, 2013).Pollinator activity matches pollinator foraging ranges, andpollination is thus consistently higher at the edges of cropfields near native habitat than in the interior of large cropmonocultures (Kremen et al., 2004; Ricketts et al., 2004, 2008;

Klein et al., 2012). As large fields of a single crop variety re-place more diversified farms, the total length of time duringwhich crop species are flowering becomes shorter. As a result,pollinators may become increasingly dependent on the wildplants that flower throughout the year in noncropped areas(Mandelik et al., 2012). Pollination services are thus not onlyhigher but also more stable at field edges than in the interior(Garibaldi et al., 2011).

Although pollination services may vary from crop to crop,pollinator to pollinator, and region to region, the positiveinfluence of natural habitat on pollinator activity has provenremarkably consistent across many studies (Ricketts et al.,2008). This consistency has allowed researchers to createspatial pollination models that estimate pollination provisionon the farm based on the composition of the surroundinglandscape (Lonsdorf et al., 2009). For instance, the InVEST, theecosystem service modeling platform operated by the NaturalCapital Project, allows land managers to predict the pollin-ation consequences of their land-use decisions and manageland assets accordingly.

Pest Control

Not all crops are animal pollinated, but every crop suffers pestdamage. The shift from diversified, agricultural landscapeswith patches of natural habitat to large monocultures that lacknatural habitat has likely brought with it more severe pestoutbreaks. High vegetation diversity ensures that specialistpests do not enjoy vast food resources (Matson et al., 1997).Further, because not all crops and vegetation in natural habitatis palatable to pests, complex landscapes may inhibit pestmovements and cause more localized outbreaks (Avelino et al.,2012). However, natural habitat can sometimes provide pestswith resources vital for completing their lifecycles and thusfacilitate outbreaks (Chaplin-Kramer et al., 2011b). For ex-ample, because aphids sequester chemicals in wild mustards(Brassica nigra) as antipredator defenses, the proximity ofnatural habitat with high mustard density may function toincrease the density of aphids in nearby crop fields (Chaplin-Kramer et al., 2011a).

Another critical consideration, however, is the predatorsof crop pests. Predators rely on natural habitat for essentialactivities, including breeding, roosting, foraging, and hiber-nating (Landis et al., 2000; Jirinec et al., 2011). Predatorabundance and diversity thus regularly decline as agriculturallandscapes shift from complex mosaics of natural habitat andcropland to simplified monocultures (Bianchi et al., 2006;Chaplin-Kramer et al., 2011b). Although diverse predatorcommunities are not always more effective at providing pestcontrol because predators sometimes consume each other(Vance-Chalcraft et al., 2007), most studies report that morepredator diversity translates to more effective pest control(Bianchi et al., 2006; Letourneau et al., 2009; Chaplin-Krameret al., 2011b).

An increasing number of studies have documented in-creased pest consumption in complex versus simple landscapes(Thies and Tscharntke, 1999; Gardiner et al., 2009; Chaplin-Kramer and Kremen, 2013; Karp et al., 2013). Fewer studies,however, have traced the benefit of maintaining natural habitat


all the way to crop yields and profits, but some have reportedpositive effects (Thies and Tscharntke, 1999; Karp et al.,2013). Like pollination, the relevant scale for pest manage-ment can vary from predator to predator and from pest topest, such that distant areas may determine the abundanceof highly mobile animals (Werling and Gratton, 2010). Sim-ply focusing on local agricultural practices may be ineffective.Because predator communities often collapse after harvest,a stream of colonizers from adjacent natural habitat maybe required to replenish the predator community in thefollowing year.

Landscape Effects on Agriculture: A Costa Rican Case Study

Tropical rainforest provides an array of ecosystem services,including water purification, water flow regulation (e.g., sup-porting hydropower production), carbon sequestration, andcultural services such as ecotourism. Recognizing this, in themid-1990s the Costa Rican government created the first na-tional payment for ecosystem services (PES) scheme, in whichlandowners were paid to maintain rainforest on their privatelands (Sánchez-Azofeifa et al., 2007). For farmers, the programprovided the dual benefit of monetary compensation for un-cultivated lands and continued provision of critical ecosystemservices.

The canton of Coto Brus in Southern Costa Rica has beenstudied as a model system for how strategic conservation ef-forts influence agricultural production. Unlike many otherparts of the country that now host vast expanses of pineapple,oil palm, or banana, Coto Brus still exists as a patchwork ofcoffee plantations, pasture, small rural villages, and tropicalwet forest, perhaps a result of its hilly terrain (Mendenhallet al., 2011). This complex configuration supports a remark-able concentration of biodiversity, often at par with nativeforest (Daily et al., 2001; Mendenhall et al., 2013). Coffee, themost extensively cultivated crop in the region, benefits fromthis biodiversity. Although coffee can self-pollinate, animalpollination increases yields, sometimes by more than 50%(Ricketts et al., 2004). Because wild bees rely on rainforest

1.5km

Figure 4 Pest control value of forest patches to coffee plantations in Southconsume the coffee berry borer beetle (Hypothenemus hampei), coffee's mokilograms of coffee berries saved from infestation by each patch of forest acforest patches embedded within or adjacent to coffee plantations provided th

habitat, coffee plants located near rainforest enjoy significantlyhigher pollination than sites in the middle of extensive plan-tations. Higher pollination translates to higher yields, bettercoffee quality, and increased profits. One study found thatyields increased by 20% and misshaped ‘peaberries’ decreasedby 27% within 1 km distance of two forest patches (Rickettset al., 2004). These benefits translated into a significant eco-nomic gain, approximately US$60 000 per year for a singlecoffee plantation.

Costa Rican coffee plantations also enjoy pest controlbenefits 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 in2005 (Staver et al., 2001). Not more than 5 years later, nativebirds had already expanded their diets to include the pest andbegan reducing infestation severity by half (Karp et al., 2013).Like wild bees, many of the pest-eating birds rely on foresthabitat, and pest control provision is higher on farms withmore forest cover (Karp et al., 2013). Small, unprotected forestpatches embedded in coffee plantations provided the mostbenefits. Forest patches smaller than 1 ha area secured ap-proximately 50% of the total pest control benefits across theCoto Brus valley (Figure 4).

Policies and Programs to Conserve and EnhanceEcosystem Services in Agricultural Landscapes

Growing interest in the management of ecosystem services hasbeen matched, in recent years, by a proliferation of policyand programmatic strategies to promote the conservation orenhancement of these services in agricultural landscapes.Traditionally, environmental management policies were oftendescribed in terms of a dichotomy between regulatory instru-ments (‘command and control’ requirements put forth bygovernments) and market-based instruments focused onshifting incentives and price signals for farmers, businesses,and other market actors. However, this dichotomy is nowunderstood to be too simplistic: not only have the boundaries

2370 kg Berries saved0 kg Berries saved

Coffee

N

km0.25

Pasture

ern Costa Rica forest provides habitat for the insectivorous birds thatst economically damaging insect pest. Maps show the estimatedross the Coto Brus Valley. Integrated together, the small, unprotectede majority of pest control value to coffee farmers.



between regulatory and market-based approaches blurred inmany cases, but the range of market-based approaches has alsoproliferated to the point where further categorization is ne-cessary (Lemos and Agrawal, 2006). This situation reflects abroader shift from the primacy of state institutions in en-vironmental governance to the inclusion – and sometimesdominance – of other groups, including corporations, con-sumers, civil society organizations, and multinational organ-izations (Liverman, 2004).

Before describing the range of policy and programmaticstrategies used to conserve and manage ecosystem servicesfrom agricultural landscapes, it is worth noting some chal-lenges endemic to the governance of agricultural systems,which have limited the effectiveness of most if not all thesestrategies to varying degrees. First, in contrast to other eco-system types that are major providers of ecosystem services(e.g., forests, wetlands, and water bodies), agricultural landsare predominately owned or managed by private individualsand companies, or in some instances collectively by ruralcommunities. This means that government authorities gener-ally cannot influence the use of these lands simply by ad-justing management plans and policies for lands and waterover which they have substantial control, as they might for astate-owned protected area or water body. Second, the his-torically private nature of agricultural enterprises means thatthere is little tradition of public sector regulation of agri-cultural activities, at least with regard to major agronomicdecisions affecting ecosystem services, such as rural land use,tillage, planting, and soil fertility management.

Third, agricultural management systems are highly context-dependent (based on climate, soils, hydrology, and otherfactors), making it inappropriate to devise ‘one size fits all’regulations and frequently inefficient to incentivize specificmanagement practices, which may not be appropriate in allcontexts. Fourth, most of the major ecosystem services anddisservices from agriculture are ‘nonpoint’ in nature, meaningthat they flow from the land itself, in heterogeneous patterns,and are, therefore, difficult to quantify, monitor, or regulate(Ribaudo et al., 2010). In contrast, point source impacts, suchas water withdrawals and factory emissions from a smokestackor effluent pipe, are much easier to monitor and regulateand have been the subject of many effective environmentalregulations. Fifth, monitoring and enforcement in agriculturalsettings is always a challenge, given the dispersed, private na-ture of agricultural activities and the nonpoint nature of keyecosystem service outcomes. This is particularly so on theworld's approximately 350 million small farms, where thetransaction and administrative costs of policies and programscan become proportionately quite high.

Table 3 provides a basic typology of policies, programs,and instruments that may be used to conserve and enhanceecosystem services from agricultural landscapes. Each of theseis described further below.

Government Regulation

Agriculture in most countries is a relatively lightly regulatedenterprise when compared with other land uses, such asindustrial facilities, mines, urban development, and even

forestry. Land-use regulations restrict or prohibit agriculture incertain locales (e.g., protected areas, watershed conservationareas, and multiuse management zones) and in some instancesaim to reduce the degree to which agriculture conflicts with theprovision of important ecosystem services. On a broader scale,both Brazil and Indonesia have enacted temporary moratoriaon deforestation for agricultural expansion, which have beencredited with reducing the loss of ecosystem services associatedwith soybean and oil palm expansion, respectively (Macedoet al., 2012). A limited number of regulation require on-farmprotection of remaining natural ecosystems (e.g., remnantforest patches), or riparian buffers, recognizing their capacity toprovide ecosystem services both within and beyond cultivatedareas. Nonetheless, these regulations are quite limited overall,and, in many places where they exist, have been poorly en-forced and widely ignored. A notable example is Brazil's ForestCode, which on paper requires farmers to establish mosaics ofnatural habitat within agricultural landscapes but in practicehas been generally flaunted.

Regulation of certain farm inputs – particularly pesticides –is robust in many countries and may help to mitigate certainnegative impacts of agriculture, including the negative off-siteimpacts on water quality. However, even where the most toxicpesticides are effectively regulated, use of other legal, but stilltoxic, pesticides may contribute to large aggregate impacts thatdiminish both water quality and habitat provision (Schiesariet al., 2013). In particular, pesticide contamination can nega-tively affect the ecological communities in waterways, resultingin degradation or loss of the important services these com-munities provide (e.g., pest control services provided bymosquito fish in small channels near populated areas; fishingand other cultural services supported by rivers and streams).

Agriculture (and the ecosystem services it provides) mayalso be governed by broader regulations that apply acrossmany sectors. However, these laws are not always applied fullyin the context of farms and ranches. For instance, in the UnitedStates, agricultural operations enjoy a variety of statutory or defacto exemptions from otherwise strong environmental lawsincluding the federal Clean Water Act, federal EndangeredSpecies Act, and certain state endangered species acts. Theseexemptions highlight both the privileged political status thatthe agriculture sector enjoys in many countries and the dif-ficulty in enforcing these types of laws in an agricultural con-text. They also underscore the need for interventions focusedon ecosystem services that support rather than compromiseproduction functions.

Market-Based Instruments

In the context of policy options, the term ‘market-based’ isused broadly to refer to strategies that seek to influence be-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 canoccur when the providers of ecosystem services do not reap thefull benefit of delivering these services, or when they avoidbearing the full cost when they diminish these services. Forinstance, farmers usually receive little or no monetary benefitfrom protecting wildlife habitat, although this is an important

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

Type of policy, program, orinstrument

Level of state involvement Role of farmers Examples

Government regulation (‘command and control’)Land use regulations High (set and enforce

regulations)Subject of regulations Land-use zoning; temporary

moratoria; riparian buffer zonerequirements

Regulation of agriculturalinputs

Bans and restrictions on use ofcertain pesticides; prohibition onplanting genetically modifiedorganisms

Regulation of otheragricultural practices

Good agricultural practicesregulations focused on food safety

Other regulations affectingagricultural lands

Regulations on water, wetlands, andendangered species

Market-based instruments (influencing price signals or incentive structures)Taxes and subsidies High (establish tax and

subsidy policies)Payer of taxes or recipient ofsubsidies

Earning tax credits for bestmanagement practices (e.g.,Resource Enhancement andProtection Program in PA, USA)subsidies for no-till planters

Markets formed throughregulation (e.g., cap-and-trade), leading to PES

Moderate to high (setregulations and overseemarket)

Buyers or sellers of ecosystemservices, where required oreligible to participate

Water quality trading, regulatedcarbon markets

Public sector PES High (deploy funds andadminister PESprogram)

Sellers of ecosystem services Agri-environment payments (Europe),Farm Bill environmental programs(USA)

Private and voluntary PES None or low Buyers or sellers of ecosystemservices

Various watershed, biodiversity, andcarbon PES involving farmers

Eco-standards andcertification

None to moderate Sellers of agricultural goodsproduced in accordance witheco-standards

IFC Performance Standards,Rainforest Alliance, andRoundtable on Sustainable Palm Oil

Rural development and farmer assistance programsTechnical assistance andcost-share programs

None to high (someprograms are funded orrun by the public sector,others by private or civilsociety entities)

Program participants andbeneficiaries

Farm Bill programs for conservationmeasures on US farms

Education and trainingprograms

Conservation Farming Unit (Zambia)

Rural development projectsand programs

Sustainable Land Managementinvestments (Global EnvironmentalFacility/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 paymentfor ecosystem services.


public benefit. Conversely, when fertilizer runoff from farmscontributes to downstream eutrophication and its attendantenvironmental and economic harms, the farmers responsiblefor these harms usually bear no economic consequences.Market-based instruments can address such environmental‘externalities,’ which would otherwise result in suboptimaldelivery of or investment in the provision of ecosystemservices.

The most long-standing types of market-based instrumentsare various forms of taxes and subsidies, which are deployedacross many different economic sectors, including agriculture.Historically, agricultural subsidies (e.g., for fertilizer inputs)played a significant role in promoting both the expansion andintensification of agriculture to the significant detriment of eco-system services. However, taxes and subsidies can also promoteconservation-friendly agriculture that may deliver increased levels

of ecosystem services. For instance, in Kazakhstan, the govern-ment in 2008 began subsidizing farmers to adopt conservationagriculture technologies – including continuous soil cover, directseeding, and no-till management – that are credited with helpingto increase farmer yields and profitability while reducing soilerosion.

PES are abroad set of market-based instruments that haveproliferated since the mid-1990s to channel new investment inecosystem services. Formally, PES has been defined as volun-tary transactions between ecosystem service seller(s) (such asfarmers or other land managers) and ecosystem service buyer(s) (such as water users or conservation organizations) thatprovide cash or other payment in exchange for the provisionof specific defined ecosystem services (Engel et al., 2008). Inpractice, however, many PES schemes do not conform to thisdefinition, for instance, because they do not target specific


ecosystem services or make payments contingent on actualdelivery of these services (Muradian et al., 2010). For instance,many publicly administered PES schemes – including those inCosta Rica, Mexico, Europe, and the United States – functionmore like environmentally focused farmer subsidy programsthan true conditional payments targeted to deliver the largestquantity of ecosystem services for the least cost.

Ecosystem service payments that involve the creation ofopen markets (as opposed to government payments) are likelyto more closely resemble market-based instruments in theclassic sense of the term. In the United States and othercountries, such markets have been established through regu-lations that cap total levels of pollution or degradation to agiven ecosystem or ecosystem type but enable landowners totrade the limited allocated rights to pollute or degrade. Such‘cap-and-trade’ mechanisms are intended to reduce the overallcost of achieving specific environmental goals and have re-sulted in robust markets for wetland mitigation, wildlifehabitat, and agricultural runoff, among other ecosystem ser-vices and disservices. Truly voluntary private markets for eco-system services involving farmers as ecosystem service sellershave also developed in places, although on a smaller scale.These markets have formed around carbon sequestration,watershed conservation, and biodiversity protection, withbuyers ranging from private companies (e.g., water bottlingbusinesses), to individuals and corporations wishing to offsettheir carbon emissions, to conservation organizations.

On a global scale, PES makes only a modest contributionto incentivizing increased ecosystem service delivery fromagricultural landscapes. However, this contribution is pro-portionately much larger in the United States, Europe, andChina, where large government PES programs – totaling per-haps US$20 billion per year – exist to support watershedprotection, biodiversity conservation, and esthetic protection(‘landscape beauty’) services (Milder et al., 2010). The futuresize of ecosystem service markets affecting farmers remainsuncertain: although it is clear that farmers deliver criticalecosystem services to a wide range of stakeholders, it is notclear whether these beneficiaries will actually be willing to payfor such services on a large scale, or whether markets will beformed that support the cost-effective procurement and man-agement of these services. The future regulation of greenhousegas emissions (or lack thereof) at national or global level is acritical factor, as farmers stand to participate heavily in carbonmarkets if they coalesce at full scale.

Experience from a wide range of contexts suggests that PESin agricultural landscapes is likely to be most effective andscalable where management practices that sustain or increaseecosystem service delivery also support agricultural product-ivity or profitability. In these situations, PES can providefarmers with supplemental revenue that helps them to over-come initial investment barriers or other constraints toadopting more conservation-friendly management practices(FAO, 2007; Majanen et al., 2011). However, where there is ahigh opportunity cost to manage agricultural landscapes forincreased levels of ecosystem services, PES schemes are un-likely to be able to compete with the profitability of en-vironmentally destructive farming and will find few willingsellers of ecosystem services. A prime example is at the agri-cultural frontiers of major commodity crops, such as palm oil

(Southeast Asia), where levels of carbon payments supportedby ecosystem service markets may provide insufficient in-centive to prevent deforestation and the significant loss ofecosystem services (Fisher et al., 2011).

A final market-based instrument is the adoption and useof voluntary sustainability standards – often called ‘eco-standards’ – and associated ‘eco-certification’ labels for agri-cultural products and investments. Agricultural sustainabilitystandards are sets of social and environmental criteria put forthto define and encourage sustainable farming by providingmarket recognition for sustainable producers. These includestandards developed and managed by nonprofit organizations(e.g., Fairtade, Rainforest Alliance, and UTZ Certified), multi-stakeholder ‘roundtables’ for various commodities (e.g., forsoybeans, palm oil, sugar, beef, and cotton), individual foodcompanies (e.g., Unilever, Nestlé, Mars, and others), and thefinance sector (e.g., IFC Performance Standards and the EquatorPrinciples). By participating in such schemes, farmers, traders,and food companies that produce and sell certified productsmay benefit from improved market access or market share, pricepremiums, or improved legitimacy and reputation in the eyes ofconsumers and regulators. Most, if not all, agricultural sus-tainability standards include provisions intended to help con-serve biodiversity, including sensitive habitat that supportsorganisms of conservation concern, and ecosystem services(e.g., water purification and water flow regulation and soilfertility and erosion control) (UNEP-WCMC, 2011). Thus, eco-certification may provide monetary incentives for farmers tomaintain or enhance ecosystem services, although such in-centives are not necessarily explicit or direct with respect tospecific ecosystem services.

Rural Development and Farmer Assistance Programs

Governments, international donors, civil society organiza-tions, and others have been involved for decades in supportingagricultural development around the world. In the past 10–15years, an increasing proportion of these efforts have begunto orient program objectives and activities toward maintainingor increasing flows of ecosystem services in concert with in-creased yields and farmer profitability. Some initiatives, par-ticularly in developed countries, provide technical assistance,farmer training, or cost sharing of on-farm investments to re-duce the negative environmental impacts of agriculture. Forinstance, a variety of programs funded under the US Farm Billprovide technical assistance and cost sharing for practices suchas improved water management structures, erosion controlpractices, integrated pest management, and transitioning toorganic practices.

In the developing world, agricultural development effortst

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