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Ecosystem services and agriculture: tradeoffs and synergies

Ecosystem services and agriculture: tradeoffs and synergies Phil. Trans. R. Soc. B (2010) 365, 2959–2971 doi:10.1098/rstb.2010.0143 Review Ecosystem services and agriculture: tradeoffs and synergies Alison G. Power* Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY, USA Agricultural ecosystems provide humans with food, forage, bioenergy and pharmaceuticals and are essential to human wellbeing. These systems rely on ecosystem services provided by natural ecosys- tems, including pollination, biological pest control, maintenance of soil structure and fertility, nutrient cycling and hydrological services. Preliminary assessments indicate that the value of these ecosystem services to agriculture is enormous and often underappreciated. Agroecosystems also produce a variety of ecosystem services, such as regulation of soil and water quality, carbon sequestration, support for biodiversity and cultural services. Depending on management practices, agriculture can also be the source of numerous disservices, including loss of wildlife habitat, nutri- ent runoff, sedimentation of waterways, greenhouse gas emissions, and pesticide poisoning of humans and non-target species. The tradeoffs that may occur between provisioning services and other ecosystem services and disservices should be evaluated in terms of spatial scale, temporal scale and reversibility. As more effective methods for valuing ecosystem services become available, the potential for ‘win – win’ scenarios increases. Under all scenarios, appropriate agricultural man- agement practices are critical to realizing the benefits of ecosystem services and reducing disservices from agricultural activities. Keywords: ecosystem services; agroecosystems; pollination; biological control; valuation of ecosystem services; soil carbon sequestration 1. INTRODUCTION recently their contributions to other types of ecosystem Agriculture is a dominant form of land management services have been recognized (MEA 2005). Influ- globally, and agricultural ecosystems cover nearly 40 enced by human management, ecosystem processes per cent of the terrestrial surface of the Earth (FAO within agricultural systems can provide services 2009). Agroecosystems are both providers and consu- that support the provisioning services, including mers of ecosystem services (figure 1). Humans value pollination, pest control, genetic diversity for future these systems chiefly for their provisioning services, agricultural use, soil retention, regulation of soil and these highly managed ecosystems are designed to fertility and nutrient cycling. Whether any particular provide food, forage, fibre, bioenergy and pharmaceu- agricultural system provides such services in support ticals. In turn, agroecosystems depend strongly on a of provisioning depends on management, and manage- suite of ecosystem services provided by natural, unma- ment is influenced by the balance between short-term naged ecosystems. Supporting services include genetic and long-term benefits. biodiversity for use in breeding crops and livestock, Management practices also influence the potential soil formation and structure, soil fertility, nutrient for ‘disservices’ from agriculture, including loss of cycling and the provision of water. Regulating services habitat for conserving biodiversity, nutrient runoff, may be provided to agriculture by pollinators and sedimentation of waterways, and pesticide poisoning natural enemies that move into agroecosystems from of humans and non-target species (Zhang et al. natural vegetation. Natural ecosystems may also 2007). Since agricultural practices can harm bio- purify water and regulate its flow into agricultural sys- diversity through multiple pathways, agriculture is tems, providing sufficient quantities at the appropriate often considered anathema to conservation. However, time for plant growth. appropriate management can ameliorate many of Traditionally, agroecosystems have been considered the negative impacts of agriculture, while largely primarily as sources of provisioning services, but more maintaining provisioning services. Agroecosystems can provide a range of other regu- lating and cultural services to human communities, *agp4@cornell.edu in addition to provisioning services and services in support of provisioning. Regulating services from agri- While the Government Office for Science commissioned this review, culture may include flood control, water quality the views are those of the author(s), are independent of Government, and do not constitute Government policy. control, carbon storage and climate regulation through greenhouse gas emissions, disease regulation, and One contribution of 23 to a Theme Issue ‘Food security: feeding the waste treatment (e.g. nutrients, pesticides). Cultural world in 2050’. 2959 This journal is q 2010 The Royal Society 2960 A. G. Power Review. Ecosystem services farm management landscape management tillage agricultural ecosystem windbreaks crop diversity services hedgerows field size riparian vegetation crop rotation natural habitat patches cover cropping ecosystem services pest control pollination nutrient re/cycling agroecosystem landscape matrix soil conservation, structure and fertility water provision, quality and quantity ecosystem disservices carbon sequestration loss of biodiversity biodiversity provisioning loss of wildlife habitat nutrient runoff services sedimentation of waterways food pesticide poisoning fibre bioenergy greenhouse gas emissions Figure 1. Impacts of farm management and landscape management on the flow of ecosystem services and disservices to and from agroecosystems. services may include scenic beauty, education, recrea- agriculture can have strong impacts on the system’s tion and tourism, as well as traditional use. ability to produce important ecosystem services, but Agricultural places or products are often used in tra- many agricultural systems can also be important ditional rituals and customs that bond human sources of services. Indeed, agricultural land use can communities. Conservation of biodiversity may also be considered an intermediate stage in a human- be considered a cultural ecosystem service influenced impact continuum between wilderness and urban by agriculture, since most cultures recognize appreci- ecosystems (Swinton et al. 2007). Just as conversion ation of nature as an explicit human value. In return, from natural ecosystems to agriculture can reduce biodiversity can contribute a variety of supporting ser- the flow of certain ecosystem services, the intensifica- vices to agroecosystems and surrounding ecosystems tion of agriculture (Matson et al. 1997) or the (Daily 1997). conversion of agroecosystems to urban or suburban Around the world, agricultural ecosystems show tre- development can further degrade the provision of mendous variation in structure and function, because beneficial services. they were designed by diverse cultures under diverse socioeconomic conditions in diverse climatic regions. Functioning agroecosystems include, among others, 2. APPROACHES TO ANALYSING annual crop monocultures, temperate perennial orch- ECOSYSTEM SERVICES ards, grazing systems, arid-land pastoral systems, The value of ecosystem services has been estimated tropical shifting cultivation systems, smallholder in various ways. In general, the framework has three mixed cropping systems, paddy rice systems, tropical main parts: (i) measuring the provision of ecosystem plantations (e.g. oil palm, coffee, cacao), agroforestry services; (ii) determining the monetary value of systems and species-rich home gardens. This variety ecosystem services; (iii) designing policy tools for of agricultural systems results in a highly variable managing ecosystem services (Polasky 2008). Ecolo- assortment and quantity of ecosystem services. Just gists and other natural scientists have been engaged as the provisioning services and products that derive in enhancing our understanding of how ecosystem ser- from these agroecosystems vary, the support services, vices are produced for over a decade (e.g. Costanza regulating services and cultural services also differ, et al. 1997; Daily 1997; MEA 2005). Basic knowledge resulting in extreme variation in the value these about ecosystem structure and function is increasing at services provide, inside and outside the agroecosystem. a rapid pace, but we know less about how these factors In maximizing the value of provisioning services, determine the provision of a complete range of ecosys- agricultural activities are likely to modify or diminish tem services from an individual ecosystem (NRC the ecological services provided by unmanaged terres- 2005). In practice, most studies focus on estimating trial ecosystems, but appropriate management of key the provision of one or two well understood ecosystem processes may improve the ability of agroecosystems services. Better understanding of the processes that to provide a broad range of ecosystem services. influence ecosystem services could allow us to predict Globally, most landscapes have been modified by the outputs of a range of ecosystem services, given par- agricultural activities and most natural, unmanaged ticular ecosystem characteristics and perturbations to ecosystems sit in a matrix of agricultural land uses. those ecosystems. That is, an ‘ecological production The conversion of undisturbed natural ecosystems to function’ might be generated (Polasky 2008). Despite Phil. Trans. R. Soc. B (2010) Review. Ecosystem services A. G. Power 2961 recent advances, this is an area of research that still effects of intensive agriculture by providing financial needs considerable attention. incentives to farmers to adopt environmentally sound The second step of valuation of ecosystem services agricultural practices. The impacts of these projects typically includes both market and non-market valua- are variable, however, and their success is debated tion. Valuing the provisioning services that derive (e.g. Baulcombe et al. 2009). A recent evaluation of from agriculture is relatively straightforward, since over 200 paired fields in five European countries indi- agricultural commodities are traded in local, regional cated that agri-environment programmes had marginal or global markets. Some ecosystem services provide to moderate positive impacts on biodiversity, but lar- an essential input to agricultural production, and gely failed to benefit rare or endangered species their value can be measured by estimating the (Kleijn et al. 2006). change in the quantity or quality of agricultural pro- The Economics of Ecosystems and Biodiversity duction when the services are removed or degraded. (TEEB) led by the United Nations Environment Pro- This approach has been used to estimate the value of gramme (UNEP), is an international effort designed pollination services and biological control services to integrate science, economics and policy around bio- (e.g. Losey & Vaughan 2006; Gallai et al. 2009). diversity and ecosystem services. A recent report for Values for such services can also be estimated by policy-makers highlights the link between poverty measuring replacement costs, such as pesticides repla- and the loss of ecosystems and biodiversity, with the cing natural pest control and hand-pollination or intent of facilitating the development of effective beehive rental replacing pollination. policy in this area (ten Brink 2009). Another approach Non-market valuation methods have been used for is the establishment of markets for pollution credits, many years to measure both the use value and the including the growing global carbon market operating non-use value of various environmental amenities under various cap and trade initiatives, such as the (Mendelsohn & Olmstead 2009). Non-market valua- European Union Emission Trading System. tion can be based on revealed preference (behaviour expressed through consumer choices) or stated prefer- 3. ECOSYSTEM SERVICES FLOWING ence (e.g. attitudes expressed through surveys). In TO AGRICULTURE contingent valuation surveys, for example, consumers The production of agricultural goods is highly depen- are asked what they would be willing to pay for the dent on the services provided by neighbouring natural ecosystem service. Another approach is to ask produ- ecosystems, but only recently have there been attempts cers—in this case farmers—what they would be to estimate the value of many of those services to agri- willing to accept to supply the ecosystem service cultural enterprises. Some services are more easily (Swinton et al. 2007). quantified than others, to the extent that they are The overarching goal of measuring and valuing eco- essential to crop production or they substitute directly system services is to use that information to shape for purchased inputs. policies and incentives for better management of eco- systems and natural resources. One of the inherent difficulties of managing ecosystem services is that the (a) Biological pest control individuals who control the supply of such services, Biological control of pest insects in agroecosystems is such as farmers and other land managers, are not an important ecosystem service that is often always the beneficiaries of these services. Many ecosys- supported by natural ecosystems. Non-crop habitats tem services are public goods. While farmers do provide the habitat and diverse food resources benefit from a variety of ecosystem services, their required for arthropod predators and parasitoids, activities may strongly influence the delivery of services insectivorous birds and bats, and microbial pathogens to other individuals who do not control the production that act as natural enemies to agricultural pests and of these services. Examples include the impact of farm- provide biological control services in agroecosystems ing practices on downstream water supply and purity (Tscharntke et al. 2005). These biological control and regional pest management. The challenge is to services can reduce populations of pest insects use emerging information about ecological production and weeds in agriculture, thereby reducing the need functions and valuation to develop policies and incen- for pesticides. tives that are easily implemented and adaptable to Because the ecosystem services provided by natural changing ecological and market conditions. enemies can substitute directly for insecticides and One approach to incentives is to provide payments crop losses to pests can often be measured, the econ- for environmental services, through government pro- omic value of these services is more easily estimated grammes or private sector initiatives (Swinton 2008). than many other services. For example, an analysis of Historically, the US has provided support for soil con- the value of natural enemy suppression of soya bean servation investments and other readily observable aphid in soya bean indicated that this ecosystem ser- practices to maintain or enhance certain ecosystem vice was worth a minimum of US$239 million in services. In the US, the Conservation Security Pro- four US states in 2007 – 2008 alone (Landis et al. gram of the 2002 farm bill established payments for 2008). Since this is an estimate of the value of suppres- environmental services, and many European countries sing a single pest in one crop, the total value of have also provided governmental support for environ- biological control services is clearly much larger. Natu- mentally sound farming practices that support ral pest control services have been estimated to save ecosystem services. Agri-environment schemes are $13.6 billion per year in agricultural crops in the US intended to moderate the negative environmental (Losey & Vaughan 2006). This estimate is based on Phil. Trans. R. Soc. B (2010) 2962 A. G. Power Review. Ecosystem services Table 1. Rate of vulnerability to pollinator loss and effect of pollinator loss on global food production for pollinator- dependent crop categories based on 2005 data. IPEV, insect pollination economic value; EV, total production economic value. Adapted from Gallai et al. (2009). relative production surplus (% of consumption) crop category rate of vulnerability (IPEV/EV) % before pollinator loss after pollinator loss stimulant crops 39.0 18 224 nuts 31.0 29 16 fruits 23.1 12 212 edible oil crops 16.3 75 40 vegetables 12.2 19 26 pulse 4.3 60 54 spices 2.7 11 8 The difference between 2005 production and consumption expressed in relative terms as % of 2005 consumption figures following FAO (http://faostat.fao.org). the value of crop losses to insect damage as well as the are also fairly crude and intended to provide a broad- value of expenditures on insecticides. Studies suggest brush assessment of potential economic benefits. that insect predators and parasitoids account for Moreover, most estimates do not take into account approximately 33 per cent of natural pest control potential changes in the value of each commodity as (Hawkins et al. 1999), therefore the value of pest demand increases owing to reduced crop production. control services attributed to insect natural enemies A recent assessment of agricultural vulnerability to has been estimated at $4.5 billion per year (Losey & loss of pollination services based on the ratio of the Vaughan 2006). economic value of insect pollination to the economic value of the crop indicated an overall vulnerability of 9.5 per cent, but vulnerability varied significantly (b) Pollination among types of commodities as well as by geographical Pollination is another important ecosystem service to region (Gallai et al. 2009). Stimulant crops (coffee, agriculture that is provided by natural habitats in agri- cacao, and tea), nuts, fruits and edible oil crops were cultural landscapes. Approximately 65 per cent of predicted to be particularly vulnerable to the loss of plant species require pollination by animals, and an pollination services (table 1). The economic impact analysis of data from 200 countries indicated that of insect pollination on world food production in 75 per cent of crop species of global significance for 2005 in the 162 FAO member countries has been cal- food production rely on animal pollination, primarily culated at 153 billion euro, but vulnerability to loss of by insects (Klein et al. 2007). Of the most important pollinators varies among geographical regions due, in animal-pollinated crops, over 40 per cent depend on part, to crop specialization (Gallai et al. 2009). For wild pollinators, often in addition to domesticated example, West African countries produce 56 per cent honeybees. Only 35 – 40% of the total volume of of the world’s stimulant crops with a vulnerability to food crop production comes from animal-pollinated pollinator loss of 90 per cent. The loss of pollination crops, however, since cereal crops typically do not services in these crops could have devastating effects depend on animal pollination. Aizen et al. (2009) on the economies of such countries in the short term used data from the United Nations Food and Agricul- and lead to significant restructuring of global prices ture Organization (FAO) on the production of 87 in the longer term (Gallai et al. 2009). globally important crops during 1961 – 2006 to esti- A crucial question is whether the loss of pollination mate that the consequences of a complete loss of services could jeopardize world food supply. Gallai pollinators for total global agricultural production et al. (2009) conclude that overall production would would be a reduction of 3 – 8%. The percentage keep pace with consumption, but a complete loss of increase in total cultivated area that would be required pollinators would cause global deficits in fruits, veg- to compensate for the decrease in production was etables and stimulants (table 1). Such declines in much higher, particularly in the developing world production could result in significant market disrup- where agriculture is more pollinator-dependent. tions as well as nutrient deficiencies, even if total Like biological control, pollination services are caloric intake is still sufficient. more readily quantified than many other services. Early estimates of the value of pollination services were based on the total value of animal-pollinated (c) Water quantity and quality crops, but recent estimates have been more nuanced. The provision of sufficient quantities of clean water is Since most crops are only partly dependent on an essential ecological service provided to agroecosys- animal pollination, a dependence ratio or a measure tems, and agriculture accounts for about 70 per cent of of the proportion reduction in production in the global water use (FAO 2003). Perennial vegetation in absence of pollinators can provide a better approxi- natural ecosystems such as forests can regulate the mation of production losses in the absence of capture, infiltration, retention and flow of water pollinators (Gallai et al. 2009). Clearly, these estimates across the landscape. The plant community plays a Phil. Trans. R. Soc. B (2010) Review. Ecosystem services A. G. Power 2963 central role in regulating water flow by retaining soil, True markets for water are rare (Mendelsohn & modifying soil structure and producing litter. Forest Olmstead 2009), and the value of hydrological ecosys- soils tend to have a higher infiltration rate than other tem services to agriculture is only partially accounted soils, and forests tend to reduce peak flows and for in most estimates. Most farmers who withdraw floods while maintaining base flows (Maes et al. surface waters directly do not pay for these services, 2009). Through hydraulic lift and vertical uplifting, except where local water sources are controlled by irri- deep rooting species can improve the availability of gation districts. Agricultural water demand estimates both water and nutrients to other species in the ecosys- are often based on production data, where the mar- tem. In addition, soil erosion rates are usually low, ginal value of water is estimated by the increase in resulting in good water quality. Fast-growing plantation profits from a unit increase in water inputs. Production forests may be an exception to this generalization, how- data can be highly variable, however, and increases in ever; they can help regulate groundwater recharge, but production can be difficult to assign to water inputs they may reduce stream flow and salinize or acidify (Mendelsohn & Olmstead 2009). Although market some soils ( Jackson et al.2005). approaches for direct water pricing are available, they Water availability in agroecosystems depends not tend to focus on blue water in a particular water only on infiltration and flow, but also on soil moisture basin. Many water prices for agricultural use are retention, another type of ecosystem service. While the based on groundwater removal, using the energy supply of surface water and groundwater (‘blue water’) costs of pumping as the key input variable. The rela- inputs to agriculture through irrigation are indispen- tively new approach of payments for environmental sable in some parts of the world, 80 per cent of services has often focused on supporting watershed agricultural water use comes from rainfall stored in protection and water quality enhancements that soil moisture (‘green water’; Molden 2007). Water target the provision of blue water (Wunder et al. storage in soil is regulated by plant cover, soil organic 2008). It has been suggested recently that farmers matter and the soil biotic community (bacteria, fungi, should receive payments or ‘green water credits’ from earthworms, etc.). Trapping of sediments and erosion downstream water users for good management prac- are controlled by the architecture of plants at or below tices that enhance green water retention as well as the soil surface, the amount of surface litter and litter blue water conservation (ISRIC 2007). decomposition rate. Invertebrates that move between the soil and litter layer influence water movement (d) Soil structure and fertility within soil, as well as the relative amounts of infil- Soil structure and fertility provide essential ecosystem tration and runoff (Swift et al. 2004). These soil services to agroecosystems (Zhang et al. 2007). processes provide essential ecosystem services to Well-aerated soils with abundant organic matter are agriculture. fundamental to nutrient acquisition by crops, as well With climate change, increased variability of rainfall as water retention. Soil pore structure, soil aggregation is predicted to lead to greater risk of drought and and decomposition of organic matter are influenced by flood, while higher temperatures will increase water the activities of bacteria, fungi and macrofauna, such demand (IPCC 2007). Estimates of water availability as earthworms, termites and other invertebrates. for agriculture often neglect the contribution of Micro-organisms mediate nutrient availability through green water, but predictions about water availability decomposition of detritus and plant residues and in 2050 are highly dependent on the inclusion of through nitrogen fixation. Agricultural management green water. Whereas more than six billion people practices that degrade soil structure and soil microbial are predicted to experience water shortages in 2050 communities include mechanical ploughing, disking, when only blue water is taken into account, this cultivating and harvesting, but management practices number drops to about four billion when both blue can also protect the soil and reduce erosion and and green water availability is taken into account runoff. Conservation tillage and other soil conser- (Rockstro ¨m et al. 2009). Some regions of the world vation measures can maintain soil fertility by are much more dependent on green water than minimizing the loss of nutrients and keeping them others (Rockstro ¨m et al. 2009). available to crops. Cover crops facilitate on-farm reten- On-farm management practices that target green tion of soil and nutrients between crop cycles, while water can significantly alter these predictions of hedgerows and riparian vegetation reduce erosion water shortages (Rost et al. 2009). For example, mod- and runoff among fields. Incorporation of crop resi- ifying the tillage regime or mulching can reduce soil dues can maintain soil organic matter, which assists evaporation by 35 – 50%. Rainwater harvest and on- in water retention and nutrient provision to crops. farm storage in ponds, dykes or subsurface dams can Together these practices conserve a suite of ecosystem allow farmers to redirect water to crops during periods services to agriculture from the soil. of water stress, recovering up to 50 per cent of water normally lost to the system. By incorporating moder- ate values (25%) for reductions in soil evaporation (e) Landscape influences on the delivery and water harvesting into a dynamic global vegetation of ecosystem services to agriculture and water balance model, Rost et al. (2009) predicted The delivery of ecosystem services to agriculture is that global crop production could be increased by highly dependent on the structure of the landscape nearly 20 per cent, a value comparable to the current in which the agroecosystem is embedded (figure 1). contribution of irrigation, from on-farm green water Agricultural landscapes span a continuum from struc- management practices. turally simple landscapes dominated by one or two Phil. Trans. R. Soc. B (2010) 2964 A. G. Power Review. Ecosystem services cropping systems to complex mosaics of diverse crop- 2007). Loss of riparian vegetation that often accom- ping systems embedded in a natural habitat matrix. panies intensification can result in significant Water delivery to agroecosystems depends on flow pat- sedimentation of waterways and dams. Other studies, terns across the landscape and can be influenced by a however, have suggested that initial conversion to agri- variety of biophysical factors. Stream flow is influenced culture can cause significant reductions in ecosystem by withdrawals for irrigation, as well as landscape services, but subsequent intensification of the system simplification. Water provisioning is also affected may not have large impacts (Steffan-Dewenter et al. by diversion to other uses in the landscape or 2007). Since the quantification of intensification can watershed, such as domestic, industrial or energy be highly variable among studies and agricultural sys- consumption. tems, these results may not be incompatible. The Both natural biological control services and pollina- bulk of evidence indicates that increasing agricultural tion services depend crucially on the movement of intensification will erode many ecosystem services, organisms across the agricultural landscape, and and projections indicate that 80 per cent of crop pro- hence the spatial structure of the landscape strongly duction growth in developing countries through to influences the magnitude of these ecological services 2030 will come through intensification (FAO 2006). to agricultural ecosystems (Tscharntke et al. 2005; Not all agricultural landscapes are currently shaped Kremen et al. 2007). In complex landscapes, natural by intensification. Interestingly, changes in agricultu- enemies and pollinators move among natural and ral policies that encourage regional specialization semi-natural habitats that provide them with refugia have led to intensification in some European land- and resources that may be scarce in crop fields (Coll scapes, accompanied by cropland abandonment in 2009). Natural enemies with the ability to disperse others (Stoate et al. 2009). Widespread abandonment long distances or that have large home ranges are of agricultural land without restoration presents its better able to survive in disturbed agricultural land- own set of problems, including landscape degradation, scapes with fewer or more distant patches of natural increased risk of erosion and fire. In some areas, both habitat (Tscharntke et al. 2005). agricultural intensification and land abandonment Agricultural intensification can jeopardize many of coexist in the same landscapes, and both processes the ecosystem services provided by the landscape may influence the delivery of ecosystem services to (Matson et al. 1997). Across large areas of North agroecosystems (Stoate et al. 2009). America and Western Europe, agricultural intensifica- tion has resulted in a simplification of landscape structure through the expansion of agricultural land, 4. ECOSYSTEM SERVICES AND DISSERVICES increase in field size, loss of field margin vegetation FROM AGRICULTURE and elimination of natural habitat (Robinson & Agroecosystems are essential sources of provisioning Sutherland 2002). This simplification tends to lead services, and the value of the products they provide to higher levels of pest damage and lower populations are readily measured using standard market analysis. of natural enemies (Brewer et al. 2008; Gardiner et al. Depending on their structure and management, they 2009; O’Rourke 2010). A meta-analysis of the effects may also contribute a number of other ecosystem ser- of landscape structure on natural enemies and pests vices (MEA 2005). Ecosystem processes operating in agriculture showed that landscape complexity within agricultural systems can provide some of the enhanced natural enemy populations in 74 per cent same supporting services described above, including of cases, whereas pest pressure was reduced in more pollination, pest control, genetic diversity for future complex landscapes in 45 per cent of cases (Bianchi agricultural use, soil retention, and regulation of soil et al. 2006). Natural enemies such as predators and fertility, nutrient cycling and water. In addition, parasitoids appear to respond to landscape structure agricultural systems can be managed to support bio- at smaller spatial scales than herbivorous insects diversity and enhance carbon sequestration—globally (Brewer et al. 2008; O’Rourke 2010) and may be important ecosystem services. more susceptible to habitat fragmentation. Based on a review of 16 studies of nine crops on four continents, Klein et al. (2007) concluded that agricultural intensi- (a) Ecosystem disservices from agriculture fication threatens wild bee communities and hence Agriculture can contribute to ecosystem services, but may degrade their stabilizing effect on pollination can also be a source of disservices, including loss of services at the landscape level. Recent studies have biodiversity, agrochemical contamination and sedi- suggested that farm-level diversification is more likely mentation of waterways, pesticide poisoning of non- to influence pests and natural enemies if the wider target organisms, and emissions of greenhouse gases landscape is structurally simple, than if it is already and pollutants (Dale & Polasky 2007; Zhang et al. very complex (Tscharntke et al. 2005; O’Rourke 2007). These disservices come at a significant cost to 2010). In complex landscapes, adding farm-level humans, but there is often a mismatch between the complexity does not necessarily enhance the benefits benefits, which accrue to the agricultural sector, of pest control services. and the costs, which are typically borne by society at Agricultural intensification in the landscape can various scales, from local communities impacted by diminish other ecosystem services as well. Protection pesticides in drinking water to the global commons of groundwater and surface water quality can be threa- affected by global warming. Linking these disservices tened by intensification because of increased nutrients, more closely to agricultural activities through incor- agrochemicals and dissolved salts (Dale & Polasky porating the externalities into the costs of production Phil. Trans. R. Soc. B (2010) Review. Ecosystem services A. G. Power 2965 Table 2. Inputs and outputs of nitrogen and phosphorus in three corn cropping systems with similar yield potential: a low- input corn-based system in western Kenya; a highly fertilized wheat-corn double-cropping system in north China; and a 21 21 corn – soya bean rotation in IL, USA. Actual yields of corn were 2000, 8500 and 8200 kg ha yr per crop in the Kenya, China and USA systems, respectively; the Chinese and USA systems also yielded wheat and soya bean, respectively, in a separate cropping season. From Vitousek et al. (2009). 21 21 nutrient balances by region (kg ha yr ) western Kenya north China midwest USA inputs and outputs NP N P N P fertilizer 7 8 588 92 93 14 biological N fixation 62 total agronomic inputs 7 8 588 92 155 14 removal in grain and/or beans 23 4 361 39 145 23 removal in other harvested products 36 3 total agronomic outputs 59 7 361 39 145 23 agronomic inputs minus harvest removals 252 þ1 þ227 þ53 þ10 29 has the potential to reduce these negative environmental right time, while minimizing nutrient losses by reducing consequences of agricultural practices. soluble inorganic nitrogen and phosphorus pools (Drinkwater & Snapp 2007). Practices such as cover cropping or intercropping enhance plant and microbial (i) Nutrient cycling and pollution assimilation of nitrogen and reduce standing pools of From the local scale to the global scale, agriculture has nitrate, the form of nitrogen that is most susceptible profound effects on biogeochemical cycles and nutri- to loss. Other good management practices include ent availability in ecosystems (Vitousek et al. 1997; diversifying nutrient sources, legume intensification Galloway et al. 2004). The two nutrients that most for biological nitrogen fixation and phosphorus- limit biological production in natural and agricultural solubilizing properties, and diversifying rotations. ecosystems are nitrogen and phosphorus, and they Integrated management of biogeochemical processes are also heavily applied in agroecosystems. Nitrogen that regulate the cycling of nutrients and carbon and phosphorus fertilizers have greatly increased the could reduce the need for surplus nutrient additions amount of new nitrogen and phosphorus in the bio- in agriculture (Drinkwater & Snapp 2007). sphere and have had complex, often harmful, effects Recent analyses forecasting human alterations of on natural ecosystems (Vitousek et al. 1997). These soil nitrogen and phosphorus cycling under various anthropogenically mobilized nutrients have entered scenarios to 2050 further emphasize that closing nutri- both groundwater and surface waters, resulting in ent cycles in agroecosystems can significantly influence many negative consequences for human health and soil nutrient balance (Bouwman et al. 2009). Spatially the environment. Approximately 20 per cent of N explicit modelling of soil nitrogen and phosphorus bal- fertilizer applied in agricultural systems moves into ances suggest that soil phosphorus will be depleted in aquatic ecosystems (Galloway et al. 2004). Impacts grasslands around the world and rock phosphate of nutrient loss from agroecosystems include ground- reserves will be reduced by 36 – 64% by 2100. Many water pollution and increased nitrate levels in scenarios indicate increases in soil nitrogen over this drinking water, eutrophication, increased frequency period along with increased leaching and denitrifica- and severity of algal blooms, hypoxia and fish kills, tion losses, though nitrogen balances are likely to and ‘dead zones’ in coastal marine ecosystems decline in North American and Europe because of (Bouwman et al. 2009). ongoing changes in management practices (Bouwman Ecosystem services within agroecosystems can be et al. 2009). supported by nutrient management strategies that Other ecosystem disservices from agriculture recouple nitrogen, phosphorus and carbon cycling include applications of pesticides that result in loss of within the agroecosystem. Under conventional prac- biodiversity and pesticide residues in surface and tice in developed countries, agroecosystems are often groundwater, which degrades the water provisioning maintained in a state of nutrient saturation and are services provided by agroecosystems. Moreover, inherently leaky as a result of chronic surplus additions agriculture modifies the species identity and root of nitrogen and phosphorus (Galloway et al. 2004; structure of the plant community, the production of Drinkwater & Snapp 2007; Vitousek et al. 2009). In litter, the extent and timing of plant cover and the developing countries, soils are more likely to be composition of the soil biotic community, all of depleted and nutrients may be much more limiting which influence water infiltration and retention in to production, though chronic nutrient surpluses the soil. The intensity of agricultural production and may still occur in some systems (table 2; Vitousek management practices affect both the quantity and et al. 2009). quality of water in an agricultural landscape. Practices To maintain ecosystem services, soil nutrient pools that maximize plant cover, such as minimum tillage, can be intentionally managed to supply crops at the polycultures or agroforestry systems are likely to Phil. Trans. R. Soc. B (2010) 2966 A. G. Power Review. Ecosystem services Table 3. Agricultural contributions to global greenhouse gas emissions by source and expected changes in agricultural greenhouse gas emissions by 2030. Adapted from FAO (2003). CO carbon N O nitrous NO nitric 2 2 x greenhouse gas dioxide CH methane oxide oxides ammonia agricultural source land use change, ruminants (15%) livestock/manure biomass burning livestock/manure (estimated % contribution especially (17%) (13%) (44%) to total emissions) deforestation rice (11%) mineral manure/mineral mineral fertilizers (8%) fertilizers (2%) fertilizers (17%) biomass burning biomass burning biomass burning (7%) (3%) (11%) agricultural emissions 15% 49% 66% 27% 93% (as % total of anthropogenic sources) expected changes in stable or rice—stable or 35 – 60% from livestock— agricultural emissions decreasing decreasing increase 60% increase by 2030 livestock—60% increase Total emissions include both natural and anthropogenic sources. decrease runoff and increase infiltration. Irrigation particularly when more nitrogen is applied than can practices also influence runoff, sedimentation and be taken up by the plants. Nitrogen is added to soils groundwater levels in the landscape. through the use of inorganic fertilizers, application of animal manure, cultivation of nitrogen-fixing plants and retention of crop residues. Globally, approxi- (ii) Emissions of greenhouse gases mately 50 per cent of N applied as fertilizer is taken Agricultural activities are estimated to be responsible up by the crop, 2 – 5% is stored as soil N, 25 per for 12 – 14% of global anthropogenic emissions of cent is lost as N O emissions and 20 per cent moves greenhouse gases, not including emissions that arise to aquatic systems (Galloway et al. 2004). In addition from land clearing (US-EPA 2006; IPCC 2007). to direct N O emissions, the production of synthetic After fossil fuel combustion, land-use change is the nitrogen fertilizers is an energy-intensive process that second largest global cause of CO emissions, and 2 produces additional greenhouse gases. Flooded rice some of this change is driven by conversion to agricul- cultivation contributes to greenhouse gas emissions ture, largely in developing countries. In developed through anaerobic decomposition of soil organic countries, forest conversion to cropland, pasture and matter by CH -emitting soil microbes. The practice rangeland were common through the middle of the of burning crop residues contributes to the production twentieth century, but current conversions are of both CH and N O. 4 2 primarily for suburban development. In addition to Livestock production also contributes to CH and losses of above-ground carbon due to deforestation N O emissions (Pitesky et al.2009), and these impacts or other land clearing, conversion of natural are likely to increase through to 2050 as the demand for ecosystems to agriculture reduces the soil carbon meat increases (FAO 2003). Ruminant livestock such as pool by 30 – 50% over 50 – 100 years in temperate cattle, sheep, goats and buffalo emit CH as a regions and 50 – 75% over 20 – 50 years in the tropics byproduct of their digestive processes (enteric (Lal 2008a). Although agricultural systems generate fermentation). Livestock waste can release both CH , very large CO fluxes to and from the atmosphere, 2 through the biological breakdown of organic com- the net flux appears to be small. However, both the pounds, and N O, through microbial metabolism of magnitude of emissions and the relative importance nitrogen contained in manure. The magnitude of of the different sources vary widely among agricultural direct emissions depends strongly on manure manage- systems around the world. ment practices, such as the use of lagoons or field Agricultural activities contribute to emissions in spreading, and to some degree on the type of livestock several ways (table 3). Approximately 49 per cent of feed. The magnitude of emissions attributed to live- global anthropogenic emissions of methane (CH ) 4 stock is controversial, ranging from 3 to 18 per cent and 66 per cent of global annual emissions of nitrous of global emissions, depending on whether the effects oxide (N O), both greenhouse gases, are attributed 2 of land-clearing (i.e. deforestation) for livestock pro- to agriculture (FAO 2003), although there is a wide duction is included in the estimate (Pitesky et al. 2009). range of uncertainty in the estimates of both the agri- cultural contribution and the anthropogenic total. N O emissions occur naturally as a part of the soil (b) Ecosystem services from agriculture nitrogen cycle, but the application of nitrogen to On-farm management practices can significantly crops can significantly increase the rate of emissions, enhance the ecosystem services provided by Phil. Trans. R. Soc. B (2010) Review. Ecosystem services A. G. Power 2967 agriculture. Farmers routinely manage for greater pro- commercial production systems in Brazil and Canada visioning services by using inputs and practices to (reviewed in Govaerts et al. 2009). Many farmers increase yields, but management practices can also have already adopted practices that retain soil C in enhance other ecosystem services, such as pollination, order to achieve higher productivity and lower costs. biological pest control, soil fertility and structure, However, even the use of soil conservation and restor- water regulation, and support for biodiversity. Habitat ation practices cannot fully restore soil carbon lost management within the agroecosystem can provide the through conversion to agriculture. It is estimated that resources necessary for pollinators or natural enemies the soil C pool attainable through best management (Tscharntke et al. 2005). Many studies have identified practices is typically 60 – 70% of the original soil C the important role of perennial vegetation in support- pool prior to conversion (Lal 2008a). ing biodiversity in general and beneficial organisms Finally, agricultural land can also be used to grow in particular (e.g. Perfecto & Vandermeer 2008). crops for bioenergy production. Bioenergy, particu- Evidence suggests that management systems that larly cellulosic biofuels, has the potential to replace a emphasize crop diversity through the use of polycul- portion of fossil fuels and to lower greenhouse gas tures, cover crops, crop rotations and agroforestry emissions (Smith et al. 2008). While burning fossil can often reduce the abundance of insect pests that fuels adds carbon to the atmosphere, bioenergy specialize on a particular crop, while providing refuge crops, if managed correctly, avoid this by recycling and alternative prey for natural enemies (Andow carbon. Although carbon is released to the atmosphere 1991). Similar practices may benefit wild pollinators, when bioenergy feedstocks are burned, carbon is including minimal use of pesticides, no-till systems recaptured during plant growth. The replacement of and crop rotations with mass-flowering crops. fossil fuel-generated energy with solar energy captured by photosynthesis has the potential to reduce CO , N O and NO emissions. 2 x (i) Mitigation of greenhouse gases emissions However, calculating net emissions from bioenergy Agricultural practices can effectively reduce or offset is tricky (Searchinger et al. 2008). First, management agricultural greenhouse gas emissions through a var- practices used to grow crops and forages for bioenergy iety of processes (Drinkwater & Snapp 2007; Lal production will influence net emissions. Development 2008a; Smith et al. 2008). Effective manure manage- of appropriate bioenergy systems based on perennial ment can significantly reduce emissions from animal plant species that do not require intensive inputs waste. Replacing synthetic nitrogen fertilizers with bio- such as tillage, fertilizers and other agrochemicals logical nitrogen fixation by legumes can reduce CO have the potential to help offset fossil fuel use in agri- emissions from agricultural production by half (Drink- culture. Bioenergy systems that rely on annual row water & Snapp 2007). The process of perennialization crops such as corn are not likely to be as beneficial, and legume intensification in agroecosystems modifies and expanding these systems can dramatically reduce internal cycling processes and increases N use effi- the delivery of other ecosystem services like biological ciency within agroecosystems via the recoupling pest control (Landis et al. 2008). Second, even with mechanisms discussed above. Chronic surplus the use of perennial species and few inputs, there is sig- additions of inorganic N, which are currently com- nificant potential for higher, rather than lower, monplace, can be reduced under these scenarios, emissions attributable to bioenergy crops, resulting leading to reductions in NO and N O emissions. from land-use change as farmers respond to higher x 2 Agriculture can offset greenhouse gas emissions by prices and convert forest and grassland to new crop- increasing the capacity for carbon uptake and storage land (Fargione et al. 2008; Searchinger et al. 2008). in soils, i.e. carbon sequestration (Lal 2008a,b). The The production of bioenergy from waste products, net flux of CO between the land and the atmosphere such as crop waste, fall grass harvests from reserve is a balance between carbon losses from land-use con- lands, or even municipal waste, could avoid land-use version and land-management practices, and carbon change and result in lower CO emissions. gains from plant growth and sequestration of decom- posed plant residues in soils. In particular, soil conservation measures such as conservation tillage 5. TRADEOFFS and no-till cultivation can conserve soil carbon, Several studies have explicitly analysed possible trade- and crop rotations and cover crops can reduce the offs between the supply of various ecosystem services degradation of subsurface carbon. In general, water from agricultural systems. In general, ecosystem ser- management and erosion control can aid in maintain- vices are not independent of one other and the ing soil organic carbon (Lal 2008a). relationships between them are likely to be highly non- Soil carbon sequestration thus provides additional linear. For agriculture, the problem is typically posed ecosystem services to agriculture itself, by conserving as a tradeoff between provisioning services—i.e. pro- soil structure and fertility, improving soil quality, duction of agricultural goods such as food, fibre or increasing the use efficiency of agronomic inputs, bioenergy—and regulating services such as water puri- and improving water quality by filtration and denatur- fication, soil conservation or carbon sequestration ing of pollutants (Lal 2008b; Smith et al. 2008). The (MEA 2005). Cultural services and biodiversity con- economic benefits of conservation agriculture have servation are also often viewed as tradeoffs with been estimated in diverse systems around the world, production. from smallholder agricultural systems in Latin Tradeoffs among ecosystem services should be con- America and sub-Saharan Africa to large-scale sidered in terms of spatial scale, temporal scale and Phil. Trans. R. Soc. B (2010) 2968 A. G. Power Review. Ecosystem services reversibility (Rodriguez et al. 2006). Are the effects of agroecosystems to support many ecosystem services the tradeoff felt locally, for example on-farm, or at a while still maintaining or enhancing the provisioning more distant location? How quickly does the tradeoff services that agroecosystems were designed to pro- occur? Are the effects reversible and if so, how quickly duce. Sustainable intensification will depend on can they be reversed? Management decisions often management of ecosystem processes rather than focus on the immediate provision of a commodity or fossil fuel inputs (Baulcombe et al. 2009). service, at the expense of this same or another ecosys- Futures scenarios are an increasingly common tool tem service at a distant location or in the future. As used to evaluate tradeoffs between commodity pro- either the temporal or spatial scale increases, tradeoffs duction, ecosystem services and the conservation of become more uncertain and difficult to manage. biodiversity in various ecosystems, including agroeco- Management is further complicated by biophysical systems (MEA 2005). In addition, advances in and socioeconomic variation, since every hectare of a spatially explicit modelling have greatly improved the given habitat is not of equal value in generating a ability to estimate the production of ecosystem services given ecosystem service (Nelson et al. 2009). For natu- from landscapes. Analysis of the provision of agricul- ral ecosystems, habitat quality, size of unit and spatial tural goods and other ecosystem services in an configuration are likely to influence the services agricultural valley in Oregon, USA, found few trade- provided by the ecosystem. For agroecosystems, man- offs between ecosystem services and biodiversity agement practices, along with access to market and conservation (Nelson et al. 2009). The spatially expli- patterns of trade are likely to be critical to the pro- cit modelling tool InVEST (integrated valuation of vision of ecosystem services. Furthermore, the values ecosystem services and tradeoffs—Tallis & Polasky of both market and non-market goods and services 2009) was used to evaluate three stakeholder-defined will vary according to various biophysical and socio- scenarios of land use through to 2050, including cur- economic factors. Without information on the factors rent land-use patterns, increased development or that influence the quantity and value of ecosystem ser- increased conservation. The models predicted changes vices, it is difficult to design policies, incentives or in commodity production, biodiversity conservation payment schemes that can optimize the delivery of and ecosystem services (hydrological services, soil con- those services (Nelson et al. 2009). servation and carbon sequestration) under the three Ecosystem services are provided to agriculture at scenarios. In general, scenarios that scored high on varying scales, and this can influence a farmer’s incen- delivering ecosystem services also scored high on tives for protecting the ecosystem service. Farmers biodiversity conservation. Scenarios with increased have a direct interest in managing ecosystem services development had higher commodity values and lower such as soil fertility, soil retention, pollination and levels of conservation and ecosystem services, but pest control, because they are provided at the field this tradeoff disappeared when payments for carbon and farm scale. At larger scales, benefits are likely to sequestration were included. Other spatially explicit accrue to others, including other farmers, in addition studies have also found that biodiversity conservation to the farmer providing the resource. A farmer who and carbon sequestration can be achieved in agricul- restores on-farm habitat complexity increases pollina- tural landscapes (Eigenbrod et al. 2009). Clearly, tion and pest control services to her neighbours as more detailed studies like these are needed to reach well as herself. The neighbours benefit from these a conclusion about the ecological and economic services without having to give up land that would conditions that may lead to tradeoffs between otherwise produce crops and generate income. Greater agricultural production and ecosystem services. landscape complexity may be considered a common pool resource, and a farmer, acting alone, may lack the incentive to set aside the optimal amount of habitat (a) Future trends for both the farmer and the neighbour (Zhang et al. Current FAO projections suggest that the rate of con- 2007). version of forested land to agriculture will continue to Recent studies suggest that tradeoffs between agri- slow through to 2050, there will be little change in cultural production and various ecosystem services grazing area, and protected areas will increase (FAO are not inevitable and that ‘win – win’ scenarios are 2003, 2006). Increases in protected areas will assist possible. An analysis of yields from agroecosystems in maintaining the flow of ecosystem services like around the world indicates that, on average, agricul- water provisioning, pollination and biological control tural systems that conserve ecosystem services by to agriculture. Advances in sustainable agriculture in using practices like conservation tillage, crop diversifi- developed countries should also lead to enhanced eco- cation, legume intensification and biological control system services in agricultural landscapes. In some perform as well as intensive, high-input systems regions, however, conversion of land to urbanization (Badgley et al. 2007). The introduction of these is expected to increase dramatically and will put sig- types of practices into resource-poor agroecosystems nificant stress on the availability of agricultural land in 57 developing countries resulted in a mean relative and protected areas. At the global scale, the growth yield increase of 79 per cent (Pretty et al. 2006). In of demand for all crop and livestock products is pro- these examples, there was no evidence that the pro- jected to be lower than in the past: 1.5 per cent per visioning services provided by agriculture were annum in the period 2000 – 2030 and 0.9 per cent jeopardized by modifying the system to improve its for 2030 – 2050 when compared with rates around ability to provide other ecological services. These 2.1 – 2.3% in the preceding four decades, in part due analyses suggest that it may be possible to manage to the lower population growth (FAO 2006). Phil. Trans. R. Soc. B (2010) Review. Ecosystem services A. G. Power 2969 Despite slowing demand growth, ecosystem maximizing synergies. 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B (2010) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Philosophical Transactions of the Royal Society B: Biological Sciences Pubmed Central

Ecosystem services and agriculture: tradeoffs and synergies

Philosophical Transactions of the Royal Society B: Biological Sciences , Volume 365 (1554) – Sep 27, 2010

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Phil. Trans. R. Soc. B (2010) 365, 2959–2971 doi:10.1098/rstb.2010.0143 Review Ecosystem services and agriculture: tradeoffs and synergies Alison G. Power* Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY, USA Agricultural ecosystems provide humans with food, forage, bioenergy and pharmaceuticals and are essential to human wellbeing. These systems rely on ecosystem services provided by natural ecosys- tems, including pollination, biological pest control, maintenance of soil structure and fertility, nutrient cycling and hydrological services. Preliminary assessments indicate that the value of these ecosystem services to agriculture is enormous and often underappreciated. Agroecosystems also produce a variety of ecosystem services, such as regulation of soil and water quality, carbon sequestration, support for biodiversity and cultural services. Depending on management practices, agriculture can also be the source of numerous disservices, including loss of wildlife habitat, nutri- ent runoff, sedimentation of waterways, greenhouse gas emissions, and pesticide poisoning of humans and non-target species. The tradeoffs that may occur between provisioning services and other ecosystem services and disservices should be evaluated in terms of spatial scale, temporal scale and reversibility. As more effective methods for valuing ecosystem services become available, the potential for ‘win – win’ scenarios increases. Under all scenarios, appropriate agricultural man- agement practices are critical to realizing the benefits of ecosystem services and reducing disservices from agricultural activities. Keywords: ecosystem services; agroecosystems; pollination; biological control; valuation of ecosystem services; soil carbon sequestration 1. INTRODUCTION recently their contributions to other types of ecosystem Agriculture is a dominant form of land management services have been recognized (MEA 2005). Influ- globally, and agricultural ecosystems cover nearly 40 enced by human management, ecosystem processes per cent of the terrestrial surface of the Earth (FAO within agricultural systems can provide services 2009). Agroecosystems are both providers and consu- that support the provisioning services, including mers of ecosystem services (figure 1). Humans value pollination, pest control, genetic diversity for future these systems chiefly for their provisioning services, agricultural use, soil retention, regulation of soil and these highly managed ecosystems are designed to fertility and nutrient cycling. Whether any particular provide food, forage, fibre, bioenergy and pharmaceu- agricultural system provides such services in support ticals. In turn, agroecosystems depend strongly on a of provisioning depends on management, and manage- suite of ecosystem services provided by natural, unma- ment is influenced by the balance between short-term naged ecosystems. Supporting services include genetic and long-term benefits. biodiversity for use in breeding crops and livestock, Management practices also influence the potential soil formation and structure, soil fertility, nutrient for ‘disservices’ from agriculture, including loss of cycling and the provision of water. Regulating services habitat for conserving biodiversity, nutrient runoff, may be provided to agriculture by pollinators and sedimentation of waterways, and pesticide poisoning natural enemies that move into agroecosystems from of humans and non-target species (Zhang et al. natural vegetation. Natural ecosystems may also 2007). Since agricultural practices can harm bio- purify water and regulate its flow into agricultural sys- diversity through multiple pathways, agriculture is tems, providing sufficient quantities at the appropriate often considered anathema to conservation. However, time for plant growth. appropriate management can ameliorate many of Traditionally, agroecosystems have been considered the negative impacts of agriculture, while largely primarily as sources of provisioning services, but more maintaining provisioning services. Agroecosystems can provide a range of other regu- lating and cultural services to human communities, *agp4@cornell.edu in addition to provisioning services and services in support of provisioning. Regulating services from agri- While the Government Office for Science commissioned this review, culture may include flood control, water quality the views are those of the author(s), are independent of Government, and do not constitute Government policy. control, carbon storage and climate regulation through greenhouse gas emissions, disease regulation, and One contribution of 23 to a Theme Issue ‘Food security: feeding the waste treatment (e.g. nutrients, pesticides). Cultural world in 2050’. 2959 This journal is q 2010 The Royal Society 2960 A. G. Power Review. Ecosystem services farm management landscape management tillage agricultural ecosystem windbreaks crop diversity services hedgerows field size riparian vegetation crop rotation natural habitat patches cover cropping ecosystem services pest control pollination nutrient re/cycling agroecosystem landscape matrix soil conservation, structure and fertility water provision, quality and quantity ecosystem disservices carbon sequestration loss of biodiversity biodiversity provisioning loss of wildlife habitat nutrient runoff services sedimentation of waterways food pesticide poisoning fibre bioenergy greenhouse gas emissions Figure 1. Impacts of farm management and landscape management on the flow of ecosystem services and disservices to and from agroecosystems. services may include scenic beauty, education, recrea- agriculture can have strong impacts on the system’s tion and tourism, as well as traditional use. ability to produce important ecosystem services, but Agricultural places or products are often used in tra- many agricultural systems can also be important ditional rituals and customs that bond human sources of services. Indeed, agricultural land use can communities. Conservation of biodiversity may also be considered an intermediate stage in a human- be considered a cultural ecosystem service influenced impact continuum between wilderness and urban by agriculture, since most cultures recognize appreci- ecosystems (Swinton et al. 2007). Just as conversion ation of nature as an explicit human value. In return, from natural ecosystems to agriculture can reduce biodiversity can contribute a variety of supporting ser- the flow of certain ecosystem services, the intensifica- vices to agroecosystems and surrounding ecosystems tion of agriculture (Matson et al. 1997) or the (Daily 1997). conversion of agroecosystems to urban or suburban Around the world, agricultural ecosystems show tre- development can further degrade the provision of mendous variation in structure and function, because beneficial services. they were designed by diverse cultures under diverse socioeconomic conditions in diverse climatic regions. Functioning agroecosystems include, among others, 2. APPROACHES TO ANALYSING annual crop monocultures, temperate perennial orch- ECOSYSTEM SERVICES ards, grazing systems, arid-land pastoral systems, The value of ecosystem services has been estimated tropical shifting cultivation systems, smallholder in various ways. In general, the framework has three mixed cropping systems, paddy rice systems, tropical main parts: (i) measuring the provision of ecosystem plantations (e.g. oil palm, coffee, cacao), agroforestry services; (ii) determining the monetary value of systems and species-rich home gardens. This variety ecosystem services; (iii) designing policy tools for of agricultural systems results in a highly variable managing ecosystem services (Polasky 2008). Ecolo- assortment and quantity of ecosystem services. Just gists and other natural scientists have been engaged as the provisioning services and products that derive in enhancing our understanding of how ecosystem ser- from these agroecosystems vary, the support services, vices are produced for over a decade (e.g. Costanza regulating services and cultural services also differ, et al. 1997; Daily 1997; MEA 2005). Basic knowledge resulting in extreme variation in the value these about ecosystem structure and function is increasing at services provide, inside and outside the agroecosystem. a rapid pace, but we know less about how these factors In maximizing the value of provisioning services, determine the provision of a complete range of ecosys- agricultural activities are likely to modify or diminish tem services from an individual ecosystem (NRC the ecological services provided by unmanaged terres- 2005). In practice, most studies focus on estimating trial ecosystems, but appropriate management of key the provision of one or two well understood ecosystem processes may improve the ability of agroecosystems services. Better understanding of the processes that to provide a broad range of ecosystem services. influence ecosystem services could allow us to predict Globally, most landscapes have been modified by the outputs of a range of ecosystem services, given par- agricultural activities and most natural, unmanaged ticular ecosystem characteristics and perturbations to ecosystems sit in a matrix of agricultural land uses. those ecosystems. That is, an ‘ecological production The conversion of undisturbed natural ecosystems to function’ might be generated (Polasky 2008). Despite Phil. Trans. R. Soc. B (2010) Review. Ecosystem services A. G. Power 2961 recent advances, this is an area of research that still effects of intensive agriculture by providing financial needs considerable attention. incentives to farmers to adopt environmentally sound The second step of valuation of ecosystem services agricultural practices. The impacts of these projects typically includes both market and non-market valua- are variable, however, and their success is debated tion. Valuing the provisioning services that derive (e.g. Baulcombe et al. 2009). A recent evaluation of from agriculture is relatively straightforward, since over 200 paired fields in five European countries indi- agricultural commodities are traded in local, regional cated that agri-environment programmes had marginal or global markets. Some ecosystem services provide to moderate positive impacts on biodiversity, but lar- an essential input to agricultural production, and gely failed to benefit rare or endangered species their value can be measured by estimating the (Kleijn et al. 2006). change in the quantity or quality of agricultural pro- The Economics of Ecosystems and Biodiversity duction when the services are removed or degraded. (TEEB) led by the United Nations Environment Pro- This approach has been used to estimate the value of gramme (UNEP), is an international effort designed pollination services and biological control services to integrate science, economics and policy around bio- (e.g. Losey & Vaughan 2006; Gallai et al. 2009). diversity and ecosystem services. A recent report for Values for such services can also be estimated by policy-makers highlights the link between poverty measuring replacement costs, such as pesticides repla- and the loss of ecosystems and biodiversity, with the cing natural pest control and hand-pollination or intent of facilitating the development of effective beehive rental replacing pollination. policy in this area (ten Brink 2009). Another approach Non-market valuation methods have been used for is the establishment of markets for pollution credits, many years to measure both the use value and the including the growing global carbon market operating non-use value of various environmental amenities under various cap and trade initiatives, such as the (Mendelsohn & Olmstead 2009). Non-market valua- European Union Emission Trading System. tion can be based on revealed preference (behaviour expressed through consumer choices) or stated prefer- 3. ECOSYSTEM SERVICES FLOWING ence (e.g. attitudes expressed through surveys). In TO AGRICULTURE contingent valuation surveys, for example, consumers The production of agricultural goods is highly depen- are asked what they would be willing to pay for the dent on the services provided by neighbouring natural ecosystem service. Another approach is to ask produ- ecosystems, but only recently have there been attempts cers—in this case farmers—what they would be to estimate the value of many of those services to agri- willing to accept to supply the ecosystem service cultural enterprises. Some services are more easily (Swinton et al. 2007). quantified than others, to the extent that they are The overarching goal of measuring and valuing eco- essential to crop production or they substitute directly system services is to use that information to shape for purchased inputs. policies and incentives for better management of eco- systems and natural resources. One of the inherent difficulties of managing ecosystem services is that the (a) Biological pest control individuals who control the supply of such services, Biological control of pest insects in agroecosystems is such as farmers and other land managers, are not an important ecosystem service that is often always the beneficiaries of these services. Many ecosys- supported by natural ecosystems. Non-crop habitats tem services are public goods. While farmers do provide the habitat and diverse food resources benefit from a variety of ecosystem services, their required for arthropod predators and parasitoids, activities may strongly influence the delivery of services insectivorous birds and bats, and microbial pathogens to other individuals who do not control the production that act as natural enemies to agricultural pests and of these services. Examples include the impact of farm- provide biological control services in agroecosystems ing practices on downstream water supply and purity (Tscharntke et al. 2005). These biological control and regional pest management. The challenge is to services can reduce populations of pest insects use emerging information about ecological production and weeds in agriculture, thereby reducing the need functions and valuation to develop policies and incen- for pesticides. tives that are easily implemented and adaptable to Because the ecosystem services provided by natural changing ecological and market conditions. enemies can substitute directly for insecticides and One approach to incentives is to provide payments crop losses to pests can often be measured, the econ- for environmental services, through government pro- omic value of these services is more easily estimated grammes or private sector initiatives (Swinton 2008). than many other services. For example, an analysis of Historically, the US has provided support for soil con- the value of natural enemy suppression of soya bean servation investments and other readily observable aphid in soya bean indicated that this ecosystem ser- practices to maintain or enhance certain ecosystem vice was worth a minimum of US$239 million in services. In the US, the Conservation Security Pro- four US states in 2007 – 2008 alone (Landis et al. gram of the 2002 farm bill established payments for 2008). Since this is an estimate of the value of suppres- environmental services, and many European countries sing a single pest in one crop, the total value of have also provided governmental support for environ- biological control services is clearly much larger. Natu- mentally sound farming practices that support ral pest control services have been estimated to save ecosystem services. Agri-environment schemes are $13.6 billion per year in agricultural crops in the US intended to moderate the negative environmental (Losey & Vaughan 2006). This estimate is based on Phil. Trans. R. Soc. B (2010) 2962 A. G. Power Review. Ecosystem services Table 1. Rate of vulnerability to pollinator loss and effect of pollinator loss on global food production for pollinator- dependent crop categories based on 2005 data. IPEV, insect pollination economic value; EV, total production economic value. Adapted from Gallai et al. (2009). relative production surplus (% of consumption) crop category rate of vulnerability (IPEV/EV) % before pollinator loss after pollinator loss stimulant crops 39.0 18 224 nuts 31.0 29 16 fruits 23.1 12 212 edible oil crops 16.3 75 40 vegetables 12.2 19 26 pulse 4.3 60 54 spices 2.7 11 8 The difference between 2005 production and consumption expressed in relative terms as % of 2005 consumption figures following FAO (http://faostat.fao.org). the value of crop losses to insect damage as well as the are also fairly crude and intended to provide a broad- value of expenditures on insecticides. Studies suggest brush assessment of potential economic benefits. that insect predators and parasitoids account for Moreover, most estimates do not take into account approximately 33 per cent of natural pest control potential changes in the value of each commodity as (Hawkins et al. 1999), therefore the value of pest demand increases owing to reduced crop production. control services attributed to insect natural enemies A recent assessment of agricultural vulnerability to has been estimated at $4.5 billion per year (Losey & loss of pollination services based on the ratio of the Vaughan 2006). economic value of insect pollination to the economic value of the crop indicated an overall vulnerability of 9.5 per cent, but vulnerability varied significantly (b) Pollination among types of commodities as well as by geographical Pollination is another important ecosystem service to region (Gallai et al. 2009). Stimulant crops (coffee, agriculture that is provided by natural habitats in agri- cacao, and tea), nuts, fruits and edible oil crops were cultural landscapes. Approximately 65 per cent of predicted to be particularly vulnerable to the loss of plant species require pollination by animals, and an pollination services (table 1). The economic impact analysis of data from 200 countries indicated that of insect pollination on world food production in 75 per cent of crop species of global significance for 2005 in the 162 FAO member countries has been cal- food production rely on animal pollination, primarily culated at 153 billion euro, but vulnerability to loss of by insects (Klein et al. 2007). Of the most important pollinators varies among geographical regions due, in animal-pollinated crops, over 40 per cent depend on part, to crop specialization (Gallai et al. 2009). For wild pollinators, often in addition to domesticated example, West African countries produce 56 per cent honeybees. Only 35 – 40% of the total volume of of the world’s stimulant crops with a vulnerability to food crop production comes from animal-pollinated pollinator loss of 90 per cent. The loss of pollination crops, however, since cereal crops typically do not services in these crops could have devastating effects depend on animal pollination. Aizen et al. (2009) on the economies of such countries in the short term used data from the United Nations Food and Agricul- and lead to significant restructuring of global prices ture Organization (FAO) on the production of 87 in the longer term (Gallai et al. 2009). globally important crops during 1961 – 2006 to esti- A crucial question is whether the loss of pollination mate that the consequences of a complete loss of services could jeopardize world food supply. Gallai pollinators for total global agricultural production et al. (2009) conclude that overall production would would be a reduction of 3 – 8%. The percentage keep pace with consumption, but a complete loss of increase in total cultivated area that would be required pollinators would cause global deficits in fruits, veg- to compensate for the decrease in production was etables and stimulants (table 1). Such declines in much higher, particularly in the developing world production could result in significant market disrup- where agriculture is more pollinator-dependent. tions as well as nutrient deficiencies, even if total Like biological control, pollination services are caloric intake is still sufficient. more readily quantified than many other services. Early estimates of the value of pollination services were based on the total value of animal-pollinated (c) Water quantity and quality crops, but recent estimates have been more nuanced. The provision of sufficient quantities of clean water is Since most crops are only partly dependent on an essential ecological service provided to agroecosys- animal pollination, a dependence ratio or a measure tems, and agriculture accounts for about 70 per cent of of the proportion reduction in production in the global water use (FAO 2003). Perennial vegetation in absence of pollinators can provide a better approxi- natural ecosystems such as forests can regulate the mation of production losses in the absence of capture, infiltration, retention and flow of water pollinators (Gallai et al. 2009). Clearly, these estimates across the landscape. The plant community plays a Phil. Trans. R. Soc. B (2010) Review. Ecosystem services A. G. Power 2963 central role in regulating water flow by retaining soil, True markets for water are rare (Mendelsohn & modifying soil structure and producing litter. Forest Olmstead 2009), and the value of hydrological ecosys- soils tend to have a higher infiltration rate than other tem services to agriculture is only partially accounted soils, and forests tend to reduce peak flows and for in most estimates. Most farmers who withdraw floods while maintaining base flows (Maes et al. surface waters directly do not pay for these services, 2009). Through hydraulic lift and vertical uplifting, except where local water sources are controlled by irri- deep rooting species can improve the availability of gation districts. Agricultural water demand estimates both water and nutrients to other species in the ecosys- are often based on production data, where the mar- tem. In addition, soil erosion rates are usually low, ginal value of water is estimated by the increase in resulting in good water quality. Fast-growing plantation profits from a unit increase in water inputs. Production forests may be an exception to this generalization, how- data can be highly variable, however, and increases in ever; they can help regulate groundwater recharge, but production can be difficult to assign to water inputs they may reduce stream flow and salinize or acidify (Mendelsohn & Olmstead 2009). Although market some soils ( Jackson et al.2005). approaches for direct water pricing are available, they Water availability in agroecosystems depends not tend to focus on blue water in a particular water only on infiltration and flow, but also on soil moisture basin. Many water prices for agricultural use are retention, another type of ecosystem service. While the based on groundwater removal, using the energy supply of surface water and groundwater (‘blue water’) costs of pumping as the key input variable. The rela- inputs to agriculture through irrigation are indispen- tively new approach of payments for environmental sable in some parts of the world, 80 per cent of services has often focused on supporting watershed agricultural water use comes from rainfall stored in protection and water quality enhancements that soil moisture (‘green water’; Molden 2007). Water target the provision of blue water (Wunder et al. storage in soil is regulated by plant cover, soil organic 2008). It has been suggested recently that farmers matter and the soil biotic community (bacteria, fungi, should receive payments or ‘green water credits’ from earthworms, etc.). Trapping of sediments and erosion downstream water users for good management prac- are controlled by the architecture of plants at or below tices that enhance green water retention as well as the soil surface, the amount of surface litter and litter blue water conservation (ISRIC 2007). decomposition rate. Invertebrates that move between the soil and litter layer influence water movement (d) Soil structure and fertility within soil, as well as the relative amounts of infil- Soil structure and fertility provide essential ecosystem tration and runoff (Swift et al. 2004). These soil services to agroecosystems (Zhang et al. 2007). processes provide essential ecosystem services to Well-aerated soils with abundant organic matter are agriculture. fundamental to nutrient acquisition by crops, as well With climate change, increased variability of rainfall as water retention. Soil pore structure, soil aggregation is predicted to lead to greater risk of drought and and decomposition of organic matter are influenced by flood, while higher temperatures will increase water the activities of bacteria, fungi and macrofauna, such demand (IPCC 2007). Estimates of water availability as earthworms, termites and other invertebrates. for agriculture often neglect the contribution of Micro-organisms mediate nutrient availability through green water, but predictions about water availability decomposition of detritus and plant residues and in 2050 are highly dependent on the inclusion of through nitrogen fixation. Agricultural management green water. Whereas more than six billion people practices that degrade soil structure and soil microbial are predicted to experience water shortages in 2050 communities include mechanical ploughing, disking, when only blue water is taken into account, this cultivating and harvesting, but management practices number drops to about four billion when both blue can also protect the soil and reduce erosion and and green water availability is taken into account runoff. Conservation tillage and other soil conser- (Rockstro ¨m et al. 2009). Some regions of the world vation measures can maintain soil fertility by are much more dependent on green water than minimizing the loss of nutrients and keeping them others (Rockstro ¨m et al. 2009). available to crops. Cover crops facilitate on-farm reten- On-farm management practices that target green tion of soil and nutrients between crop cycles, while water can significantly alter these predictions of hedgerows and riparian vegetation reduce erosion water shortages (Rost et al. 2009). For example, mod- and runoff among fields. Incorporation of crop resi- ifying the tillage regime or mulching can reduce soil dues can maintain soil organic matter, which assists evaporation by 35 – 50%. Rainwater harvest and on- in water retention and nutrient provision to crops. farm storage in ponds, dykes or subsurface dams can Together these practices conserve a suite of ecosystem allow farmers to redirect water to crops during periods services to agriculture from the soil. of water stress, recovering up to 50 per cent of water normally lost to the system. By incorporating moder- ate values (25%) for reductions in soil evaporation (e) Landscape influences on the delivery and water harvesting into a dynamic global vegetation of ecosystem services to agriculture and water balance model, Rost et al. (2009) predicted The delivery of ecosystem services to agriculture is that global crop production could be increased by highly dependent on the structure of the landscape nearly 20 per cent, a value comparable to the current in which the agroecosystem is embedded (figure 1). contribution of irrigation, from on-farm green water Agricultural landscapes span a continuum from struc- management practices. turally simple landscapes dominated by one or two Phil. Trans. R. Soc. B (2010) 2964 A. G. Power Review. Ecosystem services cropping systems to complex mosaics of diverse crop- 2007). Loss of riparian vegetation that often accom- ping systems embedded in a natural habitat matrix. panies intensification can result in significant Water delivery to agroecosystems depends on flow pat- sedimentation of waterways and dams. Other studies, terns across the landscape and can be influenced by a however, have suggested that initial conversion to agri- variety of biophysical factors. Stream flow is influenced culture can cause significant reductions in ecosystem by withdrawals for irrigation, as well as landscape services, but subsequent intensification of the system simplification. Water provisioning is also affected may not have large impacts (Steffan-Dewenter et al. by diversion to other uses in the landscape or 2007). Since the quantification of intensification can watershed, such as domestic, industrial or energy be highly variable among studies and agricultural sys- consumption. tems, these results may not be incompatible. The Both natural biological control services and pollina- bulk of evidence indicates that increasing agricultural tion services depend crucially on the movement of intensification will erode many ecosystem services, organisms across the agricultural landscape, and and projections indicate that 80 per cent of crop pro- hence the spatial structure of the landscape strongly duction growth in developing countries through to influences the magnitude of these ecological services 2030 will come through intensification (FAO 2006). to agricultural ecosystems (Tscharntke et al. 2005; Not all agricultural landscapes are currently shaped Kremen et al. 2007). In complex landscapes, natural by intensification. Interestingly, changes in agricultu- enemies and pollinators move among natural and ral policies that encourage regional specialization semi-natural habitats that provide them with refugia have led to intensification in some European land- and resources that may be scarce in crop fields (Coll scapes, accompanied by cropland abandonment in 2009). Natural enemies with the ability to disperse others (Stoate et al. 2009). Widespread abandonment long distances or that have large home ranges are of agricultural land without restoration presents its better able to survive in disturbed agricultural land- own set of problems, including landscape degradation, scapes with fewer or more distant patches of natural increased risk of erosion and fire. In some areas, both habitat (Tscharntke et al. 2005). agricultural intensification and land abandonment Agricultural intensification can jeopardize many of coexist in the same landscapes, and both processes the ecosystem services provided by the landscape may influence the delivery of ecosystem services to (Matson et al. 1997). Across large areas of North agroecosystems (Stoate et al. 2009). America and Western Europe, agricultural intensifica- tion has resulted in a simplification of landscape structure through the expansion of agricultural land, 4. ECOSYSTEM SERVICES AND DISSERVICES increase in field size, loss of field margin vegetation FROM AGRICULTURE and elimination of natural habitat (Robinson & Agroecosystems are essential sources of provisioning Sutherland 2002). This simplification tends to lead services, and the value of the products they provide to higher levels of pest damage and lower populations are readily measured using standard market analysis. of natural enemies (Brewer et al. 2008; Gardiner et al. Depending on their structure and management, they 2009; O’Rourke 2010). A meta-analysis of the effects may also contribute a number of other ecosystem ser- of landscape structure on natural enemies and pests vices (MEA 2005). Ecosystem processes operating in agriculture showed that landscape complexity within agricultural systems can provide some of the enhanced natural enemy populations in 74 per cent same supporting services described above, including of cases, whereas pest pressure was reduced in more pollination, pest control, genetic diversity for future complex landscapes in 45 per cent of cases (Bianchi agricultural use, soil retention, and regulation of soil et al. 2006). Natural enemies such as predators and fertility, nutrient cycling and water. In addition, parasitoids appear to respond to landscape structure agricultural systems can be managed to support bio- at smaller spatial scales than herbivorous insects diversity and enhance carbon sequestration—globally (Brewer et al. 2008; O’Rourke 2010) and may be important ecosystem services. more susceptible to habitat fragmentation. Based on a review of 16 studies of nine crops on four continents, Klein et al. (2007) concluded that agricultural intensi- (a) Ecosystem disservices from agriculture fication threatens wild bee communities and hence Agriculture can contribute to ecosystem services, but may degrade their stabilizing effect on pollination can also be a source of disservices, including loss of services at the landscape level. Recent studies have biodiversity, agrochemical contamination and sedi- suggested that farm-level diversification is more likely mentation of waterways, pesticide poisoning of non- to influence pests and natural enemies if the wider target organisms, and emissions of greenhouse gases landscape is structurally simple, than if it is already and pollutants (Dale & Polasky 2007; Zhang et al. very complex (Tscharntke et al. 2005; O’Rourke 2007). These disservices come at a significant cost to 2010). In complex landscapes, adding farm-level humans, but there is often a mismatch between the complexity does not necessarily enhance the benefits benefits, which accrue to the agricultural sector, of pest control services. and the costs, which are typically borne by society at Agricultural intensification in the landscape can various scales, from local communities impacted by diminish other ecosystem services as well. Protection pesticides in drinking water to the global commons of groundwater and surface water quality can be threa- affected by global warming. Linking these disservices tened by intensification because of increased nutrients, more closely to agricultural activities through incor- agrochemicals and dissolved salts (Dale & Polasky porating the externalities into the costs of production Phil. Trans. R. Soc. B (2010) Review. Ecosystem services A. G. Power 2965 Table 2. Inputs and outputs of nitrogen and phosphorus in three corn cropping systems with similar yield potential: a low- input corn-based system in western Kenya; a highly fertilized wheat-corn double-cropping system in north China; and a 21 21 corn – soya bean rotation in IL, USA. Actual yields of corn were 2000, 8500 and 8200 kg ha yr per crop in the Kenya, China and USA systems, respectively; the Chinese and USA systems also yielded wheat and soya bean, respectively, in a separate cropping season. From Vitousek et al. (2009). 21 21 nutrient balances by region (kg ha yr ) western Kenya north China midwest USA inputs and outputs NP N P N P fertilizer 7 8 588 92 93 14 biological N fixation 62 total agronomic inputs 7 8 588 92 155 14 removal in grain and/or beans 23 4 361 39 145 23 removal in other harvested products 36 3 total agronomic outputs 59 7 361 39 145 23 agronomic inputs minus harvest removals 252 þ1 þ227 þ53 þ10 29 has the potential to reduce these negative environmental right time, while minimizing nutrient losses by reducing consequences of agricultural practices. soluble inorganic nitrogen and phosphorus pools (Drinkwater & Snapp 2007). Practices such as cover cropping or intercropping enhance plant and microbial (i) Nutrient cycling and pollution assimilation of nitrogen and reduce standing pools of From the local scale to the global scale, agriculture has nitrate, the form of nitrogen that is most susceptible profound effects on biogeochemical cycles and nutri- to loss. Other good management practices include ent availability in ecosystems (Vitousek et al. 1997; diversifying nutrient sources, legume intensification Galloway et al. 2004). The two nutrients that most for biological nitrogen fixation and phosphorus- limit biological production in natural and agricultural solubilizing properties, and diversifying rotations. ecosystems are nitrogen and phosphorus, and they Integrated management of biogeochemical processes are also heavily applied in agroecosystems. Nitrogen that regulate the cycling of nutrients and carbon and phosphorus fertilizers have greatly increased the could reduce the need for surplus nutrient additions amount of new nitrogen and phosphorus in the bio- in agriculture (Drinkwater & Snapp 2007). sphere and have had complex, often harmful, effects Recent analyses forecasting human alterations of on natural ecosystems (Vitousek et al. 1997). These soil nitrogen and phosphorus cycling under various anthropogenically mobilized nutrients have entered scenarios to 2050 further emphasize that closing nutri- both groundwater and surface waters, resulting in ent cycles in agroecosystems can significantly influence many negative consequences for human health and soil nutrient balance (Bouwman et al. 2009). Spatially the environment. Approximately 20 per cent of N explicit modelling of soil nitrogen and phosphorus bal- fertilizer applied in agricultural systems moves into ances suggest that soil phosphorus will be depleted in aquatic ecosystems (Galloway et al. 2004). Impacts grasslands around the world and rock phosphate of nutrient loss from agroecosystems include ground- reserves will be reduced by 36 – 64% by 2100. Many water pollution and increased nitrate levels in scenarios indicate increases in soil nitrogen over this drinking water, eutrophication, increased frequency period along with increased leaching and denitrifica- and severity of algal blooms, hypoxia and fish kills, tion losses, though nitrogen balances are likely to and ‘dead zones’ in coastal marine ecosystems decline in North American and Europe because of (Bouwman et al. 2009). ongoing changes in management practices (Bouwman Ecosystem services within agroecosystems can be et al. 2009). supported by nutrient management strategies that Other ecosystem disservices from agriculture recouple nitrogen, phosphorus and carbon cycling include applications of pesticides that result in loss of within the agroecosystem. Under conventional prac- biodiversity and pesticide residues in surface and tice in developed countries, agroecosystems are often groundwater, which degrades the water provisioning maintained in a state of nutrient saturation and are services provided by agroecosystems. Moreover, inherently leaky as a result of chronic surplus additions agriculture modifies the species identity and root of nitrogen and phosphorus (Galloway et al. 2004; structure of the plant community, the production of Drinkwater & Snapp 2007; Vitousek et al. 2009). In litter, the extent and timing of plant cover and the developing countries, soils are more likely to be composition of the soil biotic community, all of depleted and nutrients may be much more limiting which influence water infiltration and retention in to production, though chronic nutrient surpluses the soil. The intensity of agricultural production and may still occur in some systems (table 2; Vitousek management practices affect both the quantity and et al. 2009). quality of water in an agricultural landscape. Practices To maintain ecosystem services, soil nutrient pools that maximize plant cover, such as minimum tillage, can be intentionally managed to supply crops at the polycultures or agroforestry systems are likely to Phil. Trans. R. Soc. B (2010) 2966 A. G. Power Review. Ecosystem services Table 3. Agricultural contributions to global greenhouse gas emissions by source and expected changes in agricultural greenhouse gas emissions by 2030. Adapted from FAO (2003). CO carbon N O nitrous NO nitric 2 2 x greenhouse gas dioxide CH methane oxide oxides ammonia agricultural source land use change, ruminants (15%) livestock/manure biomass burning livestock/manure (estimated % contribution especially (17%) (13%) (44%) to total emissions) deforestation rice (11%) mineral manure/mineral mineral fertilizers (8%) fertilizers (2%) fertilizers (17%) biomass burning biomass burning biomass burning (7%) (3%) (11%) agricultural emissions 15% 49% 66% 27% 93% (as % total of anthropogenic sources) expected changes in stable or rice—stable or 35 – 60% from livestock— agricultural emissions decreasing decreasing increase 60% increase by 2030 livestock—60% increase Total emissions include both natural and anthropogenic sources. decrease runoff and increase infiltration. Irrigation particularly when more nitrogen is applied than can practices also influence runoff, sedimentation and be taken up by the plants. Nitrogen is added to soils groundwater levels in the landscape. through the use of inorganic fertilizers, application of animal manure, cultivation of nitrogen-fixing plants and retention of crop residues. Globally, approxi- (ii) Emissions of greenhouse gases mately 50 per cent of N applied as fertilizer is taken Agricultural activities are estimated to be responsible up by the crop, 2 – 5% is stored as soil N, 25 per for 12 – 14% of global anthropogenic emissions of cent is lost as N O emissions and 20 per cent moves greenhouse gases, not including emissions that arise to aquatic systems (Galloway et al. 2004). In addition from land clearing (US-EPA 2006; IPCC 2007). to direct N O emissions, the production of synthetic After fossil fuel combustion, land-use change is the nitrogen fertilizers is an energy-intensive process that second largest global cause of CO emissions, and 2 produces additional greenhouse gases. Flooded rice some of this change is driven by conversion to agricul- cultivation contributes to greenhouse gas emissions ture, largely in developing countries. In developed through anaerobic decomposition of soil organic countries, forest conversion to cropland, pasture and matter by CH -emitting soil microbes. The practice rangeland were common through the middle of the of burning crop residues contributes to the production twentieth century, but current conversions are of both CH and N O. 4 2 primarily for suburban development. In addition to Livestock production also contributes to CH and losses of above-ground carbon due to deforestation N O emissions (Pitesky et al.2009), and these impacts or other land clearing, conversion of natural are likely to increase through to 2050 as the demand for ecosystems to agriculture reduces the soil carbon meat increases (FAO 2003). Ruminant livestock such as pool by 30 – 50% over 50 – 100 years in temperate cattle, sheep, goats and buffalo emit CH as a regions and 50 – 75% over 20 – 50 years in the tropics byproduct of their digestive processes (enteric (Lal 2008a). Although agricultural systems generate fermentation). Livestock waste can release both CH , very large CO fluxes to and from the atmosphere, 2 through the biological breakdown of organic com- the net flux appears to be small. However, both the pounds, and N O, through microbial metabolism of magnitude of emissions and the relative importance nitrogen contained in manure. The magnitude of of the different sources vary widely among agricultural direct emissions depends strongly on manure manage- systems around the world. ment practices, such as the use of lagoons or field Agricultural activities contribute to emissions in spreading, and to some degree on the type of livestock several ways (table 3). Approximately 49 per cent of feed. The magnitude of emissions attributed to live- global anthropogenic emissions of methane (CH ) 4 stock is controversial, ranging from 3 to 18 per cent and 66 per cent of global annual emissions of nitrous of global emissions, depending on whether the effects oxide (N O), both greenhouse gases, are attributed 2 of land-clearing (i.e. deforestation) for livestock pro- to agriculture (FAO 2003), although there is a wide duction is included in the estimate (Pitesky et al. 2009). range of uncertainty in the estimates of both the agri- cultural contribution and the anthropogenic total. N O emissions occur naturally as a part of the soil (b) Ecosystem services from agriculture nitrogen cycle, but the application of nitrogen to On-farm management practices can significantly crops can significantly increase the rate of emissions, enhance the ecosystem services provided by Phil. Trans. R. Soc. B (2010) Review. Ecosystem services A. G. Power 2967 agriculture. Farmers routinely manage for greater pro- commercial production systems in Brazil and Canada visioning services by using inputs and practices to (reviewed in Govaerts et al. 2009). Many farmers increase yields, but management practices can also have already adopted practices that retain soil C in enhance other ecosystem services, such as pollination, order to achieve higher productivity and lower costs. biological pest control, soil fertility and structure, However, even the use of soil conservation and restor- water regulation, and support for biodiversity. Habitat ation practices cannot fully restore soil carbon lost management within the agroecosystem can provide the through conversion to agriculture. It is estimated that resources necessary for pollinators or natural enemies the soil C pool attainable through best management (Tscharntke et al. 2005). Many studies have identified practices is typically 60 – 70% of the original soil C the important role of perennial vegetation in support- pool prior to conversion (Lal 2008a). ing biodiversity in general and beneficial organisms Finally, agricultural land can also be used to grow in particular (e.g. Perfecto & Vandermeer 2008). crops for bioenergy production. Bioenergy, particu- Evidence suggests that management systems that larly cellulosic biofuels, has the potential to replace a emphasize crop diversity through the use of polycul- portion of fossil fuels and to lower greenhouse gas tures, cover crops, crop rotations and agroforestry emissions (Smith et al. 2008). While burning fossil can often reduce the abundance of insect pests that fuels adds carbon to the atmosphere, bioenergy specialize on a particular crop, while providing refuge crops, if managed correctly, avoid this by recycling and alternative prey for natural enemies (Andow carbon. Although carbon is released to the atmosphere 1991). Similar practices may benefit wild pollinators, when bioenergy feedstocks are burned, carbon is including minimal use of pesticides, no-till systems recaptured during plant growth. The replacement of and crop rotations with mass-flowering crops. fossil fuel-generated energy with solar energy captured by photosynthesis has the potential to reduce CO , N O and NO emissions. 2 x (i) Mitigation of greenhouse gases emissions However, calculating net emissions from bioenergy Agricultural practices can effectively reduce or offset is tricky (Searchinger et al. 2008). First, management agricultural greenhouse gas emissions through a var- practices used to grow crops and forages for bioenergy iety of processes (Drinkwater & Snapp 2007; Lal production will influence net emissions. Development 2008a; Smith et al. 2008). Effective manure manage- of appropriate bioenergy systems based on perennial ment can significantly reduce emissions from animal plant species that do not require intensive inputs waste. Replacing synthetic nitrogen fertilizers with bio- such as tillage, fertilizers and other agrochemicals logical nitrogen fixation by legumes can reduce CO have the potential to help offset fossil fuel use in agri- emissions from agricultural production by half (Drink- culture. Bioenergy systems that rely on annual row water & Snapp 2007). The process of perennialization crops such as corn are not likely to be as beneficial, and legume intensification in agroecosystems modifies and expanding these systems can dramatically reduce internal cycling processes and increases N use effi- the delivery of other ecosystem services like biological ciency within agroecosystems via the recoupling pest control (Landis et al. 2008). Second, even with mechanisms discussed above. Chronic surplus the use of perennial species and few inputs, there is sig- additions of inorganic N, which are currently com- nificant potential for higher, rather than lower, monplace, can be reduced under these scenarios, emissions attributable to bioenergy crops, resulting leading to reductions in NO and N O emissions. from land-use change as farmers respond to higher x 2 Agriculture can offset greenhouse gas emissions by prices and convert forest and grassland to new crop- increasing the capacity for carbon uptake and storage land (Fargione et al. 2008; Searchinger et al. 2008). in soils, i.e. carbon sequestration (Lal 2008a,b). The The production of bioenergy from waste products, net flux of CO between the land and the atmosphere such as crop waste, fall grass harvests from reserve is a balance between carbon losses from land-use con- lands, or even municipal waste, could avoid land-use version and land-management practices, and carbon change and result in lower CO emissions. gains from plant growth and sequestration of decom- posed plant residues in soils. In particular, soil conservation measures such as conservation tillage 5. TRADEOFFS and no-till cultivation can conserve soil carbon, Several studies have explicitly analysed possible trade- and crop rotations and cover crops can reduce the offs between the supply of various ecosystem services degradation of subsurface carbon. In general, water from agricultural systems. In general, ecosystem ser- management and erosion control can aid in maintain- vices are not independent of one other and the ing soil organic carbon (Lal 2008a). relationships between them are likely to be highly non- Soil carbon sequestration thus provides additional linear. For agriculture, the problem is typically posed ecosystem services to agriculture itself, by conserving as a tradeoff between provisioning services—i.e. pro- soil structure and fertility, improving soil quality, duction of agricultural goods such as food, fibre or increasing the use efficiency of agronomic inputs, bioenergy—and regulating services such as water puri- and improving water quality by filtration and denatur- fication, soil conservation or carbon sequestration ing of pollutants (Lal 2008b; Smith et al. 2008). The (MEA 2005). Cultural services and biodiversity con- economic benefits of conservation agriculture have servation are also often viewed as tradeoffs with been estimated in diverse systems around the world, production. from smallholder agricultural systems in Latin Tradeoffs among ecosystem services should be con- America and sub-Saharan Africa to large-scale sidered in terms of spatial scale, temporal scale and Phil. Trans. R. Soc. B (2010) 2968 A. G. Power Review. Ecosystem services reversibility (Rodriguez et al. 2006). Are the effects of agroecosystems to support many ecosystem services the tradeoff felt locally, for example on-farm, or at a while still maintaining or enhancing the provisioning more distant location? How quickly does the tradeoff services that agroecosystems were designed to pro- occur? Are the effects reversible and if so, how quickly duce. Sustainable intensification will depend on can they be reversed? Management decisions often management of ecosystem processes rather than focus on the immediate provision of a commodity or fossil fuel inputs (Baulcombe et al. 2009). service, at the expense of this same or another ecosys- Futures scenarios are an increasingly common tool tem service at a distant location or in the future. As used to evaluate tradeoffs between commodity pro- either the temporal or spatial scale increases, tradeoffs duction, ecosystem services and the conservation of become more uncertain and difficult to manage. biodiversity in various ecosystems, including agroeco- Management is further complicated by biophysical systems (MEA 2005). In addition, advances in and socioeconomic variation, since every hectare of a spatially explicit modelling have greatly improved the given habitat is not of equal value in generating a ability to estimate the production of ecosystem services given ecosystem service (Nelson et al. 2009). For natu- from landscapes. Analysis of the provision of agricul- ral ecosystems, habitat quality, size of unit and spatial tural goods and other ecosystem services in an configuration are likely to influence the services agricultural valley in Oregon, USA, found few trade- provided by the ecosystem. For agroecosystems, man- offs between ecosystem services and biodiversity agement practices, along with access to market and conservation (Nelson et al. 2009). The spatially expli- patterns of trade are likely to be critical to the pro- cit modelling tool InVEST (integrated valuation of vision of ecosystem services. Furthermore, the values ecosystem services and tradeoffs—Tallis & Polasky of both market and non-market goods and services 2009) was used to evaluate three stakeholder-defined will vary according to various biophysical and socio- scenarios of land use through to 2050, including cur- economic factors. Without information on the factors rent land-use patterns, increased development or that influence the quantity and value of ecosystem ser- increased conservation. The models predicted changes vices, it is difficult to design policies, incentives or in commodity production, biodiversity conservation payment schemes that can optimize the delivery of and ecosystem services (hydrological services, soil con- those services (Nelson et al. 2009). servation and carbon sequestration) under the three Ecosystem services are provided to agriculture at scenarios. In general, scenarios that scored high on varying scales, and this can influence a farmer’s incen- delivering ecosystem services also scored high on tives for protecting the ecosystem service. Farmers biodiversity conservation. Scenarios with increased have a direct interest in managing ecosystem services development had higher commodity values and lower such as soil fertility, soil retention, pollination and levels of conservation and ecosystem services, but pest control, because they are provided at the field this tradeoff disappeared when payments for carbon and farm scale. At larger scales, benefits are likely to sequestration were included. Other spatially explicit accrue to others, including other farmers, in addition studies have also found that biodiversity conservation to the farmer providing the resource. A farmer who and carbon sequestration can be achieved in agricul- restores on-farm habitat complexity increases pollina- tural landscapes (Eigenbrod et al. 2009). Clearly, tion and pest control services to her neighbours as more detailed studies like these are needed to reach well as herself. The neighbours benefit from these a conclusion about the ecological and economic services without having to give up land that would conditions that may lead to tradeoffs between otherwise produce crops and generate income. Greater agricultural production and ecosystem services. landscape complexity may be considered a common pool resource, and a farmer, acting alone, may lack the incentive to set aside the optimal amount of habitat (a) Future trends for both the farmer and the neighbour (Zhang et al. Current FAO projections suggest that the rate of con- 2007). version of forested land to agriculture will continue to Recent studies suggest that tradeoffs between agri- slow through to 2050, there will be little change in cultural production and various ecosystem services grazing area, and protected areas will increase (FAO are not inevitable and that ‘win – win’ scenarios are 2003, 2006). Increases in protected areas will assist possible. An analysis of yields from agroecosystems in maintaining the flow of ecosystem services like around the world indicates that, on average, agricul- water provisioning, pollination and biological control tural systems that conserve ecosystem services by to agriculture. Advances in sustainable agriculture in using practices like conservation tillage, crop diversifi- developed countries should also lead to enhanced eco- cation, legume intensification and biological control system services in agricultural landscapes. In some perform as well as intensive, high-input systems regions, however, conversion of land to urbanization (Badgley et al. 2007). The introduction of these is expected to increase dramatically and will put sig- types of practices into resource-poor agroecosystems nificant stress on the availability of agricultural land in 57 developing countries resulted in a mean relative and protected areas. At the global scale, the growth yield increase of 79 per cent (Pretty et al. 2006). In of demand for all crop and livestock products is pro- these examples, there was no evidence that the pro- jected to be lower than in the past: 1.5 per cent per visioning services provided by agriculture were annum in the period 2000 – 2030 and 0.9 per cent jeopardized by modifying the system to improve its for 2030 – 2050 when compared with rates around ability to provide other ecological services. These 2.1 – 2.3% in the preceding four decades, in part due analyses suggest that it may be possible to manage to the lower population growth (FAO 2006). Phil. Trans. R. Soc. B (2010) Review. Ecosystem services A. G. Power 2969 Despite slowing demand growth, ecosystem maximizing synergies. 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Philosophical Transactions of the Royal Society B: Biological SciencesPubmed Central

Published: Sep 27, 2010

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