An ecosystem services framework to support bothpractical conservation and economic developmentHeather Tallis*†, Peter Kareiva‡, Michelle Marvier§, and Amy Chang¶

*Department of Biology and Natural Capital Project, Woods Institute for the Environment, Stanford University, Stanford, CA 94305;‡The Nature Conservancy, 4722 Latona Avenue NE, Seattle, WA 98105; §Environmental Studies Institute, Santa Clara University, SantaClara, CA 95053; and ¶The Nature Conservancy, Santa Clara, CA 95053

Edited by Gretchen C. Daily, Stanford University, Stanford, CA, and approved February 8, 2008 (received for review October 5, 2007)

The core idea of the Millennium Ecosystem Assessment is that the human condition is tightly linked to environmental condition. Thisassertion suggests that conservation and development projects should be able to achieve both ecological and social progress with-out detracting from their primary objectives. Whereas ‘‘win–win’’ projects that achieve both conservation and economic gains are acommendable goal, they are not easy to attain. An analysis of World Bank projects with objectives of alleviating poverty and pro-tecting biodiversity revealed that only 16% made major progress on both objectives. Here, we provide a framework for anticipatingwin–win, lose–lose, and win–lose outcomes as a result of how people manage their ecosystem services. This framework emergesfrom detailed explorations of several case studies in which biodiversity conservation and economic development coincide and casesin which there is joint failure. We emphasize that scientific advances around ecosystem service production functions, tradeoffsamong multiple ecosystem services, and the design of appropriate monitoring programs are necessary for the implementation ofconservation and development projects that will successfully advance both environmental and social goals. The potentially brightfuture of jointly advancing ecosystem services, conservation, and human well-being will be jeopardized unless a global monitoringeffort is launched that uses the many ongoing projects as a grand experiment.

poverty alleviation � pro-poor conservation � sustainable management

Poverty and environmental problemsare both children of the samemother, and that mother isignorance.

Ali Hassan Mwinyi,Tanzanian President in 1998

The Millennium Ecosystem As-sessment (MA) contains a com-pelling argument that humanwell-being depends on the ser-

vices provided by nature, and that theseservices have recently become so imper-iled that we can expect negative feed-backs to people (1). In some ways thereis nothing new in this message: peopledepend on nature, and people too oftendamage nature, thereby endangeringtheir own health and well-being. Thenovel contribution of the MA is itschampioning of a new scientific focus, afocus on understanding how nature pro-duces a wide array of ecosystem ser-vices, quantifying the rate and value ofthe delivery of these services, and mod-eling the connections between ecosys-tem services, human welfare, andeconomic systems (2).

Although the MA was a bold contri-bution that exposed huge gaps in thescience of ecosystem services, the realityis that both the conservation and eco-nomic development communities haveembraced ecosystem services for at leasta decade, without explicitly labelingthem as such. This melding of conserva-tion and development comes from twodistinct agendas: conservationists whoseek to increase public support forbiodiversity protection by integratingeconomic development, and develop-

ment agencies that seek to also providefor the stewardship of nature under themantra of sustainable development.These projects have variously been cate-gorized as integrated conservation–development projects, community-basednatural resource management, and,more recently, pro-poor conservation(3). Although these projects generallylack a formal foundation of ecosystemservice science, they all are motivatedby the general hypothesis that natureprovides humans with benefits. In fact,an analysis of the vision and missionstatements of major environmental or-ganizations, including the major conser-vation nongovernmental organizations(NGOs), found that nature is typicallyportrayed as resources necessary for hu-man well-being and sustainable develop-ment (4). Increasingly, the languageused by conservation NGOs to discussthe value of nature is becoming moreexplicit in its reference to ecosystemservices. Examining the web domains offour major conservation NGOs (Conser-vation International: http://conservation.org; The Nature Conservancy: www.nature.org; Wildlife ConservationSociety: http://wcs.org; and World Wild-life Fund: www.worldwildlife.org), wefound that, on average (�1 SE), 7.8 �1.3% of the pages that mention biodi-versity also specifically mentioned oneor more of the following terms: humanwelfare, ecosystem service(s), humanwell-being, drinking water (Googlesearch engine; August 23, 2007). Thus,the conservation community assumes aconnection between nature and human

well-being and increasingly designsprojects in terms of the provision ofecosystem services.

An Unclear Record for Projects that SeekBoth Conservation andPoverty AlleviationThere is no question that ecosystem ser-vices are now a focus for both scientistsand conservationists, but interest andwidely held beliefs do not necessarilymean that data and results support thefeasibility of helping both people andbiodiversity by maintaining ecosystemservices. What lessons have beenlearned from the many projects alreadyconducted by conservation NGOs inwhich efforts have been made to bothimprove human well-being and protectbiodiversity? Answers are not as forth-coming as one would hope. For exam-ple, in the most thorough systematic re-view we know of regarding conservationprojects, researchers were stymied bythe lack of metrics of success for eitherconservation or poverty alleviation (5).Indeed, the major conclusion of this re-view was that projects tended to rely onoverly simplistic definitions of bothbiodiversity and poverty, and few

Author contributions: H.T., P.K., and M.M. designed re-search; H.T., P.K., M.M., and A.C. performed research; H.T.,P.K., M.M., and A.C. analyzed data; and H.T., P.K., and M.M.wrote the paper.

The authors declare no conflict of interest.

This article is a PNAS Direct Submission.

†To whom correspondence should be addressed. E-mail:htallis@stanford.edu.

© 2008 by The National Academy of Sciences of the USA

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projects directly examined the causalrelationships responsible for the out-comes observed.

Arguably, the most consistently col-lected data regarding projects that seekimprovements in human well-being andthe environment (or biodiversity) arefound in the records of the WorldBank. Of the 11,155 economic develop-ment projects carried out by the WorldBank since 1947 (www.worldbank.org;accessed December 17, 2007; limited toclosed and active projects with an ap-proval date listed), 17.6% have had‘‘environment and natural resourcesmanagement’’ as a major theme. Froma conservation perspective, it is note-worthy that 20% of the World Bank’senvironmentally oriented projects havespecifically included biodiversity pro-tection as a theme (Fig. 1). Moreover,the attention to biodiversity has beengrowing over the last 20 years, nearlyquadrupling in frequency (Fig. 2).Thus, the World Bank has two decadesof experience supporting projects withthe dual goal of economic developmentand biodiversity protection (6). In ad-dition, the World Bank uses a categori-cal scoring system by which it judgesthe degree to which each completedproject achieved its stated goals. Onecan imagine three general categories ofoutcome for projects with both biodi-versity goals and economic develop-ment or poverty alleviation goals:win–win (both goals are met), lose–lose (neither goal is met), and win–lose(only one of the goals is met). Wesearched the World Bank database forprojects that (i) were approved be-tween 1993 and 2007, (ii) listed biodi-versity as a theme, (iii) had availablean Implementation Completion Report

written between July 1998 and August2006 (when the format was consistent),and (iv) stated environmental and pov-erty alleviation goals and outcomes.We found that relatively few, only fiveof 32 projects (16%), had substantialgains in terms of their stated environ-mental and poverty alleviation out-comes (Fig. 3). Thus, it is not impossibleto make gains on both biodiversity andpoverty fronts, but it is not easy. It isnoteworthy that nearly half of the WorldBank projects with biodiversity protec-tion as a major goal had no objectivesfor poverty alleviation, which precludedthem from being in our examination ofwin–win frequency.

Unfortunately, this simple tally ofWorld Bank scores cannot reveal whatstrategies or factors tend to lead to fail-ure. Failures could be caused by poorproject design or intrinsic tradeoffs be-tween ecosystem services. For example,development of more productive agricul-ture, which is often a route by whichrural poverty is alleviated (7), may inex-orably harm biodiversity. Alternatively,failures may be driven by external prob-lems such as civil conflict or weak gov-ernance that were not anticipated inproject design and have nothing to dowith ecosystem services. Understandingthe factors that determine the outcomeof projects with dual biodiversity andeconomic development goals is crucial.One path to understanding these out-comes is to develop a framework forassessing the connections between eco-system services and economic develop-ment on a project-by-project basis andsuggest indicators and metrics that couldincrease the likelihood of win–winoutcomes.

A Framework for Analyzing EcosystemService Projects Aimed at HumanWell-Being and Biodiversity ProtectionA number of authors have recently ar-gued that there are strong links betweenecosystem services and sustainable de-velopment, particularly development ef-forts that aim to reduce rural poverty(8–10). We see two distinct routes bywhich the science of ecosystem servicescan contribute to both nature conserva-tion and sustainable development. First,a thorough accounting of ecosystem ser-vices and a better understanding of howand at what rates ecosystems producethese services can be used to motivatepayment for nature conservation. Atleast part of the generated funds can beused to compensate people who sufferlost economic opportunities to protectthese services. For example, if ruralpoor are asked to take actions that re-duce farm productivity to protect andregulate water supply, those farmerscould be compensated for the reducedproductivity they experience. When thebenefits of natural ecosystems are ex-plicitly quantified, those benefits aremore valued both by the people whodirectly interact with the ecosystems andthe governmental and other agenciesthat would have to pay for substitutesources of these services if these ecosys-tems should become impaired. Appreci-ating the value of ecosystem servicescan motivate increased conservation in-vestment to prevent having to pay forsubstitutes later. This approach could becharacterized as a ‘‘government invest-ment’’ approach because the paymentswill generally come from beneficiariesoutside of the local area, and a govern-mental or other agency is typicallyresponsible for collecting and redistrib-uting the funds.

Second, a focus on the conservationof ecosystem services could improve thesuccess of projects that attempt to bothconserve nature and improve the wel-fare of the rural poor by fostering mar-kets for the goods and services thatlocal people produce or extract fromecosystems. These projects could becharacterized as more ‘‘community-based’’ because the goal is to foster themore organic, or grassroots, develop-ment of cottage industries, such as eco-tourism, or the production of bushmeator nontimber forest products, that areenhanced by better protection of localecosystems.

Using this framework, we discuss thefactors that may have contributed tofailure or success for several projects(Table 1). The scale of our analysis islocal or project level. Often the hyper-bole of ‘‘pro-poor conservation’’ might

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Fig. 1. Shown are the percentage of projects listing each environmental subtheme for the 1,961 WorldBank projects with a major theme of environment and natural resources management (ENRM) and anapproval date. The percentages sum to �100, because nearly half of the ENRM projects listed more thanone environmental subtheme. A maximum of five major themes or subthemes can be listed for eachproject.

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be mistaken for a claim that conserva-tion is a global strategy for povertyalleviation. It is not (11). The plight ofurban poor and many of the world’spoor has little to do with the productionfunctions of ecosystem services. But forrural poor, at the local level, the statusof ecosystem services can make a bigdifference in their daily lives.

Government Investments inEcosystem ServicesWhen there is clear information thatecosystem services of obvious value (likeclean water or flood control) are imper-iled, governments often invest in theirprotection. The money for these invest-ments may come from charging benefi-ciaries for the use of ecosystem services,such as clean water, and then using thepayments either to improve enforcementof protected areas or to compensatethose whose livelihoods are diminishedby the conservation efforts (12). Thesearrangements typically involve paymentsfrom beneficiaries outside of the imme-diate area. Here, we highlight twoprojects that demonstrate how ecosys-tem services can be used to motivatepayment for nature conservation.

The Quito Water Fund. Quito, the capitalcity of Ecuador, houses 1.8 million peo-ple in a region of extremely high biolog-ical diversity and endemism. In the moststrained regions around Quito, 63% ofwater needs are not met, and in 1999,most of the city’s 14 monitored water-sheds flowed with undrinkable water.The Condor Biosphere Reserve, situatedupstream of Quito, has the potential toalleviate social struggles around waterresources and environmental strugglesaround biodiversity loss. However, en-forcement of park restrictions was weak,

and unsustainable land use practicessurround the reserve, leading to con-tinuing declines in biodiversity and wa-ter quality.

In 2000, The Nature Conservancy incollaboration with the U.S. Agency forInternational Development worked toestablish a water fund that directsmoney from water users to improve pro-tection of the Condor Biosphere Re-serve (12). In 2004, the fund was worth$2.1 million, paid into by the Quito Mu-nicipal Water and Sewage Agency, theQuito Electricity Company, and theAndina Beer Company (12). In thiscase, the government and its municipalutilities chose to redirect current feesand taxes rather than raise the price ofwater.

The project reports successes on bothsocial and ecological fronts. The nearly$5 million raised for conservation actionhave been used to plant 3.5 milliontrees, hire nine new park guards thatprovide new jobs and increase enforce-ment, build local capacity for monitor-ing and conflict resolution, fund hydro-logic modeling and monitoring, andprovide environmental education tochildren (12). Financial support for con-servation came not from individualsconcerned about biodiversity or someparticularly charismatic species on theverge of extinction. Rather the supportcame from an appreciation of the rolehealthy forests play in supplying andregulating the availability of clean water.A key to the success of this project mayhave been a long record of flow andsedimentation monitoring data collectedby hydropower operations, which pro-vided a clear signal of a degrading eco-system service before any catastrophicevent.

Payment for Ecosystem Services in China.The government of China has imple-mented several payment for ecosystemservice programs. One of the betterknown is the Sloping Land ConversionProgram. This program was motivatedby large floods on the Yangtze River in1999 that many presume were worsenedby sedimentation that has reduced theflood mitigation potential of dams onthis river. The State Forestry Adminis-tration linked sedimentation to erosionfrom intensively farmed sloping lands inthe upper reaches of the watershed.

The Sloping Land Conversion Pro-gram, also known as the Grain toGreen Program, pays farmers in cashor grain to abandon farming and re-store forests on steep slopes along keyrivers (refs. 13 and 14 and www.forest-trends.org/documents/publications/ChinaPES%20from%20Caro.pdf). TheState Forestry Administration runs thisprogram and projects that 14.6 millionhectares in 24 provinces will be im-proved through this program by 2010(13). The upper watershed regions tar-geted by this program are often home tosome of the most socially marginalizedminority groups in the country, coinci-dentally allowing social, economic, andecological benefits to flow from thisprogram.

To date, payments for ecosystem ser-vices in this and other programs havecome primarily from China’s centralgovernment. In 2004, 92% of the accu-mulated value of the Sloping Lands Pro-gram ($7.6 billion) was provided by thenational government. It is expected thatthe high costs of the program will soonspur the development of privatelyfunded payment schemes (14). As withthe Quito Water Fund, this programwas not motivated by biodiversity, butrather by interests in ecosystem servicessuch as flood mitigation. If China hadnot suffered severe floods in 1999 it isunlikely that the Sloping Lands Programwould have been launched; there firstneeded to be strong evidence of a con-nection between land use and degradedecosystem services.

Aligning Conservation of EcosystemServices with Local Economic ActivityMany early projects that integratedconservation and development used eco-tourism, which offers market-based in-come and a natural alliance betweenconservation of an ecosystem serviceand economic development. Participantsin these programs typically receive fundsdirectly from corporations or others inthe private sector, rather than fromgovernments or nongovernment organi-zations. Here, we briefly outline two

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Fig. 2. For the 1,961 World Bank projects with the ENRM major theme, the percentage of projects witha pollution and environmental health theme has remained flat or declined, whereas the percentage ofprojects with subthemes of biodiversity and/or climate change has increased. The numbers of projects withthe ENRM theme are: 1983–1989, 116; 1990–1994, 417; 1995–1999, 493; 2000–2004, 521; and 2005–present, 414.

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programs that have successfully takenthis approach.

The Il’Ngwesi Ecolodge. In Kenya, theMaasai culture and highly diverse bio-logical communities have been underthreat from the same forces: cattle rus-tling and poaching, alongside pressurefrom the government to subdivide anddevelop land (15). Subdivision wouldhave led to the end of pastoral life forthe Maasai and fragmentation of someof the largest remaining tracts of wild-life habitat in Kenya. In 1995, 8,000members of a Maasai community atIl’Ngwesi agreed to establish anecolodge and promote tourism (15). Asa result, security in the region has in-creased, income from the ecolodge isfunding the local school, poaching hasbeen halted, 13 of the region’s 19 largemammals (including the endangeredGrevys zebra) have returned to the area,and some wildlife populations have in-creased by as much as 500% (15). Obvi-ously all ecotourism projects do not turnout so well, with failures commonly oc-curring because of either poor businessplanning or poor ecological manage-ment. Nonetheless, ecotourism is wellestablished as a joint development andconservation strategy, and the world’stwo largest conservation NGOs (WorldWildlife Fund and The Nature Conser-vancy) have developed special planningprocesses to help their field staffs pro-mote ecotourism (16, 17).

Namibia’s Conservancy Program. In manycases, ecotourism markets are not easilyaccessible because of regulatory struc-

tures or entry costs. Some integratedconservation and development projectshave found success in reducing thesebarriers by granting local control of themanagement of biological resources tocommunities or individuals. In Namibia,a global biodiversity hotspot (the CapeFloristic region) overlaps with highhunting and poaching pressure, highpoverty, and socially marginalized popu-lations of indigenous people. Game pop-ulations have declined, large-scale ani-mal migrations have ceased, and blackrhino populations have plummeted (18).As part of the institutional change asso-ciated with Namibia’s independence, theNature Conservation Act was passed in1996. The World Wildlife Fund becameinvolved in supporting communities whowanted to enter into a ‘‘conservancyprogram’’ established by the act.

Enrollment in the program gives com-munities rights, for the first time, tohuntable game and revenues from gameproducts and tourism (18). The act hasfundamentally changed the landscape inNamibia. More than 60 communitiesnow participate, supporting 31 conser-vancies that cover some 70,000 km2, or17% of Namibia’s land area (18). In thiscase, new revenue streams were createdby opening access to existing interna-tional markets.

Again, this project has been a successon both social and ecological fronts.Many of the conservancies are on landsthat now act as corridors between pro-tected areas (18). Wildlife populationshave increased dramatically on conser-vancy lands. Namibia now houses theworld’s largest free-roaming black rhino

population and game species such aselephants, zebra, oryx, and springbokhave increased 600% in some places(18). For the first time in 30 years, sea-sonal migrations have resumed betweenBotswana and Namibia. The programwas a major development success, withlocal incomes increased by a total of$2.5 million in 2004 and Namibia’s netnational income up by $9.6 million (18).Overall, 3,250 part-time and 547 full-time jobs were created, and the fact thatthe majority of these jobs were obtainedby women meant that gender equity wassubstantially improved (18).

Projects that Failed to AdvanceConservation and DevelopmentThe case studies described above indi-cate that both conservation and en-hancement of human well-being can beaccomplished as part of one project. Itis important, however, to ask about fail-ures. Failures are quite common. In arandom sample of 194 ImplementationCompletion Reports for World Bankprojects, 16% were judged to be unsatis-factory or highly unsatisfactory overallperformance. Political or economic fac-tors outside the control of the projectfrequently contribute to their failure(Table 1). It would be extremely foolishto neglect the influence of externalforces and global markets and corrup-tion and governance on the ability ofecosystem service projects to enhancehuman well-being. Here, we describetwo examples of projects that havefailed on both environmental and pov-erty alleviation fronts.

West African Wildlife Project. Like Nami-bia’s Conservancy Program describedabove, the West Africa Pilot Community-based Natural Resources and WildlifeManagement Project sought ‘‘a commonsolution to both development and con-servation concerns by involving localcommunities in the sustainable, profit-able exploitation of wild resources andassisting them to manage their wild landareas for their own economic benefitand for the benefit of biodiversity.’’This, however, is an example of an ef-fort that failed to achieve both its bio-diversity and development goals (19).Supported by the World Bank and initi-ated in 1995, the project faced manydifficulties including an initially very lowlevel of training among villagers, adeeply rooted mistrust of central gov-ernment within local governing bodies,and the resumption in 2004 of civil con-flict in one of the participating nations,Cote D’Ivoire.

The project’s antipoaching programfailed because of the lack of a legal ba-sis for villagers to apprehend poachers;

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Fig. 3. The World Bank database was searched for projects that (i) were approved between 1993 and2007, (ii) listed biodiversity as a theme, (iii) had available an Implementation Completion Report writtenbetween July 1998 and August 2006 (when the format was consistent), and (iv) stated environmental andpoverty alleviation goals and outcomes. A total of 32 projects were found. Projects rated as having highor substantial achievement of environmental and/or poverty alleviation outcomes are considered to havemade a gain, whereas those rated as having modest or negligible achievement are considered to havemade no gain.

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insufficient investment in high-qualityweapons, which put village teams at amajor disadvantage in conflicts withpoachers; and insufficient investment ina communications infrastructure, whichcaused slow response times. Moreover,weak and incomplete implementation ofecological and sociological monitoringmade it impossible to assess what wasworking or not working. In the end,there was no compelling evidence thatthe wildlife or the local villages hadbenefited from the project, and therewas anecdotal evidence that poachingand livestock encroachment had re-sumed in wildlife zones.

Shrimp Aquaculture in Former MangroveForests. The clearing of coastal man-grove forests for shrimp aquaculture incoastal regions of Asia provides another

example of a lose–lose situation inwhich neither people nor nature bene-fited from a well intentioned project.The original idea of a project subsidizingshrimp aquaculture in Andhra Pradesh,India was to create economic opportu-nity for local communities throughshrimp farming, which can be enor-mously profitable. Unfortunately, theclearing of mangroves for shrimp farmscan have negative impacts on the envi-ronment and the industry itself.

In many parts of the world, includingAndhra Pradesh, shrimp aquaculture isdone with the shrimp species Penaeusmonodon (20). Because it is difficult tobring this species to reproductive matu-rity in captivity, hatcheries rely on wildbroodstock to maintain production (20).The wild shrimp populations, in turn,rely on mangrove habitats. Thus, the

ecology of the farmed species sets up aconflict between shrimp pond develop-ment, which is largely done by clearingmangroves, and shrimp production,which requires mangrove habitat for theprovision of wild broodstock.

Overdevelopment of the shrimp in-dustry in the Andhra Pradesh region haspoised both economic and ecologicalsystems on the brink of collapse. Thearea’s 61 hatcheries are suffering from awidely fluctuating market with alternat-ing low demand and limited supplies ofbroodstock (20). In fact, broodstock areat times so rare in this region that theprice for a single reproductive femaleshrimp can be as high as $2,000 (20). Acareful assessment of the ecological andeconomic capacity of the system forshrimp production could have identifiedthe optimal number of farms the region

Table 1. Examples of projects that have used ecosystem services to advance both conservation and development orpoverty alleviation

Project Conservation Development/poverty alleviation

SuccessesQuito’s Water Fund 3.5 million trees planted Alternative income, nine new jobs

Nine park guards added EducationHydrology monitoring program started Clean water

Conflict resolution trainingTechnical capacity building

China’s Sloping Lands Program 14.6 million hectares reforested (2010) Alternative incomeTargeted ethnic minority groupsFlood control

Kenya’s Il’Ngwesi Ecolodge Increasing wildlife populations Alternative incomePoaching controlled Way of life

Education (school funded)Security (poaching controlled)

Namibia’s Conservancy Program Increasing wildlife populations Property rightsOvergrazing controlled IncomeLandscape connectivity improved Cultural equality

Gender equalityWay of life

South Africa’s Cape Peninsula BiodiversityProject

Invasive plant eradication Improved infrastructureAntelope species reintroduction IncomeIncreasing raptor populationsEstablishment of protected area

FailuresWest African Wildlife Project Poaching Insufficient legal power

Livestock encroachment Insufficient communication infrastructureNo monitoring Civil unrest

Insufficient capacityGovernmental distrust

India’s Shrimp Aquaculture DevelopmentProgram

Habitat destruction Unsustainable jobsOverharvest Unstable market

Azov-Black Sea Corridor Program Unenforced protected areas Insufficient legal powerUnsustainable agriculture Uninformed agricultural practicesHabitat destruction Dysfunctional environmental institutions

Kerinci Seblat Conservation andDevelopment Project

Poaching and wildlife decline Insecure land tenureAgriculture encroachment Insufficient infrastructureLogging threat Unsustainable agriculture and nontimber forest

products harvestHabitat destruction and fragmentation Weak and uncoordinated governance

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could support at maximum capacity andlow broodstock prices. Operating at thisoptimal level would have saved subsidyfunds that were used to develop thefarms, provided sustainable jobs for theregion, and retained more of the naturalmangrove habitat that is key to stormprotection (21) and the provision ofother ecosystem services. This projectfailed in large part because the myriadservices provided by intact mangroveecosystems, and the tradeoffs amongthese services, were not fully appreciated.

Scientific Understanding that CouldImprove the Likelihood ofWin–Win OutcomesProjects that use ecosystem services tosimultaneously advance conservationand human agendas could benefit fromimproved scientific understanding offour key overriding issues: sustainableuse of ecosystem services, tradeoffsamong different services, the spatialf lows of services, and economic feed-backs in ecosystem service markets. Bet-ter quantification of ecosystem serviceswill reduce the transactional costs ofpolicies based on ecosystem services,will promote greater equity, and reducethe risk of unintended consequences orsurprises. Better quantification of eco-system services can also help to identifythose situations where the economicbenefits are sufficiently large to counter-balance money that can be made fromillegal abuses of an ecosystem (such aspoaching or illegal timber harvest).

Any time a human endeavor seeks toderive something of value from our nat-ural world, there is the possibility thatoveruse or overexploitation could resultin failure. One of the most basic princi-ples of ecology is the notion of a maxi-mum sustainable yield (MSY) derivedfrom intermediate levels of use. If thislevel of use is exceeded, the ecosystemor natural resource is degraded andboth nature and humans lose (22). Oneimportant lesson from the MSY conceptis that levels of extraction that providemeaningful amounts of income may befeasible only under particular ecologicalconditions. Consider, for example, aproject similar to the conservancy pro-gram in Namibia that aims to increaselocal income and wildlife populations byencouraging a relatively low level of le-gal trophy hunting of kudu (Tragelaphusstrepsiceros), a large antelope. If the lo-cal kudu population has a low popula-tion growth rate, even a very low levelof hunting (ecosystem service use) couldlead to a decline in the population anda lose–lose outcome. Alternatively, thesame project could provide a win–winsituation if it were initiated in an areawhere the kudu population has a high

growth rate. Because the success of aproject depends to a large extent on thestarting conditions and use levels, anygiven strategy will not be equally effec-tive in all places. Further, it is relativelytrivial to show that extreme impactsarise from extreme actions, but we lackthe ecological production functions thatquantify the impacts of more incremen-tal changes. For example, it is well un-derstood that total deforestation yieldserosion, impaired water quality, and di-minished flood control, but we do nothave the ability to predict how the pro-vision of these same services would beaffected by 10% versus 20% deforesta-tion (23). Given the extensive literaturedescribing dramatic changes in ecosys-tem function in response to such thingsas complete deforestation or extremerunoff of fertilizers into waterways, weshould be able to design projects thatavoid such severe consequences. What isnot well understood is how one mightpinpoint the extent to which a resourcecan be exploited without pushing anecosystem over its tipping point.

Most real-world conservation, devel-opment, and ecosystem service projectshave paid attention to only a select fewservices that represent a narrow slice ofthe full spectrum provided by nature.Other services also deserve the atten-

tion of both conservation and develop-ment agencies. For instance, habitat lossand landscape change are documentedto have played a major role in the in-creased prevalence of vector-borne dis-eases such as Lyme disease (24), WestNile virus, Chagas disease, and tickborne encephalitis. Although claims arecommonly made about human healthbenefits from well managed natural sys-tems (25), no conservation projects haveyet taken advantage of our growing un-derstanding of the link between land-scape change and human diseases orhealth. Also largely absent from on-the-ground ecosystem service projects areany of the supporting services such assoil formation, nutrient cycling, and pol-lination. We must simultaneously con-sider multiple ecosystem services andmultiple production functions, not justto obtain a more complete understand-ing of the benefits and losses, but be-cause any one ecosystem service mightbe related, either positively or nega-tively, to other services (26, 27). Forexample, developing ecotourism canbring income to local communities andthis added revenue could foster im-proved community stewardship of thenatural features that attract ecotourists(e.g., biodiversity for wildlife viewing orsports fisheries), providing a win–win

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Fig. 4. ‘‘Tradeoff flowers’’ depicting alternative scenarios for ecotourism projects aimed at biodiversityprotection and economic growth. (a) Unrestrained ecotourism can lead to infrastructure and humantraffic that degrades many ecosystem services, and ecotourism itself collapses. (b) Ecotourism developswith good management of biodiversity and ecosystem services, so that income flows from tourism,biodiversity is enhanced, and ecosystem services are not lost. (c) Ecotourism develops and biodiversity isprotected in nature reserves, but the increase in roads and hotels undermines water quality and fisheries,causing tradeoffs among ecosystem services and development. Which outcome is realized is largely amatter of a good management plans and making sure the intensity of human use is not too high.

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situation for nature and people (Fig.4b). On the other hand, excessive devel-opment of infrastructure to supporttourism, or excessive tourism activitiessuch as hiking and fishing, can cause thedecline of the very resources touristsseek to enjoy, resulting in a lose–losesituation (Fig. 4a). For instance, rapiddevelopment of trekking in Nepal hasresulted in unsustainable overharvest offirewood for cooking, thereby damaginglocal ecosystems (28). Exactly how peo-ple manage ecosystems as they increasethe intensity of use in any natural sys-tem can result in win–win, lose–lose, ortradeoff outcomes (Fig. 4c). Althoughscientists are now vigorously examiningmultiple ecosystem services, the practiceof conservation is still almost entirelydesigned to focus on one service at atime. Interlocking production models ofthe full suite of ecosystem services areneeded.

If policy and financial incentives forconservation of ecosystem services areto be successful and equitable, we willalso need a solid scientific understand-ing of how services flow from one re-gion to another, what human groupsbenefit from ecosystem services, andwhat groups or populations would needto be compensated for protecting thoseservices. The science of ecology madehuge advances when it began to con-sider dispersal and the importance ofmovement in governing the dynamics ofecological communities (29). However,the science of ecosystem services hasnot yet made this transformation, and asa result typically depicts ecosystem ser-vices as site-bound on static maps (ref.30 and www.nj.gov/dep/dsr/naturalcap).Only when we have the scientific foun-dation to map the flows of ecosystemservices, can we hope to meld conserva-tion with delivering benefits to the poor-est of the poor.

In addition to ecosystem services,there are economic feedbacks to con-sider. Market expansion can affectprices, and there are often feedbacksbetween economic development, socialchange, and environmental condition.We see the challenges of dealing withthese complexities even in the exampleswe have outlined as successes. As supplyin any product increases, prices arelikely to fall. Because the goal of theseprojects is not to achieve an efficientmarket, but rather to encourage a liveli-hood that is good for nature and people,low prices may cause failure. For in-stance, low prices for hunting andtourism in Namibia may make theselivelihoods insufficient for well-being,and landowners may turn back to do-mestic livestock rearing or other moredestructive practices. The Namibian gov-ernment may want to limit the numberof communities that can participate inthe program so that prices remain highand participants receive enough incometo continue their investment in soundgame management. This example pointsout the need to understand the focalmarket and the nature of demand forthe product of interest.

We also need to understand how thegrowth of a market will affect the largersocial system and vice versa. For in-stance, expanding tourism in attractivenatural areas can stimulate immigrationof people hoping to benefit from ex-panded economic opportunities. This canlead to a ‘‘tourism-income-populationgrowth spiral,’’ which obviously in-creases pressure on local resources andthe environment (31) and can degradethe natural beauty that people initiallytraveled to view and enjoy. In Quito, thepopulation continues to grow at 1.6%per year (35). When will the needs forresidential development or demand onthe water supply outstrip the capacity of

one watershed to provide clean waterfor the masses? What happens whenthat threshold is passed? Will construc-tion of a water treatment plant removethe incentive for protection of the Con-dor Biosphere Reserve?

Finally, good governance, rule of law,and democracy may well be importantfor achieving joint success in conserva-tion and economic development. Statis-tical analyses of economic growth inpoor countries hint at a connection be-tween democracy and governance andeconomic success (32). It would not besurprising to find a similar link to win–win ecosystem service projects. In Table1, all of the win–win examples entailstrong functioning governments, whereaspoor governance is implicated in threeof the four lose–lose failures. We hy-pothesize that a thorough study of manycase studies would uphold this trend.

The Absence of Data Jeopardizes theSuccess of Future ProjectsIncreasingly, conservation organizationsand development groups are in the busi-ness of providing hopeful visions of peo-ple and nature jointly benefiting fromconservation efforts (ref. 4 and seeTable 2). However, the enthusiasm forecosystem services as a strategy forenhancing conservation support is faroutpacing credible evidence of what ispossible and how to best achieve themuch desired win–win outcomes. Con-servation that is justified on the basis ofenhanced ecosystem services cannot af-ford to neglect rigorous evaluation ofboth ecology and social well-being. In-deed, there are enough projects in placearound the world that if some simplemetrics were collected on each, it wouldbe possible to treat these efforts as agrand experiment. The natural science,social science, and practitioner commu-nities jointly need to establish a stan-

Table 2. The relationship between nature and human well-being from the websites of major conservation NGOs

NGO Relationship between nature and human well-being

Conservation International �The rural poor within hotspots depend on the products of healthy ecosystems, harvesting wild plants forfood, fuel, clothing, medicine and shelter. These services also help maintain energy and infrastructureactivities that underpin economic development. For example, coral reefs, wetlands and mangroves canbuffer beaches and prevent storm surges and coastal flooding. The value of these ecological services istremendous and we are only beginning to measure their significance.� (http://web.conservation.org/xp/CIWEB/strategies/humanwelfare)

The Nature Conservancy �Nature has tremendous assets that are key to human-well being and that have concrete economic value�it’sbecoming increasingly clear that the goals of conservation and the goals of alleviating poverty andimproving human health are deeply interwoven.� (www.nature.org/tncscience/bigideas/people/art19846.html)

World Wildlife Fund �The world’s poorest people bear the brunt of forest loss, since forest resources sustain most of the 1.2 billionpeople in the world who live in extreme poverty. WWF is working locally, regionally and globally toaddress this threat and at multiple levels - with communities, governments and industry. In partnership wecan ensure forests are protected for the people and species that depend on these habitats for theirlivelihoods.� (www.worldwildlife.org/forests)

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dard set of measures and approaches forquantifying and monitoring ecosystemservice levels and values. Minimally,projects should track what money fundsthe protection of ecosystem services andwho provides it, who benefits from theecosystem services, and whether theproject results in an impact on the deliv-ery of ecosystem services.

An added challenge with ecosystemservice projects is that economic returnsand signals respond relatively quickly toany action, whereas changes in ecosys-tem function may lag by decades. Forexample, the productivity gains in theMississippi River valley that resulted

from heavy fertilizer application yieldedimmediate economic benefits. However,the dead zone in the Gulf of Mexico didnot appear until 20 years after thoseinitial gains in agricultural productivity.Different ecosystems services will respondon different temporal and spatial scales,and efforts to track interactions will haveto anticipate these different scales.

Beyond the missed scientific opportu-nity, conservation groups are riskingdamaged reputations because they havelargely failed to deliver data that pro-vide evidence of a link between theiractions and any improvement in the sta-tus of biodiversity or ecosystem services

(33, 34). This is a significant mistake,and a mistake that is even more griev-ous in the case of ecosystem serviceprojects. Whereas biodiversity cannotcomplain if it is not well served by aconservation project, people supposedlybenefiting from an ecosystem serviceeffort will be quick to ask for evidenceof their enhanced well-being. Much ofthe current enthusiasm for ecosystemservice projects in the conservationworld is an act of faith. At some point,however, that faith will need to bebacked up by irrefutable data showingthat these projects benefit both peopleand nature.

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2. Carpenter S, et al. (2006) Millennium ecosystem assess-ment: Research needs. Science 314:257–258.

3. Adams WM, et al. (2004) Biodiversity conservation andthe eradication of poverty. Science 306:1146–1149.

4. Campagna C, Fernandez T (2007) A comparative anal-ysis of the vision and mission statements of interna-tional environmental organizations. Environ Values16:369–398.

5. Agrawal A, Redford K (2006) Poverty, Development,and Biodiversity Conservation: Shooting in the Dark?(Wildlife Conservation Society, New York).

6. MacKinnon K, Luz K, Sobrevila C, Wright E (2006) TheWorld Bank and Biodiversity 1988–2005: Mountains toCoral Reefs (World Bank, Washington, DC).

7. McCulloch N, Weisbrod J, Timmer CP (2007) PathwaysOut of Poverty During an Economic Crisis: An EmpiricalAssessment of Rural Indonesia (Center for Global De-velopment, Washington, DC), Working Paper 115.

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19. World Bank (2005) Implementation Completion Re-port (TF-25143 TF-25142 TF-28302 TF-28303) on aGrant in the Amount of SDR 4.5 Million (US$7.0Million Equivalent) to the Burkina Faso and Republicof Cote D’Ivoire for a West Africa Pilot Community-Based Natural Resources and Wildlife ManagementProject (World Bank, Washington, DC), Report32218.

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23. Tallis HM, Kareiva P (2006) Shaping global environmen-tal decisions using socio-ecological models. Trends EcolEvol 21:562–568.

24. Ostfeld R, Keesing F (2000) Biodiversity and diseaserisk: The case of Lyme disease. Conserv Biol 14:722–728.

25. Chivian E, Bernstein AS (2004) Embedded in nature:Human health and biodiversity. Environ Health Per-spect 112:A12–A13.

26. Bennett EM, Balvanera P (2007) The future of produc-tion systems in a globalized world. Front Ecol Environ5:191–198.

27. Heal GM, et al. (2005) Valuing Ecosystem Services:Toward Better Environmental Decision-Making (NatlAcad Press, Washington, DC).

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CELL BIOLOGY. For the article ‘‘Mitochondrial potassium channelKv1.3 mediates Bax-induced apoptosis in lymphocytes,’’ byIldiko Szabo, Jurgen Bock, Heike Grassme, Matthias Sodde-mann, Barbara Wilker, Florian Lang, Mario Zoratti, and ErichGulbins, which appeared in issue 39, September 30, 2008, of ProcNatl Acad Sci USA (105:14861–14866; first published September25, 2008; 10.1073�pnas.0804236105), the authors note that dueto a printer’s error, the e-mail address for corresponding authorErich Gulbins appeared incorrectly. The correct address iserich.gulbins@uni-duisburg-essen.de. The online version hasbeen corrected. In addition, in the Abstract, line 2, ‘‘Here, weshow that mouse and human cells that are genetically deficientin either Kv1.3 or transfected with siRNA’’ should instead read:‘‘Here, we show that mouse and human cells either geneticallydeficient in Kv1.3 or transfected with siRNA.’’ Also on page14861, right column, third full paragraph, line 4, ‘‘Fig. 1C’’ shouldappear as ‘‘Fig. S1C.’’ On page 14863, right column, last line,‘‘However, we expected this behavior’’ should instead read:‘‘However, we expected the same behavior.’’ On page 14865, leftcolumn, in line 6, ‘‘Fig. 3D’’ should appear as ‘‘Fig. S8 A and B.’’On the same page, left column, 8 lines from the bottom, ‘‘Fig.5C’’ should appear as ‘‘Fig. 4C.’’ Finally, on page 14866, in thelist of references, the reference number 6 appears twice, and thefirst instance should instead be numbered 5. The correctedreferences appear below.

5. Ardehali H, O’Rourke B (2005) Mitochondrial K(ATP) channels in cell survival and death.J Mol Cell Cardiol 39:7–16.

6. Dimmer KS, et al. (2008) LETM1, deleted in Wolf–Hirschhorn syndrome is required fornormal mitochondrial morphology and cellular viability. Hum Mol Gen 17:201–217.

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PERSPECTIVE. For the article ‘‘Ecosystem Services Special Feature:An ecosystem services framework to support both practicalconservation and economic development,’’ by Heather Tallis,Peter Kareiva, Michelle Marvier, and Amy Chang, which ap-peared in issue 28, July 15, 2008, of Proc Natl Acad Sci USA(105:9457–9464; first published July 9, 2008; 10.1073�pnas.0705797105), the authors note that on page 9459, rightcolumn, line 7, ‘‘1999’’ should have appeared as ‘‘1998.’’

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