insight review articles Consequences of changing biodiversity F.Stuart Chapin Ill,Erika S.Zavaleta,Valerie T.Eviners,Rosamond L.Naylor,Peter M.Vitousek, Heather L.Reynoldsll,David U.Hooper,Sandra Lavorel#,Osvaldo E.Sala,Sarah E.Hobbie, Michelle C.Mack*&Sandra Diaz *Institute of Arctic Biology,University of Alaska,Fairbanks,Alaska 99775,USA (e-mail:fschapin@lter.uaf.edu) +Department of Biological Sciences andInstitute for International Studies,Stanford University,Stanford,California 94305,USA $Department of Integrative Biology,University of California,Berkeley.California 94720,USA lDepartment of Biology,Kalamazoo College,Kalamazoo,Michigan 49006,USA Department of Biology,Western Washington University,Bellingham,Washington 98225,USA #Centre d'Ecologie Fonctionnelle et Evolutive,CNRS UPR 9056,34293 Montpellier Cedex 05,France Catedra de Ecologia and Instituto de Fisiologia y Ecologia Vinculadas a la Agricultura,Faculty of Agronomy,University of Buenos Aires,Ave San Martin 4453,Buenos Aires C1417DSE,Argentina Department of Ecology,Evolution,and Behavior,University of Minnesota,St Paul,Minnesota55108,USA Instituto Multidisciplinario de Biologia Vegetal,Universidad Nacional de Cordoba,FCEFyN,Casilla de Correo 495,5000 Cordoba,Argentina Human alteration of the global environment has triggered the sixth major extinction event in the history of life and caused widespread changes in the global distribution of organisms.These changes in biodiversity alter ecosystem processes and change the resilience of ecosystems to environmental change.This has profound consequences for services that humans derive from ecosystems.The large ecological and societal consequences of changing biodiversity should be minimized to preserve options for future solutions to global environmental problems. umans have extensively altered the global preserves,native species are often out-competed or con- environment, changing global sumed by organisms introduced from elsewhere.Extinction biogeochemical cycles,transforming land and is a natural process,but it is occurring at an unnaturally rapid enhancing the mobility of biota.Fossil-fuel rate as a consequence of human activities.Already we have combustion and deforestation have increased causedtheextinctionof5-20%ofthespecies in many groups the concentration of atmospheric carbon dioxide(CO,) oforganisms(Fig.2),and current rates ofextinction are esti- by 30%in the past three centuries(with more than half of mated to be 100-1,000 timesgreater than pre-humanrates5 this increase occurring in the past 40 years).We have In the absence of major changes in policy and human more than doubled the concentration of methane and behaviour,our effects on the environment will continue to increased concentrations of other gases that contribute to alter biodiversity.Land-use change is projected to have the climate warming.In the next century these greenhouse largest global impact on biodiversity by the year 2100, gases are likely to cause the most rapid climate change that followed by climate change,nitrogen deposition,species the Earth has experienced since the end of the last introductions and changing concentrations ofatmospheric glaciation 18,000 years ago and perhaps a much longer CO,(ref.6).Land-use change is expected to be of particular time.Industrial fixation of nitrogen for fertilizer and other importance in the tropics,climatic change is likely to be human activities has more than doubled the rates of important at high latitudes,and a multitude of interacting terrestrial fixation of gaseous nitrogen into biologically causeswillaffectother biomes(Fig.3).Whataretheecolog- available forms.Run off of nutrients from agricultural and ical and societal consequences of current and projected urban systems has increased several-fold in the developed effects of human activity on biological diversity? river basins of the Earth,causing major ecological changes in estuaries and coastal zones.Humans have transformed Ecosystem consequences of altered diversity 40-50%of the ice-free land surface,changing prairies, Diversity at all organizational levels,ranging from genetic forests and wetlands into agricultural and urban systems. diversity within populations to the diversity of ecosystems in We dominate(directly or indirectly)about one-third of landscapes,contributes to global biodiversity.Here we focus the net primary productivity on land and harvest fish that on species diversity,because the causes,patterns and conse- use 8%of ocean productivity.We use 54%of the available quences of changes in diversity at this level are relatively well fresh water,with use projected to increase to 70%by documented.Species diversity has functional consequences 2050.Finally,the mobility of people has transported because the number and kinds of species present determine organisms across geographical barriers that long kept the the organismal traits that influence ecosystem processes. biotic regions of the Earth separated,so that many of the Species traits may mediate energy and material fluxes direct- ecologically important plant and animal species of many ly or may alter abiotic conditions (for example,limiting areas have been introduced in historic time? resources,disturbance and climate)that regulate process Together these changes have altered the biological diver- rates.The components of species diversity that determine sity ofthe Earth(Fig.1).Many species have beeneliminated this expression of traits include the number of species from areas dominated by human influences.Even in present(species richness),their relativeabundances(species 234 2000 Macmillan Magazines Ltd NATURE|VOL 405|11 MAY 2000 www.nature.com
insight review articles 234 NATURE | VOL 405 | 11 MAY 2000 | www.nature.com Humans have extensively altered the global environment, changing global biogeochemical cycles, transforming land and enhancing the mobility of biota. Fossil-fuel combustion and deforestation have increased the concentration of atmospheric carbon dioxide (CO2) by 30% in the past three centuries (with more than half of this increase occurring in the past 40 years). We have more than doubled the concentration of methane and increased concentrations of other gases that contribute to climate warming. In the next century these greenhouse gases are likely to cause the most rapid climate change that the Earth has experienced since the end of the last glaciation 18,000 years ago and perhaps a much longer time. Industrial fixation of nitrogen for fertilizer and other human activities has more than doubled the rates of terrestrial fixation of gaseous nitrogen into biologically available forms. Run off of nutrients from agricultural and urban systems has increased several-fold in the developed river basins of the Earth, causing major ecological changes in estuaries and coastal zones. Humans have transformed 40–50% of the ice-free land surface, changing prairies, forests and wetlands into agricultural and urban systems. We dominate (directly or indirectly) about one-third of the net primary productivity on land and harvest fish that use 8% of ocean productivity. We use 54% of the available fresh water, with use projected to increase to 70% by 20501 . Finally, the mobility of people has transported organisms across geographical barriers that long kept the biotic regions of the Earth separated, so that many of the ecologically important plant and animal species of many areas have been introduced in historic time2,3. Together these changes have altered the biological diversity of the Earth (Fig. 1). Many species have been eliminated from areas dominated by human influences. Even in preserves, native species are often out-competed or consumed by organisms introduced from elsewhere. Extinction is a natural process, but it is occurring at an unnaturally rapid rate as a consequence of human activities. Already we have caused the extinction of 5–20% of the species in many groups of organisms (Fig. 2), and current rates of extinction are estimated to be 100–1,000 times greater than pre-human rates4,5. In the absence of major changes in policy and human behaviour, our effects on the environment will continue to alter biodiversity. Land-use change is projected to have the largest global impact on biodiversity by the year 2100, followed by climate change, nitrogen deposition, species introductions and changing concentrations of atmospheric CO2 (ref. 6). Land-use change is expected to be of particular importance in the tropics, climatic change is likely to be important at high latitudes, and a multitude of interacting causes will affect other biomes (Fig. 3)6 . What are the ecological and societal consequences of current and projected effects of human activity on biological diversity? Ecosystem consequences of altered diversity Diversity at all organizational levels, ranging from genetic diversity within populations to the diversity of ecosystems in landscapes, contributes to global biodiversity. Here we focus on species diversity, because the causes, patterns and consequences of changes in diversity at this level are relatively well documented. Species diversity has functional consequences because the number and kinds of species present determine the organismal traits that influence ecosystem processes. Species traits may mediate energy and material fluxes directly or may alter abiotic conditions (for example, limiting resources, disturbance and climate) that regulate process rates. The components of species diversity that determine this expression of traits include the number of species present (species richness), their relative abundances (species Consequences of changing biodiversity F. Stuart Chapin III*, Erika S. Zavaleta†, Valerie T. Eviner§, Rosamond L. Naylor‡, Peter M. Vitousek†, Heather L. Reynolds||, David U. Hooper¶, Sandra Lavorel#, Osvaldo E. Sala✩, Sarah E. Hobbie**, Michelle C. Mack* & Sandra Díaz†† *Institute of Arctic Biology, University of Alaska, Fairbanks, Alaska 99775, USA (e-mail: fschapin@lter.uaf.edu) †Department of Biological Sciences and ‡Institute for International Studies, Stanford University, Stanford, California 94305, USA §Department of Integrative Biology, University of California, Berkeley, California 94720, USA ||Department of Biology, Kalamazoo College, Kalamazoo, Michigan 49006, USA ¶Department of Biology, Western Washington University, Bellingham, Washington 98225, USA #Centre d’Ecologie Fonctionnelle et Evolutive, CNRS UPR 9056, 34293 Montpellier Cedex 05, France ✩Cátedra de Ecología and Instituto de Fisiología y Ecología Vinculadas a la Agricultura, Faculty of Agronomy, University of Buenos Aires, Ave San Martín 4453, Buenos Aires C1417DSE, Argentina **Department of Ecology, Evolution, and Behavior, University of Minnesota, St Paul, Minnesota 55108, USA ††Instituto Multidisciplinario de Biología Vegetal, Universidad Nacional de Córdoba, FCEFyN, Casilla de Correo 495, 5000 Córdoba, Argentina Human alteration of the global environment has triggered the sixth major extinction event in the history of life and caused widespread changes in the global distribution of organisms. These changes in biodiversity alter ecosystem processes and change the resilience of ecosystems to environmental change. This has profound consequences for services that humans derive from ecosystems. The large ecological and societal consequences of changing biodiversity should be minimized to preserve options for future solutions to global environmental problems. © 2000 Macmillan Magazines Ltd
insight review articles Figure 1 The role of biodiversity in global change.Human Human Global changes activities that are motivated by activities economic,cultural,intellectual. Biogeochemical cycles -elevated CO,and other aesthetic and spiritual goals(1) 2 greenhouse gases Economic Cultural, are now causing environmental -nutrient loading benefits ◆intellectual, and ecological changes of -water consumption aesthetic and soiritual global significance (2).By a Land use benefits -type variety of mechanisms,these -intensity global changes contribute to Species invasions changing biodiversity,and changing biodiversity feeds Biodiversity Ecosystem goods back on susceptibility to species -richness and services invasions (3.purple arrows;see -evenness -composition text).Changes in biodiversity. -interactions through changes in species Species traits traits,can have direct consequences for ecosystem services and,as a result, human economic and social Ecosystem processes activities (4).In addition, changes in biodiversity can influence ecosystem processes (5).Altered ecosystem processes can thereby influence ecosystem services that benefit humanity (6)and feedback to further alter biodiversity(7,red amrow).Global changes may also directly affect ecosystem processes(8.blue arrows).Depending on the circumstances,the direct effects of global change may be either stronger or weaker than effects mediated by changes in diversity.We argue that the costs of loss of biotic diversity,although traditionally considered to be 'outside the box'of human welfare,must be recognized in our accounting of the costs and benefits of human activities. evenness),the particular species present (species composition),the mycorrhizal species richness also seems to enhance plant production interactions among species (non-additive effects),and the temporal in an asymptotic fashion,although phosphorus uptake was and spatial variation in these properties.In addition to its effects on enhanced in a linear fashion from 1 to 14 species offungi.Microbial current functioning of ecosystems,species diversity influences the richness can lead to increased decomposition oforganic matter".In resilience and resistance ofecosystemstoenvironmental change. contrast,no consistent statistical relationship has been observed Species richness and evenness between plant species richness of litter inputs and decomposition Most theoretical and empirical work on the functional consequences rate.Thus,inexperimental communities(which typically focus on of changing biodiversity has focused on the relationship between only one or two trophic levels),there seems to be no universal species richness and ecosystem functioning.Theoretical possibilities relationship between species richness and ecosystem functioning, include positive linear and asymptotic relationships between rich- perhaps because processes differ in their sensitivity to species rich- nessandratesofecosystemprocesses,or thelackofasimplestatistical ness compared with other components ofdiversity(such as evenness, relationship'(Box 1).In experiments,species richness correlates composition or interactions).The absence of a simple relationship with rates of ecosystem processes most clearly at low numbers of between species richness and ecosystem processes is likely when one species.We know much less about the impact of species richness in or a few species have strong ecosystem effects. species-rich,natural ecosystems.Several studies using experimental Although the relationship of species richness to ecosystem func- species assemblages have shown that annual rates of primary produc- tioning has attracted considerable theoretical and experimental tivity and nutrient retention increase with increasing plant species attention because of the irreversibility of species extinction,human richness,but saturate at a rather low number of species' Arbuscular activities influence the relative abundances ofspecies more frequent- ly than the presence or absence of species.Changes in species evenness warrant increased attention,because they usually respond more rapidly to human activities than do changes in species richness and because they have important consequences to ecosystems long olo before aspecies is threatenedby extinction. Species composition Particular species can have strong effects on ecosystem processes by directly mediating energy and material fluxes or by altering abiotic conditions that regulate the rates of these processes (Fig.4)34 Species'alteration ofthe availability oflimiting resources,the distur- bance regime,and the climate can have particularly strongeffects on ecosystem processes.Such effects are most visible when introduced species alter previous patterns of ecosystem processes.For example, the introduction of the nitrogen-fixing tree Myrica faya to nitrogen- Fish nt limited ecosystems in Hawaii led to a fivefold increase in nitrogen inputs to the ecosystem,which in turn changed most ofthe function- Figure 2 Proportion of the global number of species of birds,mammals,fish and al and structural properties of native forests5.Introduction of the plants that are currently threatened with extinction" deep-rooted salt cedar (Tamarix sp.)to the Mojave and Sonoran Deserts of North America increased the water and soil solutes NATURE|VOL 405|11 MAY 2000 www.nature.com 2000 Macmillan Magazines Ltd 235
evenness), the particular species present (species composition), the interactions among species (non-additive effects), and the temporal and spatial variation in these properties. In addition to its effects on current functioning of ecosystems, species diversity influences the resilience and resistance of ecosystems to environmental change. Species richness and evenness Most theoretical and empirical work on the functional consequences of changing biodiversity has focused on the relationship between species richness and ecosystem functioning. Theoretical possibilities include positive linear and asymptotic relationships between richness and rates of ecosystem processes, or the lack of a simple statistical relationship7 (Box 1). In experiments, species richness correlates with rates of ecosystem processes most clearly at low numbers of species. We know much less about the impact of species richness in species-rich, natural ecosystems. Several studies using experimental species assemblages have shown that annual rates of primary productivity and nutrient retention increase with increasing plant species richness, but saturate at a rather low number of species8,9. Arbuscular mycorrhizal species richness also seems to enhance plant production in an asymptotic fashion, although phosphorus uptake was enhanced in a linear fashion from 1 to 14 species of fungi10. Microbial richness can lead to increased decomposition of organic matter11. In contrast, no consistent statistical relationship has been observed between plant species richness of litter inputs and decomposition rate12. Thus, in experimental communities (which typically focus on only one or two trophic levels), there seems to be no universal relationship between species richness and ecosystem functioning, perhaps because processes differ in their sensitivity to species richness compared with other components of diversity (such as evenness, composition or interactions). The absence of a simple relationship between species richness and ecosystem processes is likely when one or a few species have strong ecosystem effects. Although the relationship of species richness to ecosystem functioning has attracted considerable theoretical and experimental attention because of the irreversibility of species extinction, human activities influence the relative abundances of species more frequently than the presence or absence of species. Changes in species evenness warrant increased attention, because they usually respond more rapidly to human activities than do changes in species richness and because they have important consequences to ecosystems long before a species is threatened by extinction. Species composition Particular species can have strong effects on ecosystem processes by directly mediating energy and material fluxes or by altering abiotic conditions that regulate the rates of these processes (Fig. 4)13,14. Species’ alteration of the availability of limiting resources, the disturbance regime, and the climate can have particularly strong effects on ecosystem processes. Such effects are most visible when introduced species alter previous patterns of ecosystem processes. For example, the introduction of the nitrogen-fixing tree Myrica faya to nitrogenlimited ecosystems in Hawaii led to a fivefold increase in nitrogen inputs to the ecosystem, which in turn changed most of the functional and structural properties of native forests15. Introduction of the deep-rooted salt cedar (Tamarix sp.) to the Mojave and Sonoran Deserts of North America increased the water and soil solutes insight review articles NATURE | VOL 405 | 11 MAY 2000 | www.nature.com 235 Figure 1 The role of biodiversity in global change. Human activities that are motivated by economic, cultural, intellectual, aesthetic and spiritual goals (1) are now causing environmental and ecological changes of global significance (2). By a variety of mechanisms, these global changes contribute to changing biodiversity, and changing biodiversity feeds back on susceptibility to species invasions (3, purple arrows; see text). Changes in biodiversity, through changes in species traits, can have direct consequences for ecosystem services and, as a result, human economic and social activities (4). In addition, changes in biodiversity can influence ecosystem processes (5). Altered ecosystem processes can thereby influence ecosystem services that benefit humanity (6) and feedback to further alter biodiversity (7, red arrow). Global changes may also directly affect ecosystem processes (8, blue arrows). Depending on the circumstances, the direct effects of global change may be either stronger or weaker than effects mediated by changes in diversity. We argue that the costs of loss of biotic diversity, although traditionally considered to be ‘outside the box’ of human welfare, must be recognized in our accounting of the costs and benefits of human activities. Biogeochemical cycles Land use –elevated CO2 and other greenhouse gases –nutrient loading –water consumption –type –intensity Biodiversity –richness –evenness –composition –interactions Species invasions Species traits Human activities Economic benefits Cultural, intellectual, aesthetic and spiritual benefits Ecosystem goods and services Ecosystem processes 1 2 3 7 4 6 5 8 Global changes 0 5 10 15 20 Birds Mammals Fish Plants Extinction threatened (percentage of global species) Figure 2 Proportion of the global number of species of birds, mammals, fish and plants that are currently threatened with extinction4 . © 2000 Macmillan Magazines Ltd
insight review articles Box 1 Species richness and ecosystem functioning There has been substantial debate over both the form of the relationship between species richness and ecosystem processes and the mechanisms underlying these relationships5.Theoretically,rates of ecosystem processes might increase linearly with species richness if all species contribute substantially and in unique ways to a given process-that is,have complementary niches.This relationship is likely to saturate as niche overlap,or'redundancy',increases at higher levels of diversity.Several experiments indicate such an asymptotic relationship of ecosystem process rates with species richness.An asymptotic relationship between richness and process rates could,however,arise from a 'sampling effectof increased probability of including a species with strong ecosystem effects,as species richness increasest.The sampling effect has at least two interpretations.It might be an important biological property of communities that influences process rates in natural ecosystems13,or it might be an artefact of species-richness experiments in which species are randomly assigned to treatments,rather than following community assembly rules that might occur in nature.Finally,ecosystem process rates may show no simple correlation with species richness.However,the lack of a simple statistical relationship between species richness and an ecosystem process may mask important functional relationships.This could occur,for example,if process rates depend strongly on the traits of certain species or if species interactions determine the species traits that are expressed (the'idiosyncratic hypothesis').This mechanistic debate is important scientifically for understanding the functioning of ecosystems and effective management of their biotic resources.Regardless of the outcome of the debate, conserving biodiversity is essential because we rarely know a priori which species are critical to current functioning or provide resilience and resistance to environmental changes. accessed by vegetation,enhanced productivity,and increased surface rebound quickly.Similar increases in the ecological role of fire litter and salts.This inhibited the regeneration of many native resulting from grass invasions have been widely observed in the species,leading to ageneral reduction in biodiversity.The perenni- Americas,Australia and elsewhere in Oceania.The invasion ofcheat- al tussock grass,Agropyron cristatum,which was widely introduced grass(Bromus tectorum)into western North America is one of the to the northern Great Plains of North America after the 1930s most extensive of these invasions.Cheatgrass has increased fire fre- dustbowl,has substantially lower allocation to roots compared with quency by a factor of more than ten in the >40 million hectares native prairie grasses.Soil under A.cristatum has lower levels of (1ha=10'm2)thatit now dominates2. available nitrogen and-25%less total carbon than native prairie soil, Species-induced changes in microclimate can be just as impor- so the introduction of this species resulted in an equivalent reduction tant as the direct impacts of environmental change.For example,in of 480 x 102g carbon stored in soils7.Soil invertebrates,such as late-successional boreal forests,where soil temperatures have a earthworms and termites,also alter turnover of organic matter and strong influenceon nutrient supplyand productivity,the presence of nutrient supply,thereby influencing the species composition of the moss,which reduces heat flux into the soil,contributes to the stability aboveground flora and fauna's of permafrost(frozen soils)and the characteristically low rates of Species can also influence disturbance regime.For example, nutrient cycling".As fire frequency increases in response to high-lat- several species of nutritious but flammable grasses were introduced itude warming,moss biomass declines,permafrost becomes less sta- to the Hawaiian Islands to support cattle grazing.Some of these ble,the nutrient supply increases,and the species composition of grasses spread into protected woodlands,where they caused a 300- forests is altered.Plant traits can also influence climate at larger fold increase in the extent of fire.Most ofthe woody plants,including scales.Simulations with general circulation models indicate that some endangered species,are eliminated by fire,whereas grasses widespread replacement of deep-rooted tropical trees by shallow- Figure 3 Scenarios of change in species diversity in selected biomes by the year 2100.The values are the projected change in diversity for each □Other ☐Land use biome relative to the biome with greatest projected diversity change. Exotic Climate Biomes are:tropical forests (T),grasslands (G),Mediterranean (M), desert (D).north temperate forests (N).boreal forests (B)and arctic(A). Projected change in species diversity is calculated assuming three altemnative scenarios of interactions among the causes of diversity change.Scenario 1 assumes no interaction among causes of diversity change,so that the total change in diversity is the sum of the changes caused by each driver of diversity change.Scenario 2 assumes that only the factor with the greatest impact on diversity influences diversity change.Scenario 3 assumes that factors causing change in biodiversity interact multiplicatively to determine diversity change.For scenarios 1 and 2,we show the relative importance of the major causes of projected change in diversity.These causes are climatic change,change in land 0.4 use,introduction of exotic species,and changes in atmospheric Co. and/or nitrogen deposition (labelled 'other).The graph shows that all biomes are projected to experience substantial change in species diversity by 2100,that the most important causes of diversity change differ among biomes,and that the patterns of diversity change depend on assumptions about the nature of interactions among the causes of diversity change.Projected biodiversity change is most similar among TGM D N B G M D N B biomes if causes of diversity change do not interact(scenario 1)and Scenario 1 Scenario 2 Scenario 3 differ most srongy among biomes thecauses of biodiversity change interact multiplicatively (scenario 3). 236 2000 Macmillan Magazines Ltd NATURE VOL 40511 MAY 2000 www.nature.com
accessed by vegetation, enhanced productivity, and increased surface litter and salts. This inhibited the regeneration of many native species, leading to a general reduction in biodiversity16. The perennial tussock grass, Agropyron cristatum, which was widely introduced to the northern Great Plains of North America after the 1930s ‘dustbowl’, has substantially lower allocation to roots compared with native prairie grasses. Soil under A. cristatum has lower levels of available nitrogen and ~25% less total carbon than native prairie soil, so the introduction of this species resulted in an equivalent reduction of 480 2 1012 g carbon stored in soils17. Soil invertebrates, such as earthworms and termites, also alter turnover of organic matter and nutrient supply, thereby influencing the species composition of the aboveground flora and fauna18. Species can also influence disturbance regime. For example, several species of nutritious but flammable grasses were introduced to the Hawaiian Islands to support cattle grazing. Some of these grasses spread into protected woodlands, where they caused a 300- fold increase in the extent of fire. Most of the woody plants, including some endangered species, are eliminated by fire, whereas grasses rebound quickly19. Similar increases in the ecological role of fire resulting from grass invasions have been widely observed in the Americas, Australia and elsewhere in Oceania. The invasion of cheatgrass (Bromus tectorum) into western North America is one of the most extensive of these invasions. Cheatgrass has increased fire frequency by a factor of more than ten in the >40 million hectares (1 ha = 104 m2 ) that it now dominates20. Species-induced changes in microclimate can be just as important as the direct impacts of environmental change. For example, in late-successional boreal forests, where soil temperatures have a strong influence on nutrient supply and productivity, the presence of moss, which reduces heat flux into the soil, contributes to the stability of permafrost (frozen soils) and the characteristically low rates of nutrient cycling21. As fire frequency increases in response to high-latitude warming, moss biomass declines, permafrost becomes less stable, the nutrient supply increases, and the species composition of forests is altered. Plant traits can also influence climate at larger scales. Simulations with general circulation models indicate that widespread replacement of deep-rooted tropical trees by shallowinsight review articles 236 NATURE | VOL 405 | 11 MAY 2000 | www.nature.com Figure 3 Scenarios of change in species diversity in selected biomes by the year 2100. The values are the projected change in diversity for each biome relative to the biome with greatest projected diversity change6 . Biomes are: tropical forests (T), grasslands (G), Mediterranean (M), desert (D), north temperate forests (N), boreal forests (B) and arctic (A). Projected change in species diversity is calculated assuming three alternative scenarios of interactions among the causes of diversity change. Scenario 1 assumes no interaction among causes of diversity change, so that the total change in diversity is the sum of the changes caused by each driver of diversity change. Scenario 2 assumes that only the factor with the greatest impact on diversity influences diversity change. Scenario 3 assumes that factors causing change in biodiversity interact multiplicatively to determine diversity change. For scenarios 1 and 2, we show the relative importance of the major causes of projected change in diversity. These causes are climatic change, change in land use, introduction of exotic species, and changes in atmospheric CO2 and/or nitrogen deposition (labelled ‘other’). The graph shows that all biomes are projected to experience substantial change in species diversity by 2100, that the most important causes of diversity change differ among biomes, and that the patterns of diversity change depend on assumptions about the nature of interactions among the causes of diversity change. Projected biodiversity change is most similar among biomes if causes of diversity change do not interact (scenario 1) and differ most strongly among biomes if the causes of biodiversity change interact multiplicatively (scenario 3). 1 0.8 0.6 0.4 0.2 0 TGMDNBA TGMDNBA TGMDNBA Relative diversity change (proportion of maximum) Scenario 1 Scenario 2 Scenario 3 Other Exotic Land use Climate There has been substantial debate over both the form of the relationship between species richness and ecosystem processes and the mechanisms underlying these relationships85. Theoretically, rates of ecosystem processes might increase linearly with species richness if all species contribute substantially and in unique ways to a given process — that is, have complementary niches. This relationship is likely to saturate as niche overlap, or ‘redundancy’, increases at higher levels of diversity86. Several experiments indicate such an asymptotic relationship of ecosystem process rates with species richness. An asymptotic relationship between richness and process rates could, however, arise from a ‘sampling effect’ of increased probability of including a species with strong ecosystem effects, as species richness increases13. The sampling effect has at least two interpretations. It might be an important biological property of communities that influences process rates in natural ecosystems13, or it might be an artefact of species-richness experiments in which species are randomly assigned to treatments, rather than following community assembly rules that might occur in nature87. Finally, ecosystem process rates may show no simple correlation with species richness. However, the lack of a simple statistical relationship between species richness and an ecosystem process may mask important functional relationships. This could occur, for example, if process rates depend strongly on the traits of certain species or if species interactions determine the species traits that are expressed (the ‘idiosyncratic hypothesis’)7 . This mechanistic debate is important scientifically for understanding the functioning of ecosystems and effective management of their biotic resources. Regardless of the outcome of the debate, conserving biodiversity is essential because we rarely know a priori which species are critical to current functioning or provide resilience and resistance to environmental changes. Box 1 Species richness and ecosystem functioning © 2000 Macmillan Magazines Ltd
insight review articles Figure 4 Mechanisms by which Global changes Human benefits species traits affect ecosystem processes.Changes in biodiversity alter the functional traits of species in an ecosystem in ways that directly 》 Ecosystem goods influence ecosystem goods and Species traits and services services(1)either positively (for example,increased agricultural or forestry production)or negatively 3 3b (for example,loss of harvestable Abiotic Disturbance Direct species or species with strong process regime biotic controls Availability rocessing aesthetic/cultural value).Changes in Climate species traits affect ecosystem of limiting variables resources processes directly through changes in biotic controls(2)and indirectly through changes in abiotic controls, Ecosystem processes such as availability of limiting resources(3a),disturbance regime (3b),or micro-or macroclimate variables (3c).llustrations of these effects include:reduction in river flow due to invasion of deep-rooted desert trees(3a;photo by E. Zavaleta):increased fire frequency resulting from grass invasion that destroys native trees and shrubs in Hawaii(3b,photo by C.D'Antonio): and insulation of soils by mosses in arctic tundra,contributing to conditions that allow for permafrost (3c:photo by D.Hooper).Altered processes can then influence the availability of ecosystem goods and services directly(4)or indirectly by further altering biodiversity (5),resulting in loss of useful species or increases in noxious species. rooted pasture grasses would reduceevapotranspirationandlead toa overgrazed kelp2(Fig.6a).Recent over-fishing in the North Pacific warmer,drier climate2.At high latitudes,the replacement of may have triggered similar outbreaks of sea urchin,as killer whales snow-covered tundrabya dark conifer canopy will probably increase moved closer to shore and switched to sea otters as an alternate energy absorption sufficiently to act as a powerful positive feedback prey2.In the absence of dense populations of sea urchins,kelp to regional warming provides the physical structure for diverse subtidal communities Species interactions and attenuates waves that otherwise augment coastal erosion and Most ecosystem processes are non-additive functions of the traits of storm damage.Removing bass from lakes that were fertilized with two or more species,because interactions among species,rather than phosphorus caused an increase in minnows,which depleted the simple presence or absence of species,determine ecosystem charac- biomass of phytoplankton grazers and caused algal blooms" teristics(Fig.5).Species interactions,including mutualism,trophic (Fig.6b).Thealgal bloomsturned the lake froma netsource to a net interactions(predation,parasitism and herbivory),and competition sink of CO,.Thus,biotic change and altered nutrient cycles can may affect ecosystem processes directly by modifying pathways of interact to influence whole-system carbon balance.The zebra energyand material flowor indirectlyby modifying theabundances mussel (Dreissena polymorpha)is a bottom-dwelling invasive or traits ofspecies with strong ecosystem effects25 species that,through its filter feeding,markedly reduces phyto- Mutualistic species interactions contribute directly to many plankton while increasing water clarity and phosphorus availabili- essentialecosystem processes.For example,nitrogen inputs to terres- ty.Introduction ofthis species shifts the controlling interactions of trial ecosystems are mediated primarily by mutualistic associations the food web from the water column to the sediments.Trophic between plants and nitrogen-fixing microorganisms.Mycorrhizal interactions are also important in terrestrial ecosystems.At the associations between plant roots and fungi greatly aid plant micro scale,predation on bacteria by protozoan grazers speeds nutrient uptake from soil,increase primary production and speed nitrogen cycling near plant roots,enhancing nitrogen availability to succession26.Highly integrated communities (consortia)of soil plants.At the regionalscale,an improvement in huntingtechnolo- microorganisms,in which each species contributes a distinct set of gy at the end of the Pleistocene may have contributed to the loss of enzymes,speeds the decomposition of organic matter".Many of the Pleistocene megafauna and the widespread change from steppe these interactions have a high degree of specificity,which increases grassland to tundra that occurred in Siberia 10,000-18,000 years the probability that loss of a given species will have cascading effects ago.The resulting increase in mosses insulated the soil and led to on the rest ofthe system. cooler soils,less decomposition and greater sequestration ofcarbon Trophic interactions can have large effects on ecosystem process- in peat.Today,human harvest of animals continues to have a es either by directly modifying fluxes of energy and materials,or by pronounced effect ofthe functioning ofecosystems. influencing the abundances of species that control those fluxes. Competition,mutualisms and trophic interactions frequently When top predators are removed,prey populations sometimes lead to secondary interactions among other species,often with explode and deplete their food resources,leading to a cascade of strong ecosystem effects(Fig.5).For example,soil microbial com- ecological effects.For example,removal of sea otters by Russian position can modify the outcome of competition among plant fur traders allowed a population explosion of sea urchins that species,and plants modify the microbial community of their NATURE|VOL 40511 MAY 2000www.nature.com ☆©20o0 Macmillan Magazines Ltd 237
rooted pasture grasses would reduce evapotranspiration and lead to a warmer, drier climate22. At high latitudes, the replacement of snow-covered tundra by a dark conifer canopy will probably increase energy absorption sufficiently to act as a powerful positive feedback to regional warming23. Species interactions Most ecosystem processes are non-additive functions of the traits of two or more species, because interactions among species, rather than simple presence or absence of species, determine ecosystem characteristics (Fig. 5). Species interactions, including mutualism, trophic interactions (predation, parasitism and herbivory), and competition may affect ecosystem processes directly by modifying pathways of energy and material flow24or indirectly by modifying the abundances or traits of species with strong ecosystem effects25. Mutualistic species interactions contribute directly to many essential ecosystem processes. For example, nitrogen inputs to terrestrial ecosystems are mediated primarily by mutualistic associations between plants and nitrogen-fixing microorganisms. Mycorrhizal associations between plant roots and fungi greatly aid plant nutrient uptake from soil, increase primary production and speed succession26. Highly integrated communities (consortia) of soil microorganisms, in which each species contributes a distinct set of enzymes, speeds the decomposition of organic matter27. Many of these interactions have a high degree of specificity, which increases the probability that loss of a given species will have cascading effects on the rest of the system. Trophic interactions can have large effects on ecosystem processes either by directly modifying fluxes of energy and materials, or by influencing the abundances of species that control those fluxes. When top predators are removed, prey populations sometimes explode and deplete their food resources, leading to a cascade of ecological effects. For example, removal of sea otters by Russian fur traders allowed a population explosion of sea urchins that overgrazed kelp28 (Fig. 6a). Recent over-fishing in the North Pacific may have triggered similar outbreaks of sea urchin, as killer whales moved closer to shore and switched to sea otters as an alternate prey29. In the absence of dense populations of sea urchins, kelp provides the physical structure for diverse subtidal communities and attenuates waves that otherwise augment coastal erosion and storm damage30. Removing bass from lakes that were fertilized with phosphorus caused an increase in minnows, which depleted the biomass of phytoplankton grazers and caused algal blooms31 (Fig. 6b). The algal blooms turned the lake from a net source to a net sink of CO2. Thus, biotic change and altered nutrient cycles can interact to influence whole-system carbon balance. The zebra mussel (Dreissena polymorpha) is a bottom-dwelling invasive species that, through its filter feeding, markedly reduces phytoplankton while increasing water clarity and phosphorus availability32. Introduction of this species shifts the controlling interactions of the food web from the water column to the sediments. Trophic interactions are also important in terrestrial ecosystems. At the micro scale, predation on bacteria by protozoan grazers speeds nitrogen cycling near plant roots, enhancing nitrogen availability to plants33. At the regional scale, an improvement in hunting technology at the end of the Pleistocene may have contributed to the loss of the Pleistocene megafauna and the widespread change from steppe grassland to tundra that occurred in Siberia 10,000–18,000 years ago34. The resulting increase in mosses insulated the soil and led to cooler soils, less decomposition and greater sequestration of carbon in peat. Today, human harvest of animals continues to have a pronounced effect of the functioning of ecosystems. Competition, mutualisms and trophic interactions frequently lead to secondary interactions among other species, often with strong ecosystem effects (Fig. 5). For example, soil microbial composition can modify the outcome of competition among plant species35, and plants modify the microbial community of their insight review articles NATURE | VOL 405 | 11 MAY 2000 | www.nature.com 237 Figure 4 Mechanisms by which species traits affect ecosystem processes. Changes in biodiversity alter the functional traits of species in an ecosystem in ways that directly influence ecosystem goods and services (1) either positively (for example, increased agricultural or forestry production) or negatively (for example, loss of harvestable species or species with strong aesthetic/cultural value). Changes in species traits affect ecosystem processes directly through changes in biotic controls (2) and indirectly through changes in abiotic controls, such as availability of limiting resources (3a), disturbance regime (3b), or micro- or macroclimate variables (3c). Illustrations of these effects include: reduction in river flow due to invasion of deep-rooted desert trees (3a; photo by E. Zavaleta); increased fire frequency resulting from grass invasion that destroys native trees and shrubs in Hawaii (3b, photo by C. D’Antonio); and insulation of soils by mosses in arctic tundra, contributing to conditions that allow for permafrost (3c; photo by D. Hooper). Altered processes can then influence the availability of ecosystem goods and services directly (4) or indirectly by further altering biodiversity (5), resulting in loss of useful species or increases in noxious species. Global changes Human benefits Ecosystem goods and services Biodiversity Species traits Ecosystem processes Direct biotic processing Abiotic process controls Disturbance regime Availability of limiting resources Climate variables 3a 3b 3c 1 5 2 4 © 2000 Macmillan Magazines Ltd
insight review articles Global changes Human activities and benefits Biodiversity Ecosystem goods and services Species interactions -Mutualistic ◆-Competitive -Trophic Ecosystem process Species abundances Abiotic Species traits ecosystem controls Figure 5 Mechanisms by which species interactions affect ecosystem processes.Global environmental change affects species interactions(mutualism,competition and trophic interactions)both directly(1)and through its effects on altered biodiversity.Species interactions may directly affect key traits (for example,the inhibition of microbial nitrogen fixation by plant secondary metabolites)in ecosystem processes(2)or may alter the abundances of species with key traits(3).Examples of these species interactions include (a)mutualistic consortia of microorganisms,each of which produces only some of the enzymes required to break down organic matter (photo by M.Klug).(b)altered abundances of native Califoria forbs due to competition from introduced European grasses (photo by H.Reynolds),and (c)alteration of algal biomass due to presence or absence of grazing minnows(photo by M. Power).Changes in species interactions and the resulting changes in community composition(3)may feedback to cause a cascade of further effects on species interactions(4). neighbours,which,in turn,affects nitrogen supply and plant in a community,the greater is the probability that at least some of growthStream predatory invertebratesalter the behaviour oftheir these species will survive stochastic or directional changes in envi- prey,making them more vulnerable to fish predation,which leads to ronment and maintain the current properties of the ecosystem an increase in the weight gain offish In the terrestrial realm,graz- This stability of processes has societal relevance.Many traditional ers can reduce grass cover to the point that avian predators keep vole farmers plant diverse crops,not to maximize productivity in a given populations at low densities,allowing the persistence of Erodium year,but to decrease the chances of crop failure in a bad year Even botrys,a preferred food ofvoles.The presence of E.botrysincreases the loss of rare species may jeopardize the resilience of ecosystems. leaching and increases soil moisture,which often limits produc- For example,in rangeland ecosystems,rare species that are function- tion and nutrient cycling in dry grasslands.These examples clearly ally similar to abundant ones become more common when grazing indicate that all types oforganisms-plants,animals and microor- reduces their abundant counterparts.This compensation in ganisms-must be considered in understanding the effects of response to release from competition minimizes the changes in biodiversity on ecosystem functioning.Although each of these ecosystem properties9. examples is unique to a particular ecosystem,the ubiquitous nature Species diversity also reduces the probability ofoutbreaks by 'pest' of species interactions with strong ecosystem effects makes these species by diluting the availability of their hosts.This decreases host- interactions a general feature of ecosystem functioning.In many specific diseasess,plant-feeding nematodess and consumption of cases,changes in these interactions alter the traits that are expressed preferredplant species.Insoils,microbialdiversitydecreases fungal by species and therefore the effects of species on ecosystem process- diseases owingto competitionand interference among microbess3 es.Consequently,simply knowing that a species is present or absent Resistance to invasions is insufficient to predict its impact on ecosystems. Biodiversity can influence the ability ofexotic species to invade com- Many global changes alter the nature or timing ofspecies interac- munities through either the influence of traits of resident species or tions".For example,the timing ofplant floweringand theemergence some cumulative effect of species richness.Early theoretical models of pollinating insects differ in their responses to warming,with and observations of invasions on islands indicated that species-poor potentially large effects on ecosystems and communities2. communities would be more vulnerable to invasions because they Plant-herbivore interactions in diverse communities are less likely offered more empty niches.However,studies of intact ecosystems to be disrupted by elevated CO2(ref.43)than in simple systems find both negative?and positive"correlations between species rich- involvingonespecialist herbivore andits host plant ness and invasions.This occurs in part because the underlying factors Resistance and resilience to change that generate differences in diversity(for example,propagule supply, The diversity-stability hypothesis suggests that diversity provides a disturbance regime and soil fertility)cannot be controlled and may general insurance policy that minimizes the chance of large ecosys- themselves be responsible for differences in invasibility.The tem changes in response to global environmental change.Microbial diversity effects on invasibility are scale-dependent in some cases.For microcosm experiments show less variability in ecosystem processes example,at theplotscale,wherecompetitive interactionsmightexert in communities with greater species richness",perhaps because their effect,increased plant diversity correlated with lower vulnera- everyspecieshasaslightly different response to its physicalandbiotic bility to invasion in Central Plains grasslands of the United States. environment.The larger the number of functionally similar species Across landscape scales,however,ecological factors that promote 238 2000 Macmillan Magazines Ltd NATURE VOL 40511 MAY 2000 www.nature.com
neighbours, which, in turn, affects nitrogen supply and plant growth36. Stream predatory invertebrates alter the behaviour of their prey, making them more vulnerable to fish predation, which leads to an increase in the weight gain of fish37. In the terrestrial realm, grazers can reduce grass cover to the point that avian predators keep vole populations at low densities, allowing the persistence of Erodium botrys, a preferred food of voles38. The presence of E. botrys increases leaching39 and increases soil moisture40, which often limits production and nutrient cycling in dry grasslands. These examples clearly indicate that all types of organisms — plants, animals and microorganisms — must be considered in understanding the effects of biodiversity on ecosystem functioning. Although each of these examples is unique to a particular ecosystem, the ubiquitous nature of species interactions with strong ecosystem effects makes these interactions a general feature of ecosystem functioning. In many cases, changes in these interactions alter the traits that are expressed by species and therefore the effects of species on ecosystem processes. Consequently, simply knowing that a species is present or absent is insufficient to predict its impact on ecosystems. Many global changes alter the nature or timing of species interactions41. For example, the timing of plant flowering and the emergence of pollinating insects differ in their responses to warming, with potentially large effects on ecosystems and communities42. Plant–herbivore interactions in diverse communities are less likely to be disrupted by elevated CO2 (ref. 43) than in simple systems involving one specialist herbivore and its host plant44. Resistance and resilience to change The diversity–stability hypothesis suggests that diversity provides a general insurance policy that minimizes the chance of large ecosystem changes in response to global environmental change45. Microbial microcosm experiments show less variability in ecosystem processes in communities with greater species richness46, perhaps because every species has a slightly different response to its physical and biotic environment. The larger the number of functionally similar species in a community, the greater is the probability that at least some of these species will survive stochastic or directional changes in environment and maintain the current properties of the ecosystem47. This stability of processes has societal relevance. Many traditional farmers plant diverse crops, not to maximize productivity in a given year, but to decrease the chances of crop failure in a bad year48. Even the loss of rare species may jeopardize the resilience of ecosystems. For example, in rangeland ecosystems, rare species that are functionally similar to abundant ones become more common when grazing reduces their abundant counterparts. This compensation in response to release from competition minimizes the changes in ecosystem properties49. Species diversity also reduces the probability of outbreaks by ‘pest’ species by diluting the availability of their hosts. This decreases hostspecific diseases50, plant-feeding nematodes51 and consumption of preferred plant species52. In soils, microbial diversity decreases fungal diseases owing to competition and interference among microbes53. Resistance to invasions Biodiversity can influence the ability of exotic species to invade communities through either the influence of traits of resident species or some cumulative effect of species richness. Early theoretical models and observations of invasions on islands indicated that species-poor communities would be more vulnerable to invasions because they offered more empty niches54. However, studies of intact ecosystems find both negative55 and positive56 correlations between species richness and invasions. This occurs in part because the underlying factors that generate differences in diversity (for example, propagule supply, disturbance regime and soil fertility) cannot be controlled and may themselves be responsible for differences in invasibility56. The diversity effects on invasibility are scale-dependent in some cases. For example, at the plot scale, where competitive interactions might exert their effect, increased plant diversity correlated with lower vulnerability to invasion in Central Plains grasslands of the United States. Across landscape scales, however, ecological factors that promote insight review articles 238 NATURE | VOL 405 | 11 MAY 2000 | www.nature.com Global changes Biodiversity Species abundances Species interactions Human activities and benefits Ecosystem goods and services – Mutualistic – Competitive – Trophic Species traits Abiotic ecosystem controls Ecosystem processes a b c 1 4 3 2 Figure 5 Mechanisms by which species interactions affect ecosystem processes. Global environmental change affects species interactions (mutualism, competition and trophic interactions) both directly (1) and through its effects on altered biodiversity. Species interactions may directly affect key traits (for example, the inhibition of microbial nitrogen fixation by plant secondary metabolites) in ecosystem processes (2) or may alter the abundances of species with key traits (3). Examples of these species interactions include (a) mutualistic consortia of microorganisms, each of which produces only some of the enzymes required to break down organic matter (photo by M. Klug), (b) altered abundances of native California forbs due to competition from introduced European grasses (photo by H. Reynolds), and (c) alteration of algal biomass due to presence or absence of grazing minnows84 (photo by M. Power). Changes in species interactions and the resulting changes in community composition (3) may feedback to cause a cascade of further effects on species interactions (4). © 2000 Macmillan Magazines Ltd
insight review articles Figure 6 Trophic interactions can affect ecosystem processes by influencing species'abundances. a,Removal of sea otters by Russian fur traders caused an explosion in the population of sea urchins that overgrazed kelp.(Photographs courtesy of M. Sewell/Still Pictures and J.Rotman/BBC Natural History Unit.)b.Similarly,changes in the species balance and the abundance of fish can deplete phytoplankton grazers and cause algal blooms.(Photograph courtesy of J. Foott/BBC Natural History Unit.) native plant diversity(for example,soil type and disturbance regime) changes in community composition and vulnerability to invasion. also promote species invasions37 Introduction ofexotic species or changes in community composition Experimentalstudies with plantsor soil microorganisms often can affect ecosystem goods or services either by directly reducing show that vulnerability to invasion is governed more strongly by the abundances of useful species (by predation or competition),or by traits of resident and invading species than by species richness per se. altering controls on critical ecosystem processes(Fig.4). Both competition and trophic interactions contribute to these effects These impacts can be wide-ranging and costly.For example,the of community composition on invasibility.For example,in its native introduction of deep-rooted species in arid regions reduces supplies range,the Argentine ant (Linepithaema humile)is attacked by and increases costs of water for human use.Marginal water losses to species-specific parasitoids that modify its behaviour and reduce its the invasive star thistle,Centaurea solstitialis,in the Sacramento River ability to dominate food resources and competitively exclude other valley,California,have been valued at US$16-56million per year(J.D. ant species.These parasitoids are absent from the introduced range Gerlach,unpublished results)(Fig.7).In South Africa's Cape region, of Argentine ants,which may explain their success at eliminating the presence of rapidly transpiring exotic pines raises the unit cost of native ant communities in North America.Observational and water procurement by nearly 30%(ref.62).Increased evapotranspi- experimental studies together indicate that the effect of species ration due to the invasion of Tamarix in the United States costs an diversity on vulnerability to invasion depends on the components of estimated $65-180 million per year in reduced municipaland agricul- diversity involved (richness,evenness,composition and species tural water supplies In addition to raising water costs,the presence interactions)and their interactions with other ecological factors such of sediment-trapping Tamarix stands has narrowed river channels as disturbance regime,resource supply and rate of propagule arrival. and obstructed over-bank flows throughout the western United Humans significantly affect all of these factors (Figs 1,4),thereby States,increasing flood damages by as much as $50 million annually3 dramatically increasing the incidence of invasions worldwide. Those species changes that have greatest ecological impact frequently incur high societal costs.Changes in traits maintaining Societal consequences of altered diversity regional climate2 constitute an ecosystem service whose value in Biodiversity and its links to ecosystem properties have cultural, tropical forests has been estimated at $220 hayr(ref.64).The loss intellectual,aesthetic and spiritual values that are important to or addition of species that alter disturbance regimes can also be society.In addition,changes in biodiversity that alter ecosystem func- costly.The increased fire frequency resulting from the cheatgrass tioning have economic impacts through the provision of ecosystem invasion in the western United States has reduced rangeland values goods and services to society(Fig.I and Box 2).Changes in diversity and air quality and led to increased expenditures on fire suppres- can directly reduce sources of food,fuel,structural materials,medici- sion.The disruption of key species interactions can also have large nals or genetic resources.These changes can also alter the abundance societal and ecological consequences.Large populations ofpassenger of other species that control ecosystem processes,leading to further pigeons (Ectopistes migratorius)in the northeastern United States NATURE|VOL 40511 MAY 2000www.nature.com 2000 Macmillan Magazines Ltd 239
native plant diversity (for example, soil type and disturbance regime) also promote species invasions57. Experimental studies with plants58 or soil microorganisms59 often show that vulnerability to invasion is governed more strongly by the traits of resident and invading species than by species richness per se. Both competition and trophic interactions contribute to these effects of community composition on invasibility. For example, in its native range, the Argentine ant (Linepithaema humile) is attacked by species-specific parasitoids that modify its behaviour and reduce its ability to dominate food resources and competitively exclude other ant species60. These parasitoids are absent from the introduced range of Argentine ants, which may explain their success at eliminating native ant communities in North America61. Observational and experimental studies together indicate that the effect of species diversity on vulnerability to invasion depends on the components of diversity involved (richness, evenness, composition and species interactions) and their interactions with other ecological factors such as disturbance regime, resource supply and rate of propagule arrival. Humans significantly affect all of these factors (Figs 1, 4), thereby dramatically increasing the incidence of invasions worldwide. Societal consequences of altered diversity Biodiversity and its links to ecosystem properties have cultural, intellectual, aesthetic and spiritual values that are important to society. In addition, changes in biodiversity that alter ecosystem functioning have economic impacts through the provision of ecosystem goods and services to society (Fig. 1 and Box 2). Changes in diversity can directly reduce sources of food, fuel, structural materials, medicinals or genetic resources. These changes can also alter the abundance of other species that control ecosystem processes, leading to further changes in community composition and vulnerability to invasion. Introduction of exotic species or changes in community composition can affect ecosystem goods or services either by directly reducing abundances of useful species (by predation or competition), or by altering controls on critical ecosystem processes (Fig. 4). These impacts can be wide-ranging and costly. For example, the introduction of deep-rooted species in arid regions reduces supplies and increases costs of water for human use. Marginal water losses to the invasive star thistle, Centaurea solstitialis, in the Sacramento River valley, California, have been valued at US$16–56 million per year (J. D. Gerlach, unpublished results) (Fig. 7). In South Africa’s Cape region, the presence of rapidly transpiring exotic pines raises the unit cost of water procurement by nearly 30% (ref. 62). Increased evapotranspiration due to the invasion of Tamarix in the United States costs an estimated $65–180 million per year in reduced municipal and agricultural water supplies63. In addition to raising water costs, the presence of sediment-trapping Tamarix stands has narrowed river channels and obstructed over-bank flows throughout the western United States, increasing flood damages by as much as $50 million annually63. Those species changes that have greatest ecological impact frequently incur high societal costs. Changes in traits maintaining regional climate22 constitute an ecosystem service whose value in tropical forests has been estimated at $220 ha–1 yr–1 (ref. 64). The loss or addition of species that alter disturbance regimes can also be costly. The increased fire frequency resulting from the cheatgrass invasion in the western United States has reduced rangeland values and air quality and led to increased expenditures on fire suppression65. The disruption of key species interactions can also have large societal and ecological consequences. Large populations of passenger pigeons (Ectopistes migratorius) in the northeastern United States insight review articles NATURE | VOL 405 | 11 MAY 2000 | www.nature.com 239 a b Figure 6 Trophic interactions can affect ecosystem processes by influencing species’ abundances. a, Removal of sea otters by Russian fur traders caused an explosion in the population of sea urchins that overgrazed kelp. (Photographs courtesy of M. Sewell/Still Pictures and J. Rotman/BBC Natural History Unit.) b, Similarly, changes in the species balance and the abundance of fish can deplete phytoplankton grazers and cause algal blooms. (Photograph courtesy of J. Foott/BBC Natural History Unit.) © 2000 Macmillan Magazines Ltd
insight review articles may once have controlled Lyme tick-bearing mice by out-competing Box 2 them for food".The loss of the passenger pigeon to nineteenth- Ecosystem services century over-hunting may,therefore,have contributed to the rise of Lyme disease in humans in the twentieth century.The economic Ecosystem services are defined as the processes and conditions of impacts of invasions of novel species are particularly well document- natural ecosystems that support human activity and sustain human ed.The introduction and spread of single pests such as the golden life.Such services include the maintenance of soil fertility,climate apple snail (Pomacea canaliculata)and the European corn borer regulation and natural pest control,and provide flows of ecosystem (Ostrinia nubilalis)have had major impacts on food production and goods such as food,timber and fresh water.They also provide farm incomes.Estimates of the overall cost of invasions by exotic intangible benefits such as aesthetic and cultural values species in the United States range widely from $1.1 to $137 billion Ecosystem services are generated by the biodiversity present in annually.70.In Australia,plant invasions alone entail an annual cost natural ecosystems.Ecologists and economists have begun to ofUS$2.1 billion" quantify the impacts of changes in biodiversity on the delivery of The provision of tangible ecosystem goods and services by ecosystem services and to attach monetary value to these changes. natural systems depends not only on species'presence or absence Techniques used to attach value to biodiversity change range from but also on their abundance.Large populations ofthe white-footed direct valuation based on market prices to estimates of what mouse (Peromyscus leucopus)in the northeastern United States individuals are willing to pay to protect endangered wildlife control outbreaks of gypsy moth (Lymatria dispar)but spread Although there are estimates of the global values of ecosystem Lyme disease,whereas small populations of the mouse decrease the services,valuation of the marginal losses that accompany specific incidence of Lyme disease but allow gypsy moth defoliation2.An biodiversity changes are most relevant to policy decisions. analysis of the costs of changes in biodiversity thus involves more Predicting the value of such losses involves uncertainty,because than just analysis ofextinctions and invasions.Theloss ofa species ecological and societal systems interact in nonlinear ways and to extinction is of special societal concern,however,because it is because human preferences change through time.Assumptions irreversible.Future opportunities to learn and derive newly recog- today about future values may underestimate the values placed on nized benefits from an extinct species are lost forever.Preventing natural systems by future generations.Therefore,minimizing loss such a loss preserves an 'option value'for society-the value of of biodiversity offers a conservative strategy for maintaining this attaining more knowledge about species and their contribution to value. human well being in order to make informed decisions in the future4 For example,significant value($230-330 million)has been attributed to genetic information gained from preventing Global environmental changes have the potential to exacerbate land conversion in Jalisco,Mexico,in an area containing a wild the ecological and societal impacts of changes in biodiversity In grass,teosinte (Euchlaena mexicana),that can be used to develop many regions,land conversion forces declining populations towards viral-resistant strains ofperennial corn.Ifthis land had been con- the edges of their species range,where they become increasingly verted to agriculture or human settlements,the societal benefits of vulnerable to collapse if exposed to further human impact?.Warm- development would have come at the expense ofan irreversible loss ing allows the poleward spread of exotics and pathogens,such as in genetic material that could be used for breeding viral resistance dengue-and malaria-transmitting mosquitoes(Aedesand Anopheles in one of the most widely consumed cereal crops in the world.The sp.)%6and pests of key food crops,such as corn-boring insects perceived costs of diversity loss in this situation might have been Warming can also exacerbate the impacts of water-consuming small-especially relative to the development benefits-whereas invasive plant species in water-scarce areas by increasing regional the actual (unrecognized)costs of losing genetic diversity would water losses.The Tamarix-invaded Colorado River in the United have been significant(Fig.8).Decisions to preserve land to gain States currently has a mean annual flow that is 10%less than regional further information about the societal value of species diversity or water allocations for human use.Warming by4'Cwould reduce the ecosystem function typically involve a large degree of uncertainty, flow of the Colorado River by more than 20%,further increasing the which often leads to myopic decisions regarding land use. marginal costs of water losses to Tamarix?s.Similar impacts ofglobal change in regions such as Sahelian Africa,which have less water and less well developed distribution mechanisms,might directly affect Figure 7 Water losses to human survival.In many cases,accelerated biodiversity loss is the invasive,deep-rooted alreadyjeopardizing thelivelihoods oftraditionalpeoples star thistle,C.solstitialis, The combination of irreversible species losses and positive provides an example of feedbacks between biodiversity changes and ecosystem processes are the financial impacts of likely to cause nonlinear cost increases to society in the future,partic- introducing exotic species ularly when thresholds of ecosystem resilience are exceeded.For on ecosystem example,Imperata cylindrica,an aggressive indigenous grass, composition.(Photograph colonizes forest lands of Asia that are cleared for slash-and-burn courtesy of P.Collins/A-Z agriculture,forminga monoculture grassland with no vascular plant Botanical Collection.) diversity and many fewer mammalian species than the native forest. The total area of Imperata in Asia is currently about 35 million ha(4% of land area).Once in place,Imperata is difficult and costly to remove and enhances fire,which promotes the spread of the grass. The annual cost of reversing this conversion in Indonesia,where 4% of the nation's area(8.6 million ha)is now in Imperata grasslands, would be over $400 million if herbicides are used,and $1.2 billion if labour is used to remove the grass manually.Farmers typically burn the fields because herbicides and labour are too expensive.Burning these grasslands,however,increases losses of soil nitrogen and carbon,which erode agricultural productivity,and enhances regen- eration of Imperata.This positive feedback with nonlinear changes in land cover will probably continue in the future aslands are deforested 240 2000 Macmillan Magazines Ltd NATURE VOL 405|11 MAY 2000 www.nature.com
may once have controlled Lyme tick-bearing mice by out-competing them for food66. The loss of the passenger pigeon to nineteenthcentury over-hunting may, therefore, have contributed to the rise of Lyme disease in humans in the twentieth century. The economic impacts of invasions of novel species are particularly well documented. The introduction and spread of single pests such as the golden apple snail (Pomacea canaliculata) and the European corn borer (Ostrinia nubilalis) have had major impacts on food production and farm incomes67,68. Estimates of the overall cost of invasions by exotic species in the United States range widely from $1.1 to $137 billion annually69,70. In Australia, plant invasions alone entail an annual cost of US$2.1 billion71. The provision of tangible ecosystem goods and services by natural systems depends not only on species’ presence or absence but also on their abundance. Large populations of the white-footed mouse (Peromyscus leucopus) in the northeastern United States control outbreaks of gypsy moth (Lymatria dispar) but spread Lyme disease, whereas small populations of the mouse decrease the incidence of Lyme disease but allow gypsy moth defoliation72. An analysis of the costs of changes in biodiversity thus involves more than just analysis of extinctions and invasions. The loss of a species to extinction is of special societal concern, however, because it is irreversible. Future opportunities to learn and derive newly recognized benefits from an extinct species are lost forever. Preventing such a loss preserves an ‘option value’ for society — the value of attaining more knowledge about species and their contribution to human well being in order to make informed decisions in the future73,74. For example, significant value ($230–330 million) has been attributed to genetic information gained from preventing land conversion in Jalisco, Mexico, in an area containing a wild grass, teosinte (Euchlaena mexicana), that can be used to develop viral-resistant strains of perennial corn73. If this land had been converted to agriculture or human settlements, the societal benefits of development would have come at the expense of an irreversible loss in genetic material that could be used for breeding viral resistance in one of the most widely consumed cereal crops in the world. The perceived costs of diversity loss in this situation might have been small — especially relative to the development benefits — whereas the actual (unrecognized) costs of losing genetic diversity would have been significant (Fig. 8). Decisions to preserve land to gain further information about the societal value of species diversity or ecosystem function typically involve a large degree of uncertainty, which often leads to myopic decisions regarding land use. Global environmental changes have the potential to exacerbate the ecological and societal impacts of changes in biodiversity6 . In many regions, land conversion forces declining populations towards the edges of their species range, where they become increasingly vulnerable to collapse if exposed to further human impact75. Warming allows the poleward spread of exotics and pathogens, such as dengue- and malaria-transmitting mosquitoes (Aedes and Anopheles sp.)76 and pests of key food crops, such as corn-boring insects68. Warming can also exacerbate the impacts of water-consuming invasive plant species in water-scarce areas by increasing regional water losses. The Tamarix-invaded Colorado River in the United States currently has a mean annual flow that is 10% less than regional water allocations for human use77. Warming by 4˚C would reduce the flow of the Colorado River by more than 20%, further increasing the marginal costs of water losses to Tamarix78. Similar impacts of global change in regions such as Sahelian Africa, which have less water and less well developed distribution mechanisms, might directly affect human survival. In many cases, accelerated biodiversity loss is already jeopardizing the livelihoods of traditional peoples79. The combination of irreversible species losses and positive feedbacks between biodiversity changes and ecosystem processes are likely to cause nonlinear cost increases to society in the future, particularly when thresholds of ecosystem resilience are exceeded80. For example, Imperata cylindrica, an aggressive indigenous grass, colonizes forest lands of Asia that are cleared for slash-and-burn agriculture, forming a monoculture grassland with no vascular plant diversity and many fewer mammalian species than the native forest. The total area of Imperata in Asia is currently about 35 million ha (4% of land area)81. Once in place, Imperata is difficult and costly to remove and enhances fire, which promotes the spread of the grass. The annual cost of reversing this conversion in Indonesia, where 4% of the nation’s area (8.6 million ha) is now in Imperata grasslands, would be over $400 million if herbicides are used, and $1.2 billion if labour is used to remove the grass manually. Farmers typically burn the fields because herbicides and labour are too expensive. Burning these grasslands, however, increases losses of soil nitrogen and carbon, which erode agricultural productivity, and enhances regeneration of Imperata. This positive feedback with nonlinear changes in land cover will probably continue in the future as lands are deforested insight review articles 240 NATURE | VOL 405 | 11 MAY 2000 | www.nature.com Figure 7 Water losses to the invasive, deep-rooted star thistle, C. solstitialis, provides an example of the financial impacts of introducing exotic species on ecosystem composition. (Photograph courtesy of P. Collins/A-Z Botanical Collection.) Ecosystem services are defined as the processes and conditions of natural ecosystems that support human activity and sustain human life. Such services include the maintenance of soil fertility, climate regulation and natural pest control, and provide flows of ecosystem goods such as food, timber and fresh water. They also provide intangible benefits such as aesthetic and cultural values88. Ecosystem services are generated by the biodiversity present in natural ecosystems. Ecologists and economists have begun to quantify the impacts of changes in biodiversity on the delivery of ecosystem services and to attach monetary value to these changes. Techniques used to attach value to biodiversity change range from direct valuation based on market prices to estimates of what individuals are willing to pay to protect endangered wildlife89. Although there are estimates of the global values of ecosystem services64, valuation of the marginal losses that accompany specific biodiversity changes are most relevant to policy decisions. Predicting the value of such losses involves uncertainty, because ecological and societal systems interact in nonlinear ways and because human preferences change through time. Assumptions today about future values may underestimate the values placed on natural systems by future generations89. Therefore, minimizing loss of biodiversity offers a conservative strategy for maintaining this value. Box 2 Ecosystem services © 2000 Macmillan Magazines Ltd
insight review articles the most vulnerableareas In sum,these examples indicate a tight coupling between altered species diversity,ecosystem function and societal costs.A pressing task for ecologists,land managers and environmental policy makers is to determine where and when such tight couplings exist.Policies to safeguard ecosystem services must be able to respond dynamically to new knowledge,the rapidly changing global environment,and evolv- ingsocietal needs.Nonlinearity,uncertainty andirreversibilitycall for Time a more aggressive approach to mitigating changes in biodiversity than is now being pursued so that future options are not foreclosed. Conclusion We are in the midst ofone of the largest experiments in the history of the Earth.Human effects on climate,biogeochemical cycles,land use and mobility oforganisms have changed the local and global diversi- ty ofthe planet,with important ecosystem and societal consequences (Fig.1).The most important causesofalteredbiodiversityare factors Time that can be regulated by changes in policy:emissions of greenhouse gases,land-use change and species introductions.In the past,the international community has moved to reduce detrimental human impacts with unambiguous societal consequences.For example,the Montreal Protocol prohibited release of chlorofluorocarbons in response to evidence that these chemicals caused loss of ozone and increased levels of cancer-producing UV-B radiation.Strong evidence for changes in biodiversity and its ecosystem and societal consequences calls for similar international actions.We urge the Time following blueprint for action. The scientific community should intensify its efforts to identify Figure 8 Ecosystem and societal consequences of changes in biodiversity.a,A linear the causes of nonlinearities and thresholds in the response of change in biodiversity through time.b,This change might(1)induce a linear response ecosystem and social processes to changes in biodiversity. in ecosystem processes,(2)have increasingly large impacts on ecosystem functioning, The scientific community and informed citizens should become yielding exponential ecosystem change through time,or(3)exhibit abrupt thresholds engaged in conveying to the public,policy-makers and land man- owing to the loss of a keystone species,the loss of the last member of a key functional agers the enormity and irreversibility of current rapid changes in group,or the addition of a new species trait.c.Even if ecosystem response to diversity biodiversity.Despite convincing scientific evidence,there is a changes is linear,associated societal costs through time may respond nonlinearly. general lack of public awareness that change in biodiversity is a Departures from a linear increase(1)in societal costs over time might include larger global change with important ecological and societal impacts and cost increases(2)associated with each additional unit of change in ecosystem that these changes are not amenable to mitigation after they have processes,yielding an exponential cost curve through time.Reductions of resource occurred. supply below threshold levels may induce step increases in societal costs(3a),such as Managers should consider the ecological and social consequences reductions in water supply below the point where all consumers have aocess to enough of biodiversity change at all stages in land-use planning.For for desired uses.If changes in resource supply or ecosystem processes exceed example,environmental impact assessments should consider thresholds for supporting large segments of society,stepwise cost increases may be both the current costs of ecosystem services that will be lost and unmeasurable or essentially infinite (3b).The perceived ecological changes and societal the risk of nonlinear future change.Managed landscapes can costs of diversity change may be small(4).Actual,unrecognized costs may be far higher support a large proportion of regional biodiversity with proper (ines 1,2 and 3)and discovered only later as lost option values.Conservation of planning,management and adaptive responses. biodiversity can help avoid such negative ecological and economic'surprises' Scientists and other citizens should collaborate with governmen- tal organizations,from local to national levels,in developing and implementing policies and regulations that reduce environmen- for timber and agricultural purposes,causing further declines in tal deterioration and changes in biodiversity.For example,more regional biodiversity. stringent restrictions on the import ofbiotic materials could curb Uncertainty related to positive feedbacks and nonlinear changes the rate of biotic invasions,and improved land and watershed in land cover and biodiversity make social adaptation to change more management could reduce their rates ofspread. difficult and costly(Fig.8).It may be more important from an ● A new international body that would be comparable to the Inter- economic perspective to understand the nature and timing of rapid governmental Panel on Climate Change (IPCC)should assess or nonlinear changes in societal costs caused by loss of biodiversity changes in biodiversity and their consequences as an integral and associated ecosystem services than it is to predict average conse- component of the assessment of the societal impacts of global quences of current trends of species decline.By analogy,economic change. models of ecological 'surprises'in response to climatic change show Internationalbodies should establish andimplement agreements that the information about the nonlinearities in damage from warm- such as the Convention on Biological Diversity that institute ing is worth up to six times more than information about current mechanisms for reducing activities that drive the changes in trends in damage levels.In the Imperata example,the costs of biodiversity.These activities include fossil-fuel emissions, replacing the original ecosystem goods and services from the forest land-use change and biotic introductions. Q -including timber products,fire stability and soil nutrients- -rise 1.Postel,S.L.Daily,G.C.&Ehrlich,P.R.Human appropriation of renewable fresh water.Science 271. sharply as Imperata spreads.If these nonlinearities in the ecological 785-788119961. and economic effects of this conversion had been anticipated, 2.Vitousek,P.M.,Mooney,H.A.,Lubchenco,).Melillo,)M.Human domination of Farth's policies could have been implemented to encourage agroforestry ecosystems.Science277,494-499(1997). instead of rice production or to reduce migration and settlement in 3.Kattenberg.A.etal in Climate Change 1995.The Science ofClimate Change(ed.Houghton,I.T.) 285-357(Cambridge Univ.Press,Cambridge,1996). NATURE|VOL 40511 MAY 2000 www.nature.com 2000 Macmillan Magazines Ltd 241
for timber and agricultural purposes, causing further declines in regional biodiversity. Uncertainty related to positive feedbacks and nonlinear changes in land cover and biodiversity make social adaptation to change more difficult and costly (Fig. 8). It may be more important from an economic perspective to understand the nature and timing of rapid or nonlinear changes in societal costs caused by loss of biodiversity and associated ecosystem services than it is to predict average consequences of current trends of species decline. By analogy, economic models of ecological ‘surprises’ in response to climatic change show that the information about the nonlinearities in damage from warming is worth up to six times more than information about current trends in damage levels82. In the Imperata example, the costs of replacing the original ecosystem goods and services from the forest — including timber products, fire stability and soil nutrients — rise sharply as Imperata spreads. If these nonlinearities in the ecological and economic effects of this conversion had been anticipated, policies could have been implemented to encourage agroforestry instead of rice production or to reduce migration and settlement in the most vulnerable areas83. In sum, these examples indicate a tight coupling between altered species diversity, ecosystem function and societal costs. A pressing task for ecologists, land managers and environmental policy makers is to determine where and when such tight couplings exist. Policies to safeguard ecosystem services must be able to respond dynamically to new knowledge, the rapidly changing global environment, and evolving societal needs. Nonlinearity, uncertainty and irreversibility call for a more aggressive approach to mitigating changes in biodiversity than is now being pursued so that future options are not foreclosed. Conclusion We are in the midst of one of the largest experiments in the history of the Earth. Human effects on climate, biogeochemical cycles, land use and mobility of organisms have changed the local and global diversity of the planet, with important ecosystem and societal consequences (Fig. 1). The most important causes of altered biodiversity are factors that can be regulated by changes in policy: emissions of greenhouse gases, land-use change and species introductions. In the past, the international community has moved to reduce detrimental human impacts with unambiguous societal consequences. For example, the Montreal Protocol prohibited release of chlorofluorocarbons in response to evidence that these chemicals caused loss of ozone and increased levels of cancer-producing UV-B radiation. Strong evidence for changes in biodiversity and its ecosystem and societal consequences calls for similar international actions. We urge the following blueprint for action. ● The scientific community should intensify its efforts to identify the causes of nonlinearities and thresholds in the response of ecosystem and social processes to changes in biodiversity. ● The scientific community and informed citizens should become engaged in conveying to the public, policy-makers and land managers the enormity and irreversibility of current rapid changes in biodiversity. Despite convincing scientific evidence, there is a general lack of public awareness that change in biodiversity is a global change with important ecological and societal impacts and that these changes are not amenable to mitigation after they have occurred. ● Managers should consider the ecological and social consequences of biodiversity change at all stages in land-use planning. For example, environmental impact assessments should consider both the current costs of ecosystem services that will be lost and the risk of nonlinear future change. Managed landscapes can support a large proportion of regional biodiversity with proper planning, management and adaptive responses. ● Scientists and other citizens should collaborate with governmental organizations, from local to national levels, in developing and implementing policies and regulations that reduce environmental deterioration and changes in biodiversity. For example, more stringent restrictions on the import of biotic materials could curb the rate of biotic invasions, and improved land and watershed management could reduce their rates of spread. ● A new international body that would be comparable to the Intergovernmental Panel on Climate Change (IPCC) should assess changes in biodiversity and their consequences as an integral component of the assessment of the societal impacts of global change. ● International bodies should establish and implement agreements such as the Convention on Biological Diversity that institute mechanisms for reducing activities that drive the changes in biodiversity. These activities include fossil-fuel emissions, land-use change and biotic introductions. ■ 1. Postel, S. L., Daily, G. C. & Ehrlich, P. R. Human appropriation of renewable fresh water. Science 271, 785–788 (1996). 2. Vitousek, P. M., Mooney, H. A., Lubchenco, J. & Melillo, J. M. Human domination of Earth’s ecosystems. Science 277, 494–499 (1997). 3. Kattenberg, A. et al. in Climate Change 1995. The Science of Climate Change(ed. Houghton, J. T.) 285–357 (Cambridge Univ. Press, Cambridge, 1996). insight review articles NATURE | VOL 405 | 11 MAY 2000 | www.nature.com 241 Change in biodiversity Cost to society Ecosystem functioning/ processes Time Time Time a b c 1 3 2 1 3b 3a 2 4 Figure 8 Ecosystem and societal consequences of changes in biodiversity. a, A linear change in biodiversity through time. b, This change might (1) induce a linear response in ecosystem processes, (2) have increasingly large impacts on ecosystem functioning, yielding exponential ecosystem change through time, or (3) exhibit abrupt thresholds owing to the loss of a keystone species, the loss of the last member of a key functional group, or the addition of a new species trait. c, Even if ecosystem response to diversity changes is linear, associated societal costs through time may respond nonlinearly. Departures from a linear increase (1) in societal costs over time might include larger cost increases (2) associated with each additional unit of change in ecosystem processes, yielding an exponential cost curve through time. Reductions of resource supply below threshold levels may induce step increases in societal costs (3a), such as reductions in water supply below the point where all consumers have access to enough for desired uses. If changes in resource supply or ecosystem processes exceed thresholds for supporting large segments of society, stepwise cost increases may be unmeasurable or essentially infinite (3b). The perceived ecological changes and societal costs of diversity change may be small (4). Actual, unrecognized costs may be far higher (lines 1, 2 and 3) and discovered only later as lost option values. Conservation of biodiversity can help avoid such negative ecological and economic ‘surprises’. © 2000 Macmillan Magazines Ltd
insight review articles 4.Pimm,S.L.Russell,G..Gittleman,I.L.Brooks,T.M.The future of biodiversity.Science269. Hill New York 19901 347-350(1995) 49.Walker,B..Kinzig.A&Langridge.I Plant attribute diversity,resilience,and ecosystem function:the Lawton..H.&May.R.M.Extinction Rates(Oxford Univ.Press,Oxford,1995) nature and significance of dominant and minor species.Ecosystems 2,95-113(1999). 6.Sala,O.E et al.Global biodiversity scenarios for the year 2100.Science 287,1770-1776(2000). 50.Burdon,I.I.The structure of pathogen populations in natural plant communities.Arm Rev. 7.Lawton,I.H.What do species do in ecosystems?Oiks71,367-374(1994). Phytopathol.31,5-323(1993). 8.Tilman,D.,Wedin,D.Knops,I.Productivity and sustainability influenced by biodiversity in 51.Wasilewska,L.Differences in development of soil nematode communities in single-and multi- grassland ecosystems.Natcre379,718-720(1996). species grass experimental treatments.Appl.Soil Ecol.2,53-64(1995). 9.Hector.Pant diversity and productivity experiments in European 52.Bertness,M.D.&Leonard,G.H.The role ofpositive interactions in communities:lessons from 1123-1127(1999). intertidal habitats.Ecology78,1976-1989(1997) 10.van der Heijden,M.G.A.ctal Mycorrhiral fungal diversity determines plant biodiversity.ecosystem 53.Nitta.T.Diversity of root fungal floras its implications for soil-borne diseases and crop growth.lap. variability and productivity.Nanre69-72(1998) Agric.Res.Quart.25,6-11(1991). 11.Salonius,P.O.Metabolic capabalities of forest soil microbial populations with reduced species 54.Elton,C.S.The Ecology of Imvasions by Animals and Plants (Methuen,London,1958). diversity.Soil Biol.Biochem.13.I-10 (1981). 55.Tilman,D.Community invasibility.recruitment limitation,and grassland biodiversity.Ecology 78, 12.Wardle,D.A.Bonner,K.1&Nicholson,K.$.Biodiversity andplant litter:experimental evidence 81-92(1997. which does not support the view that enhanced species richness improves ecosystem function.Oikos 56.Levine,I.M.D'Antonio.C.M.Elton revisited:a review ofevidence linking diversity and 79,247-258(1997). invasibility.Oikos 87.15-26(1999). 13.Hooper,D.U.&Vitousek,M.The effects of plant diversityon of native plant diversity.Ecol Monogr.69. processes..Science277.1302-1305(1997). 25-46(1999). 14.Tilman,D.etal The influence of functional diversity and composition on ecosystem processes 58.Lavorel,S.Prieur-Richard.A.-H.Grig vasibility and diversity of plant communities:from Science277,1300-1302(1997). patterns to processes.Diverstfy Distnb.5,41-49 (1999). 15.Vitousek,P.M.,Walker,L R.,Whiteaker,L D..Mueller-Dombois,D.Matson,P.A.Biological 59.McGrady-Steed,J,Harris,P.M.Morin,P.I Biodiversity regulates ecosystem predictability.Nature invasion by development in Hawaii Science38,82-84(1987). 390162-16519971 16.Berry.W.LCharacteristics of salts secreted by Tamarix.Am .Bot.57,1226-1230(1970). 60.Or.M.R.&Seike,S.H.Parasitoids deter foraging by Argentine ants (Linepithema humile)in their 17.Christian,J.M.&Wilson,S.D.Long-term impactsof an introduced grass in the northern Great native habitat in Brazil.Oecologia 117,420-425(1998). Plains.Ecology 80,2397-2407(199) 61.Holway.D.A.Competitive isms underlying the displa ants by the invasive 18.Lavelle,P.,Bignell,D.Lepage,M.Soil function in achanging world:the role ofinvertebrate Argentine ant.Fcology80,238-251 (1999). ecosystem engineers.Fuer.I.Soil Biol.33,159-193(1997). 62.Van Wilgen,B.W,Cowling.R.M.Burgers,C.I.Valuation of ecosystem services:a case study from 19.D'Antonio,C.M.&Vitousek,P M.Biological invasionsby exotic grasses,the grass-fire cycle,and South African fynbos ecosystems.BioScienc 46,184-189(1996). global change.Amnu.Rev Erol.Syst 23,63-87 (1992). 63.Zavaleta,E.S.in asive SpeciesinChanging World(eds Hobbs,R&Mooney.H.A)(Island. 20.Whisenant,S.Changing Fire Frequencies on Idaho's Snake River Plains Ecological Man Washington DC.in the press) Implicrtion4-10(US Forest Service General Technical Report INT-276,Washington,1990) 64.Costanz R.et al The value of the world's ecosys es and natural capital.Nature387 21.Van Cleve,K.,Chapin,F.S.III,Dryness,C.T.Viereck,L.A.Element cycling in taiga forest:state- 253-260(1997). factor control.Bioscience 41.78-88 (1991). 65 Stewart G.&Hull A.C Cheats tass Bro an ecological intruder in southern 22 Shukla,Nobre,C.&Sellers,P.Amazon deforestation 247,1322-1325 Idsho.Ecology 30,58-74(1949) 〔19901. 66.Blockstein.D.E.Letter to the editor.Science 279,1831(1998). 23.Foley,I.A.,Kutzbach,I.E..Coe,M.T.Levis,S.Feedbacks between climate and boreal forests 67.Naylor,R.1 Invasions inagriculture:a sing the cost of the golden apple snail in Asia.Ambio25. during the Holocene epoch.Nature371,52-54(1994). 443-448(1996). 24.de Ruiter,P.C..Neutel,A.Moore,J.C.Energetics,patterns of interaction strengths,and stability in 68.Porter,I.H,Parry.M.L.Carter,T.R.The potential effects of climatic change on agricultural insect real ecosystems.Science269,1257-1260(1995). pests.Agric.For.Meteorol.57,221-240(1991). 25.Power,M.E.etal.Challenges in the quest for keystones.BioScience 46,609(1996) 69.Pimentel,D.,Lach,L.Zuniga,R.Morrison,D.Environmental and economic costs of 26.Read,D.J.Mycorrhizasin ecosystems.Experientia 47,376-391(1991). nonindiginous species in the United States.BioScience 50,53-65(2000). 27.Paerl,H.W.&Pinckney,LA mini-review of microbial consortia:their roles in aquatic production 70.USOT Assessment Harmful Non-indigenous Species in the United States(US Government Printing and biogeochemical cycling.Microbial Ecol31,225-247(1996). Office,Washington,1993). 28.Estes,)A.Palmisano,.F.Sea otters:their role in structuring nearshore communities.Science 185. 71.Thorp,)The National Weeds Strategy:A Strategic Approach to Weed Problems of National Significance 1058-1060(1974). (Agric 29.Estes,J.A.,Tinker,M.T.,Williams,T.M.Doak,D.F.Killer whale predation on sea otters linking 72.Jones,C.G Ostfeld,R.$Richard,M.P..Schauber,E.M.Wolff,J.O.Chain reactions linking oceanic and nearshore ecosystems.Science282.473-476 (1998). sy moth outbreaks and Lyme disease risk.Scence279.1023-1026(1998). 30.Mork,M.The effect ofkelp in wave damping.Sa i80,323-327(1996) 73.Fisher,A.C&Haneman W.M.Option value and the extinction of Appl Micr-Eco 31.Schindler,D.E..Carpenter,S.R,Cole,I.L,Kitchell,I.F.Pace,M.L.Influence of food web structure 4.169-190(1986). on carbon exchange between lakes and the atmosphere.Science 277,248-251(1997). 74.Naylor,R.L in Imusive Speries in a Changing World(eds Hobbs,R.Mooney,H.A.)(Island. in the press). grazing.Ecology 78,588-602(1997). 75.Channell,R&Lomolino,M.V.Dynamic biogeography and conservation of endangered species. aure40384-862000). Soil Biol Biochem.17,181-187(1985). 76.Bryan.I.H.Foley.D.H.&Suthe st,R.W.Mal and climate change in Australia 34.Zimov,S.A.etal Steppe-tundra transition:an herbivore-driven biome shift at the end of the Me显L.Ast.164.345-347(1996). Pleistocene Am.Nat.146,765-794(1995). 77.Morrison,I.1.The Sustainable Useo Colorado River Basin(Pacific Institute and 35.Chanway.C.P.,Turkington,R&Holl,F B.Ecological implications of specificity between plants and the Global Water Policy Project,Oakland,1996). thizosphere micro-organisms.Adhv.Ecol.Res.21,121-169(1991). 78.Zavaleta,E.S.The emergence ofwaterfowl conservation among Yup'ik hunters in the Yukon- 36.Lawley.R.A..Newman,E.I.&Campbell,R.Abundance ofendomye Kuskokwim Delta Alaska Humt Ecol 27.231-266 (2000) microorganismson three grasses grown separately and in mixtures.Sol Biol Biochem.14,237-240 79.Warren.D.M.&Pinkston.in Linking Social and Ecological Systems (eds&Folke.C. 19821 158-189 (Cambridge Univ.Press,Cambridge,1998). 37.Soluck,D.A&Richardson..S The role of stoneflies in enhancing growth oftrout:a test of the 80.Schlesinger.W.H.etal Biological feedbacks in global desertification.Science 247,1043-1048(1990 importance of predator-predator facilitation within a stream community.Oikos80.214-219 (1997) 81.Garrity.D.P.et al The Imperata grasslands of tropical Asia:area.distribution.and typology.Agrofor. 38.Rice,K.I.Interaction of disturbance patch size and herbivory in Erodiumcoloniration.Ecology 68, 1xt361-29‘1997 1113-1115(1987 82.Peck,S.C.&Teisberg.T.in Assesing Surprises and Nonlin 39.Shock.C.C..lones M.B..Williams.W.A.&Center.D.M.Competition of S and Nby associations of Darmstadter.L Toman.M.A.)80-83 (Resources for the Future,Washington.1993). three annual range species in lysimeters Plant Soil81,311-321(1984). 83.Tomich,T.P..Kuusipalo,L.Menz,K.Byron,N.Impe erata economics and policy.Agrofor.Syst.36, 40.Gordon,D.R.&Rice,K I.Partitioning of water between twe nual grassland 233-261(1997). species.Am..Bet.79,967-976(1992). 84.Power.M.E..Matthews.W.I.Steward.A.L Grazing minnows.piscivorous bass,and stream algae: 41.Jfon,LLFriend,A.L&Berrang P.C.Species mixture and soil-resource availability affect the root dynamics of a strong interaction.Ecology66,1448-1456(1985). growth response of tree seedlings toelevated atmospheric CO.J.For.Res.25,824-832(1995) 85.Johnson.K.G.Vogt,K.AClark.H.Schmitz.&Vogt,D.J.Biodiversity and the productivity 42.Harrington,R..Woiwod,L Sparks,T.Climate change and trophic interactions.Trends Ecol Evol and stability of ecosystems.Trends Ecol.EvoL 11,372-377(1996). 14.146-15019991. 86.Vitousek,P.M.Hoo er,D.U.in Biodiversity and Ecosystem Function (eds Schulze,E.D.&Mooney 3.,,I.P&Falcruk,V.The impact of elevated CO,on plant-herbivore H.A.)3-14(Springer.Berlin,1993) interactions experimental evidence of moderating effects at the community level.Oerologia 117, 87.Huston,M.A.Hidden treatments in ecological experiments re-evaluating the ecosystem function of 177-186(1998). biodiversity.Oecologia110,449-460(1997). 44.Lindroth,RL in Carbon Diocide and Terrestrial Ecosystems (eds Koch,G.W.&Mooney.H.A.) 88.Daily,G.C.Nature's Services:Societal Dependence on Natural Ecsystems (Island,Washington DC. 105-120 (Academic Press,San Diego,1996). 19971 45.MeNaughton,S.I.Diversity and stability of ecological communities:a co ment on the role of 89.Goulder,LH.&Kennedy.D.in Nature's Services:Societal Dependence on Natural Ecosystems(ed. empiricism in ecology.Am.Nat.111,515-525(1977). Daily,G.C.)23-48 (Island.Washington DC.1997) 46.Naeem,S.Li,S.Biodiversity enhances ecosystem reliability.Nature 390,507-509(1997). ments environmental manipulations in the field.Eclogy 66,564-576(1985). We thank B.R.Tershy for valuable inputs and I.D.Gerlach for access to his unpublished 48.Altieri,M.A.in Agroecology(eds Carrol,C.R.,Vandermeer,J.H.Rosset,P.M)551-564(McGraw manuscript. 242 2000 Macmillan Magazines Ltd NATURE VOL 40511 MAY 2000 www.nature.com
4. Pimm, S. L., Russell, G. J., Gittleman, J. L. & Brooks, T. M. The future of biodiversity. Science 269, 347–350 (1995). 5. Lawton, J. H. & May, R. M. Extinction Rates(Oxford Univ. Press, Oxford, 1995). 6. Sala, O. E. et al. Global biodiversity scenarios for the year 2100. Science 287, 1770–1776 (2000). 7. Lawton, J. H. What do species do in ecosystems? Oikos 71, 367–374 (1994). 8. Tilman, D., Wedin, D. & Knops, J. Productivity and sustainability influenced by biodiversity in grassland ecosystems. Nature 379, 718–720 (1996). 9. Hector, A. et al. Plant diversity and productivity experiments in European grasslands. Science 286, 1123–1127 (1999). 10. van der Heijden, M. G. A. et al. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396, 69–72 (1998). 11. Salonius, P. O. Metabolic capabilities of forest soil microbial populations with reduced species diversity. Soil Biol. Biochem. 13, 1–10 (1981). 12. Wardle, D. A., Bonner, K. I. & Nicholson, K. S. Biodiversity and plant litter: experimental evidence which does not support the view that enhanced species richness improves ecosystem function. Oikos 79, 247–258 (1997). 13. Hooper, D. U. & Vitousek, P. M. The effects of plant composition and diversity on ecosystem processes. Science 277, 1302–1305 (1997). 14. Tilman, D. et al. The influence of functional diversity and composition on ecosystem processes. Science 277, 1300–1302 (1997). 15. Vitousek, P. M., Walker, L. R., Whiteaker, L. D., Mueller-Dombois, D. & Matson, P. A. Biological invasion by Myrica faya alters ecosystem development in Hawaii. Science 238, 802–804 (1987). 16. Berry, W. L. Characteristics of salts secreted by Tamarix aphylla. Am. J. Bot. 57, 1226–1230 (1970). 17. Christian, J. M. & Wilson, S. D. Long-term impacts of an introduced grass in the northern Great Plains. Ecology 80, 2397–2407 (1999). 18. Lavelle, P., Bignell, D. & Lepage, M. Soil function in a changing world: the role of invertebrate ecosystem engineers. Eur. J. Soil Biol. 33, 159–193 (1997). 19. D’Antonio, C. M. & Vitousek, P. M. Biological invasions by exotic grasses, the grass-fire cycle, and global change. Annu. Rev. Ecol. Syst. 23, 63–87 (1992). 20. Whisenant, S. Changing Fire Frequencies on Idaho’s Snake River Plains: Ecological Management Implications 4–10 (US Forest Service General Technical Report INT-276, Washington, 1990). 21. Van Cleve, K., Chapin, F. S. III, Dryness, C. T. & Viereck, L. A. Element cycling in taiga forest: statefactor control. BioScience 41, 78–88 (1991). 22. Shukla, J., Nobre, C. & Sellers, P. Amazon deforestation and climate change. Science 247, 1322–1325 (1990). 23. Foley, J. A., Kutzbach, J. E., Coe, M. T. & Levis, S. Feedbacks between climate and boreal forests during the Holocene epoch. Nature 371, 52–54 (1994). 24. de Ruiter, P. C., Neutel, A. & Moore, J. C. Energetics, patterns of interaction strengths, and stability in real ecosystems. Science 269, 1257–1260 (1995). 25. Power, M. E. et al. Challenges in the quest for keystones. BioScience 46, 609 (1996). 26. Read, D. J. Mycorrhizas in ecosystems. Experientia 47, 376–391 (1991). 27. Paerl, H. W. & Pinckney, J. L. A mini-review of microbial consortia: their roles in aquatic production and biogeochemical cycling. Microbial Ecol. 31, 225–247 (1996). 28. Estes, J. A. & Palmisano, J. F. Sea otters: their role in structuring nearshore communities. Science 185, 1058–1060 (1974). 29. Estes, J. A., Tinker, M. T., Williams, T. M. & Doak, D. F. Killer whale predation on sea otters linking oceanic and nearshore ecosystems. Science 282, 473–476 (1998). 30. Mork, M. The effect of kelp in wave damping. Sarsia 80, 323–327 (1996). 31. Schindler, D. E., Carpenter, S. R., Cole, J. J., Kitchell, J. F. & Pace, M. L. Influence of food web structure on carbon exchange between lakes and the atmosphere. Science 277, 248–251 (1997). 32. Caraco, N. F. et al. Zebra mussel invasion in a large, turbid river: phytoplankton response to increased grazing. Ecology 78, 588–602 (1997). 33. Clarholm, M. Interactions of bacteria, protozoa and plants leading to mineralization of soil nitrogen. Soil Biol. Biochem. 17, 181–187 (1985). 34. Zimov, S. A. et al. Steppe-tundra transition: an herbivore-driven biome shift at the end of the Pleistocene Am. Nat. 146, 765–794 (1995). 35. Chanway, C. P., Turkington, R. & Holl, F. B. Ecological implications of specificity between plants and rhizosphere micro-organisms. Adv. Ecol. Res. 21, 121–169 (1991). 36. Lawley, R. A., Newman, E. I. & Campbell, R. Abundance of endomycorrhizas and root-surface microorganisms on three grasses grown separately and in mixtures. Soil Biol. Biochem. 14, 237–240 (1982). 37. Soluck, D. A. & Richardson, J. S. The role of stoneflies in enhancing growth of trout: a test of the importance of predator–predator facilitation within a stream community. Oikos 80, 214–219 (1997). 38. Rice, K. J. Interaction of disturbance patch size and herbivory in Erodium colonization. Ecology 68, 1113–1115 (1987). 39. Shock, C. C., Jones, M. B., Williams, W. A. & Center, D. M. Competition of S and N by associations of three annual range species in lysimeters Plant Soil 81, 311–321 (1984). 40. Gordon, D. R. & Rice, K. J. Partitioning of space and water between two California annual grassland species. Am. J. Bot. 79, 967–976 (1992). 41. Jifon, J. L., Friend, A. L. & Berrang, P. C. Species mixture and soil-resource availability affect the root growth response of tree seedlings to elevated atmospheric CO2. Can. J. For. Res. 25, 824–832 (1995). 42. Harrington, R., Woiwod, I. & Sparks, T. Climate change and trophic interactions. Trends Ecol. Evol. 14, 146–150 (1999). 43. Díaz, S., Fraser, L. H., Grime, J. P. & Falczuk, V. The impact of elevated CO2 on plant–herbivore interactions: experimental evidence of moderating effects at the community level. Oecologia 117, 177–186 (1998). 44. Lindroth, R. L. in Carbon Dioxide and Terrestrial Ecosystems(eds Koch, G. W. & Mooney, H. A.) 105–120 (Academic Press, San Diego, 1996). 45. McNaughton, S. J. Diversity and stability of ecological communities: a comment on the role of empiricism in ecology. Am. Nat. 111, 515–525 (1977). 46. Naeem, S. & Li, S. Biodiversity enhances ecosystem reliability. Nature 390, 507–509 (1997). 47. Chapin, F. S. III & Shaver, G. R. Individualistic growth response of tundra plant species to environmental manipulations in the field. Ecology 66, 564–576 (1985). 48. Altieri, M. A. in Agroecology (eds Carrol, C. R., Vandermeer, J. H. & Rosset, P. M.) 551–564 (McGraw Hill, New York, 1990). 49. Walker, B., Kinzig, A. & Langridge, J. Plant attribute diversity, resilience, and ecosystem function: the nature and significance of dominant and minor species. Ecosystems 2, 95–113 (1999). 50. Burdon, J. J. The structure of pathogen populations in natural plant communities. Annu. Rev. Phytopathol. 31, 305–323 (1993). 51. Wasilewska, L. Differences in development of soil nematode communities in single- and multispecies grass experimental treatments. Appl. Soil Ecol. 2, 53–64 (1995). 52. Bertness, M. D. & Leonard, G. H. The role of positive interactions in communities: lessons from intertidal habitats. Ecology 78, 1976–1989 (1997). 53. Nitta, T. Diversity of root fungal floras: its implications for soil-borne diseases and crop growth. Jap. Agric. Res. Quart. 25, 6–11 (1991). 54. Elton, C. S. The Ecology of Invasions by Animals and Plants(Methuen, London, 1958). 55. Tilman, D. Community invasibility, recruitment limitation, and grassland biodiversity. Ecology 78, 81–92 (1997). 56. Levine, J. M. & D’Antonio, C. M. Elton revisited: a review of evidence linking diversity and invasibility. Oikos 87, 15–26 (1999). 57. Stohlgren, T. J. et al. Exotic plant species invade hot spots of native plant diversity. Ecol. Monogr. 69, 25–46 (1999). 58. Lavorel, S., Prieur-Richard, A.-H. & Grigulis, K. Invasibility and diversity of plant communities: from patterns to processes. Diversity Distrib. 5, 41–49 (1999). 59. McGrady-Steed, J., Harris, P. M. & Morin, P. J. Biodiversity regulates ecosystem predictability. Nature 390, 162–165 (1997). 60. Orr, M. R. & Seike, S. H. Parasitoids deter foraging by Argentine ants (Linepithema humile) in their native habitat in Brazil. Oecologia 117, 420–425 (1998). 61. Holway, D. A. Competitive mechanisms underlying the displacement of native ants by the invasive Argentine ant. Ecology 80, 238–251 (1999). 62. Van Wilgen, B. W., Cowling, R. M. & Burgers, C. J. Valuation of ecosystem services: a case study from South African fynbos ecosystems. BioScience 46, 184–189 (1996). 63. Zavaleta, E. S. in Invasive Species in a Changing World (eds Hobbs, R. J. & Mooney, H. A.) (Island, Washington DC, in the press). 64. Costanza, R. et al. The value of the world’s ecosystem services and natural capital. Nature 387, 253–260 (1997). 65. Stewart, G. & Hull, A. C. Cheatgrass (Bromus tectorum L.) — an ecological intruder in southern Idaho. Ecology 30, 58–74 (1949). 66. Blockstein, D. E. Letter to the editor. Science 279, 1831 (1998). 67. Naylor, R. L. Invasions in agriculture: assessing the cost of the golden apple snail in Asia. Ambio 25, 443–448 (1996). 68. Porter, J. H., Parry, M. L. & Carter, T. R. The potential effects of climatic change on agricultural insect pests. Agric. For. Meteorol. 57, 221–240 (1991). 69. Pimentel, D., Lach, L., Zuniga, R. & Morrison, D. Environmental and economic costs of nonindiginous species in the United States. BioScience 50, 53–65 (2000). 70. USOT Assessment. Harmful Non-indigenous Species in the United States(US Government Printing Office, Washington, 1993). 71. Thorp, J. The National Weeds Strategy: A Strategic Approach to Weed Problems of National Significance (Agriculture and Resource Management Council of Australia and New Zealand, Canberra, 1997). 72. Jones, C. G., Ostfeld, R. S., Richard, M. P., Schauber, E. M. & Wolff, J. O. Chain reactions linking acorns to gypsy moth outbreaks and Lyme disease risk. Science 279, 1023–1026 (1998). 73. Fisher, A. C. & Hanemann, W. M. Option value and the extinction of species. Adv. Appl. Micro-Econ. 4, 169–190 (1986). 74. Naylor, R. L. in Invasive Species in a Changing World (eds Hobbs, R. & Mooney, H. A.) (Island, Washington DC, in the press). 75. Channell, R. & Lomolino, M. V. Dynamic biogeography and conservation of endangered species. Nature 403, 84–86 (2000). 76. Bryan, J. H., Foley, D. H. & Sutherst, R. W. Malaria transmission and climate change in Australia. Med. J. Aust. 164, 345–347 (1996). 77. Morrison, J. I. The Sustainable Use of Water in the Lower Colorado River Basin (Pacific Institute and the Global Water Policy Project, Oakland, 1996). 78. Zavaleta, E. S. The emergence of waterfowl conservation among Yup’ik hunters in the YukonKuskokwim Delta, Alaska. Hum. Ecol. 27, 231–266 (2000). 79. Warren, D. M. & Pinkston, J. in Linking Social and Ecological Systems(eds Berkes, F. & Folke, C.) 158–189 (Cambridge Univ. Press, Cambridge, 1998). 80. Schlesinger, W. H. et al. Biological feedbacks in global desertification. Science 247, 1043–1048 (1990). 81. Garrity, D. P. et al. The Imperata grasslands of tropical Asia: area, distribution, and typology. Agrofor. Syst. 36, 1–29 (1997). 82. Peck, S. C. & Teisberg, T. J. in Assessing Surprises and Nonlinearities in Greenhouse Warming (eds Darmstadter, J. & Toman, M. A.) 80–83 (Resources for the Future, Washington, 1993). 83. Tomich, T. P., Kuusipalo, J., Menz, K. & Byron, N. Imperata economics and policy. Agrofor. Syst. 36, 233–261 (1997). 84. Power, M. E., Matthews, W. J. & Steward, A. J. Grazing minnows, piscivorous bass, and stream algae: dynamics of a strong interaction. Ecology 66, 1448–1456 (1985). 85. Johnson, K. G., Vogt, K. A., Clark, H. J., Schmitz, O. J. & Vogt, D. J. Biodiversity and the productivity and stability of ecosystems. Trends Ecol. Evol. 11, 372–377 (1996). 86. Vitousek, P. M. & Hooper, D. U. in Biodiversity and Ecosystem Function (eds Schulze, E.-D. & Mooney, H. A.) 3–14 (Springer, Berlin, 1993). 87. Huston, M. A. Hidden treatments in ecological experiments: re-evaluating the ecosystem function of biodiversity. Oecologia 110, 449–460 (1997). 88. Daily, G. C. Nature’s Services: Societal Dependence on Natural Ecosystems(Island, Washington DC, 1997). 89. Goulder, L. H. & Kennedy, D. in Nature’s Services: Societal Dependence on Natural Ecosystems(ed. Daily, G. C.) 23–48 (Island, Washington DC, 1997). Acknowledgements We thank B. R. Tershy for valuable inputs and J. D. Gerlach for access to his unpublished manuscript. insight review articles 242 © 2000 Macmillan Magazines Ltd NATURE | VOL 405 | 11 MAY 2000 | www.nature.com
