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.comneighbours, 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, graz￾ers 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 produc￾tion and nutrient cycling in dry grasslands. These examples clearly indicate that all types of organisms — plants, animals and microor￾ganisms — 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 process￾es. 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 interac￾tions41. 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 ecosys￾tem 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 envi￾ronment 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 function￾ally 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 host￾specific 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 com￾munities 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 rich￾ness 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 vulnera￾bility 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