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 237rooted 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 charac￾teristics (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 terres￾trial 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 process￾es 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 phyto￾plankton while increasing water clarity and phosphorus availabili￾ty32. 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 technolo￾gy 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 com￾position 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