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BIODIVERSITY AND ECOSYSTEM FUNCTION: DO SPECIES MATTER? Paul S. Giller and Grace O’Donovan ABSTRACT Biological communities perform a variety of functions within ecosystems, including regulation of climatic processes, breakdown of waste, recycling of nutrients, maintenance of soil fertility and provision of natural resources. Although exact numbers and timescales are difficult to determine, it is clear that biodiversity (species and habitat richness, genetic diversity and community complexity) is declining. Studies of biodiversity are thus assuming greater significance as ecologists try desperately to document global biodiversity in the face of unprecedented perturbations, habitat loss and extinction rates. How will such decline in biodiversity affect the biosphere and the quality of human life on the planet? Does biodiversity matter? Internationally, research has begun to investigate whether the current unprecedented losses in biodiversity will damage the functioning of ecosystems. This paper reviews this work and highlights the general patterns identified. Scientific evidence continues to show that, in general, biodiversity does influence the rates or nature of ecosystem processes, and a majority of studies have found that a reduction in biodiversity does have a negative effect on ecosystem function. The paper also considers the potential indirect effects of biodiversity losses on conservation, particularly in relation to fragmentation and critical transition zones between terrestrial and aquatic habitats. Paul S. Giller, Department of Zoology and Animal Ecology, University College Cork, Republic of Ireland (corresponding author; e-mail: [email protected]); Grace O’Donovan, Department of Environmental Resource Management, University College Dublin, Belfield, Dublin 4, Republic of Ireland. BIOLOGY AND INTRODUCTION Currently, there is unprecedented interest in the earth’s biological diversity, with the year 2001 –2 designated as International Biodiversity Observation Year by a range of international bodies, including the International Union of Biological Sciences (IUBS), the Scientific Committee on Problems of the Environment (SCOPE), Diversitas and UNESCO among others. At the Earth Summit in Rio in 1992, more than 150 countries signed the Convention on Biological Diversity, which came into force in 1993 and was ratified by Ireland in 1996. This Convention and a range of other international conventions and directives oblige Ireland to work towards establishing legal and institutional frameworks for the protection and enhancement of biodiversity and environmental quality. The state must take measures, by developing or adapting existing national strategies, plans and programmes, to ensure the conservation and sustainable use of biological diversity. In the Rio Convention, biological diversity is defined as ‘the variability among living organisms from all sources including, inter alia, terrestrial, marine and other aquatic ecosystems and the ecological complexes of which they are part; this includes diversity within species, between species and of ecosystems’. Biodiversity must therefore be considered at three interdependent levels: ENVIRONMENT: PROCEEDINGS OF THE ecosystem diversity, species diversity and genetic diversity within species. With advances in science and technology, we are on the verge of understanding the natural world while at the same time in real danger of destroying it. The environment is larger and much more complex than any man-made machinery, and the consequences of system failure are thus more disastrous. Every human activity has some effect on the natural environment as a whole, and over the past few decades, there has been a growing recognition and concern that increasing economic activity and development carry environmental costs. Environmental trends such as urban congestion; increasing waste production and inadequacies of waste disposal; erosion; global warming and climate change; and pollution and ozone depletion —with consequent deterioration of landscape quality, loss of biodiversity and habitats and over-exploitation and depletion of resources —are all symptoms of environmental deterioration. What we know of past, present and projected rates of habitat change, species extinction and human population growth and development suggests some profoundly disturbing conclusions about the future of the earth’s biosphere (Gaston 1996). Environmental policy-making is more or less genuinely science-based (Porritt 1994) and thus requires high-quality, objective and informative ROYAL IRISH ACADEMY, VOL. 102B, NO. 3, 129– 139 (2002). © ROYAL IRISH ACADEMY 129 BIOLOGY AND science to underpin it, yet we commonly make decisions about the management of the environment with scarcely any adequate indications regarding environmental trends, the state of the environment or its response to our activities. The result is often unforeseen damage, decreasing productivity and loss of sustainability, defined as ‘the ability to meet the needs of today without jeopardising the ability of future generations to meet their own needs’ (Holdgate 1991). Much more information is required if we are to optimise responses to the worsening situation. The development of new technologies and disciplines, such as GIS and remote sensing, molecular biology, telemetric remote sampling equipment, analytical methodologies, controlled environmental chambers and taxonomic expertise, has provided many of the necessary tools to make great strides forward in our understanding of, and ability to sustainably manage, the natural world. Never before has ecology been of such critical importance in tackling the major social and economic problems that the world faces, and this role poses challenges to the subject itself as a scientific discipline. How can we overcome the bottleneck in our ability to quantify biological diversity fully? How can we make ecological predictions at the scale appropriate to the current and future problems that need to be addressed? What kind of data do we need to tackle the problems? What are the important interactions and ecological processes, and how are they affected by environmental change and species loss? Biological communities and their associated chemical and physical processes are collectively referred to as ecosystems and perform a variety of functions, including regulation of climatic processes, breakdown of waste and recycling of nutrients, maintenance of soil fertility and provision of natural resources. These functions in turn provide to humans, directly or indirectly, a range of benefits (ecological services) that have recently been valued at US$33 trillion per year (Costanza et al. 1997). Living organisms integrate the effects of many variables within the environment, and their biological efficiency, productivity or balance within the ecosystem indicates the overall health of the system (Spellerberg 1991). Biodiversity has thus been promoted to centre stage in national and international strategies and debates concerning the environment. Biodiversity studies are increasingly important at a time when global biodiversity is in flux, with unprecedented perturbations, habitat loss and extinction rates. International research efforts are now focused on answering the question of whether current unprecedented losses in biodiversity will negatively affect ecosystem functioning (see ‘Nature insight: biodiversity’, Nature 405 (2000), 207–53). 130 ENVIRONMENT Concern has usually been focused on what the entities of biodiversity are and where they are, with increasing concentration on the most diverse and understudied habitats, e.g. tropical rainforests or deep-sea and hydrothermal vents. The soil, for example, is perhaps one of the most understudied of habitats, yet it is probably also one of the most diverse (Giller 1996) and has only recently received significant attention (Brussaard et al. 1997; Wall Freckman et al. 1997; see also BioScience 50 (12) (2000): special issue on soil and sediment biodiversity). Ecologists have also been studying systems for a long time and getting a better idea of biodiversity levels. For example, the bestdocumented stream system is the Breitenbach stream near Schlitz in Germany, where Joachim Illies, Peter Zwick, Rudiger Wagner and others have been sampling entire animal communities for over 25 years. Allan (1995) offered a compilation of the data, showing that 642 insect species (including 476 dipterans, 70 coleopterans and 57 trichopterans), and 446 non-insect taxa (approximately half of which were nematodes and rotifers) had been recorded. Despite the obvious widespread interest in, and importance of, biodiversity, estimates of the number of species on earth are vague. Larger organisms are relatively well studied, but it is among the invertebrates, particularly insects and marine invertebrates, that much remains to be done to develop a more complete systematic knowledge and to understand the taxonomic relatedness of species. By the beginning of 1988, 1.82 million species had been named, including 9,020 birds, 18,818 fish, 225,000 plants and approximately one million insects (Rosenzweig 1995), but estimates of the likely total number range from 5 million to 30 million. In the 1995 book Global Biodiversity Assessment, Hammond suggests a conservative estimate of around 14 million species (Hammond 1995). In fact, this figure represents merely a fraction of all species that have ever existed. Mass extinctions have occurred in the past, brought about by natural catastrophic environmental change, and have generally been followed by bursts of speciation. In recent years, however, we have been witnessing another dramatic drop in biological diversity as a result of human activity, with both species extinctions and gene pool declines occurring at rates unprecedented in the earth’s history (Spellerberg and Hardes 1992). Recent estimates put the total number of recorded extinctions (mostly vertebrates) at around 1,100 species since 1600, but the rate of extinction rose dramatically over the last century, with global loss estimates varying between 1% and 11% (Jenkins 1992). Absolute rates of species loss in rain forests are 1,000 to 10,000 times the level before human intervention (Vitousek et al. 1997), and it is also BIODIVERSITY AND estimated that we could lose 50% of total biotic diversity in the next 100 years (Soule 1991). DOES BIODIVERSITY MATTER? Although exact numbers and timescales are difficult to determine, it is clear that biodiversity (species and habitat richness, genetic diversity and community complexity) is declining. How will such a decline in biodiversity affect the biosphere and the quality of human life on the planet? Does biodiversity matter? Despite the conceptual simplicity of this question, it has been difficult to study in the real world. There is now general acceptance that ‘biodiversity per se is a good thing, that its loss is bad and that something should be done to preserve it’ (Gaston 1996). This is so for a number of reasons (Spellerberg and Hardes 1992; Kunin and Lawton 1996; Oksanen 1997; O’Neill 1997), including the following: We have a moral and ethical responsibility to preserve life on earth. Biodiversity has aesthetic value. Biodiversity has monetary and utilitarian value, through provision of drugs, food, genes, industrial processes, etc. Biodiversity provides a useful measure of the quality of the environment and of the probability of sustainability. Biodiversity has ecological value, through provision of ecosystem services, including maintenance of atmospheric composition and biogeochemical cycles, soil binding, soil fertility, decomposition and disposal of wastes, production, pest control and water purification. It is this relationship between biodiversity and ecosystem functioning that has recently become a focus of ecological research (Hector 2000), for three reasons. Firstly, concern is growing that the high rates of species extinction described earlier could be detrimental to the ecosystem services. Secondly, enhancing biodiversity in agricultural systems may improve their performance and productivity and decrease inputs of energy, fertilisers and pesticides. Thirdly, experimental manipulation of biodiversity is intrinsically valuable as a means of improving our understanding of the structure and functioning of ecological communities. HYPOTHESES RELATING BIODIVERSITY TO FUNCTION A meeting of experts in Germany in the early 1990s resulted in an edited volume of papers on the nature of the relationship between biodiversity and ecosystem function (Schultze and Mooney ECOSYSTEM FUNCTION 1993), and this made it clear that, at that time, we knew embarrassingly little. Thus, over the last few years research has focused on the question of whether the loss of biodiversity will negatively affect the functioning of ecosystems (Naeem et al. 1996; Tilman et al. 1996; 1997; Grime 1997; Tilman 1997; Hector et al. 1999; Loreau et al. 2001). Possible interactions of biodiversity with ecosystem processes include the following: Biodiversity may support specific processes: communities with high biodiversity may contain specialists that are absent in less diverse ones, e.g. pollinators of certain plants. Biodiversity may influence rates of ecosystem processes, with increasing, decreasing or stabilising rates. Biodiversity may influence standing stocks, biomass or production. A diverse array of hypotheses has been proposed to predict the effect of species loss on ecosystem function (Erlich and Erlich 1981; Lawton 1994; Walker 1992; Naeem et al. 1995 and others (see also Johnson et al. 1996; Martinez 1996; Stiling 1999)). Although these hypotheses are not mutually exclusive, and do overlap to a greater or lesser extent, the major features can be illustrated by plots of the predicted relationships between biodiversity and function rate (Fig. 1). The following are the major hypotheses: (i) The null hypothesis suggests that there is no relationship at all between biodiversity and ecosystem function. (ii) The rivet hypothesis suggests that every species plays a role in ecosystem function and that all species have an equal and additive effect on function; hence, all species matter. (iii) The modified rivet hypothesis predicts that, as resources are finite, at some point the relationship must saturate; hence, the curve rises asymptotically. (iv) The redundant species hypothesis predicts a more strongly saturating relationship between biodiversity and function. Above the saturation point, species can be lost without significant effect on ecosystem function, i.e. not all species matter, so some species are redundant. Implicit in this hypothesis is that other species can take over the role of, or compensate for, lost species. (This may be related to the notion of functional groups, whereby species within a group may be lost without effect, but loss of a group itself results in significant loss of function.) (v) The keystone species hypothesis holds that keystone species by definition are not redundant. These are defined as species whose effects on the community or 131 BIOLOGY AND ecosystem are much larger than expected on the basis of abundance. If large changes occur in abundances or composition of a community when a species is removed, the species is known as a strong interactor; if not, it is a weak interactor. As strong interactors are fewer in number than weak interactors, biodiversity per se may not be critical to function, but the presence or absence of a keystone species is. The question remains, however, as to whether keystone species are keystone (strong interactors) throughout their range. (vi) The uniqueness hypothesis is related to the keystone hypothesis. When a species is lost, a particular function of the ecological system is also largely eliminated. This hypothesis relates particularly to ecological engineers, e.g. beavers. (vii) The idiosyncratic hypothesis suggests that changing the number of species influences ecosystem processes, but no obvious pattern is evident; hence, the role of biodiversity is unpredictable. Some inverse relationships are also possible between biodiversity and ecosystem function: (viii) The inverse rivet hypothesis suggests that an increase in biodiversity leads to a proportional decrease in function. Examples include a vegetation effect on water yield from a catchment, whereby increasing biodiversity and biomass lead to a decreasing water yield and a situation in which production levels of a crop plant in an agricultural habitat are maintained only by use of pesticides, herbicides and fungicides to eliminate consumers, parasites and competitors. (ix) The gradual decline parabolic (Type 6 ) curve describes a relationship whereby an increase in biodiversity gradually reduces some processes, e.g. the relationship between diversity of plants and microbes and inorganic matter in soil (Martinez 1996). The relationships are dependant to a large extent on the process or function in question and on the target species or set of species. There is still no consensus on the relative merits or validity of the relationships between biodiversity and ecosystem processes, but empirical evidence is growing. EMPIRICAL EVIDENCE OF RELATIONSHIPS What has the scientific evidence shown? In general, biodiversity influences the rates or nature of ecosystem processes, and a majority of studies 132 ENVIRONMENT Fig. 1 —Pictorial representation of the various hypotheses linking biodiversity to ecosystem function. have found that a reduction in biodiversity has a negative effect on ecosystem function (Schmid et al. 2000; Bolger 2001; Loreau et al. 2001). A range of examples are given in Table 1. In particular, biodiversity has been demonstrated to maintain and increase predictability (McGrady-Steed et al. 1997), reliability (Naeem and Li 1997), invasibility (Symstad 2000), process efficiency (Heneghan et al. 1999), productivity (Hector et al. 1999) and sustainability (Tilman et al. 1996). Most of these studies were undertaken on terrestrial plant communities and involved the measurement of nutrient uptake, changes in carbon dioxide levels or gain in biomass. A survey of the effect of plant diversity on productivity (Schläpfer and Schmid 1999) showed positive relationships (log–linear or linear) in thirteen of seventeen studies. Similarly, Schwartz et al. (2000) found biodiversity effects on ecosystem processes in 95% of the manipulation studies they identified and reviewed; the effects were predominantly saturating (tending towards the redundant hypothesis). Both comparative and experimental studies thus suggest that a large pool of species is required to sustain the assembly and functioning of ecosystems in landscapes that are subject to increasingly intensive land use (Loreau et al. 2001). In contrast, few studies on the role of biodiversity in ecosystem function have been undertaken among animal communities (Mikola and Setala 1998; Heneghan et al. 1999; Jonsson and Malmqvist 2000; Jonsson et al. 2001), but apart from Mikola and Setala (1998), they seem to show BIODIVERSITY AND ECOSYSTEM FUNCTION quite strong positive relationships (Table 1). A more detailed look at a few of these studies can be instructive. Naeem et al. (1995) published results of the first experimental study to investigate the biodiversity – function relationship. The Ecotron is an elaborate set of fourteen controlled environment chambers, in which replicated terrestrial communities of 9, 15 and 31 species were established across four trophic levels that differed only in biodiversity. Decomposers included earthworms and Collembola; primary producers were annual plants; herbivores included aphids, white flies, snails and slugs; and parasites that attacked the insect herbivores represented the top trophic level. The processes measured included community respiration, decomposition and nutrient retention and productivity. The results were clear. Productivity increased by two to three times as biodiversity increased (close to the rivet hypothesis). Other processes indicated idiosyncratic responses or redundancy at low levels of species richness. A more recent microbial study in aquatic microcosms was also carried out by Naeem et al. (2000). Decomposers transfer organic nutrients into inorganic forms through mineralisation, which provides the main pathway of inorganic nutrients to producers. Decomposers cannot acquire carbon from organic sources, but they can transform organic carbon from sources supplied by producers as exudates or dead organic matter. Laboratory experiments were based on manipulations of species richness of unicellular green algae and heterotrophic bacteria and on measurements of algal production, decomposer production and carbon-source usage from 95 different sources. Increasing producer diversity led to increasing productivity, increasing bacterial richness led to increased bacterial production, and increasing both bacterial and algal richness increased both algal and bacterial production. The number of carbon sources used was positively correlated with decomposer diversity, and algal production was shown to be a joint function of both algal and bacterial diversity. This type of study shows the value of laboratory microcosms in unravelling complex relationships between biodiversity and function through the kind of manipulations that are impossible in the field. However, this approach and that of the Ecotron have been challenged because they are solely laboratory-based. One of the first field-based studies centred on grasslands in Cedar Creek, Minnesota, USA, where Tilman and co-workers have been studying relationships between function and biodiversity since the early 1990s. Earlier studies suggested that increased biodiversity led to increased drought resistance and resilience (Tilman and Downing 1994). Later studies (Tilman et al. 1996) involved much larger experiments, with 147 plots sown with 1, 2, 4, 6, 8, 12 or 24 species and 20 replicates per treatment. The species sown were drawn randomly from the 24-species pool. The results demonstrated clearly that the more diverse the community, the greater the productivity and the more efficient the system was at using nutrients. These patterns matched those in natural communities in the area. Table 1 — Examples of diversity–function relationships. System Authors Ecotron study Grassland Mycorrhizal fungi Naeem et al. 1995 Tilman et al. 1994 van der Heijden et al. 1998 Microbial mesocosms Naeem and Li 1997 Aquatic microbes McGrady-Steed et al. 1997 Soil microarthropods Semi-natural grasslands Aquatic microbes Heneghan et al. 1999 Hector et al. 1999 Naeem et al. 2000 Stream detritivores Jonsson and Malmqvist 2000; Jonsson et al. 2001 Englehardt and Ritchie 2001 Wetland macrophytes Effects of increasing diversity Productivity increased Drought resistance enhanced Plant diversity, nutrient capture, productivity increased Ecosystem reliability enhanced (and insurance) More predictable (less variable) community, respiration Decomposition rate increased Production increased Increase in productivity and in the number of carbon and algae sources utilised Increased litter decomposition by stream invertebrates Algal and total plant biomass increased, phosphate loss decreased 133 BIOLOGY AND One problem to date has been that experiments such as those at Cedar Creek have been restricted to single locations or laboratories, thus limiting the ability of researchers to generalise and predict. This problem has been overcome to a great extent by a large-scale experimental study called BIODEPTH, based on common experiments in semi-natural grassland communities in eight different locations around Europe (Hector et al. 1999; 2002). Plant diversity was manipulated directly in the field by establishing plant communities of different species richness and of planned functional diversity from seed. A total of 480 experimental plant communities were established with three functional groups (grasses, legumes and herbs), and a range of parameters were measured, including production, decomposition, invasibility, use of space, associated insect diversity and nutrient retention. The general results for production across all sites (published by Hector et al. 1999) suggest multiple control of productivity of experimental plant assemblages by geographical location, number and type of plant species and number and type of functional groups. The detailed pattern differed somewhat among locations: for example, the Greek site data supported the null hypothesis, whereas the data from several others supported the redundant species hypothesis (including the Irish site at Riverstick, Co. Cork (Fig. 2), and the UK site at Silwood) or the rivet hypothesis (Portugal, Switzerland). Overall, however, a similar log– linear reduction in above-ground production was seen with loss of species (Hector et al. 1999). For a given number of species, communities with fewer functional groups were also less productive. The number of species and number of functional groups were roughly similar in the strength of their effects on production. These patterns occurred along with differences in geographical location and differences in species composition, thus representing a very powerful test of the biodiversity–function relationship. Data on the effect of biodiversity on herbivory were also investigated at the County Cork site. The expectation is that increasing plant species richness may lead to a reduction in herbivory of any particular plant species, owing to greater heterogeneity of the herbivore’s trophic resources: the concept of apparency. Indeed, results in our study support this (Fig. 3a). Similarly, pathogen infection (Fig. 3b) and invasibility (Fig. 4) both declined with increasing biodiversity, but the response for decomposition was idiosyncratic. No effect of plant species richness on decomposition was found at other sites (e.g. Hector et al. 2000a). Caution in interpretation of biodiversity– function results has been urged by Huston and colleagues 134 ENVIRONMENT Fig. 2 —Relationship between species richness and peak above-ground biomass over the three-year study period at the BIODEPTH Riverstick study site in Co. Cork, Ireland (data from J. Finn, R. Harris, P. Giller, G. O’Donovan and J. Good). (Huston 1997; Huston et al. 2000), especially with regard to biodiversity–production relationships. Plant communities are usually dominated by individuals of the largest species. Hence, the likelihood of selecting a species of high growth, biomass or production in a treatment is likely to increase with increasing species richness— the so-called ‘sampling effect’. A pattern of increasing production with biodiversity may thus be nothing more than the result of an increasing probability that the community will include and become dominated by the most productive species as biodiversity increases. However, this may be viewed as the simplest possible mechanism linking biodiversity with ecosystem functioning. We can overcome such criticism in number of ways (Hector 1998; Loreau 1998; Hector et al. 2000b; Loreau and Hector 2001). The relative yield (RY) of a species is its yield in a mixture expressed as a proportion of its yield in monoculture, and the relative yield total (RYT) of a mixture is simply the sum of the individual species’ RYs. The sampling effect model assumes an RY of approximately 1 for the dominant species and therefore an RYT of 1; if the RYT significantly exceeds 1, this model can be dismissed. Similarly, if the total biomass of a mixture of species exceeds that of the monoculture biomass of the highest-yielding species in the mixture (the concept known as ‘over-yielding’), BIODIVERSITY AND Fig. 3— (a) Percentage of leaves of Trifolium repens with insect herbivore damage in plots of different plant species richness; (b) percentage of leaves of Trifolium repens with fungal pathogens in plots of different plant species richness. In both graphs, mean 9SE included (data from S. Duggan, J. Finn, P. Giller, G. O’Donovan and J. Good). the sampling effect can again be overruled (Hector et al. 1999). This was found to be true in the BIODEPTH experiment (Hector et al. 1999; 2002; Caldeira et al. 2001; Loreau and Hector 2001) and is considered to be largely due to complementarity between species in a mixture, where interspecific competition is reduced through resource partitioning. In contrast, high intraspecific competition is found in monocultures. Studies on animal communities have reached similar conclusions (e.g. Jonsson et al. 2001). These results ECOSYSTEM FUNCTION do not mean that individual species or functional groups play no part in controlling ecosystem function— in the BIODEPTH project, the presence of the legume Trifolium increased production by 360g m − 2 on average. However, a consensus is being reached within the research community that complementarity does occur in diverse communities, particularly as the communities develop over time: thus, species diversity per se does matter (outcome of discussions at an NSF/DIVERSITAS/LINKECOL workshop on biodiversity and ecosystem function in Paris, December 2000) (Loreau et al. 2002; see also Loreau et al. 2001). However, not all studies have been so unequivocal in terms of the biodiversity–ecosystem function relationship, particularly those based on terrestrial decomposition processes. The frequently complex experimental designs and relatively short-term experiments have sometimes generated equivocal results, making them difficult to interpret. Of 21 studies on the effects of plant diversity on mineralisation/decomposition, 5 produced idiosyncratic responses, 6 negative relationships (most curvilinear), 3 positive relationships and 7 no relationships (Schmid et al. 2000). These studies may be, to some extent, examining the wrong group of organisms, and perhaps relationships between microbial diversity and decomposition are more appropriate, although plant diversity may enhance microbial diversity (Giller 1996) and would thus be expected to enhance decomposition rates. The relationship between biodiversity and invasibility is theoretically predicted to be negative, and empirical studies tracking the assembly of communities have generally suggested that communities decline in invasibility over time as species accumulate (Levine and D’Antonio 1999). Constructed/experimental community studies, however, have found both positive and negative effects in both the field and microcosms (Levine and D’Antonio 1999; Levine 2000; Hector et al. 2001). Does this mean that biodiversity does not matter for certain ecosystem functions or under certain situations? Other hypotheses relating biodiversity to stability may help with the answer. OTHER HYPOTHESES RELATING BIODIVERSITY AND FUNCTION An additional value of biodiversity is as an insurance against future change—the so-called ‘insurance hypothesis’ (Walker 1992; Yatchi and Loreau 1999) or ‘portfolio effect’ (Tilman 1999). The well-established biodiversity–stability hypothesis (see McCann 2000) introduced the 135 BIOLOGY AND notion that increasing the number of trophically interacting species in a community should increase the collective ability of member populations to maintain their abundances after disturbance (i.e. high resistance) or to recover quickly from a disturbance (i.e. high resilience). It is suggested that more-diverse ecosystems are more likely to contain some species that can withstand environmental perturbations and thus compensate for functional loss of other species that are reduced or eliminated by the perturbation. Tilman and Downing (1994) concluded that primary productivity is more resistant to, and recovers more quickly from, a drought perturbation in more-diverse communities. Other experiments have concluded that the positive biodiversity– stability correlation is not purely a species effect but is related more to functional diversity (McCann 2000). Field tests at the scale of the food web are also few in number. One example (McNaughton 1985) tested seven stability– biodiversity measures in the Serengeti grazing ecosystem under strong seasonal variations and found that five of the seven measures were positively related to biodiversity, but again it appeared that functional diversity was more important than species diversity. Microcosm experiments have also tended to agree that biodiversity is positively related to ecosystem stability (McCann 2000). The two main explanations for these responses are that (a) increasing biodiversity increases the chances that at least some species will respond differentially to the environmental fluctuations and disturbances, and (b) greater biodiversity increases the chance that the ecosystem will have some functional redundancy in the form of species capable of functionally replacing other important species. Taken together, these two ideas form the insurance hypothesis (McCann 2000). Overall, experimental studies are rare, and the crucial question of how critical biodiversity is for resilience and resistance of communities and ecosystem processes remains largely unanswered at present. This represents a major area for further research. CONSERVATION ISSUES In addition to the purely ecological and theoretical insights arising from the study of relationships between biodiversity and ecosystem function and stability, some pragmatic issues also arise with direct relevance to conservation. The redundant species hypothesis has been used to discuss priorities for species conservation (Gitay et al. 1996). However, as Covich (1996) points out, establishing habitat protection policies based on those species that provide the essential ecosystem 136 ENVIRONMENT Fig. 4 —(a) Invasibility of plant communities of different species richness; (b) invasibility in relation to the total percentage plant cover of plots in Fig. 4a. Invasibility was measured as the number of weed species found growing in the plots (data from S. Duggan, J. Finn, P. Giller, G. O’Donovan and J. Good). functions is complex and very much limited by our knowledge gaps as well as by our ability to deal with timescales appropriate to both ecological and evolutionary processes. Until we have a fuller appreciation of the different roles that species play under different environmental conditions, any such approach will probably fail. However, we are simply unable to assist all species under threat, so priorities are essential. One possibility lies in the identification of ‘biodiversity hotspots’ — areas of extreme biotic diversity. Recent research has suggested that up to 44% of all species of vascular plant and 35% of all species in four major vertebrate groups (mammals, birds, reptiles and BIODIVERSITY AND amphibians) are confined to 25 hotspots that occupy only 1.4% of the earth’s land surface (Myers et al. 2000). Concentration of effort in such areas may be the most pragmatic way forward at present, although this approach may be hindered by the fact that species-rich areas for different types of taxa frequently do not coincide (Prendergast et al. 1993; Gaston and Williams 1996). In addition, in 1995, nearly 20% of the world’s population were living within an area that covers about 12% of the earth’s land surface and includes all of these hotspots (Cincotta et al. 2000). There are two further conservation-related research areas that are worth mentioning, in both of which the biodiversity– ecosystem function debate is relevant. FRAGMENTATION We have seen that biodiversity can have profound effects on ecosystem processes. We also know that area plays a major role in controlling species richness through the species–area relationship. One of the major conservation concerns at present is habitat fragmentation, which involves both reduction in area and increasing isolation of habitats. The resulting loss of species may therefore be compounded by subsequent loss of function within the fragmented system. Fragmentation is particularly dramatic in forests and can disrupt biological functions that maintain biodiversity, such as pollination, seed dispersal and nutrient recycling mediated largely by insects (Didham et al. 1996). For example, fragmentation of forests in central Amazonia has led directly to a decline in the species richness and abundance of pollinators and indirectly to changes in their behaviour and flight patterns (Powell and Powell 1987), and in Sweden, plant reproductive success has declined with increasing forest fragmentation (Jennersen 1988). Likewise, in dung beetle communities, a sharp decrease in the rate of dung decomposition has been reported with increasing fragmentation, again in central Amazonia (Klein 1989). Similar changes are likely to be occurring in many other habitats subjected to fragmentation. CRITICAL TRANSITION ZONES The role of biodiversity in the functioning of critical transition zones (or ecotones) also needs to be examined. Ecotones are zones that form an interface between major terrestrial and aquatic habitats (Wall Freckman et al. 1997), for example between soils and groundwaters or between land and freshwater habitats. Many of these zones, especially riparian zones along rivers, have been ECOSYSTEM FUNCTION under significant threat because of changes in landscape management and intensification of agriculture and forestry. Natural riparian zones are among the most diverse and complex of terrestrial habitats and contain valuable water resources and biota in their own right (Naiman and Decamps 1997). The linear nature of lotic ecosystems enhances the importance of riparian zones, which constitute one of the most dynamic portions of the landscape, forming mosaics of land forms, communities and environments (Gregory et al. 1991). These zones play an immensely important role in the functioning of adjacent ecosystems, but we know very little about the biodiversity of the zones or the way in which such biodiversity influences their role in the movement of energy, nutrients, particles and organisms from one ecosystem to another. Again, they represent prime candidates for future research. 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