Vol. 14, No. 4, April 1999 News and Comment Biodiversity, ecosystems and interactions that transcend the interface David A. Wardle wardled@landcare.cri.nz Trends in Ecology & Evolution 1999, 14:125-127 Landcare Research, PO Box 69, Lincoln, New Zealand

The biodiversity of the planet has varied tremendously over the past 600 million years, during which there have been around five major extinction events. We are currently in the middle of a sixth wave of extinction, and continue to lose species rapidly at all spatial scales as a result of human economic activity and associated habitat destruction. Over the past decade, topics relating to biodiversity have shot to the top of international and national research agendas. A key question has been how the loss of species affects the provision of ecosystem goods and services necessary for our survival. Two meetings, held in the Netherlands in October 1998, sought to address specific aspects relevant to the issue of biodiversity effects and the consequences of species loss in ecosystems.

The diversity and function issue

The first meeting, held in Wageningen and organized by Hans de Kroon (Wageningen Agricultural University, The Netherlands), focused on the diversity-function issue. It has been about only six years since the first experimental studies were initiated to test explicitly whether diversity and function are causally related. These studies claimed to present evidence that several measures of ecosystem function (notably productivity) were greatest in treatments that had more species ^1,2 . This conclusion has led to the 'diversity debate', which is focused on two issues: (1) the poor agreement between results of experimental and observational studies or 'pattern and process' in nature; and (2) whether there are underlying factors or 'hidden treatments', which co-vary with diversity in many diversity experiments and thus confound their results ³.

J. Philip Grime (University of Sheffield, UK) reminded us of the relevance of 'dominance-diversity' curves ⁴ to the diversity-function debate and used this as a basis for a 'mass ratio' hypothesis ⁵. This proposes that different subsets of a plant community could act as 'dominants' (with important contemporary effects on function), 'subordinates' (which filter or select dominants after disturbance, thus determining their composition) and 'transients' (which represent dominants in other ecosystems and might be important in the long term). The mass ratio hypothesis highlights the importance of species composition and species traits in governing ecosystem properties, a message also emphasized by Frank Berendse (Wageningen Agricultural University). Berendse used two contrasting examples of heathland plants (Erica and Molinia) to demonstrate the effects that plant traits can exert on ecosystem properties.

The gulf between the results of recent observational and experimental studies was explored by Shahid Naeem (University of Washington, Seattle, USA), who suggested how Simpson's Paradox (conflating within and among responses to treatments) could help explain this discrepancy. Naeem also presented new experimental data. One dataset concerned the Cedar Creek LTER (long term ecological research) site, where effects of plant diversity on the ability of weeds to invade, and interactive effects between plant diversity and global change phenomena [such as carbon dioxide (CO₂) enrichment and nitrogen fertilization] are being tested. The other new data came from microcosm studies, in which diversity is manipulated across trophic levels.

Experimental approaches were also emphasized by Bernhard Schmid (University of Zürich, Switzerland), who presented recent results from the ongoing BIODEPTH (biodiversity and ecosystem processes in terrestrial herbaceous ecosystems) experiment, in which replicated plant diversity treatments are maintained at each of eight locations across Europe. Results show there are emerging biomass-diversity patterns both within and between sites.

Moving below ground (where most terrestrial biodiversity resides), Peter de Ruiter (University of Utrecht, The Netherlands) showed, using modelling-based approaches, that stability of food webs is governed by the strengths of interactions between the different trophic groupings constituting the food web ⁶. Augmenting this theoretical work with experimental data, de Ruiter also demonstrated that fumigated soils with reduced diversity were both less resistant and less resilient to a second stress (copper addition) than nonfumigated soils. Wim van der Putten (Netherlands Institute of Ecology, Heteren, The Netherlands) continued the below-ground theme, emphasizing feedbacks between above-ground and below-ground communities. This included presenting results from the first two years of the trans-European CLUE (changing land use: enhancement of biodiversity and ecosystem development) project, which showed that manipulation of plant diversity had little impact on a range of taxa of soil biota.

David Hooper (Western Washington University, Bellingham, USA) focused on three studies published consecutively in Science last year ^7–9 , which collectively demonstrated that species composition was more important than species or functional-group richness in affecting a range of ecosystem properties. He concentrated on the policy implications of this: the question that inevitably emerges is whether biodiversity does not matter as much as we thought it did. The answer is clearly that conservation of diversity does matter, because these studies still point to the considerable importance of community composition and individual species effects in maintaining ecosystems under changing conditions, and ultimately long-term ecosystem sustainability.

This policy angle is especially important, because many ecologists suggest, informally at least, that the diversity debate could help to undermine attempts to conserve species. If conservation policy is determined by whether experimental studies show causative relationships between diversity and ecosystem properties, then we as ecologists have collectively done a poor job of persuading the policy community of all the other extremely important scientific, not to mention ethical, reasons as to why it is a good idea not to let species continue to go extinct.


Diversity and interfaces

The second meeting was a SCOPE (scientific committee on problems of the environment) workshop on soil and sediment biodiversity and ecosystem functioning (SSBF), held in Lunteren and organized by Diana Wall and Gina Adams (both from Colorado State University, Fort Collins, USA) and Lijbert Brussaard (Wageningen Agricultural University). It brought together 44 ecologists from 16 countries to discuss and synthesize current knowledge of the relationships between biodiversity above and below the surfaces of soils and sediments in each of three domains: terrestrial, freshwater and marine.

The emphasis of the workshop was placed on interactions between organisms or processes that occur above the surface interface, and those that occur below (or, in the case of many aquatic systems, at) the interface. Last year a SCOPE SSBEF workshop initiated a synthesis of cross-domain relationships between biodiversity and ecosystem function ¹⁰. This year's workshop consisted of both within-domain working groups and across-domain discussions, aimed at addressing each of three questions.

The first question considered mechanisms by which biodiversity above the surface interface could be connected to that at or below the interface. There is a dearth of studies explicitly addressing this relationship, although several pieces of theoretical and empirical evidence were presented both for and against why we might expect the relationship to be strong. Insights can be gained by considering subsets of the above-surface and below-surface biodiversity that demonstrate strong associations with each other and generate feedbacks that transcend the interface.

For example, conversion of forest to pasture in Amazonia reduces resident macroinvertebrate biodiversity, which encourages domination by the earthworm Pontoscolex corethrurus. The earthworm causes soil compaction and reduced soil infiltration, which induces above-ground feedbacks by reducing pasture production ¹¹. Similarly, in freshwater, those colonies of the cyanobacterium Nostoc parmelioides (inhabiting the sediment surface interface) that house larvae of the midge Cricoptus nostocicola change colony shape during development. The new shape enables them to respond better to light, thus enhancing both productivity and nitrogen fixation ¹², with ecosystem-level consequences for both sides of the interface.

The second question explored how relationships between biodiversity above and below the surface affect the stability (resistance and resilience) of communities and ecosystem processes. Although detritus has apparent stabilizing properties on below-surface foodwebs – and it would seem plausible that these effects feed back to the above-surface subsystem – the subject of linkages between above-surface and below-surface stability remains almost entirely unexplored. A better understanding of linkages across the surface interface that involve stability is essential if ecosystems are to be sustainably managed. For example, intense fishing pressure off the coast of Newfoundland (Canada) has resulted in replacement of an entire above-surface functional group (pelagic feeding fish, such as cod and herring) with another functional group (skates and rays) that live among the sediment layer and cause significant below-surface disturbance. Extremely low resilience of the system means that there is little sign of this switch being reversed even after cessation of fishing in the area for several years.

The third question considered how relationships between above-surface and below-surface biodiversity might respond to global change and feed back to determine further ecosystem responses to global change. The components of global change that are likely to be most important are very different across the three domains. In terrestrial ecosystems, phenomena such as CO₂ enrichment and land-use change are likely to have major ecosystem effects. There is a growing literature on how these effects might transcend the interface between above ground and below ground.

Climate-change patterns are probably important in affecting trans-surface relationships in all three domains, although the mechanisms involved are likely to be very different. In the marine domain, one potentially very significant, although little understood, aspect of global change is the nature of changes that are likely to occur in oceanic circulation patterns, such as movements of the Gulf Stream. Invasions of organisms into new habitats is an extremely important component of global change in all domains, and yet astonishingly little is known about the effects of invaders on organisms on the other side of the surface interface.

A key theme of this workshop was to compare trans-surface relationships across all three domains. Although there are strong parallels across the domains, there are many important differences. For example, the origin of organic-matter inputs differs markedly ¹³. Detritus in terrestrial systems tends to come from plants in the same vicinity; in streams, detritus often originates from upstream as well as laterally; and in marine systems detritus passes through the pelagic water column before reaching the benthic surface. The nature of trans-surface interactions is another important difference between the three domains. For example, plant–microbial mutualisms aimed at enhanced acquisition of nutrients, and below-surface manifestations of effects of herbivory, are likely to be more important in terrestrial ecosystems than in many aquatic ones.


Underlying themes

Both meetings explored fundamental and emerging aspects of biodiversity research that are relevant to understanding the consequences of species loss from ecosystems. One aspect that has mushroomed in particular over the past five years is how biodiversity affects ecosystem properties. There are now several large experiments investigating this. Consideration of the relationship between above-surface and below-surface diversity feeds into the issue of how biodiversity affects ecosystem properties by addressing how the biodiversity of one group (e.g. trophic level or guild) of organisms affects the biodiversity of another. This latter topic is in its infancy; indeed, only two experimental studies have explicitly considered how plant diversity affects diversity of consumer trophic levels, one focusing below-ground ¹⁴ and the other focusing above-ground ¹⁵.

The results of ongoing studies and syntheses aimed at developing a mechanistic understanding of the consequences of species loss from ecosystems, as emphasized at these meetings, will be essential for two reasons: (1) to improve our understanding of how we can manage our resources in a more sustainable manner; and (2) to understand better the consequences for the earth's ecosystems of allowing the current rate of loss of species to continue unabated.


Acknowledgements
The Wageningen symposium was organized by the Centre of Ecology (Wageningen) and was sponsored by the Wageningen Agricultural University and Research Centre, the Graduate School for Functional Ecology, the C.T. de Wit Research School for Production Ecology, the Wageningen Institute for Environment and Climate Research and the Institute of Forestry and Nature Research. The Lunteren SCOPE SSBEF workshop was sponsored by the Netherlands Ministries of Agriculture, Environment and Public Roads and Waterways, the Royal Netherlands Academy of Arts and Sciences, and an anonymous USA foundation.

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