MARK REES PLANT DIVERSITY

Do trade-offs hold the key?

Recent studies highlight the importance of trade-offs between life-history traits and spatial sub-division of the habitat in maintaining diversity in natural communities.

Understanding why species coexist in natural communi- ties is one of the cerrtral problems in ecology. Knowledge of the mechanisms that prevent species from becoming extinct would allow the scientific management of ecologi- cal communities and provide a basis for rational decisions to be made concerning the conservation of biodiversity. At present, however, ecologists do not even have a realistic description of patterns of biodiversity on the planet, let alone a thorough qu:antitative model of a single commu- nity that would allow predictions to be made about the effects of mar-made perturbations arising from habitat destruction or pollution.

Against this rather gloomy backdrop, it should be em- phasized that curremly there is no shortage of possible mechanisms that could explain the patterns of diversity observed in well-studied communities. Classical compe- tition theory predicts that at equilibrium, in a spatially homogeneous environment, no more species can co- exist than there are limiting resources. When considering plant communities this raises a problem, because plants are autotrophic - they all require the same essential re- sources for growth, s,uch as light, carbon dioxide, water, and various mineral nutrients. How, therefore, do we ex- plain the extreme diversity we observe in some plant com- munities? A square mletre of chalk grassland, for example, may contain 30-40 species of vascular plants (Fig. 1). If each species was limited by a specific nutrient resource re- quired for growth then we should expect no more than five or six plant species to co-occur.

To get around this problem, it has been suggested that species are differentiated with respect to, say, their re- generation requirements [I] or the ratios of different nutrients required for growth [2], and that spatial and temporal variation in these quantities - so that commu- nities are not at equilibrium - might allow many species to coexist. It has also become clear that in order to under- stand the composition of any community it is important to study the transport processes that bring species to it - the so-called Gleasonian dimension. Gleason was a plant ecologist who viewed community structure as simply the “resultant of two factors, the fluctuating and fortuitous im- migration of plan&and an equally fluctuating and variable environment” [3]. This view, with its emphasis on stochas- ticity and dispersal, fell from plant ecologists’ favour in the 1970s and 1980s perhaps because of the difficulty in

Fig. 1. An area of calcareous habitat with numerous species of flowering vascular plants. (Photograph courtesy MJ Crawley.)

studying dispersal processes, but is now seen as an in- creasingly important paradigm for community structure.

In a paper soon to be published in Ecology [4], Tilman emphasizes that strong neighbourhood interactions com- monly occur between plants and that the dynamics and diversity of a community depend, not only on neighbour- hood interactions but also, on the dispersal of organisms among neighbourhoods. Tilman’s experimental work has shown that nitrogen is the only limiting resource in the old fields and prairie of Cedar Creek National History Area. Using models that assume a single limiting soil nutrient he has been able, for the first time, to predict success- fully the outcome of competition between four species of perennial grass, without first observing the species grow- ing together. The models, and experiments used to test them, assume the species are well mixed and as a re- sult predict competitive exclusion, which is observed in the experimental plots 151. At Cedar Creek, however, the species coexist, which suggests the mechanism that allows coexistence is missing from the models and experimental studies.

In order to reconcile the theoretical and experimental pre- diction that competitive exclusion should occur when the species compete, Tilman [4] developed a new model for several species competing for a single limiting resource. In the model, he assumes the environment is spatially

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subdivided and asks if this subdivision would allow a Iarge number of species to coexist when exclusion would oc- cur in an undivided hsnbitat. He also asks what traits foster coexistence and are such traits likely?

2000 4000 6000 8000 10000 Time 6)

Fig. 2. Dynamics of a 40 species community in a model with spa- tial sub-division of the habitat. With a spatially sub-divided habi- tat all 40 species coexist, whereas when there is no spatial sub- division competitive excllusion occurs and only a single species persists. (Adapted from Ml.)

Each species in the model is characterized by three pa- rameters: its colonization rate, its mortality rate and its competitive rank. In order to make the model tractable, Tilman assumes the species can be ranked competitively such that species with1 lower ranks (better competitors) can displace those with higher ranks, but not vice zlesa. For ‘biologically sensible’ sets of parameters (in other words, none of the species is inlinitely long-lived and all have finite colonization rates) there is no limit on the number of species that can coexist stably in the model (Fig. 2). If the habitat was not spatially subdi- vided, then the superior competitor would displace all other species. This coexistence mechanism Tilman calls the spatial competition hypothesis. Curiously, although there is no upper limit on the number of species that can coexist in the model there is a limit on the similar- ity of adjacent species in the competitive hierarchy. This means that the traits of the inferior competitor must differ from those of the superior competitor by a linite amount in order for coexistence to occur.

Species coexistence requires that different species must have the appropriate two- or three-way trade-offs among competitive ability, co~o~zation ability and longevity. A trade-off occurs when large values of one trait are as- sociated with low values of another: for example, if highly competitive species have low colonization ability then there would be a trade-off between competitive ability and colonization ability. Tiknan argues that there may be an unavo.jdablle trade-off between competitive and colonization abilities, simply because resources al- located to competitive structures cannot simultaneously be allocated to dis$!&al structures (see Figure 3 for an empirical example).

In contrast, it seems unlikely that there is a trade- off between competitive ability and longevity because in many ecosystems the longest-lived species are of- ten the competitively dominant. However, evolutionary theory predicts that long-lived species should have rela- tively short-lived seeds [6] and comparative studies have demonstrated this to be true for several plant communi- ties (M Rees, manusc~pt submitted). If long-lived species are also competitively dominant, then this provides an- other way in which a trade-off between competitive ability and colonization ability might arise; Comparative studies have also shown that long-lived species tend to have larger seeds and that these suffer higher levels of herbivory than seeds of short-lived species [7]. Again, this could result in long-lived, competitive species having low colonization success, leading to a trade-off between competitive ability and colonization ability. Hence, one of the impost re- quirements of the spatial competition hypothesis appears to be true for several plant communities.

: i R* for nitrogen (mg-N/kg-soil) . . .

Fig. 3. The trade-off between competitive ability and colonization ability in five grass species. The level to which a species reduces the limiting resource is its R* value, and in this case the R* val- ues for nitrogen determine the competitive abiiity of a species - those with low R* values are good competitors. Species with good colonization ability arrive within a few years of a site being created and are generally poor competitors (they have large R* values). in contrast, species with poor colonization abilities take many years to arrive at a site and are good competitors (they have low R* values). (Adapted from I4l.j

Importantly, Tilman also discusses how the models can be tested using manipulative experiments. He suggests that seed addition experiments could be used to deter- mine the extent to which local community structure is controlled by dispersal processes or by competitive in- teractions between species. Clearly, if seeds of the com- petitively dominant species are added to sites, resulting in local extinctions, then the spatial subd~sion of the habitat is likely to be important in maintaining diversity.

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Previously, it was thought that spatial variability in the con- centration of soil nitrogen controls the species richness of Tiltrun’s study sites [ 21. However, in experiments where the level of spatial variability of soil nitrogen has been ma- nipulated, no change in the species richness of the site was observed [S]. Evidently, the spatial variation in nitro- gen concentration cannot be the most important factor determining the spelcies richness of a site. When nitrogen levels are increased,, there is an increase in productivity and generally a decrease in species richness. This de- crease in species richness appears to be a widespread phenomenon, occurring in several communities, and is the result of either decreased local colonization or in- creased local extinction, or a combination of the two. The experiments at Cedar Creek demonstrate that the reduc- tion of species richness in the high productivity plots is caused as much by lower rates of colonization as by in- creased rates of species loss. Further experimental studies are required to tease apart the interaction between com- petition and colonization that determines which species are lost and why the likelihood of successful colonization is reduced. Experimentai studies are currently in progress to do just this.

In all the work I h,ave described there is an interplay between observation, theory and experiment. Ideas are explored theoretically and then tested in the field; ideas that are found wanting are then rejected. Such a rigor- ous research program is to be commended and it is perhaps worth remembering that demonstrating a pro- cess is unimportant in determining the structure of a

community is, in itself, progress, and should not be dis- missed lightly. Further studies that integrate observation, theory and experiment, particularly in species-rich tropical systems, will undoubtedly provide a deeper understanding of how diversity is maintained in plant communities.

References

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GRUBB PJ: The maintenance of species-richness in plant com- munities: the importance of the regeneration niche. Biol Reu 1977, 52:107-145. TILMAN D: Resource Competition and Community Structure. Princeton: Universily Press; 1982. GLEASON H: The individualistic concept of the plant associa- tion. Bull Torrq Bot Club 1926, 53:4@42. TILMAN D: Competition and biodiversity in spatially structured habitats. Ecology, in press. WEDIN D, TILMAN D: Competition among grasses along a ni- trogen gradient: initial conditions and mechanisms of com- petition. EcoZogical Monographs 1993, 63~199-229. REES M: Delayed germination of seeds: the effects of adult longevity and reproductive strategy. Am Nat, in press. THOMPSON K: Seeds and seed banks. New Pbytol 1987, 106:23-34. TILMAN D: Species richness of experimental productivity gra- dients: how important is colonisation limitation? Ecology, in press.

Mark Rees, Department of Biology and NERC Centre for Population Biology, Imperial College at Silwood Park, Ascot, Berkshire SL5 7PY, UK.