Spatial Scale and the Determinants of Plant Species Richness Michael Auerbach and Avi Shmida Traditional ecological theory has stressed the importance oj competitive interactions in regulating species richness. Recent research has transcended this viewpoint by considering the role of stochastic processes, mosaic phenomena and nonequilibrium conditions in the regulation of richness. This growing body of work indicates that the determinants of plant species richness may vary predictably over different spatial scales. One of the great challenges to biologists is to explain the phenomenal geographical variation in the number of species on our planet. A complete answer must embody both the evolutionary processes which produce species in the first place and the ecological processes which secondarily regulate species richness. In this short review, we must forgo the issue of speciation, and simply take the wealth of organisms as given. Instead we focus on a central theme of modern ecology, the elucidation of determinants of species richness. We also limit our discussion to plants. Traditional ecological theory offers two principal answers to the question of what determines the number of coexisting species at the local (community) level1'2: (1) species partition limiting resources so that each is limited by a different component of available resources (resource differentiation); and (2) species use different portions of available habitats or differ in the range of habitats in which they are competitively superior (habitat differentiation). Both explanations invoke the concept of a trophic niche - an organism's role in a community as defined by resource use and species interactions. Under both viewpoints interpretations of species coexistence were predicated on the competitive exclusion principle, which states that coexisting species must differ in their trophic niches2. Michael Auerbach is at the Dept of Biology, University of North Dakota, Grand Forks, ND 58202, USA; Avi Shmida is at the Dept of Botany, Hebrew University. Jerusalem. Israel. One need only glance at chapters in any of several new volumes on. community ecology to appreciate that the issue of determination of species richness has been carefully re-examined over the last decade3-5. The deterministic, equilibrium explanations based on competition and niche theory have been superseded by models incorporating dynamic processes that influence species coexistence. Current research concentrates on three interrelated areas in particular: stochastic processes, patch dynamics, and equilibrium versus non-equilibrium states6-8. To illustrate this change in thinking, we examine in detail a familiar pattern of species richness, the species-area relationship. It has long been recognized that species number tends to increase with increasing sampling area9 (Fig. 1). It is clear from Fig. 1 that the relative importance of various determinants of species richness varies with spatial scale. To account for scale and to categorize the myriad of possible determinants, we partition them into four groups: niche relations, habitat heterogeneity, mass effects, trophic equivalency10. This is by no means the only method of classification and space does not permit us to discuss all the suggested regulators of species richness. We present this example simply to illustrate some new avenues of research. Niche relations Plant species differ in their edaphic, climatic and biotic micro-habit requirements and tolerances2; these niche relations, in combination with the size of source floras (available species pool), are important determinants of species richness over small spatial scales10 (Fig. 1). Much of plant ecophysio-logy has focused on delineating the tolerances of plants to different abiotic regimes and elucidating the role of differential tolerance in limiting geographical distribution". However, tolerance of environmental conditions alone is not sufficient for continued local existence because interspecific interactions, such as predation or allelopathy, may restrict niche dimensions. In fact, classic niche theory, which was developed largely by animal ecol-ogists, viewed the impact of interspecific interactions (particularly competition) on niche dimensions as the principal determinant of local species richness1'2. Even though resource and habitat differentiation undoubtedly influence local species richness, it is difficult to envisage every plant species in a species-rich community occupying a different habitat niche (Box I). Coexistence of species with similar habitat niches may be possible because of variation in other niche components12. For example, differences in size, productivity and architecture may permit coexistence, such ,as the cooccurrence of trees and herbs with similar resource requirements. In addition, differences in life form may enhance local richness because of dependent relationships, such as those between parasitic plants (or lianas, vines, etc.) and their hosts. Phenological differences between species that result in temporal division of resources may also increase local richness by mitigating competitive interactions12. One aspect of niche relations, the regeneration niche, may be particularly important in regulating local species richness12'13 (Box I). A species' regeneration niche encompasses the environmental conditions, biological attributes and biotic interactions required for perpetuation of a species in a community. Thus, germination requirements, mode and timing of seed dispersal, growth form, environmental tolerances of seeds and seedlings, characteristics of nearby vegetation, and interactions wjth pests and disease, are important elements of a species' regeneration niche. The concept of regeneration niches emphasizes the importance of investigating habitat requirements of all life-history stages of a plant, rather than just those of adults, since they may shift over a species life cycle14. For example, common short-lived forbs of chalk grasslands exhibit different micro-site preferences in seedling and in vegetative and reproductive stages15. Age-specific changes in Trophic equivalency^ niche relations suggest that species may not always be able to colonize an open microsite produced by death of a mature conspecific. Despite the many ways in which differentiation in various niche components may facilitate coexistence, some researchers have suggested that there need not be any significant differences in the niches of some co-occurring species16, particularly sparse ones13'17 (see below]. Habitat heterogeneity As sampling area begins to exceed the size of individual organisms, habitat heterogeneity becomes a determinant of richness. The influence of habitat diversity on species richness is apparent over many spatial scales from local pattern of microsites to regional spatial heterogeneity10. Traditionally, habitat heterogeneity was interpreted to influence richness through the niche-based processes of interspecific competition, habitat differentiation and resource partitioning2. Obviously, an increase in local habitat diversity provides a more varied backdrop for differentiation and specialization. Recent research, however, suggests numerous other ways in which heterogeneity, particularly microsite pattern, can influence richness. Better understanding of the impact of microsite pattern on richness has emerged from greater appreciation of the causes of micro-site heterogeneity, the regeneration process, and the nature of plant competition. Over the last decade, plant communities, including non-serai ones, have increasingly been viewed as mosaics of microsites that differ in environmental attributes and successional status7'8. Some of this within-community heterogeneity is relatively static and predictable, such as local variation in topography or edaphic factors. However, habitat mosaics are frequently created by a variety of stochastic disturbances. Within-community patches result from small-scale disturbances, such as the death of a tree which opens a new microsite for colonization. Larger disturbances, such as fires, hurricanes or other extrinsic factors, are usually invoked to account for intercommunity mosaics8. The importance of disturbance and patch dynamics in regulating community richness is an extremely active area of ecological research. Virtually every type of plant association has been re-interpreted in the context of disturbance and habitat mosaics8'18. A major theme emerging from this research is that not all disturbances are catastrophic ones that reduce richness. Instead, the predictability, frequency and intensity of disturbance will determine which of the existing species may be expected to withstand the perturbation. Within-habitat heterogeneity in resource quality and availability can influence richness substantially through its impact on the regeneration process. As mentioned above, age-specific differences among and within species in their microsite requirements can, if a mosaic of such microhabitats exists, provide a basis for specialization, and thereby promote richness19. However, regeneration depends upon successful colonization of such suitable habitats, the location of which may be unpredictable in space or time. Which propagules reach a microsite depends on species composition of the source pool of potential colonists and the dispersal ability, reproductive biology and phenology of these species8'18,20. The dynamic aspect of regeneration is reflected in the population dynamics and life histories of many plants. For example, local extinction of biennials is common in many habitats because conditions suitable for germination and seedling establishment are transient21. For these species to persist, they must repeatedly colonize new habitat patches. One finds myriad adaptations among plant species to the unpredictability in time and space of safe sites, including seed dormancy, delayed flowering and variable dispersal propensities6'22. Considerations of regeneration processes have frequently led to suggestions that in many plant communities preemptive competition (competition to reach and occupy a suitable microsite first) is more intense than interactive competition among established individuals22'23. Dissatisfaction with two basic tenets of niche theory has paralleled appreciation of the import- ' 0.1 hectare /World ^Europe ^-^Israei _..---'*Carmel province I 102-E ° '10"' 10' 103 10s 107 103 1011 10" 10IS : Area (m2) Flg. I. Species-area curve extending over several scales, from samples in the mattoral (chaparral) in Israel to the entire world. The depth of each hatched area shows the postulated contribution of each factor to species richness at different spatial scales. Redrawn, wiik permission, from Ref. I0. ance of preemptive competition and regeneration in determining local richness. Unlike most of traditional niche theory, much of the research in the last decade neither assumes equilibrium assemblages, nor ignores stochastic environmental variation23-26. By considering patchy distribution of resources and small-scale spatial and temporal disturbances, recent empirical and theoretical research suggests that in many communities more than one species can occupy the same (or at least a very similar) trophic niche6'16-23. We refer to these species as trophic equivalents, stressing the notion that despite similar patterns of resource use and habitat preferences, these species may differ in ecologically significant traits such as reproductive behaviour or seed dispersal mechanism. Spatial or temporal habitat heterogeneity can promote trophic equivalency6. First, consider temporal environmental variation. As noted above, predictable seasonal events may permit phenological Box 1, Components of a plant niche To account for the diverse aspects that define a plant's niche, Grubb12 has subdivided the niche into four components: habitat, life-form, phenological and regeneration niches. Habitat niches are defined by the physical and chemical limits tolerated by mature plants. Life-form niches are related to growth form and productivity. Seasonal patterns of development delimit phenological niches. Regeneration niches encompass all conditions required for perpetuation of a species in a community. separation of potential competitors. Alternatively, the suitability of a microsite for a given species may depend on stochastic environmental variation. For instance, three codominant grasses co-occur in parts of central Texas27. Although the relative favorability of different microsite types varies little among the species, differences do exist in the effect of soil moisture on germination. Codominance of these species appears to result from differential year-to-year success among species as a result of fluctuations in timing of rainfall and temperature27. Numerous mathematical models have also demonstrated the possibility of coexistence of trophically equivalent species provided there is environmental fluctuation. Prominent among these are 'lottery' models which assume that competition among recruits is for space and that space is allocated randomly to propagules of different species6-26. Although there are many variations on the basic model, two criteria for coexistence generally must be met. First, environmental variation is necessary so that each species has periods of strong recruitment at low densities. Second, generations must be overlapping. This criterion need not be met only by adult cohort persistence; annual plants with a seed bank may also be considered to have overlapping generations. Long-term coexistence results when each species has positive average population growth because of occasional periods of strong recruitment26. Spatial variation in recruitment based upon habitat patchiness can likewise produce coexistence of trophically equivalent species, provided there is non-uniform seed dispersal between patches26. In this case dispersal takes the place of overlapping generations. One may infer from models of spatial heterogeneity that species with alternative life histories, such as a superior competitor and a superior disperser, can coexist6. Frequently, spatial and temporal heterogeneity coincide, suggesting a multiplicity of ways in which variation in colonization strategy can promote coexistence. Weedy plants, for example, exhibit a suite of highly correlated adaptations ranging from an annual growth form with limited dispersal ability but long seed dormancy to perennial, vegetatively-reproducing species with long range seed dispersal but limited seed dormancy22. Disturbances per se may also maintain local species richness by altering competitive interactions among adults. For example, shifts in competitive dominance resulting from differential response to spring versus autumn droughts appear to be one of the mechanisms promoting coexistence of two species of Erod/uw28. In addition, any disturbance that reduces or maintains population sizes of resident species below a point at which competitive exclusion is possible (or rapid), but not intense enough to result in local extinctions, may permit trophically similar or equivalent species to coexist6'13. The extent to which this occurs may depend on the intensity of competition and degree of dominance found within a community. Variability in competitive ability and dominance of species in different communities may in turn be associated with differences in productivity. Grime20 suggests that intermediate productivity allows interactions among niche differentiation, disturbance and habitat heterogeneity which together maintain high richness. This hypothesis, that productivity influences the impact of disturbance on biotic interactions, and consequently richness, is supported by studies of subalpine meadow vegetation29. Either biotic or abiotic 'disturbances' may be involved in maintaining species richness. For instance, disturbance from wave action and fluctuating water levels appears more important in regulating coexistence of lakeshore vegetation than does specialization along a water-depth gradient30. Similarly, predation or pathogen attack focused upon more vigorous species (compensatory mortality) can reduce dominance and prevent exclusion of inferior competitors31'32. By altering dominance patterns, disturbances may be extremely important in maintaining the sparse and patchily distributed species that comprise a large proportion of the total richness of many communities13'17. The low population sizes and spatial arrangement of these species suggests that they may be more suppressed by dominant species than by each other. Many interpretations of within-community mosaics and patch dynamics assume an overall dynamic equilibrium state at the community level, despite disequilibria at the patch level28. However, other hypotheses suggest that in some communities disturbance is frequent enough that steady-state conditions are never attained. Prominent among these is the 'intermediate disturbance hypothesis' which predicts that the highest richness should be maintained when disturbance is intermediate in frequency and intensity25. If disturbance is too frequent, low richness will result from insufficient time or inappropriate conditions for recolonization. If disturbance is very infrequent, richness will decrease because of competitive elimination of some species. Despite its prominence in current ecological literature, the generality of the intermediate disturbance hypothesis is questionable. As noted above, disturbance can maintain richness through its influence on niche differentiation, regeneration or dominance expression. The impact of disturbance, therefore, should depend on the type of- competitive interactions found within a community, and the extent to which species, especially dominant ones, are affected -selectively. Yodzis23 distinguishes three types of competitive structure: (1) niche control, in which consumptive competition is paramount; (2) dominance control, in which spatial (preemptive) competition predominates and functional dominants occur; and (3) founder control, in which spatial competition operates through colonization because dominants are lacking. The relationship between disturbance intensity and richness varies among these community types. Unlike niche-dependent theory, non-equilibrium models emphasize the importance of chance and history in determining species richness. For instance, the phenomenally high local diversity of tropical rain forests is frequently discussed in terms of non-equilibrium conditions resulting from stochastic disturbance24'25. Hubbell and Foster16 argue that a history of disturbance has produced guilds of functionally equivalent generalist tree species, in part because neighbors, and hence inter-tree interactions, are temporally and spatially unpredictable. High local richness results from the slow dynamics of competitive elimination under these conditions. These mechanisms demonstrate how habitat heterogeneity and the processes producing heterogeneity can influence species richness at the community level. The stochastic nature of many of these mechanisms also explains much of the variability among community samples. As sampling area exceeds the size of a community, habitat heterogeneity will continue to contribute to an increase in richness because of the inclusion of new habitat types10. Mass effects Mass effect is the transient dispersal and establishment of species from nearby habitats into sites where they are not self-maintaining10 (Fig. 2). Since natural communities are not closed systems, some propagules arriving at any site may belong to species established in nearby communities. A subset of these species may be able to survive but not reproduce in the new habitat. Persistence of these species in less favorable areas depends on copious seed production in, and continued dispersal from, their source habitats. The contribution of mass effects to species richness depends on the amount of dispersal of species from their regions of self-maintenance, size and environmental complexity of the region of invasion, and the richness of nearby biotas10. Generally, mass effects are most important at meso-spatial scales (Fig. 1). in small areas, limited target area will constrain the invasion of species. Similarly, at scales that exceed the dispersal distances of most species mass effects will be minimized. Mass effects should be most pronounced in areas of transition between distinct floras10. Trophic equivalency Although trophic equivalency can small to medium spatial scales through habitat heterogeneity (discussed above), its greatest effect is probably at larger (regional to continental) scales. At such scales, topographic and geographical barriers to dispersal restrict the possibility of mingling. Geographically Isolated species may, in fact, have not only similar trophic niches but also similar reproductive and dispersal syndromes10 (ecological equivalency). Conclusions in summary, a multitude of factors may regulate species richness, and the relative importance of any given factor varies with spatial scale". We have emphasized the influence of habitat heterogeneity, because recent research on stochastic processes and patch dynamics has greatly enhanced understanding of richness determination. This research also demonstrates that different determinants do not function assoclatively, but rather Interact in diverse ways to govern richness. Further understanding of the determinants of richness and their interactions should help reconcile some current debates in community ecology. For example, the idea of community convergence extends the concept of ecological equivalency to the community level, suggesting that communities in geographically isolated but environmentally similar regions should converge in growth form or species richness34-35. Convergence would imply that contemporary climate and edaphic conditions are paramount in determining richness, whereas non-convergence would suggest differences in phytogeo-graphy, floristic history and disturbance33. Current empirical evidence on convergence in richness is equivocal, due in part to inadequate sampling procedures, but also to differences in the scale of comparisons34. For instance, comparisons made over small spatial scales where niche relations are a primary richness determinant are probably more likely to show convergence than are ones made over large scales where the impact of disturbance and history is more pronounced. Resolution of the Issue of convergence, as well as 120 100 m 'o I 80 "o g 60 I | 40 E =s O '20 D .* T2 — 107 spp. \.'------" T3=»80spp. 44 spp. L 0 10 20 30 40 50 Contiguous sequential 1 mz quadrats Fig. 2. The influence of mass effect on species richness. The upper diagram shows three transects In the ludean Desert, Israel: T„ across a homogeneous valley habitat (A); Tj, across foothills encompassing four habitat types (8-Eb and T,, along the same homogeneous valley except ad|acent to the foothills. The lower diagram shows the relationship between richness and sampling area over the three transects described above; the arrows Indicate the positions of the habitat boundaries crossed by Tj. Transect T, has 36 more species than transect T,s the presence of 29 of these can be attributed to mass effects. More rapid increases In species richness along transect Tj coincide with habitat transitions along transect T3. 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