Popul Ecol (2002) 44:189200

The Society of Population Ecology and Springer-Verlag Tokyo 2002

SPECIAL FEATURE: REVIEW

Mutsunori Tokeshi Peter E. Schmid

Niche division and abundance: an evolutionary perspective

Received: February 4, 2002 / Accepted: October 25, 2002

Abstract In recent years, biodiversity has become an issue of broad academic interest, and its assessment and maintenance are now recognized as an important area of ecological research. While the concept of biodiversity encompasses, rst and foremost, the total number of species co-occurring in a locality, it has increasingly been realized that information on the relative abundances of co-occurring species is also required for a better understanding of the patterns and dynamics of biodiversity. In many areas of ecological research, abundance constitutes a key variable that characterizes populations and communities. The relative abundances of species in natural communities reect evolutionary and contemporary processes occurring on different spatiotemporal scales. The idea of niche apportionment has been developed to provide an integrated conceptual framework for the study of species abundance patterns in communities. This article reviews a number of important issues surrounding the concept of niche apportionment, including some aspects that have received very little or no consideration in previous ecological literature. The main emphasis here is on possible evolutionary implications and backgrounds. Further, as a universal factor which affects species abundance in one way or another, body size is highlighted and its relationship with abundance (densitybody-size relation) is considered, referring in particular to a recent comprehensive analysis of freshwater benthic data. Consideration of this and other studies has led to the formulation of the biomass equivalence rule, that suggests the independence of the biomass measure of abundance from body size, which strengthens the logical basis of niche apportionment models. It is suggested that, compared with Hubbells neutral theory of biodiversity, niche appor-

tionment with the biomass equivalence rule represents a conceptually more sound and widely applicable approach to elucidating species abundance patterns. Key words Species abundance patterns Niche apportionment Body size

Introduction
Niche division and species abundances are closely related aspects that are linked in a fundamental manner to biodiversity. Biodiversity itself has increasingly been recognized as an issue of major importance from both academic and social points of view, with its ramications and scientic challenges being discussed in a wide range of publications and conferences (Wilson 1988, 1992). As separate aspects related to biodiversity, niche division and the abundances of species are thought to reect a suite of processes operating on different spatiotemporal scales. This paper reviews some recent developments in the conceptual framework and analysis of niche division and species abundance patterns, mainly from evolutionary viewpoints. In essence, species abundance patterns can be framed as a product of evolutionary processes that may be elucidated from different angles. Abundance patterns may be linked to various scenarios of niche division through evolutionary time. There are different issues of importance surrounding this approach, which may not have been fully discussed or recognized in previous work. In this respect, both empirical and theoretical analyses of data are considered necessary in order to assess the variability and temporal trajectories in community patterns. In this article, some important issues concerning the concepts and analyses of species abundance patterns are highlighted. Studies on diverse ecological assemblages have generated various hypotheses relating the pattern of abundances to a number of ecological parameters, most notably body size. However, the exploration of community structure, including densitysize relationships, has often suffered from

M. Tokeshi (*) Amakusa Marine Biological Laboratory, Graduate School of Sciences, Kyushu University, Reihoku-Amakusa, Kumamoto 863-2507, Japan M. Tokeshi P.E. Schmid School of Biological Sciences, Queen Mary, University of London, London, UK

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the inadequacy and incompleteness of available data, casting some doubt on the true nature of reported patterns. In an attempt to rectify this situation, a research project was undertaken involving a thorough analysis of density body-size relationships in two comprehensive data sets encompassing geographically separate stream benthic communities in Europe. This work revealed remarkably similar densitysize patterns in the two communities, although their faunal composition was different. Furthermore, ndings from this and other recent studies have led to a novel hypothesis concerning the distribution of biomass among species of different sizes in an assemblage. The implications of this hypothesis in the context of analyzing abundance patterns are considered.

Species richness and diversity

At the most fundamental level of ecological inquiry, research into biodiversity concerns species and their richness occurring in a dened area at a particular point in time. Similarly, the principle of niche division is implicitly concerned with species, rather than subspecies (varieties), genera, or higher categories. A species represents the most basic phylogenetic unit that is evolutionarily more concrete than higher units such as genera, order, and family (Ghiselin 1984). This is the reason why attention should rst be focused on species diversity, rather than on generic or familial diversity. This parallels the view that an evolutionary pattern at the species level has an existence of its own, whereas patterns above the species level may be regarded as nothing more than epiphenomena, which are dependent upon species-level processes and are consequently less valuable in revealing true evolutionary trends. On the other hand, the issue of using information on higher-level taxonomic categories as surrogates of species-level patterns is of distinct practical importance (Tokeshi 1999), and is often considered in relation to temporal patterns of species richness. In the modern biological species concept, the state of interbreeding and reproductive isolation has been considered to be an important element in the denition of a species (Mayr 1942, 1963, 1970; Wiley 1981; Templeton 1989; Avise and Ball 1990). However, in the vast majority of cases, the taxonomy has lacked access to information on breeding, and has relied solely on morphological characteristics. While the situation is improving fast with the easy availability of a battery of molecular techniques which allow the extraction of genetic information from even a single individual, morphological analysis still predominates over taxonomy. Such a reliance on morphology inevitably led to a situation where doubt was cast upon the concordance between morphological species and the idealized species concept based on reproductive isolation. This was fuelled by studies on Paramecium, Drosophila, and many others, which showed that morphology alone cannot separate species (Dobzhanski 1951). The problem is more acute in palaeontology, where morphological information, often

quite incomplete owing to the nature of fossil preservation, is normally the only basis on which taxonomic work is conducted (although again in this discipline molecular techniques are increasingly applied, and the availability of nonmorphological information is gradually improving). Given such circumstances, Smith (1994) proposed the use of a different term, phenon (plural phena), in place of an ambiguous use of species, to denote a group of morphologically identical, consistently diagnosable fossil forms. Although this practice is certainly useful, and is scientically rigorous when one is trying to resolve the phylogenetic relationships of extinct organisms found in widely scattered stratigraphic horizons, the same problem of morphologybased taxonomy exists for the classication of contemporary species occurring in wide/separate geographical regions. Given the enormous range of organisms and our limited resources for taxonomic work, the majority of extant organisms are, and will continue to be, classied solely on the basis of morphology. Thus, the same types of ambiguity remain with both contemporary and fossil species; the difference between these is no more than a matter of degree. Therefore, it is reasonable, and less confusing, to use the term species for organisms of all ages. The perceived difculty in applying the biological species concept to actual taxonomy (Mallet 1995) is indeed fundamentally related to the crucial issues of speciation, particularly micro- to macroevolution. Species richness is ultimately dependent upon a balance between the rates of origination and extinction through evolutionary time. This necessitates a consideration of speciation as the starting point of any discussion on biodiversity. Speciation is a subject that has traditionally lain outside the sphere of community ecology, although an increasing number of studies deal with aspects of speciation in community contexts. As long as the efcacy of Darwinian selection appilies, speciation is a supremely ecological issue. On the other hand, the genetic (not ecological) background of speciation lies outside the scope of this article, and therefore will not be considered here. A brief discussion of terminology may now be appropriate. Diversity is a long-standing ecological concept that has recently been rivaled by the more recent, popular term biodiversity. While the term diversity has had a ubiquitous appeal among ecologists (Cherrett 1989), and is frequently used in the ecological and palaeobiological literature, it now seems that biodiversity has overtaken the prime position. In reality, however, one can nd little substantive difference between diversity and biodiversity, since they overlap to a large extent. On the other hand, it should perhaps be noted that the current use of the term biodiversity is heavily inclined to the aspect of species richness, rather than genetic/functional diversity or anything else (e.g., Wilson 1988). Indeed, one of the biggest questions posed by the recent spate of research into biodiversity concerns estimations of absolute species richness, or the total number of species living on the Earth. Biodiversity research is in a state of evolution, and aspects other than species richness are increasingly incorporated in order to document organismal diversity with all its ramications. Its ancestral

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form, diversity, has also frequently been used in synonymy with species richness, especially in the palaeobiological literature (indeed a large part of the discussion here, which involves palaeobiological considerations, relies on this use of the term). However, it should be stressed that in many works, diversity implies not only the species richness aspect, but also the relative abundance aspect of its strict, technical denition (cf. Pielou 1975). Here, our argument is that research into biodiversity will gain substantially if the aspects of absolute and relative abundances of species are considered together with the aspect of species richness. Dealing only with the number of species will inevitably constrain our understanding of the processes underlying biodiversity.

Niche division: conceptual background

One can start with questions as to whether, and how, the pattern of relative abundance matters in a consideration of biodiversity. A simple example sufces. When species assemblages from different localities are compared, they differ not only in species richness, but also in the relative abundances of constituent species. Even if species richness happens to be the same, different assemblages are likely to demonstrate different patterns of relative abundance. Suppose there are two assemblages containing the same number of individuals (n 1000) and of species (S 10): one assemblage has 100 individuals in each of the ten species, while another assemblage has 910 individuals in one species and 10 individuals in each of the remaining nine species. Although this is an extreme case, and real assemblages may not show as large a difference as in this example (but some do), it is reasonable to suggest that the underlying mechanisms or factors which govern the abundances of species may be fundamentally different among assemblages. Furthermore, it is also apparent that the second assemblage has a higher probability of experiencing the extinction of some species and hence a reduction in species richness, as nine species are numerically closer to zero abundance than the species constituting the rst assemblage. Apparently there is a conspicuous difference between these two assemblages in the nature of their biodiversity. Thus, variations in abundance patterns have a close bearing on species richness. This illustrates that there is potentially a great deal to be gained from an analysis of relative abundance patterns, or species abundance patterns, in understanding the dynamics of community organization and biodiversity. While ecological processes such as birth, death, immigration, and emigration determine the abundances of species under the inuence of various biotic and abiotic factors (Begon et al. 1996), their long-term average levels of relative abundance are more likely to result from evolutionary processes of niche occupation in an adaptive landscape. Such evolutionary processes have operated in different forms and strengths until the present time, and consequently all extant species that occur in the adaptive landscape reect the varied inuences of those evolutionary

processes. Therefore, relative abundances reect the combination of evolutionary and contemporary ecological forces acting upon organisms. This adds weight to the view that an investigation of relative abundance patterns could provide an insight into the mechanistic processes of diversity, i.e., how species multiply and coexist in evolutionary contexts. Extending the link between variations in species richness and in relative abundances, we can pose the fundamental question of how changes in diversity might occur in species assemblages over evolutionary time. The question here concerns the possible modes of increase in diversity. As diversity and organismal abundances are ultimately related to the availability of niche space or resources, a consideration of a niche spectrum is useful in this respect. Here, the measure of abundance needs to be expanded to include not only the numerical abundance of a species (i.e., number of individuals), but also the biomass and its surrogates, as the latter may be more appropriate when applied to the concept of niche division. While an ecological niche encompasses a multiplicity of facets, or multidimensionality (Tokeshi 1999), conceptually it can be represented as a single, allinclusive mass or spectrum that is subject to division by a set of species. Considered in simple and broad terms, an increase in diversity may be envisaged as one of two, not necessarily mutually exclusive, processes. First, organisms may acquire the ability to exploit new resources (or niches) that have not previously been utilized by existing species, i.e., invasion of a new adaptive zone (sensu Simpson 1944, 1953) (Fig. 1a). Second, an existing resource pool may be progressively divided or shared by an increasing number of species; in other words, invasion/division of an already exploited niche space (Fig. 1b). If peripatric speciation has been the dominant mode in the evolutionary origination of species, this second process is perhaps an appropriate representation in many cases. An ancestral species that spreads over a wide resource spectrum, in terms of habitat space or food resources, may split into two or more species, each specializing in a narrower range of resources. These two processes, i.e., niche expansion and fragmentation, may operate simultaneously or merge together in and across various taxonomic groups. Broadly speaking, however, the former is more signicantly associated with diversication of higher taxa such as phyla, orders, and families, whereas the latter tends to characterize phylogenetically closer groupings such as genera, species, and sub/sibling species. For example, increases in the diversity of marine benthos (the number of families, in particular) from the early to mid-Palaeozoic (Sepkoski 1979) and during the Mesozoic (Bambach 1977, 1983) seem to have been accompanied by increases in the range of morphologies and life styles exhibited by the organisms concerned, which presumably indicate a widening resource spectrum. In contrast, an assemblage of species that broadly share the same resource spectrum (or form a trophic guild) is often closely related phylogenetically, and is likely to have been derived from some processes of fragmentation of the original niche space of an ancestral species. Further, it is possible that in

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Fig. 1. Different modes of increasing diversity with time. a Niche expansion; b niche fragmentation; c niche lling. See text for explanation

many taxa these two modes of diversication/resource use grade into each other (cf. Sepkoski 1988), e.g., the wellknown trophic diversication in the cichlid shes of Lake Malawi (i.e., widening of the resource spectrum), with the concurrent existence of groups of species apparently sharing the same resource in the same manner (Fryer and Iles 1972). Another salient example refers to distinct insect herbivore assemblages associated with different tropical plants which, at the same time, demonstrate a number of species sharing the same host plants (e.g., Strong 1982). A consideration of shorter time scales suggests a different mode of increase in diversity. While the spectrum of resources available to the Earths biota has steadily widened over evolutionary time, it may be argued that for a period of less than 1 Myr (which was still a long enough time for speciation in many groups, but too short for the

diversication of higher taxonomic categories), the size of the total resource pool available to a particular lineage of taxa remained roughly at around the same level. Under such circumstances, an increase in (local) diversity may be envisaged as a more or less sequential lling up of the potential total niche space, which may correspond to the formation of a guild (Fig. 1c). This situation is considered as an intermediate between diversication based on expansion into new niche space (Fig. 1a, undened total niche space) and that based on a progressively ne division of an already exploited niche space (Fig. 1b, full exploitation of the total niche space since the beginning). Some palaeontological evidence suggests that such processes of community assembly might have occurred repeatedly over the relatively short time scale of 20100 kyr following climatic changes (Milankovitch cycles: Bennett 1990; Coope 1994). In terms of guild formation, niche fragmentation (Fig. 1b) and niche lling (Fig. 1c) may represent two extreme cases, with many actual assemblages probably lying between them. In a phenomenological treatment of the theory, however, the difference between these modes can disappear in practice, and the two can be dealt with in a single framework (see below). The entire evolutionary increase in diversity can indeed be postulated as a combination of some major events representing expansions into a new niche space, and a progressive lling up or division of the newly emerged niche space. This conforms with the idea of Knoll and Bambach (2000) that six stages (termed megatrajectories) capture the essence of vectorial change in the history of life. They suggested that six megatrajectories of life have progressively and cumulatively appeared on Earth, forming major ladders of diversity increase. These are: (1) the origination of life to the last common ancestor (LCA) of all extant life, where the LCA was characterized by DNA, RNA, ribosomes, multiple enzymes, membranes, and ATP; (2) the appearance of prokaryotes, i.e., the metabolic diversication of bacteria and Archaea; (3) the appearance of unicellular eukaryotes; (4) the appearance of multicellularity; (5) the invasion of the land; (6) the development of intelligence and technology. (It should perhaps be noted here that while the last megatrajectory certainly seems to have led to an increased level of exploitation of the ecospace on Earth, at the same time it has had a negative impact on biodiversity as a whole. Therefore, this stage lies outside the intended context of the present argument, and will be excluded from consideration here.) The addition of each trajectory may be considered as a jump to another stage of niche use, which corresponds to an expansion into a new niche space as well as an expansion of the total niche space (Fig. 1a). Following this, the occupation of the newly available niche space may be envisaged as either a niche fragmentation or a nichelling process. As the rst species or lineage of species enters a new niche space, it is naturally expected to occupy a small portion of the space. In the rst scenario, this rst invader may come to occupy all the new niche space, and after (near-) complete occupation, a gradual evolutionary splitting up of species occurs, accompanied by niche division. In the second scenario, after the invasion of the rst

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Fig. 2. Schematic diagram showing the step-wise increase in niche space (solid line) and taxa richness (dotted line)

species, the remaining niche space will gradually be lled up by newly emerging species. In between these two scenarios, there exist various degrees of intermediate cases. Whatever forms the occupation of a new niche space by a lineage or different lineages of species may have taken, the whole total diversity (i.e., taxa richness) is supposed to have increased in a jagged manner, in a series of curves forming loose steps (Fig. 2). Thus, the invasion of a niche space can take different forms over different time scales and taxonomic resolutions. In these examples, the number of species in an assemblage (species richness) is represented by the total number of fragments, the relative sizes of which represent the relative abundances of species. Thus, this simple scheme to represent changes in diversity takes into account both the species-richness component and the relative-abundance component. This forms a conceptual background of the niche apportionment models of relative abundances.

Rationale of niche-apportionment
A conceptual pathway whereby niche apportionment models dene species abundances involves two-stage processes (Fig. 3). In the rst stage, the total niche is divided into species niches by some division rule. This is followed by the second, translation stage where species niches are converted to the abundances of different species. In the latter process, the most straightforward and reasonable supposition is that abundance is directly related to niche space, i.e., a larger niche results in a higher abundance. As a broad approximation, this is considered to be true and acceptable, although in some cases interspecic differences in the efciency of converting resources into organismal bodies may distort the linear relationship between niche space and abundance among a set of species. The chance of such a distortion causing a serious problem may be reduced if (i) an assemblage does not include groups with very distant phylogenies and/or body plans, and (ii) biomass rather than the number of individuals is used as an abundance measure. To express species abundances, biomass and number of

Fig. 3. Schematic diagram showing the conversion of total niche space into species abundances

individuals are generally the most convenient measures in many cases. It is of course possible to use measures such as degree of spatial coverage, in so far as they can adequately reect the magnitude of resource utilization (Tokeshi 1993). The crucial aspect, then, is the rst stage: what possibilities are there for dividing the total niche into species niches? As patterns in nature are underpinned by many different processes, it is reasonable to consider a range of possibilities rather than a single scenario in this respect. In earlier literature on species abundance patterns, a distinction was made between sequential and simultaneous breakage models, referring in particular to Motomuras (1932) geometric series (sequential) model and

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MacArthurs (1957) broken stick (simultaneous) model (Pielou 1975). However, Tokeshi (1990, 1993) has demonstrated that there is no need to retain this distinction. The broken stick model is best replaced by the MacArthur fraction model, which produces the same results as the former through a sequential process, thus allowing a direct theoretical linkage with other forms of niche apportionment. A comprehensive formulation of niche apportionment as a sequential (as opposed to a simultaneous) process relates more closely to an evolutionary pattern of events, as these events are considered to have occurred in temporal sequence (which must be true, from a probabilistic viewpoint, as no two events occur at exactly the same time). This allows a uniform treatment of different possibilities of niche apportionment and diversication. In the previous discussion about guild formation within a xed total niche space, two separate cases were represented: niche fragmentation and niche lling (Fig. 1b,c). It should be noted here that despite an apparent differences in the processes, these two schemes can in theory be considered within a single framework of niche apportionment. To see this point, we can ignore the identity of species associated with particular portions of niche space at a particular point in time. It then becomes clear that an invasion of niche space may occur irrespective of the presence/absence of species in the portion of a niche to be invaded. In other words, a new species may carve out its own niche space from either vacant or already occupied niche space in exactly the same manner (i.e., if the shading in Fig. 1c is ignored, the process converges to Fig. 1b). Thus, niche fragmentation and the sequential lling of a niche may be understood to represent two different facets of the same niche apportionment processes. The demarcation between these two modes becomes progressively less distinct as there are more species in an assemblage. On the other hand, niche fragmentation, whereby the total niche space occupied by all the species combined is unity at any time, perhaps allows a simpler and more uniform treatment of the different processes of apportionment than sequential lling. It can thus facilitate a comparison of patterns across systems. Indeed, the original niche apportionment models (Tokeshi 1990) were all framed as niche fragmentation rather than niche lling processes. At this juncture, it is worth mentioning another aspect of niche formation that has not been considered in previous work. This is niche amalgamation, whereby a latercoming species sequesters not only one, but two or more niche spaces of the existing species (Fig. 4). The question remains as to how prevalent such a situation may be in the contemporary and evolutionary development of communities. As this scenario implies the clear superiority of a newly emerging or invading species over existing members of an assemblage, it is probably more akin to evolutionary replacement of one lineage by another, a phenomenon which belongs to a relatively long time-scale (although from palaeobiological perspectives, such a replacement event might be described to have happened within a relatively short evolutionary time). A similar situation may also be considered in the case of the invasion of an island by a new

Fig. 4. Schematic diagram illustrating niche amalgamation. See text for details

species or group of taxa which exterminates (part of) the existing biota. The point in the present context, however, is how the phenomenon of niche amalgamation, if it does occur, may affect the framework of niche apportionment. Although at rst sight such a situation appears to be completely contrary to the idea of niche apportionment, in essence the occurrence of amalgamation can be interpreted as setting the clock backward, i.e., a process of fragmentation starts at the moment the species concerned invades an assemblage. In other words, the new species has in effect changed the rule of niche apportionment, and a new process of niche occupation begins with its appearance on the scene (stage Y in Fig. 4). Thus interpreted, the possibility of niche amalgamation does not affect the basic conceptual framework of niche apportionment. The subtlety of interpretation indicated here represents some areas of the niche-oriented model approach that merit further investigation. Notwithstanding this caveat, the argument above serves as a conceptual basis on which niche apportionment models can be developed with reference to a supposed total niche space and its division processes. As details of different niche apportionment models have already been described elsewhere, this article does not attempt another round of reviewing. While the geometric series model is deterministic in its division rule, other models are all stochastic. Stochastic niche apportionment models can be classied according to the probability that the largest niche segment (i.e., the most abundant species) in an assemblage is chosen for a subsequent division. This probability increases from zero (P 0) in the dominance preemption model, and increases progressively in the order random assortment, random fraction, power fraction, and MacArthur fraction, to the dominance decay model in which the largest segment is always chosen (P 1). The differences in the patterns of these models can easily be

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recognized on the rankabundance diagram, where abundance is generally expressed on a logarithmic scale (Tokeshi 1993).

Hierarchical structure of the niche and niche division

In the previous discussion of changes in diversity over the entire evolutionary history, two distinct processes of diversity increase were suggested: niche expansion and fragmentation. As niche fragmentation is thought to occur consequent upon the creation of an expanded, new niche space, this is essentially a hierarchical structure of niche formation and diversication. While the niche expansion considered above is in largescale, functionally major steps in the history of life, it is possible to think of much smaller- and intermediate-scale niche expansion phenomena. For example, the evolution of tiered, progressively taller sessile guilds and an infaunal guild in the benthic marine community, and the evolution of large-bodied predatory guilds and various parasitic guilds in both marine and terrestrial communities, may each be considered as an expansion into a new niche space, which was subsequently subdivided by sequential fragmentation (Fig. 5). However, the incorporation of such a hierarchical niche structure into the models of niche apportionment has not yet been explored. If each expanded niche space is considered separately, the concept of niche apportionment can be applied to each; in such a case, there may be no apparent framework to link those individual niche apportionment processes and their products. This issue also relates to a broader problem of demarcating an assemblage to be considered in the models of niche apportionment: to what extent should species of different taxonomic and ecological closeness be included? It is easier to restrict an analysis to a

Modes of speciation (sympatric vs allopatric) and community formation

In considering various processes of niche apportionment by a group of taxa, the question may be raised as to whether it is necessary to take into account different modes of speciation such as sympatry and allopatry. The above theory of niche apportionment does not explicitly specify how new species emerge or come to occupy a portion of the total niche space. Broadly speaking, the concept of niche apportionment gives preference to neither allopatric nor sympatric speciation; as long as species do emerge on the scene, the mode of their origination does not matter, and the concept requires no further investigation. Thus, the problem of speciation largely lies outside the scope of this inquiry. On the other hand, it may be conjectured that the answer partly hinges upon how a community the under study has been formed. In the case of small, local communities, the relative abundances of constituent taxa are less likely to reect the direct inuences of species origination processes. Rather, patterns of (re)invasion of a habitat through time by a set of already existing species, with possible subsequent interactions among them (i.e., community formation through the establishment of secondary contacts and reassembly), largely determine the relative abundance pattern. Here, the mode of speciation has little direct relevance, and therefore the theory of niche apportionment does not necessarily require such information. In contrast, larger-scale (e.g., regional) communities may reect more speciation-associated trends in their species abundance patterns, and therefore a consideration of the mode of speciation becomes more relevant. However, this does not mean that any particular mode of species origination is suggested as the most likely scenario underlying a species abundance pattern. Depending on how spatial scale is dened for the community in question, either allopatric/peripatric or sympatric speciation is feasible as a process generating species that come to partition a niche space within the framework of niche apportionment. In this respect, the processes of niche division can be interpreted as representing both allopatric and sympatric speciation, setting aside the question of the exact mechanisms and circumstances in which the latter, in particular, may occur (which is not dealt with by the theory under consideration here). By denition, sympatric speciation refers to a species splitting into two within a habitat, which generally means small spatial scales; therefore, sympatric speciation, if it occurs at all, can be linked to niche apportionment processes, and species abundance patterns in general, only on relatively small spatial scales. In contrast, allopatric and peripatric speciation may be more relevant to niche apportionment on medium to large scales.

Fig. 5. Hierarchical formation of niche expansion and fragmentation

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single guild or a group of closely associated species. On the other hand, there is no absolute theoretical necessity to erect an arbitrary boundary to membership of an assemblage. It can even be argued that since all species share a composite energy resource on Earth, they are all considered as rightful participants in a game of niche apportionment. Indeed, there could be no concrete objection to models such as random fractions being applied to an assemblage encompassing species of different guilds as long as an appropriate measure of abundance is adopted. How different hierarchical levels of niche structure can be linked in the application of niche apportionment theory remains to be explored.

Abundance and body size

It is probably not an exaggeration to state that abundance is the most important parameter in ecology, and the whole discipline of population ecology and a large part of community ecology center around this single parameter. Consequently, there is a vast range of approaches that can be adopted to study abundances. Analysis of species (relative) abundance patterns, as discussed above, is one important line of investigation within community ecology. Another, relatively new area of research called macroecology (Brown 1995) has adopted a related, but slightly different, approach to the variability of abundances in animal assemblages, and attempts to explain abundance in relation to body size and its correlates. Body size is considered to be one of the most important attributes of an organism, as it dictates, or strongly inuences, the organisms energetic requirements, its potential resource exploitation, and its susceptibility to predation. In many animal assemblages, the relationship between population density and body size has been described by a power function with the exponent in the range 0 to 1. Generally, analyses of the densitybody size relationship in terrestrial and aquatic habitats have yielded linear relations on logarithmically transformed scales (Damuth 1981; Peters 1983). A large body of data, particularly from terrestrial assemblages, has demonstrated that population density (D) scales allometrically with body mass (W ) as D W, where the exponent is around 0.75 when the ordinary least square (OLS) regression is used (Damuth 1981; Peters 1983). Since individual metabolic rates (R) scale with body mass according to R W 0.75 (Kleiber 1961), 0.75 means DR a constant, which in turn implies that population density is limited by its energy requirements. Energetic limitation suggests that an approximately equal amount of energy is available to each species in an assemblage, which has been referred to as the energy equivalence rule (Nee et al. 1991). In contrast, using the reduced major axis (RMA) regression (LaBarbera 1989), Grifths (1998) showed that most published data reveal a slope close to 1.0, and thus, within communities, small organisms may use more energy than large ones. These contrasting results are derived from data collected through different sampling procedures and subjected to different regression methods

(Marquet et al. 1990). It has also been argued that data compiled from the literature result in constructed density versus body-size relations of assemblages that may be greatly affected by sampling bias against small and rare species which are usually not well represented in ecological studies (Lawton 1989). An underestimation of the densities of rarer species is likely to result in a shallower slope and a less signicant, more scattered relationship. Further, analyses in this direction have mainly involved terrestrial assemblages, with a bias towards taxonomically related species, and few studies have considered aspects of scaling across many taxonomic groups in an ecosystem (Marquet et al. 1990). In order to assess the generality of the densitybody-size relationship and the energy equivalence rule in stream systems, Schmid et al. (2000) used extensive data from two geographically separate communities of stream invertebrates. These data encompassed species in wide taxonomic and body-size ranges, and allowed the authors to achieve a taxonomic resolution far greater than in previous studies in this discipline. Further, population densities of all the species in an assemblage were estimated with reference to the same habitat area, thus avoiding the problem of using densities obtained from unrelated areas, as was the case with most previous studies involving data assembled from the literature. The two mountain streams in question, Oberer Seebach in Austria and Afon Mynach in Great Britain, were similar in mean annual water discharge and fractal dimension of habitat, but were different in grain-size composition. Quantitative eld sampling was carried out within rife/pool sections of these streams, which generated data on population density and body size for all species from each of the two streams. A total of 448 and 260 invertebrate species occurred in the streambed sediments of the Oberer Seebach and Afon Mynach, respectively. In both communities, abundance declined with increasing body mass in a broad band (Fig. 6). Body weight accounted for a considerable amount of the variation observed in population density in both communities. As some doubt has been cast on the possible technical limitations of OLS regressions in previous studies, the OLS-bisector regression (OLSBIS) was also employed to evaluate the relationship between population density and body mass. The OLSBIS regression gave a slope of 1.03 for both streams. This value was not signicantly different from 1, but was different from 0.8. In contrast, the slopes of the OLS regression were signicantly different from 1, but not from 0.75, and did not differ signicantly between streams. Even where a densitybody-size relationship characterises a community, different trophic guilds may have different patterns of scaling. However, when groups of detritivores and predators (including omnivores) were separately subjected to the same test, the scaling of population density with body size was not signicantly different between these feeding guilds in the two streams. On the other hand, the OLSBIS (but not the OLS) regression demonstrated that detritivore density declined more rapidly with increasing body mass than did predator density.

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Fig. 6. Densitybody-size relationships of stream zoobenthos in Seebach, Austria, and Mynach, UK. (Data adapted from Schmid et al. 2000)

If resource use is dependent upon species identity and their specic energetic requirements, it may be postulated that the densityweight relationships should differ systematically between the assemblages of species occurring in both streams and of those occurring in only one of the streams. There were 17.4% of all invertebrate species found in both streams, and this showed a similar population density to body-mass scaling (Fig. 7a). Nevertheless, owing to differences in population densities, regression intercepts differed signicantly between streams. The slopes and intercepts of the densitybody-mass relationship were similar between the species assemblages which were restricted to one of the streams (Fig. 7b). Moreover, the regression intercepts differed signicantly between the assemblages of species common to the two streams and those occurring only in the Seebach. No differences were found between the shared assemblages and those restricted to the Mynach. The OLS slopes of the species assemblages restricted to one of the two streams differed signicantly from 0.75 and 1, while the regression exponents of common species departed from 1 but not from 0.75 in both streams (Fig. 7a). Even when

the regression slopes did not differ signicantly from the predicted value of energy equivalence, the variation in population density at any given body size was such that species in an assemblage are unlikely to obtain an equivalent amount of resources. In addition, all OLSBIS slopes for common and restricted species departed signicantly from 0.8 but not from 1. If stream communities are governed by a general energetic rule, it may be expected that the same pattern exists both across taxonomic groups and within each taxonomic group. Therefore, an analysis was conducted to see if within-taxon relationships were similar to the observed across-taxa relationships. The OLS and OLSBIS slopes of the eight most species-rich taxonomic groups (Testacea, Turbellaria, Insecta, Crustacea, Oligochaeta, Rotifera, Nematoda, Hydracarina) assumed both positive and negative values, falling randomly around means of 0.66 and 1.28, respectively, in the Seebach and means of 0.63 and 1.10, respectively, in the Mynach. Thus, as the slope of the density-size regression varied widely among taxonomic groups, the model of energy equivalence cannot be claimed to constitute a general rule of benthic community structure. On the other hand, although energy equivalence may not be ubiquitous, the fact that some rocky intertidal communities (Marquet et al. 1990) and the two stream communities had similar values for the allometric exponent seems to add weight to the generality of the densitysize relationship itself, despite apparent ecological differences among communities. Energy limitation is unlikely among invertebrate species in the two strteam assemblages, as many smaller species are no more abundant than larger species, and there is no indication of food/space limitation within these ecosystems (Schmid et al. 2000). For these stream benthic animals, food and space are generally nonlimiting; they feed on a wide range of particle and prey sizes (supplied and replenished by water currents), and occur at the sediment surface as well as in the hyporheic interstitial, using the habitat in a three-dimensional way (Schmid and Schmid-Araya 1997). Although the faunal composition was different between the two geographically separated streams, the scaling of population density with body size was not different. This has led to a suggestion that the population density scaling in the two streams may be controlled by similarities in their environmental characteristics, in particular the physical complexity (fractal D) of the habitat (Morse et al. 1985; Tokeshi 1999; Schmid et al. 2000). Thus, in sum, these comprehensive data sets encompassing a large number of invertebrate taxa with a wide range of body sizes demonstrated that an inverse proportionality between density and body size is a consistent feature in these geographically separated stream communities. The scaling of the densitybody-size relationship across taxa was not statistically different between the two systems, indicating a convergent pattern of communities. These communities, that have only 17.4% of species in common, appear to have acquired a similar densitysize structure, probably due to similarities in discharge regimes and fractal habitat structure (Schmid et al. 2002; P. Schmid and M. Tokeshi, unpub-

198 Fig. 7. Densitybody-size relationships in Mynach and Seebach for a species common to both streams, and b species found only in either Mynach or Seebach. (Data adapted from Schmid et al. 2000)

lished ms.). However, these communities are not governed universally by a single rule of energetic constraints, as shown by the variation in the regression slope among different taxonomic groups.

Linking the densitybody-size relationship to niche apportionment

While studies on densitybody-size relationships has progressed independently of those on species abundance patterns, the above analysis of stream community data points to an important link between the two lines of research. If abundance is somehow constrained by body-size characteristics, it may then be surmised that species abundance pattern is also under the inuence of body size. Although causal relationships between density and body size cannot

denitely be established from a regression analysis alone, it is reasonable to assume that if there is any causal link, it is density that is inuenced by body size, and not the other way round, as body size is more the result of evolution, i.e., it is strongly constrained by the ecophysiological characteristics and evolutionary histories of the organisms concerned. Thus, the question is raised of whether and how species abundance patterns are also constrained by (the frequency distribution of) body sizes. In the following discussion, the importance of distinguishing density and biomass (and other measures), as mentioned earlier for the expression of abundance, should be noted, as the conclusions are different depending on what is meant by abundance. If a signicantly negative densitybody-size relationship characterizes an assemblage, the species abundance pattern, as expressed by numbers of individuals, is considered to reect the distribution of body sizes in the assemblage.

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Overall, common species tend to be small-bodied, while rare species are large-bodied. This implies that an analysis of species abundance patterns can in part be substituted by an analysis of the ranked distribution of body sizes, although this will depend on the strength of the densitysize relationship. A substantial scatter of points around a regression line (e.g., Fig. 6) indicates that body size can account for only some part of the variation in species density, and hence abundance expressed as number of individuals. Further, if a negative densitybody-size relationship is characterized by 0.75, there also emerges the possibility of the abundance pattern being affected by energy availability. However, this possibility is unlikely to be a general case, as the energy equivalence rule is not supported by detailed community data such as those of Schmid et al. (2000). Thus, while it is expected that body size can partially explain a species abundance pattern based on numbers, the extent and the exact nature of such an explanation is still unknown. In contrast to numerical abundance data, a somewhat unexpected situation occurs with patterns of abundance based on biomass. If, as many data indicate, the general densitysize relationship has a slope close to 1, it will then follow that biomass abundance (B) is roughly constant among species, i.e., B DW cWW cW1 c This implies that in principle the same amount of biomass resource is available for each species in an assemblage. In other words, body size (and other size-related traits of organisms) does not a priori constrain abundance values; abundance (i.e., biomass) is independent of body size. This seemingly important conclusion is here termed the biomass equivalence rule, recognizing its similarity to its energetic forebear. This does not mean that all species always secure the same amount of biomass; it simply stipulates that biomass is not constrained by body size, and species of different sizes have the potential to achieve similar levels of population biomass. Incidentally, this provides powerful support to the logic of niche apportionment models, the random fraction (RF) model in particular. The random fraction model assumes that the processes of niche division are all random, i.e., the operational equivalence of all the species in an assemblage. It is notable that the RF model has frequently achieved the best t to abundance data, giving credence to its descriptive power. The biomass equivalence rule can constitute a fundamental principle on which the mechanics of niche apportionment is based. Signicantly, biomass as a measure of species abundance is free from the effects of systematic variation in body size. Thus, it is more convenient to use biomass for analyses of species abundance patterns, as (i) unknown inuences of body size are mainly eliminated, and (ii) the supposed null condition of niche apportionment models is given a logical basis. Thus, while numbers of individuals are frequently used as the most fundamental measure of abundance, the use of biomass should be emphasised as a conceptually sound and logically appropriate measure of abundance when applying niche apportionment models.

Toward a new generation of research in species abundance patterns

Over the past decade, research into species abundance patterns has gained renewed emphasis with the development of niche apportionment models, an exploration of abundance body-size relationships, and more recently, Hubbells (2001) neutral theory of biodiversity. However, the integration of these different lines of enquiry is yet to be achieved. The consideration of body size in the context of analysing species abundance patterns has not been fully explored, and further developments are expected in future studies. As mentioned above, one signicant perspective emanating from recent studies of densitybody-size relationships, including the one on stream benthic assemblages, is the biomass equivalence rule, referring to the independence of the biomass measure of abundance from the (possible) inuences of body size, and the fundamentally equitable nature of biomass availability to different species. Therefore, species abundance patterns based on biomass are justiably appropriate for analyses with niche apportionment models. Further, in a slightly different vein, another recent analysis of fossil community data suggests a bodysize-dependent pattern of relative abundance where the apportionment of energy among taxa is described well by the random fraction model, and that larger-sized taxa tend to sequester a greater amount of energy (M. Tokeshi, unpublished data). Forcefully argued as a general explanation of biodiversity, Hubbells theory has two principal assumptions: neutrality (i.e., the equivalence of all individuals belonging to all species in terms of probabilities of birth, death, immigration, and emigration) and a zero-sum game, whereby an individual gained by one species must be preceded by an individual of another species being lost from the assemblage under consideration. These assumptions are diametrically opposed to situations where a densitybody-size analysis is applied: individuals differ in size, and consequently in lifehistory traits such as rates of birth, death, immigration, and emigration. Under such circumstances, a zero-sum game is unlikely to apply. Therefore, Hubbells theory is, in principle, applicable only to a set (or guild) of taxa with similar body sizes. While it is perhaps premature to make a denite judgment on the claim that the model apparently (supercially?) ts many observed patterns of species abundance, the fundamental premises of the theory appear so restrictive that any correspondence with real data should be treated with the utmost caution. Unfortunately, there is no way of telling what is a true/spurious pattern in the framework of Hubbells model. Given the fact that the vast majority of communities consist of species with different body sizes, it is questionable whether a theory based on equal body sizes is widely acceptable as a fundamental theory of ecological communities in general. In this respect, the approach of niche apportionment models with the biomass equivalence rule is conceptually more sound, and is likely to lead to a sound understanding of community patterns. A new generation of research incorporating varying cases of biomass

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equivalence may lead to new insights into the evolutionary and contemporary processes of community formation.

References
Avise JC, Ball RM (1990) Principles of genealogical concordance in species concepts and biological taxonomy. Oxf Surv Evolut Biol 7:4567 Bambach RK (1977) Species richness in marine benthic environments through the Phanerozoic. Paleobiology 3:152167 Bambach RK (1983) Ecospace utilization and guilds in marine communities through the Phanerozoic. In: Tavesz MJS, McCall PL (eds) Biotic interactions in recent and fossil benthic communities. Plenum, New York, p 719746 Begon M, Harper JL, Townsend CR (1996) Ecology 3rd edn. Blackwell Science, Oxford Bennett KD (1990) Milankovitch cycles and their effects on species in ecological and evolutionary time. Paleobiology 16:1121 Brown JH (1995) Macroecology. University of Chicago Press, Chicago Cherrett JM (1989) Key concepts: the results of a survey of our members opinions. In: Cherrett JM (ed) Ecological concepts: the contribution of ecology to an understanding of the natural world. Blackwell Scientic, Oxford, p 116 Coope GR (1994) The response of insect faunas to glacialinterglacial climatic uctuations. Phil Trans R Soc Lond B 344:1926 Damuth J (1981) Population density and body size in mammals. Nature 290:699700 Dobzhansky T (1951) Genetics and the origin of species. 3rd edn. Columbia University Press, New York Fryer G, Iles TD (1972) The Cichlid shes of the Great Lakes of Africa. Oliver and Boyd, Edinburgh Ghiselin MT (1984) Denition, character, and other equivocal terms. Syst Zool 33:104110 Grifths D (1998) Sampling effort, regression method, and the shape and slope of sizeabundance relations. J Anim Ecol 67:795804 Hubbell SP (2001) The unied neutral theory of biodiversity and biogeography. Princeton University Press, Princeton Kleiber M (1961) The re of life: an introduction to animal energetics. Wiley, New York Knoll AH, Bambach RK (2000) Directionality in the history of life: diffusion from the left wall or repeated scaling of the right? In: Erwin DH, Wing SL (eds) Deep time: paleobiologys perspective. p 114. Supplement to Paleobiology vol 26 LaBarbera M (1989) Analysing body size as a factor in ecology and evolution. Annu Rev Ecol Syst 20:97117 Lawton JH (1989) What is the relationship between population density and body size in animals? Oikos 55:429434 MacArthur RH (1957) On the relative abundance of bird species. Proc Natl Acad Sci USA 43:293295 Mallet J (1995) A species denition for the modern synthesis. Trends Ecol Evolut 10:294299 Marquet PA, Navarette SA, Castilla JC (1990) Scaling population density to body size in rocky intertidal communities. Science 250:11251127

Mayr E (1942) Systematics and the origin of species. Columbia University Press, New York Mayr E (1963) Animal species and evolution. Harvard University Press, Cambridge Mayr E (1970) Populations, species, and evolution. Belknap, Cambridge Morse DR, Lawton JH, Dodson MM, Williamson MH (1985) Fractal dimension of vegetation and the distribution of arthropod body lengths. Nature 314:731733 Motomura I (1932) A statistical treatment of associations (in Japanese). Jpn J Zool 44:379383 Nee S, Read AF, Greenwood JJD, Harvey PH (1991) The relationship between abundance and body size in British birds. Nature 351: 312313 Peters RH (1983) The ecological implications of body size. Cambridge University Press, Cambridge Pielou EC (1975) Ecological diversity. Wiley-Interscience, New York Schmid PE, Schmid-Araya JM (1997) Predation on meiobenthic assemblages: resource use of a tanypod guild (Chironomidae, Diptera) in a gravel stream. Freshwater Biol 38:6791 Schmid PE, Tokeshi M, Schmid-Araya JM (2000) Relationship between population density and body size in stream communities. Science 289(5484):11571160 Schmid PE, Tokeshi M, Schmid-Araya JM (2002) Scaling in stream communities. Proc R Soc Lond B, in press Sepkoski JJ Jr (1979) A kinetic model of Phanerozoic taxonomic diversity. II. Early Phanerozoic families and multiple equilibria. Paleobiology 5:222251 Sepkoski JJ Jr (1988) Alpha, beta, or gamma: where does all the diversity go? Paleobiology 14:221234 Simpson GG (1944) Tempo and mode in evolution. Columbia University Press, New York Simpson GG (1953) The Major features of evolution. Columbia University Press, New York Smith AB (1994) Systematics and the fossil record. Blackwell Scientic, Oxford Strong DR Jr (1982) Harmonious coexistence of hispine beetles on Heliconia in experimental and natural communities. Ecology 63:10391049 Templeton AR (1989) The meaning of species and speciation: a genetic perspective. In: Otte D, Endler JA, (eds) Speciation and its consequences. Snauer, Sunderland, p 327 Tokeshi M (1990) Niche apportionment or random assortment: species abundance patterns revisited. J Anim Ecol 59:11291146 Tokeshi M (1993) Species abundance patterns and community structure. Adv Ecol Res 24:111186 Tokeshi M (1999) Species coexistence: ecological and evolutionary perspectives. Blackwell Science, Oxford Wiley ED (1981) Phylogenetics: the theory and practice of phylogenetic systematics. Wiley-Interscience, New York Wilson EO (ed) (1988) Biodiversity. National Academy, Washington, DC Wilson EO (1992) The diversity of life. Belknap/Harvard University Press, Cambridge