Species abundance distributions: pattern or process?

Hubbell's (2001) ‘unified neutral theory of biodiversity and biogeography’ raises many intriguing, and sometimes perplexing, questions (Whitfield 2002). It is remarkable that a model that assumes that the demographic properties of individuals are independent of the identity of the species to which those individuals belong can generate distributions of species abundance that replicate, to a considerable degree, those observed in real communities. The hypothesis that species are ecologically identical, at least in terms of their contribution to community and regional diversity, has been considered elsewhere (see, for example, Brown 2001; Condit et al. 2002; Clark Volkov et al. 2003) relate to the mutation model of speciation which predicts that species abundances will be distributed according to Fisher's (Fisher et al. 1943) log-series. For example, in a recent defence of the neutral model, Volkov et al. state that: ‘Under neutrality at large spatial and temporal scales, Fisher's log-series distribution is the expected steady-state distribution of relative species abundance at the speciation–extinction equilibrium in the metacommunity when the per capita birth and death rates are density independent and the same for all species, and speciation is introduced’. In this paper I therefore revisit Fisher's model and consider its potential as a descriptor of large-scale patterns of species abundance. I also highlight the need for better methods of distinguishing between rival species abundance distributions and the theories that underpin them. Hubbell (2001, p. 5) defines a ‘local’ or ‘ecological’ community as a ‘group of trophically similar, sympatric species that actually or potentially compete in a local area for the same or similar resources’. In doing so he offers a more restrictive definition of a community than is usual in investigations of biological diversity; most ecologists measure the diversity of a taxonomically (and geographically) delimited set of organisms, such as forest beetles or pelagic fish, rather than a trophically delimited one (Magurran 2004). However, even though this neutral theory is conceived in the context of a grouping that might otherwise be termed an ‘ecological guild’ or ‘ensemble’ (Fauth et al. 1996), its ability to fit much broader assemblages, such as Amazonian fish communities, which typically contain species occupying a variety of niches (A. E. Magurran, personal observation) suggests robustness against variation in species role. Local communities are embedded in a ‘metacommunity’, which is defined as a regional collection of communities. The metacommunity is the arena in which speciation occurs and the source from which local communities are colonized. The immigration rate, m, is the proportion of individuals in a local community that are replaced by individuals from the metacommunity. When m = 1 the local community is not isolated from the metacommunity and will share the same species abundance distribution (the log-series). As m decreases, the local community becomes more isolated and supports fewer rare species. This has the effect of translating a log-series type distribution in the metacommunity into a log-normal type distribution of abundance in the local community. One of the successes of Hubbell's neutral theory has been to show how shifts in the value of m can generate the sort of negatively skewed log-normal distribution that has so intrigued ecologists (Nee et al. 1991; Harte et al. 1999; Gaston Magurran Magurran 2004). However, the log-series distribution may also arise as a sampling distribution (Taylor 1978). At small sample sizes the log-series and (truncated) log-normal distributions are often indistinguishable (see Figs 2·13 and 2·14 in Magurran 2004). It is only when sample size increases and the ‘veil line’ (Preston 1948) is pulled back to reveal the mode of the distribution that the full log-normal becomes apparent and the log-series ceases to be a good fit. This transition from log-series to log-normal is clearly seen in Williams's (1964) 8-year survey of Rothamsted moths (see also Fig. 2·4 in Hubbell 2001). In a related observation Magurran Magurran 2004.) Small populations are known to be vulnerable to extinction. Although a threshold of 50 individuals (Franklin 1980) is often cited, recent work shows that populations may need to be large to ensure persistence (Reed Hudec et al. 1995; Gaston Coyne Hubbell 2003). This produces a relative abundance distribution that falls between the high-diversity, log-normal like, random fission and the low-diversity, log-series like, point mutation. These models differ in their assumptions about the size of the founding population. In reality huge variance in the size of emergent species is likely. One thorny issue in ecology is how best to discriminate between completing solutions to a problem. For example, there are at least five different explanations for the excess of rare species (log-left or negative skew) often found in log-normal distributions (Sugihara 1980; Tokeshi 1996; Harte et al. 1999; Hubbell 2001; Magurran Colwell Magurran 2004) can change the outcome of goodness-of-fit tests. The usual advice is to replicate sampling (Pielou 1975; Wilson 1988; Tokeshi 1993) since one snapshot of community structure may give a biased image of the outcome of many probabilistic events. But replicated inventories of large communities, whose recorded species abundance distributions are often in any case an amalgam of samples collected over space and time, is rarely feasible. There is a pressing need for better methods of assessing fit. As Volkov et al. (2003, p. 1037) remark, ‘fitting exercises in and of themselves do not constitute an adequate test of underlying theory’. Failure to reject a null hypothesis does not necessarily vindicate the assumptions upon which it is based; the putative mechanisms involved must be demonstrated to be correct beyond all reasonable doubt. It is disappointing that despite a long history of attempts to explain the relative abundances of species in terms of niche apportionment (see Magurran 2004 for a review) there have been few direct experimental tests of the processes involved. Correlations between expected species abundance distributions and empirical ones only tell part of the story. A recent study, which presented experimental evidence for apparent competition in a tropical forest food web (Morris et al. 2004), exemplifies the power of direct tests of ecological theory. Hubbell's neutral model has been invaluable in forcing ecologists to look again at how communities are assembled. The challenge now is to devise better tests of the assumptions and predictions of null models in order to answer fundamental questions they raise about the relative abundance of species (May 1986; Hubbell 2003). Testing the relationship between dispersal limitation, resource use and species abundances in some tractable local communities might not be a bad place to start. I am grateful to the referees for their helpful comments.