Ecologists continue to wrestle with a central question in biodiversity studies — the prediction of species' distributions in various environments. A merger of different theories is the long-term prospect.
The most useful scientific models are those with the fewest parameters and the least-disputable assumptions. By testing real data against these ‘null models’, researchers are insured against over-interpreting their data. If the null model can successfully characterize the data, there is often no compelling reason to go beyond it to seek explanations.
In a new look at how species coexist in coral-reef communities, Dornelas et al. (page 80 of this issue)1 have found a significant departure from the neutral theory of biodiversity2 — community ecology's most recent and elegant null model. They also provide empirical support for an often overlooked component of niche theory, one of ecology's oldest and most influential explanations for the coexistence of species.
Neutral theory is one of the most exciting conceptual advances in ecology in decades. It provides a simple tool to assess the degree to which variation in the composition of natural communities can be explained solely by random demographic processes. There are only two major assumptions. The first is that every individual in a community has the same probability of birth, death, migration and speciation. Differences among species are assumed to be irrelevant when it comes to predicting community composition. The second is that the community is characterized by a zero-sum game — when one individual emigrates or dies, the space it leaves is immediately occupied by another individual. Everyone, including the theory's architect Steve Hubbell, knows that species differ in many ways. After all, not all coral species participate in the annual ‘coral-reef orgy’ mass spawning event; some species brood internally every month. The real question that neutral theory asks is whether or not we need to take these differences into account to predict species-distribution patterns.
Recent tests of the neutral theory have centred on the shape of species-abundance curves3. As prima facie evidence against non-neutral systems, Hubbell offers the successful fitting of zero-sum multinomial functions, which meet the requirements of neutral theory, to curves from data collected in Barro Colorado Island, Panama2. Since then, others have made similar comparisons using these and additional data sets, and have found both agreement with and departures from the predicted curves. More recent work has shown that most of these comparisons are weak, primarily because more than one ecological mechanism can give rise to very similar theoretical distributions, and the ‘best-fit’ distribution depends on what measure of ‘best-fit’ we use. If any model can fit, the shape that the species-abundance curves ultimately take may not be so important3.
In a paper that will turn our attention in a completely new direction, Dornelas et al.1 describe an approach that will join an emerging next generation of tests of the neutral theory. Out go the old equivocal comparisons of the fit of different models to species-abundance distributions, and in come the new — tests that actually relate theoretical assumptions to the biological reality inherent in ecological communities4,5.
Dornelas et al. set out to see whether local communities really do show the vast differences in species composition predicted by the demographic randomness inherent in neutral theory. Instead, they found something unexpected and initially puzzling. Coral communities along a traverse spanning part of the Indian and Pacific oceans are dramatically less similar to each other and even more variable than predicted by neutral theory. But the results are in the opposite direction to those predicted by many opponents of neutral theory, who generally argue for ecological building ‘rules’ that culminate in similar communities repeatedly being constructed in the same habitat.
The main alternative to neutral theory is niche theory, which explains relative species abundance in a community in a far more complex fashion6. In this theory, species have evolved adaptations to different environmental conditions and sort themselves out along ‘niche axes’. These environmental conditions are both abiotic (water temperature and rainfall, for example) and biotic (competition, food supply, predation, symbiosis and so on). All else being equal, species adaptations to the environment should lead to more closely similar communities occurring over time and space than those generated by neutral theory. So, at first glance, the limited similarity in coral community composition observed by Dornelas et al. cannot easily be explained by traditional niche theory.
What, then, can explain this marked spatial dissimilarity in community composition? The authors suggest that environmental variability has a strong influence (Fig. 1), even though they intentionally sampled consistently similar reef habitats. Their hunch is that local communities still experience considerable fluctuations in environmental conditions. Many disturbances on coral reefs, such as cyclones, outbreaks of crown-of-thorns starfish and coral bleaching, can be quite localized, so even adjacent parts of the same reef can have very different environmental histories. Thus, the low level of community similarity might relate more to the relationship between sequential changes in communities and the time since disturbance than to random demographic processes. Although this does not show that niches have no role in species coexistence, it does place fluctuation-mediated coexistence in a stronger light7.
Perhaps the most instructive part of the new study is the amazingly high similarity and low variance among computer-simulated neutral-theory communities. Dornelas et al. tried fiddling with the parameters of neutral theory, such as migration rate and species turnover, to decrease the community similarity and increase its variance, but the simulated neutral communities remained far less variable than their real counterparts. We will have to ask some hard questions about how to interpret this result. What are the implications of a neutral model that presupposes no role for inherent differences among species, but leads to greater order and predictability in community composition than nature can provide? Will Dornelas and colleagues' conclusions hold up when the observed community similarity is much higher or less variable over different spatial8 or temporal9,10 scales? Previous authors have show that there is less variation among communities than expected under neutral theory8,9,10. Dornelas et al. have now demonstrated that there is too much. Neutral theory is caught in the middle. This, perhaps, shows the strength of a null model. By making clear predictions, we can explore deviations in both directions from a point of neutrality.
Dornelas and colleagues' study1 will invigorate debate over the importance of biological details in determining the coexistence of species within communities. Their fresh and falsifiable approach leads us farther down the path to merging neutral theory and niche theory — a process that bears striking similarities to its evolutionary counterpart of successfully integrating theories concerning neutral genes and natural selection.
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