Should we still be testing neutral theory? If so, how?

Siepielski, A.M. , Hung, K-L., Bein, E.E.B, McPeek, M.A. 2010. Experimental evidence for neutral community dynamics governing an insect assemblage. Ecology. 91. 847-857

For many ecologists, neutral theory was a (good/bad, you choose) idea that dominated ecology for the last decade but failed to provide the burden of empirical proof necessary for its acceptance. Even its creator Stephen Hubbell  recently suggested that the controversial hypothesis is no longer a plausible description of community structure, going as far to say that it is “good starting point”, a “valuable null model”, and a “useful baseline” (in Etienne et al 2011). 

But ideas, when they’re shared, are no longer the sole property of their creators. Other researchers continue to study neutral theory, and despite the apparent consensus that neutral theory is not an important explanation of community structure and dynamics, papers testing neutral theory continue to be published. This leads to an important question: do we still want to test for neutral dynamics? And if we do, how should we approach it, given what we have learned from the past decade of strawman arguments and using pattern-based evidence for processes (e.g. looking at species-area relationships and species abundance distributions)? What empirical evidence would provide strong support for the predictions of neutral theory?

Damselfly larvae
(http://www.uta.edu/biology/robinson/odonate_research.htm)

In “Experimental evidence for neutral community dynamics governing an insect assemblage”, Siepielski et al. (2010) attempt to provide a more rigorous test of neutral theory using two Enallagma (damselfly) larvae. Siepielski et al. focus on changes in demographic rates (growth, mortality) in response to changes in species relative and total abundances. In particular, they predicted that if niche differences drive coexistence, increasing a species’ relative abundance should drive lower growth rates and higher mortality, since that species is above its equilibrium; lowered relative abundances should result in higher growth rates and lowered mortality since the species is below its equilibrium density. As a result, species should return to their equilibrial abundances. Raising the total abundances but leaving the relative abundances untouched should have similar demographic responses across species and have no effect on the relative abundances. In contrast, neutral theory predicts that if all species are equal, their demographic rates depend on the density of the entire group (total abundance) and not on each individual species’ relative abundance. Therefore the response of demographic rates to changes in species relative abundances, while the total abundance is held constant, should provide support to either neutral or niche theory.

For two Enallagma sp. larvae Siepielski et al. used cages in the littoral zone of lakes, with cages receiving different treatments of relative abundance and/or total abundance manipulation. The result of these manipulations were that replicates with increased total abundances and constant relative abundances had lowered per-capita growth rates, while replicates with manipulated relative abundances and constant total abundances showed no change in demographic rates. Both species had similar mortality rates across the experimental treatments, although their growth rates differed slightly. From these results, Siepielski et al. concluded that these species are ecologically equivalent.

One of the reasons work (such as this) from Mark McPeek’s lab is interesting is because he is an outlier: someone whose work is deeply rooted in a natural system, and yet who also argues that ecological equivalency seems plausible, and attempts to support that argument. Regardless of whether the Enallagma species are in fact ecologically equivalent, this paper provides an example of how coexistence theory can be more rigorously tested than simply observing species co-ocurrences and concluding species coexistence. Further, it provides some interesting discussion about whether ecological equivalency is possible within functional groups, with niche differences occurring between functional groups (see Leibold and McPeek 2006, and from MacNaughton and Wolf 1970 for similar suggestions). Future work might focus on questions such as how to capture the effects of small niche differences, which, if balanced against very similar fitnesses could explain stable coexistence. In addition, it might be valuable to look at how resources fluctuate and how much overlap there is in resource requirements among species, when looking at how growth and mortality change with species densities.

With Adam Siepielski, Mark McPeek also published the paper “On the evidence for species coexistence: a critique of the coexistence program” about the apparently lowered standards for tests of niche-based species coexistence compared to those of neutral theory. What is certainly true is that experimental tests of coexistence theory are often less rigorous than necessary to support any coexistence theory, and should strive to take a more rigorous approach. If nothing else, this will allow criticism of particular theories to focus on the ideas themselves, rather than on how those ideas were tested.