'Synthesizing ecology': revisiting an Oikos classic

Oikos’ motto is ‘Synthesizing ecology’. This has always struck me as an intriguing slogan, because it can be read in multiple ways. It might be thought to highlight our desire for generality. As our instructions to authors note, Oikos strives to publish papers with broad implications, which will therefore be of interest to many ecologists. On this reading, ‘synthesizing’ is synonymous with ‘generalizing’. For instance, Persson et al. (Oikos 119:741-51 [2010]) pull together (‘synthesize’) data on stoichiometric homeostasis for many different species, thereby allowing them to reach the general conclusion that all heterotrophs exhibit stoichiometric homeostasis.

But a second, related but distinct reading is possible. ‘Synthesizing’ can refer to combining different parts or ingredients into a new, unified whole, as when chemists synthesize a new compound. Indeed, this is the dictionary definition of ‘synthesizing’. Synthesizing in this sense is a teleological (goal-directed) activity—one must ‘decide’ (consciously or otherwise) what ‘whole’ one wants to make, what ingredients to use, and how to combine them. These decisions are constrained. Choosing what one wants to make constrains one’s choice of ingredients and ways of combining them. And choosing ingredients and ways of combining them constrains what one can make.

Ecological generalizations are ‘synthetic’ in this second sense. Ecologists choose what questions to ask—we choose what ‘wholes’ we want to make. After all, ecological systems—organisms, populations, communities, ecosystems—have an infinity of properties one might measure, and so there is an infinity of questions we might ask. Only once we’ve chosen the question does nature answer it. And the way in which we frame our questions shapes what ‘ingredients’ we can use (e.g., what sorts of data we need), and what sort of answers we get.

This second sense of ‘synthesis’ grounds my own response to John Lawton’s ‘Are there general laws in ecology?’ (Oikos 84:177-92 [1999]). It’s a classic Oikos article—cited 399 times to date, and the annual citation rate has hardly declined over time. In it, John provocatively suggests that the answer to the question posed by his title is ‘scale dependent’. There are (contingent) generalizations at the ‘small’ scale of population ecology. For instance, there are millions of species, but only a few distinct kinds of population dynamics, and only a few key factors (e.g., intrinsic rate of increase, strength of density dependence) that govern what kinds of dynamics occur. There are also generalizations at the ‘large’ scale of macroecology, where the ‘noise’ of species- and system-specific details ‘averages out’. General macroecological patterns include power law species-area curves and lognormal species-abundance distributions. But at the ‘intermediate’ scale of community ecology, the contingency is overwhelming and there are no generalities—every community is a special case. The contingency is overwhelming because (unlike population ecology) there are too many relevant causal factors, and because (unlike macroecology) communities are too small-scale for these contingent details to average out. Provocatively, John (a community ecologist himself) says that traditional community ecology is a questionable use of ecologists’ time and effort, and ecologists ought to ‘move on’!

As a community ecologist myself, I can certainly see where John’s coming from; his argument absolutely deserves the widespread attention it has received. Part of my own answer to his argument is to sidestep it by saying that general patterns are important, but describing and explaining them isn’t the only way to do good ecology. (Peter Kareiva articulates this view in a fine essay for NCEAS, still available here in a forgotten backwater on one of NCEAS’ servers) But my main answer is to suggest that the apparent overwhelming contingency of community ecology, and the apparent (relative) simplicity of population ecology and macroecology, isn’t some brute fact of nature. It’s our own creation. It reflects the questions we’ve chosen to ask—the syntheses we’ve tried to make, and the ingredients out of which we’ve tried to make them.

Anything in nature can be described in more or less general terms. I’m a human being, but I’m also a mammal, a vertebrate, an animal, a living organism, and a chunk of matter (and a lot of other things too!) The level of generality with which we frame our questions is our choice. Key questions in population ecology often have been framed at a very high level of generality—for instance, whether per-capita growth rates generally are density-dependent or not. Without this highly-general framing, population ecology would appear just as complex as community ecology. What if, instead of asking questions about density-dependence, we instead chose to ask questions about the relative importance of all the many different sources of density-dependence—predators, parasitoids, pathogens, intraspecific competition, indirect effects, maternal effects, etc., plus all possible combinations of these? Population ecology would suddenly appear to be an overwhelmingly complicated collection of special cases. Not that we couldn’t make it even more complex than that, if we so chose (what about subcategories, such as competition for food vs. for territories vs. for mates?). The same goes for macroecology, where debate often centers on whether we should focus on general trends, or on the variation around them. From the latter point of view, the general trends are trivial statistical epiphenomena, created by averaging away interesting variation among different special cases.

So if the questions we often ask in community ecology have highly contingent answers, maybe we should ask more general questions. For instance, are community dynamics generally characterized by negative frequency dependence—i.e. do species that become sufficiently rare (relative to the others) tend to bounce back? That’s a very important question; it basically amounts to asking if species are stably coexisting or not. The answer has immediate implications for a large body of mathematical theory, and for the practical conservation of biodiversity. That question also is quite closely related to the population ecologist’s question about density-dependence, since density-dependence at the single-species level is manifested as negative frequency dependence at the community level. Now, there are of course many different underlying mechanisms that can give rise to negative frequency dependence. But the fact that all those mechanisms generate frequency dependence is a key general feature they all share, so why not start by focusing on that general feature? And then follow up by asking only slightly more detailed questions, such as whether negative frequency dependence arises primarily from variation-independent mechanisms (i.e., mechanisms that could operate even in a homogeneous, equilibrial world) or variation-dependent mechanisms (i.e. mechanisms that only operate in a spatially- and temporally-variable world)? These questions aren’t hypothetical, nor are they my idea. For instance, Peter Chesson’s theoretical work has long been addressing such questions (Chesson 2000 Ann. Rev. Ecol. Syst. 31:343-66), and field ecologists are now doing so as well (e.g., Adler et al. 2006 PNAS 103:12,793-8). One strand of my own work (shameless plug alert!) tries to develop general theoretical frameworks that would let us ask such general questions in areas where we can’t currently do so (e.g., Fox 2010 Oikos 119:1823-33).

My point is not to criticize the level of generality at which John, and many of my fellow community ecologists, ask community ecology questions. More and less general descriptions of nature complement one another, and a strong science needs both. As John points out, if we only ask detailed questions, the answers we get will tend to look like a stamp collection. But conversely, if we only ask very general questions, we are likely to get only general, imprecise answers, or perhaps even no answers at all (many of the macroecological patterns John cites are infamous for ecologists’ inability to agree on their causes). But if we ask both more and less general questions, the more general ones provide a framework with which to organize the answers to the less general ones. At the same time, the less-general questions provide precision we would otherwise lack. Evolutionary biology is a good example of a field which draws strength from asking both sorts of questions. Without the general theory of evolution by natural selection, studies of, say, changes over time in the bill sizes of Darwin’s finches and in bacterial antibiotic resistance would not have any apparent connection at all, never mind be recognized as two classic examples of natural selection in action. But without detailed studies of specific cases, we could make no quantitative statements about, e.g., how strong selection typically is. We would be limited to making axiomatic statements about evolution, such as Fisher’s Fundamental Theorem.

It’s ecologists who ‘synthesize’ ecology. If we are clever enough, we can get nature to answer any question we ask. So if we don’t like the answers we’re getting, it’s up to us to ask different questions. I look forward to seeing what sort of ecology Oikos authors will create in the future.