Justifying assumptions: tests of seed size/mass tradeoffs

Ben-Hur, E. et al. 2012. Functional trade-offs increase species diversity in experimental plant communities. Ecology Letters. DOI: 10.1111/j.1461-0248.2012.01850.x

When ecologists develop theory and models, we generally need to make assumptions. The nicest definition of an assumption is that they are the framework we use to capture our beliefs about a system. All future analyses will treat these assumptions as true, and so ultimately the validity of a model is tied to the validity of its assumptions. As Joseph Connell said: “Ecological theory does not establish or show anything about nature. It simply lays out the consequences of certain assumptions. Only a study of nature itself can tell us whether these assumptions and consequences are true.” Often times the most interesting advances in ecology come when we questions popular assumptions, such as that species are ecologically different, that interspecific differences are more important than intraspecific differences, or that ecological interactions occur much more rapidly then evolutionary changes. 

Assumptions in models and theory can often serve as a sort of shorthand for ideas that there is some general evidence for, but for which comprehensive data may be lacking. Community ecology is full of assumptions about functional tradeoffs that mediate coexistence between species. Various assumptions about plant species coexistence include that species experience tradeoffs between competition and colonization, growth versus reproduction, or seed size versus seed number. A simplistic explanation for such tradeoffs is that you can’t do everything well: a strong competitor can’t be a good colonizer too, which creates opportunities for strong colonizers but poor competitors, etc.

Tests of these functional tradeoffs are lacking, or lag behind the theory that relies on them. For example, the idea that there should be a tradeoff between seed size and seed number has long been proposed to explain why plants have highly variable seed sizes. Plants with small seeds should produce more offspring, and these seeds should be more successful at reaching empty sites. Large seeded species should be more competitive in the seedling stage or more tolerant of difficult conditions, and so have higher survival. Theoretical models that rely on such a tradeoff suggest that many species could co-exist and that the resulting community would exhibit a wide variety of seed sizes. 

But though many studies and theories depend on this assumed tradeoff, a comprehensive experimental test was lacking. Ben-Hur et al. have finally provided such an experiment, testing the basic prediction that a negative correlation between seed size and seed number should increase species richness. They also tested whether small-seeded species were more likely to remain in the community when this tradeoff existed, increasing the amount of among-species variation in seed size. To do so, the authors created 3 ‘community treatments’ of 15 plant species. The abundance of each species in the starting seed mix was manipulated to create either (1) positive correlation between seed mass and seed number; (2) negative correlation between seed mass and seed number or (3) random allocation of the 15 species regardless of seed size.

From Ben-Hur et al. 2012. Ecology Letters. a) Final number of species in the community, when the correlation between seed size and seed number is negative, random, or positive. b) Seed mass distribution in community under positive correlation between seed size and seed number (left), and negative correlation (right). 

Ben-Hur et al.’s results strongly suggest that a seed size/seed mass functional tradeoff can increase species richness (figure, a). Further, when there is such a tradeoff, the variation in seed size represented in a community increases, again in agreement with predictions (figure, b). The results are particularly convincing because the authors used experimental manipulation of the strength of the correlation (i.e. from negative to positive) to test its importance. The authors suggest that the tradeoff they simulated did not involve competitive differences (i.e. was not a competition-colonisation tradeoff), and more likely reflects a trade-off in establishment probability and colonisation (Dalling and Hubbell 2002; Muller-Landau 2010).

Of course, these results represent relatively short-term coexistence, and community richness may have changed had the experiment been allowed to continue for longer. But as a starting point, this suggests that theories that rely on functional tradeoffs in seed characteristics to explain coexistence are capturing a mechanism that has some experimental support. 

The niche as a changeable entity: phenotypic plasticity in community ecology

Schiffers, K. et al. 2011. Root plasticity buffers competition among plants: theory meets experimental data. Ecology. 92:3.

Ashton et al. 2010. Niche complementarity due to plasticity in resource use: plant partitioning of chemical N forms. Ecology. 91:11.

Nearly all explanations for coexistence in communities focus on differences between species. The scale of these differences may occur over large temporal (e.g. evolutionary history, phylogenetic relationships) or spatial scales (e.g. environmental tolerances), or at the scale of the individual. In plants, interactions at the local scale are given particular attention, including interactions mediated by trait differences between species. At finer scales still, there has been recent focus on differences between individuals of the same species, whether they are driven by genotypic differences (link) or plastic changes in individual phenotypes.

From Ashton et al. 2010

Phenotypic plasticity can be defined as phenotypic differences among individuals of the same genotype that occur in response to an environmental cue. The ability of plant species to alter their usage of resources, for example, has clear relevance to resource partitioning among species, since a given individual could adaptively take advantage of alternate resources in response to their particular competitive environment. In such a case, an individual’s realized niche is a function of phenotypic changes in response to the biotic and abiotic environment and thus physiologically-determined. This is in contrast to the usual approach to species’ niches, where physiological constraints are considered to determine a species’ fundamental niche. Although the plant literature shows clear examples of phenotypic plasticity among plants, including in response to competition (for example, perception of light quality leading to changes in growth form), the topic usually receives only passing mention in the community ecology literature.

The number of papers addressing questions of coexistence and competition through the lens of phenotypic plasticity is slowly rising.

From Schiffer et al. 2011, Lithium uptake is
significantly higher on the non-competitor side

A couple of papers from the last few years provide tantalizing glimpses into the possible contribution of plasticity to coexistence. In Schiffers et al. (2011), the authors use experimental and modeling approaches to test whether root uptake can change in response to the proximity of competitors. In the experimental study, the authors looked at the uptake of lithium (a stable nutrient that will be taken up in the place of potassium) by Bromus hordeaceus. They planted pairs of B. hordeaceus  at varying distances apart and then injected lithium into the soil at different differences from the focal plant. They found that lithium uptake was significantly higher on the non-competitor side of the focal plant than on the competitor side, suggesting that plastic changes in resource uptake occurred in response to competitor proximity. Modelling results from the same study suggest that plasticity may allow individuals minimize competitive pressure by making changes in belowground architecture, thereby using available space more efficiently.

Ashton et al. (2010) take a similar approach, looking at how the uptake of nutrients (in this case three forms of nitrogen (N)) varies among species depending on their competitive environment. They explored the ways in which plasticity could lead to changes in the realized niche. In particular, they explored two hypotheses: that plants would exhibit niche preemption, where the inferior competitor switched to a different form of nitrogen in the presence of the superior competitor; or dominant plasticity, where plasticity actually enhances competitive ability.  The authors looked at 4 species, 3 common and 1 rare(r), in an alpine tundra community, isolating naturally occurring pairs of each combination of species. These ‘competitive arenas’ were isolated, and other species within the arena were removed. After a year, the authors added N¹⁵ tracers to each arena, in three forms (NH4+, NO3-, and glycine): these tracers would allow them to track the N once it was incorporated into the plant tissue. The plants were then harvested and the amount of each type of nitrogen in each was measured. Plant biomass was also recorded, and used to estimate the ‘competitive response’ (basically the ratio of biomass when grown with a competitor compared biomass to when grown solo). Their findings were rather neat: the 3 common plants experienced no negative effect on biomass from growing in competition with the rare plant, but the rare plant had much lower biomass when grown in the presence of any of the common plants. Further, while the common plants showed changes in the form of N they used when growing with the rare plant, the rare plant did not switch its N preference. The rare plant’s lack of plasticity in response to competition may relate to its lower biomass when grown with superior competitors, and ultimately its lower abundance.

Although limited, these studies hint at the role that phenotypic plasticity could play in interspecific interactions. Unfortunately plasticity may be difficult to measure in many contexts, particularly since variation within a species can be attributed to genetic differences or phenotypic plasticity, and these factors must be teased apart. Further, there is an issue of differentiating the effects of resource limitations from ‘adaptive’ plastic changes in growth. While plants are relatively tractable for these types of studies (they’re sessile, they use limited abiotic resources), other organisms are less explored for a reason.

What these studies can’t address is the question of ‘how important is phenotypic plasticity, really’? Reviews of coexistence mechanisms list numerous possible ways by which coexistence is facilitated among species. For plants especially, the limited number of resources required for survival has lead to great consideration of the possible niche axes over which species can differentiate themselves. Phenotypic plasticity's contribution to coexistence may be that it provides another way by which plants can partition resources at very fine scales. And if nothing else, such results provide further evidence that variation within species may be an important component of coexistence.

Thanks to Kelly Carscadden for discussions on the topic.

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.

Ecology needs more evolution (and vice versa)

One historical weakness in community ecology is its singular focus on ecology in the absence of any consideration of the role of evolution. Ecological theory may attempt to explain and expand on mechanisms of coexistence, but this is done in ignorance of whether such a mechanism could have reasonably evolved in the first place. Evolutionary biology has equally ignored the role of ecology (for example, just-so stories invented in the absence of ecological support). Fortunately, it is becoming more common to see papers that incorporate, empirically or theoretically, evolution and community ecology.

A recent paper by Robin Snyder and Peter Adler attempts to incorporate both ecology and evolution in reference to the storage effect, a mechanism in which species coexist as a result of environmental variability and corresponding differential variation in species fecundity in response to the environment. As a simplistic example, consider a system of two annual plants for which each species has their highest recruitment at different temperatures, and temperature varies randomly between years. Each species is expected to have high recruitment in different years/environmental conditions, and this high recruitment in good years can then buffer that species’ fitnesses in years of poor conditions, provided the species have some way of “storing” fitness (such as long-lived seedbanks). The storage effect therefore predicts that environmental variability can mediate the coexistence of otherwise unequal competitors. Because the requirements of the storage effect appear so ubiquitous (environmental variation, differential species responses to the environment, some sort of buffer), it seems that the storage effect could be very common. However, there is also theory suggesting that variation in demographic rates should come at a fitness cost, since the long term mean growth rate will be lower if demographic rates vary than if they are fixed (as the result of geometric averaging). This predicts that there should be selection against flexible—rather than fixed—demographic rates, including rates that vary in response to environmental or other cues. Is it possible then for variable demographic rates, which are necessary for the storage effect, to evolve?

Snyder and Adler discuss this disconnect between community ecology and evolution, questioning whether the storage effect can be supported by both evolutionary and ecological theory. To this end, the authors explore whether, and under what conditions, the storage effect could evolve. Snyder and Adler use a simple model of competition between two annual plants, in which fecundity fluctuates due to environmental variation, and germination rate can be temporally fixed, or variable. Germination rates should be constant, despite environmental variation, due to the cost of variability. Germination rates would be expected to vary year to year only if this conferred a fitness benefit to the species. Hypothesized benefits of variable germination rates include if germination rates are positively correlated with fecundity (that is, in good years germination is higher as well), or if it allows a species to avoid competition (by having high germination when their competitor has low germination). To test this hypothesis, the authors varied the correlation between fecundity and germination, and the correlation between the two species’ germination rates. They then examined the conditions under which variable germination rates were an evolutionarily stable strategy (ESS).

Snyder and Adler’s results suggest that the storage effect is expected to evolve only under anarrow set of conditions. A variable germination rate was most likely to evolve if there was a strong correlation between fecundity and germination rate. They note that such a correlation might occur if seed production and germination depended on similar environmental cues or similar resource requirements. A variable germination rate was also a stable strategy if one species was limited in its ability to evolve, in which case the other species evolved variable germination rates. If these specific conditions didn’t hold, the storage effect was not evolutionarily stable.

These results are meaningful because they highlight how different the conclusions of community ecology, which has proposed that the storage effect could be a widespread contributor to coexistence, and evolutionary theory, which suggests that the storage effect may only occur under particular conditions, can be. This kind of reconciliation of community ecology and evolution tells us more about natural systems than either approach can on its own. It also hints that theory and conclusions we’ve drawn in community ecology in the absence of evolution may be limited and incomplete.

The empirical divide

Has there been a shift in how ecology is done? In an interesting editorial in the most recent ESA Bulletin, titled “Losing the Culture of Ecology”, David Lindenmayer and Gene Likens wrote that “empirical and place-based research”, such as field studies and taxonomy, appear to be falling out of favor. They suggest that ecological modeling, meta-analysis, and data-mining (the three M’s) are more lucrative (and popular) approaches today, because these methods are faster, cheaper, and “easier” to perform, allowing more rapid publication. While they recognize the important advancements resulting from these methods, the result—they suggest—is that field-based empirical research is becoming less prevalent, to the detriment of ecology.

This is a polarizing issue, and the response of those ecologists we spoke to depended on where they position themselves on the field/theoretical divide. Those who define themselves as field ecologists tended to feel embattled in the face of long, expensive months of fieldwork, with slow returns in terms of data and publications. Some felt there is a subtle insinuation that fieldwork is less generalizable and so less valuable than techniques such as meta-analysis and ecological modeling, which by their nature tend to be theory-based and general.

On the other side, some theoretical ecologists we spoke to felt the need to defend the validity of doing “indoor” ecology, noting that theory and modeling can link pattern and process, without the confounding variation common in field experiments/observations. Although field ecologists felt that they have a more difficult time obtaining funding, theoretical ecologists noted that they often receive far less money because the assumption is that theory is “free”. Further, with the exception of very specialized funding opportunities (e.g., NCEAS), meta-analyses do not typically get funded as stand-alone projects.

It’s important to note that in its short history, ecology has frequently struggled with the balance between the field and lab. The primary criticism of field-based research at the turn of the 20th century was that it was “unscientific”, inseparable from natural history, producing lists of species names rather than furthering understanding, while labwork was considered to be too divorced from natural systems to be informative (producing so-called “armchair ecologists”). These conflicts split some of the first organismal departments in the United States (*) and tensions exist to this day. No doubt these criticisms are not unfamiliar to many modern ecologists.

There needs to be a balance between the production and consumption of data. Obviously abandoning fieldwork and using only meta-analysis, modeling, and data-mining is not sustainable, but these are important methods for modern ecology. In addition, the perceptions of bias against fieldwork may be due to a general decline in funding and greater overall competitiveness for the rewards of academic labour (jobs, grants, publishing in top journals, etc.), rather than a true decline in field ecology. As we discussed this article, it became clear that our own perceptions, and perhaps those of the broader community, have formed in the absence of empirical data. We examined the last few issues of some highly-ranked ecological journals that publish primary research (Ecology Letters, Molecular Ecology, American Naturalist), and recorded the number of papers that used empirical data, and further the number of those that collected their own data (versus using data from databases, literature, etc). Surprisingly, the vast majority of studies were based on empirical data, mostly data collected by the authors. In Molecular Ecology, 27 out of 28 papers were empirical, and 26 of these used data collected by the author(s); in Ecology Letters, 17 out of 20 papers were empirical, and 12 of these used data collected by the author(s). Even in American Naturalist, which is known for its theoretical bent, 44 out of 70 papers were empirical, and 32 used the author(s)’ own data. Overall, these journals, where competition for space is most severe, primarily publish empirical research.

It appears then, that neither grants nor publications systemically bias towards the three M’s. But is there still a cost to researchers on either side of the data producer-consumer divide? The answer is likely yes. The three M’s result in quicker publications, which means these researchers look more productive on paper, resulting in greater visibility. With more publications, they are likely to make it to the top of hiring committee lists. Conversely, unless a specific job has been advertised as a modeling position, candidates giving job talks focusing on the three M’s do not come across as knowledgeably as a very skilled field person. One of us (MWC) has seen job searches at four different institutions, and the unadvertised stipulation for many departmental faculty or committee members is that the candidate will come and establish a field program. Another common criticism of 3-M candidates is that they will not be able to secure large amounts of research funding.

Given this double-edged sword, what is the optimal strategy? The glib, easy answer is that ecologists need to become less specialized, to do both theory and empirical work, if they want a successful career. And maybe this is the solution, at least for some ecologists. But is having everyone become a generalist really the answer? Most field ecologists will tell you that they do fieldwork in part because they love being in the field and they’re good at it; most theoretical ecologists are adept at manipulating ideas and theory. Perhaps there is still a role for the specialist: after all quantitative ecology—which produces data—and theoretical ecology—which consumes it—are inseparable. They have a complementary relationship, in which field observations and data fuel new models and ideas, which in turn provides new hypotheses to be tested in the field. It’s obvious that people should be able to specialize, and that the focus should be on increasing collaboration between the two groups.

Despite the hand-wrenching, perhaps this collaboration is already happening. Many of the very best 3-M papers unite theoretically-minded with empirically-grounded ecologists. The working-group style funding by NCEAS (and its emulates) explicitly links together data producers and data consumers. These papers may be deserving of greater visibility. If collaboration is the future of ecology, why does the tension still exist between lab and field? The historical tension was not really about the laboratory vs. the field, but rather about scientific philosophy, and we think this holds true today. Ecology has tangibly moved towards hypothesis-driven research, at the expense of inductive science, which was more common in the past. The tensions between “indoor ecology” and field ecology have been conflated with changes in the philosophy of modern ecology, in the difficulties of obtaining funding and publishing as a modern ecologist, and some degree of thinking the “grass is always greener” in the other field. In fact, the empirical divide may not be as wide as is often suggested.

By Caroline Tucker and Marc Cadotte


* Robert E. Kohler. Landscapes and labscapes: Exploring the lab-field border in biology. 2002. University of Chicago Press. (This is a fascinating book about the early years of ecology, and definitely worth a read).

Nature’s little blue pill

Something often happens to mature community ecology studies as they get older that we don’t like to talk about much. Occasionally, when biodiversity and ecosystem functioning experiments are performed in a controlled, homogeneous setting, they can suffer from flaccid response curves. It’s perfectly normal, happens to lots of healthy microcosm communities, but it can be troubling and embarrassing nonetheless. After all, who doesn’t want a nice stiff linear response curve?

Bear with me here for a minute.

A few weeks ago, Bradley Cardinale published a study in which he tested the effects of algal biodiversity on water quality in streams. It’s a pretty classic diversity-function experiment; lots of artificial streams with different numbers of species of algae in them, and he measured productivity and nitrogen uptake. As is usually the case, the more species he put in each stream, the more these ecosystem functions increased.

But Cardinale did something else in this experiment that has never been done before, at least not on this scale. He added extra niche opportunities to some of the streams, so that they offered multiple different habitats for algae. He did this by introducing heterogeneity through flow and disturbance manipulations.

Figures from Cardinale 2011, Nature. a and b are the heterogeneous streams, d and e are the homogeneous ones.

You might be familiar with that saturating response curve that is typical of so many diversity-function experiments. It starts off with large increases in ecosystem functioning as species are added to communities, and then it levels off so that as additional species are added, they only increase ecosystem functioning by small amounts (figures d and e). The theory behind this is that there are only so many niches in an environment, and as more and more species are added some of them become redundant.

Well when Cardinale threw those extra habitats into his artificial streams, that floppy old saturating curve sprang up like a regressional jack-in-the-box (figures a and b).

What happened was the homogeneous streams became dominated by just a single species that was well adapted to that environment. The heterogeneous streams allowed different species to coexist and this let them make more efficient use of the resources in those streams.

This is a major finding for a few reasons. First, it confirms that one of the main mechanisms behind diversity-function relationships is niche partitioning. I’ve said in the past that knowledge of these mechanisms is sorely needed. Second, it links coexistence theory to ecosystem functioning, two fields that are closely related but often disconnected.

Finally, it means that biodiversity is even more valuable than we had previously thought. The natural world doesn’t contain very many homogeneous streams; it’s a complicated place. The real world is probably better represented by figures a and b than by figures d and e. So while controlled experiments have shown that some species are redundant for ecosystem functioning, there is no evidence here for any redundancy in more natural settings.

This paper also underlines the fact that these studies need to be done in nature as opposed to labs. Cardinale was able to simulate nature fairly realistically because he was using algae. That’s harder to do with more complex organisms. It’s difficult to recreate environmental heterogeneity in artificial ecosystems, and if ecosystem functioning depends on both biodiversity and heterogeneity, then it’s time to take this research outside. Manipulative field studies are a good start, but completely natural settings will probably reveal more of the true story.

So although it’s very common for artificial communities to suffer from Ecological Dysfunction, there is no reason that they can’t enjoy a healthy relationship with biodiversity like any other community. All they need is a little heterogeneity to spice things up and put that spring back in their step.

Andy Hector has written an excellent perspective on the study. I recommend reading it, particularly if you don’t want to read the entire original article.

Happy 10th birthday, neutral theory!

Rosindell, Hubbell, and Etienne. (2011). The unified neutral theory of biodiversity and biogeography at age ten.

I would argue that neutral theory is not only the most controversial idea, but also the most successful idea to permeate community ecology in the last ten years. A quick keyword search suggests that ~30 ecological papers related to the topic were published in the last year, including some with titles still reflecting the controversy; “Different but equal: the implausible assumption at the heart of neutral theory”. Neutral theory makes a seemingly unreasonable assumption—that species identity doesn’t matter—and yet seems to predict species-area relationships and species abundance distributions as well or better than niche theory does. This made it an infuriating challenge for many ecologists. The number and quality of papers that it inspired—both in support and opposition—are a reminder that disagreement is good for science.

It’s been a decade since the publication of “The Unified Neutral Theory of Biodiversity and Biogeography”, in which Steve Hubbell proposed a controversial model in which coexistence results from drift, dispersal and speciation, rather than ecological differences between species. To mark this anniversary, a review in TREE by James Rosindell, Stephen Hubbell, and Rampal Etienne reflects on neutral theory’s first ten years, and examine the influence neutral theory has had in many areas of community ecology. The authors also note that some of the limitations of neutral theory can be dealt with by extending the classic formulation of the model, so that unrealistic assumptions related to spatial structure, speciation rates, or the zero-sum assumption can be relaxed. The excessive interest in neutral theory’s species-abundance predictions left its other predictions unexamined, and there is still room for tests of how neutral theory informs species-time relationships, modes of speciation, and even conservation decisions.

Despite these accomplishments, the review is remarkably subdued, underlined by statements such as neutral theory is a “good starting point”, a “valuable null model”, and a “useful baseline”. However, it seems unnecessary to state, as some have, that "neutral theory is dead". Its legacy, captured in the final paragraphs, is still incredibly important: “…niches have dominated our attention and left less obvious, but still important processes forgotten… Perhaps the most important contribution of neutral theory has been to highlight the key roles of dispersal limitation, speciation and ecological drift, by showing how much can be explained by these processes alone...”

George Box said it best: “All models are wrong, but some are useful”.

Biodiversity and ecosystem functioning – without fungi?

Different subfields of ecology have a propensity to remain remarkably isolated – researchers in aquatic systems independently develop hypotheses that already exist in some form in other systems, and vice versa. Population ecology and community ecology, despite their obvious relevance to each other, are rarely integrated. There is a tendency – resulting from limits on our time, experience, and possibly imagination – to stay within whatever box we’ve defined for ourselves.

Historically, it seems that biodiversity and ecosystem functioning has lost sight of the progress made in classical ecology in understanding the mechanisms behind species coexistence (and all the functional implications that follow). Studies of ecosystem functioning often vaguely reference concepts such as “niche partitioning”, which would hardly be explicit enough for most papers on coexistence. Fortunately, there are periodically attempts to unifying ecological knowledge.

One of the most important contributions to understanding coexistence is Chesson’s (2000) framework of equalizing and stabilizing effects. Unlike previous approaches to species interactions, which tended to reference these vaguely-defined “niche differences”, Chesson proposed that species interactions depended on both fitness differences (differences in absolute growth rates after niche differences are controlled for) and niche differences (ecological differences between species which cause intraspecific competition to exceed interspecific competition). He also suggested rigorous methods to quantify these concepts. This framework has been applied both to the obvious questions of species coexistence and diversity maintenance, as well as predator-prey relationships (2008) and the phylogenetic structure of communities (2010).

In a recent paper, Ian Carroll et al. apply this framework to the search for the mechanisms behind biodiversity and ecosystem functioning. They point out that the questions in studies of ecosystem functioning are directly analogous to Chesson’s concepts – selection effects result from fitness or competitive differences between species, while complementarity relates to the partitioning of resources, or niche differences between species. The added benefit is that Chesson has provided clear definitions for these concepts.

While this may not be world-altering, it’s encouraging. Anytime different areas of ecology intersect, both benefit. Of course there are difficulties – no doubt the question of how to measure niche differences and fitness differences will be contentious (as attempts to translate ecological theory into ecological methodology often are) - but the possibility that a few general ecological concepts explain diverse observations is worth pursuing.

Competitive coexistence, it's all about individuals.

Understanding how species coexist has been the raison d'etre for many ecologists over the past 100 years. The quest to understand and explain why so many species coexist together has really been a journey of shifting narratives. The major road stops on this journey have included searching for niche differences among species -from single resources to multidimensional niches, elevating the role for non-equilibrial dynamics -namely disturbances, and assessing the possibility that species actually differ little and diversity patterns follow neutral process. Along this entire journey, researchers (especially theoreticians) have reminded the larger community that that coexistence is a product of the balance between interactions among species (interspecific) and interactions among individuals within species (intraspecific). Despite this occasional reminder, ecologists have largely searched for mechanisms dictating the strength of interspecific interactions.

Image used under Flickr creative commons license, taken by Tinken

In order for two species to coexist, intraspecific competition must be stronger than interspecific -so sayeth classic models of competition. While people have consistently looked for niche differences that reduce interspecific competition, no one has really assessed the strength of intraspecific competition. Until now that is. In a recent paper in Science, Jim Clark examines intra- vs interspecific interactions from data following individual tree performances, across multiple species, for up to 18 years. This data set included annual growth and reproduction, resulting in 226,000 observations across 22,000 trees in 33 species!

His question was actually quite simple -what is the strength of intraspecific interactions relative to interspecific ones? There are two alternatives. First, that intraspecific competition is higher, meaning that among species differences only need to be small for coexistence to occur; or secondly, that intraspecific competition is lower, requiring greater species niche differences for coexistence. To answer this he looked at correlations in growth and fecundity between individuals either belonging to the same or different species, living in proximity to one another. He took a strong positive correlation as evidence for strong competition and a negative or weak correlation as evidence for resource or temporal niche partitioning. What he found was that individuals within species were much more likely to show correlated responses to fluctuating environments, than individuals among species.

This paper represents persuasive evidence that within-species competition is generally extremely high, meaning that to satisfy the inequality leading to coexistence: intra > inter, subtle niche differences can be sufficient. These findings should spur a new era of theoretical predictions and empirical tests as our collective journey to understanding coexistence continues.

Clark, J. (2010). Individuals and the Variation Needed for High Species Diversity in Forest Trees Science, 327 (5969), 1129-1132 DOI: 10.1126/science.1183506