Don't forget the details! Trait ecology and generality

The search for generality is perhaps the greatest driver of modern ecology and probably also the greatest source of ecological angst. Though ecological trends frequently reflect the newest, brightest hope for generality, the search for generality (perhaps by definition) encourages us to ignored details and complexities. Maybe this means that some areas of study won't develop fully until they've fallen out of fashion. And maybe this means that the most interesting science happens when the pressure to 'save community ecology' is gone. A great example of the kind of post-hype, thoughtful approach for trait-based ecology comes from Reynolds et al. (2017) in Tree Physiology. They do a really nice job of highlighting some of the details that must inform trait-based ecology. Here, Reynolds et al. take a broad comparative approach across species, but incorporate important details that have at times been overlooked - especially the role of the environment, recognizing and measuring both constitutive and plastic traits, captures that there are multiple paths (or trait combinations) that can result in similar functioning.

The authors look at four conspecific tree species (Brachychiton spp.) with different average positions along an observed moisture gradient (CMD or climate moisture deficit). Two species occupied drier areas of Australia ('xeric species'), while the other two were found in more moderate areas ('mesic species'). The authors assumed that the different distributions of these species reflect different hydraulic niches. Were species' hydraulic niches associate meaningfully with their traits, specifically those trait associated with drought stress responses. Though these species are closely related--and so huge divergences in form and function might not be expected--the costs and benefits of drought resistance should differ among the species. In dry environments, drought resistance strategies should be more important, and may select for particular traits or sets of traits. Trait states associated with drought conditions include "reduced leaf area, enhanced stomatal control, safer or more efficient xylem, increased tissue water capacitance...and/or deeper root systems " may all be selected for. On the other hand, investment in these traits when water is not limited is often costly, reducing growth and competition. This suggests a meaningful selective regime associated with the CMD gradient and trait values might exist.

One important, but oft-overlooked aspect of trait ecology is that trait values depend on both genes and the environment. Reynold et al. incorporate this fact this by manipulating water availability between drought and control treatments. They measured both constitutive components of trait values – those driven by genetics and expressed regardless of environments – and the plastic or environment-dependent components. For instance, in the presence of prolonged drought, trees might increase root production or change leaf characteristics. In addition to manipulating water availability between treatments, the authors measured nine traits related to morphology and allocation.

From Reynolds et al. 

Given the expectation that trait values reflect the complex interaction of genetics and the environment in different species, is it possible to even make simple predictions about trait-environment relationships? The authors find that "These complex relationships illustrate that assuming that individual traits (often measured on individuals under a single set of environmental conditions) reflect drought resistance is likely to be overly simplistic and may be erroneous for many species. However, our results do suggest that generalization may be possible, provided multiple traits are measured to explore specific integrated drought strategies."

Indeed, some results are relatively predictable relationships: under well-watered control conditions, the allocation of biomass matched the expectation: xeric species had higher investment in below-ground biomass and in transport tissues than the mesic species (both characteristic of a water-conserving species).

On the other hand, leaf traits such as SLA did not show any trend related to species' assumed drought tolerance, either for constitutive or plastic trait components. Sometimes traits associated with the leaf economic spectrum such as SLA are assumed to indicate stress tolerance, but this was not the case.

By far the most interesting result was the observation that the xeric species had the highest assimilation and stomatal conductance rate and the lowest water use efficiency under well-watered conditions. Only by also examining these species under drought conditions was it possible to observe that they are highly plastic with regards to water use efficiency. In fact, they show a feast or famine approach to water usage - "where high photosynthetic rates per unit leaf area and high investment in root and stem tissue even in well-watered conditions are achieved through profligate water use during rare periods of water availability, in order to establish a root system and stem storage tissues necessary to survive long periods of water stress." Under drought conditions, these species show reduced root tissue investment; in contrast, mesic species follow expected patterns and plastically increase root tissue investment.

This paper is a reminder that the details are also fascinating and informative. As humans, we may have a simplistic understanding of the realized environment sometimes. To us perhaps all water stress is similar, but for each species in this study, the long term selective pressures may be meaningfully different - in timing, duration, and life stage. This creates the potential for complex differences between species which may best be reflected via life history strategies involving multiple traits. That may still imply some degree of generality is possible, but it is multi-dimensional.

Works cited:
Victoria A Reynolds, Leander D L Anderegg, Xingwen Loy, Janneke HilleRisLambers, Margaret M Mayfield; Unexpected drought resistance strategies in seedlings of four Brachychiton species, Tree Physiology, https://doi.org/10.1093/treephys/tpx143

Problems with over-generalizing the dynamics of communities

Community ecologists talk about communities as experiencing particular processes in a rather general way. We fall into rather Clementsian language, asking whether environmental filtering dominates a community or if biotic interactions are disproportionately strong. This is in contrast to the typical theoretical focus on pairwise interactions, as it acts as though all species in a community are responding similarly to similar processes.

Some approaches to community ecology have eschewed this generality, particularly those that focus on ecological ‘strategies’ differentiating between species. For example, Grimes argued that species in a community represented a tradeoff between three potential strategies - competitive, stress-tolerant, and ruderal (CRS). Other related work describes rarity as the outcome of very strong density-dependence. The core-transient approach to understanding communities differentiates between core species, which have deterministic dynamics tied to the mean local environment, in contrast to transient species which are decoupled from local environmental conditions and have dynamics are driven by stochastic events (immigration, environmental fluctuations, source-sink dynamics). Assuming environmental stationarity, core species will have predictable and consistent abundances through time, in comparison to transient species.

If species do respond differently to different processes, then attempting to analyse all members of a community in the same way and in relation to the same processes will be less informative. Tests for environment-trait relationships to understand community composition will be weaker, since the species present in a community do not equally reflect the environmental conditions. In “A core-transient framework for trait-based community ecology: an example from a tropical tree seedling community”, Umana et al (2017) ask whether differentiating between core and transient species can improve trait-based analyses. They analyse tropical forest communities in Yunnan, China, predicting that core species "will have strong trait–environment relationships that increase the growth rates and probability of survival that will lead to greater reproductive success, population persistence and abundance".

The data for this test came from 218 1 m2 seedling plots, which differed in soil and light availability. The authors estimated the performance of individual seedlings in terms of relative growth rate (RGR). They also gathered eight traits related to biomass accumulation, and stem, root and leaf organ characteristics. They were particularly interested in how the RGR of any individual seedling differed from the mean expectation for their species. Did this RGR deviation relate to environmental differences between sites?  If a species’ presence is strongly influenced by the environment, then RGR deviation should vary predictably based on environmental conditions.

They then modelled RGR deviation as a function of the traits or environmental conditions (PCA axes). They considered various approaches for binning species based on commonness vs. rarity, but the general result was that bins containing rarer species had fewer PCA axes significantly associated with their RGR deviation and/or those relationships were weaker (e.g. see Figure below).

They conclude  that “the main results of our study show that the strength of demography-environment/trait and trait-environment relationships is not consistent across species in a community and the strength of these effects is related to abundance”. Note that other studies similarly find variation in the apparent mechanism of coexistence in communities. For example, Kraft et al. 2015  found that local fitness and niche differences only predict coexistence for a fraction of species co-occurring in their sites.

Umana et al.'s result is a reminder that work looking for general processes at the community level may be misleading. It isn't clear that there is a good reason to divide species into only two categories (e.g. core versus transients): like unhappy families, transient species may each be transient in their own way.

What is a community ecologist anyways?

I am organizing a 'community ecology' reading group, and someone asked me whether I didn’t think focusing on communities wasn’t a little restrictive. And no. The thought never crossed my mind. Which I realized is because I internally define community ecology as a large set of things including ‘everything I work on’ :-) When people ask me what I do, I usually say I’m a community ecologist.

Obviously community ecology is the study of ecological communities [“theoretical ideal the complete set of organisms living in a particular place and time as an ecological community sensu lato”, Vellend 2016]. But in practice, it's very difficult to define the boundaries of what a community is (Ricklefs 2008), and the scale of time and space is rather flexible.

So I suppose my working definition has been that a community ecologist researches groups of organisms and understands them in terms of ecological processes. There is flexibility in terms of spatial and temporal scale, number and type of trophic levels, interaction type and number, or response variables of interest. It’s also true that this definition could be encompass much of modern ecology…

On the other hand, a colleague argued that only the specific study of species interactions should be considered as ‘community ecology’: e.g. pollination ecology, predator-prey interactions, competition, probably food web and multi-trophic level interactions. 

Perhaps my definition is so broad as to be uninformative, and my colleague's is too narrow to include all areas. But it is my interest in community ecology that leads me to sometimes think about larger spatial and temporal scales. Maybe that's what community ecologists have in common: the flexibility needed to deal with the complexities of ecological communities.

When individual differences matter - intraspecific variation in 2016

Maybe it is just confirmation bias, but there seems to have been an upswing in the number of cool papers on the role of intraspecific variation in ecology. For example, three new papers highlight the importance of variation among individuals for topics ranging from conservation, coexistence, and community responses to changing environments. All are worth a deeper read.

‘An Anthropocene map of genetic diversity’ asks how intraspecific variation is distributed globally, a simple but important question. Genetic diversity in a species is an important predictor of their ability to adapt to changing environments. For many species, however, as their populations decline in size, become fragmented, or experience strong selection related to human activities, genetic diversity may be in decline. Quantifying a baseline for global genetic diversity is an important goal. Further, with the rise of ‘big data’ (as people love to brand it) it is now an accessible one: there are now millions of genetic sequences in GenBank and associated GPS coordinates. 

Many of the global patterns in genetic diversity agree with those seen for other forms of diversity: for example, some of the highest levels are observed in the tropical Andes and Amazonia, and there is a peak in the mid-latitudes and human presence seems to decrease genetic diversity.

From Miraldo et al. (2016): Map of uncertainty. Areas in green represent high sequence availability and taxonomic coverage (of all species known to be present in a cell). All other colors represent areas lacking important data.

The resulting data set represents ~ 5000 species, so naturally the rarest species and the least charismatic are underrepresented. The authors identify this global distribution of ignorance, highlighting just how small our big data still is.

Miraldo, Andreia, et al. "An Anthropocene map of genetic diversity." Science353.6307 (2016): 1532-1535.


In ‘How variation between individuals affects species coexistence’, Simon Hart et al. do the much needed work to answer the question of how intraspecific variation fits into coexistence theory. Their results reinforce the suggestion that in general, intraspecific variation should making coexistence more difficult, since it increases the dominance of superior competitors, and reduces species' niche differentiation. (Note this is a contrast to the argument Jim Clark has made with individual trees, eg. Clark 2010)

Hart, Simon P., Sebastian J. Schreiber, and Jonathan M. Levine. "How variation between individuals affects species coexistence." Ecology letters (2016).


The topic of evolutionary rescue is an interesting, highlighting (see work from Andy Gonzalez and Graham Bell for more details) the ability of populations to adapt to stressors and changing environments, provided enough underlying additive genetic variation and time is available. It has been suggested that phenotypic plasticity can reduce the chance of evolutionary rescue, since it reduces selection on genetic traits. Alternatively, by increasing survival time following environmental change, it may aid evolutionary rescue. Ashander et al. use a theoretical approach to explore how plasticity interacts with a change in environmental conditions (mean and predictability/autocorrelation) to affect extinction risk (and so the chance of evolutionary rescue). Their results provide insight into how the predictability of new environments, through an affect on stochasticity, in turn changes extinction risk and rescue.

Ashander, Jaime, Luis-Miguel Chevin, and Marissa L. Baskett. "Predicting evolutionary rescue via evolving plasticity in stochastic environments." Proc. R. Soc. B. Vol. 283. No. 1839. The Royal Society, 2016.

The future of community phylogenetics

Community phylogenetics has received plenty of criticism over the last ten years (e.g. Mayfield and Levine, 2010; Gerhold et al. 2015). Much of the criticism is tied to concerns about pattern-based inference, the use of proxy variables, and untested assumptions. These issues are hardly unique to community phylogenetics, and I think that few ideas are solely ''good or solely 'bad'. They are useful in moulding our thinking as ecologists and inspiring new directions of thought. Many influential ideas in ecology have bobbled in confidence through time, but remain valuable nonetheless [e.g. interspecific competition, character displacement (Schoener 1982; Strong 1979)]. But still, it can be hard to see exactly how to use phylogenetic distances to inform community-level analyses in a rigorous way. Fortunately, there is research showing exactly this. The key, to me at least, to avoid treating a phylogeny as just another matrix to analyze, but to consider and test the mechanisms that might link the outcome of millions of years of evolution to community-level interactions.

A couple of potential approaches to move forward questions about community phylogenetics are discussed below. The first is to consider the mechanisms behind the pattern-inference analyses and ask whether assumptions hold.

1) Phylogenies and traits - testing assumptions about proxy value
As you know, if you have read the introductory paragraph of many community phylogenetic papers, Charles Darwin was the first to highlight that two closely related species might have different interactions than two distantly related species. People have tested this hypothesis in many ways in various systems, with mixed results. The most important directions forward is to make explicit the assumptions behind such ideas and experimentally test them. I.e. Do phylogenetic distances/divergence between species capture trait and ultimately ecological divergence between species?

From Kelly et al. 2015 Fig 1b.

Because evolutionary divergence should relate to feature divergence (sensu Faith), the most direct question to ask is how functionally important trait differences increase with increasing phylogenetic distances. For example, Kelly et al. (2014) found that “close relatives share more features than distant relatives but beyond a certain threshold increasingly more distant relatives are not more divergent in phenotype”, although in a limited test based only on patristic distances. This suggests that at short distances, phylogenetic distances may be a reasonable proxy for feature divergence, but that the relationship is not useful for making predictions about distant relatives.

Phylogenies and coexistence/competition. Ecological questions about communities may not be interested in traits alone. The key assumption behind many early analyses was that closely related species shared more similar *niches*, and so competed more strongly than distantly related species. Thus the question is one step removed from trait evolution, asking instead how phylogenetic divergence correlates into fitness differences or interaction strength. Not surprisingly, current papers suggest there is a fairly mixed, less predictable relationship between phylogenetic relatedness and competitive outcomes.

Recent findings have varied from “Stabilising niche differences were unrelated to phylogenetic distance, while species’ average fitness showed phylogenetic structure” (California grassland plants, Godoy et al. 2014); to, there is no signal in fitness or niche differences (algae species, Narwani et al. 2013); to, when species are sympatric, both stabilizing and fitness differences increase with phylogenetic distance (mediterranean annual plants; Germain et al. 2016). Given constraints, tradeoffs and convergence of strategies, it is really not surprising that the idea of simply inferring the importance of competition from patterns along a phylogenetic tree is not generally possible (Kraft et al. 2015; blogpost).

2) Phylogenies and the regional species pool
Really more interesting than testing for proxy value is to think about the mechanisms that tie evolution and community dynamics together. A key role for evolution in questions about community ecology is to ask what we can learn about the regional species pool—from which local communities are assembled. What information about the history of the lineages in a regional species pool informs the composition of local composition?

The character of the regional species pool is determined in part by the evolutionary history of the region, and this can in turn greatly constrain the evolutionary history of the community (Bartish et al. 2010). The abundance of past habitat types may alter the species pool, while certain communities may act as 'museums' harbouring particular clades. For example, Bartish et al. 2016 found that the lineages represented in different habitat types in a region differ in the evolutionary history they represent, with communities in dry habitats disproportionately including lineages from dry epochs and similar for wet habitats. Here, considering the phylogeny provides insight into the evolutionary component of an ecological idea like 'environmental filtering'.

Similarly, species pools are formed by both ecological processes (dispersal and constraints on dispersal) and evolutionary ones (extinctions, speciation in situ), and one suggestion is that appropriate null models for communities may need to consider both ecological and evolutionary processes (Pigot and Etienne, 2015).
Invasive species also should be considered in the context of evolution and ecology. Gallien et al. 2016 found that “currently invasive species belong to lineages that were particularly successful at colonizing new regions in the past.”

I think using phylogenies in this way is philosophically in line with ideas like Robert Ricklef's 'regional community' concept. The recognition is that a single time scale may be limiting in terms of understanding ecological communities.

References:

1. Mayfield, Margaret M., and Jonathan M. Levine. "Opposing effects of competitive exclusion on the phylogenetic structure of communities." Ecology letters 13.9 (2010): 1085-1093.
2. Gerhold, Pille, et al. "Phylogenetic patterns are not proxies of community assembly mechanisms (they are far better)." Functional Ecology 29.5 (2015): 600-614.
3. Schoener, Thomas W. "The controversy over interspecific competition: despite spirited criticism, competition continues to occupy a major domain in ecological thought." American Scientist 70.6 (1982): 586-595. 
4. Strong Jr, Donald R., Lee Ann Szyska, and Daniel S. Simberloff. "Test of community-wide character displacement against null hypotheses." Evolution(1979): 897-913. 
5. Kelly, Steven, Richard Grenyer, and Robert W. Scotland. "Phylogenetic trees do not reliably predict feature diversity." Diversity and distributions 20.5 (2014): 600-612.
6. Godoy, Oscar, Nathan JB Kraft, and Jonathan M. Levine. "Phylogenetic relatedness and the determinants of competitive outcomes." Ecology Letters17.7 (2014): 836-844.
7. Narwani, Anita, et al. "Experimental evidence that evolutionary relatedness does not affect the ecological mechanisms of coexistence in freshwater green algae." Ecology Letters 16.11 (2013): 1373-1381.
8. Rachel M. Germain, Jason T. Weir, Benjamin Gilbert. Species coexistence: macroevolutionary relationships and the contingency of historical interactions. Proc. R. Soc. B 2016 283 20160047
9. Nathan J. B. Kraft, Oscar Godoy, and Jonathan M. Levine. Plant functional traits and the multidimensional nature of species coexistence. 2015. PNAS.
10. Bartish, Igor V., et al. "Species pools along contemporary environmental gradients represent different levels of diversification." Journal of Biogeography 37.12 (2010): 2317-2331.
11. IV Bartish, WA Ozinga, MI Bartish, GW Wamelink, SM Hennekens. 2016. Different habitats within a region contain evolutionary heritage from different epochs depending on the abiotic environment. Global Ecology and Biogeography
12. Pigot, Alex L., and Rampal S. Etienne. "A new dynamic null model for phylogenetic community structure." Ecology letters 18.2 (2015): 153-163.
13. Gallien, L., Saladin, B., Boucher, F. C., Richardson, D. M. and Zimmermann, N. E. (2016), Does the legacy of historical biogeography shape current invasiveness in pines?. New Phytol, 209: 1096–1105.

What explains persistent species' rarity in communities?

Someone asked me what is the most important or lingering issue in community ecology recently. (There’s probably a whole post to answer that question (to come...)). One answer is the mystery of species coexistence: for more than 50 years (from Hutchinson’s paradox of the plankton through today) we have tried to explain the immense and variable diversity on earth by understanding what allows two or more species to coexist. There are many ways to explain coexistence, and yet the details and the specifics for any given system are also still usually incompletely understood.

A good and fascinating example is that of persistent rarity. Why are so many species in communities rare? What allows species to remain rare for long periods of time, given that small populations should be at greater risk for stochastic extinction? A new preprint from Yenni et al. (1) considers the empirical evidence for one potential explanation for persistent rarity: asymmetric negative frequency dependence (see also Yenni et al. 2012 (2)).

Coexistence theory (Chesson 2000) considers stabilizing mechanisms to be those that allow intraspecific competition to be greater than interspecific competition (often defined as ‘niche’ mechanisms). The strength of such stabilizing mechanisms can be estimated by looking at how a species’ population growth rate is limited by the frequency of conspecifics compared to the frequency of heterospecifics in the community. Negative frequency dependence is expected when stabilizing mechanisms are strong. This allows species to increase when rare, since limitation by conspecifics is low, followed by a decline in growth rates as conspecific frequency increases.

Asymmetric negative frequency dependence may explain persistent rarity, since it suggests especially strong conspecific limitation. As a species’ frequency increases, their growth rate greatly declines and intraspecific interactions, rather than interspecific competition, determine abundances. Species are rare, but also less likely to experience extinctions through competition with other species. The authors suggest that as a result of this, we should expect rare species to have stronger negative frequency dependence, in comparison to more common species. They look for evidence for asymmetric frequency dependence using data from 148 communities collected across multiple taxonomic groups (birds, fish, herpetofauna, invertebrates, mammals, and plants), 5 continents, and 3 trophic levels. The data represented time series of species abundances, which the authors used to estimate negative frequency dependence as the relationship between a species’ frequency in the community and their annual per capita population growth rate.

Several aspects of the results are particularly interesting. First, the authors had to omit rare species that are not persistent, since other processes likely explain the presence of such ephemeral members of communities. The frequency of ephemeral species (not stably coexisting at a local scale), for example, was quite high, particularly in plant communities (average of 82 species per community, of which only 22.6 species were on average identified as ‘persistent’). This may suggest the importance of spatial mechanisms for coexistence or co-occurrence. Their overall prediction of stronger negative frequency dependence in rare species appeared to holds in 46% of the communities they examined, consistently for all of the taxonomic groups but one (herps!). Additionally, the opposite pattern (common species having stronger negative frequency dependence) was never observed.

Rarity in nature is common :-) but not well predicted using most coexistence theory. Many interesting and important questions arise from it, and from results like those shown in Yanni et al. For example, do rare species have rare traits or rare niches? Is the frequency dependent growth rate context dependent (i.e. can a species be strongly limited by conspecifics in one environment but not another)?

*Note I haven’t reproduced any figures here, since this is a preprint. However, it is openly available, so do have a look (link 1 below). I’m not certain if there is a rule of thumb on blogging about preprints, but I imagine it is much like blogging about conference talks. The work may not have been peer reviewed/published yet, but the broad results and ideas remain interesting to discuss.

References:

1. Glenda Yenni, Peter Adler, Morgan Ernest. Do persistent rare species experience stronger negative frequency dependence than common species? doi: http://dx.doi.org/10.1101/040360. Preprint.

2. Yenni, Glenda, Peter B. Adler, and S. K. Ernest. "Strong self‐limitation promotes the persistence of rare species." Ecology 93.3 (2012): 456-461.

New ways to address an old idea: rethinking the regional species pool

Like many concepts in ecology (metacommunity, community), the idea of a regional species pool is useful, makes conceptual sense, and is incredibly difficult to apply to real data. Originally, the idea of a species pool came from the theory of island biogeography (MacArthur and Wilson, 1967), where it referred to all the species that could disperse to an island. Today, the regional species pool appears frequently, across null models, studies of community assembly both empirical and theoretical, and metacommunity theory. 

Understanding how particular processes shape community membership—whether the environmental, competition, or dispersal limitation—depends on knowing the identity of all the species that could have potentially assembled there. The species pool as defined by the research provides the frame of reference against which to consider a community's composition. Most null models of community assembly rely on correctly identifying this set of species, and worse, tend to be very sensitive to bias in how the regional pool is defined. If you include all species physically present in a region, in your species pool, environmental filtering may appear to be particularly important simply because many of those species can’t actually survive in your community (the narcissus effect). Given the importance of null models to community ecology, defining the species pool appropriately is an ongoing concern.

There are many decisions that can be made when asking 'which species could potentially be members of a community'? You could include all species that can physically arrive at a site (so only dispersal or geographic distance limits membership), or only include those species that can both arrive and establish (both dispersal and environmental conditions limit membership). Further, the availability of data is key: if you use observational data used to determine the environmental limitations, you may also incorporate the outcome of biotic interactions indirectly. If some species are rare and have low observation likelihoods, they will be under-represented. Abundances may be useful but inaccurate depending on how they are measured. Finally, it is common to define species as either present or not present for a species pool; this binary approach may conceal ecologically important information.

The 'filtering' heuristic for understanding community membership. Species groups 1-3 could each be defined as a regional species pool, depending on the definition applied.

A number of recent papers provide alternative approaches to constructing species pools, meant to avoid these pitfalls. Researchers can define multiple contrasting species pools, each pool representing an ecological process (or perhaps multiple processes) of interest. Each species pool can be modified further to reflect the strength of a particular process in constraining membership. The regional pool is not seen as a single entity but as a number of possible configurations whose utility is in comparison.

Lessard et al. (2016) illustrates how to produce this kind of process-based species pool with various constraints (figure below). Their three-step approach is to:

1. Define absolutely all possible members of regional pool. This is determined by identifying all assemblages in the region containing at least one species also found in the focal community (creating a 'dispersion field') (figure below, section A). This delineates a large region and identifies all species within it.
2. Calculate the probability of resampling a species from the focal community elsewhere in the dispersion field. This is done in the context of the process of interest. For example, the probability of observing a species in the focal community and another community might be determined based on the geographical or environmental distance between those sites. Every site in the dispersion field would now have a probability (or distance really) associated with it, representing some similarity with the focal site.
3. Finally, apply constraints to the calculated probabilities. You might choose to consider only the species within communities that are at least 50% similar to the focal community, for example. Such constraints would reflect the strength or importance of filtering by the process of interest.

Another recent paper (Karger et al., 2016) takes an approach with a number of commonalities to the Lessard et al. method. However, rather than resampling to produce potential pools of species (with species being defined as present or absent), they advocate a probabilistic approach to species pools. They suggest that species pools should be thought of as a set of probabilities of membership, which may be more reflective of ecological reality. In some ways, this is a simply a formalization of probabilistic sampling from Lessard, but instead of applying constraints, the researcher acknowledges that probabilities vary for different species. “Hence, a species pool can simply be defined as a function of probabilities of a species’ occurrence in the focal unit given the unit’s environmental and biotic conditions, geographical location and the time frame of interest”.

Both comparative and probabilistic approaches to defining species are logical advances, and one way of dealing with the untidy concept of the species pool. If this topic is of interest, a few other papers, albeit slightly less recent, are definitely worth reading: Pigot and Etienne 2015; Lessard et al. 2012, Carsten et al., 2013.

From Lessard et al., 2016. The three steps to build a species pool.

Have humans altered community interactions?

A recent Nature paper argues that there is evidence for human impacts on communities starting at least six thousand years ago, which altered the interactions that structure communities. “Holocene shifts in the assembly of plant and animal communities implicate human impacts” from Lyons et al. (2016, Nature) analyses data spanning modern communities through to 300 million year old fossils, to measure how the co-occurrence structure of communities has changed. The analyses look at the co-occurrence of pairs of species, and identifies those that are are significantly more likely ('aggregation') or less likely ('segregation') than a null expectation. Once the authors identified the species pairs with non-random co-occurrences, they calculated the proportion of these that were aggregated (i.e. y-axis on Figure 1). Compared to the ancient past, the authors suggest that modern species had fewer aggregated species pairs than in the past, perhaps reflecting an increase in negative interactions or distinct habitat preferences. 

Main figure from Lyons et al. 2016.

The interpretation offered by the paper is “[o]ur results suggest that assemblage co-occurrence patterns remained relatively consistent for 300 Myr but have changed over the Holocene as the impact of humans has dramatically increased.” and "...that the rules governing the assembly of communities have recently been changed by human activity". 

There are many important and timely issues related to this – changing processes in natural systems, lasting human effects, the need to use all available data from across scales, the value of cross-disciplinary collaboration. But, in my view, the paper ignores a number of the assumptions and considerations that are essential to community ecology. There are a number of statistical issues that others have pointed out (e.g. temporal autocorrelation, use of loess regression, null model questions), but a few in particular are things I was warned about in graduate courses. Such as the peril of proportions as response data (Jackson 1997), and the collapsing of huge amounts of data into an analysis of a summary of the data ("the proportion of significant pairwise associations that are aggregated"). Beyond the potential issues with calculating correct error terms, interpretation is made much more difficult for the reader. 

Most importantly, in my view, the Nature paper commits the sin of ignoring the essential role of scale in community ecology. A good amount of time and writing has been spent reconciling issues of spatial and temporal scale in ecology. These concepts are essential even to the definition of a 'community'. And yet, scale is barely an afterthought for these analyses.  (Sorry, perhaps that's a bit over-dramatic....) Fossils—undeniably an incomplete and biased sample of the an assemblage—can't be described to more than a very broad spatial and temporal scale. E.g. a 2 million year old fossil and a 2.1 million year old fossil may or may not have interacted, habitats may have varied between those times, and populations of S1 and S2 may well have differed greatly over a few thousand years. Compare this to modern data, which represents species occurring at the exact same time and in relatively small areas. The differences in scale is huge, and so these data are not directly comparable.

Furthermore, because we know that scale matters, we might predict that co-occurrences should increase at larger spatial grains (you include more habitat, so more species with the same broad requirements will be routinely found in a large area). But the authors reported that they found no significant relationship between dataset scale and the degree of aggregation observed (their Figure 2, not replicated here): this might suggest the methodology or analyses needs further consideration. Co-occurrence data is also, unfortunately, a fairly weak source of inference for questions about community assembly, without other data. So while the questions remain fascinating to me - is community assembly changing fundamentally over time? is that a frequent occurrence or driven by humans? what did paleo-communities look like? - I think that the appropriate data and analyses to answer these questions are not so easy to find and apply.


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Response from Brian McGill:

My comment I was trying to post was:

Interesting perspective Caroline! As a coauthor, I of course am bound to disagree. I'll keep it short, but 3 thoughts:

1) The authors definitely agonized over potential confounding effects. Indeed spent over a year on it. In my experience paleoecologists default to assuming everything is an artefact in their data until they can convince themselves otherwise, much more than neo-ecologists do.

2) They did analyze the effects of scale (both space and time) and found it didn't seem to have much effect at all on the variable of interest (% aggregations). You interpret this as "this might suggest the methodology or analyses needs further consideration". But to me, I hardly think we know enough about scaling of species interactions to reject empirical data when it contradicts our very limited theoretical knowledge (speculation might be a better word) of how species interactions scale.

3) To me (and I think most of the coauthors) by far the most convincing point is that the pattern (a transition around 8000 years ago plus or minus after 300,000,000 years of constancy) occurs WITHIN the two datasets that span it (pollen of North America and mammal bones of North America both span about 20,000 years ago to modern times) and they have consistent taphonomies, sampling methods, etc and yet both show the transition.

I agree that better data without these issues is difficult (impossible?) to find. The question is what you do with that. Do you not anwwer certain questions. Or do you do the best you can and put it it out for public assessment. Obviously I side with the latter.

Thanks for the provoking commentary.

Cheers

Brian

Does context alter the dilution effect?

Understanding disease and parasites from a community context is an increasingly popular approach and one that has benefited both disease and ecological research. In communities, disease outbreaks can reduce host populations, which will in turn alter species' interactions and change community composition, for example. Community interactions can also alter disease outcomes - decreases in diversity can incr-

Frogs in California killed by the chytrid fungus
(source: National Geographic News)

ease disease risk for vulnerable hosts, a phenomenon known as the dilution effect. For example, in a high diversity system, a mosquito may bite individuals from multiple resistant species as well as those from a focal host, potentially reducing the frequency of focal host-parasite contact. Hence the dilution effect may be a potential benefit of biodiversity, and multiple recent studies provide evidence for its existence.

Not all recent studies support this diversity-disease risk relationship, however, and it is not clear whether the dilution effect might depend on spatial scale, the definition of disease risk used, or perhaps the system of study. A recent paper in Ecology Letters from Alexander Strauss et al. does an excellent job of deconstructing the assumptions and implicit models behind the dilution effect and exploring whether context dependence might explain some of the variation in published results. The authors develop theoretical models capturing hypothesized mechanisms, and then use these to predict the outcomes of mesocosm experiments.

Suggested mechanisms behind the dilution effect include 1) that diluter species (i.e. not the focal host) reduce parasite encounters for focal hosts, with little or no risk to themselves (resistant); and 2) diluters may compete for resources or space against the focal host and so reduce the host population, which should in turn reduce density dependent disease risk. But, if these are the mechanisms, there are a number of corollaries that should not be ignored. For example, what if the diluter species is the poorer competitor and so competition reduces diluter populations? What if diluter species aren't completely resistant to disease and at large populations are susceptible? The cost/benefit analysis of having additional species present may differ depending on any number of factors in a system.

The authors focus on a relatively simple system - a host species Daphnia dentifera, a virulent fungus Metschnikowia bicuspidata, and a competitor species Ceriodaphnia sp.. Observations suggest that epidemics in the Daphnia species may smaller where the second species occurs - Ceriodaphnia removes spores when filter feeding and also competes for food. By measuring a variety of traits, they could estimate the R* and R0 values - roughly, low R* values indicated strong competitors and high  R0 values indicated groups that have high disease transmission rates. Context dependence is introduced by considering three different genotypes of the Daphnia: these genotypes varied in R* and R0 values, allowing them to test whether changing competitive ability and disease transmission in the Daphnia might alter the strength or even presence of a dilution effect. Model predictions were then tested directly against matching mesocosm experiments.

The results show clear evidence of context dependence in the dilution effect (and rather nice matches between model expectations and mesocosm data). Three possible scenarios are compared, which differ in the Daphnia host genotype and its competitive and transmission characteristics. 

1. Dilution failure: the result of a host genotype that is a strong competitor, and a large epidemic (low R*, high R0). 
2. Dilution success: the result of a host that is a weak competitor and a moderate epidemic (host has high R*, moderate R0). 
3. Dilution irrelevance: the outcome of a host that is a weak competitor, and a small epidemic (high R*, low R0). 

From Strauss et al. 2015. The y-axis shows percent host population infected, solid lines show the disease prevalence without the diluter; dashed show host infection when diluter is present.

Of course, all models are simplifications of the real world, and it is possible that in more diverse systems the dilution effect might be more difficult to predict. However, as competition is a component of most natural systems, its inclusion may better inform models of disease risk. Other models for other systems might suggest different outcomes, but this one provides a robust jumping off point for future research into the dilution effect.

Alexander T. Strauss, David J. Civitello, Carla E. Caceres and Spencer R. Hall. 2015. Success, failure and ambiguity of the dilution effect among competitors. Ecology Letters. 18: 916–926. 

Ecology in evolutionary times

Ecological and evolutionary perspectives on community assembly. 2015. Gary G. Mittelbach, Douglas W. Schemske. Trends in Ecology and Evolution.

Phylogenetic patterns are not proxies of community assembly mechanisms (they are far better). 2015. Pille Gerhold, James F. Cahill Jr, Marten Winter, Igor V. Bartish and Andreas Prinzing. Functional Ecology

Community assembly has always provided some of the most challenging puzzles for ecologists. Communities are complex, vaguely delimited, involve multi-species interactions, and assemble with seemingly immense variation. Thousands of papers have been dedicated to understanding community assembly, and many have proposed different approaches understanding communities. These range from the ever popular abiotic/biotic filtering concept, functional traits, coexistence theory, island biogeography, metacommunity theory, neutral theory, and phylogenetic patterns. It is probably fair to say that no one existing approach is adequate to completely describe or predict community assembly.

One response to this problem is the growing demand to expand the lens of “community” to cover greater spatial and temporal scales. This owes a lot, directly and indirectly, to Robert Ricklefs’ influential Sewall Wright Award lecture on the Disintegration of the Ecological Community. There is also a strong trend towards re-integrating evolutionary history into studies of community ecology. Coincidentally, or perhaps not, this is occurring as so-called ‘eco-phylogenetic’ approaches have been increasingly criticised. If nothing else, eco-phylogenetics provided a path for, and popularized, the idea of reintegrating evolution into community ecology.

I’ll highlight two particular papers that address this re-integration in surprisingly convergent ways. Both have macroevolution slants (that is, they focus on the impacts and drivers of speciation and extinction, sympatry, allopatry, etc), and an interest in the feedbacks between community interactions and these processes. The first, from Pille Gerhold, James F. Cahill Jr, Marten Winter, Igor V. Bartish and Andreas Prinzing, positions itself as the phoenix from the ashes of eco-phylogenetics (as seen in their particularly enthusiastic title :) ). Evolutionary history, captured by phylogenies, was originally of interest to ecologists not for what it was, but because it could (sometimes, maybe) act as a proxy for species traits and niches. This paper does an excellent job of laying out the various hypotheses that went behind this type of approach and showing why they are not reliably true. If for no other reason, it is worth reading the paper for its clear critique of the foundation of eco-phylogenetics. Using patterns in phylogenies as proxies for the outcomes of particular ecological processes being clearly suspect, the authors argue that explicitly thinking of phylogenetic patterns as the result of both ecological and evolutionary processes is far more informative. [I’ll return to this in a bit with their examples below].

The second paper is written by two big names in their respective fields: Gary Mittlebach (ecology) and Doug Schemske (evolution). The title is a bit vague (“Ecological and evolutionary perspectives on community assembly”), but it turns out that they too have converged on the importance of considering evolutionary history in order to understand community assembly. In particular they focus on the problematic nature of the species pool: species pools are nearly always treated as a static object changing little through time or space and are notoriously difficult to define. However, the species pool underlies null model approaches used to test communities for differences from a random expectation. So defining it correctly is important.

From the early days, Elton and others defined the species pool as the group of species that can disperse to and colonize a community. However, the species pool may be dynamic, and they note “To date, relatively little attention has been focused on the feedback that occurs between local community species composition, biotic interactions, and the diversification processes that generate regional species pools.”

This paper does an excellent job of explaining how macroevolutionary processes can alter a regional species pool. The most obvious example is the process of adaptive radiation in island-like systems, where competition for resources drives ecological divergence and speciation. Darwin’s finches, Anolis lizards, and cichlid fishes provide well-known examples of this rapid expansion of the species pool through inter-specific interactions. On mainland systems, speciation may be more likely to occur in allopatry, and the rate limiting step for range expansion (leading to secondary sympatry and only then increasing a species pool) is often interspecific interactions. One study found that secondary sympatry took 7my on average, though speciation alone took only 3my. So the species pool is the outcome of constant feedbacks between species interactions and evolutionary processes.

From Mittlebach & Schemske. Figure illustrating the feedbacks between evolution and ecological interactions, in producing the species pool.

Both papers provide useful examples of how such incorporating evolution into community ecology may prove useful. As a simple example, Mittlebach and Schemske point out that evolution can greatly alter the utility of Island Biogeography Theory: given enough time, speciation events including adaptive radiations, greatly increase the (non-mainland) species pool and would strongly alter predictions of diversity, especially for distant islands.

The Gerhold et al. paper provides the below illustrations as additional possibilities for how evolution and community interactions may feedback.

From Gerhold et al. Two examples of how evolution and communities might interact.

It is certainly interesting to see this shift towards how we envision and study communities. The historical focus on local space and time no doubt reflects ecologists' attempt to limit the problem to a manageable frame. But there is some logic behind expanding our definition of communities to larger spatial scales and greater time periods, especially since there are usually no true boundaries defining communities in space and time. Answering which specific time scales and spatial scales most useful to understanding communities is difficult: if we increase the time or space we consider, how and when does the additional information provided decline? The next step is to consider evolution in this fashion for real organisms, and evaluate the true utility of this approach.  

Equalizing and stabilizing traits?

Plant functional traits and the multidimensional nature of species coexistence. 2015. Nathan J. B. Kraft, Oscar Godoy, and Jonathan M. Levine. PNAS.

(This isn’t a brand new paper, but somehow I’m already behind on reading papers in the new year...) 

A recent paper from Kraft et al. in PNAS does a really nice job in filling a gap that has been in literature for a while, which is to extend the influential theoretical work on coexistence from Chesson (and extended more recently by Jonathan Levine et al.) to explicitly incorporate functional traits and trait-based approaches to ecology. Chesson’s work (particularly ARES 2000) lays out a framework for understanding coexistence and competitive interactions, which focuses on the importance of stabilizing effects (niche differences) and equalizing effects (fitness differences) between competing species (e.g.). This theory makes strong predictions of when and how coexistence is expected (for example, when species have strong enough niche differences). However, accurate application of the theory is somewhat difficult, perhaps because identifying and calculating niche and fitness differences requires heavy use of mathematical models and careful experimental design.

In contrast, the value of the focus on functional traits in ecology is that they are readily measured, easily conceptualized, and databases of values already exist. In common with equalizing/stabilizing effects, traits are meant to inform our understanding of species' niches, but in contrast, traits are empirically friendly. One of the more common critiques of the Chesson framework was that empirical measures, particularly traits, couldn't be shoehorned into it. After all, traits likely contribute to both equalizing and stabilizing forces in complicated ways that may well shift during a species' life.

What Nathan Kraft and coauthors have done is show that this is not a limitation - traits can contribute to both equalizing and stabilizing forces, and mathematical models can tease these effects apart. They relate detailed measurements of leaf, root, seed and whole plant traits for 18 California annual plants with the results of mathematical models of competition and coexistence between these species. The authors found strong and exciting relationships between the theoretically motivated measures of competitive processes and species' traits. Average fitness differences had significant correlations with functional traits, particularly maximum height, leaf [N], leaf area, rooting depth, and phenology.

From Kraft et al. 2015: Correlations between species traits and A) Stabilizing niche differences, and B) Average fitness differences.
The key to interpreting these plots is to understand that where the coloured line overlaps with the grey shading, the correlation is not different than the null model. When the line is between the null and the center of the figure, the correlation is significant and negative; where it is between the null and the external edge, the correlation is significant and positive.

No individual traits correlated with niche differences, but models including multiple traits considered together do correlate with niche differences. A rather nice bit of support for the multidimensional view of the niche.

This paper does a nice job of expanding Chesson's framework a little bit farther towards empirical applications. Further, it reinforces the value of trait approaches. There are still some important limitations - the first is that this particular system of annual plants has been studied in great detail. It seems unlikely that the traits identified in this paper can necessarily be generalized as "equalizing" traits. A trait with an equalizing effect in a California grassland may well contribute less to fitness in a desert system, for example. Perennial species are altogether less integrated into experimental applications of Chesson's framework (life time fitness, among other things, being much easier to capture in annual plants). But this paper is a suggestion of a useful way forward, albeit a way that requires much more data and careful experimentation. The authors acknowledge that more study is due, but also the potential: “These complex relationships argue against the simple use of single traits to infer community assembly processes but lay the foundation for a theoretically robust trait-based community ecology.”

A changing world: Themes from the 2014 BES-SFE meeting in Lille #BESSfe

I attended the joint British Ecological Society/Société Française d’Ecologie (BES/SFE) meeting held in Lille, France, Dec. 9-12. I quite enjoy BES meetings, but this one felt just a little more dynamic and exciting. The meeting did a great job of bringing people together who otherwise might not attend the same meetings. The overall quality of talks was excellent and the impression was that labs were presenting their best, most exciting results. One thing that always fascinates me about meetings is the fact that emergent themes arise that reflect what people are currently excited about. Over the three days of talks, I felt that three emergent themes seemed particularly strong among the talks I attended:

1) Pollinators in a changing world

Photo by Marc Cadotte

There were a surprising number of talks focusing on human-caused changes to landscapes affect pollinator abundance and diversity. I am an Editor of a British Journal (Journal of Applied Ecology) and work on pollinator diversity has always been stronger in the UK, but there were just so many talks that it is obvious that this is an important issue for many people in the UK and Europe. Nick Isaac examined whether butterfly abundance was related to the abundance of host plants –which should be a measure of habitat quality. Plants that serves as hosts for caterpillars were more important than those that supply nectar to adults, presumably because the adults can better find resources. And specialist species were especially sensitive to host plant diversity.

Adriana De Palma gave a great talk on reanalyzing global patterns of bee responses to land-use and showed that biases in where research is done is influencing generalities. Bee communities in some well-studied regions appear more sensitive to land-use change and those regions with many bumblebees mask effects that on other types of bees. Bill Kunin examined patterns at a regional scale (UK) where a pollinator crisis was identified in the late 2000s and causes have been attributed to everything from land-use change to pesticide use to cell phones -to the second coming of Jesus. Habitat quality and flora resources do not seem to be that important at large scales, but there seems to be a strong effect of pesticide use. But at a smaller landscape scale, Florence Hecq showed that habitat heterogeneity within agricultural landscapes and the size of semi-natural grasslands were important for maintaining pollinator diversity. Changes in pollinator diversity have consequences for crop yield, as shown nicely by Colin Fontaine.

Photo by Marc Cadotte

 In a really interesting study, Olivia Norfolk showed that traditional agriculture practices by Bedouin minorities in Egypt enhanced pollinator abundance. Because their agricultural practices support high plant diversity, both wild and domestic plant species, pollinators fare better than in intense agriculture. Moreover, one of the most important crops, almonds, sees higher yield with higher plant diversity –though this effect is lost when there are a lot of introduced honeybees.

2) Effects of land-use on biodiversity

A number of other talks examined how human-caused changes influence biodiversity patterns and resulting functions across a number of taxa. Jonathan Tonkin examined a number of different types of species (plants, beetles, spiders, etc.) that occur along riparian habitats and showed that there weren’t concordant changes in richness, but there were simultaneous shifts in composition. Human stressed caused multiple communities to shift to very nonrandom community types. In Agricultural systems, Colette Bertrand showed that agriculture that changed frequently (e.g., crop rotation) supported more beetle species that systems where the same crops are planted year after year.

Human deforestation greatly changes many biodiversity patterns and we need to better understand these make sound conservation decisions. Cecile Albert examined land-use change and fragmentation in southern Quebec and showed that we can determine the importance of forest patches in human-dominated landscapes for the ability of species to move between large forested areas. Using her model she can identify where conservation and habitat protection should be focused. Nicolas Labriere studied how different forest changes influenced the delivery of ecosystem services, including carbon storage, diversity and soil retention. He showed that only intact forests were able to maximally deliver all ecosystem services.

 

From WWF

3) Species differences and dynamics at different scales

A major theme is how species differences are important for ecological processes, ecosystem function and conservation. I’ve argued elsewhere that we are heading into a paradigm shift in ecology, where we've moved from counting species to accounting for species. Wilfried Thuiller asked how well European reserves conserve different forms of biodiversity, namely functional and phylogenetic diversity. He prioritized species by their distinctiveness and range size so that the most important were functionally or phylogenetically unique and have a small range. Distinct mammals tend to not be well protected and the modern reserve system does not maximally protect biodiversity. This is most acute in eastern Europe where there is a order of magnitude less protected area than in western Europe.

Georges Kunstler argued that trait approaches to understanding competition are valuable because they can reduce the dimensionality of students, from all pairwise species interactions to relative simple measures of trait differences. He showed, using an impressive global forest dataset, that competition appears stronger when neighbour trees are more similar in their traits.

A number of talks examined if measures of species differences can explain biodiversity patterns. At very large scales, Kyle Dexter showed that phylogenetic diversity does not explain where species are across the neotropics. In some places species are in the same habitat as a close relative and sometimes with a distant relative. At smaller scales, talks explored trait or phylogenetic patterns Andros Gianuca, Anne Pilière and Lars Götzenberger all assessed the relative contributions of trait and phylogenetic differences to explain community patterns and all showed that phylogeny may be a stronger explanation than the traits they measured.

4) Species dynamics, coexistence and ecosystem function

Understanding tree growth and dispersal are key to predicting how forests will respond to environmental change and to successfully managing and conserving them. Sean MacMahon showed that the seasonality of tree growth is critical to modelling carbon flux in forests. He developed an ingenious set of modelling approaches to analyze daily tree diameter change and showed that growth is highly concentrated in the middle of the growing season, which is at odds with traditional conceptual models where tree growth is constant from spring to fall. Noelle Beckman examined tree dispersal and the consequence of losing vertebrate seed dispersers. She showed that reducing the number of seed dispersers results in low seeding survival because seedlings are locally very dense, instead of being dispersed, and seed predators and other enemies have an easier time finding them.

The mechanism most often cited by plant community ecologists is competition, but Christian Damgaard states that this simple mechanism is almost never tested. Further, models of competition are often based on numbers of individuals, but plants make such counts notoriously difficult. Instead he developed a very elegant model showing how plant height and horizontal cover feedback to competition. What he calls vertical density is a predictor of the following season’s horizontal cover. Competition is also key to observing a relationship between species richness and ecosystem function. Rudolf Rohr showed, using a series of Lotka-Volterra models that randomly assembling communities always results in a positive relationship between richness and function –which is why experiments often support this pattern. In natural communities, this relationship often disappears, and he shows that simulations with competitive sorting break this relationship.

Finally, Florian Altermatt examined whether the physical structure of stream networks influences the distribution of diversity in streams using protozoan and bacterial communities in series of connected tubes that look like a branch, and compared these to linear tubes. He found that diversity is highest in the interior branches (see image to the left), much like real rivers, and the linear system had no such pattern of diversity. He attributed part of this diversity gradient to competitive differences among species and differences in movement of the organisms.