Should I stay or should I go? Coral bleaching from the symbionts' perspective.

Coral bleaching, the stress-induced breakdown of coral-algal symbiosis, threatens reefs globally. Paradoxically, despite adverse fitness effects, corals bleach annually, even outside of abnormal temperatures. This generally occurs shortly after the once-per-year mass coral spawning. Here, we propose a hypothesis linking annual coral bleaching and the transmission of symbionts to the next generation of coral hosts. We developed a dynamic model with two symbiont growth strategies, and found that high sexual recruitment and low adult coral survivorship and growth favour bleaching susceptibility, while the reverse promotes bleaching resilience. Otherwise, unexplained trends in the Indo-Pacific align with our hypothesis, where reefs and coral taxa exhibiting higher recruitment are more bleaching susceptible. The results from our model caution against interpreting potential shifts towards more bleaching-resistant symbionts as evidence of climate adaptation-we predict such a shift could also occur in declining systems experiencing low recruitment rates, a common scenario on today's reefs.

Pervasive within-species spatial repulsion among adult tropical trees.

For species to coexist, performance must decline as the density of conspecific individuals increases. Although evidence for such conspecific negative density dependence (CNDD) exists in forests, the within-species spatial repulsion it should produce has rarely been demonstrated in adults. In this study, we show that in comparison to a null model of stochastic birth, death, and limited dispersal, the adults of dozens of tropical forest tree species show strong spatial repulsion, some to surprising distances of approximately 100 meters. We used simulations to show that such strong repulsion can only occur if CNDD considerably exceeds heterospecific negative density dependence-an even stronger condition required for coexistence-and that large-scale repulsion can indeed result from small-scale CNDD. These results demonstrate substantial niche differences between species that may stabilize species diversity.

The ecological causes of functional distinctiveness in communities.

Recent work has shown that evaluating functional trait distinctiveness, the average trait distance of a species to other species in a community offers promising insights into biodiversity dynamics and ecosystem functioning. However, the ecological mechanisms underlying the emergence and persistence of functionally distinct species are poorly understood. Here, we address the issue by considering a heterogeneous fitness landscape whereby functional dimensions encompass peaks representing trait combinations yielding positive population growth rates in a community. We identify four ecological cases contributing to the emergence and persistence of functionally distinct species. First, environmental heterogeneity or alternative phenotypic designs can drive positive population growth of functionally distinct species. Second, sink populations with negative population growth can deviate from local fitness peaks and be functionally distinct. Third, species found at the margin of the fitness landscape can persist but be functionally distinct. Fourth, biotic interactions (positive or negative) can dynamically alter the fitness landscape. We offer examples of these four cases and guidelines to distinguish between them. In addition to these deterministic processes, we explore how stochastic dispersal limitation can yield functional distinctiveness. Our framework offers a novel perspective on the relationship between fitness landscape heterogeneity and the functional composition of ecological assemblages.

Plant community impact on productivity: Trait diversity or key(stone) species effects?

Outside controlled experimental plots, the impact of community attributes on primary productivity has rarely been compared to that of individual species. Here, we identified plant species of high importance for productivity (key species) in >29,000 diverse grassland communities in the European Alps, and compared their effects with those of community-level measures of functional composition (weighted means, variances, skewness and kurtosis). After accounting for the environment, the five most important key species jointly explained more deviance of productivity than any measure of functional composition alone. Key species were generally tall with high specific leaf areas. By dividing the observations according to distinct habitats, the explanatory power of key species and functional composition increased and key-species plant types and functional composition-productivity relationships varied systematically, presumably because of changing interactions and trade-offs between traits. Our results advocate for a careful consideration of species' individual effects on ecosystem functioning in complement to community-level measures.

Global distribution and conservation status of ecologically rare mammal and bird species.

Identifying species that are both geographically restricted and functionally distinct, i.e. supporting rare traits and functions, is of prime importance given their risk of extinction and their potential contribution to ecosystem functioning. We use global species distributions and functional traits for birds and mammals to identify the ecologically rare species, understand their characteristics, and identify hotspots. We find that ecologically rare species are disproportionately represented in IUCN threatened categories, insufficiently covered by protected areas, and for some of them sensitive to current and future threats. While they are more abundant overall in countries with a low human development index, some countries with high human development index are also hotspots of ecological rarity, suggesting transboundary responsibility for their conservation. Altogether, these results state that more conservation emphasis should be given to ecological rarity given future environmental conditions and the need to sustain multiple ecosystem processes in the long-term.

Counting niches: Abundance-by-trait patterns reveal niche partitioning in a Neotropical forest.

Tropical forests challenge us to understand biodiversity, as numerous seemingly similar species persist on only a handful of shared resources. Recent ecological theory posits that biodiversity is sustained by a combination of species differences reducing interspecific competition and species similarities increasing time to competitive exclusion. Together, these mechanisms counterintuitively predict that competing species should cluster by traits, in contrast with traditional expectations of trait overdispersion. Here, we show for the first time that trees in a tropical forest exhibit a clustering pattern. In a 50-ha plot on Barro Colorado Island in Panama, species abundances exhibit clusters in two traits connected to light capture strategy, suggesting that competition for light structures community composition. Notably, we find four clusters by maximum height, quantitatively supporting the classical grouping of Neotropical woody plants into shrubs, understory, midstory, and canopy layers.

Generalizing clusters of similar species as a signature of coexistence under competition.

Patterns of trait distribution among competing species can potentially reveal the processes that allow them to coexist. It has been recently proposed that competition may drive the spontaneous emergence of niches comprising clusters of similar species, in contrast with the dominant paradigm of greater-than-chance species differences. However, current clustering theory relies largely on heuristic rather than mechanistic models. Furthermore, studies of models incorporating demographic stochasticity and immigration, two key players in community assembly, did not observe clusters. Here we demonstrate clustering under partitioning of resources, partitioning of environmental gradients, and a competition-colonization tradeoff. We show that clusters are robust to demographic stochasticity, and can persist under immigration. While immigration may sustain clusters that are otherwise transient, too much dilutes the pattern. In order to detect and quantify clusters in nature, we introduce and validate metrics which have no free parameters nor require arbitrary trait binning, and weigh species by their abundances rather than relying on a presence-absence count. By generalizing beyond the circumstances where clusters have been observed, our study contributes to establishing them as an update to classical trait patterning theory.

Emergent niche structuring leads to increased differences from neutrality in species abundance distributions.

Species abundance distributions must reflect the dynamic processes involved in community assembly, but whether and when specific processes lead to distinguishable signals is not well understood. Biodiversity and species abundances may be shaped by a variety of influences, but particular attention has been paid to competition, which can involve neutral dynamics, where competitor abundances are governed only by demographic stochasticity and immigration, and dynamics driven by trait differences that enable stable coexistence through the formation of niches. Key recent studies of the species abundance patterns of communities with niches employ simple models with pre-imposed niche structure. These studies suggest that species abundance distributions are insensitive to the relative contributions of niche and neutral processes, especially when diversity is much higher than the number of niches. Here we analyze results from a stochastic population model with competition driven by trait differences. With this model, niche structure emerges as clumps of species that persist along the trait axis, and leads to more substantial differences from neutral species abundance distributions than have been previously shown. We show that heterogeneity in "between-niche" interaction strength (i.e., in the strength of competition between species in different niches) plays the dominant role in shaping the species abundances along the trait axis, acting as a biotic filter favoring species at the centers of niches. Furthermore, we show that heterogeneity in "within-niche" interactions (i.e., in the competition between species in the same niche) counteracts the influence of heterogeneity in "between-niche" interactions on the SAD to some degree. Our results suggest that competitive interactions that produce niches can also influence the shapes of SADs.

Translucent windows: how uncertainty in competitive interactions impacts detection of community pattern.

Traits can provide a window into the mechanisms that maintain coexistence among competing species. Recent theory suggests that competitive interactions will lead to groups, or clusters, of species with similar traits. However, theoretical predictions typically assume complete knowledge of the map between competition and measured traits. These assumptions limit the plausible application of these patterns for inferring competitive interactions in nature. Here, we relax these restrictions and find that the clustering pattern is robust to contributions of unknown or unobserved niche axes. However, it may not be visible unless measured traits are close proxies for niche strategies. We conclude that patterns along single niche axes may reveal properties of interspecific competition in nature, but detecting these patterns requires natural history expertise firmly tying traits to niches.

Biodiversity maintenance may be lower under partial niche differentiation than under neutrality.

Niche differentiation is normally regarded as a key promoter of species coexistence in competitive systems. One might therefore expect that relative to neutral assemblages, niche-differentiated communities should support more species with longer persistence and lower probability of extinction. Here we compare stochastic niche and neutral dynamics in simulated assemblages, and find that when local dynamics combine with immigration from a regional pool, the effect of niches can be more complex. Trait variation that lessens competition between species will not necessarily give all immigrating species their own niche to occupy. Such partial niche differentiation protects certain species from local extinction, but precipitates exclusion of others. Differences in regional abundances and intrinsic growth rates have similar impacts on persistence times as niche differentiation, and therefore blur the distinction between niche and neutral dynamical patterns-although niche dynamics will influence which species persist longer. Ultimately, unless the number of niches available to species is sufficiently high, niches may actually heighten extinction rates and lower species richness and local persistence times. Our results help make sense of recent observations of community dynamics, and point to the dynamical observations needed to discern the influence of niche differentiation.

Can Clustering in Genotype Space Reveal "Niches"?

Community ecology lacks the success enjoyed by population genetics to quantify the relative roles played by deterministic and stochastic processes. It has been proposed that clustered patterns of abundance in genotype space provide evidence of selection in microbial communities, since no such clustering would arise in the absence of selection. We critique this test for its unrealistic null hypothesis. We show mathematically and with simulations that point mutations alone lead to clustering in genotype space by causing correlations between abundances of similar genotypes. We also show potential deviations from the mutation-only pattern caused by immigration from a source pool. Clustered patterns in genotype space may still be revealing of selection if analyzed quantitatively but only if neutral and selective regimes can be distinguished once mutation and immigration are included in the null model.

Sensitivity analysis of coexistence in ecological communities: theory and application.

Sensitivity analysis, the study of how ecological variables of interest respond to changes in external conditions, is a theoretically well-developed and widely applied approach in population ecology. Though the application of sensitivity analysis to predicting the response of species-rich communities to disturbances also has a long history, derivation of a mathematical framework for understanding the factors leading to robust coexistence has only been a recent undertaking. Here we suggest that this development opens up a new perspective, providing advances ranging from the applied to the theoretical. First, it yields a framework to be applied in specific cases for assessing the extinction risk of community modules in the face of environmental change. Second, it can be used to determine trait combinations allowing for coexistence that is robust to environmental variation, and limits to diversity in the presence of environmental variation, for specific community types. Third, it offers general insights into the nature of communities that are robust to environmental variation. We apply recent community-level extensions of mathematical sensitivity analysis to example models for illustration. We discuss the advantages and limitations of the method, and some of the empirical questions the theoretical framework could help answer.

Fixed point sensitivity analysis of interacting structured populations.

Sensitivity analysis of structured populations is a useful tool in population ecology. Historically, methodological development of sensitivity analysis has focused on the sensitivity of eigenvalues in linear matrix models, and on single populations. More recently there have been extensions to the sensitivity of nonlinear models, and to communities of interacting populations. Here we derive a fully general mathematical expression for the sensitivity of equilibrium abundances in communities of interacting structured populations. Our method yields the response of an arbitrary function of the stage class abundances to perturbations of any model parameters. As a demonstration, we apply this sensitivity analysis to a two-species model of ontogenetic niche shift where each species has two stage classes, juveniles and adults. In the context of this model, we demonstrate that our theory is quite robust to violating two of its technical assumptions: the assumption that the community is at a point equilibrium and the assumption of infinitesimally small parameter perturbations. Our results on the sensitivity of a community are also interpreted in a niche theoretical context: we determine how the niche of a structured population is composed of the niches of the individual states, and how the sensitivity of the community depends on niche segregation.

Predator attack rate evolution in space: the role of ecology mediated by complex emergent spatial structure and self-shading.

Predation interactions are an important element of ecological communities. Population spatial structure has been shown to influence predator evolution, resulting in the evolution of a reduced predator attack rate; however, the evolutionary role of traits governing predator and prey ecology is unknown. The evolutionary effect of spatial structure on a predator's attack rate has primarily been explored assuming a fixed metapopulation spatial structure, and understood in terms of group selection. But endogenously generated, emergent spatial structure is common in nature. Furthermore, the evolutionary influence of ecological traits may be mediated through the spatial self-structuring process. Drawing from theory on pathogens, the evolutionary effect of emergent spatial structure can be understood in terms of self-shading, where a voracious predator limits its long-term invasion potential by reducing local prey availability. Here we formalize the effects of self-shading for predators using spatial moment equations. Then, through simulations, we show that in a spatial context self-shading leads to relationships between predator-prey ecology and the predator's attack rate that are not expected in a non-spatial context. Some relationships are analogous to relationships already shown for host-pathogen interactions, but others represent new trait dimensions. Finally, since understanding the effects of ecology using existing self-shading theory requires simplifications of the emergent spatial structure that do not apply well here, we also develop metrics describing the complex spatial structure of the predator and prey populations to help us explain the evolutionary effect of predator and prey ecology in the context of self-shading. The identification of these metrics may provide a step towards expansion of the predictive domain of self-shading theory to more complex spatial dynamics.

How specialised must natural enemies be to facilitate coexistence among plants?

The Janzen-Connell hypothesis proposes that plant interactions with host-specific antagonists can impair the fitness of locally abundant species and thereby facilitate coexistence. However, insects and pathogens that associate with multiple hosts may mediate exclusion rather than coexistence. We employ a simulation model to examine the effect of enemy host breadth on plant species richness and defence community structure, and to assess expected diversity maintenance in example systems. Only models in which plant enemy similarity declines rapidly with defence similarity support greater species richness than models of neutral drift. In contrast, a wide range of enemy host breadths result in spatial dispersion of defence traits, at both landscape and local scales, indicating that enemy-mediated competition may increase defence-trait diversity without enhancing species richness. Nevertheless, insect and pathogen host associations in Panama and Papua New Guinea demonstrate a potential to enhance plant species richness and defence-trait diversity comparable to strictly specialised enemies.

Revising the tolerance-fecundity trade-off; or, on the consequences of discontinuous resource use for limiting similarity, species diversity, and trait dispersion.

The recently proposed tolerance-fecundity trade-off model represents a step forward in the study of seed size diversity in plant communities. However, it uses an oversimplified picture of seed tolerance, with an infinitely sharp threshold: the probability that a seed tolerate a given stress level is either 1 or 0. This invites a revision of the model, presented here. We demonstrate that this simplification has large impacts on model behavior, including altering predictions regarding limiting similarity, raising expected diversity levels, and lessening expected spacing between species along the trait axis. Such dramatic impacts ultimately stem from the fact that a discontinuity in the probability of tolerating a site drastically reduces competition between similar species. This is one example of a class of models with a nondifferentiable peak in the competition kernel, which we recently showed is produced by resource use unrealistically modeled as discontinuous and affects fundamental predictions regarding limiting similarity. This article illustrates those general results and offers a revised model of the tolerance-fecundity trade-off.

The consequences of spatial structure for the evolution of pathogen transmission rate and virulence.

The distribution of organisms in space can be an important mediator of species interactions, but its evolutionary effects on those interactions are only beginning to be explored. These effects may be especially relevant to pathogen-host interactions. A detailed understanding of how and when spatial structure will affect the evolution of pathogen traits is likely to aid our ability to control rapidly emerging infectious diseases. Here we review a growing body of theoretical studies suggesting that spatial structure can lead to the evolution of an intermediate pathogen transmission rate and virulence. We explain the results of these studies in terms of a competition-persistence trade-off. These studies strongly suggest that local host interactions, local host dispersal, and relatively low host reproduction rates create a host population spatial structure that enforces this trade-off and leads to the evolution of lower pathogen transmission rates and virulence. They also suggest that when spatial structure exists, it can dominate over the shape of the transmission-virulence trade-off in determining pathogen traits. We also identify important areas of future research, including quantifying pathogen fitness in a spatial context in order to gain a more mechanistic understanding of the effects of spatial structure and observationally and experimentally testing theoretical predictions.

Taking species abundance distributions beyond individuals.

The species abundance distribution (SAD) is one of the few universal patterns in ecology. Research on this fundamental distribution has primarily focused on the study of numerical counts, irrespective of the traits of individuals. Here we show that considering a set of Generalized Species Abundance Distributions (GSADs) encompassing several abundance measures, such as numerical abundance, biomass and resource use, can provide novel insights into the structure of ecological communities and the forces that organize them. We use a taxonomically diverse combination of macroecological data sets to investigate the similarities and differences between GSADs. We then use probability theory to explore, under parsimonious assumptions, theoretical linkages among them. Our study suggests that examining different GSADs simultaneously in natural systems may help with assessing determinants of community structure. Broadening SADs to encompass multiple abundance measures opens novel perspectives in biodiversity research and warrants future empirical and theoretical developments.

Comment on "Functional traits and niche-based tree community assembly in an Amazonian forest".

Kraft et al. (Reports, 24 October 2008, p. 580) used a variety of metrics describing the distribution of functional traits within a tropical forest community to demonstrate simultaneous environmental filtering and niche differentiation. We discuss how these results could have arisen from sampling design and statistical assumptions, suggesting alternative approaches that could better resolve these questions.

The implicit assumption of symmetry and the species abundance distribution.

Species abundance distributions (SADs) have played a historical role in the development of community ecology. They summarize information about the number and the relative abundance of the species encountered in a sample from a given community. For years ecologists have developed theory to characterize species abundance patterns, and the study of these patterns has received special attention in recent years. In particular, ecologists have developed statistical sampling theories to predict the SAD expected in a sample taken from a region. Here, we emphasize an important limitation of all current sampling theories: they ignore species identity. We present an alternative formulation of statistical sampling theory that incorporates species asymmetries in sampling and dynamics, and relate, in a general way, the community-level SAD to the distribution of population abundances of the species integrating the community. We illustrate the theory on a stochastic community model that can accommodate species asymmetry. Finally, we discuss the potentially important role of species asymmetries in shaping recently observed multi-humped SADs and in comparisons of the relative success of niche and neutral theories at predicting SADs.