Extinction–immigration dynamics lag behind environmental filtering in shaping the composition of tropical dry forests within a changing landscape

The impact of rapid habitat loss and fragmentation on biodiversity is a major issue. However, we still lack an integrative understanding of how these changes influence biodiversity dynamics over time. In this study, we investigate the effects of these changes in terms of both niche-based and neutral dynamics. We hypothesize that habitat loss has delayed effects on neutral immigration–extinction dynamics, while edge effects and environmental heterogeneity in habitat patches have rapid effects on niche-based dynamics. We analyzed taxonomic and functional composition of 100 tree communities in a tropical dry forest landscape of New-Caledonia subject to habitat loss and fragmentation. We designed an original, process-based simulation framework, and performed Approximate Bayesian Computation to infer the influence of niche-based and neutral processes. Then, we performed partial regressions to evaluate the relationships between inferred parameter values of communities and landscape metrics (distance to edge, patch area, and habitat amount around communities), derived from either recent or past (65 yr ago) aerial photographs, while controlling for the effect of soil and topography. We found that landscape structure influences both environmental filtering and immigration. Immigration rate was positively related to past habitat amount surrounding communities. In contrast, environmental filtering was mostly affected by present landscape structure and mainly influenced by edge vicinity and topography. Our results highlight that landscape changes have contrasting spatio-temporal influences on niche-based and neutral assembly dynamics. First, landscape-level habitat loss and community isolation reduce immigration and increase demographic stochasticity, resulting in slow decline of local species diversity and extinction debt. Second, recent edge creation affects environmental filtering, incurring rapid changes in community composition by favoring species with edge-adapted strategies. Our study brings new insights about temporal impacts of landscape changes on biodiversity dynamics. We stress that landscape history critically influences these dynamics and should be taken into account in conservation policies.     

Tropical Forests Are Non-Equilibrium Ecosystems Governed by Interspecific Competition Based on Universal 1/6 Niche Width

Tropical forests are mega-diverse ecosystems that display complex and non-equilibrium dynamics. However, theoretical approaches have largely focused on explaining steady-state behaviour and fitting snapshots of data. Here we show that local and niche interspecific competition can realistically and parsimoniously explain the observed non-equilibrium regime of permanent plots of nine tropical forests, in eight different countries. Our spatially-explicit model, besides predicting with accuracy the main biodiversity metrics for these plots, can also reproduce their dynamics. A central finding is that tropical tree species have a universal niche width of approximately 1/6 of the niche axis that echoes the observed widespread convergence in their functional traits enabling them to exploit similar resources and to coexist despite of having large niche overlap. This niche width yields an average ratio of 0.25 between interspecific and intraspecific competition that corresponds to an intermediate value between the extreme claims of the neutral model and the classical niche-based model of community assembly (where interspecific competition is dominant). In addition, our model can explain and yield observed spatial patterns that classical niche-based and neutral theories cannot.     

The Neutral—Niche Debate: A Philosophical Perspective

Ecological communities around the world are under threat while a consensus theory of community structure remains elusive. In the last decade ecologists have struggled with two seemingly opposing theories: niche-based theory that explains diversity with species’ differences and the neutral theory of biodiversity that claims that much of the diversity we observe can be explained without explicitly invoking species’ differences. Although ecologists are increasingly attempting to reconcile these two theories, there is still much resistance against the neutral theory of biodiversity. Here we argue that the dispute between the two theories is a classic example of the dichotomy between philosophical perspectives, realism and instrumentalism. Realism is associated with specific, small-scale and detailed explanations, whereas instrumentalism is linked to general, large-scale, but less precise accounts. Recognizing this will help ecologists get both niche-based and neutral theories in perspective as useful tools for understanding biodiversity patterns.     

Reconciling niche and neutrality: the continuum hypothesis

In this study, we ask if instead of being fundamentally opposed, niche and neutral theories could simply be located at the extremes of a continuum. First, we present a model of recruitment probabilities that combines both niche and neutral processes. From this model, we predict and test whether the relative importance of niche vs. neutral processes in controlling community dynamics will vary depending on community species richness, niche overlap and dispersal capabilities of species (both local and long distance). Results demonstrate that niche and neutrality form ends of a continuum from competitive to stochastic exclusion. In the absence of immigration, competitive exclusion tends to create a regular spacing of niches. However, immigration prevents the establishment of a limiting similarity. The equilibrium community consists of a set of complementary and redundant species, with their abundance determined, respectively, by the distribution of environmental conditions and the amount of immigration.     

The shifting balance of facilitation and competition affects the outcome of intra- and interspecific interactions over the life history of California grassland annuals

Trait-based resource competition in plants, wherein more similar plants compete more strongly for resources, is a foundation of niche-based explanations for the maintenance of diversity in plant communities. Alternatively, neutral theory predicts that community diversity can be maintained despite equivalent resource requirements among species. We examined interactions at three life history stages (germination, survival, and juvenile-adult growth) for three native and three exotic California annual species in a glasshouse experiment. We varied plant density and species composition in small pots, with pots planted with either intraspecific seeds or in a three species mix of intra- and interspecific neighbors. We saw a range of facilitative, neutral, and competitive interactions that varied significantly by species, rather than by native or exotic status. There were more competitive interactions at the emergence and juvenile-adult growth stages and more facilitative interactions for survival. Consequently, the relative strength of competition in intraspecific versus mixed-species communities depended on whether we considered only the juvenile-adult growth stage or the entire life history of the interacting plants. Using traditional analysis of juvenile-adult growth only, all species showed negative density-dependent interactions for final biomass production. However, when the net effect of plant interactions from seed to adult was considered, which is a prediction of population growth, two native species ceased to show negative density dependence, and the difference between intraspecific and mixed-species competition was only significant for one exotic species. Results were consistent with predictions of neutral, rather than niche, theory for five of six species.     

Coexistence and invasibility in a two-species competition model with habitat-preference

The outcome of competition among species is influenced by the spatial distribution of species and effects such as demographic stochasticity, immigration fluxes, and the existence of preferred habitats. We introduce an individual-based model describing the competition of two species and incorporating all the above ingredients. We find that the presence of habitat preference—generating spatial niches—strongly stabilizes the coexistence of the two species. Eliminating habitat preference—neutral dynamics—the model generates patterns, such as distribution of population sizes, practically identical to those obtained in the presence of habitat preference, provided an higher immigration rate is considered. Notwithstanding the similarity in the population distribution, we show that invasibility properties depend on habitat preference in a non-trivial way. In particular, the neutral model results more invasible or less invasible depending on whether the comparison is made at equal immigration rate or at equal distribution of population size, respectively. We discuss the relevance of these results for the interpretation of invasibility experiments and the species occupancy of preferred habitats.     

When can we distinguish between neutral and non‐neutral processes in community dynamics under ecological drift?

Determining whether the composition of ecological communities (species presence and abundance), can be predicted from species demographic traits, rather than being a result of neutral drift, is a key ecological question. Here we compare the similarity of community composition, from different community assembly models run under identical environmental conditions, where interspecific competition is assumed to be either neutral or niche-based. In both cases, species colonize a focal patch from a network of neighbouring patches in a metacommunity. We highlight the circumstances (rate and spatial scale of dispersal, and the relative importance of ecological drift) where commonly used community similarity metrics or species rank–abundance relationships are likely to give similar results, regardless of the underlying processes (neutral or non-neural) driving species' dynamics. As drift becomes more important in driving species abundances, deterministic niche structure has a smaller influence. Our ability to discriminate between different underlying processes driving community organization depends on the relative importance of different drift processes that operate on different spatial scales.     

Demographic stochasticity alters expected outcomes in experimental and simulated non‐neutral communities

Theory has shown that the effects of demographic stochasticity on communities may depend on the magnitude of fitness differences between species. In particular, it has been suggested that demographic stochasticity has the potential to significantly alter competitive outcomes when fitness differences are small (nearly neutral), but that it has negligible effects when fitness differences are large (highly non‐neutral). Here we test such theory experimentally and extend it to examine how demographic stochasticity affects exclusion frequency and mean densities of consumers in simple, but non‐neutral, consumer–resource communities. We used experimental microcosms of protists and rotifers feeding on a bacterial resource to test how varying absolute population sizes (a driver of demographic stochasticity) affected the probability of competitive exclusion of the weakest competitor. To explore whether demographic stochasticity could explain our experimental results, and to generalize beyond our experiment, we paired the experiment with a continuous‐time stochastic model of resource competition, which we simulated for 11 different fitness inequalities between competiting consumers. Consistent with theory, in both our experiments and our simulations we found that demographic stochasticity altered competitive outcomes in communities where fitness differences were small. However, we also found that demographic stochasticity alone could affect communities in other ways, even when fitness differences between competitors were large. Specifically, demographic stochasticity altered mean densities of both weak and strong competitors in experimental and simulated communities. These findings highlight how demographic stochasticity can change both competitive outcomes in non‐neutral communities and the processes underlying overall community dynamics.     

Extinctions in competitive communities forced by coloured environmental variation

Understanding the relationships between environmental fluctuations, population dynamics and species interactions in natural communities is of vital theoretical and practical importance. This knowledge is essential in assessing extinction risks in communities that are, for example, pressed by changing environmental conditions and increasing exploitation. We developed a model of density dependent population renewal, in a Lotka–Volterra competitive community context, to explore the significance of interspecific interactions, demographic stochasticity, population growth rate and species abundance on extinction risk in populations under various autocorrelation (colour) regimes of environmental forcing. These factors were evaluated in two cases, where either a single species or the whole community was affected by the external forcing. Species' susceptibility to environmental noise with different autocorrelation structure depended markedly on population dynamics, species' position in the abundance hierarchy and how similarly community members responded to external forcing. We also found interactions between demographic stochasticity and environmental noise leading to a reversal in extinction probabilities from under- to overcompensatory dynamics. We compare our results with studies of single species populations and contrast possible mechanisms leading to extinctions. Our findings indicate that abundance rank, the form of population dynamics, and the colour of environmental variation interact in affecting species extinction risk. These interactions are further modified by interspecific interactions within competitive communities as the interactions filter and modulate the environmental noise.     

Local community size mediates ecological drift and competition in metacommunities

The outcome of competitive interactions is likely to be influenced by both competitive dominance (i.e. niche-based dynamics) and ecological drift (i.e. neutral dynamics governed by demographic stochasticity). However, spatial models of competition rarely consider the joint operation of these two processes. We develop a model based on the original competition-colonization trade-off model that incorporates niche and neutral processes and several realistic facets of ecological dynamics: it allows local competition (i.e. competition within a patch) to occur within communities of a finite size, it allows competitors to vary in the degree of competitive asymmetry, and it includes the role of local migration (i.e. propagule pressure). The model highlights the role of community size, i.e. the number of competitors in the local community, in mediating the relative importance of stochastic and deterministic forces. In metacommunities where local communities are small, ecological drift is substantial enough that strong competitors become effectively neutral, creating abrupt changes in the outcome of competition not predicted by the standard competition-colonization trade-off. Importantly, the model illustrates that, even when other aspects of species interactions (e.g. migration ability, competitive ability) are unchanged, local community size can alter the dynamics of metacommunity persistence. Our work demonstrates that activities which reduce the size of local communities, such as habitat destruction and degradation, effectively compound the extinction debt.     

Species diversity in local neutral communities

We extend the neutral theory of macroecology by deriving biodiversity models (relative species abundance and species-area relationships) in a local community-metacommunity system in which the local community is embedded within the metacommunity. We first demonstrate that the local species diversity patterns converge to that of the metacommunity as the size (scale) of the embedded local community increases. This result shows that in continuous landscapes no sharp boundaries dividing the communities at the two scales exist; they are an artificial distinction made by the current spatially implicit neutral theory. Second, we remove the artificial restriction that speciation cannot occur in a local community, even if the effects of local speciation are small. Third, we introduce stochasticity into the immigration rate, previously treated as constant, and demonstrate that local species diversity is a function not only of the mean but also of the variance in immigration rate. High variance in immigration rates reduces species diversity in local communities. Finally, we show that a simple relationship exists between the fundamental diversity parameter of neutral theory and Simpson's index for local communities. Derivation of this relationship extends recent work on diversity indices and provides a means of evaluating the effect of immigration on estimates of the fundamental diversity parameter derived from relative species abundance data on local communities.     

Modeling Taxa-Abundance Distributions in Microbial Communities using Environmental Sequence Data

We show that inferring the taxa-abundance distribution of a microbial community from small environmental samples alone is difficult. The difficulty stems from the disparity in scale between the number of genetic sequences that can be characterized and the number of individuals in communities that microbial ecologists aspire to describe. One solution is to calibrate and validate a mathematical model of microbial community assembly using the small samples and use the model to extrapolate to the taxa-abundance distribution for the population that is deemed to constitute a community. We demonstrate this approach by using a simple neutral community assembly model in which random immigrations, births, and deaths determine the relative abundance of taxa in a community. In doing so, we further develop a neutral theory to produce a taxa-abundance distribution for large communities that are typical of microbial communities. In addition, we highlight that the sampling uncertainties conspire to make the immigration rate calibrated on the basis of small samples very much higher than the true immigration rate. This scale dependence of model parameters is not unique to neutral theories; it is a generic problem in ecology that is particularly acute in microbial ecology. We argue that to overcome this, so that microbial ecologists can characterize large microbial communities from small samples, mathematical models that encapsulate sampling effects are required.     

Immigration,Local Dispersal Limitation,and the Repeatability of Community Composition under Neutral and Niche Dynamics

Repeatability of community composition has been a critical aspect for community structure, which is closely associated with community stability, predictability, conservation biology and ecological restoration. It has been shown that both immigration and local dispersal limitation can affect the community composition in both neutral and niche model. Hence, we use a spatially explicit individual-based model to investigate the potential influence of immigration rate and strength of local dispersal limitation on repeatability in both neutral and niche models. Similarity measures are used to quantify repeatability. We examine the repeatability of community composition among replicate communities (which means the same community repeats many times), and between niche and neutral replicate communities. We find the correlation between repeatability and immigration rate is positive in the neutral model and an inverted unimodal in the niche model. The correlation between repeatability and local dispersal distance is positive in the niche model and negative in the neutral model. High repeatability between niche communities and neutral communities is observed with high immigration rates or when high local dispersal distance appears in the niche model or low local dispersal distance in the neutral model. Our results show that repeatability of community composition is not only dependent on the types of community models (niche vs. neutrality) but also strongly determined by immigration rates and local dispersal limitation.     

Nested species interactions promote feasibility over stability during the assembly of a pollinator community

The foundational concepts behind the persistence of ecological communities have been based on two ecological properties: dynamical stability and feasibility. The former is typically regarded as the capacity of a community to return to an original equilibrium state after a perturbation in species abundances and is usually linked to the strength of interspecific interactions. The latter is the capacity to sustain positive abundances on all its constituent species and is linked to both interspecific interactions and species demographic characteristics. Over the last 40 years, theoretical research in ecology has emphasized the search for conditions leading to the dynamical stability of ecological communities, while the conditions leading to feasibility have been overlooked. However, thus far, we have no evidence of whether species interactions are more conditioned by the community''s need to be stable or feasible. Here, we introduce novel quantitative methods and use empirical data to investigate the consequences of species interactions on the dynamical stability and feasibility of mutualistic communities. First, we demonstrate that the more nested the species interactions in a community are, the lower the mutualistic strength that the community can tolerate without losing dynamical stability. Second, we show that high feasibility in a community can be reached either with high mutualistic strength or with highly nested species interactions. Third, we find that during the assembly process of a seasonal pollinator community located at The Zackenberg Research Station (northeastern Greenland), a high feasibility is reached through the nested species interactions established between newcomer and resident species. Our findings imply that nested mutualistic communities promote feasibility over stability, which may suggest that the former can be key for community persistence.     

The relative importance of positive and negative interactions for pollinator attraction in a plant community

Plant–pollinator interactions provide ideal frameworks for studying interactions in plant communities. Despite the large potential influence of such interactions on plant community structure, biodiversity and evolutionary processes, we know surprisingly little about the relative importance of positive and negative interactions among plant species for pollinator attraction. Therefore, we explored the relationships between conspecific and heterospecific floral densities and the flower visitation rates of nine plant species mainly visited by bumble bees, and six plant species mainly visited by flies, in a temperate grassland, through stepwise multiple regressions. Significant relationships were interpreted as interactions for pollinator attraction. Our results revealed that positive intra- and interspecific interactions for pollinator attraction were far more frequent than negative ones. Seventeen interspecific interactions were revealed of which 14 were significantly positive, whereas three of four significant intraspecific interactions were positive. Seven species experienced only positive interactions and two species experienced only negative interactions. The results presented here indicate that negative interactions are not necessarily the dominant ecological interaction for pollination among plants within a community, and the study represents a straightforward approach to study intra- and interspecific interactions among multiple species within a community. We discuss which mechanisms may drive the positive interactions for pollinator attraction and whether this may result in facilitative effects on reproductive success. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Niches versus neutrality: uncovering the drivers of diversity in a species-rich community

Ecological models suggest that high diversity can be generated by purely niche-based, purely neutral or by a mixture of niche-based and neutral ecological processes. Here, we compare the degree to which four contrasting hypotheses for coexistence, ranging from niche-based to neutral, explain species richness along a body mass niche axis. We derive predictions from these hypotheses and confront them with species body-mass patterns in a highly sampled marine phytoplankton community. We find that these patterns are consistent only with a mechanism that combines niche and neutral processes, such as the emergent neutrality mechanism. In this work, we provide the first empirical evidence that a niche-neutral model can explain niche space occupancy pattern in a natural species-rich community. We suggest this class of model may be a useful hypothesis for the generation and maintenance of species diversity in other size-structured communities.     

Demographic analysis of Hubbell's neutral theory of biodiversity

Hubbell's neutral model is increasingly applied in both theoretical and empirical studies but so far little attention has been paid to the ecological mechanisms that determine species diversity in neutral communities. In this contribution we use a stochastic individual-based Markovian model to provide an explicit derivation of Hubbell's local community model from the fundamental processes of reproduction, mortality, and immigration, and show that such derivation provides important insights on the mechanisms regulating species diversity that cannot be obtained from the original model and its previous extensions. One important insight is that the basic parameters of Hubbell's model, community size (J) and the probability that a dying individual will be replaced by an immigrant (m), cannot be considered independent and that their interdependency leads to a counterintuitive trade-off between community size and species diversity. We further demonstrate that Hubbell's treatment of community size as a free parameter hides fundamental mechanisms that influence species diversity through their effect on the size of the community. For example, while in Hubbell's model immigration can only increase species diversity by promoting colonization rates, the demographic derivation shows that immigration can also promote species diversity by reducing extinction rates. Our demographic derivation also unifies previous contrasting predictions about the effect of reproduction on species diversity by showing that both positive and negative effects are possible, and that the balance between the two effects depends on the size of the community. The demographic derivation also reconciles an apparent contradiction between Hubbell's theory and patch occupancy theory, and integrates three previously proposed mechanisms of species diversity, the More Individuals Hypothesis, the rescue effect, and the dilution effect, within a single, unified framework.     

Assessing the relative importance of neutral stochasticity in ecological communities

A central current debate in community ecology concerns the relative importance of deterministic versus stochastic processes underlying community structure. However, the concept of stochasticity presents several profound philosophical, theoretical and empirical challenges, which we address here. The philosophical argument that nothing in nature is truly stochastic can be met with the following operational concept of neutral stochasticity in community ecology: change in the composition of a community (i.e. community dynamics) is neutrally stochastic to the degree that individual demographic events – birth, death, immigration, emigration – which cause such changes occur at random with respect to species identities. Empirical methods for identifying the stochastic component of community dynamics or structure include null models and multivariate statistics on observational species‐by‐site data (with or without environmental or trait data), and experimental manipulations of ‘stochastic’ species colonization order or relative densities and frequencies of competing species. We identify the fundamental limitations of each method with respect to its ability to allow inferences about stochastic community processes. Critical future needs include greater precision in articulating the link between results and ecological inferences, a comprehensive theoretical assessment of the interpretation of statistical analyses of observational data, and experiments focusing on community size and on natural variation in species colonization order. Synthesis Community structure and dynamics have often been described as being underlain by ‘stochastic’ or ‘neutral’ processes, but there is great confusion as to what exactly this means. We attempt to provide conceptual clarity by specifying precisely what focal ecological variable (e.g. species distributions, community composition, demography) is considered to be stochastic with respect to what other variables (e.g. other species' distributions, traits, environment) when using different empirical methods. We clarify what inferences can be drawn by different observational and experimental approaches, and we suggest future avenues of research to better understand the role of neutral stochasticity in community ecology.     

Analyzing tropical forest tree species abundance distributions using a nonneutral model and through approximate Bayesian inference

The neutral theory of biodiversity challenges the classical niche-based view of ecological communities, where species attributes and environmental conditions jointly determine community composition. Functional equivalence among species, as assumed by neutral ecological theory, has been recurrently falsified, yet many patterns of tropical tree communities appear consistent with neutral predictions. This may mean that neutral theory is a good first-approximation theory or that species abundance data sets contain too little information to reject neutrality. Here we present a simple test of neutrality based on species abundance distributions in ecological communities. Based on this test, we show that deviations from neutrality are more frequent than previously thought in tropical forest trees, especially at small spatial scales. We then develop a nonneutral model that generalizes Hubbell's dispersal-limited neutral model in a simple way by including one additional parameter of frequency dependence. We also develop a statistical method to infer the parameters of this model from empirical data by approximate Bayesian computation. In more than half of the permanent tree plots, we show that our new model fits the data better than does the neutral model. Finally, we discuss whether observed deviations from neutrality may be interpreted as the signature of environmental filtering on tropical tree species abundance distributions.     

Niche partitioning at multiple scales facilitates coexistence among mosquito larvae

A theoretical dichotomy in community ecology distinguishes between mechanisms that stabilize species coexistence and those that cause neutral drift. Stable coexistence is predicted to occur in communities where competing species have niche-partitioning mechanisms that reduce interspecific competition. Neutral communities are predicted to be structured by stochastic processes that are not influenced by species identity, but that may be influenced by priority effects and dispersal limitation. Recent developments have suggested that neutral interactions may be more common at local scales, while niche structuring may be more common at larger scales. We tested for mechanisms that could promote either stable coexistence or neutral drift in a bromeliad-dwelling mosquito community by evaluating A) if a hypothesized within-bromeliad niche partitioning mechanism occurs in the community, B) if this mechanism correlates with local species co-occurrence patterns, and C) if patterns of coexistence at the larger (metacommunity) scale were consistent with those at the local scale. We found that mosquitoes in this community do partition space within containers, and that species with the strongest potential for competition co-occurred least. Species with overlapping spatial niches minimized co-occurrence by specialising in bromeliads of differing sizes, effectively changing the scale at which they coexist. In contrast, we found no evidence to support neutral dynamics in mosquito communities at either scale. In this community, a niche-based mechanism that is predicted to stabilize species coexistence explains co-occurrence patterns within and among bromeliads.