How the storage effect and the number of temporal niches affect biodiversity in stochastic and seasonal environments.

Temporal environmental variations affect diversity in communities of competing populations. In particular, the covariance between competition and environment is known to facilitate invasions of rare species via the storage effect. Here we present a quantitative study of the effects of temporal variations in two-species and in diverse communities. Four scenarios are compared: environmental variations may be either periodic (seasonal) or stochastic, and the dynamics may support the storage effect (global competition) or not (local competition). In two-species communities, coexistence is quantified via the mean time to absorption, and we show that stochastic variations yield shorter persistence time because they allow for rare sequences of bad years. In diverse communities, where the steady-state reflects a colonization-extinction equilibrium, the actual number of temporal niches is shown to play a crucial role. When this number is large, the same trends hold: storage effect and periodic variations increase both species richness and the evenness of the community. Surprisingly, when the number of temporal niches is small global competition acts to decrease species richness and evenness, as it focuses the competition to specific periods, thus increasing the effective fitness differences.

Quantifying invasibility.

Invasibility, the chance of a population to grow from rarity and become established, plays a fundamental role in population genetics, ecology, epidemiology and evolution. For many decades, the mean growth rate of a species when it is rare has been employed as an invasion criterion. Recent studies show that the mean growth rate fails as a quantitative metric for invasibility, with its magnitude sometimes even increasing while the invasibility decreases. Here we provide two novel formulae, based on the diffusion approximation and a large-deviations (Wentzel-Kramers-Brillouin) approach, for the chance of invasion given the mean growth and its variance. The first formula has the virtue of simplicity, while the second one holds over a wider parameter range. The efficacy of the formulae, including their accompanying data analysis technique, is demonstrated using synthetic time series generated from canonical models and parameterised with empirical data.

Quantitative Characteristics of Stabilizing and Equalizing Mechanisms.

AbstractAn understanding of the mechanisms that facilitate coexistence in ecological communities poses a major challenge to theoretical ecology. A popular paradigmatic scheme distinguishes between two qualitatively different processes that help species to coexist: stabilizing mechanisms increase niche differentiation, making the intraspecific competition stronger than the interspecific one, while equalizing mechanisms diminish fitness differences, making the competition less decisive. Here, we provide an analytic and numeric examination of the quantitative features associated with this scheme for a simple, two-species competition model. We show that the main metrics of persistence change only slightly along the stabilizing-equalizing continuum, where niche overlap increases while fitness differences decreases. Therefore, persistence properties cannot indicate the dominant mechanism that promotes coexistence and vice versa. Cross correlations between abundance time series are shown to provide a decent characterization of the mechanisms that promote coexistence. The relevance of these insights to the analysis of diverse assemblages is discussed.

How temporal environmental stochasticity affects species richness: Destabilization, neutralization and the storage effect.

Temporal environmental stochasticity (TES), along with the variations of demographic rates associated with it, is ubiquitous in nature. Here we study the effect of TES on the species richness of diverse communities. In such communities the biodiversity at equilibrium reflects the balance between the rate at which new types are added (via migration, mutation or speciation) and the rate of extinction. We analyze a few generic models in which the speciation rate is fixed and TES affects the rate of extinction, and identify three different mechanisms. First, TES increases abundance variations and shortens extinction times, thus decreasing the species richness (destabilizing effect). Second, TES blurs the time-independent fitness differences between species, making the dynamics more symmetric and thereby increasing the diversity (neutralizing effect). Third, the storage effect allows TES to facilitate the invasion of inferior species, again contributing to the species richness. The stabilizing effect of storage declines significantly in diverse communities and it can overcome the destabilizing effect of TES only when environmental fluctuations are rapid enough.

Competition with abundance-dependent fitness and the dynamics of heterogeneous populations in fluctuating environment.

Species competition takes place in a fluctuating environment, so the selective forces on different populations vary through time. In many realistic situations the mean fitness and the amplitude of its temporal variations are abundance-dependent. Here we present a theory of two-species competition with abundance-dependent stochastic fitness variations and solve for the chance of ultimate fixation, the time to absorption and the time to fixation. We then examine the ability of this two-species system to serve as an effective model for high-diversity assemblages and to account for the presence of an intra-specific differential response to environmental variations. The effective model is shown to capture the main features of competition between composite populations.

Mean growth rate when rare is not a reliable metric for persistence of species.

The coexistence of many species within ecological communities poses a long-standing theoretical puzzle. Modern coexistence theory (MCT) and related techniques explore this phenomenon by examining the chance of a species population growing from rarity in the presence of all other species. The mean growth rate when rare, E [ r ] , is used in MCT as a metric that measures persistence properties (like invasibility or time to extinction) of a population. Here we critique this reliance on E [ r ] and show that it fails to capture the effect of temporal random abundance variations on persistence properties. The problem becomes particularly severe when an increase in the amplitude of stochastic temporal environmental variations leads to an increase in E [ r ] , since at the same time it enhances random abundance fluctuations and the two effects are inherently intertwined. In this case, the chance of invasion and the mean extinction time of a population may even go down as E [ r ] increases.

Invasion growth rate and its relevance to persistence: a response to Technical Comment by Ellner et al.

Ellner et al. (2020) state that identifying the mechanisms producing positive invasion growth rates (IGR) is useful in characterising species persistence. We agree about the importance of the sign of IGR as a binary indicator of persistence, but question whether its magnitude provides much information once the sign is given.

Phase Diagram for Logistic Systems under Bounded Stochasticity.

Extinction is the ultimate absorbing state of any stochastic birth-death process; hence, the time to extinction is an important characteristic of any natural population. Here we consider logistic and logisticlike systems under the combined effect of demographic and bounded environmental stochasticity. Three phases are identified: an inactive phase where the mean time to extinction T increases logarithmically with the initial population size, an active phase where T grows exponentially with the carrying capacity N, and a temporal Griffiths phase, with a power-law relationship between T and N. The system supports an exponential phase only when the noise is bounded, in which case the continuum (diffusion) approximation breaks down within the Griffiths phase. This breakdown is associated with a crossover between qualitatively different survival statistics and decline modes. To study the power-law phase we present a new WKB scheme, which is applicable both in the diffusive and in the nondiffusive regime.

Stability of two-species communities: Drift, environmental stochasticity, storage effect and selection.

The dynamics of two competing species in a finite size community is one of the most studied problems in population genetics and community ecology. Stochastic fluctuations lead, inevitably, to the extinction of one of the species, but the relevant timescale depends on the underlying dynamics. The persistence time of the community has been calculated both for neutral models, where the only driving force of the system is drift (demographic stochasticity), and for models with strong selection. Following recent analyses that stress the importance of environmental stochasticity in empirical systems, we present here a general theory of the persistence time of a two-species community where drift, environmental variations and time independent selective advantage are all taken into account.

Fixation and absorption in a fluctuating environment.

A fundamental problem in the fields of population genetics, evolution, and community ecology, is the fate of a single mutant, or invader, introduced in a finite population of wild types. For a fixed-size community of N individuals, with Markovian, zero-sum dynamics driven by stochastic birth-death events, the mutant population eventually reaches either fixation or extinction. The classical analysis, provided by Kimura and his coworkers, is focused on the neutral case, [where the dynamics is only due to demographic stochasticity (drift)], and on time-independent selective forces (deleterious/beneficial mutation). However, both theoretical arguments and empirical analyses suggest that in many cases the selective forces fluctuate in time (temporal environmental stochasticity). Here we consider a generic model for a system with demographic noise and fluctuating selection. Our system is characterized by the time-averaged (log)-fitness s0 and zero-mean fitness fluctuations. These fluctuations, in turn, are parameterized by their amplitude γ and their correlation time δ. We provide asymptotic (large N) formulas for the chance of fixation, the mean time to fixation and the mean time to absorption. Our expressions interpolate correctly between the constant selection limit γ → 0 and the time-averaged neutral case s0=0.

Predicting catastrophic shifts.

Catastrophic shifts are known to pose a serious threat to ecology, and a reliable set of early warning indicators is desperately needed. However, the tools suggested so far have two problems. First, they cannot discriminate between a smooth transition and an imminent irreversible shift. Second, they aimed at predicting the tipping point where a state loses its stability, but in noisy spatial system the actual transition occurs when an alternative state invades. Here we suggest a cluster tracking technique that solves both problems, distinguishing between smooth and catastrophic transitions and to identify an imminent shift in both cases. Our method may allow for the prediction, and thus hopefully the prevention of such transitions, avoiding their destructive outcomes.

The effect of environmental stochasticity on species richness in neutral communities.

Environmental stochasticity is known to be a destabilizing factor, increasing abundance fluctuations and extinction rates of populations. However, the stability of a community may benefit from the differential response of species to environmental variations due to the storage effect. This paper provides a systematic and comprehensive discussion of these two contradicting tendencies, using the metacommunity version of the recently proposed time-average neutral model of biodiversity which incorporates environmental stochasticity and demographic noise and allows for extinction and speciation. We show that the incorporation of demographic noise into the model is essential to its applicability, yielding realistic behavior of the system when fitness variations are relatively weak. The dependence of species richness on the strength of environmental stochasticity changes sign when the correlation time of the environmental variations increases. This transition marks the point at which the storage effect no longer succeeds in stabilizing the community.

Model for macroevolutionary dynamics.

The highly skewed distribution of species among genera, although challenging to macroevolutionists, provides an opportunity to understand the dynamics of diversification, including species formation, extinction, and morphological evolution. Early models were based on either the work by Yule [Yule GU (1925) Philos Trans R Soc Lond B Biol Sci 213:21-87], which neglects extinction, or a simple birth-death (speciation-extinction) process. Here, we extend the more recent development of a generic, neutral speciation-extinction (of species)-origination (of genera; SEO) model for macroevolutionary dynamics of taxon diversification. Simulations show that deviations from the homogeneity assumptions in the model can be detected in species-per-genus distributions. The SEO model fits observed species-per-genus distributions well for class-to-kingdom-sized taxonomic groups. The model's predictions for the appearance times (the time of the first existing species) of the taxonomic groups also approximately match estimates based on molecular inference and fossil records. Unlike estimates based on analyses of phylogenetic reconstruction, fitted extinction rates for large clades are close to speciation rates, consistent with high rates of species turnover and the relatively slow change in diversity observed in the fossil record. Finally, the SEO model generally supports the consistency of generic boundaries based on morphological differences between species and provides a comparator for rates of lineage splitting and morphological evolution.

A neutral theory with environmental stochasticity explains static and dynamic properties of ecological communities.

Understanding the forces shaping ecological communities is crucial to basic science and conservation. Neutral theory has made considerable progress in explaining static properties of communities, like species abundance distributions (SADs), with a simple and generic model, but was criticised for making unrealistic predictions of fundamental dynamic patterns and for being sensitive to interspecific differences in fitness. Here, we show that a generalised neutral theory incorporating environmental stochasticity may resolve these limitations. We apply the theory to real data (the tropical forest of Barro Colorado Island) and demonstrate that it much better explains the properties of short-term population fluctuations and the decay of compositional similarity with time, while retaining the ability to explain SADs. Furthermore, the predictions are considerably more robust to interspecific fitness differences. Our results suggest that this integration of niches and stochasticity may serve as a minimalistic framework explaining fundamental static and dynamic characteristics of ecological communities.

Emergence of structured communities through evolutionary dynamics.

Species-rich communities, in which many competing species coexist in a single trophic level, are quite frequent in nature, but pose a formidable theoretical challenge. In particular, it is known that complex competitive systems become unstable and unfeasible when the number of species is large. Recently, many studies have attributed the stability of natural communities to the structure of the interspecific interaction network, yet the nature of such structures and the underlying mechanisms responsible for them remain open questions. Here we introduce an evolutionary model, based on the generic Lotka-Volterra competitive framework, from which a stable, structured, diverse community emerges spontaneously. The modular structure of the competition matrix reflects the phylogeny of the community, in agreement with the hierarchial taxonomic classification. Closely related species tend to have stronger niche overlap and weaker fitness differences, as opposed to pairs of species from different modules. The competitive-relatedness hypothesis and the idea of emergent neutrality are discussed in the context of this evolutionary model.

Niche versus neutrality: a dynamical analysis.

Understanding the forces shaping ecological communities is of crucial importance for basic science and conservation. After 50 years in which ecological theory has focused on either stable communities driven by niche-based forces or nonstable "neutral" communities driven by demographic stochasticity, contemporary theories suggest that ecological communities are driven by the simultaneous effects of both types of mechanisms. Here we examine this paradigm using the longest available records for the dynamics of tropical trees and breeding birds. Applying a macroecological approach and fluctuation analysis techniques borrowed from statistical physics, we show that both stabilizing mechanisms and demographic stochasticity fail to play a dominant role in shaping assemblages over time. Rather, community dynamics in these two very different systems is predominantly driven by environmental stochasticity. Clearly, the current melding of niche and neutral theories cannot account for such dynamics. Our results highlight the need for a new theory of community dynamics integrating environmental stochasticity with weak stabilizing forces and suggest that such theory may better describe the dynamics of ecological communities than current neutral theories, deterministic niche-based theories, or recent hybrids.

Temporal fluctuation scaling in populations and communities.

Taylor's law, one of the most widely accepted generalizations in ecology, states that the variance of a population abundance time series scales as a power law of its mean. Here we reexamine this law and the empirical evidence presented in support of it. Specifically, we show that the exponent generally depends on the length of the time series, and its value reflects the combined effect of many underlying mechanisms. Moreover, sampling errors alone, when presented on a double logarithmic scale, are sufficient to produce an apparent power law. This raises questions regarding the usefulness of Taylor's law for understanding ecological processes. As an alternative approach, we focus on short-term fluctuations and derive a generic null model for the variance-to-mean ratio in population time series from a demographic model that incorporates the combined effects of demographic and environmental stochasticity. After comparing the predictions of the proposed null model with the fluctuations observed in empirical data sets, we suggest an alternative expression for fluctuation scaling in population time series. Analyzing population fluctuations as we have proposed here may provide new applied (e.g., estimation of species persistence times) and theoretical (e.g., the neutral theory of biodiversity) insights that can be derived from more generally available short-term monitoring data.

Neutral-like abundance distributions in the presence of selection in a continuous fitness landscape.

The neutral theory of biodiversity has successfully explained the observed composition of many ecological communities but it relies on strict demographic equivalence among species and provides no room for evolutionary processes such as selection and adaptation. Here we show how to embed the neutral theory within the Darwinian framework. In a continuous fitness landscape with a quadratic maximum, typical for quantitative traits, selection does restrict the extant species to have trait values close to optimal, but due to the continuous nature of the landscape, there are always many such species available, and so competition among them is effectively neutral. For sufficiently small mutational steps, the community structure fits perfectly to the Fisher log-series species abundance distribution. In general, the selection-mutation process, when superimposed on demographic and environmental noise, yields a small set of characteristic patterns for species abundance curves. A survey of these patterns is given.

Population dynamics in a time-varying environment with fat-tailed correlations.

Temporal environmental noise (EN) is a prevalent natural phenomenon that controls population and community dynamics, shaping the destiny of biological species and genetic types. Conventional theoretical models often depict EN as a Markovian process with an exponential distribution of correlation times, resulting in two distinct qualitative dynamical categories: quenched (long environmental timescales) and annealed (short environmental timescales). However, numerous empirical studies demonstrate a fat-tailed decay of correlation times. Here we study the consequences of power-law correlated EN on the dynamics of isolated and competing populations. We analyze the intermediate region that lies between the quenched and annealed regimes and show that it can widen indefinitely. Within this region, dynamics is primarily driven by rare, yet not exceedingly rare, long periods of almost-steady environmental conditions. For an isolated population, the time to extinction in this region exhibits a power-law scaling with the logarithm of the abundance and also a nonmonotonic dependence on the spectral exponent.

Processes governing species richness in communities exposed to temporal environmental stochasticity: A review and synthesis of modelling approaches.

Research into the processes governing species richness has often assumed that the environment is fixed, whereas realistic environments are often characterised by random fluctuations over time. This temporal environmental stochasticity (TES) changes the demographic rates of species populations, with cascading effects on community dynamics and species richness. Theoretical and applied studies have used process-based mathematical models to determine how TES affects species richness, but under a variety of frameworks. Here, we critically review such studies to synthesise their findings and draw general conclusions. We first provide a broad mathematical framework encompassing the different ways in which TES has been modelled. We then review studies that have analysed models with TES under the assumption of negligible interspecific interactions, such that a community is conceptualised as the sum of independent species populations. These analyses have highlighted how TES can reduce species richness by increasing the frequency at which a species becomes rare and therefore prone to extinction. Next, we review studies that have relaxed the assumption of negligible interspecific interactions. To simplify the corresponding models and make them analytically tractable, such studies have used mean-field theory to derive fixed parameters representing the typical strength of interspecific interactions under TES. The resulting analyses have highlighted community-level effects that determine how TES affects species richness, for species that compete for a common limiting resource. With short temporal correlations of environmental conditions, a non-linear averaging effect of interspecific competition strength over time gives an increase in species richness. In contrast, with long temporal correlations of environmental conditions, strong selection favouring the fittest species between changes in environmental conditions results in a decrease in species richness. We compare such results with those from invasion analysis, which examines invasion growth rates (IGRs) instead of species richness directly. Qualitative differences sometimes arise because the IGR is the expected growth rate of a species when it is rare, which does not capture the variation around this mean or the probability of the species becoming rare. Our review elucidates key processes that have been found to mediate the negative and positive effects of TES on species richness, and by doing so highlights key areas for future research.