David A. Vasseur

Why intraspecific trait variation matters in community ecology

Natural populations consist of phenotypically diverse individuals that exhibit variation in their demographic parameters and intra- and inter-specific interactions. Recent experimental work indicates that such variation can have significant ecological effects. However, ecological models typically disregard this variation and focus instead on trait means and total population density. Under what situations is this simplification appropriate? Why might intraspecific variation alter ecological dynamics? In this review we synthesize recent theory and identify six general mechanisms by which trait variation changes the outcome of ecological interactions. These mechanisms include several direct effects of trait variation per se and indirect effects arising from the role of genetic variation in trait evolution.

Increased temperature variation poses a greater risk to species than climate warming.

Increases in the frequency, severity and duration of temperature extremes are anticipated in the near future. Although recent work suggests that changes in temperature variation will have disproportionately greater effects on species than changes to the mean, much of climate change research in ecology has focused on the impacts of mean temperature change. Here, we couple fine-grained climate projections (2050–2059) to thermal performance data from 38 ectothermic invertebrate species and contrast projections with those of a simple model. We show that projections based on mean temperature change alone differ substantially from those incorporating changes to the variation, and to the mean and variation in concert. Although most species show increases in performance at greater mean temperatures, the effect of mean and variance change together yields a range of responses, with temperate species at greatest risk of performance declines. Our work highlights the importance of using fine-grained temporal data to incorporate the full extent of temperature variation when assessing and projecting performance.

A bioenergetic framework for the temperature dependence of trophic interactions

Changing temperature can substantially shift ecological communities by altering the strength and stability of trophic interactions. Because many ecological rates are constrained by temperature, new approaches are required to understand how simultaneous changes in multiple rates alter the relative performance of species and their trophic interactions. We develop an energetic approach to identify the relationship between biomass fluxes and standing biomass across trophic levels. Our approach links ecological rates and trophic dynamics to measure temperature-dependent changes to the strength of trophic interactions and determine how these changes alter food web stability. It accomplishes this by using biomass as a common energetic currency and isolating three temperature-dependent processes that are common to all consumer-resource interactions: biomass accumulation of the resource, resource consumption and consumer mortality. Using this framework, we clarify when and how temperature alters consumer to resource biomass ratios, equilibrium resilience, consumer variability, extinction risk and transient vs. equilibrium dynamics. Finally, we characterise key asymmetries in species responses to temperature that produce these distinct dynamic behaviours and identify when they are likely to emerge. Overall, our framework provides a mechanistic and more unified understanding of the temperature dependence of trophic dynamics in terms of ecological rates, biomass ratios and stability.

Phase-locking and environmental fluctuations generate synchrony in a predator–prey community

Spatially synchronized fluctuations in system state are common in physical and biological systems ranging from individual atoms to species as diverse as viruses, insects and mammals. Although the causal factors are well known for many synchronized phenomena, several processes concurrently have an impact on spatial synchrony of species, making their separate effects and interactions difficult to quantify. Here we develop a general stochastic model of predator–prey spatial dynamics to predict the outcome of a laboratory microcosm experiment testing for interactions among all known synchronizing factors: (1) dispersal of individuals between populations; (2) spatially synchronous fluctuations in exogenous environmental factors (the Moran effect); and (3) interactions with other species (for example, predators) that are themselves spatially synchronized. The Moran effect synchronized populations of the ciliate protist Tetrahymena pyriformis; however, dispersal only synchronized prey populations in the presence of the predator Euplotes patella. Both model and data indicate that synchrony depends on cyclic dynamics generated by the predator. Dispersal, but not the Moran effect, ‘phase-locks’ cycles, which otherwise become ‘decoherent’ and drift out of phase. In the absence of cycles, phase-locking is not possible and the synchronizing effect of dispersal is negligible. Interspecific interactions determine population synchrony, not by providing an additional source of synchronized fluctuations, but by altering population dynamics and thereby enhancing the action of dispersal. Our results are robust to wide variation in model parameters representative of many natural predator–prey or host–pathogen systems. This explains why cyclic systems provide many of the most dramatic examples of spatial synchrony in nature.

Mutual interference is common and mostly intermediate in magnitude.

BackgroundInterference competition occurs when access to resources is negatively affected by the presence of other individuals. Within a species or population, this is known as mutual interference, and it is often modelled with a scaling exponent, m, on the number of predators. Originally, mutual interference was thought to vary along a continuum from prey dependence (no interference; m = 0) to ratio dependence (m = -1), but a debate in the 1990s and early 2000s focused on whether prey or ratio dependence was the better simplification. Some have argued more recently that mutual interference is likely to be mostly intermediate (that is, between prey and ratio dependence), but this possibility has not been evaluated empirically.ResultsWe gathered estimates of mutual interference from the literature, analyzed additional data, and created the largest compilation of unbiased estimates of mutual interference yet produced. In this data set, both the alternatives of prey dependence and ratio dependence were observed, but only one data set was consistent with prey dependence. There was a tendency toward ratio dependence reflected by a median m of -0.7 and a mean m of -0.8.ConclusionsOverall, the data support the hypothesis that interference is mostly intermediate in magnitude. The data also indicate that interference competition is common, at least in the systems studied to date. Significant questions remain regarding how different factors influence interference, and whether interference can be viewed as a characteristic of a particular population or whether it generally shifts from low to high levels as populations increase in density.

Character Convergence under Competition for Nutritionally Essential Resources

Resource competition is thought to drive divergence in resource use traits (character displacement) by generating selection favoring individuals able to use resources unavailable to others. However, this picture assumes nutritionally substitutable resources (e.g., different prey species). When species compete for nutritionally essential resources (e.g., different nutrients), theory predicts that selection drives character convergence. We used models of two species competing for two essential resources to address several issues not considered by existing theory. The models incorporated either slow evolutionary change in resource use traits or fast physiological or behavioral change. We report four major results. First, competition always generates character convergence, but differences in resource requirements prevent competitors from evolving identical resource use traits. Second, character convergence promotes coexistence. Competing species always attain resource use traits that allow coexistence, and adaptive trait change stabilizes the ecological equilibrium. In contrast, adaptation in allopatry never preadapts species to coexist in sympatry. Third, feedbacks between ecological dynamics and trait dynamics lead to surprising dynamical trajectories such as transient divergence in resource use traits followed by subsequent convergence. Fourth, under sufficiently slow trait change, ecological dynamics often drive one of the competitors to near extinction, which would prevent realization of long‐term character convergence in practice.

Eco-Evolutionary Dynamics Enable Coexistence via Neighbor-Dependent Selection

Recent studies suggest that selection can allow coexistence in situations where ecological dynamics lead to competitive exclusion, provided that there is a trade-off between traits optimal for interacting with conspecifics and traits optimal for interacting with heterospecifics. Despite compelling empirical evidence, there is no general framework for elucidating how and when selection will allow coexistence in natural communities. Here we develop such a framework for a mechanism that we term “neighbor-dependent selection.” We show that this mechanism can both augment coexistence when ecological conditions allow for niche partitioning and enable coexistence when ecological conditions lead to competitive exclusion. The novel insight is that when ecological conditions lead to exclusion, neighbor-dependent selection can allow coexistence via cycles driven by an intransitive loop; selection causes one species to be a superior interspecific competitor when it is rare and an inferior interspecific competitor when it is abundant. Our framework predicts the conditions under which selection can enable coexistence, as opposed to merely augmenting it, and elucidates the effects of heritability on the eco-evolutionary feedbacks that drive coexistence. Given increasing evidence that evolution operates on ecological timescales, our approach provides one means for evaluating the role of selection and trait evolution in species coexistence.

The Body Size Dependence of Trophic Cascades

Trophic cascades are indirect positive effects of predators on resources via control of intermediate consumers. Larger-bodied predators appear to induce stronger trophic cascades (a greater rebound of resource density toward carrying capacity), but how this happens is unknown because we lack a clear depiction of how the strength of trophic cascades is determined. Using consumer resource models, we first show that the strength of a trophic cascade has an upper limit set by the interaction strength between the basal trophic group and its consumer and that this limit is approached as the interaction strength between the consumer and its predator increases. We then express the strength of a trophic cascade explicitly in terms of predator body size and use two independent parameter sets to calculate how the strength of a trophic cascade depends on predator size. Both parameter sets predict a positive effect of predator size on the strength of a trophic cascade, driven mostly by the body size dependence of the interaction strength between the first two trophic levels. Our results support previous empirical findings and suggest that the loss of larger predators will have greater consequences on trophic control and biomass structure in food webs than the loss of smaller predators.

Competition and the density dependence of metabolic rates

Although mass and temperature are strong predictors of metabolic rates, there is considerable unexplained variation in metabolic rates both within and across species after body size and temperature are taken into account. Some of this variation may be due to changes in the rate of food intake with population density, as metabolism depends on the throughput of food to fuel biochemical reactions. Using data collected from the literature, we show that individual metabolic rates are negatively correlated with population density for a wide range of organisms including primary producers and consumers. Using new data for the zooplankter Daphnia ambigua, we also find genotypic variation in the relationship between metabolic rate and population density. The relationship between metabolic rate and population density generally follows a power law scaling, and within a population, density-correlated variation in metabolism can span two orders of magnitude. We suggest that density-dependent metabolic rates arise via competitive effects on foraging rates (both exploitation and interference competition), combined with an activity response to accommodate the resource constraint induced by competition. Standard ecological models predict the kind of density-dependent foraging patterns that could give rise to density-dependent metabolic rates, but this has generally not been investigated. Our results indicate that after body mass and temperature, population density represents an important third axis that may account for a large amount of unexplained variance in metabolic rates within and among species. The effect of population density on metabolism has implications for the scaling of metabolic rates from individuals to populations and the relative performance of species and genotypes and therefore also for community assembly and evolution.

Phase locking, the Moran effect and distance decay of synchrony: experimental tests in a model system

Spatially separated populations of many species fluctuate synchronously. Synchrony typically decays with increasing interpopulation distance. Spatial synchrony, and its distance decay, might reflect distance decay of environmental synchrony (the Moran effect), and/or short-distance dispersal. However, short-distance dispersal can synchronize entire metapopulations if within-patch dynamics are cyclic, a phenomenon known as phase locking. We manipulated the presence/absence of short-distance dispersal and spatially decaying environmental synchrony and examined their separate and interactive effects on the synchrony of the protist prey species Tetrahymena pyriformis growing in spatial arrays of patches (laboratory microcosms). The protist predator Euplotes patella consumed Tetrahymena and generated predator-prey cycles. Dispersal increased prey synchrony uniformly over both short and long distances, and did so by entraining the phases of the predator-prey cycles. The Moran effect also increased prey synchrony, but only over short distances where environmental synchrony was strongest, and did so by increasing the synchrony of stochastic fluctuations superimposed on the predator-prey cycle. Our results provide the first experimental demonstration of distance decay of synchrony due to distance decay of the Moran effect. Distance decay of the Moran effect likely explains distance decay of synchrony in many natural systems. Our results also provide an experimental demonstration of long-distance phase locking, and explain why cyclic populations provide many of the most dramatic examples of long-distance spatial synchrony in nature.