Predation risk influences food‐web structure by constraining species diet choice

The foraging behaviour of species determines their diet and, therefore, also emergent food‐web structure. Optimal foraging theory (OFT) has previously been applied to understand the emergence of food‐web structure through a consumer‐centric consideration of diet choice. However, the resource‐centric viewpoint, where species adjust their behaviour to reduce the risk of predation, has not been considered. We develop a mechanistic model that merges metabolic theory with OFT to incorporate the effect of predation risk on diet choice to assemble food webs. This ‘predation‐risk‐compromise’ (PR) model better captures the nestedness and modularity of empirical food webs relative to the classical optimal foraging model. Specifically, compared with optimal foraging alone, risk‐mitigated foraging leads to more‐nested but less‐modular webs by broadening the diet of consumers at intermediate trophic levels. Thus, predation risk significantly affects food‐web structure by constraining species’ ability to forage optimally, and needs to be considered in future work.     

Rainfall variability maintains grass‐forb species coexistence

Environmental variability can structure species coexistence by enhancing niche partitioning. Modern coexistence theory highlights two fluctuation‐dependent temporal coexistence mechanisms —the storage effect and relative nonlinearity – but empirical tests are rare. Here, we experimentally test if environmental fluctuations enhance coexistence in a California annual grassland. We manipulate rainfall timing and relative densities of the grass Avena barbata and forb Erodium botrys, parameterise a demographic model, and partition coexistence mechanisms. Rainfall variability was integral to grass–forb coexistence. Variability enhanced growth rates of both species, and early‐season drought was essential for Erodium persistence. While theoretical developments have focused on the storage effect, it was not critical for coexistence. In comparison, relative nonlinearity strongly stabilised coexistence, where Erodium experienced disproportionately high growth under early‐season drought due to competitive release from Avena. Our results underscore the importance of environmental variability and suggest that relative nonlinearity is a critical if underappreciated coexistence mechanism.     

The Impact of Physiological Demands on Foraging Decisions under Predation Risk: A Test with the Whelk Acanthina monodon

We study whether and how physiological demands affect foraging decisions under predation risk, by evaluating the effect of starvation on the rate of food consumption and prey‐size preferences and the potential trade‐off between starvation and predation risk on foraging behavior in the whelk Acanthina monodon, a gastropod inhabiting the intertidal rocky shores of central Chile. These whelks appear to adjust their foraging strategy to physiological (nutritional) demand and predation risk. Starvation reduced the effect of predation risk on the rate of food consumption by A. monodon. Thus, in the absence of the predator sea star, the rate of food consumption by starved and satiated whelks was similar. When a predator was present, starved whelks fed faster than satiated whelks. Our results indicate that foraging behaviour represents an integrated and hierarchical response to environmental conditions and the physiological conditions of the forager.     

How to quantify the temporal storage effect using simulations instead of math

The storage effect has become a core concept in community ecology, explaining how environmental fluctuations can promote coexistence and maintain biodiversity. However, limitations of existing theory have hindered empirical applications: the need for detailed mathematical analysis whenever the study system requires a new model, and restricted theory for structured populations. We present a new approach that overcomes both these limitations. We show how temporal storage effect can be quantified by Monte Carlo simulations in a wide range of models for competing species. We use the lottery model and a generic integral projection model (IPM) to introduce ideas, and present two empirical applications: (1) algal species in a chemostat with variable temperature, showing that the storage effect can operate without a long‐lived life stage and (2) a sagebrush steppe community IPM. Our results highlight the need for careful modelling of nonlinearities so that conclusions are not driven by unrecognised model constraints.     

Mechanisms of species coexistence: a field test of theoretical models using intertidal snails

Competitor coexistence is often facilitated by spatial segregation. Traditionally, spatial segregation is predicted to occur when species differ in the habitat in which they are either superior at competing for resources or less susceptible to predation. However, predictions from a behavioural model demonstrate that spatial segregation and coexistence can also occur in the absence of such interspecific trade‐offs in competitive ability and vulnerability to predation. Unlike other models of competitor coexistence this model predicts that when species rank both habitat productivity and ‘riskinesses’ similarly, but differ slightly in their habitat‐specific vulnerabilities to predators, they will tend to segregate across habitats, with the species experiencing the higher ratio of mortality risk across the habitats occurring primarily in the safer habitat. Here, we investigate the hypothesis that intraspecific trade‐offs between resource availability and mortality risk can lead to spatial segregation of competing species by (1) documenting the spatial (i.e. intertidal) distribution of two marine snails, Littorina sitkana and L. subrotundata and (2) performing field experiments to quantify growth and mortality rates of each species at ‘low’ and ‘high’ intertidal heights. Our results indicate that both species agree on the rankings of habitat riskiness and productivity, experiencing higher predation and higher growth in low‐ than in high‐intertidal habitats. However, L. sitkana and L. subrotundata experienced differences in their habitat‐specific mortality risks and growth rates. Despite both species being similarly at risk of predation in high‐intertidal habitats (where mortality was lower), L. subrotundata was subject to significantly higher mortality than L. sitkana at the low‐intertidal height. In contrast, growth rate differences between habitats were greater for L. sitkana than for L. subrotundata. Whereas both species grew at the same rate at the high‐intertidal level (where growth was lower), L. sitkana individuals grew more rapidly than L. subrotundata snails at the low‐intertidal level. As predicted by the behavioural model, the species that experienced the higher ratio of mortality across habitats (i.e. L. subrotundata) occurred exclusively in the safer, high‐intertidal habitat. Taken together, these results provide support for the hypothesis that spatial segregation, and potentially competitor coexistence, can occur in the absence of interspecific trade‐offs in resource acquisition ability or vulnerability to predation.     

Transient dynamics limit the effectiveness of keystone predation in bringing about coexistence

We analyze the transient dynamics of simple models of keystone predation, in which a predator preferentially consumes the dominant of two (or more) competing prey species. We show that coexistence is unlikely in many systems characterized both by successful invasion of either prey species into the food web that lacks it and by a stable equilibrium with high densities of all species. Invasion of the predator-resistant consumer species often causes the resident, more vulnerable prey to crash to such low densities that extinction would occur for many realistic population sizes. Subsequent transient cycles may entail very low densities of the predator or of the initially successful invader, which may also preclude coexistence of finite populations. Factors causing particularly low minimum densities during the transient cycles include biotic limiting resources for the prey, limited resource partitioning between the prey, a highly efficient predator with relatively slow dynamics, and a vulnerable prey whose population dynamics are rapid relative to the less vulnerable prey. Under these conditions, coexistence of competing prey via keystone predation often requires that the prey's competitive or antipredator characteristics fall within very narrow ranges. Similar transient crashes are likely to occur in other food webs and food web models.     

Field evidence of trait-mediated indirect interactions in a rocky intertidal food web

Studies on the implications of food web interactions to community structure have often focused on density-mediated interactions between predators and their prey. This approach emphasizes the importance of predator regulation of prey density via consumption (i.e. lethal effects), which, in turn, leads to cascading effects on the prey's resources. A more recent and contrasting view emphasizes the importance of non-lethal predator effects on prey traits (e.g. behaviour, morphology), or trait-mediated interactions. On rocky intertidal shores in New England, green crab ( Carcinus maenas ) predation is thought to be important to patterns of algal abundance and diversity by regulating the density of herbivorous snails ( Littorina littorea ). We found, however, that risk cues from green crabs can dramatically suppress snail grazing, with large effects on fucoid algal communities. Our results suggest that predator-induced changes in prey behaviour may be an important and under-appreciated component of food web interactions and community dynamics on rocky intertidal shores.     

Quantifying predator dependence in the functional response of generalist predators

A long‐standing debate concerns how functional responses are best described. Theory suggests that ratio dependence is consistent with many food web patterns left unexplained by the simplest prey‐dependent models. However, for logistical reasons, ratio dependence and predator dependence more generally have seen infrequent empirical evaluation and then only so in specialist predators, which are rare in nature. Here we develop an approach to simultaneously estimate the prey‐specific attack rates and predator‐specific interference (facilitation) rates of predators interacting with arbitrary numbers of prey and predator species in the field. We apply the approach to surveys and experiments involving two intertidal whelks and their full suite of potential prey. Our study provides strong evidence for predator dependence that is poorly described by the ratio dependent model over manipulated and natural ranges of species abundances. It also indicates how, for generalist predators, even the qualitative nature of predator dependence can be prey‐specific.     

Temporal stability of European rocky shore assemblages: variation across a latitudinal gradient and the role of habitat‐formers

Compensatory dynamics, overyielding and statistical averaging are mechanisms promoting the temporal stability of natural communities. Using the model of European intertidal rocky shore assemblages and collating 17 datasets, we investigated how the strength of these stability‐enhancing mechanisms varies with latitude and how it can be altered by the loss of habitat‐formers (e.g. canopy‐forming macroalgae). Community stability decreased with increasing latitude, mostly as a consequence of a greater synchronization of species fluctuations. Statistical averaging and overyielding (i.e. richness effect) promoted stability, but their strength did not vary with latitude. An experimental removal of macroalgal canopies caused a strengthening of the statistical averaging effect that was consistent across the latitudinal gradient investigated. Nonetheless, the loss of canopies depressed stability by enhancing the synchronization of species fluctuations on southernmost shores, while it had weak effects on shores at higher latitudes. Variation in life‐history traits among canopy‐forming species and/or in prevailing environmental conditions across a gradient of latitude could underlie variable effects of habitat‐formers on species fluctuations. Our study shows 1) that the stability of intertidal assemblages and strength of compensatory dynamics varies with latitude, 2) that canopy‐forming macroalgae, exerting a strong control on understorey species, can influence the strength of compensatory dynamics and 3) that biological forcing (i.e. facilitation) can be as important as environmental forcing in enhancing the synchronization of species fluctuations.     

Community regulation: the relative importance of recruitment and predation intensity of an intertidal community dominant in a seascape context

Predicting the strength and context-dependency of species interactions across multiple scales is a core area in ecology. This is especially challenging in the marine environment, where populations of most predators and prey are generally open, because of their pelagic larval phase, and recruitment of both is highly variable. In this study we use a comparative-experimental approach on small and large spatial scales to test the relationship between predation intensity and prey recruitment and their relative importance in shaping populations of a dominant rocky intertidal space occupier, mussels, in the context of seascape (availability of nearby subtidal reef habitat). Predation intensity on transplanted mussels was tested inside and outside cages and recruitment was measured with standard larval settlement collectors. We found that on intertidal rocky benches with contiguous subtidal reefs in New Zealand, mussel larval recruitment is usually low but predation on recruits by subtidal consumers (fish, crabs) is intense during high tide. On nearby intertidal rocky benches with adjacent sandy subtidal habitats, larval recruitment is usually greater but subtidal predators are typically rare and predation is weaker. Multiple regression analysis showed that predation intensity accounts for most of the variability in the abundance of adult mussels compared to recruitment. This seascape-dependent, predation-recruitment relationship could scale up to explain regional community variability. We argue that community ecology models should include seascape context-dependency and its effects on recruitment and species interactions for better predictions of coastal community dynamics and structure.     

Predicting food‐web structure with metacommunity models

Synthesis Metacommunity theory aims to elucidate the relative influence of local and regional‐scale processes in generating diversity patterns across the landscape. Metacommunity research has focused largely on assemblages of competing organisms within a single trophic level. Here, we test the ability of metacommunity models to predict the network structure of the aquatic food web found in the leaves of the northern pitcher plant Sarracenia purpurea. The species‐sorting and patch‐dynamics models most accurately reproduced nine food web properties, suggesting that local‐scale interactions play an important role in structuring Sarracenia food webs. Our approach can be applied to any well‐resolved food web for which data are available from multiple locations. The metacommunity framework explores the relative influence of local and regional‐scale processes in generating diversity patterns across the landscape. Metacommunity models and empirical studies have focused mostly on assemblages of competing organisms within a single trophic level. Studies of multi‐trophic metacommunities are predominantly restricted to simplified trophic motifs and rarely consider entire food webs. We tested the ability of the patch‐dynamics, species‐sorting, mass‐effects, and neutral metacommunity models, as well as three hybrid models, to reproduce empirical patterns of food web structure and composition in the complex aquatic food web found in the northern pitcher plant Sarracenia purpurea. We used empirical data to determine regional species pools and estimate dispersal probabilities, simulated local food‐web dynamics, dispersed species from regional pools into local food webs at rates based on the assumptions of each metacommunity model, and tested their relative fits to empirical data on food‐web structure. The species‐sorting and patch‐dynamics models most accurately reproduced nine food web properties, suggesting that local‐scale interactions were important in structuring Sarracenia food webs. However, differences in dispersal abilities were also important in models that accurately reproduced empirical food web properties. Although the models were tested using pitcher‐plant food webs, the approach we have developed can be applied to any well‐resolved food web for which data are available from multiple locations.     

Climate‐driven trends and ecological implications of event‐scale upwelling in the California Current System

Eastern boundary current systems are among the most productive and lucrative ecosystems on Earth because they benefit from upwelling currents. Upwelling currents subsidize the base of the coastal food web by bringing deep, cold and nutrient‐rich water to the surface. As upwelling is driven by large‐scale atmospheric patterns, global climate change has the potential to affect a wide range of significant ecological processes through changes in water chemistry, water temperature, and the transport processes that influence species dispersal and recruitment. We examined long‐term trends in the frequency, duration, and strength of continuous upwelling events for the Oregon and California regions of the California Current System in the eastern Pacific Ocean. We then associated event‐scale upwelling with up to 21 years of barnacle and mussel recruitment, and water temperature data measured at rocky intertidal field sites along the Oregon coast. Our analyses suggest that upwelling events are changing in ways that are consistent with climate change predictions: upwelling events are becoming less frequent, stronger, and longer in duration. In addition, upwelling events have a quasi‐instantaneous and cumulative effect on rocky intertidal water temperatures, with longer events leading to colder temperatures. Longer, more persistent upwelling events were negatively associated with barnacle recruitment but positively associated with mussel recruitment. However, since barnacles facilitate mussel recruitment by providing attachment sites, increased upwelling persistence could have indirect negative impacts on mussel populations. Overall, our results indicate that changes in coastal upwelling that are consistent with climate change predictions are altering the tempo and the mode of environmental forcing in near‐shore ecosystems, with potentially severe and discontinuous ramifications for ecosystem structure and functioning.     

Thermal acclimation modulates the impacts of temperature and enrichment on trophic interaction strengths and population dynamics

Global change affects individual phenotypes and biotic interactions, which can have cascading effects up to the ecosystem level. However, the role of environmentally induced phenotypic plasticity in species interactions is poorly understood, leaving a substantial gap in our knowledge of the impacts of global change on ecosystems. Using a cladoceran–dragonfly system, we experimentally investigated the effects of thermal acclimation, acute temperature change and enrichment on predator functional response and metabolic rate. Using our experimental data, we next parameterized a population dynamics model to determine the consequences of these effects on trophic interaction strength and food‐chain stability. We found that (1) predation and metabolic rates of the dragonfly larvae increase with acute warming, (2) warm‐acclimated larvae have a higher maximum predation rate than cold‐acclimated ones, and (3) long‐term interaction strength increases with enrichment but decreases with both acclimation and acute temperatures. Overall, our experimental results show that thermal acclimation can buffer negative impacts of environmental change on predators and increase food‐web stability and persistence. We conclude that the effect of acclimation and, more generally, phenotypic plasticity on trophic interactions should not be overlooked if we aim to understand the effects of climate change and enrichment on species interaction strength and food‐web stability.     

Environmental fluctuations can stabilize food web dynamics by increasing synchrony

Natural food webs are species-rich, but classical theory suggests that they should be unstable and extinction-prone. Asynchronous fluctuations in the densities of competing consumers can stabilize food web dynamics in constant environments. However, environmental fluctuations often synchronize dynamics in nature. Using the same 'diamond-shape' food web model first used to demonstrate the stabilizing effects of asynchrony in constant environments, we show that weak-to-moderate environmentally induced fluctuations in consumer mortality rates stabilize food webs while disrupting asynchrony. Synchrony actually promotes stability because: (i) synchronous declines in consumer density reduce the maximum abundance of top predators and (ii) resource competition quickly converts synchronous increases in consumer density into synchronous declines. These results are robust to details of food web topology and the implementation of environmental fluctuations. The fluctuation strengths that enhance stability are within the range experienced naturally by many species, suggesting that stabilization via environmental fluctuations is a realistic possibility.     

Pyramids of species richness: the determinants and distribution of species diversity across trophic levels

How species richness is distributed across trophic levels determines several dimensions of ecosystem functioning, including herbivory, predation, and decomposition rates. We perform a meta‐analysis of 72 large published food webs to investigate their trophic diversity structure and possible endogenous, exogenous, and methodological causal variables. Consistent with classic theory, we found that published food webs can generally be described as ‘pyramids of species richness’. The food webs were more predator‐poor, prey‐rich and hierarchical than is expected by chance or by the niche or cascade models. The trophic species richness distribution also depended on centrality, latitude, ecosystem‐type and methodological bias. Although trophic diversity structure is generally pyramidal, under many conditions the structure is consistently uniform or inverse‐pyramidal. Our meta‐analysis adds nuance to classic assumptions about food web structure: diversity decreases with trophic level, but not under all conditions, and the decrease may be scale‐dependent. Synthesis The distribution of species richness across trophic levels has not been evaluated in recent decades, despite improvement in food web resolution and the relevance of biodiversity distribution to ecosystem function. Our meta‐analysis of 72 large, recent food webs, illustrates that published food webs can generally be described as basal‐rich, top‐poor ‘pyramids of species richness’, consistent with classic theory. Although trophic diversity structure is generally pyramidal, under some environmental and ecological conditions the structure is uniform or inverse‐pyramidal. Our meta‐analysis confirms classic theory about food web structure, while adding nuance by describing conditions under which classic pyramid structure is not observed.     

Water temperature, predation, and the neglected role of physiological rate effects in rocky intertidal communities

Ecologists and physiologists working on rocky shores have emphasizedthe effects of environmental stress on the distribution of intertidalorganisms. Although consumer stress models suggest that physicalextremes may often reduce predation and herbivory through negativeimpacts on the physiological performance of consumers, few fieldstudies have rigorously tested how environmental variation affectsfeeding rates. I review and analyze field experiments that quantifiedper capita feeding rates of a keystone predator, the sea starPisaster ochraceus, in relation to aerial heat stress, waveforces, and water temperature at three rocky intertidal siteson the Oregon coast. Predation rates during 14-day periods wereunrelated to aerial temperature, but decreased significantlywith decreasing water temperature. There was suggestive butinconclusive evidence that predation rates also declined withincreasing wave forces. Data-logger records suggested that thermalstress was rare in the wave-exposed habitats that I studied;sea star body temperatures likely reached warm levels (>24°C)on only 9 dates in 3 yr. In contrast, wind-driven upwellingregularly generated 3 to 5°C fluctuations in water temperature,and field and laboratory results suggest that such changes significantlyalter feeding rates of Pisaster. These physiological rate effects,near the center of an organism's thermal range, may not reducegrowth or fitness, and thus are distinct from the effects ofenvironmental stress. This study underscores the need to considerorganismal responses both under "normal" conditions, as wellas under extreme conditions. Examining both kinds of responsesis necessary to understand how different components of environmentalvariation regulate physiological performance and the strengthof species interactions in intertidal communities.     

Exploring the temporal variability of a food web using long‐term biomonitoring data

Ecological communities are constantly being reshaped in the face of environmental change and anthropogenic pressures. Yet, how food webs change over time remains poorly understood. Food web science is characterized by a trade‐off between complexity (in terms of the number of species and feeding links) and dynamics. Topological analysis can use complex, highly resolved empirical food web models to explore the architecture of feeding interactions but is limited to a static view, whereas ecosystem models can be dynamic but use highly aggregated food webs. Here, we explore the temporal dynamics of a highly resolved empirical food web over a time period of 18 years, using the German Bight fish and benthic epifauna community as our case study. We relied on long‐term monitoring ecosystem surveys (from 1998 to 2015) to build a metaweb, i.e. the meta food web containing all species recorded over the time span of our study. We then combined time series of species abundances with topological network analysis to construct annual food web snapshots. We developed a new approach, ‘node‐weighted’ food web metrics by including species abundances to represent the temporal dynamics of food web structure, focusing on generality and vulnerability. Our results suggest that structural food web properties change through time; however, binary food web structural properties may not be as temporally variable as the underlying changes in species composition. Further, the node‐weighted metrics enabled us to detect that food web structure was influenced by changes in species composition during the first half of the time series and more strongly by changes in species dominance during the second half. Our results demonstrate how ecosystem surveys can be used to monitor temporal changes in food web structure, which are important ecosystem indicators for building marine management and conservation plans.     

Optimal intraguild foraging and population stability

This article explores effects of adaptive intraguild predation on species coexistence and community structure in three species' food webs. Two Lotka-Volterra models that assume a trade-off between competition and predation strength are considered in detail. The first model does not explicitly model resource dynamics and is considered with both nonadaptive and adaptive intraguild predation; in the latter case predators choose their diet in order to maximize their instantaneous population growth rate. The second model includes resource population dynamics. Effects of adaptive intraguild predation on the community structure along a gradient in environment productivity are analyzed and compared with some experimental results of protist food webs. Conditions under which intraguild predation is adaptive are discussed for both models. It is proved that if intraguild predators are perfect optimizers then intraguild predation should decrease with increasing environmental productivity and adaptive intraguild predation is a stabilizing factor provided environmental productivity is high enough.