Predator–prey interactions in a grassland food chain vary with temperature and food quality

Because species interactions are often context‐dependent, abiotic factors such as temperature and biotic factors such as food quality may alter species interactions with potential consequences to ecosystem structure and function. For example, altered predator–prey interactions may influence the dynamics of trophic cascades, affecting net primary production. In a three‐year field experiment, we manipulated a plant–grasshopper–spider food chain in mesic tallgrass prairie to investigate the effects of temperature and food quality on grasshopper performance, and to understand the direct and indirect tritrophic interactions that contribute to trophic cascades. Because spiders are active at cooler temperatures than grasshoppers in our system, we hypothesized that predator effects would be strongest in cooled treatments, and weakest in warmed treatments. Grasshopper spider interactions were highly context‐dependent and varied significantly with food quality, temperature treatment and year. Spiders most often reduced grasshopper survival in the cooled and ambient temperature treatments, but had little to no effect on grasshopper survival in the warmed treatments, as hypothesized. In some years, plants compensated for grasshopper herbivory and trophic cascades were not observed despite significant effects of predators on grasshopper survival. However, in the year they were observed, trophic cascades only occurred in cooled treatments where predator effects on grasshoppers were strongest. Predicting ecosystem responses to climate change will require an understanding of how temperature influences species interactions. Our results demonstrate that changes in daily temperature regimes can alter predator–prey interactions among arthropods with consequences for ecosystem processes such as primary production and the relative importance of top–down and bottom–up processes.     

Temperature alters food web body-size structure

The increased temperature associated with climate change may have important effects on body size and predator–prey interactions. The consequences of these effects for food web structure are unclear because the relationships between temperature and aspects of food web structure such as predator–prey body-size relationships are unknown. Here, we use the largest reported dataset for marine predator–prey interactions to assess how temperature affects predator–prey body-size relationships among different habitats ranging from the tropics to the poles. We found that prey size selection depends on predator body size, temperature and the interaction between the two. Our results indicate that (i) predator–prey body-size ratios decrease with predator size at below-average temperatures and increase with predator size at above-average temperatures, and (ii) that the effect of temperature on predator–prey body-size structure will be stronger at small and large body sizes and relatively weak at intermediate sizes. This systematic interaction may help to simplify forecasting the potentially complex consequences of warming on interaction strengths and food web stability.     

Predator diversity and environmental change modify the strengths of trophic and nontrophic interactions

Understanding the dependence of species interaction strengths on environmental factors and species diversity is crucial to predict community dynamics and persistence in a rapidly changing world. Nontrophic (e.g. predator interference) and trophic components together determine species interaction strengths, but the effects of environmental factors on these two components remain largely unknown. This impedes our ability to fully understand the links between environmental drivers and species interactions. Here, we used a dynamical modelling framework based on measured predator functional responses to investigate the effects of predator diversity, prey density, and temperature on trophic and nontrophic interaction strengths within a freshwater food web. We found that (i) species interaction strengths cannot be predicted from trophic interactions alone, (ii) nontrophic interaction strengths vary strongly among predator assemblages, (iii) temperature has opposite effects on trophic and nontrophic interaction strengths, and (iv) trophic interaction strengths decrease with prey density, whereas the dependence of nontrophic interaction strengths on prey density is concave up. Interestingly, the qualitative impacts of temperature and prey density on the strengths of trophic and nontrophic interactions were independent of predator identity, suggesting a general pattern. Our results indicate that taking multiple environmental factors and the nonlinearity of density‐dependent species interactions into account is an important step towards a better understanding of the effects of environmental variations on complex ecological communities. The functional response approach used in this study opens new avenues for (i) the quantification of the relative importance of the trophic and nontrophic components in species interactions and (ii) a better understanding how environmental factors affect these interactions and the dynamics of ecological communities.     

Temperature and prey density jointly influence trophic and non‐trophic interactions in multiple predator communities

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Interactive influence of biotic and abiotic cues on the plasticity of preferred body temperatures in a predator–prey system

The ability to modify phenotypes in response to heterogeneity of the thermal environment represents an important component of an ectotherm's non-genetic adaptive capacity. Despite considerable attention being dedicated to the study of thermally-induced developmental plasticity, whether or not interspecific interactions shape the plastic response in both a predator and its prey remains unknown. We tested several predictions about the joint influence of predator/prey scents and thermal conditions on the plasticity of preferred body temperatures (T (p)) in both actors of this interaction, using a dragonfly nymphs-newt larvae system. Dragonfly nymphs (Aeshna cyanea) and newt eggs (Ichthyosaura alpestris) were subjected to fluctuating cold and warm thermal regimes (7-12 and 12-22°C, respectively) and the presence/absence of a predator or prey chemical cues. Preferred body temperatures were measured in an aquatic thermal gradient (5-33°C) over a 24-h period. Newt T (p) increased with developmental temperature irrespective of the presence/absence of predator cues. In dragonflies, thermal reaction norms for T (p) were affected by the interaction between temperature and prey cues. Specifically, the presence of newt scents in cold regime lowered dragonfly T (p). We concluded that predator-prey interactions influenced thermally-induced plasticity of T (p) but not in a reciprocal fashion. The occurrence of frequency-dependent thermal plasticity may have broad implications for predator-prey population dynamics, the evolution of thermal biology traits, and the consequences of sustaining climate change within ecological communities.     

Climate change enhances the negative effects of predation risk on an intermediate consumer

Predators are a major source of stress in natural systems because their prey must balance the benefits of feeding with the risk of being eaten. Although this ‘fear’ of being eaten often drives the organization and dynamics of many natural systems, we know little about how such risk effects will be altered by climate change. Here, we examined the interactive consequences of predator avoidance and projected climate warming in a three‐level rocky intertidal food chain. We found that both predation risk and increased air and sea temperatures suppressed the foraging of prey in the middle trophic level, suggesting that warming may further enhance the top‐down control of predators on communities. Prey growth efficiency, which measures the efficiency of energy transfer between trophic levels, became negative when prey were subjected to predation risk and warming. Thus, the combined effects of these stressors may represent an important tipping point for individual fitness and the efficiency of energy transfer in natural food chains. In contrast, we detected no adverse effects of warming on the top predator and the basal resources. Hence, the consequences of projected warming may be particularly challenging for intermediate consumers residing in food chains where risk dominates predator‐prey interactions.     

The ecological consequences of environmentally induced phenotypic changes

Population dynamics and species persistence are often mediated by species traits. Yet many important traits, like body size, can be set by resource availability and predation risk. Environmentally induced changes in resource levels or predation risk may thus have downstream ecological consequences. Here, we assess whether quantity and type of resources affect the phenotype, the population dynamics, and the susceptibility to predation of a mixotrophic protist through experiments and a model. We show that cell shape, but not size, changes with resource levels and type, and is linked to carrying capacity, thus affecting population dynamics. Also, these changes lead to differential susceptibility to predation, with direct consequences for predator‐prey dynamics. We describe important links between environmental changes, traits, population dynamics and ecological interactions, that underscore the need to further understand how trait‐mediated interactions may respond to environmental shifts in resource levels in an increasingly changing world.     

The relevance of food peak architecture in trophic interactions

Phenological shifts and associated changes in the temporal match between trophic levels have been a major focus of the study of ecological consequences of climate change. Previously, the food peak has been thought to respond as an entity to warming temperatures. However, food peak architecture, that is, timings and abundances of prey species and the level of synchrony between them, determines the timing and shape of the food peak. We demonstrate this with a case example of three passerine prey species and their predator. We explored temporal trends in the timing, height, width, and peakedness of prey availabilities and explained their variation with food peak architecture and ambient temperatures of prebreeding and breeding seasons. We found a temporal match between the predator's breeding schedule and food availability. Temporal trends in the timing of the food peak or in the synchrony between the prey species were not found. However, the food peak has become wider and more peaked over time. With more peaked food availabilities, predator's breeding success will depend more on the temporal match between its breeding schedule and the food peak, ultimately affecting the timing of breeding in the predator population. The height and width of the food peak depended on the abundances and breeding season lengths of individual prey species and their reciprocal synchronies. Peakednesses of separate prey species' availability distributions alone explained the peakedness of the food peak. Timing and quantity of food production were associated with temperatures of various time periods with variable relevance in different prey species. Alternating abundances of early and late breeding prey species caused high annual fluctuation in the timing of the food peak. Interestingly, the food peak may become later even when prey species' schedules are advanced. Climate warming can thus produce unexpected changes in the food availabilities, intervening in trophic interactions.     

Climate change effects on behavioral and physiological ecology of predator–prey interactions: Implications for conservation biological control

Habitat management under the auspices of conservation biological control is a widely used approach to foster conditions that ensure a diversity of predator species can persist spatially and temporally within agricultural landscapes in order to control their prey (pest) species. However, an emerging new factor, global climate change, has the potential to disrupt existing conservation biological control programs. Climate change may alter abiotic conditions such as temperature, precipitation, humidity and wind that in turn could alter the life-cycle timing of predator and prey species and the behavioral nature and strength of their interactions. Anticipating how climate change will affect predator and prey communities represents an important research challenge. We present a conceptual framework—the habitat domain concept—that is useful for understanding contingencies in the nature of predator diversity effects on prey based on predator and prey spatial movement in their habitat. We illustrate how this framework can be used to forecast whether biological control by predators will become more effective or become disrupted due to changing climate. We discuss how changes in predator–prey interactions are contingent on the tolerances of predators and prey species to changing abiotic conditions as determined by the degree of local adaptation and phenotypic plasticity exhibited by species populations. We conclude by discussing research approaches that are needed to help adjust conservation biological control management to deal with a climate future.     

Coevolution in Multispecific Interactions among Free-Living Species

Ecological interactions among species are the backbone of biodiversity. Interactions take a tremendous variety of forms in nature and have pervasive consequences for the population dynamics and evolution of species. A persistent challenge in evolutionary biology has been to understand how coevolution has produced complex webs of interacting species, where a large number of species interact through mutual dependences (e.g., mutualisms) or influences (e.g., predator–prey interactions in food webs). Recent work on megadiverse species assemblages in ecological communities has uncovered interesting repeated patterns that emerge in these complex networks of multispecies interactions. They include the presence of a core of super- generalists, proper patterns of interaction (that resemble nested chinese boxes), and multiple modules that act as the basic blocks of the complex network. The structure of multispecies interactions resembles other complex networks and is central to understanding its evolution and the consequences of species losses for the persistence of the whole network. These patterns suggest both precise ways on how coevolution goes on beyond simple pairwise interactions and scales up to whole communities.     

Temperature,predator–prey interaction strength and population stability

Warming could strongly stabilize or destabilize populations and food webs by changing the interaction strengths between predators and their prey. Predicting the consequences of warming requires understanding how temperature affects ingestion (energy gain) and metabolism (energy loss). Here, we studied the temperature dependence of metabolism and ingestion in laboratory experiments with terrestrial arthropods (beetles and spiders). From this data, we calculated ingestion efficiencies (ingestion/metabolism) and per capita interaction strengths in the short and long term. Additionally, we investigated if and how body mass changes these temperature dependencies. For both predator groups, warming increased metabolic rates substantially, whereas temperature effects on ingestion rates were weak. Accordingly, the ingestion efficiency (the ratio of ingestion to metabolism) decreased in all treatments. This result has two possible consequences: on the one hand, it suggests that warming of natural ecosystems could increase intrinsic population stability, meaning less fluctuations in population density; on the other hand, decreasing ingestion efficiencies may also lead to higher extinction risks because of starvation. Additionally, predicted long‐term per capita interaction strengths decreased with warming, which suggests an increase in perturbation stability of populations, i.e., a higher probability of returning to the same equilibrium density after a small perturbation. Together, these results suggest that warming has complex and potentially profound effects on predator–prey interactions and food‐web stability.     

Warming up the system: higher predator feeding rates but lower energetic efficiencies

Predictions on the consequences of the rapidly increasing atmospheric CO₂ levels and associated climate warming for population dynamics, ecological community structure and ecosystem functioning depend on mechanistic energetic models of temperature effects on populations and their interactions. However, such mechanistic approaches combining warming effects on metabolic (energy loss of organisms) and feeding rates (energy gain by organisms) remain a key, yet elusive, goal. Aiming to fill this void, we studied the metabolic rates and functional responses of three differently sized, predatory ground beetles on one mobile and one more resident prey species across a temperature gradient (5, 10, 15, 20, 25 and 30 °C). Synthesizing metabolic and functional‐response theory, we develop novel mechanistic predictions how predator–prey interaction strengths (i.e., functional responses) should respond to warming. Corroborating prior theory, warming caused strong increases in metabolism and decreases in handling time. Consistent with our novel model, we found increases in predator attack rates on a mobile prey, whereas attack rates on a mostly resident prey remained constant across the temperature gradient. Together, these results provide critically important information that environmental warming generally increases the direct short‐term per capita interaction strengths between predators and their prey as described by functional‐response models. Nevertheless, the several fold stronger increase in metabolism with warming caused decreases in energetic efficiencies (ratio of per capita feeding rate to metabolic rate) for all predator–prey interactions. This implies that warming of natural ecosystems may dampen predator–prey oscillations thus stabilizing their dynamics. The severe long‐term implications; however, include predator starvation due to energetic inefficiency despite abundant resources.     

Size‐based ecological interactions drive food web responses to climate warming

Predicting climate change impacts on animal communities requires knowledge of how physiological effects are mediated by ecological interactions. Food‐dependent growth and within‐species size variation depend on temperature and affect community dynamics through feedbacks between individual performance and population size structure. Still, we know little about how warming affects these feedbacks. Using a dynamic stage‐structured biomass model with food‐, size‐ and temperature‐dependent life history processes, we analyse how temperature affects coexistence, stability and size structure in a tri‐trophic food chain, and find that warming effects on community stability depend on ecological interactions. Predator biomass densities generally decline with warming – gradually or through collapses – depending on which consumer life stage predators feed on. Collapses occur when warming induces alternative stable states via Allee effects. This suggests that predator persistence in warmer climates may be lower than previously acknowledged and that effects of warming on food web stability largely depend on species interactions.     

Rapid prey evolution and the dynamics of two-predator food webs

Traits affecting ecological interactions can evolve on the same time scale as population and community dynamics, creating the potential for feedbacks between evolutionary and ecological dynamics. Theory and experiments have shown in particular that rapid evolution of traits conferring defense against predation can radically change the qualitative dynamics of a predator–prey food chain. Here, we ask whether such dramatic effects are likely to be seen in more complex food webs having two predators rather than one, or whether the greater complexity of the ecological interactions will mask any potential impacts of rapid evolution. If one prey genotype can be well-defended against both predators, the dynamics are like those of a predator–prey food chain. But if defense traits are predator-specific and incompatible, so that each genotype is vulnerable to attack by at least one predator, then rapid evolution produces distinctive behaviors at the population level: population typically oscillate in ways very different from either the food chain or a two-predator food web without rapid prey evolution. When many prey genotypes coexist, chaotic dynamics become likely. The effects of rapid evolution can still be detected by analyzing relationships between prey abundance and predator population growth rates using methods from functional data analysis.     

Effects of warming on predator–prey interactions – a resource‐based approach and a theoretical synthesis

We theoretically explore consequences of warming for predator–prey dynamics, broadening previous approaches in three ways: we include beyond‐optimal temperatures, predators may have a type III functional response, and prey carrying capacity depends on explicitly modelled resources. Several robust patterns arise. The relationship between prey carrying capacity and temperature can range from near‐independence to monotonically declining/increasing to hump‐shaped. Predators persist in a U‐shaped region in resource supply (=enrichment)‐temperature space. Type II responses yield stable persistence in a U‐shaped band inside this region, giving way to limit cycles with enrichment at all temperatures. In contrast, type III responses convey stability at intermediate temperatures and confine cycles to low and high temperatures. Warming‐induced state shifts can be predicted from system trajectories crossing stability and persistence boundaries in enrichment‐temperature space. Results of earlier studies with more restricted assumptions map onto this graph as special cases. Our approach thus provides a unifying framework for understanding warming effects on trophic dynamics.     

Using functional response modeling to investigate the effect of temperature on predator feeding rate and energetic efficiency

Temperature is one of the most important environmental parameters influencing all the biological processes and functions of poikilothermic organisms. Although extensive research has been carried out to evaluate the effects of temperature on animal life histories and to determine the upper and lower temperature thresholds as well as the optimal temperatures for survival, development, and reproduction, few studies have investigated links between thermal window, metabolism, and trophic interactions such as predation. We developed models and conducted laboratory experiments to investigate how temperature influences predator-prey interaction strengths (i.e., functional response) using a ladybeetle larva feeding on aphid prey. As predicted by the metabolic theory of ecology, we found that handling time exponentially decreases with warming, but--in contrast with this theory--search rate follows a hump-shaped relationship with temperature. An examination of the model reveals that temperature thresholds for predation depend mainly on search rate, suggesting that predation rate is primarily determined by searching activities and secondly by prey handling. In contrast with prior studies, our model shows that per capita short-term predator-prey interaction strengths and predator energetic efficiency (per capita feeding rate relative to metabolism) generally increase with temperature, reach an optimum, and then decrease at higher temperatures. We conclude that integrating the concept of thermal windows in short- and long-term ecological studies would lead to a better understanding of predator-prey population dynamics at thermal limits and allow better predictions of global warming effects on natural ecosystems.     

The long‐term impacts of predators on prey: inducible defenses,population dynamics,and indirect effects

Despite the amount of research on the inducible defenses of prey against predators, our understanding of the long‐term significance of non‐lethal predators on prey phenotypes, prey population dynamics, and community structure has rarely been explored. Our objectives were to assess the effects of predators on prey defenses, prey population dynamics, and the relative magnitude of density‐ versus trait‐mediated indirect interactions (DMIIs and TMIIs) over multiple prey generations. Using a freshwater snail and three common snail predators, we constructed a series of community treatments with pond mesocosms that manipulated trophic structure, the identity of the top predator, and whether predators were caged or uncaged. We quantified snail phenotypes, snail population size, and resource abundance over multiple snail generations. We found that snails were expressing inducible defenses in our system although the magnitude of the responses varied over time and across predator species. Despite the expression of inducible defenses, caged predators did not reduce snail population size. There also was no evidence of TMIIs throughout the experiment suggesting that TMIIs have a minimal role in the long‐term structure of our communities. The absence of TMIIs was largely driven by the lack of predator‐induced reductions in resource consumption and the lack of consistent reductions in population size with predator cues. In contrast, we detected strong DMIIs associated with lethal predators suggesting that DMIIs are the dominant long‐term mechanism influencing community structure. Our results demonstrate that although predators can have significant effects on prey phenotypes and sometimes cause short‐term TMIIs, there may be few long‐term consequences of these responses on population dynamics and indirect interactions, at least within simple food webs. Research directed towards addressing the long‐term consequences of predator–prey interactions within communities will help to reveal whether the conclusions and predictions generated from short‐term experiments are applicable over ecological and evolutionary timescales.     

Local spatial structure and predator-prey dynamics: counterintuitive effects of prey enrichment

The Lotka-Volterra predator-prey model with prey density dependence shows the final prey density to be independent of its vital rates. This result assumes the community to be well mixed so that encounters between predators and prey occur as a product of the landscape densities, yet empirical evidence suggests that over small spatial scales this may not be the normal pattern. Starting from an individual-based model with neighborhood interactions and movements, a deterministic approximation is derived, and the effect of local spatial structure on equilibrium densities is investigated. Incorporating local movements and local interactions has important consequences for the community dynamics. Now the final prey density is very much dependent on its birth, death, and movement rates and in ways that seem counterintuitive. Increasing prey fecundity or mobility and decreasing the coefficient of competition can all lead to decreases in the final density of prey if the predator is also relatively immobile. However, analysis of the deterministic approximation makes the mechanism for these results clear; each of these changes subtly alters the emergent spatial structure, leading to an increase in the predator-prey spatial covariance at short distances and hence to a higher predation pressure on the prey.     

Influence of density dependence on predator-prey seabird interactions at large spatio-temporal scales

Theoretical investigations of competitive dynamics have noted that numbers of predator and prey influence each other. However, few empirical studies have demonstrated how a life-history trait of the prey (such as fecundity) can be affected simultaneously by its own density and the density of predators. For instance, density dependence can reduce fecundity with increasing number of prey, while inverse density dependence or Allee effects may occur especially when the prey is a social organism. Here we analysed an intraguild predator-prey system of two seabird species at a large spatio-temporal scale. As expected, we found that fecundity of prey was negatively affected by predator density. Nevertheless, fecundity of prey also increased nonlinearly with its own density and strikingly with the prey-predator ratio. Small groups of prey were probably not able to defend their nests especially against large number of predators. At the highest prey densities (i.e. when anti-predator strategies should be most efficient), prey fecundity also lowered, suggesting the appearance of density dependence mediated by food competition. Allee effects and density dependence occurred across a broad range of population sizes of both the prey and the predator at several local populations facing different ecological environments.     

When is overkill optimal? Tritrophic interactions reveal new insights into venom evolution

Organisms embedded within food webs must balance arms races with their predators and prey. For venom users, venom may mediate each arms race, but the dynamical evolutionary changes in venom production in response to the two arms races are still poorly understood. Here, we use a simple model to evaluate the evolutionary response of a venomous consumer to the presence of an apex generalist predator and evolution of the consumer’s prey. We find that introduction of the apex predator can weaken the arms race between the two lower trophic levels. In addition, when consumer prey capture and predator defense venoms functionally overlap, a reduced evolutionary response in the prey population can drive investment in venom used for prey capture going beyond what is optimal for subduing prey. These dynamics suggest that interactions with multiple trophic levels can substantially alter the venom complexity in predatory venomous animals and may explain the paradox of the overkill hypothesis.