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.     

Enrichment can damp population cycles: a balance of inflexible and flexible interactions

Destabilization of one predator–one prey systems with an increase in nutrient input has been viewed as a paradox. We report that enrichment can damp population cycles by a food‐web structure that balances inflexible and flexible interaction links (i.e. specialist and generalist predators). We modeled six predator–prey systems involving three or four species in which the predators practice optimal foraging based on prey profitability determined by handling time. In all models, the balance of interaction links simultaneously decreased the amplitude of population oscillations and increased the minimum density with increasing enrichment, leading to a potential theoretical resolution of the paradox of enrichment in non‐equilibrium dynamics. The stabilization mechanism was common to all of the models. Important previous studies on the stability of food webs have also demonstrated that a balance of interaction strengths stabilizes systems, suggesting a general rule of ecosystem stability.     

Influence of intra‐ and interspecific variation in predator–prey body size ratios on trophic interaction strengths

1. Predation is a pervasive force that structures food webs and directly influences ecosystem functioning. The relative body sizes of predators and prey may be an important determinant of interaction strengths. However, studies quantifying the combined influence of intra‐ and interspecific variation in predator–prey body size ratios are lacking.
2. We use a comparative functional response approach to examine interaction strengths between three size classes of invasive bluegill and largemouth bass toward three scaled size classes of their tilapia prey. We then quantify the influence of intra‐ and interspecific predator–prey body mass ratios on the scaling of attack rates and handling times.
3. Type II functional responses were displayed by both predators across all predator and prey size classes. Largemouth bass consumed more than bluegill at small and intermediate predator size classes, while large predators of both species were more similar. Small prey were most vulnerable overall; however, differential attack rates among prey were emergent across predator sizes. For both bluegill and largemouth bass, small predators exhibited higher attack rates toward small and intermediate prey sizes, while larger predators exhibited greater attack rates toward large prey. Conversely, handling times increased with prey size, with small bluegill exhibiting particularly low feeding rates toward medium–large prey types. Attack rates for both predators peaked unimodally at intermediate predator–prey body mass ratios, while handling times generally shortened across increasing body mass ratios.
4. We thus demonstrate effects of body size ratios on predator–prey interaction strengths between key fish species, with attack rates and handling times dependent on the relative sizes of predator–prey participants.
5. Considerations for intra‐ and interspecific body size ratio effects are critical for predicting the strengths of interactions within ecosystems and may drive differential ecological impacts among invasive species as size ratios shift.

     

Body masses,functional responses and predator–prey stability

The stability of ecological communities depends strongly on quantitative characteristics of population interactions (type‐II vs. type‐III functional responses) and the distribution of body masses across species. Until now, these two aspects have almost exclusively been treated separately leaving a substantial gap in our general understanding of food webs. We analysed a large data set of arthropod feeding rates and found that all functional‐response parameters depend on the body masses of predator and prey. Thus, we propose generalised functional responses which predict gradual shifts from type‐II predation of small predators on equally sized prey to type‐III functional‐responses of large predators on small prey. Models including these generalised functional responses predict population dynamics and persistence only depending on predator and prey body masses, and we show that these predictions are strongly supported by empirical data on forest soil food webs. These results help unravelling systematic relationships between quantitative population interactions and large‐scale community patterns.     

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.     

Not attackable or not crackable—How pre‐ and post‐attack defenses with different competition costs affect prey coexistence and population dynamics

It is well‐known that prey species often face trade‐offs between defense against predation and competitiveness, enabling predator‐mediated coexistence. However, we lack an understanding of how the large variety of different defense traits with different competition costs affects coexistence and population dynamics. Our study focusses on two general defense mechanisms, that is, pre‐attack (e.g., camouflage) and post‐attack defenses (e.g., weaponry) that act at different phases of the predator—prey interaction. We consider a food web model with one predator, two prey types and one resource. One prey type is undefended, while the other one is pre‐ or post‐attack defended paying costs either by a higher half‐saturation constant for resource uptake or a lower maximum growth rate. We show that post‐attack defenses promote prey coexistence and stabilize the population dynamics more strongly than pre‐attack defenses by interfering with the predator's functional response: Because the predator spends time handling “noncrackable” prey, the undefended prey is indirectly facilitated. A high half‐saturation constant as defense costs promotes coexistence more and stabilizes the dynamics less than a low maximum growth rate. The former imposes high costs at low resource concentrations but allows for temporally high growth rates at predator‐induced resource peaks preventing the extinction of the defended prey. We evaluate the effects of the different defense mechanisms and costs on coexistence under different enrichment levels in order to vary the importance of bottom‐up and top‐down control of the prey community.     

Effects of prey-size and predator-instar on the predation of Daphnia by Notonecta

Abstract. 1. Attack rates and handling times are measured by a series of separate functional response experiments for each instar of Notonecta glauca attacking four size classes of Daphnia magna as prey. The resulting attack rate and handling time surfaces are complex, with maximum attack rates for small predators attacking small prey, and large predators attacking large prey. Adult Notonecta have lower attack rates than the two previous juvenile instars (4 and 5).
2. The literature on attack rates and handling times in other predator—prey interactions that involve a series of different predator and prey size or age classes is reviewed in the context of the Notonecta-Daphnia results. The data suggest that small predator instars will usually compete with large instars for food, unless there is spatial or temporal separation between them.
3. Complex attack rate and handling time surfaces are to be expected wherever a wide range of prey and predator sizes is involved.
4. Size related changes in attack rates and handling times can introduce very complex dynamics into predator-prey interactions.     

Functional responses of contrasting seed predator guilds to masting in two Mediterranean oak species

The predator satiation hypothesis poses that synchronous and variable seed production during masting events increases seed escape through seed predator satiation. The success of this strategy depends upon the type of consumer functional response, in this case defined as the change in seed consumption rate by a predator as a function of change in seed density. Type II (where the proportion of seed consumed is highest at low levels of seed availability) and type III (where the proportion of seed consumed is highest at some intermediate level of seed availability and then declines towards zero) functional responses describe negative density‐dependence and indicate predator satiation. The type of function response should be contingent upon herbivore traits: type II responses are predicted for dietary specialist predators with low mobility, and type III responses are predicted for highly mobile, dietary generalist predators. Surprisingly, most studies have not evaluated whether functional responses vary among seed predator guilds. Here we describe the functional responses at population and individual tree level of highly mobile generalist (birds and rodents) and less mobile specialist (insects) pre‐dispersal seed predators attacking acorns of two sympatric oaks (Quercus suber and Q. canariensis) over a 10‐year period. Our results showed that in most cases specialist seed predators exhibited the predicted type II functional response at both the individual tree and population level for both oak species. However, generalist seed predators did not exhibit the predicted type III response; instead, they also exhibited a type II response at the individual tree and population level for both oak species. By independently assessing the effects of multiple seed predators associated with the same host tree species, our work highlights the influence of herbivore traits on the outcome of plant–seed predator interactions in masting species, and thus furthers our understanding of the ecological and evolutionary mechanisms underlying masting behaviour.     

Omnivory and stability of food webs

The role and prevalence of omnivory, defined as feeding on more than one trophic level, are critical to understand food web structure and dynamics. Whether omnivory stabilizes or destabilizes food webs depends on the assumptions of theoretical models. Recently, Tanabe and Namba [Tanabe, K., Namba, T., 2005. Omivory creates chaos in simple food web models. Ecology 86, 3411–3414] found that omnivory can create chaos in a simple food web model with linear functional responses and 12 model parameters. In this paper, first we numerically examined bifurcation diagrams with all the parameters as bifurcation parameters, including self-limitation of the intermediate consumer and predator. Chaos spontaneously appears when the intraguild predator’s consumption rates are low for nutrient-rich intraguild prey and high for nutrient-poor basal resource and the intraguild prey reproduces efficiently feeding on the basal resource. Second, we investigated effects of the addition of a species into the basic model food web which exhibits chaos. The additional species is assumed to consume only one of the basal resource, intermediate consumer, or omnivorous predator. Consequences of the addition greatly depend on the trophic level on which the additional species feeds. While the increased diversity of predators feeding on the intermediate consumer stabilizes the web, the increased diversity of prey feeding on the basal resource induces collapse of the food web through exploitative competition for the basal resource. The food chain with the top predator feeding on the omnivorous predator is highly unstable unless the mortality of the top predator is extremely low. We discuss the possibility of real-world chaos and the reason why stability of food webs strongly depends on the topological structure of the webs. Finally, we consider the implications of our results for food web theory and resource management.     

Antagonistic and Synergistic Interactions Among Predators

The structure and dynamics of food webs are largely dependent upon interactions among consumers and their resources. However, interspecific interactions such as intraguild predation and interference competition can also play a significant role in the stability of communities. The role of antagonistic/synergistic interactions among predators has been largely ignored in food web theory. These mechanisms influence predation rates, which is one of the key factors regulating food web structure and dynamics, thus ignoring them can potentially limit understanding of food webs. Using nonlinear models, it is shown that critical aspects of multiple predator food web dynamics are antagonistic/synergistic interactions among predators. The influence of antagonistic/synergistic interactions on coexistence of predators depended largely upon the parameter set used and the degree of feeding niche differentiation. In all cases when there was no effect of antagonism or synergism (a _ij =1.00), the predators coexisted. Using the stable parameter set, coexistence occurred across the range of antagonism/synergism used. However, using the chaotic parameter strong antagonism resulted in the extinction of one or both species, while strong synergism tended to coexistence. Whereas using the limit cycle parameter set, coexistence was strongly dependent on the degree of feeding niche overlap. Additionally increasing the degree of feeding specialization of the predators on the two prey species increased the amount of parameter space in which coexistence of the two predators occurred. Bifurcation analyses supported the general pattern of increased stability when the predator interaction was synergistic and decreased stability when it was antagonistic. Thus, synergistic interactions should be more common than antagonistic interactions in ecological systems.     

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 acute and chronic temperature changes on the functional responses of the dogfish <Emphasis Type="Italic">Scyliorhinus canicula</Emphasis> (Linnaeus, 1758) towards amphipod prey <Emphasis Type="Italic">Echinogammarus marinus</Emphasis> (Leach, 1815)

Predation is a strong driver of population dynamics and community structure and it is essential to reliably quantify and predict predation impacts on prey populations in a changing thermal landscape. Here, we used comparative functional response analyses to assess how predator-prey interactions between dogfish and invertebrate prey change under different warming scenarios. The Functional Response Type, attack rate, handling time and maximum feeding rate estimates were calculated for Scyliorhinus canicula preying upon Echinogammarus marinus under temperatures of 11.3 °C and 16.3 °C, which represent both the potential daily variation and predicted higher summer temperatures within Strangford Lough, N. Ireland. A two x two design of “Predator Acclimated”, “Prey Acclimated”, “Both Acclimated”, and “Both Unacclimated” was implemented to test functional responses to temperature rise. Attack rate was higher at 11.3 °C than at 16.3 °C, but handling time was lower and maximum feeding rates were higher at 16.3 °C. Non-acclimated predators had similar maximum feeding rate towards non-acclimated and acclimated prey, whereas acclimated predators had significantly higher maximum feeding rates towards acclimated prey as compared to non-acclimated prey. Results suggests that the predator attack rate is decreased by increasing temperature but when both predator and prey are acclimated the shorter handling times considerably increase predator impact. The functional response of the fish changed from Type II to Type III with an increase in temperature, except when only the prey were acclimated. This change from population destabilizing Type II to more stabilizing Type III could confer protection to prey at low densities but increase the maximum feeding rate by Scyliorhinus canicula in the future. However, predator movement between different thermal regimes may maintain a Type II response, albeit with a lower maximum feeding rate. This has implications for the way the increasing population Scyliorhinus canicula in the Irish Sea may exploit valuable fisheries stocks in the future.     

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.     

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.     

A spatial theory for emergent multiple predator–prey interactions in food webs

Predator–prey interaction is inherently spatial because animals move through landscapes to search for and consume food resources and to avoid being consumed by other species. The spatial nature of species interactions necessitates integrating spatial processes into food web theory and evaluating how predators combine to impact their prey. Here, we present a spatial modeling approach that examines emergent multiple predator effects on prey within landscapes. The modeling is inspired by the habitat domain concept derived from empirical synthesis of spatial movement and interactions studies. Because these principles are motivated by synthesis of short‐term experiments, it remains uncertain whether spatial contingency principles hold in dynamical systems. We address this uncertainty by formulating dynamical systems models, guided by core habitat domain principles, to examine long‐term multiple predator–prey spatial dynamics. To describe habitat domains, we use classical niche concepts describing resource utilization distributions, and assume species interactions emerge from the degree of overlap between species. The analytical results generally align with those from empirical synthesis and present a theoretical framework capable of demonstrating multiple predator effects that does not depend on the small spatial or temporal scales typical of mesocosm experiments, and help bridge between empirical experiments and long‐term dynamics in natural systems.     

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.     

Testing the validity of functional response models using molecular gut content analysis for prey choice in soil predators

Analysis of predator–prey interactions is a core concept of animal ecology, explaining structure and dynamics of animal food webs. Measuring the functional response, i.e. the intake rate of a consumer as a function of prey density, is a powerful method to predict the strength of trophic links and assess motives of prey choice, particularly in arthropod communities. However, due to their reductionist set‐up, functional responses, which are based on laboratory feeding experiments, may not display field conditions, possibly leading to skewed results. Here, we tested the validity of functional responses of centipede predators and their prey by comparing them with empirical gut content data from field‐collected predators. Our predator–prey system included lithobiid and geophilomorph centipedes, abundant and widespread predators of forest soils and their soil‐dwelling prey. First, we calculated the body size‐dependent functional responses of centipedes using a published functional response model in which we included natural prey abundances and animal body masses. This allowed us to calculate relative proportions of specific prey taxa in the centipede diet. In a second step, we screened field‐collected centipedes for DNA of eight abundant soil‐living prey taxa and estimated their body size‐dependent proportion of feeding events. We subsequently compared empirical data for each of the eight prey taxa, on proportional feeding events with functional response‐derived data on prey proportions expected in the gut, showing that both approaches significantly correlate in five out of eight predator–prey links for lithobiid centipedes but only in one case for geophilomorph centipedes. Our findings suggest that purely allometric functional response models, which are based on predator–prey body size ratios are too simple to explain predator–prey interactions in a complex system such as soil. We therefore stress that specific prey traits, such as defence mechanisms, must be considered for accurate predictions.     

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.     

Predator interference alters foraging behavior of a generalist predatory arthropod

Interactions between predators foraging in the same patch may strongly influence patch use and functional response. In particular, there is continued interest in how the magnitude of mutual interference shapes predator–prey interactions. Studies commonly focus on either patch use or the functional response without attempting to link these important components of the foraging puzzle. Predictions from both theoretical frameworks suggest that predators should modify foraging efforts in response to changes in feeding rate, but this prediction has received little empirical attention. We study the linkage between patch departure rates and food consumption by the hunting spider, Pardosa milvina, using field enclosures in which prey and predator densities were manipulated. Additionally, the most appropriate functional response model was identified by fitting alternative functional response models to laboratory foraging data. Our results show that although prey availability was the most important determinant of patch departure rates, a greater proportion of predators left enclosures containing elevated predator abundance. Functional response parameter estimation revealed significant levels of interference among predators leading to lower feeding rates even when the area allocated for each predator was kept constant. These results suggest that feeding rates determine patch movement dynamics, where interference induces predators to search for foraging sites that balance the frequency of agonistic interactions with prey encounter rates.