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.     

Foraging theory predicts predator-prey energy fluxes

1. In natural communities, populations are linked by feeding interactions that make up complex food webs. The stability of these complex networks is critically dependent on the distribution of energy fluxes across these feeding links. 2. In laboratory experiments with predatory beetles and spiders, we studied the allometric scaling (body-mass dependence) of metabolism and per capita consumption at the level of predator individuals and per link energy fluxes at the level of feeding links. 3. Despite clear power-law scaling of the metabolic and per capita consumption rates with predator body mass, the per link predation rates on individual prey followed hump-shaped relationships with the predator-prey body mass ratios. These results contrast with the current metabolic paradigm, and find better support in foraging theory. 4. This suggests that per link energy fluxes from prey populations to predator individuals peak at intermediate body mass ratios, and total energy fluxes from prey to predator populations decrease monotonically with predator and prey mass. Surprisingly, contrary to predictions of metabolic models, this suggests that for any prey species, the per link and total energy fluxes to its largest predators are smaller than those to predators of intermediate body size. 5. An integration of metabolic and foraging theory may enable a quantitative and predictive understanding of energy flux distributions in natural food webs.     

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.     

Microgeographic divergence of functional responses among salamanders under antagonistic selection from apex predators

A predator''s functional response determines predator–prey interactions by describing the relationship between the number of prey available and the number eaten. Its shape and parameters fundamentally govern the dynamic equilibrium of predator–prey interactions and their joint abundances. Yet, estimates of these key parameters generally assume stasis in space and time and ignore the potential for local adaptation to alter feeding responses and the stability of trophic dynamics. Here, we evaluate if functional responses diverge among populations of spotted salamander (Ambystoma maculatum) larvae that face antagonistic selection on feeding strategies based on their own risk of predation. Common garden experiments revealed that spotted salamander from ponds with varying predation risks differed in their functional responses, suggesting an evolutionary response. Applying mechanistic equations, we discovered that the combined changes in attack rates, handling times and shape of the functional response enhanced feeding rate in environments with high densities of gape-limited predators. We suggest how these parameter changes could alter community equilibria and other emergent properties of food webs. Community ecologists might often need to consider how local evolution at fine scales alters key relationships in ways that alter local diversity patterns, food web dynamics, resource gradients and community responses to disturbance.     

How allometric scaling relates to soil abiotics

For most species, the logarithm of their average body mass is negatively related to the logarithm of their relative population density, i.e. the numerical abundance. In this way, the allometric scaling (both mass–abundance regressions and body–size spectra) becomes useful in ecological theory to build and explain food webs. Using empirical evidence derived from 145 Dutch sites, a hypothesis is formulated to explain how soil microbivores, detritivores and predators react to increasing resource availability. Shifts in size distribution, and subsequently changes in soil food‐web structure, are further discussed in the perspective of Holling's sequential interactions between basic system functions. We show that the allometric scaling and the averages of the (log‐transformed) prey:predator body‐mass ratios are reliable predictors for assessing faunal responses to nutrient availability. We view this work as a first attempt toward an extensive comparison of ecological processes in different soil systems.     

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.

     

A size-constrained feeding-niche model distinguishes predation patterns between aquatic and terrestrial food webs

Understanding the formation of feeding links provides insights into processes underlying food webs. Generally, predators feed on prey within a certain body-size range, but a systematic quantification of such feeding niches is lacking. We developed a size-constrained feeding-niche (SCFN) model and parameterized it with information on both realized and non-realized feeding links in 72 aquatic and 65 terrestrial food webs. Our analyses revealed profound differences in feeding niches between aquatic and terrestrial predators and variation along a temperature gradient. Specifically, the predator–prey body-size ratio and the range in prey sizes increase with the size of aquatic predators, whereas they are nearly constant across gradients in terrestrial predator size. Overall, our SCFN model well reproduces the feeding relationships and predation architecture across 137 natural food webs (including 3878 species and 136,839 realized links). Our results illuminate the organisation of natural food webs and enables novel trait-based and environment-explicit modelling approaches.     

Trophic cascades alter eco-evolutionary dynamics and body size evolution

Trait evolution in predator–prey systems can feed back to the dynamics of interacting species as well as cascade to impact the dynamics of indirectly linked species (eco-evolutionary trophic cascades; EETCs). A key mediator of trophic cascades is body mass, as it both strongly influences and evolves in response to predator–prey interactions. Here, we use Gillespie eco-evolutionary models to explore EETCs resulting from top predator loss and mediated by body mass evolution. Our four-trophic-level food chain model uses allometric scaling to link body mass to different functions (ecological pleiotropy) and is realistically parameterized from the FORAGE database to mimic the parameter space of a typical freshwater system. To track real-time changes in selective pressures, we also calculated fitness gradients for each trophic level. As predicted, top predator loss generated alternating shifts in abundance across trophic levels, and, depending on the nature and strength in changes to fitness gradients, also altered trajectories of body mass evolution. Although more distantly linked, changes in the abundance of top predators still affected the eco-evolutionary dynamics of the basal producers, in part because of their relatively short generation times. Overall, our results suggest that impacts on top predators can set off transient EETCs with the potential for widespread indirect impacts on food webs.     

Allometry and catastrophic regime shifts in food chains

Population dynamics can reflect the body mass distribution of species because there is an allometric relationship between the average body mass of species and its metabolic timescale. Since predators are generally larger than their prey, a hierarchical structure from fast timescales to slow timescales can be a general structure in food webs. In this paper, we show that changes of the metabolic timescale ratio can cause catastrophic shifts. Then, we investigate a two-dimensional parameter space with the timescale ratio and the carrying capacity of basal species, and reveal that the timescale ratio characterizes the response of the system to environmental variation. Finally, in a bistable regime, we try to clarify the relationship between the trophic position of a species and the extent to which the species induces attractor switching. We saw that, in a 4-species food chain, top predators and second consumers induce attractor switching easily compared to first consumers and basal species.     

Consequences of size structure in the prey for predator-prey dynamics: the composite functional response

1. Current formulations of functional responses assume that the prey is homogeneous and independent of intraspecific processes. Most prey populations consist of different coexisting size classes that often engage in asymmetrical intraspecific interactions, including cannibalism, which can lead to nonlinear interaction effects. This may be important as the size structure with the prey could alter the overall density-dependent predation rates. 2. In a field experiment with damselfly and dragonfly larvae, 16 treatments manipulated the density of a small prey stage, the presence of large conspecific prey and the presence of heterospecific predators. 3. Size structure in the prey (i.e. when both prey stages were present) decreased the impact of the predator on overall prey mortality by 25-48% at mid and high prey densities, possibly due to density-dependent size-structured cannibalism in the prey. The predation rates on small prey stages were determined by the interaction of large prey and predators. Predation rates increased with prey density in the absence of large prey, but predation rates were constant across densities when large conspecifics were present. 4. The functional response for unstructured prey followed a Holling type III model, but the predation rate for size-structured prey was completely different and followed a complex pattern that could not be explained with any standard functional response. 5. Using additional laboratory experiments, a mortality model was developed and parameterized. It showed that the overall prey mortality of size-structured prey can be adequately predicted with a composite functional response model that modelled the individual functional responses of each prey stage separately and accounted for their cannibalistic interaction. 6. Thus, treating a prey population as a homogeneous entity will lead to erroneous predictions in most real-world food webs. However, if we account for the effects of size structure and the intraspecific interactions on functional responses by treating size classes as different functional groups, it is possible to reliably predict the dynamics of size-structured predator-prey systems.     

On the context‐dependent scaling of consumer feeding rates

The stability of consumer–resource systems can depend on the form of feeding interactions (i.e. functional responses). Size‐based models predict interactions – and thus stability – based on consumer–resource size ratios. However, little is known about how interaction contexts (e.g. simple or complex habitats) might alter scaling relationships. Addressing this, we experimentally measured interactions between a large size range of aquatic predators (4–6400 mg over 1347 feeding trials) and an invasive prey that transitions among habitats: from the water column (3D interactions) to simple and complex benthic substrates (2D interactions). Simple and complex substrates mediated successive reductions in capture rates – particularly around the unimodal optimum – and promoted prey population stability in model simulations. Many real consumer–resource systems transition between 2D and 3D interactions, and along complexity gradients. Thus, Context‐Dependent Scaling (CDS) of feeding interactions could represent an unrecognised aspect of food webs, and quantifying the extent of CDS might enhance predictive ecology.     

The effect of predation pressure and predator adaptive foraging on the relative importance of consumptive and non‐consumptive predator net effects in a freshwater model system

An important challenge in community ecology is identifying the functional characteristics capable of predicting the nature and strength of predator effects on food webs. We developed an individual‐based model, based on a shallow lake model system, to evaluate the total, consumptive, and non‐consumptive indirect effect that predators have on basal resources when the predators differ in their foraging types (active adaptive foraging or sedentary foraging). Overall, both predator types caused similar total indirect effects on lower trophic levels. However, the nature net effects of predators diverged between predator foraging types. Active predators caused larger non‐consumptive effects, relative to the total indirect effect, irrespective of predation pressure levels. On the other hand, sedentary predators caused larger non‐consumptive effects for lower predation pressure levels, but consumptive effects became more important as predation pressure increased. Our simulations showed that the reliance on a particular mechanism driving consumer–resource interactions is altered by predator foraging behavior and highlight the importance of both prey and predator foraging behaviors to predict the causes and consequences of cascading effects observed in food webs.     

Predator hunting mode influences patterns of prey use from grazing and epigeic food webs

Multichannel omnivory by generalist predators, especially the use of both grazing and epigeic prey, has the potential to increase predator abundance and decrease herbivore populations. However, predator use of the epigeic web (soil surface detritus/microbe/algae consumers) varies considerably for reasons that are poorly understood. We therefore used a stable isotope approach to determine whether prey availability and predator hunting style (active hunting vs. passive web-building) impacted the degree of multichannel omnivory by the two most abundant predators on an intertidal salt marsh, both spiders. We found that carbon isotopic values of herbivores remained constant during the growing season, while values for epigeic feeders became dramatically more enriched such that values for the two webs converged in August. Carbon isotopic values for both spider species remained midway between the two webs as values for epigeic feeders shifted, indicating substantial use of prey from both food webs by both spider species. As the season progressed, prey abundance in the grazing food web increased while prey abundance in the epigeic web remained constant or declined. In response, prey consumption by the web-building spider shifted toward the grazing web to a much greater extent than did consumption by the hunting spider, possibly because passive web-capture is more responsive to changes in prey availability. Although both generalist predator species engaged in multichannel omnivory, hunting mode influenced the extent to which these predators used prey from the grazing and epigeic food webs, and could thereby influence the strength of trophic cascades in both food webs.     

Foraging mode affects the evolution of egg size in generalist predators embedded in complex food webs

Ecological networks incorporate myriad biotic interactions that determine the selection pressures experienced by the embedded populations. We argue that within food webs, the negative scaling of abundance with body mass and foraging theory predict that the selective advantages of larger egg size should be smaller for sit‐and‐wait than active‐hunting generalist predators, leading to the evolution of a difference in egg size between them. Because body mass usually scales negatively with predator abundance and constrains predation rate, slightly increasing egg mass should simultaneously allow offspring to feed on more prey and escape from more predators. However, the benefits of larger offspring would be relatively smaller for sit‐and‐wait predators because (i) due to their lower mobility, encounters with other predators are less common, and (ii) they usually employ a set of alternative hunting strategies that help to subdue relatively larger prey. On the other hand, for active predators, which need to confront prey as they find them, body‐size differences may be more important in subduing prey. This difference in benefits should lead to the evolution of larger egg sizes in active‐hunting relative to sit‐and‐wait predators. This prediction was confirmed by a phylogenetically controlled analysis of 268 spider species, supporting the view that the structure of ecological networks may serve to predict relevant selective pressures acting on key life history traits.     

The impact of nonlinear functional responses on the long-term evolution of food web structure

We investigate the long-term web structure emerging in evolutionary food web models when different types of functional responses are used. We find that large and complex webs with several trophic layers arise only if the population dynamics is such that it allows predators to focus on their best prey species. This can be achieved using modified Lotka-Volterra or Holling/Beddington functional responses with effective couplings that depend on the predator's efficiency at exploiting the prey, or a ratio-dependent functional response with adaptive foraging. In contrast, if standard Lotka-Volterra or Holling/Beddington functional responses are used, long-term evolution generates webs with almost all species being basal, and with additionally many links between these species. Interestingly, in all cases studied, a large proportion of weak links result naturally from the evolution of the food webs.     

Energetic conditions promoting top-down control of prey by predators

Humans remove large amounts of biomass from natural ecosystems, and large bodied high trophic level animals are especially sensitive and vulnerable to exploitation. The effects of removing top-predators on food webs are often difficult to predict because of limited information on species interaction strengths. Here we used a three species predator-prey model to explore relationships between energetic properties of trophodynamic linkages and interaction strengths to provide heuristic rules that indicate observable energetic conditions that are most likely to lead to stable and strong top-down control of prey by predator species. We found that strong top-down interaction strengths resulted from low levels of energy flow from prey to predators. Strong interactions are more stable when they are a consequence of low per capita predation and when predators are subsidized by recruitment. Diet composition also affects stability, but the relationship depends on the form of the functional response. Our results imply that for generalist satiating predators, strong top-down control on prey is most likely for prey items that occupy a small portion of the diet and when density dependent recruitment is moderately high.     

The predators of insects

Abstract. 1. Insect–insectivore trophic relations were reviewed using presence–absence data from sixty-one invertebrate-dominated food webs and fifteen food webs from Briand's (1983) original forty web collection. From counts of prey links in higher taxa (orders, classes, phyla), six phyla and thirteen classes of non-insect insectivores and fourteen orders of insect predators and prey were found. 2. Detritus-based habitats (phytotelmata, felled logs, carcasses, dungpads) harboured fewer orders of insects, that interact with other insects, than webs from grazer-based (host plants, some galls) and mixed-based systems (aquatic webs). Consumer–resource networks of higher insect taxa in these webs shared several features found in some species-level biological networks: the trend was towards few pairs of strong asymmetrical links, several weak links and many null interactions. 3. From counts of insect predator–insect prey links, hymenopterans as terrestrial predators and parasitoids interacted with the most number of higher insect taxa. Hymenopterans were also linked as prey more often than other terrestrial insects. In freshwater habitats, plecopterans were linked as predators more often than other aquatic taxa, whereas dipterans were listed as prey more often than other insects. 4. Dipterans were linked in the diets of non-insect insectivores from seven of eight common taxonomic classes. Arachnids were identified as insect predators by food web researchers in the largest number of webs, followed by passerine birds and cyprinodont fishes. From analysis of prey links at the ordinal level, predaceous insects were less polyphagous than other predators (other ectotherms and endotherms). 5. Analysis of chain lengths, as expected, showed that insect prey occupied mostly lowermost trophic levels, non-insect insectivores were found mostly at uppermost trophic levels, and predaceous insects were found mostly at intermediate trophic levels across most habitats. 6. This analysis offers evidence that insects are not just occupying intermediate trophic levels in some communities. Indeed, some taxa feed at the upper ends of long food chains, for example eupelmids in galls, staphylinids in carcasses, and perlid plecopterans in streams.     

Effects of trophic similarity on community composition

Understanding how ecological processes determine patterns among species coexisting within ecosystems is central to ecology. Here, we explore relationships between species’ local coexistence and their trophic niches in terms of their feeding relationships both as consumers and as resources. We build on recent concepts and methods from community phylogenetics to develop a framework for analysing mechanisms responsible for community composition using trophic similarity among species and null models of community assembly. We apply this framework to 50 food webs found in 50 Adirondack lakes and find that species composition in these communities appears to be driven by both bottom‐up effects by which the presence of prey species selects for predators of those prey, and top‐down effects by which prey more tolerant of predation out‐compete less tolerant prey of the same predators. This approach to community food webs is broadly applicable and shows how species interaction networks can inform an increasingly large array of theory central to community ecology.     

Seasonal shifts in predator body size diversity and trophic interactions in size-structured predator-prey systems

1.?Theory suggests that the relationship between predator diversity and prey suppression should depend on variation in predator traits such as body size, which strongly influences the type and strength of species interactions. Prey species often face a range of different sized predators, and the composition of body sizes of predators can vary between communities and within communities across seasons. 2.?Here, I test how variation in size structure of predator communities influences prey survival using seasonal changes in the size structure of a cannibalistic population as a model system. Laboratory and field experiments showed that although the per-capita consumption rates increased at higher predator-prey size ratios, mortality rates did not consistently increase with average size of cannibalistic predators. Instead, prey mortality peaked at the highest level of predator body size diversity. 3.?Furthermore, observed prey mortality was significantly higher than predictions from the null model that assumed no indirect interactions between predator size classes, indicating that different sized predators were not substitutable but had more than additive effects. Higher predator body size diversity therefore increased prey mortality, despite the increased potential for behavioural interference and predation among predators demonstrated in additional laboratory experiments. 4.?Thus, seasonal changes in the distribution of predator body sizes altered the strength of prey suppression not only through changes in mean predator size but also through changes in the size distribution of predators. In general, this indicates that variation (i.e. diversity) within a single trait, body size, can influence the strength of trophic interactions and emphasizes the importance of seasonal shifts in size structure of natural food webs for community dynamics.     

Taxonomic versus allometric constraints on non‐linear interaction strengths

Recently, the importance of body mass and allometric scaling for the structure and dynamics of ecological networks has been highlighted in several ground‐breaking studies. However, advances in the understanding of generalities across ecosystem types are impeded to a considerable extent by a methodological dichotomy contrasting a considerable portion of marine ecology on the one hand opposite to traditional community ecology on the other hand. Many marine ecologists are bound to the taxonomy‐neglecting size spectrum approach when describing and analysing community patterns. In contrast, the mindset of the other school is focused on taxonomies according to the Linnean system at the cost of obscuring information due to applying species or population averages of body masses and other traits. Following other pioneering studies, we addressed this lingering gap, and studied non‐linear interaction strengths (i.e. functional responses) between two taxonomically‐distinct terrestrial arthropod predators (centipedes and spiders) of varying individual body masses and their prey. We fitted three non‐linear functional response models to the data: (1) a taxonomic model not accounting for variance in body masses amongst predator individuals, (2) an allometric model ignoring taxonomic differences between predator individuals, and (3) a combined model including body mass and taxonomic effects. Ranked according to their AICs, the combined model performs better than the allometric model, which provides a superior fit to the data than the taxonomic model. These results strongly indicate that the body masses of predator and prey individuals were responsible for most of the variation in non‐linear interaction strengths. Taxonomy explained some specific patterns in allometric exponents between groups and revealed mechanistic insights in predation efficiencies. Reconciling quantitative allometric models as employed by the marine size‐spectrum approach with taxonomic information may thus yield quantitative results that are generalized across ecosystem types and taxonomic groups. Using these quantitative models as novel null models should also strengthen subsequent taxonomic analyses.