Evolution mediates the effects of apex predation on aquatic food webs

Ecological and evolutionary mechanisms are increasingly thought to shape local community dynamics. Here, I evaluate if the local adaptation of a meso-predator to an apex predator alters local food webs. The marbled salamander (Ambystoma opacum) is an apex predator that consumes both the spotted salamander (Ambystoma maculatum) and shared zooplankton prey. Common garden experiments reveal that spotted salamander populations which co-occur with marbled salamanders forage more intensely than those that face other predator species. These foraging differences, in turn, alter the diversity, abundance and composition of zooplankton communities in common garden experiments and natural ponds. Locally adapted spotted salamanders exacerbate prey biomass declines associated with apex predation, but dampen the top-down effects of apex predation on prey diversity. Countergradient selection on foraging explains why locally adapted spotted salamanders exacerbate prey biomass declines. The two salamander species prefer different prey species, which explains why adapted spotted salamanders buffer changes in prey composition owing to apex predation. Results suggest that local adaptation can strongly mediate effects from apex predation on local food webs. Community ecologists might often need to consider the evolutionary history of populations to understand local diversity patterns, food web dynamics, resource gradients and their responses to disturbance.     

A spatial theory for characterizing predator–multiprey interactions in heterogeneous landscapes

Trophic interactions in multiprey systems can be largely determined by prey distributions. Yet, classic predator–prey models assume spatially homogeneous interactions between predators and prey. We developed a spatially informed theory that predicts how habitat heterogeneity alters the landscape-scale distribution of mortality risk of prey from predation, and hence the nature of predator interactions in multiprey systems. The theoretical model is a spatially explicit, multiprey functional response in which species-specific advection–diffusion models account for the response of individual prey to habitat edges. The model demonstrates that distinct responses of alternative prey species can alter the consequences of conspecific aggregation, from increasing safety to increasing predation risk. Observations of threatened boreal caribou, moose and grey wolf interacting over 378 181 km² of human-managed boreal forest support this principle. This empirically supported theory demonstrates how distinct responses of apparent competitors to landscape heterogeneity, including to human disturbances, can reverse density dependence in fitness correlates.     

Prey and predator density‐dependent interactions under different water volumes

Predation is a critical ecological process that directly and indirectly mediates population stabilities, as well as ecosystem structure and function. The strength of interactions between predators and prey may be mediated by multiple density dependences concerning numbers of predators and prey. In temporary wetland ecosystems in particular, fluctuating water volumes may alter predation rates through differing search space and prey encounter rates. Using a functional response approach, we examined the influence of predator and prey densities on interaction strengths of the temporary pond specialist copepod Lovenula raynerae preying on cladoceran prey, Daphnia pulex, under contrasting water volumes. Further, using a population dynamic modeling approach, we quantified multiple predator effects across differences in prey density and water volume. Predators exhibited type II functional responses under both water volumes, with significant antagonistic multiple predator effects (i.e., antagonisms) exhibited overall. The strengths of antagonistic interactions were, however, enhanced under reduced water volumes and at intermediate prey densities. These findings indicate important biotic and abiotic contexts that mediate predator–prey dynamics, whereby multiple predator effects are contingent on both prey density and search area characteristics. In particular, reduced search areas (i.e., water volumes) under intermediate prey densities could enhance antagonisms by heightening predator–predator interference effects.     

Predator size and phenology shape prey survival in temporary ponds

Theoretical efforts suggest that the relative sizes of predators and their prey can shape community dynamics, the structure of food webs, and the evolution of life histories. However, much of this work has assumed static predator and prey body sizes. The timing of recruitment and the growth patterns of both predator and prey have the potential to modify the strength of predator–prey interactions. In this study, I examined how predator size dynamics in 40 temporary ponds over a 3-year period affected the survival of spotted salamander (Ambystoma maculatum) larvae. Across communities, gape-limited predator richness, but not size, was correlated with habitat duration (pond permanence). Within communities, mean gape-limited predator size diminished as the growing season progressed. This size reduction occurred because prey individuals grew into a body size refuge and because the largest of the predators left ponds by mid-season. Elevated gape-limited predation risk across time and space was predicted by the occurrence of two large predatory salamanders: marbled salamander larvae (Ambystoma opacum) and red-spotted newt adults (Notophthalmus viridescens). The presence of the largest gape-limited predator, A. opacum, predicted A. maculatum larval survival in the field. The distribution of large predatory salamanders among ponds and across time is expected to lead to differing community dynamics and to generate divergent natural selection on early growth and body size in A. maculatum. In general, a dynamic perspective on predator size often will be necessary to understand the ecology and evolution of species interactions. This will be especially true in frequently disturbed or seasonal habitats where phenology and ontogeny interact to determine body size asymmetries. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Molecular gut content analysis indicates the inter‐ and intra‐guild predation patterns of spiders in conventionally managed vegetable fields

Inter‐ and intra‐guild interactions are important in the coexistence of predators and their prey, especially in highly disturbed vegetable cropping systems with sporadic food resources. Assessing the dietary range of a predator taxon characterized by diverse foraging behavior using conventional approaches, such as visual observation and conventional molecular approaches for prey detection, has serious logistical problems. In this study, we assessed the prey compositions and compare the dietary spectrum of a functionally diverge group of predators—spiders—to characterize their trophic interactions and assess biological control potential in Brassica vegetable fields. We used high‐throughput sequencing (HTS) and biotic interaction networks to precisely annotate the predation spectrum and highlight the predator–predator and predator–prey interactions. The prey taxa in the gut of all spider families were mainly enriched with insects (including dipterans, coleopterans, orthopterans, hemipterans, and lepidopterans) with lower proportions of arachnids (such as Araneae) along with a wide range of other prey factions. Despite the generalist foraging behavior of spiders, the community structure analysis and interaction networks highlighted the overrepresentation of particular prey taxa in the gut of each spider family, as well as showing the extent of interfamily predation by spiders. Identifying the diverse trophic niche proportions underpins the importance of spiders as predators of pests in highly disturbed agroecosystems. More specifically, combining HTS with advanced ecological community analysis reveals the preferences and biological control potential of particular spider taxa (such as Salticidae against lepidopterans and Pisauridae against dipterans), and so provides a valuable evidence base for targeted conservation biological control efforts in complex trophic networks.     

Salamander evolution across a latitudinal cline in gape-limited predation risk

General predictions of community dynamics require that insights derived from local habitats can be scaled up to explain phenomena across geographic scales. Across these larger spatial extents, adaptation can play an increasing role in determining the outcome of species interactions. If local adaptation is common, then our ability to generalize measures of species interaction strength across communities will be limited without an additional understanding of the genetic variation underlying interaction traits. In the context of predator–prey interactions, prey individuals commonly are expected to reduce risky foraging behaviors and subsequent growth under predation threat. However, rapid growth into a large body size can defend against gape-limited predators, creating a tradeoff between increased predation risk due to elevated foraging activity and decreased predation risk due to large size. Here I combine field observations, natural selection experiments, and common garden assays to understand potential adaptations of spotted salamander Ambystoma maculatum larvae to gape-limited and gape-unconstrained predators. Field observations and natural selection trials suggested antagonistic selection on prey body size among ponds dominated by gape-limited predator salamanders A. opacum and gape-unconstrained beetle larvae Dytiscus . In common garden experiments, prey from sites with high gape-limited predation risk grew larger than those from other sites, suggesting the evolution of rapid growth into a prey size refuge. Larvae from all sites grew to a large size when exposed to the gape-limited N. viridescens predator's kairomones. Hence, induced rapid growth into a size refuge may be an adaptive response to gape-limited predation risk. Results point to an important role for cross-community generalizations based on functional classifications of predators by their gape constraints and inter-site genetic variation in prey growth rates and behaviors.     

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.     

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.     

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.     

Behavioral “bycatch” from camera trap surveys yields insights on prey responses to human‐mediated predation risk

Human disturbance directly affects animal populations and communities, but indirect effects of disturbance on species behaviors are less well understood. For instance, disturbance may alter predator activity and cause knock‐on effects to predator‐sensitive foraging in prey. Camera traps provide an emerging opportunity to investigate such disturbance‐mediated impacts to animal behaviors across multiple scales. We used camera trap data to test predictions about predator‐sensitive behavior in three ungulate species (caribou Rangifer tarandus; white‐tailed deer, Odocoileus virginianus; moose, Alces alces) across two western boreal forest landscapes varying in disturbance. We quantified behavior as the number of camera trap photos per detection event and tested its relationship to inferred human‐mediated predation risk between a landscape with greater industrial disturbance and predator activity and a “control” landscape with lower human and predator activity. We also assessed the finer‐scale influence on behavior of variation in predation risk (relative to habitat variation) across camera sites within the more disturbed landscape. We predicted that animals in areas with greater predation risk (e.g., more wolf activity, less cover) would travel faster past cameras and generate fewer photos per detection event, while animals in areas with less predation risk would linger (rest, forage, investigate), generating more photos per event. Our predictions were supported at the landscape‐level, as caribou and moose had more photos per event in the control landscape where disturbance‐mediated predation risk was lower. At a finer‐scale within the disturbed landscape, no prey species showed a significant behavioral response to wolf activity, but the number of photos per event decreased for white‐tailed deer with increasing line of sight (m) along seismic lines (i.e., decreasing visual cover), consistent with a predator‐sensitive response. The presence of juveniles was associated with shorter behavioral events for caribou and moose, suggesting greater predator sensitivity for females with calves. Only moose demonstrated a positive behavioral association (i.e., longer events) with vegetation productivity (16‐day NDVI), suggesting that for other species bottom‐up influences of forage availability were generally weaker than top‐down influences from predation risk. Behavioral insights can be gleaned from camera trap surveys and provide complementary information about animal responses to predation risk, and thus about the indirect impacts of human disturbances on predator–prey interactions.     

Food webs in space: On the interplay of dynamic instability and spatial processes

Ecologists increasingly recognize that a consideration of spatial dynamics is essential for resolving many classical problems in community ecology. In the present paper, I argue that understanding how trophic interactions influence population stability can have important implications for the expression of spatial processes. I use two examples to illustrate this point. The first example has to do with spatial determinants of food chain length. Prior theoretical and empirical work has suggested that colonization–extinction dynamics can influence food chain length, at least for specialist consumers. I briefly review evidence and prior theory that food chain length is sensitive to area. A metacommunity scenario, in which each of various patches can have a food chain varying in length (but in which a consumer is not present on a patch unless its required resource is also present), shows that alternative landscape states are possible. This possibility arises if top predators moderate unstable interactions between intermediate predators and basal resources. The second example has to do with the impact of recurrent immigration on the stability of persistent populations. Immigration can either stabilize or destabilize local population dynamics. Moreover, an increase in immigration can decrease average population size for unstable populations with direct density-dependence, or in predator–prey systems with saturating functional responses. These theoretical models suggest that the interplay of temporal variation and spatial fluxes can lead to novel qualitative phenomena.     

Predation risk suppresses the positive feedback between size structure and cannibalism

1.?Cannibalism can play a prominent role in the structuring and dynamics of ecological communities. Previous studies have emphasized the importance of size structure and density of cannibalistic species in shaping short- and long-term cannibalism dynamics, but our understanding of how predators influence cannibalism dynamics is limited. This is despite widespread evidence that many prey species exhibit behavioural and morphological adaptations in response to predation risk. 2.?This study examined how the presence and absence of predation risk from larval dragonflies Aeshna nigroflava affected cannibalism dynamics in its prey larval salamanders Hynobius retardatus. 3.?We found that feedback dynamics between size structure and cannibalism depended on whether dragonfly predation risk was present. In the absence of dragonfly risk cues, a positive feedback between salamander size structure and cannibalism through time occurred because most of the replicates in this treatment contained at least one salamander larvae having an enlarged gape (i.e. cannibal). In contrast, this feedback and the emergence of cannibalism were rarely observed in the presence of the dragonfly risk cues. Once salamander size divergence occurred, experimental reversals of the presence or absence of dragonfly risk cues did not alter existing cannibalism dynamics as the experiment progressed. Thus, the effects of risk on the mechanisms driving cannibalism dynamics likely operated during the early developmental period of the salamander larvae. 4.?The effects of dragonfly predation risk on behavioural aspects of cannibalistic interactions among hatchlings may prohibit the initiation of dynamics between size structure and cannibalism. Our predation trials clearly showed that encounter rates among hatchlings and biting and ingestion rates of prospective prey by prospective cannibals were significantly lower in the presence vs. absence of dragonfly predation risk even though the size asymmetry between cannibals and victims was similar in both risk treatments. These results suggest that dragonfly risk cues first suppress cannibalism among hatchlings and then prevent size variation from increasing through time. 5.?We suggest that the positive feedback dynamics between size structure and cannibalism and their modification by predation risk may also operate in other systems to shape the population dynamics of cannibalistic prey species as well as overall community dynamics.     

Rapid contemporary evolution and clonal food web dynamics

Character evolution that affects ecological community interactions often occurs contemporaneously with temporal changes in population size, potentially altering the very nature of those dynamics. Such eco-evolutionary processes may be most readily explored in systems with short generations and simple genetics. Asexual and cyclically parthenogenetic organisms such as microalgae, cladocerans and rotifers, which frequently dominate freshwater plankton communities, meet these requirements. Multiple clonal lines can coexist within each species over extended periods, until either fixation occurs or a sexual phase reshuffles the genetic material. When clones differ in traits affecting interspecific interactions, within-species clonal dynamics can have major effects on the population dynamics. We first consider a simple predator–prey system with two prey genotypes, parametrized with data from a well-studied experimental system, and explore how the extent of differences in defence against predation within the prey population determine dynamic stability versus instability of the system. We then explore how increased potential for evolution affects the community dynamics in a more general community model with multiple predator and multiple prey genotypes. These examples illustrate how microevolutionary ‘details’ that enhance or limit the potential for heritable phenotypic change can have significant effects on contemporaneous community-level dynamics and the persistence and coexistence of species.     

Can size distributions of European lake fish communities be predicted by trophic positions of their fish species?

An organism''s body size plays an important role in ecological interactions such as predator–prey relationships. As predators are typically larger than their prey, this often leads to a strong positive relationship between body size and trophic position in aquatic ecosystems. The distribution of body sizes in a community can thus be an indicator of the strengths of predator–prey interactions. The aim of this study was to gain more insight into the relationship between fish body size distribution and trophic position in a wide range of European lakes. We used quantile regression to examine the relationship between fish species'' trophic position and their log‐transformed maximum body mass for 48 fish species found in 235 European lakes. Subsequently, we examined whether the slopes of the continuous community size distributions, estimated by maximum likelihood, were predicted by trophic position, predator–prey mass ratio (PPMR), or abundance (number per unit effort) of fish communities in these lakes. We found a positive linear relationship between species'' maximum body mass and average trophic position in fishes only for the 75% quantile, contrasting our expectation that species'' trophic position systematically increases with maximum body mass for fish species in European lakes. Consequently, the size spectrum slope was not related to the average community trophic position, but there were negative effects of community PPMR and total fish abundance on the size spectrum slope. We conclude that predator–prey interactions likely do not contribute strongly to shaping community size distributions in these lakes.     

Food level and sex shape predator-induced physiological stress: immune defence and antioxidant defence

Despite the potential impact on prey fitness and predator–prey interactions, most studies of predation risk ignore physiological responses and their dependence upon food level and sex. Therefore, we reared male and female larvae of the damselfly Lestes viridis under predator stress (dragonfly larvae) at high and low food levels, and subsequently scored for important variables of insect immune defence (i.e. phenoloxidase) and antioxidant defence [i.e. superoxide dismutase, and catalase (CAT)]. Under predation risk, larvae did not decrease growth rate or immune defence, and only slightly reduced food intake in the high food treatment, probably because of time stress, i.e. little time available to complete the larval development. However, larvae facing predator stress did show an upregulation of antioxidant enzymes. This upregulation was dependent upon food level for CAT and both food level and sex for SOD, consistent with energetic constraints and sex differences in the link between longevity and adult fitness. Our results illustrate that predator stress can influence life history, behavioural and physiological responses differentially and in a context-dependent way. This implies that non-consumptive physiological effects of predators on their prey show independent yet similar complexities in behavioural and life history response variables. In general, our results advocate that mechanistic studies on predator–prey interactions may benefit from including physiological variables.     

A stochastic foraging model with predator training effects: I. Functional response,switching, and run lengths

Training effects are changes in a predator's behavior while it is searching for the next prey to eat which are caused by the predator's experience with the last prey encountered. A stochastic foraging model is formulated incorporating several specific types of training effects, and their impact on the functional response shape, switching, and mean prey run lengths is evaluated. The main result is that training effects such as search image formation can cause sigmoid functional responses and switching, and can result in runs of prey captures longer than expected in the absence of training.     

Separating spatial search and efficiency rates as components of predation risk

Predation risk is an important driver of ecosystems, and local spatial variation in risk can have population-level consequences by affecting multiple components of the predation process. I use resource selection and proportional hazard time-to-event modelling to assess the spatial drivers of two key components of risk—the search rate (i.e. aggregative response) and predation efficiency rate (i.e. functional response)—imposed by wolves (Canis lupus) in a multi-prey system. In my study area, both components of risk increased according to topographic variation, but anthropogenic features affected only the search rate. Predicted models of the cumulative hazard, or risk of a kill, underlying wolf search paths validated well with broad-scale variation in kill rates, suggesting that spatial hazard models provide a means of scaling up from local heterogeneity in predation risk to population-level dynamics in predator–prey systems. Additionally, I estimated an integrated model of relative spatial predation risk as the product of the search and efficiency rates, combining the distinct contributions of spatial heterogeneity to each component of risk.     

Artificial selection for timing of dispersal in predatory mites yields lines that differ in prey exploitation strategies

Dispersal is the main determinant of the dynamics and persistence of predator–prey metapopulations. When defining dispersal as a predator exploitation strategy, theory predicts the existence of a continuum of strategies: from some dispersal throughout the predator–prey interaction (the Milker strategy) to dispersal only after the prey had been exterminated (the Killer strategy). These dispersal strategies relate to differences in prey exploitation at the population level, with more dispersal leading to longer predator–prey interaction times and higher cumulative numbers of dispersing predators. In the predatory mite Phytoseiulus persimilis, empirical studies have shown genetic variation for prey exploitation as well as for the timing of aerial dispersal in the presence of prey. Here, we test whether artificial selection for lines that differ in timing of dispersal also results in these lines differing in prey exploitation. Six rounds of selection for early or late dispersal resulted in predator lines displaying earlier or later dispersal. Moreover, it resulted—at the population level—in predicted differences in the local predator–prey interaction time and in the cumulative numbers of dispersers in a population dynamics experiment. We pose that timing of dispersal is a heritable trait that can be selected in P. persimilis, which results in lines that show quantitative differences in local predator–prey dynamics. This opens ways to experimentally investigate the evolution of alternative prey exploitation strategies and to select for predator strains with prey exploitation strategies resulting in better biological control.     

Noise-induced reduction in the attack rate of a planktivorous freshwater fish revealed by functional response analysis

1. Anthropogenic noise can affect animals physically, physiologically, and behaviourally. Although individual responses to noise are well documented, the consequences in terms of community structure, species coexistence, and ecosystem functioning remain fairly unknown.
2. The impact of noise on predation has received a growing interest and alterations in trophic links are observed when animals shift from foraging to stress-related behaviours, are distracted by noise, or because of acoustic masking. However, the experimental procedures classically used to quantify predation do not inform on the potential demographic impact on prey.
3. We derived the relationship between resource use and availability (the functional response) for European minnows (Phoxinus phoxinus) feeding on dipteran larvae (Chaoborus sp.) under two noise conditions: ambient noise and ambient noise supplemented with motorboat noise. The shape and magnitude of the functional response are powerful indicators of population outcomes and predator–prey dynamics. We also recorded fish behaviour to explore some proximate determinants of altered predation.
4. For both noise conditions, fish displayed a saturating (type II) functional response whose shape depends on two parameters: attack rate and handling time. Boat noise did not affect handling time but significantly reduced attack rate, resulting in a functional response curve of the same height but with a less steep initial slope. Fish exhibited a stress-related response to noise including increased swimming distance, more social interactions, and altered spatial distribution.
5. Our study shows the usefulness of the functional response approach to study the ecological impacts of noise and illustrates how the behavioural responses of predators to noise can modify the demographic pressure on prey. It also suggests that prey availability might mediate the negative effect of noise on predation. Community outcomes are expected if the reduced consumption of the main food sources goes with the overconsumption of alternative food sources, changing the distribution pattern of interaction strengths. Predation release could also trigger a trophic cascade, propagating the effect of noise to lower trophic levels.

     

Examining predator–prey body size,trophic level and body mass across marine and terrestrial mammals

Predator–prey relationships and trophic levels are indicators of community structure, and are important for monitoring ecosystem changes. Mammals colonized the marine environment on seven separate occasions, which resulted in differences in species'' physiology, morphology and behaviour. It is likely that these changes have had a major effect upon predator–prey relationships and trophic position; however, the effect of environment is yet to be clarified. We compiled a dataset, based on the literature, to explore the relationship between body mass, trophic level and predator–prey ratio across terrestrial (n = 51) and marine (n = 56) mammals. We did not find the expected positive relationship between trophic level and body mass, but we did find that marine carnivores sit 1.3 trophic levels higher than terrestrial carnivores. Also, marine mammals are largely carnivorous and have significantly larger predator–prey ratios compared with their terrestrial counterparts. We propose that primary productivity, and its availability, is important for mammalian trophic structure and body size. Also, energy flow and community structure in the marine environment are influenced by differences in energy efficiency and increased food web stability. Enhancing our knowledge of feeding ecology in mammals has the potential to provide insights into the structure and functioning of marine and terrestrial communities.