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.     

Predator–prey relationships in a Mediterranean vertebrate system: Bonelli’s eagles,rabbits and partridges

How predators impact on prey population dynamics is still an unsolved issue for most wild predator–prey communities. When considering vertebrates, important concerns constrain a comprehensive understanding of the functioning of predator–prey relationships worldwide; e.g. studies simultaneously quantifying ‘functional’ and ‘numerical responses’ (i.e., the ‘total response’) are rare. The functional, the numerical, and the resulting total response (i.e., how the predator per capita intake, the population of predators and the total of prey eaten by the total predators vary with prey densities) are fundamental as they reveal the predator’s ability to regulate prey population dynamics. Here, we used a multi-spatio-temporal scale approach to simultaneously explore the functional and numerical responses of a territorial predator (Bonelli’s eagle Hieraaetus fasciatus) to its two main prey species (the rabbit Oryctolagus cuniculus and the red-legged partridge Alectoris rufa) during the breeding period in a Mediterranean system of south Spain. Bonelli’s eagle responded functionally, but not numerically, to rabbit/partridge density changes. Type II, non-regulatory, functional responses (typical of specialist predators) offered the best fitting models for both prey. In the absence of a numerical response, Bonelli’s eagle role as a regulating factor of rabbit and partridge populations seems to be weak in our study area. Simple (prey density-dependent) functional response models may well describe the short-term variation in a territorial predator’s consumption rate in complex ecosystems.     

Habitat context influences predator interference interactions and the strength of resource partitioning

Despite increasing evidence that habitat structure can shape predator–prey interactions, few studies have examined the impact of habitat context on interactions among multiple predators and the consequences for combined foraging rates. We investigated the individual and combined effects of stone crabs (Menippe mercenaria) and knobbed whelks (Busycon carica) when foraging on two common bivalves, the hard clam (Mercenaria mercenaria) and the ribbed mussel (Geukensia demissa) in oyster reef and sand flat habitats. Because these species co-occur across these and other estuarine habitats of varying physical complexity, this system is ideal for examining how habitat context influences foraging rates and the generality of predator interactions. Consistent with results from previous studies, consumption rates of each predator in isolation from the other were higher in the sand flat than in the more structurally complex oyster reef habitat. However, consumption by the two predators when combined surprisingly did not differ between the two habitats. This counterintuitive result probably stems from the influence of habitat structure on predator–predator interactions. In the sand-flat habitat, whelks significantly reduced their consumption of their less preferred prey when crabs were present. However, the structurally more complex oyster reef habitat appeared to reduce interference interactions among predators, such that consumption rates when the predators co-occurred did not differ from predation rates when alone. In addition, both habitat context and predator–predator interactions increased resource partitioning by strengthening predator dietary selectivity. Thus, an understanding of how habitat characteristics such as physical complexity influence interactions among predators may be critical to predicting the effects of modifying predator populations on their shared prey.     

Predation, individual variability and vertebrate population dynamics

Both predation and individual variation in life history traits influence population dynamics. Recent results from laboratory predator–prey systems suggest that differences between individuals can also influence predator–prey dynamics when different genotypes experience different predation-associated mortalities. Despite the growing number of studies in this field, there is no synthesis identifying the overall importance of the interactions between predation and individual heterogeneity and their role in shaping the dynamics of free-ranging populations of vertebrates. We aim to fill this gap with a review that examines how individual variability in prey susceptibility, in predation costs, in predator selectivity, and in predatory performance, might influence prey population dynamics. Based on this review, it is clear that (1) predation risk and costs experienced by free-ranging prey are associated with their phenotypic attributes, (2) many generalist predator populations consist of individual specialists with part of the specialization associated with their phenotypes, and (3) a complete understanding of the population dynamic consequences of predation may require information on individual variability in prey selection and prey vulnerability. Altogether, this work (1) highlights the importance of maintaining long-term, detailed studies of individuals of both predators and prey in contrasting ecological conditions, and (2) advocates for a better use of available information to account for interactive effects between predators and their prey when modelling prey population dynamics.     

Joint evolution of predator body size and prey-size preference

We studied the joint evolution of predator body size and prey-size preference based on dynamic energy budget theory. The predators’ demography and their functional response are based on general eco-physiological principles involving the size of both predator and prey. While our model can account for qualitatively different predator types by adjusting parameter values, we mainly focused on ‘true’ predators that kill their prey. The resulting model explains various empirical observations, such as the triangular distribution of predator–prey size combinations, the island rule, and the difference in predator–prey size ratios between filter feeders and raptorial feeders. The model also reveals key factors for the evolution of predator–prey size ratios. Capture mechanisms turned out to have a large effect on this ratio, while prey-size availability and competition for resources only help explain variation in predator size, not variation in predator–prey size ratio. Predation among predators is identified as an important factor for deviations from the optimal predator–prey size ratio.     

Facilitation between herons and smallmouth bass foraging on common prey

Understanding how multiple predators affect one another and their shared prey is an increasingly important goal for ecologists examining predator–prey dynamics and food-web structure. In a field experiment, we examined the outcome of interactions between terrestrial and freshwater predators foraging for the same prey in two temperate North American streams. We used a factorial design to examine the combined foraging effects of herons and smallmouth bass on striped shiners and central stonerollers. We found that there was facilitation between the two predators, resulting in risk-enhancement for the prey species, with particularly pronounced effects on the smallest (<70 mm) size classes. Facilitation is the least well-documented predator–predator interaction and has not been quantitatively demonstrated for freshwater and terrestrial predators. Our results indicate that bass may gain a net benefit from the presence of wading birds such as herons and egrets, and that concerns about the negative effects of birds on fish stocks through competition may be unwarranted.     

Evolutionary ecology of inducible morphological plasticity in predator–prey interaction: toward the practical links with population ecology

The outcome of species interactions is often strongly influenced by variation in the functional traits of the individuals participating. A rather large body of work demonstrates that inducible morphological plasticity in predators and prey can both influence and be influenced by species interaction strength, with important consequences for individual fitness. Much of the past research in this area has focused on the ecological and evolutionary significance of trait plasticity by studying single predator–prey pairs and testing the performance of individuals having induced and noninduced phenotypes. This research has thus been critical in improving our understanding of the adaptive value of trait plasticity and its widespread occurrence across species and community types. More recently, researchers have expanded this foundation by examining how the complexity of organismal design and community-level properties can shape plasticity in functional traits. In addition, researchers have begun to merge evolutionary and ecological perspectives by linking trait plasticity to community dynamics, with particular attention on trait-mediated indirect interactions. Here, we review recent studies on inducible morphological plasticity in predators and their prey with an emphasis on internal and external constraints and how the nature of predator–prey interactions influences the expression of inducible phenotypes. In particular, we focus on multiple-trait plasticity, flexibility and modification of inducible plasticity, and reciprocal plasticity between predator and prey. Based on our arguments on these issues, we propose future research directions that should better integrate evolutionary and population studies and thus improve our understanding of the role of phenotypic plasticity in predator–prey population and community dynamics.     

Behavioural and developmental responses of predatory coral reef fish to variation in the abundance of prey

Ecological theory suggests that the behaviour, growth and abundance of predators will be strongly influenced by the abundance of prey. Predators may in turn play an important role in structuring prey populations and communities. Responses of predators to variation in prey abundance have most commonly been demonstrated in low-diversity communities where food webs are relatively simple. How predators respond in highly diverse assemblages such as in coral reef habitats is largely unknown. This study describes an experiment that examined how the movement, diet and growth of the coral reef piscivore, Cephalopholis boenak (Serranidae) responded to variation in the abundance of its prey. Predator densities were standardised on small patch reefs made from the lagoonal reef-building coral, Porites cylindrica. These patch reefs exhibited natural variation in the abundance and community structure of multiple species of prey. However, our experiment generated a relatively simple predator–prey relationship, with C. boenak primarily responding to the most abundant species of prey. Three responses of predators were observed: aggregative, functional and developmental. Thirty-one per cent of individuals moved between patch reefs during the experiment, all from areas of relatively low to high prey density. Feeding rates were higher on patch reefs of high prey density, while growth rates of fish that remained on low prey density reefs throughout the experiment were lower. Growth rates of C. boenak on the experimental reefs were also much higher than for those living on natural patch reefs over the same time period, corresponding with overall differences in prey abundance. These results suggest that local abundance, feeding rate and growth of C. boenak were closely linked to the abundance of their main prey. This combination of predatory responses is a potential mechanism behind recent observations of density-dependent mortality and population regulation of prey in coral reef fish communities.     

Emergence of donor control in patchy predator—prey systems

We study a general predator—prey system in a spatially heterogeneous environment. The predation process, which occurs on a behavioural time-scale, is much faster than the other processes (reproduction, natural mortality and migrations) occurring on the population dynamics time-scale. We show that, taking account of this difference in time-scales, and assuming that the prey have a refuge, the dynamics of the system on a slow time-scale become donor-controlled. Even though predators may control the prey density locally and on a behavioural fast time-scale, nevertheless, both globally and on a slow time-scale, the prey dynamics are independent of predator density: the presence of predators generates a constant prey mortality. In other words, in heterogeneous environments, the prey population dynamics depend in a switch-like manner on the presence or absence of predators, not on their actual density.     

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 density and the functional responses of coral reef fish

Predation is a key process driving coral reef fish population dynamics, with higher per capita prey mortality rates on reefs with more predators. Reef predators often forage together, and at high densities, they may either cooperate or antagonize one another, thereby causing prey mortality rates to be substantially higher or lower than one would expect if predators did not interact. However, we have a limited mechanistic understanding of how prey mortality rates change with predator densities. We re-analyzed a previously published observational dataset to investigate how the foraging response of the coney grouper (Cephalopholis fulva) feeding on the bluehead wrasse (Thalassoma bifasciatum) changed with shifts in predator and prey densities. Using a model-selection approach, we found that per-predator feeding rates were most consistent with a functional response that declines as predator density increases, suggesting either antagonistic interactions among predators or a shared antipredator behavioral response by the prey. Our findings suggest that variation in predator density (natural or anthropogenic) may have substantial consequences for coral reef fish population dynamics.     

Modelling the Canada lynx and snowshoe hare population cycle: the role of specialist predators

Mathematical models of the snowshoe hare (Lepus americanus) and Canada lynx (Lynx canadensis) population cycles in the boreal forest have largely focused on the interaction between a single specialist predator and its prey. Here, we consider the role that other hare predators play in shaping the cycles, using a predator–prey model for up to three separate specialist predators. We consider the Canada lynx, coyote (Canis latrans) and great horned owl (Bubo virginianus). Our model improves on past modelling efforts in two ways: (1) our model solutions more closely represent the boreal hare and predator cycles with respect to the cycle period, maximum and minimum hare densities and maximum and minimum predator densities for each predator, and (2) our model sheds light on the role each specialist plays in regulation of the hare cycle, in particular, the dynamics of the raptor appear to be crucial for characterising the low hare densities correctly.     

Evolutionary ecology of movement by predators and prey

An essential key to explaining the mechanistic basis of ecological patterns lies in understanding the consequences of adaptive behavior for distributions and abundances of organisms. We developed a model that simultaneously incorporates (a) ecological dynamics across three trophic levels and (b) evolution of behaviors via the processes of mutation, selection, and drift in populations of variable, unique individuals. Using this model to study adaptive movements of predators and prey in a spatially explicit environment produced a number of unexpected results. First, even though predators and prey had limited information and sometimes moved in the “wrong” direction, evolved movement mechanisms allowed them to achieve average spatial distributions approximating optimal, ideal free distributions. Second, predators’ demographic parameters had marked, nonlinear effects on the evolution of movement mechanisms in the prey: As the predator mortality rate was increased past a critical point, prey abruptly shifted from making very frequent movements away from predators to making infrequent movements mainly in response to resources. Third, time series analyses revealed that adaptive, conditional movements coupled ecological dynamics across species and space. Our results provide general predictions, heretofore lacking, about how predators and prey should respond to one another on both ecological and evolutionary time scales.     

No evidence of nonlinear effects of predator density,refuge availability,or body size of prey on prey mortality rates

Predator density, refuge availability, and body size of prey can all affect the mortality rate of prey. We assume that more predators will lead to an increase in prey mortality rate, but behavioral interactions between predators and prey, and availability of refuge, may lead to nonlinear effects of increased number of predators on prey mortality rates. We tested for nonlinear effects in prey mortality rates in a mesocosm experiment with different size classes of western mosquitofish (Gambusia affinis) as the prey, different numbers of green sunfish (Lepomis cyanellus) as the predators, and different levels of refuge. Predator number and size class of prey, but not refuge availability, had significant effects on the mortality rate of prey. Change in mortality rate of prey was linear and equal across the range of predator numbers. Each new predator increased the mortality rate by about 10% overall, and mortality rates were higher for smaller size classes. Predator–prey interactions at the individual level may not scale up to create nonlinearity in prey mortality rates with increasing predator density at the population level.     

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.     

The rules of engagement: how to defend against combinations of predators

Studies of inducible defenses have traditionally examined prey responses to one predator at a time. However, prey in nature encounter combinations of predators that should force them to produce phenotypic compromises. We examined how snails (Helisoma trivolvis) alter their phenotype in the presence of three different predator species that were presented alone and in pairwise combinations. When snails were exposed to each predator alone, they formed predator-specific defenses that reflected the differences in each predator’s foraging mode. When snails were exposed to pairwise combinations of predators, their phenotype was dependent on their ability to detect each predator, the risk posed by each predator, and the effectiveness of a given defense against each predator. Consequently, responses to combined predators were typically biased towards one of the predators in the pair. This suggests that prey facing combined predators do not form simple intermediate defenses and, as a result, may experience enhanced mortality risk when they encounter natural predator regimes.     

Vertebrate exploitation of pulsed marine prey: a review and the example of spawning herring

Short-term bursts of prey availability occur in many ecosystems and have potential important consequences for both predator biology and ecosystem function. Examples of prey ‘pulses’ in marine ecosystems include spawning runs of several anadromous and marine fishes, horseshoe crab spawning, and salmonid juvenile outmigrations, which are exploited by numerous species of vertebrate predators. In a few cases, the fitness or demographic consequences of such predator–prey interactions are known or inferred, but too often that information remains unknown. We explored the extent of temporal and spatial variation in one example of a pulsed marine resource: the spawning of Pacific herring (Clupea pallasii). Spawning herring provide a rich, aggregated resource to which dozens of species of vertebrate predators often exhibit strong numerical responses. However, the spawning events are often variable in both time (annual differences of several to many weeks) and space (both regional and more local differences in size and timing of events). Such variability must affect more mobile predators less than area-restricted predators, and thus its effect would vary not only among species but also within species, depending on constraints of the predator life history. Unpredictability of the prey concentrations, whatever their proximate causes, may contribute to maintenance of metapopulations of prey such as herring, if unpredictability lessens the impact of predation.     

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.     

Bayesian Inference for Functional Response in a Stochastic Predator–Prey System

We present a Bayesian method for functional response parameter estimation starting from time series of field data on predator–prey dynamics. Population dynamics is described by a system of stochastic differential equations in which behavioral stochasticities are represented by noise terms affecting each population as well as their interaction. We focus on the estimation of a behavioral parameter appearing in the functional response of predator to prey abundance when a small number of observations is available. To deal with small sample sizes, latent data are introduced between each pair of field observations and are considered as missing data. The method is applied to both simulated and observational data. The results obtained using different numbers of latent data are compared with those achieved following a frequentist approach. As a case study, we consider an acarine predator–prey system relevant to biological control problems.