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.     

The temporal selfish herd: predation risk while aggregations form

The hypothesis of the selfish herd has been highly influential to our understanding of animal aggregation. Various movement strategies have been proposed by which individuals might aggregate to form a selfish herd as a defence against predation, but although the spatial benefits of these strategies have been extensively studied, little attention has been paid to the importance of predator attacks that occur while the aggregation is forming. We investigate the success of mutant aggregation strategies invading populations of individuals using alternative strategies and find that the invasion dynamics depend critically on the time scale of movement. If predation occurs early in the movement sequence, simpler strategies are likely to prevail. If predators attack later, more complex strategies invade. If there is variation in the timing of predator attacks (through variation within or between individual predators), we hypothesize that groups will consist of a mixture of strategies, dependent upon the distribution of predator attack times. Thus, behavioural diversity can evolve and be maintained in populations of animals experiencing a diverse range of predators differing solely in their attack behaviour. This has implications for our understanding of predator–prey dynamics, as the timing of predator attacks will exert selection pressure on prey behavioural responses, to which predators must respond.     

Variation in foraging success among predators and its implications for population dynamics

The effects of the expected predation rate on population dynamics have been studied intensively, but little is known about the effects of predation rate variability (i.e., predator individuals having variable foraging success) on population dynamics. In this study, variation in foraging success among predators was quantified by observing the predation of the wolf spider Pardosa pseudoannulata on the cricket Gryllus bimaculatus in the laboratory. A population model was then developed, and the effect of foraging variability on predator–prey dynamics was examined by incorporating levels of variation comparable to those quantified in the experiment. The variability in the foraging success among spiders was greater than would be expected by chance (i.e., the random allocation of prey to predators). The foraging variation was density‐dependent; it became higher as the predator density increased. A population model that incorporates foraging variation shows that the variation influences population dynamics by affecting the numerical response of predators. In particular, the variation induces negative density‐dependent effects among predators and stabilizes predator–prey dynamics.     

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.     

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.     

Scaling up population dynamic processes in a ladybird–aphid system

Here, we study how scaling up to the metapopulation level affects predictions of a population dynamics model motivated by an aphidophagous predator–aphid system. The model incorporates optimization of egg distribution in predatory females, cannibalism among their offspring, and self-regulation of the prey population. These factors determine the within-year dynamics of the system and translate the numbers of prey and predator individuals at the beginning of the season into their numbers at the end of the season at the level of one patch—one suitable host plant or a group of these. At the end of each season, all populations of prey and all populations of predators are mixed (this simulates aphid host-alternation and ladybird migration to hibernation sites), and then redistributed at the beginning of the next season. Prey individuals are distributed at random among the patches as a “prey rain”, while adult predators that survived from the previous season optimize the distribution of their offspring, in that they prefer patches with sufficient amount of prey and absence of other predators. This redistribution followed by within-season dynamics is then iterated over many seasons. We look at whether small-scale trends in population dynamics predicted by this model are consistent with large-scale outcomes. Specifically, we show that even on the metapopulation scale, the impact of predators on prey metapopulation is relatively low. We further show how the dates of predator arrival to and departure from the system affect the qualitative behaviour of the model predictions.     

Incidental nest predation in freshwater turtles: inter- and intraspecific differences in vulnerability are explained by relative crypsis

There has long been interest in the influence of predators on prey populations, although most predator–prey studies have focused on prey species that are targets of directed predator searching. Conversely, few have addressed depredation that occurs after incidental encounters with predators. We tested two predictions stemming from the hypothesis that nest predation on two sympatric freshwater turtle species whose nests are differentially prone to opportunistic detection—painted turtles (Chrysemys picta) and snapping turtles (Chelydra serpentina)—is incidental: (1) predation rates should be density independent, and (2) individual predators should not alter their foraging behavior after encountering nests. After monitoring nest survival and predator behavior following nest depredation over 2 years, we confirmed that predation by raccoons (Procyon lotor), the primary nest predators in our study area, matched both predictions. Furthermore, cryptic C. picta nests were victimized with lower frequency than more detectable C. serpentina nests, and nests of both species were more vulnerable in human-modified areas where opportunistic nest discovery is facilitated. Despite apparently being incidental, predation on nests of both species was intensive (57% for painted turtles, 84% for snapping turtles), and most depredations occurred within 1 day of nest establishment. By implication, predation need not be directed to affect prey demography, and factors influencing prey crypsis are drivers of the impact of incidental predation on prey. Our results also imply that efforts to conserve imperiled turtle populations in human-modified landscapes should include restoration of undisturbed conditions that are less likely to expose nests to incidental predators.     

Diet quality in a wild grazer declines under the threat of an ambush predator

Predators influence prey populations not only through predation itself, but also indirectly through prompting changes in prey behaviour. The behavioural adjustments of prey to predation risk may carry nutritional costs, but this has seldom been studied in the wild in large mammals. Here, we studied the effects of an ambush predator, the African lion (Panthera leo), on the diet quality of plains zebras (Equus quagga) in Hwange National Park, Zimbabwe. We combined information on movements of both prey and predators, using GPS data, and measurements of faecal crude protein, an index of diet quality in the prey. Zebras which had been in close proximity to lions had a lower quality diet, showing that adjustments in behaviour when lions are within short distance carry nutritional costs. The ultimate fitness cost will depend on the frequency of predator–prey encounters and on whether bottom-up or top-down forces are more important in the prey population. Our finding is the first attempt to our knowledge to assess nutritionally mediated risk effects in a large mammalian prey species under the threat of an ambush predator, and brings support to the hypothesis that the behavioural effects of predation induce important risk effects on prey populations.     

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.     

Complementary predation on metamorphosing species promotes stability in predator–prey systems

Functionally redundant predation and functionally complementary predation are both widespread phenomena in nature. Functional complementary predation can be found, for example, when predators feed on different life stages of their prey, while functional redundant predation occurs when different predators feed on all life stages of a shared prey. Both phenomena are common in nature, and the extent of differential life-stage predation depends mostly on prey life history; complementary predation is expected to be more common on metamorphosing prey species, while redundant predation is thought to be higher on non-metamorphosing species. We used an ordinary differential equation model to explore the effect of varying degree of complementary and redundant predation on the dynamic properties of a system with two predators that feed on an age-structured prey. Our main finding was that predation on one stage (adult or juvenile) resulted in a more stable system (i.e., it is stable for a wider range of parameters) compared to when the two predators mix the two prey developmental stages in their diet. Our results demonstrate that predator–prey dynamics depends strongly on predators' functionality when predator species richness is fixed. Results also suggest that systems with metamorphosing prey are expected to be more diverse compared to systems with non-metamorphosing prey.     

Habitat complexity dampens selection on prey activity level

Conspecific prey individuals often exhibit persistent differences in behavior (i.e., animal personality) and consequently vary in their susceptibility to predation. How this form of selection varies across environmental contexts is essential to predicting ecological and evolutionary dynamics, yet remains currently unresolved. Here, we use three separate predator–prey systems (sea star–snail, wolf spider–cricket, and jumping spider–cricket) to independently examine how habitat structural complexity influences the selection that predators impose on prey behavioral types. Prior to conducting staged predator–prey interaction encounters, we ran prey individuals through multiple behavioral assays to determine their average activity level. We then allowed individual predators to interact with groups of prey in either open or structurally complex habitats and recorded the number and individual identity of prey that were eaten. Habitat complexity had no effect on overall predation rates in any of the three predator–prey systems. Despite this, we detected a pervasive interaction between habitat structure and individual prey activity level in determining individual prey survival. In open habitats, all predators imposed strong selection on prey behavioral types: sea stars preferentially consumed sedentary snails, while spiders preferentially consumed active crickets. Habitat complexity dampened selection within all three systems, equalizing the predation risk that active and sedentary prey faced. These findings suggest a general effect of habitat complexity that reduces the importance of prey activity level in determining individual predation risk. We reason this occurs because activity level (i.e., movement) is paramount in determining risk within open environments, whereas in complex habitats, other behavioral traits (e.g., escape ability to a refuge) may take precedence.     

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.     

Revealing the role of predator interference in a predator–prey system with disease in prey population

Predation on a species subjected to an infectious disease can affect both the infection level and the population dynamics. There is an ongoing debate about the act of managing disease in natural populations through predation. Recent theoretical and empirical evidence shows that predation on infected populations can have both positive and negative influences on disease in prey populations. Here, we present a predator–prey system where the prey population is subjected to an infectious disease to explore the impact of predator on disease dynamics. Specifically, we investigate how the interference among predators affects the dynamics and structure of the predator–prey community. We perform a detailed numerical bifurcation analysis and find an unusually large variety of complex dynamics, such as, bistability, torus and chaos, in the presence of predators. We show that, depending on the strength of interference among predators, predators enhance or control disease outbreaks and population persistence. Moreover, the presence of multistable regimes makes the system very sensitive to perturbations and facilitates a number of regime shifts. Since, the habitat structure and the choice of predators deeply influence the interference among predators, thus before applying predators to control disease in prey populations or applying predator control strategy for wildlife management, it is essential to carefully investigate how these predators interact with each other in that specific habitat; otherwise it may lead to ecological disaster.     

Predation risk in tadpole populations shapes behavioural responses of prey but not strength of trait‐mediated indirect interactions

Prey animals often respond to predators by reducing activity levels. This can produce a trait‐mediated indirect interaction (TMII) between predators and prey resources, whereby reduced foraging by prey in the presence of a predator causes an increase in prey resources. TMIIs play important roles in structuring communities, and it is important to understand factors that determine their strength. One such influence may be behavioural variation in the prey species, with indirect effects of predators being stronger within populations that are more responsive to the presence of a predator. We tested 1) whether the behavioural responsiveness of populations of wood frog tadpoles to predator cues was related to the predation risk in their native ponds, and 2) whether more responsive tadpoles yielded stronger TMIIs. To do this, we 1) measured the activity of tadpoles from 18 populations in mesocosms with and without caged predators, and 2) measured changes in the biomass of periphyton (the tadpoles’ diet) between predator treatments for each population. We found that tadpoles from higher predation risk ponds reduced their time outside refuges more in the presence of predators and tended to move less when visible, suggesting possible local adaptation to predation regimes. Though the presence of predators generally resulted in higher periphyton biomass – a TMII – there was no evidence that the strength of this TMII was affected by variation in tadpole behaviour. Foraging activity and general activity may be decoupled to some extent, enabling high predation risk‐adapted tadpoles to limit the fitness costs of reduced foraging when predators are present.     

Heterogeneous landscapes and the role of refuge on the population dynamics of a specialist predator and its prey

How, and where, a prey species survives predation by a specialist predator during low phases of population fluctuations or a cycle, and how the increase phase of prey population is initiated, are much-debated questions in population and theoretical ecology. The persistence of the prey species could be due mainly to habitats that act as refuges from predation and/or due to anti-predatory behaviour of individuals. We present models for the former conjecture in two (and three) habitat systems with a specialist predator and its favoured prey. The model is based on dispersal of prey between habitats with high reproductive output but high risk of predation, and less productive habitats with relatively low risk of predation. We illustrate the predictions of our model using parameters from one of the most intriguing vertebrate predator–prey systems, the multi-annual population cycles of boreal voles and their predators. We suggest that cyclic population dynamics could result from a sequence of extinction and re–colonization events. Field voles (Microtus agrestis), a key vole species in the system, can be hunted to extinction in their preferred meadow habitat, but persist in sub-optimal wet habitats where their main predator, the least weasel (Mustela nivalis nivalis) has a low hunting efficiency. Re–colonization of favourable habitats would occur after the predator population crashes. At the local scale, the model suggests that the periodicity and amplitude of population cycles can be strongly influenced by the relative availability of risky and safe habitats for the prey. Furthermore, factors like intra-guild predation may lead to reduced predation pressure on field voles in sub-optimal habitats, which would act as a refuge for voles during the low phase of their population cycles. Elasticity analysis suggested that our model is quite robust to changes in most parameters but sensitive to changes in the population dynamics of field voles in the optimal grassland habitat, and to the maximum predation rate of weasels.     

Induced changes in island fox (Urocyon littoralis) activity do not mitigate the extinction threat posed by a novel predator

Prey response to novel predators influences the impacts on prey populations of introduced predators, bio-control efforts, and predator range expansion. Predicting the impacts of novel predators on native prey requires an understanding of both predator avoidance strategies and their potential to reduce predation risk. We examine the response of island foxes (Urocyon littoralis) to invasion by golden eagles (Aquila chrysaetos). Foxes reduced daytime activity and increased night time activity relative to eagle-na?ve foxes. Individual foxes reverted toward diurnal tendencies following eagle removal efforts. We quantified the potential population impact of reduced diurnality by modeling island fox population dynamics. Our model predicted an annual population decline similar to what was observed following golden eagle invasion and predicted that the observed 11% reduction in daytime activity would not reduce predation risk sufficiently to reduce extinction risk. The limited effect of this behaviorally plastic predator avoidance strategy highlights the importance of linking behavioral change to population dynamics for predicting the impact of novel predators on resident prey populations.     

Local prey vulnerability increases with multiple attacks by a predator

Theory and empirical evidence suggest that predator activity makes prey more wary and less vulnerable to predation. However if at least some prey in the population are energetically or spatially constrained, then predators may eventually increase local prey vulnerability because of the cumulative costs of anti‐predation behaviour. We tested whether repeated attacks by a predator might increase prey vulnerability in a system where redshanks on a saltmarsh are attacked regularly by sparrowhawks from adjacent woodland. Cumulative attack number led to a reduction in redshank numbers and flock size (but had no effect on how close redshanks fed to predator‐concealing cover) because some redshanks moved to safer but less profitable habitats, leaving smaller flocks on the saltmarsh. This effect held even though numbers of redshank on the saltmarsh increased with time of day. As a result of the change in flock size, predicted attack‐success increased up to 1.6‐fold for the sparrowhawk, while individual risk of capture for the redshank increased up to 4.5‐fold among those individuals remaining on the saltmarsh. The effect did not arise simply because hawks were more likely to attack smaller flocks because attack rate was not dependent on flock size or abundance. Our data demonstrate that when some individual prey are constrained in their ability to feed on alternative, safer foraging sites, their vulnerability to predation increases as predator attacks accumulate, although those, presumably better quality individuals that leave the immediate risky area will have lower vulnerability, so that the mean vulnerability across the entire population may not have changed substantially. This suggests that the selective benefits of multiple low‐cost attacks by predators on prey could potentially lead to 1) locally heightened trait‐mediated interactions, 2) locally reduced interference among competing predators, and 3) the evolution of active prey manipulation by predators.     

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.     

The influence of generalist predators in spatially extended predator–prey systems

The presence of generalist predators is known to have important ecological impacts in several fields. They have wide applicability in the field of biological control. However, their role in the spatial distribution of predator and prey populations is still not clear. In this paper, the spatial dynamics of a predator–prey system is investigated by considering two different types of generalist predators. In one case, it is considered that the predator population has an additional food source and can survive in the absence of the prey population. In the other case, the predator population is involved in intraguild predation, i.e., the source of the additional food of the predator coincides with the food source of the prey population and thus both prey and predator populations compete for the same resource. The conditions for linear stability and Turing instability are analyzed for both the cases. In the presence of generalist predators, the system shows different pattern formations and spatiotemporal chaos which has important implications for ecosystem functioning not only in terms of their predictability, but also in influencing species persistence and ecosystem stability in response to abrupt environmental changes. This study establishes the importance of the consideration of spatial dynamics while determining optimal strategies for biological control through generalist predators.     

Revisiting the Role of Individual Variability in Population Persistence and Stability

Populations often exhibit a pronounced degree of individual variability and this can be important when constructing ecological models. In this paper, we revisit the role of inter-individual variability in population persistence and stability under predation pressure. As a case study, we consider interactions between a structured population of zooplankton grazers and their predators. Unlike previous structured population models, which only consider variability of individuals according to the age or body size, we focus on physiological and behavioural structuring. We first experimentally demonstrate a high degree of variation of individual consumption rates in three dominant species of herbivorous copepods (Calanus finmarchicus, Calanus glacialis, Calanus euxinus) and show that this disparity implies a pronounced variation in the consumption capacities of individuals. Then we construct a parsimonious predator-prey model which takes into account the intra-population variability of prey individuals according to behavioural traits: effectively, each organism has a ‘personality’ of its own. Our modelling results show that structuring of prey according to their growth rate and vulnerability to predation can dampen predator-prey cycles and enhance persistence of a species, even if the resource stock for prey is unlimited. The main mechanism of efficient top-down regulation is shown to work by letting the prey population become dominated by less vulnerable individuals when predator densities are high, while the trait distribution recovers when the predator densities are low.