Tracking prey or tracking the prey's resource? Mechanisms of movement and optimal habitat selection by predators

We synthesize previous theory on ideal free habitat selection to develop a model of predator movement mechanisms, when both predators and prey are mobile. We consider a continuous environment with an arbitrary distribution of resources, randomly diffusing prey that consume the resources, and predators that consume the prey. Our model introduces a very general class of movement rules in which the overall direction of a predator's movement is determined by a variable combination of (i) random diffusion, (ii) movement in the direction of higher prey density, and/or (iii) movement in the direction of higher density of the prey's resource. With this model, we apply an adaptive dynamics approach to two main questions. First, can it be adaptive for predators to base their movement solely on the density of the prey's resource (which the predators do not consume)? Second, should predator movements be exclusively biased toward higher densities of prey/resources, or is there an optimal balance between random and biased movements? We find that, for some resource distributions, predators that track the gradient of the prey's resource have an advantage compared to predators that track the gradient of prey directly. Additionally, we show that matching (consumers distributed in proportion to resources), overmatching (consumers strongly aggregated in areas of high resource density), and undermatching (consumers distributed more uniformly than resources) distributions can all be explained by the same general habitat selection mechanism. Our results provide important groundwork for future investigations of predator-prey dynamics.     

Habitat selection by predators and prey in communities with asymmetrical intraguild predation

Competition and predation have broad ecological consequences as they may influence individual behavior and community structure. In some cases, they are linked and predator and prey are also competitors (intraguild predation). I present a game theoretic model of habitat use by predators and prey under conditions of asymmetrical intraguild predation. This model predicts that when the diet of intraguild predators is restricted to intraguild prey and the resource for which predators and prey compete (the basal resource), co-occurrence is only stable when dietary overlap is low and productivity of the basal resource is not high. The addition of alternative resources for predators results in co-occurrence under all conditions. Variation in alternative resource productivity produces a continuum of intraguild prey distributions from matching relative habitat safety, to one that reflects both food and predation risk. When there is a substantial alternative resource for predators, the distribution of predators matches that of alternative resource availability while the distribution of prey is influenced by both habitat riskiness and food availability. The density and distribution of the predator's alternative resource thus influence habitat selection by the intraguild prey. This stresses the importance of indirect interactions in structuring habitat use in communities and the need to view habitat selection in a community context.     

Coexistence of predator and prey in intraguild predation systems with ontogenetic niche shifts

In basic intraguild predation (IGP) systems, predators and prey also compete for a shared resource. Theory predicts that persistence of these systems is possible when intraguild prey is superior in competition and productivity is not too high. IGP often results from ontogenetic niche shifts, in which the diet of intraguild predators changes as a result of growth in body size (life-history omnivory). As a juvenile, a life-history omnivore competes with the species that becomes its prey later in life. Competition can hence limit growth of young predators, while adult predators can suppress consumers and therewith neutralize negative effects of competition. We formulate and analyze a stage-structured model that captures both basic IGP and life-history omnivory. The model predicts increasing coexistence of predators and consumers when resource use of stage-structured predators becomes more stage specific. This coexistence depends on adult predators requiring consumer biomass for reproduction and is less likely when consumers outcompete juvenile predators, in contrast to basic IGP. Therefore, coexistence occurs when predation structures the community and competition is negligible. Consequently, equilibrium patterns over productivity resemble those of three-species food chains. Life-history omnivory thus provides a mechanism that allows intraguild predators and prey to coexist over a wide range of resource productivity.     

The influence of temporally variable predation risk on indirect interactions in an aquatic food chain

We know little about how temporally variable predation risk influences prey behavior. The risk allocation hypothesis predicts that prey facing more frequent risk should show weak anti-predator responses, and should be particularly active foragers during rare periods of safety, compared to prey facing infrequent risk. Several studies offer support for the risk allocation hypothesis, but how these responses might propagate through the larger ecological community remains largely unknown. We experimentally investigated the relative strength of trait- and density-mediated indirect effects of a predator on its prey’s resource across predation treatments that varied the lethality (caged or free-swimming predators) and temporal variability (always, often, or sometimes present) of predation. We performed this experiment in pond mesocosms using a giant water bug predator (Belostoma lutarium), an herbivorous pond snail (Physa gyrina), and algae as the basal resource. Snails greatly reduced the abundance of their algal resource when in the absence of predation. Lethal predation at low and medium intensities had significant positive indirect effects on the abundance of algae, mostly by reducing snail density. Snails responded behaviorally to high levels of deadly predation by foraging more and hiding less than in other situations, as predicted by the risk allocation hypothesis, and thus ameliorated the density-mediated indirect effects of predators on algae. Behavioral responses to caged predators, and the subsequent trait-mediated indirect effects, were negligible regardless of predation intensity. Our previous work has demonstrated that trait-mediated indirect effects are weak when resources are abundant, as they were in this experiment. This work demonstrates that temporal variation in predation intensity plays a key role in determining the relative strength of TMIIs and DMIIs in an aquatic food chain.     

Effects of partitioning allochthonous and autochthonous resources on food web stability

The flux of energetic and nutrient resources across habitat boundaries can exert major impacts on the dynamics of the recipient food web. Competition for these resources can be a key factor structuring many ecological communities. Competition theory suggests that competing species should exhibit some partitioning to minimize competitive interactions. Species should partition both in situ (autochthonous) resources and (allochthonous) resources that enter the food web from outside sources. Allochthonous resources are important sources of energy and nutrients in many low productivity systems and can significantly influence community structure. The focus of this paper is on: (i) the influence of resource partitioning on food web stability, but concurrently we examine the compound effects of; (ii) the trophic level(s) that has access to allochthonous resources; (iii) the amount of allochthonous resource input; and (iv) the strength of the consumer–resource interactions. We start with a three trophic level food chain model (resource–consumer–predator) and separate the higher two trophic levels into two trophospecies. In the model, allochthonous resources are either one type available to both consumers and predators or two distinct types, one for consumers and one for predators. The feeding preferences of the consumer and predator trophospecies were varied so that they could either be generalists or specialists on allochthonous and/or autochthonous resources. The degree of specialization influenced system persistence by altering the structure and, therefore, the indirect effects of the food web. With regard to the trophic level(s) that has access to allochthonous resources, we found that a single allochthonous resource available to both consumers and predators is more unstable than two allochthonous resources. The results demonstrate that species populating food webs that experience low to moderate allochthonous resources are more persistent. The results also support the notion that strong links destabilize food web dynamics, but that weak to moderate strength links stabilize food web dynamics. These results are consistent with the idea that the particular structure, resource availability, and relative strength of links of food webs (such as degree of specialization) can influence the stability of communities. Given that allochthonous resources are important resources in many ecosystems, we argue that the influence of such resources on species and community persistence needs to be examined more thoroughly to provide a clearer understanding of food web dynamics.     

The positive effects of negative interactions: Can avoidance of competitors or predators increase resource sampling by prey?

Spatial overlap between predators and prey is key to predicting their interaction strength and population dynamics. We constructed a spatially-explicit simulation model to explore how predator and prey behavioral traits and patterns of resource distribution influence spatial overlap between predators, prey, and prey resources. Predator and prey spatial association primarily followed the ideal free distribution. Departures from this model were intriguing, especially from the interactions of predator and prey behavior. When prey weakly avoided conspecifics, they associated more highly with resources when predators were present. Predators increased the rate of prey movement between patches, which increased their ability to sample their environment and aggregate in patches with high resources. When prey strongly avoided each other, predators decreased prey association with resources. That is, an increased rate of prey movement increased the probability that prey would interact and avoid each other without regard to the distribution of resources. More generally, a more highly clumped distribution of resources acted as a spatial anchor that generally increased prey, predator, and resource association. Prey tended to congregate with resources and predators generally congregated with prey.     

Spatiotemporal food web dynamics along a desert riparian–upland transition

Increased awareness of spatiotemporal variation in species interactions has motivated the study of temporally-resolved food web dynamics at the landscape level. Empiricists have focused attention on cross-habitat flows of materials, nutrients, and prey, largely ignoring the movement of predators between habitats that differ in productivity (and how predators integrate pulses in resource availability over time). We set out to study seasonal variation in food web interactions between mammalian carnivores and their rodent prey along a riparian–upland gradient in semi-arid southeastern Arizona which features both spatial and temporal heterogeneity in resource availability. Specifically, we tested whether mammalian carnivores spill over from productive, near-river habitats into adjacent, desert-scrub habitats; and if they do, to document the effects of this spillover on rodent communities. Furthermore, we examined seasonal variation in top-down effects by measuring changes in carnivore diet and distribution patterns and rodent populations over time. The results indicate that carnivores track seasonally-abundant resources across the landscape, varying both their diet and movement patterns. In turn, desert-scrub rodent population dynamics track seasonal shifts in carnivore habitat use but not resource availability, suggesting that predation plays a role in structuring rodent communities along the San Pedro River. Further evidence comes from data on rodent community composition, which differs between desert-scrub habitats near and far from the river, despite similarities in resource availability. Our data also suggest that seasonal omnivory helps predators survive lean times, increasing their effects on prey populations. Taken together, these results underscore the importance of spatiotemporal variation in species interactions, highlighting the complexity of natural systems and the need for further detailed studies of food web dynamics.     

Trophic cascades in rocky shore tide pools: distinguishing lethal and nonlethal effects

The effects of predators on the density of their prey can have positive indirect effects on the abundance of the preys resource via a trophic cascade. This concept has strongly influenced contemporary views of how communities are structured. However, predators also can transmit indirect effects by inducing changes in prey traits. We show that the mere presence of predator risk cues can initiate a trophic cascade in rocky shore tide pools. In large (mean surface area =9 m²), natural tide pools, we manipulated crab density and their foraging ability to examine the relative importance of lethal (density-mediated) and non-lethal (trait-mediated) predator effects to algal community development. We found that perceived predation risk reduced snail density as much as the direct predation treatment, showing that green crab predation was not an important factor regulating local snail density. Instead, snail emigration away from resident crabs appears to be the most important factor regulating local snail density. As a result, the abundance of ephemeral green algae was similar in the predation risk and direct predation treatments, suggesting that the consumption of snails by crabs plays a minimal role in mediating the trophic cascade. Increased attention to trait-mediated effects that are transmitted by predator-induced changes in prey behavior may change our view of how predators exert their strong influence on community structure.     

Continuous cycling of grouped vs. solitary strategy frequencies in a predator-prey model

We present a model of predator and prey grouping strategies using game theory. As predators respond strategically to prey behavior and vice versa, the model is based on a co-evolution approach. Focusing on the "many eyes-many mouths" trade-off, this model considers the benefits and costs of being in a group for hunting predators and foraging prey: predators in a group have more hunting success than solitary predators but they have to share the prey captured; prey in a group face a lower risk of predation but greater competition for resources than lone prey. The analysis of the model shows that the intersections of four curves define distinct areas in the parameter space, corresponding to different strategies used by predators and prey at equilibrium. The model predictions are in accordance with empirical evidence that an open habitat encourages group living, and that low risks of predation favor lone prey. Under some conditions, continuous cycling of the relative frequencies of the different strategies may occur. In this situation, the proportions of grouped vs. solitary predators and prey oscillate over time.     

Remembering the good and the bad: memory-based mediation of the food–safety trade-off in dynamic landscapes

Predator–prey interactions are central to fitness as animals simultaneously avoid death and consume resources to ensure growth and reproduction. Along with direct effects, predators can also exert strong non-consumptive effects. For example, prey shift habitat use in the presence of predators, a potentially learned behavior. The impact of cognition on movement and predator interactions is largely unexplored despite evidence of learned responses to predation threat. We explore how learning and spatial memory influence predator–prey dynamics by introducing predators into a memory-driven movement modeling framework. To model various aspects of risk, we vary predator behavior: their persistence and spatial correlation with the prey’s resources. Memory outperforms simpler movement processes most in patchy environments with more predictable predators that are more easily avoided once learned. In these cases, memory aids foragers in managing the food–safety trade-off. For example, particular parameterizations of the predation memory reduce encounters while maintaining consumption. We found that non-consumptive effects are highest in landscapes of concentrated, patchy resources. These effects are intensified when predators are highly correlated with the forager’s resources. Smooth landscapes provide more opportunities for foragers to simultaneously consume resources and avoid predators. Predators are able to effectively guard all resources in very patchy landscapes. These non-consumptive effects are also seen with the shift away from the best quality habitat compared to foraging in a predator-free environment.     

Optimum search speed and activity: a dynamic game in a three-link trophic system

We analysed how a consumer should simultaneously trade-off search speed and time active in a game with predators that optimise their search speed. Both the consumers and the predators are continuously reproducing and maximise fitness by maximising the per capita growth rate. The impact of the predator's presence on consumer behaviour, and the effects of type I and II functional responses on the behaviour of both species are considered. In the analyses, consumers were allowed to co-ordinate activity or behave independently in relation to other consumers. The ESS-analysis of the game ensures that no mutant can invade the system. The independent activity was found to be optimal in all analyses, while the co-ordinated activity was only optimal at full activity where the two activity strategies coincided. The model showed that consumers should change activity to account for predation risk. Activity generally decreased with predation risk. Concerning the energetic aspects, both activity and search speed were important to account for the reproductive output. The functional responses influenced the optimum activity and search speed of consumers and predators. In general, the optimum behaviours showed complex non-linear responses in relation to the resource and the consumer density. A predator type II functional response had profound impacts on the properties of the optima, the stability and presence of alternative strategies. As a result of the optimum behaviours, the realised functional responses of both species became sigmoidal.     

Predation risk tradeoffs in prey: effects on energy and behaviour

The complexity of behavioural interactions in predator-prey systems has recently begun to capture trait-effects, or non-lethal effects, of predators on prey via induced behavioural changes. Non-lethal predation effects play crucial roles in shaping population and community dynamics, particularly by inducing changes to foraging, movement and reproductive behaviours of prey. Prey exhibit trade-offs in behaviours while minimizing predation risk. We use a novel evolutionary ecosystem simulation EcoSim to study such behavioural interactions and their effects on prey populations, thereby addressing the need for integrating multiple layers of complexity in behavioural ecology. EcoSim allows complex intra- and inter-specific interactions between behaviourally and genetically unique individuals called predators and prey, as well as complex predator-prey dynamics and coevolution in a tri-trophic and spatially heterogeneous world. We investigated the effects of predation risk on prey energy budgets and fitness. Results revealed that energy budgets, life history traits, allocation of energy to movements and fitness-related actions differed greatly between prey subjected to low-predation risk and high-predation risk. High-predation risk suppressed prey foraging activity, increased total movement and decreased reproduction relative to low-risk. We show that predation risk alone induces behavioural changes in prey which drastically affect population and community dynamics, and when interpreted within the evolutionary context of our simulation indicate that genetic changes accompanying coevolution have long-term effects on prey adaptability to the absence of predators.     

The negative effects of pathogen‐infected prey on predators: a meta‐analysis

Intra‐guild predation (IGP) – where a top predator (IG_Pred) consumes both a basal resource and a competitor for that resource (IG_Prey) – has become a fundamental part of understanding species interactions and community dynamics. IGP communities composed of intraguild predators and prey have been well studied; however, we know less about IGP communities composed of predators, pathogens, and resources. Resource quality plays an important role in community dynamics and may influence IGP dynamics as well. We conducted a meta‐analysis on predator–pathogen–resource communities to determine whether resource quality mediated by the pathogen affected predator life‐history traits and if these effects met the theoretical constraints of IGP communities. To do this, we summarized results from studies that investigated the use of predators and pathogens to control insect pests. In these systems, the predators are the IG_Pred and pathogens are the IG_Prey. We found that consumer longevity, fecundity, and survival decreased by 26%, 31% and 13% respectively, when predators consumed pathogen‐infected prey, making the infected prey a low quality resource. Predators also significantly preferred healthy prey over infected prey. When we divided consumers by enemy type, strict predators (e.g. wolf spiders) had no preference while parasitoids preferred healthy prey. Our results suggest that communities containing parasitoids and pathogens may rarely exhibit intraguild predation; whereas, communities composed of strict predators and pathogens are more likely dominated by IGP dynamics. In these latter communities, the consumption of low and high quality resources suggests that IGP communities composed of strict predators, pathogens and prey should naturally persist, supporting IGP theory. Synthesis We investigated how consuming pathogen‐infected prey influence important life‐history parameters of insect predators. Pathogens are used in a variety of biocontrol programs, especially to control crop pests. We found that true predators (i.e. wolf spiders) have no preference for healthy or infected prey and have reduced fecundity, survival and longevity consuming infected prey. However, parasitoids avoided infected prey when possible. In biocontrol programs with multiple control agents, parasitoids and pathogens would do a better job controlling pests as predators would reduce the amount of pathogen available and have reduced fitness from consuming infected prey. However, theory suggests that true predators, prey and pathogens may coexist long term.     

Threshold levels of generalist predation determine consumer response to resource pulses

Many ecological systems are characterized by brief periods of increased resource availability called resource pulses. Empirical studies suggest that some populations of primary consumers grow rapidly in response to resource pulses, but others instead remain at low abundance despite increases in resource availability. Previous theory suggests that the lack of increase in primary consumers might be due to predators, which can respond to increased prey density both numerically, by increasing their own population, and functionally, by killing prey at a faster rate. The complexity of potential population responses to resource pulses can be assessed with simulations, but analytical conditions determining when one observes qualitatively distinct dynamics have yet to be identified. Here we use a graphical method based on a bifurcation diagram to derive the conditions leading to qualitatively distinct steady state and transient prey population dynamics as levels of predation (abundance and diversity) vary. When predation thresholds are crossed, consumer populations respond numerically to increases in their resources and provide a secondary resource pulse to their predators and parasites. These community dynamics have broad implications for the impact of changing predator communities on insect and rodent population outbreaks, which are economically and epidemiologically important.     

Temporal resource variability and the habitat-matching rule

Summary The ideal free distribution of competitors in a heterogeneous environment often predicts habitat matching, where the equilibrium number of consumers in a patch is proportional to resource abundance in that patch. We model the interaction between habitat matching and temporal variation in resource abundance. In one patch the rate of resource input follows a Markov chain; a second patch does not vary temporally. We predict patch use by scaling transition rates in the variable patch to the time that consumers require to respond to changes in rates of resource input. If consumers respond very quickly, habitat matching tracks temporal variability. If resource input fluctuates faster than consumers respond, habitat matching averages over the equilibrium of the Markov chain. Tracking and averaging produce the same mean resource consumption for individuals, but long-term mean occupation of the patches differs. When habitat matching tracks temporal variability in resources, consumer density in the variable patch has a lower mean and a higher variance than when habitat matching reflects only average rates of resource input.We tested our model by feeding free-living mallard ducks (Anas platyrynchos) at two artificial patches. The foragers' behavior satisfied the quantitative predictions of the model in each of two experiments.     

Dangerous dive cycles and the proverbial ostrich

Data rarely are available to address the level of predation risk faced by diving animals in different parts of the water column. Consequently, most published research on diving behaviour implicitly assumes – like the proverbial ostrich – that 'unseen' predators are functionally unimportant. We argue that failure to consider diving in a predation risk framework may have precluded many insights into the ecology of aquatic foragers that breathe air. Using existing literature and a simple model, we suggest that fear from submerged predators in several systems might be influencing patch residence time, and therefore the duration of other dive cycle components. These analyses, along with an earlier model of predation risk faced by diving animals at the surface, suggest that dive cycle organisation can be modified to increase safety from predators, but only at the cost of reduced energy gain. Theoretical arguments presented here can seed hypotheses on factors contributing to population declines of diving species. For instance, adjustments to the dive cycle that reduce predation risk might be unaffordable if resources are scarce. Thus, if animals are to avoid imminent starvation or substantial loss of reproductive potential, resource declines might indirectly increase predation rates by limiting the extent to which dive cycles can deviate from those that would maximize energy gain. We hope that ideas presented in this paper stimulate other researchers to further develop theory and test predictions on how predation risk might influence diving behaviour and its ecological consequences.     

Predator-prey shell games: large-scale movement and its implications for decision-making by prey

Many classical models of food patch use under predation risk assume that predators impose patch-specific predation risks independent of prey behavior. These models predict that prey should leave a chosen patch only if and when the food depletes below some critical level. In nature, however, prey individuals may regularly move among food patches, even in the apparent absence of food depletion. We suggest that such prey movement is part of a predator-prey "shell game", in which predators attempt to learn prey location, and the prey attempt to be unpredictable in space. We investigate this shell game using an individual-based model that allows predators to update information about prey location, and permits prey to move with some random component among patches, but with reduced energy intake. Our results show the best prey strategy depends on what the predator does. A non-learning (randomly moving) predator favors non-moving prey – moving prey suffer higher starvation and predation. However, a learning predator favors prey movement. In general, the best prey strategy involves movement biased toward, but not completely committed to, the richer food patch. The strategy of prey movement remains beneficial even in combination with other anti-predator defenses, such as prey vigilance.     

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

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

Network analyses reveal the role of large snakes in connecting feeding guilds in a species‐rich Amazonian snake community

In ecological communities, interactions between consumers and resources lead to the emergence of ecological networks and a fundamental problem to solve is to understand which factors shape network structure. Empirical and theoretical studies on ecological networks suggest predator body size is a key factor structuring patterns of interaction. Because larger predators consume a wider resource range, including the prey consumed by smaller predators, we hypothesized that variation in body size favors the rise of nestedness. In contrast, if resource consumption requires specific adaptations, predators are expected to consume distinct sets of resources, thus favoring modularity. We investigate these predictions by characterizing the trophic network of a species‐rich Amazonian snake community (62 species). Our results revealed an intricate network pattern resulting from larger species feeding on higher diversity of prey and therefore promoting nestedness, whereas snakes with specific lifestyles and feeding on distinct resources, promoting modularity. Species removal simulations indicated that the nested structure is favored mainly by the presence of five species of the family Boidae, which because of their body size and generalist lifestyles connect modules in the network. Our study highlights the particular ways traits affect the structure of interactions among consumers and resources at the community level.     

Scale Dependence of Female Ungulate Reproductive Success in Relation to Nutritional Condition,Resource Selection and Multi-Predator Avoidance

Female ungulate reproductive success is dependent on the survival of their young, and affected by maternal resource selection, predator avoidance, and nutritional condition. However, potential hierarchical effects of these factors on reproductive success are largely unknown, especially in multi-predator landscapes. We expanded on previous research of neonatal white-tailed deer (Odocoileus virginianus) daily survival within home ranges to assess if resource use, integrated risk of 4 mammalian predators, maternal nutrition, winter severity, hiding cover, or interactions among these variables best explained landscape scale variation in daily or seasonal survival during the post-partum period. We hypothesized that reproductive success would be limited greater by predation risk at coarser spatiotemporal scales, but habitat use at finer scales. An additive model of daily non-ideal resource use and maternal nutrition explained the most (69%) variation in survival; though 65% of this variation was related to maternal nutrition. Strong support of maternal nutrition across spatiotemporal scales did not fully support our hypothesis, but suggested reproductive success was related to dam behaviors directed at increasing nutritional condition. These behaviors were especially important following severe winters, when dams produced smaller fawns with less probability of survival. To increase nutritional condition and decrease wolf (Canis lupus) predation risk, dams appeared to place fawns in isolated deciduous forest patches near roads. However, this resource selection represented non-ideal resources for fawns, which had greater predation risk that led to additive mortalities beyond those related to resources alone. Although the reproductive strategy of dams resulted in greater predation of fawns from alternative predators, it likely improved the life-long reproductive success of dams, as many were late-aged (>10 years old) and could have produced multiple litters of fawns. Our study emphasizes understanding the scale-dependent hierarchy of factors limiting reproductive success is essential to providing reliable knowledge for ungulate management.