Trade-offs, temporal variation, and species coexistence in communities with intraguild predation

Intraguild predation/parasitism (IGP: competing species preying on or parasitizing each other) is widespread in nature, but the mechanisms by which intraguild prey and predators coexist remain elusive. Theory predicts that a trade-off between resource competition and IGP should allow local niche partitioning, but such trade-offs are expressed only at intermediate resource productivity and cannot explain observations of stable coexistence at high productivity. Coexistence must therefore involve additional mechanisms beside the trade-off, but very little is known about the operation of such mechanisms in nature. Here I present the first experimental test of multiple coexistence mechanisms in a natural community exhibiting IGP. The results suggest that, when resource productivity constrains the competition-IGP trade-off, a temporal refuge for the intraguild prey can not only promote coexistence, but also change species abundances to a pattern qualitatively different from that expected based on the trade-off or a refuge alone. This is the first empirical study to demonstrate a mechanism for why communities with IGP do not lose species diversity in highly productive environments. These results have implications for diversity maintenance in multi-trophic communities, and the use of multiple natural enemies in biological control.     

Alternative prey and the dynamics of intraguild predation: theoretical perspectives

A rich body of theoretical literature now exists focused on the three-species module of intraguild predation (IGP), in which a top predator both attacks and competes with an intermediate predator. Simple models of intraguild predation are often unstable, either because one consumer is excluded, or because sustained oscillations emerge from long feedback loops. Yet, many natural IGP systems robustly persist. Standard models of intraguild predation simplify natural systems in crucial ways that could influence persistence; in particular, many empirical IGP systems are embedded in communities with alternative prey species. We briefly review the key conclusions of standard three-species IGP theory, and then present results of theoretical explorations of how alternative prey can influence the persistence and stability of a focal intraguild predation interaction.     

The interaction of cannibalism and omnivory: consequences for community dynamics

Although cannibalism is ubiquitous in food webs and frequent in systems where a predator and its prey also share a common resource (intraguild predation, IGP), its impacts on species interactions and the dynamics and structure of communities are still poorly understood. In addition, the few existing studies on cannibalism have generally focused on cannibalism in the top-predator, ignoring that it is frequent at intermediate trophic levels. A set of structured models shows that cannibalism can completely alter the dynamics and structure of three-species IGP systems depending on the trophic position where cannibalism occurs. Contrary to the expectations of simple models, the IG predator can exploit the resources more efficiently when it is cannibalistic, enabling the predator to persist at lower resource densities than the IG prey. Cannibalism in the IG predator can also alter the effect of enrichment, preventing predator-mediated extinction of the IG prey at high productivities predicted by simple models. Cannibalism in the IG prey can reverse the effect of top-down cascades, leading to an increase in the resource with decreasing IG predator density. These predictions are consistent with current data. Overall, cannibalism promotes the coexistence of the IG predator and IG prey. These results indicate that including cannibalism in current models can overcome the discrepancy between theory and empirical data. Thus, we need to measure and account for cannibalistic interactions to reliably predict the structure and dynamics of communities.     

Coexistence of intraguild predators and prey in resource-rich environments

The prevalence of intraguild predation (IGP) in productive environments has long puzzled ecologists. Theory predicts the exclusion of intraguild prey from such environments, but data consistently defy this expectation. This suggests that coexistence mechanisms at high resource productivity may differ from those at lower productivity. Here I present a mathematical model that investigates multiple coexistence mechanisms. I incorporate two biological features widely observed in IGP communities: intraspecific interference via cannibalism or superparasitism, and temporal refuges arising from differential sensitivities to abiotic variation. I develop predictions based on three aspects of the IG prey-IG predator interaction: mutual invasibility, transient dynamics, and long-term abundances. These predictions specify the conditions under which coexistence mechanisms reinforce vs. deter one another: when a competition-IGP trade-off allows coexistence at intermediate productivity a temporal refuge for the intraguild prey always allows coexistence at high productivity, but intraspecific interference does so only at a net fitness cost to the intraguild predator. Intraspecific interference that benefits the intraguild predator not only reduces tradeoff-mediated coexistence at intermediate productivity, but also undermines the refuge's coexistence-enhancing effect at high productivity. Different mechanism combinations yield characteristic signatures in time series data during transient dynamics. By judicious measurement of parameters and examining time series for critical signatures, one can elucidate the mechanisms that allow IGP to prevail in resource-rich environments.     

Intraguild predation in the presence of a shared natural enemy

Intraguild predation (IGP) is a widespread phenomenon in nature, and yet the simplest theoretical models of IGP predict that coexistence of intraguild predator and prey is only possible under restrictive assumptions. Here I examine how a specialist or generalist natural enemy of these species affects their long-term persistence and abundance, as functions of the natural enemy's relative attack severity and fecundity on each species. Notably, I show that failure to include the effects of a higher trophic level in models of IGP can lead to incorrect predictions about the coexistence or exclusion of guild members. I then consider how an interaction between native species and a natural enemy is perturbed by the arrival of an invasive intraguild predator. I outline the conditions under which the native species and/or its natural enemy are threatened by the arrival of the intraguild predator, and also when the natural enemy is beneficial in preventing the initial invasion or eventual dominance of the invader. This work provides new insights on the influence of omnivory on food web stability, and also generates testable hypotheses for predicting the impact of a novel intraguild predator on the recipient community at multiple trophic levels.     

Habitat structure affects intraguild predation

Intraguild predation is thought to be ubiquitous in natural food webs. Yet, theory on intraguild predation predicts the intraguild prey to persist only under limited conditions. This gap between theory and empirical observations needs scrutiny. One reason might be that theory has focused on equilibrium dynamics and a limited set of species (usually three) that interact in well-mixed populations in unstructured habitats, and these assumptions will often not hold in natural systems. In this review, we focus on the effects of habitat structure on intraguild predation. Habitat structure could reduce encounter rates between predators and prey and could create refuges for prey. In both cases, habitat structure could reduce the strength of intraguild interactions, thereby facilitating species coexistence. A meta-analysis of studies on manipulation of habitat structure shows that intraguild prey indeed suffer less from intraguild predation in structured habitats. This was further confirmed by a meta-analysis in which studies on intraguild predation were classified according to habitat structure. Intraguild predation reduced densities of the intraguild prey significantly more in habitats with little structure than in habitats rich in structure. The effect of intraguild predation on the shared prey was negative, and not significantly affected by habitat structure. We conclude that habitat structure may increase persistence of the intraguild prey by decreasing the strength of the interaction between intraguild predator and intraguild prey.     

The influence of intraguild predation on prey suppression and prey release: a meta-analysis

Intraguild predation (IGP) occurs when one predator species consumes another predator species with whom it also competes for shared prey. One question of interest to ecologists is whether multiple predator species suppress prey populations more than a single predator species, and whether this result varies with the presence of IGP. We conducted a meta-analysis to examine this question, and others, regarding the effects of IGP on prey suppression. When predators can potentially consume one another (mutual IGP), prey suppression is greater in the presence of one predator species than in the presence of multiple predator species; however, this result was not found for assemblages with unidirectional or no IGP. With unidirectional IGP, intermediate predators were generally more effective than the top predator at suppressing the shared prey, in agreement with IGP theory. Adding a top predator to an assemblage generally caused prey to be released from predation, while adding an intermediate predator caused prey populations to be suppressed. However, the effects of adding a top or intermediate predator depended on the effectiveness of these predators when they were alone. Effects of IGP varied across different ecosystems (e.g., lentic, lotic, marine, terrestrial invertebrate, and terrestrial vertebrate), with the strongest patterns being driven by terrestrial invertebrates. Finally, although IGP theory is based on equilibrium conditions, data from short-term experiments can inform us about systems that are dominated by transient dynamics. Moreover, short-term experiments may be connected in some way to equilibrium models if the predator and prey densities used in experiments approximate the equilibrium densities in nature.     

Food webs and intraguild predation: community interactions of a native mesocarnivore

Trophic level interactions between predators create complex relationships such as intraguild predation. Theoretical research has predicted two possible paths to stability in intraguild systems: intermediate predators either outcompete higher-order predators for shared resources or select habitat based on security. The effects of intraguild predation on intermediate mammalian predators such as swift foxes (Vulpes velox) are not well understood. We examined the relationships between swift foxes and both their predators and prey, as well the effect of vegetation structure on swift fox-coyote (Canis latrans) interactions, between August 2001 and August 2004. In a natural experiment created by the Pinon Canyon Maneuver Site in southeastern Colorado, USA, we documented swift fox survival and density in a variety of landscapes and compared these parameters in relation to prey availability, coyote abundance, and vegetation structure. Swift fox density varied significantly between study sites, while survival did not. Coyote abundance was positively related to the basal prey species and vegetation structure, while swift fox density was negatively related to coyote abundance, basal prey species, and vegetation structure. Our results support the prediction that, under intraguild predation in terrestrial systems, top predator distribution matches resource availability (resource match), while intermediate predator distribution inversely matches predation risk (safety match). While predation by coyotes may be the specific cause of swift fox mortality in this system, the more general mechanism appears to be exposure to predation moderated by shrub density.     

Effects of combining an intraguild predator with a cannibalistic intermediate predator on a species-level trophic cascade

A greater diversity of natural enemies can in some cases disrupt prey suppression, particularly when natural enemies engage in intraguild predation, where natural enemies compete with and prey upon each other. However, empirical studies have often demonstrated enhanced prey suppression despite intraguild predation. A recent theoretical study proposed the hypothesis that, when the intermediate predator is cannibalistic, intraguild predation can reduce cannibalism within the intermediate predator population, leading to little change in intermediate predator mortality and thus enhanced prey suppression. The goal of this study was to examine this hypothesis empirically. Two summer-long field enclosure experiments were conducted in cotton fields. We investigated the effects of adding an intraguild predator, Zelus renardii, on (1) the abundance of a cannibalistic intermediate predator, Geocoris pallens, (2) the abundance of a herbivore, Lygus hesperus, and (3) cotton plant performance. G. pallens adult abundance did not increase, even when food availability was high and natural enemies were absent, suggesting that density-dependent cannibalism imposes an upper limit on its densities. Furthermore, although Z. renardii is an intraguild predator of G. pallens, G. pallens long-term densities were unaffected by Z. renardii. In the presence of the intermediate predator, the addition of the intraguild predator Z. renardii enhanced suppression of L. hesperus, and there were suggestions that Z. renardii and G. pallens partitioned the L. hesperus population. Effects of herbivore suppression cascaded to the plant level, improving plant performance. In conclusion, we provide empirical support for the hypothesis that the addition of an intraguild predator may enhance prey suppression if the intermediate predator expresses density-dependent cannibalism. Intraguild predation and cannibalism co-occur in many communities; thus their joint effects may be broadly important in shaping predator effects on herbivores and plant performance.     

Adaptive prey behavior and the dynamics of intraguild predation systems

Intraguild predation constitutes a widespread interaction occurring across different taxa, trophic positions and ecosystems, and its endogenous dynamical properties have been shown to affect the abundance and persistence of the involved populations as well as those connected with them within food webs. Although optimal foraging decisions displayed by predators are known to exert a stabilizing influence on the dynamics of intraguild predation systems, few is known about the corresponding influence of adaptive prey decisions in spite of its commonness in nature. In this study, we analyze the effect that adaptive antipredator behavior exerts on the stability and persistence of the populations involved in intraguild predation systems. Our results indicate that adaptive prey behavior in the form of inducible defenses act as a stabilizing mechanism and show that, in the same direction that adaptive foraging, enhances the parameter space in which species can coexist through promoting persistence of the IG-prey. At high levels of enrichment, the intraguild predation system exhibits unstable dynamics and zones of multiples attractors. In addition, we show that the equilibrium density of the IG-predator could be increased at intermediate values of defense effectiveness. Finally we conclude that adaptive prey behavior is an important mechanism leading to species coexistence in intraguild predation systems and consequently enhancing stability of food webs.     

The community effects of phenotypic and genetic variation within a predator population

Natural populations are heterogeneous mixtures of individuals differing in physiology, morphology, and behavior. Despite the ubiquity of phenotypic variation within natural populations, its effects on the dynamics of ecological communities are not well understood. Here, we use a quantitative genetics framework to examine how phenotypic variation in a predator affects the outcome of apparent competition between its two prey species. Classical apparent competition theory predicts that prey have reciprocally negative effects on each other. The addition of phenotypic trait variation in predation can marginalize these negative effects, mediate coexistence, or generate positive indirect effects between the prey species. Long-term coexistence or facilitation, however, can be preceded by long transients of extinction risk whenever the heritability of phenotypic variation is low. Greater heritability can circumvent these ecological transients but also can generate oscillatory and chaotic dynamics. These dramatic changes in ecological outcomes, in the sign of indirect effects, and in stability suggest that studies which ignore intraspecific trait variation may reach fundamentally incorrect conclusions regarding ecological dynamics.     

Impact of cannibalism on predator-prey dynamics: size-structured interactions and apparent mutualism

Direct and indirect interactions between two prey species can strongly alter the dynamics of predator-prey systems. Most predators are cannibalistic, and as a consequence, even systems with only one predator and one prey include two prey types: conspecifics and heterospecifics. The effects of the complex direct and indirect interactions that emerge in such cannibalistic systems are still poorly understood. This study examined how the indirect interaction between conspecific and heterospecific prey affects cannibalism and predation rates and how the direct interactions between both species indirectly alter the effect of the cannibalistic predator. I tested for these effects using larvae of the stream salamanders Eurycea cirrigera (prey) and Pseudotriton ruber (cannibalistic predator) by manipulating the relative densities of the conspecific and heterospecific prey in the presence and absence of the predator in experimental streams. The rates of cannibalism and heterospecific predation were proportional to the respective densities and negatively correlated, indicating a positive indirect interaction between conspecific and heterospecific prey, similar to "apparent mutualism." Direct interactions between prey species did not alter the effect of the predator. Although both types of prey showed a similar 30% reduction in night activity and switch in microhabitat use in response to the presence of the predator, cannibalism rates were three times higher than heterospecific predation rates irrespective of the relative densities of the two types of prey. Cumulative predation risks differed even more due to the 48% lower growth rate of conspecific prey. Detailed laboratory experiments suggest that the 3:1 difference in cannibalism and predation rate was due to the higher efficiency of heterospecific prey in escaping immediate attacks. However, no difference was observed when the predator was a closely related salamander species, Gyrinophilus porphyriticus, indicating that this difference is species specific. This demonstrates that cannibalism can result in the coupling of predator and prey mortality rates that strongly determines the dynamics of predator-prey systems.     

A predator-prey model with satiation and intraspecific competition

We present a new predator-prey model where, except for the prey growth, assumed to be logistic, we endeavor to give some behavioral justification to all elements of the predator-prey interaction. The functional response takes account of predator satiation and predator competition. It is supported by some experimental evidence. We distinguish two contributions to the numerical response: the positive part, proportional to the functional response, is the birth rate of predators; the negative part is the death rate due to hunger.Two outcomes are possible. If the prey are unable to grow fast enough to replace the amount killed by the predators, both species become extinct. In the opposite case, both populations stabilize at a constant population. At this equilibrium level, the prey are not abundant enough to satiate the predators.The predation rate that allows the highest predator population is one half of the ideal prey growth rate. A higher exploitation rate can allow higher populations only temporarily. Evolved predator behavior, reguges for the prey, or other mechanisms can explain this regulation.Two more population behaviors (cycles and predator extinction) can be obtained with a time-lag in one of the responses. This is shown in a separate paper.The model is structurally stable. It can thus withstand small environmental perturbations.     

Can rare positive interactions become common when large carnivores consume livestock?

Livestock populations in protected areas are viewed negatively because of their interaction with native ungulates through direct competition for food resources. However, livestock and native prey can also interact indirectly through their shared predator. Indirect interactions between two prey species occur when one prey modifies either the functional or numerical responses of a shared predator. This interaction is often manifested as negative effects (apparent competition) on one or both prey species through increased predation risk. But indirect interactions can also yield positive effects on a focal prey if the shared predator modifies its functional response toward increased consumption of an abundant and higher-quality alternative prey. Such a phenomenon between two prey species is underappreciated and overlooked in nature. Positive indirect effects can be expected to occur in livestock-dominated wildlife reserves containing large carnivores. We searched for such positive effects in Acacia-Zizhypus forests of India's Gir sanctuary where livestock (Bubalus bubalis and Bos indicus) and a coexisting native prey (chital deer, Axis axis) are consumed by Asiatic lions (Panthera leo persica). Chital vigilance was higher in areas with low livestock density than in areas with high livestock density. This positive indirect effect occurred because lion predation rates on livestock were twice as great where livestock were abundant than where livestock density was low. Positive indirect interactions mediated by shared predators may be more common than generally thought with rather major consequences for ecological understanding and conservation. We encourage further studies to understand outcomes of indirect interactions on long-term predator-prey dynamics in livestock-dominated protected areas.     

Intraguild predation by <Emphasis Type="Italic">Harmonia axyridis</Emphasis> on coccinellids revealed by exogenous alkaloid sequestration

Summary.  Under laboratory conditions, the multicolored Asian lady beetle, Harmonia axyridis is well known as an intraguild predator of other ladybirds. However the real impact of this exotic species on native species was poorly investigated in the field. Because many ladybird species produce alkaloids as defensive compounds, we propose here a new method of intraguild predation monitoring in coccinellids based on alkaloid quantification by GC-MS. In laboratory experiments, adaline was unambiguously detected in fourth instar larvae of H. axyridis having ingested one egg or one first instar larva of Adalia bipunctata. Although prey alkaloids in the predator decreased with time, traces were still detected in pupae, exuviae and imagines of H. axyridis having ingested one prey when they were fourth instar larvae. Analysis of H. axyridis larvae collected in two potato fields shows for the first time in Europe the presence of exogenous alkaloids in 9 out of 28 individuals tested. This new method of intraguild predation detection could be used more widely to follow the interactions between predators and potential chemically defended insect preys.     

A model for intraguild predation dynamics between immature stages

Dynamical models usually assume that predation occurs between mature stages and/or between mature and immature stages. In this work a stage-structured discrete time model is developed for a system where intraguild predation takes place only in the course of immature stages of predator and its prey. Therefore, the proposed mathematical setup demands functional relations linking predation in immature life stages with survival and fecundity in mature stages. The behavior of the model is examined in order to investigate the interplay among predator attack rate, its satiation of prey consumption and the success of intraguild predator invasion.     

Predator diversity and trophic interactions

The recognition that predators play important roles in ecosystems has prompted research to resolve how combinations of predator species influence ecosystem functions. Interactions among predator species and their prey can lead to a host of linear and nonlinear effects. Understanding the conditions causing these effects is critical for assigning predator species to functional groups in ways that lead to predictive theory of predator diversity effects on trophic interactions. To this end, I provide a synthesis of experiments examining multiple-predator-species effects on mortality of single shared prey. I show how experimental design and experimental venue can determine the conclusion about the importance of predator diversity on trophic interactions. In addition, I link natural history insights on predator species habitat and hunting behavior with linear and nonlinear multiple-predator effects to derive a new concept of predator diversity effects on trophic interactions. This concept holds that the nature of predator diversity effects is contingent upon predator species hunting mode plus predator and prey species habitat domain (defined as the spatial extent to which a microhabitat is used by a species). This concept allows the classification of multiple-predator effects into four broad functional categories: substitutable, nonlinear due to predator species interference, nonlinear due to intraguild predation, and nonlinear due to predator species synergism. Experimental evidence so far provides ample and comparatively equal support for substitutable, interference, and intraguild effects, and equivocal support for nonlinear synergisms. The paper closes by discussing ways to further a research program aimed at using the building blocks presented here to understand predator functional diversity and trophic interactions in complex ecological systems.     

Influence of prey reserve capacity on predator–prey dynamics

In this article the dynamics of a predator and prey population has been modelled when a reserve is created to protect a certain number of prey population from predation. This investigation is essential to derive some guiding principles to conserve the prey population and also to understand the behaviour and dependence of predator population on the reserve capacity. The present study concerns analysis of a fairly general model and hence some of the existing results based on specific explicit models, like Lotka–Volterra model and Rosenzweig–MacArthur model, can be derived from this work. In this study, conditions have been derived for coexistence of predator and prey, and extinction of predators. Results are obtained for global stability of required equilibrium of the model. Also, a method is suggested to compute reserve capacity in order to drive the ecosystem state to a required level. The key results developed in this article have been illustrated using numerical simulation. These results can be interpreted in different contexts like resource conservation, pest management, bio-economics of a renewable resource, etc.     

Functional responses: a question of alternative prey and predator density

Throughout the study of ecology, there has been a growing realization that indirect effects among species cause complexity in food webs. Understanding and predicting the behavior of ecosystems consequently depends on our ability to identify indirect effects and their mechanisms. The present study experimentally investigates indirect interactions arising between two prey species that share a common predator. In a natural field experiment, we introduced different densities of mealworms (Tenebrio molitor), an alternative prey, to a previously studied predator-prey system in which paper wasps (Polistes dominulus) preyed on shield beetle larvae (Cassida rubiginosa). We tested if alternative prey affects predation on the first prey (i.e., the predator-dependent functional response of paper wasps) by modifying either interference among predators or the effective number of predators foraging on shield beetles. Presence of mealworms significantly reduced the effective number of predators, whereas predator interference was not affected. In this way, the experimentally introduced alternative prey altered the wasps' functional response and thereby indirectly influenced C. rubiginosa density. In all prey-density combinations offered, paper wasps constantly preferred T. molitor. This led to an asymmetrical, indirect interaction between both prey species: an increase in mealworm density significantly relaxed predation on C. rubiginosa, whereas an increase in C. rubiginosa density intensified predation on mealworms. Such asymmetrical outcomes of a fixed food preference can significantly affect the population dynamics of the species involved. In spite of the repeated finding of a Type III functional response in this system, our experiment did not reveal switching behavior in paper wasps. The variety of mechanisms underlying direct and indirect interactions within our study system exemplifies the importance of incorporating alternative prey when investigating the impact of a generalist predator on a focal prey population under realistic field conditions.     

Stronger predation in the tropics shapes species richness patterns in marine communities

Species interactions are widely assumed to be stronger at lower latitudes, but surprisingly few experimental studies test this hypothesis, and none ties these processes to observed patterns of species richness across latitude. We report here the first experimental field test that predation is both stronger and has a disproportionate effect on species richness in the tropics relative to the temperate zone. We conducted predator-exclusion experiments on communities of sessile marine invertebrates in four regions, which span 32 degrees latitude, in the western Atlantic Ocean and Caribbean Sea. Over a three-month timescale, predation had no effect on species richness in the temperate zone. In the tropics, however, communities were from two to over ten times more species-rich in the absence of predators than when predators were present. While micro-and macro-predators likely compete for the limited prey resource in the tropics, micropredators alone were able to exert as much pressure on the invertebrate communities as the full predator community. This result highlights the extent to which exposure to even a subset of the predator guild can significantly impact species richness in the tropics. Patterns were consistent in analyses that included relative and total species abundances. Higher species richness in the absence of predators in the tropics was also observed when species occurrences were pooled across two larger spatial scales, site and region, demonstrating a consistent scaling relationship. These experimental results show that predation can both limit local species abundances and shape patterns of regional coexistence in the tropics. When preestablished diverse tropical communities were then exposed to predation for different durations, ranging from one to several days, species richness was always reduced. These findings confirmed that impacts of predation in the tropics are strong and consistent, even in more established communities. Our results offer empirical support for the long-held prediction that predation pressure is stronger at lower latitudes. Furthermore, we demonstrate the magnitude to which variation in predation pressure can contribute to the maintenance of tropical species diversity.