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.     

Predators, parasitoids, and pathogens: a cross-cutting examination of intraguild predation theory

Although the canonical concept of intraguild predation evokes images of predators and prey, several subdisciplines within ecology have developed theory not specifically framed in terms of predation and competition and often using system-specific terminology, yet functionally quite similar. Here, we formulate models combining exploitation and competition in predator-prey, host-parasitoid, and host-pathogen communities to compare dynamics, food web structure, and coexistence criteria for these disparate communities. Although dynamic stability in the coexistence region varies strongly among systems, in all cases coexistence of two consumers on a single resource occurs only if the intraguild prey species is more efficient than the intraguild predator at suppressing the abundance of the basal resource, and if the intraguild predator accrues a sufficient gain from attacking the intraguild prey. In addition, equilibrial abundances of all species in all three formulations respond similarly to increases in productivity of the basal resource. Our understanding of predator-prey and parasitoid-host communities has benefited from explicit examination of intraguild predation (IGP) theory, and we suggest that future research examining pathogen communities, in particular, will benefit substantially from explicit recognition of predictions from IGP theory.     

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.     

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.     

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.     

On the evidence for species coexistence: a critique of the coexistence program

A major challenge in ecology is to understand how the millions of species on Earth are organized into biological communities. Mechanisms promoting coexistence are one such class of organizing processes, which allow multiple species to persist in the same trophic level of a given web of species interactions. If some mechanism promotes the coexistence of two or more species, each species must be able to increase when it is rare and the others are at their typical abundances; this invasibility criterion is fundamental evidence for species coexistence regardless of the mechanism. In an attempt to evaluate the level of empirical support for coexistence mechanisms in nature, we surveyed the literature for empirical studies of coexistence at a local scale (i.e., species found living together in one place) to determine whether these studies satisfied the invasibility criterion. In our survey, only seven of 323 studies that drew conclusions about species coexistence evaluated invasibility in some way in either observational or experimental studies. In addition, only three other studies evaluated necessary but not sufficient conditions for invasibility (i.e., negative density dependence and a trade-off in performance that influences population regulation). These results indicate that, while species coexistence is a prevalent assumption for why species are able to live together in one place, critical empirical tests of this fundamental assumption of community structure are rarely performed. These tests are central to developing a more robust understanding of the relative contributions of both deterministic and stochastic processes structuring biological communities.     

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.     

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.     

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.     

Zooplankton biodiversity and lake trophic state: explanations invoking resource abundance and distribution

While empirical studies linking biodiversity to local environmental gradients have emphasized the importance of lake trophic status (related to primary productivity), theoretical studies have implicated resource spatial heterogeneity and resource relative ratios as mechanisms behind these biodiversity patterns. To test the feasibility of these mechanisms in natural aquatic systems, the biodiversity of crustacean zooplankton communities along gradients of total phosphorus (TP) as well as the vertical heterogeneity and relative abundance of their phytoplankton resources were assessed in 18 lakes in Quebec, Canada. Zooplankton community richness was regressed against TP, the spatial distribution of phytoplankton spectral groups, and the relative biomass of spectral groups. Since species richness does not adequately capture ecological function and life history of different taxa, features which are important for mechanistic theories, relationships between zooplankton functional diversity (FD) and resource conditions were examined. Zooplankton species richness showed the previously established tendency to a unimodal relationship with TP, but functional diversity declined linearly over the same gradient. Changes in zooplankton functional diversity could be attributed to changes in both the spatial distribution and type of phytoplankton resource. In the studied lakes, spatial heterogeneity of phytoplankton groups declined with TP, even while biomass of all groups increased. Zooplankton functional diversity was positively related to increased heterogeneity in cyanobacteria spatial distribution. However, a smaller amount of variation in functional diversity was also positively related to the ratio of biomass in diatoms/chrysophytes to cyanobacteria. In all observed relationships, a greater variation of functional diversity than species richness measures was explained by measured factors, suggesting that functional measures of zooplankton communities will benefit ecological research attempting to identify mechanisms behind environmental gradients affecting diversity.     

Intraguild predation and mesopredator release effect on long-lived prey

Complete extirpation of a species can generate cascading effects throughout an ecosystem, yet are precisely the goal of island eradications of pest species. “Mesopredator release effect”, an asymmetrical special case of intraguild predation, has been hypothesised as a possible indirect effect from eradications, where superpredator removal can generate a mesopredator increase which may increase the impact on their shared prey. Theoretically this suggests that for intraguild predators, the superpredator may protect the shared prey from mesopredation, and removal of superpredators alone is not recommended. We create a model of long-lived age-structured shared prey and explore the non-equilibrium dynamics of this system. The superpredator can impact all prey life-stages (adult survival and reproductive success) whereas the smaller mesopredator can only impact early life-stages (reproductive success). This model is independently tested with data from a closed oceanic island system where eradication of introduced intraguild predators is possible for conservation of threatened birds. Mesopredator release only occurs in strongly top-down moderated (resource-abundant) systems. Even when mesopredator release can occur, the negative impact of more mesopredators is outweighed by the benefit of superpredator removal, allowing recovery of the prey population. Results are robust to 10% variation in model parameters. The consideration of age-structured prey contradicts previous theoretical results for mesopredator release effect and intraguild predation. Superpredator eradication is vital for population recovery of long-lived insular species. Nonetheless island conservation must retain a whole-ecosystem perspective given the complex trophic relationships among multiple species on islands.     

Competition-colonization trade-offs and disturbance effects at multiple scales

The competition-colonization trade-off has long been a mechanism explaining patterns of species coexistence and diversity in nonequilibrium systems. It forms one explanation of the intermediate disturbance hypothesis (IDH) for local communities--specifically that diversity should be maximized at intermediate disturbance frequencies, yet only a fraction of empirical studies support IDH predictions. Similarly, this trade-off is also a powerful explanation of coexistence at larger spatial scales. I show, with a microbial experimental system, that the diversity-disturbance relationship is dependent on the relative distribution of species along this trade-off. Here I show that, when species are skewed toward late-successional habits, local diversity declines with disturbance. Yet, despite this trait skew, diversity at scales larger than the patch appears insensitive to the trade-off distribution. Intermediate disturbance frequencies produce the greatest diversity in patch successional stage, thus benefiting the maximum number of species at larger scales.     

Competition, predation and coexistence in a three trophic system

Simple ecological models that mostly operate with population densities using continuous variables, explain quite well the behavior of real populations. In this work we propose and discuss the continuous dynamics of a system of three species, which belongs to the well-known family of Lotka–Volterra models. In particular, the proposed model includes direct effects such as predation and competition among species, and indirect effects such as refuge. The model is proposed to explain recent studies about a group of crustacean (amphipods of genus Hyallela) found in all the plain streams and shallow lakes of the American continent. The studied system includes three compartments: algae, a strictly herbivore amphipod and an omnivore (herbivore and carnivore) one. The analysis of the model shows that there are stable extinction equilibria throughout all the parameters’ space. There are also equilibria with stable coexistence of the three species and two interesting binary equilibria: one with stable coexistence of algae and herbivore and other with coexistence between algae and omnivore amphipods. The presence of Allee effect in the algae growth and the existence of refuge for the herbivore amphipod (prey) determine a bottom-up control.     

Consumptive and nonconsumptive effects of predators on metacommunities of competing prey

Although predators affect prey both via consumption and by changing prey migration behavior, the interplay between these two effects is rarely incorporated into spatial models of predator-prey dynamics and competition among prey. We develop a model where generalist predators have consumptive effects (i.e., altering the likelihood of local prey extinction) as well as nonconsumptive effects (altering the likelihood of colonization) on spatially separated prey populations (metapopulations). We then extend this model to explore the effects of predators on competition among prey. We find that generalist predators can promote persistence of prey metapopulations by promoting prey colonization, but predators can also hasten system-wide extinction by either increasing local extinction or reducing prey migration. By altering rates of prey migration, predators in one location can exert remote control over prey dynamics in another location via predator-mediated changes in prey flux. Thus, the effect of predators may extend well beyond the proportion of patches they visit. In the context of prey metacommunities, predator-mediated shifts in prey migration and mortality can shift the competition-colonization trade-off among competing prey, leading to changes in the prey community as well as changes in the susceptibility of prey species to habitat loss. Consequently, native prey communities may be susceptible to invasion not only by exotic prey species that experience reduced amounts of mortality from resident predators, but also by exotic prey species that exhibit strong dispersal in response to generalist native predators. Ultimately, our work suggests that the consumptive and nonconsumptive effects of generalist predators may have strong, yet potentially cryptic, effects on competing prey capable of mediating coexistence, fostering invasion, and interacting with anthropogenic habitat alteration.     

Evolving metacommunities: toward an evolutionary perspective on metacommunities

The metacommunity framework predicts that local coexistence depends on the outcome of local species interactions and regional migration. In analogous fashion, spatial structure among populations can shape species interactions through evolutionary mechanisms. Yet, most metacommunity theories assume that populations do not evolve. Here, we evaluate how evolution shapes local species coexistence and exclusion within the multiscale and multispecies context embodied by the metacommunity framework. In general, coexistence in joint ecological-evolutionary models requires low to intermediate dispersal rates that can promote maintenance of both regional species and genetic diversity. These conditions support a set of key mechanisms that modify patterns of species coexistence including local adaptation, gene storage effects, genetic rescue effects, spatial genetic subsidies, and metacommunity evolution. Multispecies extensions indicate that correlated selection can further alter the outcome of interspecific interactions depending on the magnitude and direction of correlations and shape of fitness trade-offs. We suggest that an evolving metacommunity perspective has the potential to generate novel predictions about community structure and function by incorporating the genetic and species diversity that characterize natural communities. In adopting such a perspective, we seek to facilitate understanding about the interactions between evolutionary and metacommunity dynamics.     

Biodiversity mediates productivity through different mechanisms at adjacent trophic levels

Biodiversity may enhance productivity either because diverse communities more often contain productive species (selection effects) or because they show greater complementarity in resource use. Our understanding of how these effects influence community production comes almost entirely from studies of plants. To test whether previous results apply to higher trophic levels, we first used simulations to derive expected contributions of selection and complementarity to production in competitive assemblages defined by either neutral interactions, dominance, or a trade-off between growth and competitive ability. The three types of simulated assemblages exhibited distinct interaction signatures when diversity effects were partitioned into selection and complementarity components. We then compared these signatures to those of experimental marine communities. Diversity influenced production in fundamentally different ways in assemblages of macroalgae, characterized by growth-competition trade-offs, vs. in herbivores, characterized by dominance. Forecasting the effects of changing biodiversity in multitrophic ecosystems will require recognizing that the mechanism by which diversity influences functioning can vary among trophic levels in the same food web.     

Suppression of soybean aphid by generalist predators results in a trophic cascade in soybeans.

Top-down regulation of herbivores in terrestrial ecosystems is pervasive and can lead to trophic cascades that release plants from herbivory. Due to their relatively simplified food webs, agroecosystems may be particularly prone to trophic cascades, a rationale that underlies biological control. However, theoretical and empirical studies show that, within multiple enemy assemblages, intraguild predation (IGP) may lead to a disruption of top-down control by predators. We conducted a factorial field study to test the separate and combined effects of predators and parasitoids in a system with asymmetric IGP. Specifically we combined ambient levels of generalist predators (mainly Coccinellidae) of the soybean aphid, Aphis glycines Matsumura, with controlled releases of the native parasitoid Lysiphlebus testaceipes (Cresson) and measured their impact on aphid population growth and soybean biomass and yield. We found that generalist predators provided strong, season-long aphid suppression, which resulted in a trophic cascade that doubled soybean biomass and yield. However, contrary to our expectations, L. testaceipes provided minor aphid suppression and only when predators were excluded, which resulted in nonadditive effects when both groups were combined. We found direct and indirect evidence of IGP, but because percentage parasitism did not differ between predator exclusion and ambient predator treatments, we concluded that IGP did not disrupt parasitism during this study. Our results support theoretical predictions that intraguild predators which also provide strong herbivore suppression do not disrupt top-down control of herbivores.