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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

Predator diversity and identity drive interaction strength and trophic cascades in a food web

Declining predator diversity may drastically affect the biomass and productivity of herbivores and plants. Understanding how changes in predator diversity can propagate through food webs to alter ecosystem function is one of the most challenging ecological research topics today. We studied the effects of predator removal in a simple natural food web in the Sierra Nevada mountains of California (USA). By excluding the predators of the third trophic level of a food web in a full-factorial design, we monitored cascading effects of varying predator diversity and composition on the herbivorous beetle Chrysomela aeneicollis and the willow Salix orestera, which compose the first and second trophic levels of the food web. Decreasing predator diversity increased herbivore biomass and survivorship, and consequently increased the amount of plant biomass consumed via a trophic cascade. Despite this simple linear mean effect of diversity on the strength of the trophic cascade, we found additivity, compensation, and interference in the effects of multiple predators on herbivores and plants. Herbivore survivorship and predator-prey interaction strengths varied with predator diversity, predator identity, and the identity of coexisting predators. Additive effects of predators on herbivores and plants may have been driven by temporal niche separation, whereas compensatory effects and interference occurred among predators with a similar phenology. Together, these results suggest that while the general trends of diversity effects may appear linear and additive, other information about species identity was required to predict the effects of removing individual predators. In a community that is not temporally well-mixed, predator traits such as phenology may help predict impacts of species loss on other species. Information about predator natural history and food web structure may help explain variation in predator diversity effects on trophic cascades and ecosystem function.     

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.     

Birds defend oil palms from herbivorous insects.

Top-down forces are expected to be important in regulating herbivore populations in most agricultural systems where primary productivity is high and species diversity is low. Under such conditions, trophic cascades are predicted to occur when predator populations are reduced or removed. Studies on how predator removal indirectly affects herbivory rates in agricultural systems are lacking. Through a bird-exclosure experiment, I test the hypothesis that insectivorous birds indirectly defend oil palms (Elaeis guineensis) from herbivorous insects. Results show that bird exclusion significantly increased herbivory damage to oil palms, and that the size of this exclusion effect increased with bird density, although the latter result was not statistically significant. These findings suggest that insectivorous birds deliver a natural pest control service for oil palm agriculture, which is important not only for the direct benefits it delivers for human welfare, but also in strengthening the economic justifications for conserving the remaining natural habitats and biodiversity in agricultural landscapes.     

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.     

Simulated predator extinctions: predator identity affects survival and recruitment of oysters

The rate of species loss is increasing at a global scale, and human-induced extinctions are biased toward predator species. We examined the effects of predator extinctions on a foundation species, the eastern oyster (Crassostrea virginica). We performed a factorial experiment manipulating the presence and abundance of three of the most common predatory crabs, the blue crab (Callinectes sapidus), stone crab (Menippe mercenaria), and mud crab (Panopeus herbstii) in estuaries in the eastern United States. We tested the effects of species richness and identity of predators on juvenile oyster survival, oyster recruitment, and organic matter content of sediment. We also manipulated the density of each of the predators and controlled for the loss of biomass of species by maintaining a constant mass of predators in one set of treatments and simultaneously using an additive design. This design allowed us to test the density dependence of our results and test for functional compensation by other species. The identity of predator species, but not richness, affected oyster populations. The loss of blue crabs, alone or in combination with either of the other species, affected the survival rate of juvenile oysters. Blue crabs and stone crabs both affected oyster recruitment and sediment organic matter negatively. Mud crabs at higher than ambient densities, however, could fulfill some of the functions of blue and stone crabs, suggesting a level of ecological redundancy. Importantly, the strong effects of blue crabs in all processes measured no longer occurred when individuals were present at higher-than-ambient densities. Their role as dominant predator is, therefore, dependent on their density within the system and the density of other species within their guild (e.g., mud crabs). Our findings support the hypothesis that the effects of species loss at higher trophic levels are determined by predator identity and are subject to complex intraguild interactions that are largely density dependent. Understanding the role of biodiversity in ecosystem functioning or addressing practical concerns, such as loss of predators owing to overharvesting, remains complicated because accurate predictions require detailed knowledge of the system and should be drawn from sound experimental evidence, not based on observations or generalized models.     

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.     

Increasing enemy biodiversity strengthens herbivore suppression on two plant species

Concern over biodiversity loss, especially at higher trophic levels, has led to a surge in studies investigating how changes in natural enemy diversity affect community and ecosystem functioning. These studies have found that increasing enemy diversity can strengthen, weaken, and not affect prey suppression, demonstrating that multi-enemy effects on prey are context-dependent. Here we ask how one factor, plant species identity, influences multi-enemy effects on prey. We focused on two plant species of agricultural importance, potato (Solanum tuberosum), and collards (Brassica oleracea L.). These species share a common herbivorous pest, the green peach aphid (Myzus persicae), but vary in structural and chemical traits that affect aphid reproductive rates and which may also influence inter-enemy interactions. In a large-scale field experiment, overall prey exploitation varied dramatically among the plant species, with enemies reducing aphid populations by approximately 94% on potatoes and approximately 62% on collards. Increasing enemy diversity similarly strengthened aphid suppression on both plants, however, and there was no evidence that plant species identity significantly altered the relationship between enemy diversity and prey suppression. Microcosm experiments suggested that, on both collards and potatoes, intraspecific competition among natural enemies exceeded interspecific competition. Enemy species showed consistent and significant differences in where they foraged on the plants, and enemies in the low-diversity treatment tended to spend less time foraging than enemies in the high-diversity treatment. These data suggest that increasing enemy diversity may strengthen aphid suppression because interspecific differences in where enemies forage on the plant allow for greater resource partitioning. Further, these functional benefits of diversity appear to be robust to changes in plant species identity.     

Consequences of stage-structured predators: cannibalism, behavioral effects, and trophic cascades

Cannibalistic and asymmetrical behavioral interactions between stages are common within stage-structured predator populations. Such direct interactions between predator stages can result in density- and trait-mediated indirect interactions between a predator and its prey. A set of structured predator-prey models is used to explore how such indirect interactions affect the dynamics and structure of communities. Analyses of the separate and combined effects of stage-structured cannibalism and behavior-mediated avoidance of cannibals under different ecological scenarios show that both cannibalism and behavioral avoidance of cannibalism can result in short- and long-term positive indirect connections between predator stages and the prey, including "apparent mutualism." These positive interactions alter the strength of trophic cascades such that the system's dynamics are determined by the interaction between bottom-up and top-down effects. Contrary to the expectation of simpler models, enrichment increases both predator and prey abundance in systems with cannibalism or behavioral avoidance of cannibalism. The effect of behavioral avoidance of cannibalism, however, depends on how strongly it affects the maturation rate of the predator. Behavioral interactions between predator stages reduce the short-term positive effect of cannibalism on the prey density, but can enhance its positive long-term effects. Both interaction types reduce the destabilizing effect of enrichment. These results suggest that inconsistencies between data and simple models can be resolved by accounting for stage-structured interactions within and among species.     

Invasion, Disturbance, and Competition: Modeling the Fate of Coastal Plant Populations

Abstract:  Wetland habitats are besieged by biotic and abiotic disturbances such as invasive species, hurricanes, habitat fragmentation, and salinization. Predicting how these factors will alter local population dynamics and community structure is a monumental challenge. By examining ecologically similar congeners, such as Iris hexagona and I. pseudacorus (which reproduce clonally and sexually and tolerate a wide range of environmental conditions), one can identify life-history traits that are most influential to population growth and viability. We combined empirical data and stage-structured matrix models to investigate the demographic responses of native ( I. hexagona ) and invasive ( I. pseudacorus ) plant populations to hurricanes and salinity stress in freshwater and brackish wetlands. In our models I. hexagona and I. pseudacorus responded differently to salinity stress, and species coexistence was rare. In 82% of computer simulations of freshwater marsh, invasive iris populations excluded the native species within 50 years, whereas native populations excluded the invasive species in 99% of the simulations in brackish marsh. The occurrence of hurricanes allowed the species to coexist, and species persistence was determined by the length of time it took the ecosystem to recover. Rapid recovery (2 years) favored the invasive species, whereas gradual recovery (30 years) favored the native species. Little is known about the effects of hurricanes on competitive interactions between native and invasive plant species in marsh ecosystems. Our models contribute new insight into the relationship between environmental disturbance and invasion and demonstrate how influential abiotic factors such as climate change will be in determining interspecific interactions.     

Food resource partitioning in a Mediterranean demersal fish assemblage: the effect of body size and niche width

We investigated the effects of body size, feeding strategy and depth distribution on the trophic resource partitioning among the 26 dominant fish consumers in a fish assemblage on the central Mediterranean shelf-break. The fish assemblage was structured in two major trophic guilds: epibenthic and zooplanktonic feeders, according to the position of each predator along the benthos–plankton gradient. Within each main guild, the species were segregated along a prey-size or fish-size gradient into five further guilds. Fish size and prey size were strongly correlated, indicating that the prey-size niche can be well explained by predator size. Fish consumers showed a significant negative correlation between the similarity in prey type and the similarity in depth distribution; most species with similar trophic preferences segregated along the depth dimension. The only predators overlapping in both food and depth preferences were those with a more specialist trophic behavior. These results suggest that fish body size and depth preferences are the two main niche dimensions, explaining a large part of the coexistence between the Mediterranean shelf-break fish consumers.