Optimal intraguild foraging and population stability

This article explores effects of adaptive intraguild predation on species coexistence and community structure in three species' food webs. Two Lotka-Volterra models that assume a trade-off between competition and predation strength are considered in detail. The first model does not explicitly model resource dynamics and is considered with both nonadaptive and adaptive intraguild predation; in the latter case predators choose their diet in order to maximize their instantaneous population growth rate. The second model includes resource population dynamics. Effects of adaptive intraguild predation on the community structure along a gradient in environment productivity are analyzed and compared with some experimental results of protist food webs. Conditions under which intraguild predation is adaptive are discussed for both models. It is proved that if intraguild predators are perfect optimizers then intraguild predation should decrease with increasing environmental productivity and adaptive intraguild predation is a stabilizing factor provided environmental productivity is high enough.     

Order of invasion affects the spatial distribution of a reciprocal intraguild predator

When intraguild predation is reciprocal, i.e. two predator species kill and feed on each other, theory predicts that well-mixed populations of the two species cannot coexist. At low levels of the shared resource, only the best competitor exists, whereas if the level of the common resource is high, the first species to arrive on a patch can reach high numbers, which prevents the invasion of the second species through intraguild predation. The order of invasion may therefore be of high importance in systems with reciprocal intraguild predation with high levels of productivity, with the species arriving first excluding the other species. However, natural systems are not well mixed and usually have a patchy structure, which gives individuals the possibility to choose patches without the other predator, thus reducing opportunities for intraguild predation. Such avoidance behaviour can cause spatial segregation between predator species, which, in turn, may weaken the intraguild interaction strength and facilitate their co-occurrence in patchy systems. Using a simple set-up, we studied the spatial distribution of two reciprocal intraguild predators when either of them was given priority on a patch with food. We released females of two predatory mite species sequentially and found that both species avoided patches on which the other species was resident. This resulted in partial spatial segregation of the species and thus a lower chance for the two species to encounter each other. Such behaviour reinforces segregation, because heterospecifics avoid patches with established populations of the other species. This may facilitate coexistence of two intraguild predators that would exclude each other in well-mixed populations.     

Reciprocal intraguild predation and predator coexistence

Intraguild predation is a mix of competition and predation and occurs when one species feeds on another species that uses similar resources. Theory predicts that intraguild predation hampers coexistence of species involved, but it is common in nature. It has been suggested that increasing habitat complexity and the presence of alternative food may promote coexistence. Reciprocal intraguild predation limits possibilities for coexistence even further. Habitat complexity and the presence of alternative food are believed to promote coexistence. We investigated this using two species of predatory mites, Iphiseiodes zuluagai and Euseius concordis, by assessing co‐occurrence in the field and on arenas differing in spatial structure in the laboratory. The predators co‐occured on the same plants in the field. In the laboratory, adults of the two mites fed on juveniles of the other species, both in the presence and the absence of a shared food source, showing that the two species are involved in reciprocal intraguild predation. Adults of I. zuluagai also attacked adults of E. concordis. This suggests limited possibilities for coexistence of the two species. Indeed, E. concordis invariably went extinct extremely rapidly on arenas without spatial structure with populations consisting of all stages of the two predators and with a shared resource. Coexistence was prolonged on host plant leaves with extra food sources, but E. concordis still went extinct. On small, intact plants, coexistence of the two species was much longer, and ended with the other species, I. zuluagai, often going extinct. These results suggest that spatial structure and the presence of alternative food increase the coexistence period of intraguild predators.     

Dynamics of a intraguild predation model with generalist or specialist predator

Intraguild predation (IGP) is a combination of competition and predation which is the most basic system in food webs that contains three species where two species that are involved in a predator/prey relationship are also competing for a shared resource or prey. We formulate two intraguild predation (IGP: resource, IG prey and IG predator) models: one has generalist predator while the other one has specialist predator. Both models have Holling-Type I functional response between resource-IG prey and resource-IG predator; Holling-Type III functional response between IG prey and IG predator. We provide sufficient conditions of the persistence and extinction of all possible scenarios for these two models, which give us a complete picture on their global dynamics. In addition, we show that both IGP models can have multiple interior equilibria under certain parameters range. These analytical results indicate that IGP model with generalist predator has “top down” regulation by comparing to IGP model with specialist predator. Our analysis and numerical simulations suggest that: (1) Both IGP models can have multiple attractors with complicated dynamical patterns; (2) Only IGP model with specialist predator can have both boundary attractor and interior attractor, i.e., whether the system has the extinction of one species or the coexistence of three species depending on initial conditions; (3) IGP model with generalist predator is prone to have coexistence of three species.     

Effects of intraguild predation on resource competition.

In this work, a simple Lotka-Volterra model of intraguild predation with three species is analysed, searching for the effect of the top predator on the coexistence with its prey-competitor species. Apart from the well-known result that the intraguild prey must be superior in the competition for the shared prey in order to make coexistence possible, the magnitude of intraguild predation and the form by which the intraguild predator makes use of the intraguild prey have important consequences upon the dynamics, extending or restricting the possibilities of coexistence. These results are easily obtained by nullcline analysis. Also, some interesting results are obtained for the same model but including saturating functional response.     

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

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

Invasion success in communities with reciprocal intraguild predation depends on the stage structure of the resident population

The probability of individuals being targeted as prey often decreases as they grow in size. Such size‐dependent predation risk is very common in systems with intraguild predation (IGP), i.e. when predatory species interact through predation and competition. Theory on IGP predicts that community composition depends on productivity. When recently testing this prediction using a terrestrial experimental system consisting of two phytoseiid mite species, Iphiseius degenerans as the IG‐predator and Neoseiulus cucumeris as the IG‐prey, and pollen (Typha latifolia) as the shared resource, we could not find the predicted community shift. Instead, we observed that IG‐prey excluded IG‐predators when the initial IG‐prey/IG‐predator ratio was high, whereas the opposite held when the initial ratio was low, which is also not predicted by theory. We therefore hypothesized that the existence of vulnerable and invulnerable stages in the two populations could be an important driver of the community composition. To test this, we first demonstrate that IG‐prey adults indeed attacked IG‐predator juveniles in the presence of the shared resource. Second, we show that the invasion capacity of IG‐predators at high productivity levels indeed depended on the structure of resident IG‐prey populations. Third, we further confirmed our hypothesis by mimicking successive invasion events of IG‐predators into an established population of IG‐prey at high productivity levels, which consistently failed. Our results show that the interplay between stage structure of populations and reciprocal intraguild predation is decisive at determining the species composition of communities with intraguild predation.     

Influence of predator‐specific defense adaptation on intraguild predation

The persistence of intraguild predation (IGP), the prey–predator interaction between competing species, is puzzling because simple IGP models readily predict species extinction. In this study, we explored a mathematical model incorporating predator‐specific defense adaptation of basal prey against intraguild prey and intraguild predator. The model explicitly described the dynamics of the defense effort against each predator under the assumption that anti‐predator defense was associated with reducing effort allocated to reproduction. The model predicted that defense adaptation (i.e. the ability to reallocate defense effort) would facilitate coexistence, particularly when system productivity is high; at low productivity, coexistence would be facilitated or inhibited depending on initial effort allocation prior to defense adaptation. In addition, we found that three‐species dynamics became more stable at higher adaptation rates. The results suggest that common behavioral changes, such as predator‐specific defense adaptation, have significant implications for the community structure and dynamics of IGP systems.     

Trophic supplements to intraguild predation

Intraguild predation (IGP) is a dominant community module in terrestrial food webs that occurs when multiple consumers feed both on each other and on a shared prey. This specific form of omnivory is common in terrestrial communities and is of particular interest for conservation biology and biological control given its potential to disrupt management of threatened or pest species. Extensive theory exists to describe the dynamics of three-species IGP, but these models have largely overlooked the potential for other, exterior interactions, to alter the dynamics within the IGP module. We investigated how three forms of feeding outside of the IGP module by intraguild predators (i.e. trophic supplementation) affect the dynamics of the predators (both IG predator and IG prey) and their shared resource. Specifically, we examined how the provision of a constant donor-controlled resource, the availability of an alternative prey species, and predator plant-feeding affect the dynamics of IGP models. All three forms of trophic supplements modified the basic expectations of IGP theory in two important ways, and their effects were similar. First, coexistence was possible without the IG prey being a superior competitor for the original shared resource if the IG prey could effectively exploit one of the types of trophic supplements. However, supplements to the IG predator restricted the potential for coexistence. Second, supplements to the IG prey ameliorated the disruptive effects of the IG predator on the suppression of the shared resource, promoting effective control of the resource in the presence of both predators. Consideration of these three forms of trophic supplementation, all well documented in natural communities, adds substantial realism and predictive power to intraguild predation theory.     

Size-dependent interactions inhibit coexistence in intraguild predation systems with life-history omnivory

Growth in body size during ontogeny often results in changes in diet, leading to life-history omnivory. In addition, growth is often dependent on food density. Using a physiologically structured population model, we investigated the effects of these two aspects of individual growth in a system consisting of two size-structured populations, an omnivorous top predator and an intermediate consumer. With a single shared resource for both populations, we found that life-history omnivory decreases the likelihood of coexistence between top predator and intermediate consumer in this intraguild predation (IGP) system. This result contrasts with previous unstructured models and stage-structured models without food-dependent development. Food-dependent development and size-dependent foraging abilities of the predator resulted in a positive feedback between foraging success on the shared resource at an early life stage and foraging success on the intermediate consumer later in life. By phenomenologically incorporating this feedback in an unstructured IGP model, we show that it also demotes coexistence in this simple setting, demonstrating the robustness of the negative effect of this feedback.     

The influence of vigilance on intraguild predation

Theoretical work on intraguild predation suggests that if a top predator and an intermediate predator share prey, the system will be stable only if the intermediate predator is better at exploiting the prey, and the top predator gains significantly from consuming the intermediate predator. In mammalian carnivore systems, however, there are examples of top predator species that attack intermediate predator species, but rarely or never consume the intermediate predator. We suggest that top predators attacking intermediate predators without consuming them may not only reduce competition with the intermediate predators, but may also increase the vigilance of the intermediate predators or alter the vigilance of their shared prey, and that this behavioral response may help to maintain the stability of the system. We examine two models of intraguild predation, one that incorporates prey vigilance, and a second that incorporates intermediate predator vigilance. We find that stable coexistence can occur when the top predator has a very low consumption rate on the intermediate predator, as long as the attack rate on the intermediate predator is relatively large. However, the system is stable when the top predator never consumes the intermediate predator only if the two predators share more than one prey species. If the predators do share two prey species, and those prey are vigilant, increasing top predator attack rates on the intermediate predator reduces competition with the intermediate predator and reduces vigilance by the prey, thereby leading to higher top predator densities. These results suggest that predator and prey behavior may play an important dynamical role in systems with intraguild predation.     

Aggregation, intraguild interactions and the coexistence of competitors on small ephemeral patches

It is well established that intraspecific aggregation has the potential to promote coexistence in communities of species competing for patchy ephemeral resources. We developed a simulation model to explore the influence of aggregation on coexistence in such communities when an important assumption of previous studies – that interspecific interactions have only negative effects on the species involved – is relaxed. The model describes a community of competing insect larvae in which an interaction that is equivalent to intraguild predation (IGP) can occur, and is unusual in that it considers species exploiting very small resource patches (carrying capacity=1). Model simulations show that, in the absence of any intraspecific aggregation, variation between species in the way that resource heterogeneity affects survival increases the likelihood of species coexistence. Simulations also show that intraspecific aggregation of the dominant competitor's eggs across resource patches can promote coexistence by reducing the importance of interspecific competition relative to that of intraspecific competition. Crucially, however, this effect is altered if one competitor indulges in IGP. In general, coexistence is only possible when the species that is capable of IGP is less effective at exploiting the shared resource than its competitor. Because it reduces the relative importance of interspecific interactions, intraspecific aggregation of the eggs of a species that is the victim of IGP actually reduces the likelihood of coexistence in parts of parameter space in which the persistence of the other species is dependent on its ability to exploit its competitor. Since resource heterogeneity, intraspecific aggregation and IGP are all common phenomena, these findings shed light on mechanisms that are likely to influence diversity in communities exploiting patchy resources.     

Impact of intraguild predation and stage structure on simple communities along a productivity gradient

We analyze the consequences of intraguild predation and stage structure for the possible composition of a three-species community consisting of resource, consumer, and predator. Intraguild predation, a special case of omnivory, induces two major differences with traditional linear food chain models: the potential for the occurrence of two alternative stable equilibria at intermediate levels of resource productivity and the extinction of the consumer at high productivities. At low productivities, the consumer dominates, while at intermediate productivities, the predator and the consumer can coexist. The qualitative behavior of the model is robust against addition of an invulnerable size class for the consumer population and against addition of an initial, nonpredatory stage for the predator population, which means that the addition of stage structure does not change the pattern. Unless the top predator is substantially less efficient on the bottom resource, it tends to drive the intermediate species extinct over a surprisingly large range of productivities, thus making coexistence generally impossible. These theoretical results indicate that the conditions for stable food chains involving intraguild predation cannot involve strong competition for the bottommost resource.     

Comparison of predator–prey interactions with and without intraguild predation by manipulation of the nitrogen source

Theory predicts that intraguild predation leads to different community dynamics than the trophic cascades of a linear food chain. However, experimental comparisons of these two food‐web modules are rare. Mixotrophic plankton species combine photoautotrophic and heterotrophic nutrition by grazing upon other phytoplankton species. We found that the mixotrophic chrysophyte Ochromonas can grow autotrophically on ammonium, but not on nitrate. This offered a unique opportunity to compare predator–prey interactions in the presence and absence of intraguild predation, without changing the species composition of the community. With ammonium as nitrogen source, Ochromonas can compete with its autotrophic prey for nitrogen and therefore acts as intraguild predator. With nitrate, Ochromonas acts solely as predator, and is not in competition with its prey for nitrogen. We parameterized a simple intraguild predation model based on chemostat experiments with monocultures of Ochromonas and the toxic cyanobacterium Microcystis. Subsequently, we tested the model predictions by inoculating Ochromonas into the Microcystis monocultures, and vice versa. The results showed that Microcystis was a better competitor for ammonium than Ochromonas. In agreement with theoretical predictions, Microcystis was much more strongly suppressed by intraguild predation on ammonium than by top–down predation on nitrate. Yet, Microcystis persisted at very low population densities, because the type III functional response of Ochromonas implied that the grazing pressure upon Microcystis became low when Microcystis was rare. Our results provide experimental support for intraguild predation theory, and indicate that intraguild predation may enable biological control of microbial pest species.     

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

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

Leaf domatia reduce intraguild predation among predatory mites

1. Although theory suggests that intraguild predation destabilises food webs and may result in exclusion of species, empirical observations of food webs reveal that it is a common interaction. It has been proposed that habitat structure reduces the interaction strength of intraguild predation, thus facilitating the coexistence of species. 2. This was tested using acarodomatia, tiny structures on plant leaves, and predatory mites, which usually reside in these domatia. Sweet pepper plants (Capsicum annuum L.) were used, which possess domatia consisting of tufts of hair, and coffee plants (Coffea arabica L.) with pit‐shaped domatia. 3. On sweet pepper, the predatory mites Neoseiulus cucumeris Oudemans and Iphiseius degenerans Berl. feed on each other's juveniles. Larvae of each of the species were therefore used as intraguild prey with adult females of the other species as intraguild predators. On coffee, a similar set‐up was used, with larvae and adult females of Amblyseius herbicolus Chant and Iphiseiodes zuluagai Denmark & Muma as intraguild prey and intraguild predators, respectively. 4. Domatia on detached, isolated sweet pepper and coffee leaves were either closed with glue or left open, after which larvae and adult predators were released. As a control, larvae were released on leaves with open or closed domatia without an adult predator. 5. Survival of larvae was high in the absence of the adult (intraguild) predator. In the presence of the intraguild predator, survival was significantly higher on leaves with open domatia than on leaves with closed domatia. 6. This shows that even such tiny structures as plant domatia may significantly affect the interaction strength of intraguild predation.     

Productivity, dispersal and the coexistence of intraguild predators and prey

A great deal is known about the influence of dispersal on species that interact via competition or predation, but very little is known about the influence of dispersal on species that interact via both competition and predation. Here, I investigate the influence of dispersal on the coexistence and abundance-productivity relationships of species that engage in intraguild predation (IGP: competing species that prey on each other). I report two key findings. First, dispersal enhances coexistence when a trade-off between resource competition and IGP is strong and/or when the Intraguild Prey has an overall advantage, and impedes coexistence when the trade-off is weak and/or when the Intraguild Predator has an overall advantage. Second, the Intraguild Prey's abundance-productivity relationship depends crucially on the dispersal rate of the Intraguild Predator, but the Intraguild Predator's abundance-productivity relationship is unaffected by its own dispersal rate or that of the Intraguild Prey. This difference arises because the two species engage in both a competitive interaction as well as an antagonistic (predator-prey) interaction. The Intraguild Prey, being the intermediate consumer, has to balance the conflicting demands of resource acquisition and predator avoidance, while the Intraguild Predator has to contend only with resource acquisition. Thus, the Intraguild Predator's abundance increases monotonically with resource productivity regardless of either species' dispersal rate, while the Intraguild Prey's abundance-productivity relationship can increase, decrease, or become hump-shaped with increasing productivity depending on the Intraguild Predator's dispersal rate. The important implication is that a species' trophic position determines the effectiveness of dispersal in sampling spatial environmental heterogeneity. The dispersal behavior of a top predator is likely to have a stronger effect on coexistence and spatial patterns of abundance than the dispersal behavior of an intermediate consumer.     

A growth/mortality trade-off in larval salamanders and the coexistence of intraguild predators and prey

Behavioral and morphological traits often influence a key trade-off between resource acquisition and vulnerability to predation, and understanding trait differences between species can provide critical insight into their interactions with other species and their distributions. Such an approach should enhance our understanding of the criteria for coexistence between species that can interact through both competition and predation (i.e. intraguild predators and prey). I conducted a common garden experiment that revealed strong differences between three guild members (larval salamanders Ambystoma laterale, A. maculatum, and A. tigrinum) in behavior, morphology, and growth in the presence and absence of a shared top predator (the larval dragonfly Anax longipes). All three species also reduced their activity and modified their tail fin depth, tail muscle length, and body length in response to non-lethal Anax. Species that act as intraguild predators were more active and could grow faster than their intraguild prey species, but they also suffered higher mortality in laboratory predation trials with Anax. I also used survey data from natural communities to compare the distribution of Ambystoma species between ponds differing in abiotic characteristics and predatory invertebrate assemblages. An intraguild prey species (A. maculatum) was found more reliably, occurred at higher densities, and was more likely to persist late into the larval period in ponds with more diverse invertebrate predator assemblages. Taken together, these results indicate that top predators such as Anax may play an important role in influencing intraguild interactions among Ambystoma and ultimately their local distribution patterns.     

Predator diversity and the functioning of ecosystems: the role of intraguild predation in dampening trophic cascades

Single trophic‐level studies of the relationship between biodiversity and ecosystem functioning highlight the importance of mechanisms such as resource partitioning, facilitation, and sampling effect. In a multi‐trophic context, trophic interactions such as intraguild predation may also be an important mediator of this relationship. Using a salt‐marsh food web, we investigated the interactive effects of predator species richness (one to three species) and trophic composition (strict predators, intraguild predators, or a mixture of the two) on ecosystem functions such as prey suppression and primary production via trophic cascades. We found that the trophic composition of the predator assemblage determined the impact of increasing predator species richness on the occurrence of trophic cascades. In addition, increasing the proportion of intraguild predator species present diminished herbivore suppression and reduced primary productivity. Therefore, trophic composition of the predator assemblage can play an important role in determining the nature of the relationship between predator diversity and ecosystem function.     

Effects of productivity, disturbance, and ecosystem size on food-chain length: insights from a metacommunity model of intraguild predation

Traditionally, productivity and disturbance have been hypothesized as important determinants of food-chain length. More recently, growing empirical evidence suggests a strong role of ecosystem size. To theoretically explore the effects of basal productivity, disturbance, and ecosystem size on food-chain length, we develop and analyze a metacommunity model of intraguild predation (IGP). The model finds that, when local IGP is weak, increasing basal productivity, weakening disturbance, and increasing ecosystem size will generally increase food-chain length. When local IGP is strong, by contrast, increasing basal productivity or weakening disturbance favors intraguild predators and hinders the coexistence of intraguild predators and intraguild prey, limiting food-chain length. In contrast, increasing ecosystem size can promote coexistence even when local IGP is strong, increasing food-chain length through inserting intraguild prey and changing the degree of omnivory by intraguild predators. Intraguild prey needs to be the superior colonizer to intraguild predators for this to occur. We discuss that these theoretical predictions appear consistent with empirical patterns.