Intraguild Prey Research Articles

Adaptive and variable intraguild predators facilitate local coexistence in an intraguild predation module

BackgroundIntraguild predation (IGP) is common in nature, but its ecological role is still illusive. A number of studies have investigated a three species IGP module that consists of an intraguild predator, intraguild prey, and resource species in which the intraguild predator and the intraguild prey exploitatively compete for the resource while the intraguild predator also consumes the intraguild prey. A common prediction of models of the IGP module is that the coexistence of the species is difficult, which is considered inconsistent to the ubiquity of IGP in nature. This study revisits the IGP module and provides an alternative coexistence mechanism by focusing on a commonly used analysis method (i.e., invasion analysis) in light of individual variation in adaptive behavior.ResultsInvasion analysis underestimates the possibility of coexistence regardless of the presence or absence of adaptive behavior. Coexistence is possible even when invasion analysis predicts otherwise. The underestimation by invasion analysis is pronounced when the intraguild predator forages adaptively, which is even further pronounced when the expression of foraging behavior is variable among intraguild predators.ConclusionsThe possibility of coexistence in the IGP module is greater than previously thought, which may have been partly due to how models were analyzed. Inconsistent conclusions may result from the same model depending on how the model is analyzed. Individual variation in adaptive behavior can be an important factor promoting the coexistence of species in IGP modules.

Direct and indirect top-down effects of previous contact with an enemy on the feeding behavior of blowfly larvae

We investigated the addition of a trophic level to a simple food web. Direct and indirect effects caused by the presence of a new species in the food web were quantified by estimating survival and consumption rates on the basal resource. We focused on a blowfly intraguild prey–predator system with various ecological interactions taking place during the larval period. The experiments were designed to set Chrysomya megacephala (Fabricius) (Diptera: Calliphoridae) as the intraguild prey and Chrysomya albiceps (Wiedemann) as the intraguild predator and/or cannibal. The generalist pupal parasitoid Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae) was introduced into the system during a non-susceptible life stage of the interacting blowfly species. The cascading parasitoid effects induced behavioral changes in the blowfly larvae, increasing the impact of intraguild predation and cannibalism on blowfly survival. The results suggest that blowfly larvae can change their feeding behavior in response to the presence of a parasitoid.

Adaptive behaviour, tri-trophic food-web stability and damping of chaos

We examine the effect of adaptive foraging behaviour within a tri-trophic food web with intra-guild predation. The intra-guild prey is allowed to adjust its foraging effort so as to achieve an optimal per capita growth rate in the face of realized feeding, predation risk and foraging cost. Adaptive fitness-seeking behaviour of the intra-guild prey has a stabilizing effect on the tri-trophic food-web dynamics provided that (i) a finite optimal foraging effort exists and (ii) the trophic transfer efficiency from resource to predator via the intra-guild prey is greater than that from the resource directly. The latter condition is a general criterion for the feasibility of intra-guild predation as a trophic mode. Under these conditions, we demonstrate rigorously that adaptive behaviour will always promote stability of community dynamics in the sense that the region of parameter space in which stability is achieved is larger than for the non-adaptive counterpart of the system.

Mixed competition–predation: potential vs. realized interactions

1. Life-history omnivory or size-induced mixed competition-predation systems have under many conditions theoretically been shown to be fragile, whereas at the same time existing empirical data suggest such systems to be common in nature. 2. In a whole lake experiment covering 17 years, we analysed the effects of the introduction of the intraguild prey roach (Rutilus rutilus) on the population size and individual performance of the intraguild predator perch (Perca fluviatilis) and on resource levels in two low productivity systems. 3. A strong long-term effect of roach on the zooplankton resource but not on the macroinvertebrate resource was present. Competitive effects of roach on perch were observed in one of the lakes the first years after the introduction, but at the end of the study no competitive effect of roach on either size class of perch was observed in any of the two lakes. In contrast, a positive predatory effect reflected in improved growth rates of older perch was present. 4. The lack of a support for a competitive effect of roach on small perch raises the question of the importance of mixed competition-predation interactions in life-history omnivorous systems and the problem of comparing descriptive data on feeding relationships with theoretical predictions based on interaction modules.

BIOLOGICAL CONTROL OF APHIDS BY THE PREDATORY MIDGE APHIDOLETES APHIDIMYZA IN THE PRESENCE OF INTRAGUILD PREDATORY BUGS AND THRIPS

BIOLOGICAL CONTROL OF APHIDS BY THE PREDATORY MIDGE APHIDOLETES APHIDIMYZA IN THE PRESENCE OF INTRAGUILD PREDATORY BUGS AND THRIPS

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.

Effects of habitat complexity, prey type, and abundance on intraguild predation between larval odonates

Intraguild predation is an important interaction in which predators feed on a shared prey as well as on each other. It occurs frequently between larval odonates in freshwater lentic communities, and understanding the factors influencing this interaction remains an important objective. An experiment carried out in mesocosms and utilizing a factorial design investigated the strength of intraguild interactions between the dragonfly, Sympetrum vicinum, and the damselfly, Enallagma civile, under two levels each of habitat complexity (high or low), prey abundance (high or low) and prey type (amphipods or blackworms). Effects of treatments on size, mortality and emergence of larval odonates were evaluated. Shared prey abundance had little impact on intraguild interactions, affecting only the mass of the intraguild prey E. civile. Habitat complexity affected the size of E. civile damselflies, as length and wet mass were significantly greater in low complexity mesocosms. Prey type seemed to be the most important factor in the experiment, influencing all response variables measured. When shared prey consisted of larger, more active blackworms, intraguild predation decreased, and E. civile damselflies experienced lower mortality, achieved greater length and mass, and had greater emergence success. Results of this study suggest that prey type and habitat complexity can be more important than prey abundance in mediating intraguild predation.

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.

Influence of extraguild prey density on intraguild predation by heteropteran predators: A review of the evidence and a case study

Heteropteran predators constitute an important component of predatory guilds in terrestrial and aquatic ecosystems. Most heteropteran species have generalist diets, and intraguild predation has been documented in most heteropteran families. Zoophytophagous species also frequently engage in intraguild interactions. An increase in extraguild prey density is often predicted to reduce intraguild predation between guild members by providing abundant alternate prey. However, an increase of extraguild prey density may also be associated with an increase in the density of intraguild predators, which could instead strengthen intraguild predation. Evaluating the combined effect of these potentially opposing influences on intraguild predation is difficult. Most studies have been carried out in the laboratory, using artificially simplified communities of predators and prey and employing spatial and temporal scales that may not reflect field conditions. We review experimental studies examining how extraguild prey density influences the intensity of intraguild predation and then report an observational case study examining the influence of extraguild prey density on the intensity of intraguild predation at larger spatial and temporal scales in unmanipulated cotton fields. Fields with more abundant extraguild prey (aphids, mites) were not associated with elevated densities of intraguild predators, and were strongly associated with increased survival of intraguild prey (lacewing larvae). In this system, the ability of extraguild prey to relax the intensity of intraguild predation, as previously documented in small-scale field experiments, also extends to the larger spatial and temporal scales of commercial agriculture.

Diet-dependent intraguild predation between the predatory mites Neoseiulus californicus and Neoseiulus cucumeris

Based on the hypothesis that matching diets of intraguild (IG) predator and prey indicate strong food competition and thus intensify intraguild predation (IGP) as compared to non-matching diets, we scrutinized diet-dependent mutual IGP between the predatory mites Neoseiulus cucumeris and N. californicus. Both are natural enemies of herbivorous mites and insects and used in biological control of spider mites and thrips in various agricultural crops. Both are generalist predators that may also feed on plant-derived substances such as pollen. Irrespective of diet (pollen or spider mites), N. cucumeris females had higher predation and oviposition rates and shorter attack latencies on IG prey than N. californicus. Predation rates on larvae were unaffected by diet but larvae from pollen-fed mothers were a more profitable prey than those from spider-mite fed mothers resulting in higher oviposition rates of IG predator females. Pollen-fed protonymphs were earlier attacked by IG predator females than spider-mite fed protonymphs. Spider mite-fed N. californicus females attacked protonymphs earlier than did pollen-fed N. californicus females. Overall, our study suggests that predator and prey diet may exert subtle influences on mutual IGP between bio-control agents. Matching diets did not intensify IGP between N. californicus and N. cucumeris but predator and prey diets proximately influenced IGP through changes in behaviour and/or stoichiometry.

Role of intraguild predation in aphidophagous guilds

AbstractThe concept of intraguild predation (IGP) appeared in 1987–1989 to describe trophic interactions within a guild of arthropods inhabiting a sand dune desert: consumers B prey on consumers A and both of them prey on a common resource. Theory predicts that the two types of consumers should only coexist if consumer A is more efficient in the conversion of the common resource than B. As a consequence, this resource is more abundant in the presence than in the absence of intraguild predators. Such a theoretical prediction probably explains the vivid interest shown by ecologists involved in biological control for IGP. It is therefore not surprising that many papers report on IGP among natural enemies of aphids. A close examination of these reported cases indicates that they rarely fulfil the theoretical requirements for IGP. That is, guilds of aphidophagous insects are rarely the theatre of IGP but frequently of interspecific predation. This is confirmed by experimental assessment of the cost of attacking and eating intraguild prey instead of extraguild in ladybird beetles.

Coexistence in streams: do source–sink dynamics allow salamanders to persist with fish predators?

Theory suggests that source-sink dynamics can allow coexistence of intraguild predators and prey, but empirical evidence for this coexistence mechanism is limited. We used capture-mark-recapture, genetic methods, and stable isotopes to test whether source-sink dynamics promote coexistence between stream fishes, the intraguild predator, and stream salamanders (Dicamptodon aterrimus), the intraguild prey. Salamander populations from upstream reaches without fish were predicted to maintain or supplement sink populations in downstream reaches with fish. We found instead that downstream reaches with fish were not sinks even though fish consumed salamander larvae-apparent survival, recruitment, and population growth rate did not differ between upstream and downstream reaches. There was also no difference between upstream and downstream reaches in net emigration. We did find that D. aterrimus moved frequently along streams, but believe that this is a response to seasonal habitat changes rather than intraguild predation. Our study provides empirical evidence that local-scale mechanisms are more important than dispersal dynamics to coexistence of streams salamanders and fish. More broadly, it shows the value of empirical data on dispersal and gene flow for distinguishing between local and spatial mechanisms of coexistence.

Which prey sustains cold-adapted invertebrate generalist predators in arable land? Examining prey choices by molecular gut-content analysis

Summary 1. Generalist predators such as carabid and cantharid beetles form an important component within natural enemy communities in arable land. Usually, predator–prey interactions are examined during the vegetation period, largely ignoring food web interactions occurring in the cold season. This is, however, when the larval stages of many polyphagous beetles develop whose survival critically depends on the availability of suitable prey. 2. In this study, we examined intra- and extraguild feeding links in larval Cantharis spp. (Coleoptera: Cantharidae) and Nebria brevicollis (Coleoptera: Carabidae), both abundant cold-adapted invertebrate predators in European arable land. As these immature beetles are fluid feeders, which impedes a microscopic analysis of their gut content, multiplex polymerase chain reaction assays were developed to examine trophic linkages in the field. 3. Collembolan DNA was detected in 49% and 54% of cantharid and carabid larvae, respectively. Earthworms were consumed by 34% of cantharid and 24% of carabid larvae. Significant differences in lumbricid and collembolan prey detection rates occurred between sampling dates in Cantharis spp. and N. brevicollis larvae, respectively, suggesting that these predators utilized different feeding strategies. In both predator taxa, however, only few individuals (0·2–1%) tested positive for DNA of intraguild prey, indicating that predator–predator trophic interactions were scarce in this community. 4. Synthesis and applications. We present conclusive evidence that cold-adapted predatory beetle larvae are strongly linked to the detrital food chain by feeding on collembolans and earthworms. By improving the habitat conditions for detritivores in arable land by mulching, compost applications, or provision of plant cover during winter, their densities can be increased easily. Applying these measures year round will retain and sustain predatory beetles during their whole life cycle in arable land. Ultimately, we expect that these measures will enhance the ability of polyphagous beetle predators to provide their fundamental ecosystem service as regulators of agricultural pests.

Alkaloids provide evidence of intraguild predation on native coccinellids by Harmonia axyridis in the field

Over a period of less than 5 years, Belgium was thoroughly invaded by the multicolored Asian coccinellid, Harmonia axyridis. At the same time, a decline of some native coccinellid species was observed in tree habitats. One hypothesis about the cause of this decline was that it might have been due to intraguild predation (IGP) by H. axyridis. In natural conditions, IGP between coccinellids can be tracked by using defensive compounds. Exogenous alkaloids in H. axyridis were therefore examined by gas chromatography-mass spectrometry (GC–MS), using individuals sampled from lime trees that were also occupied by other species of coccinellids. Harmonia axyridis was the dominant species at all life stages, in terms of both numbers of sites occupied and local abundance. The GC–MS analysis of H. axyridis larvae revealed traces of exogenous alkaloids from 19 of the 20 sites and, in nine of those 19 sites, more than 30% of the larvae analyzed contained exogenous alkaloids. Three alkaloids were detected: adaline from Adalia spp., calvine from Calvia spp. and propyleine from Propylea quatuordecimpunctata. Predation by H. axyridis on two different coccinellid species was also detected in the same larva, reinforcing the status of H. axyridis as a top predator. A generalized linear model indicated that IGP frequency was positively influenced by two variables: the abundance of extraguild and intraguild prey; and the interaction between these two variables. Our results therefore support the hypothesis that IGP by H. axyridis on native coccinellids in tree habitats has led to the decline of several of these species.

Prey-mediated avoidance of an intraguild predator by its intraguild prey

Intraguild (IG) predation is an important factor influencing community structure, yet factors allowing coexistence of IG predator and IG prey are not well understood. The existence of spatial refuges for IG prey has recently been noted for their importance in allowing coexistence. However, reduction in basal prey availability might lead IG prey to leave spatial refuges for greater access to prey, leading to increased IG predation and fewer opportunities for coexistence. We determined how the availability of prey affected space-use patterns of bobcats (Lynx rufus, IG prey) in relation to coyote space-use patterns (Canis latrans, IG predators). We located animals from fall 2007 to spring 2009 and estimated bobcat home ranges and core areas seasonally. For each bobcat relocation, we determined intensity of coyote use, distance to water, small mammal biomass, and mean small mammal biomass of the home range during the season the location was collected. We built generalized linear mixed models and used Akaike Information Criteria to determine which factors best predicted bobcat space use. Coyote intensity was a primary determinant of bobcat core area location. In bobcat home ranges with abundant prey, core areas occurred where coyote use was low, but shifted to areas intensively used by coyotes when prey declined. High spatial variability in basal prey abundance allowed some bobcats to avoid coyotes while at the same time others were forced into more risky areas. Our results suggest that multiple behavioral strategies associated with spatial variation in basal prey abundance likely allow IG prey and IG predators to coexist.

Stronger inducible defences enhance persistence of intraguild prey

1. Intraguild predation is widespread in nature despite its potentially destabilizing effect on food web dynamics. 2. Anti-predator inducible defences affect both birth and death rates of populations and have the potential to substantially modify food web dynamics and possibly increase persistence of intraguild prey. 3. In a chemostat experiment, we investigated the long-term effects of inducible defences on the dynamics of aquatic microbial food webs consisting of an intraguild predator, intraguild prey, and a basal resource. We controlled environmental conditions and selected strains of intraguild prey that varied in the strength of expressed inducible defences. 4. We found that intraguild prey with a stronger tendency to induce an anti-predator morphology persist for significantly longer periods of time. In addition, model selection analysis implied that flexibility in defensive phenotype (inducibility itself) is most likely the factor responsible for the enhanced persistence. 5. As patterns at the community level often emerge as a result of the life-history traits of individuals, we propose that inducible defences increase the persistence of populations and may contribute to the widespread occurrence of theoretically unstable intraguild predation systems in nature.

Size-structured cannibalism between top predators promotes the survival of intermediate predators in an intraguild predation system

Individuals in most natural populations of predators vary in size, and size differences among individuals often result in cannibalism. Cannibalism is an extremely common phenomenon in the animal kingdom, particularly among generalist predators that engage in intraguild predation (IGP). However, few studies have specifically addressed the effects of cannibalism on IGP. The aim of my study was to investigate how trophic and behavioral interactions between 2 size classes of an intraguild (IG) predator influenced the survival and behavior of IG prey and a shared prey resource. I tested for these effects with larval odonates by exposing a shared prey resource (Ischnura verticalis) to the presence or absence of IG prey (Pachydiplax longipennis) and 2 size classes of IG predators (small or large Anax junius) in a 2 × 2 × 2 factorial design. Mortality rates of the shared resource in all single-predator treatments were significantly greater than in nonpredator controls, and risk reduction was observed when the shared resource was exposed to combinations of predators. The significant negative effect of large A. junius on P. longipennis survival and activity level was greater than that of small A. junius. Cannibalism occurred between large and small A. junius in size-structured IG predator treatments, and the effects of the size classes were not additive for the survival of IG prey. Cannibalism was not solely responsible for risk reduction in IG prey, and reduced activity level of small A. junius in the presence of larger conspecifics probably had a positive influence on P. longipennis survival. My results demonstrate that cannibalism among IG predators can influence the survival of IG prey and might contribute to coexistence among predators in systems with strong IGP.

Cues of intraguild predators affect the distribution of intraguild prey.

Theory on intraguild (IG) predation predicts that coexistence of IG-predators and IG-prey is only possible for a limited set of parameter values, suggesting that IG-predation would not be common in nature. This is in conflict with the observation that IG-predation occurs in many natural systems. One possible explanation for this difference might be antipredator behaviour of the IG-prey, resulting in decreased strength of IG-predation. We studied the distribution of an IG-prey, the predatory mite Neoseiulus cucumeris (Acari: Phytoseiidae), in response to cues of its IG-predator, the predatory mite Iphiseius degenerans. Shortly after release, the majority of IG-prey was found on the patch without cues of IG-predators, suggesting that they can rapidly assess predation risk. IG-prey also avoided patches where conspecific juveniles had been killed by IG-predators. Because it is well known that antipredator behaviour in prey is affected by the diet of the predator, we also tested whether IG-prey change their distribution in response to the food of the IG-predators (pollen or conspecific juveniles), but found no evidence for this. The IG-prey laid fewer eggs on patches with cues of IG-predators than on patches without cues. Hence, IG-prey changed their distribution and oviposition in response to cues of IG-predators. This might weaken the strength of IG-predation, possibly providing more opportunities for IG-prey and IG-predators to co-exist.

Prey persistence and abundance in systems with intraguild predation and type-2 functional responses

The apparent prevalence of intraguild predation in productive environments has been regarded as puzzling because some simple models suggest that the intraguild prey species is often either reduced in abundance or driven extinct at high resource productivity. While various theoretical mechanisms that avoid this prediction have been uncovered, they have often been viewed as being narrowly applicable. This article examines the fate of the intraguild prey in models in which consumer species may have type-2 functional responses; these are usually characterized by sustained fluctuations in population density at high enough resource productivities. The models also include adaptive, but imperfect diet choice by the top predator. We concentrate on two situations: (1) the prey exhibits less saturation in its functional response to the resource than does the predator and (2) the predator is unable to persist on the basal resource alone. The reasons given by previous studies for discounting these cases are re-examined. The present analysis shows that prey abundance often increases with increasing productivity in both cases, as does the range of prey parameters that allows prey persistence. It is also possible for the prey to coexist with the predator in spite of having a larger equilibrium requirement for the resource. Different assumptions about the dynamics of diet choice can have a large impact on population responses to enrichment. We argue that the persistence and/or increase in abundance of intraguild prey at higher productivity should not be regarded as puzzling because observations are consistent with a range of theoretical models that reflect commonly observed mechanisms.

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.