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.     

Role of intraguild predation in aphidophagous guilds

The 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.     

Detecting arthropod intraguild predation in the field

The process of biological control carries a distinct risk that an alien biological control agent (BCA) will become established as an invasive alien species with an associated threat to the local ecosystem biodiversity. It is imperative that a wide-ranging environmental risk assessment (ERA) is performed before the release of any BCA. This should include considering various potential but difficult to observe ecological interactions between the BCA and members of the native community, including disruption of intraguild relationships. Detection of intraguild predation (IGP) events involving predatory arthropods in the field can be done by analyzing their gut contents. Polymerase chain reaction (PCR) is a sensitive and specific tool to identify target prey DNA within a predator’s gut. This paper reviews the efficiency of a DNA based approach for detecting IGP in the field, compared with detection by the use of monoclonal antibodies or gas chromatography. Prey specificity, detection times after prey consumption, capacity for quantification, multiple prey targeting and the time and costs involved in developing and using the different methods are considered.     

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.     

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.     

Density-dependent intraguild predation of an aphid parasitoid

A growing body of research has examined the effect of shared resource density on intraguild predation (IGP) over relatively short time frames. Most of this work has led to the conclusion that when the shared resource density is high, the strength of IGP should be lower, due to prey dilution. However, experiments addressing this topic have been done using micro- or mesocosms that excluded the possibility of intraguild predator aggregation. We examined the effect of shared resource density on IGP of an aphid parasitoid in an open field setting where the effects of prey dilution and predator aggregation could occur simultaneously. We brought potted soybean plants with 2, 20, or 200 soybean aphids (Aphis glycines) and 20 pupae (‘mummies’) of the soybean aphid parasitoid Binodoxys communis into soybean fields in Minnesota, USA. We monitored predator aggregation onto the potted plants, predation of parasitoid mummies, and successful adult emergence of B. communis. We found that predator aggregation was higher at the higher aphid densities on our experimental plants and that this coincided with lower adult emergence of B. communis, indicating that even if a prey dilution effect occurred in our study, it was overcome by short-term predator aggregation. Our results suggest that the effect of shared resource density on IGP may be more nuanced in a field setting than in microcosms due to predator aggregation.     

Alternative stable states in communities with intraguild predation

Intraguild predation (IGP) is a widespread ecological phenomenon in which two consumers that share a resource also engage in a predator-prey interaction. Theory on IGP predicts the occurrence of alternative stable states, but empirical evidence of such states is scarce. This raises the question of whether alternative states are a rare phenomenon that is unlikely to be observed in nature. Here we analyze a model in which the resource exhibits logistic or chemostat dynamics and consumers have saturating (Type II) functional responses. We show that alternative states can arise for a wide range of biological scenarios and that environmental constraints can make their detection difficult. Our analysis identifies three possible combinations of alternative states: (i) IG prey or IG predator, (ii) coexistence or IG predator, and (iii) coexistence or IG prey. Bifurcation diagrams reveal that alternative states are possible over large regions of the parameter space. However, they can be limited to narrow ranges along the resource productivity axis, which may make it difficult to observe the occurrence of alternative states in communities with IGP. Microcosm experiments provide a promising avenue for detecting combinations of asymptotically stable states along a productivity gradient.     

寄生对集团内捕食系统中物种入侵的影响

寄生已被证明是影响生物入侵动态的关键因素,可通过直接或间接作用影响物种间相互作用。基于元胞自动机模型,探讨了寄生感染对宿主种群的间接作用(寄生对宿主的密度调节和特征调节效应)在外来种入侵动态中的作用。结果显示,寄生对宿主的3种调节效应均对外来种的入侵起到了抑制作用;同时,相对于密度调节效应,寄生的特征调节对捕食者种群入侵的抑制作用更明显,而两者的耦合调节效应对入侵的抑制能力明显高于单种效应的作用。综上,该研究在一定意义上丰富和发展了生物入侵的理论,为生物入侵的有效控制提供了理论参考。     

Effects of intraguild predation on aphid parasitoid survival

To assess the potential selection pressure caused by intraguild predation between predators and parasitoids of aphids an estimate was made of the predation risk to Aphis fabaeScop. mummified by Lysiphlebus fabarum(Marshall, 1896) on sugar beet. Mummified aphids were exposed to a natural community of predators. Their survival time was estimated during a 10-day field survey. Additionallythe role of alternative prey on parasitoid survival was investigated by adding unparasitised aphids to half of the mummy aggregations.The field data were evaluated by survival analysis. Two covariates were tested within a Cox proportional hazard model: (i) the presence of the alternative prey and (ii) the patch structure (number of proximal mummies attacked). Within 4–5 days after exposure predators destroyed approx. 50% of the mummies. The model with both covariates revealed a significant difference concerning survival of the mummies in the two treatments (Likelihood ratio test, ²=78.03, P=0.0001). Alternative prey reduced the predation risk on mummies by 29%, while a high level of predation on proximal mummies increased the individual predation risk by 4%. The results are discussed in the context of prey location by predators and the evolution of anti-predator mechanisms.     

Impact of intraguild predation on parasitoid foraging behaviour

1. Trophic interactions between predators and parasitoids can be described as intraguild predation (IGP) and are often asymmetric. Parasitoids (typically the IG prey) may respond to the threat of IGP by mitigating the predation risk for their offspring. 2. We used a system with a facultative predator Macrolophus caliginosus, the parasitoid Aphidius colemani, and their shared prey, the aphid Myzus persicae. We examined the functional responses of the parasitoid in the presence/absence of the predator on two host plants (aubergine and sweet pepper) with differing IGP risk. 3. Estimated model parameters such as parasitoid handling time increased on both plants where the predator was present, but impact of the predator varied with plant species. The predator, which could feed herbivorously on aubergine, had a reduced impact on parasitoid foraging on that plant. IG predator presence could reduce the searching effort of the IG prey depending on the plant, and on likely predation risk. 4. The results are discussed with regard to individual parasitoid's foraging behaviour and population stability; it is suggested that the presence of the predator can contribute to the stabilisation of host–parasitoid dynamics     

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.     

The ubiquity of intraguild predation among predatory arthropods

Intraguild predation (IGP) occurs when one predator species attacks another predator species with which it competes for a shared prey species. Despite the apparent omnipresence of intraguild interactions in natural and managed ecosystems, very few studies have quantified rates of IGP in various taxa under field conditions. We used molecular analyses of gut contents to assess the nature and incidence of IGP among four species of coccinellid predators in soybean fields. Over half of the 368 predator individuals collected in soybean contained the DNA of other coccinellid species indicating that IGP was very common at our field site. Furthermore, 13.2% of the sampled individuals contained two and even three other coccinellid species in their gut. The interaction was reciprocal, as each of the four coccinellid species has the capacity to feed on the others. To our knowledge, this study represents the most convincing field evidence of a high prevalence of IGP among predatory arthropods. The finding has important implications for conservation biology and biological control.     

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.     

Leaf pubescence mediates intraguild predation between predatory mites

Plant morphological traits such as leaf pubescence may affect herbivores and their natural enemies at the individual, population and community levels. Leaf pubescence has been repeatedly shown to mediate predator‐herbivore interactions whereas the influence of leaf pubescence on predator–predator interactions such as intraguild predation (IGP) has seldom been investigated. Using a three‐pronged approach we assessed the influence of leaf pubescence on the predatory mites Kampimodromus aberrans and Euseius finlandicus. Both predators occur on broad‐leaved trees in Europe. Euseius finlandicus is mostly found on trees with glabrous leaves whereas K. aberrans mainly occurs on trees with pubescent leaves. We hypothesized that leaf pubescence mediates IGP between K. aberrans and E. finlandicus and thereby determines their dominance and proportional abundance. A field survey on apple revealed that the abundance of K. aberrans and E. finlandicus is negatively correlated, with the former predominating on cultivars with strongly pubescent leaves and the latter predominating on cultivars with little pubescent or glabrous leaves. Microhabitat choice tests showed that K. aberrans preferentially resides on pubescent leaves whereas E. finlandicus preferentially resides on glabrous leaves. The effects of leaf pubescence on survival and development of immature IG predators and IG prey were reversed for K. aberrans and E. finlandicus. In the presence of the IG predator E. finlandicus, immature K. aberrans had higher survival probabilities on pubescent leaves than on glabrous ones. In contrast, the survival chances of immature E. finlandicus were higher on glabrous leaves than on pubescent ones when the IG predator K. aberrans was present. Artificial leaf pubescence enhanced IG prey capture by immature K. aberrans and prolonged their longevity but impaired IG prey capture by immature E. finlandicus and shortened their longevity. We conclude that leaf pubescence mediates IGP strength and symmetry and discuss the implications to natural and biological control.     

Competition and intraguild predation among three sympatric carnivores

We examined the relative roles of dominance in agonistic interactions and energetic constraints related to body size in determining local abundances of coyotes (Canis latrans, 8-20 kg), gray foxes (Urocyon cinereoargenteus, 3-5 kg) and bobcats (Felis rufus, 5-15 kg) at three study sites (hereafter referred to as NP, CP, and SP) in the Santa Monica Mountains of California. We hypothesized that the largest and behaviorally dominant species, the coyote, would exploit a wider range of resources (i.e., a higher number of habitat and/or food types) and, consequently, would occur in higher density than the other two carnivores. We evaluated our hypotheses by quantifying their diets, food overlap, habitat-specific abundances, as well as their overall relative abundance at the three study sites. We identified behavioral dominance of coyotes over foxes and bobcats in Santa Monica because 7 of 12 recorded gray fox deaths and 2 of 5 recorded bobcat deaths were due to coyote predation, and no coyotes died as a result of their interactions with bobcats or foxes. Coyotes and bobcats were present in a variety of habitats types (8 out of 9), including both open and brushy habitats, whereas gray foxes were chiefly restricted to brushy habitats. There was a negative relationship between the abundances of coyotes and gray foxes (P=0.020) across habitats, suggesting that foxes avoided habitats of high coyote predation risk. Coyote abundance was low in NP, high in CP, and intermediate in SP. Bobcat abundance changed little across study sites, and gray foxes were very abundant in NP, absent in CP, and scarce in SP; this suggests a negative relationship between coyote and fox abundances across study sites, as well. Bobcats were solely carnivorous, relying on small mammals (lagomorphs and rodents) throughout the year and at all three sites. Coyotes and gray foxes also relied on small mammals year-round at all sites, though they also ate significant amounts of fruit. Though there were strong overall interspecific differences in food habits of carnivores (P<0.0001), average seasonal food overlaps were high due to the importance of small mammals in all carnivore diets [bobcat-gray fox: 0.79ǂ.09 (SD), n=4; bobcat-coyote: 0.69ǂ.16, n=6; coyote-gray fox: 0.52ǂ.05, n=4]. As hypothesized, coyotes used more food types and more habitat types than did bobcats and gray foxes and, overall, coyotes were the most abundant of the three species and ranged more widely than did gray foxes. We propose that coyotes limit the number and distribution of gray foxes in Santa Monica Mountains, and that those two carnivores exemplified a case in which the relationship between their body size and local abundance is governed by competitive dominance of the largest species rather than by energetic equivalences. However, in the case of the intermediate-sized bobcat no such a pattern emerged, likely due to rarity or inconsistency of agonistic interactions and/or behavioral avoidance of encounters by subordinate species.     

Coincidental intraguild predation by caterpillars on spider mites

Intraguild predation (IGP) is defined as the killing and eating of prey species by a predator that also can utilize the resources of the prey. It is mainly reported among carnivores that share common herbivorous prey. However, a large chewing herbivore could prey upon sedentary and/or micro herbivores in addition to utilizing a host plant. To investigate such coincidental IGP, we observed the behavioral responses of the polyphagous mite Tetranychus kanzawai Kishida (Acari: Tetranychidae) when its host plant Cayratia japonica (Thunb.) Gagnep. (Vitaceae) was attacked by hornworms, Theretra japonica Boisduval (Sphingidae) and T. oldenlandiae Fabricius (Sphingidae). We also examined an interaction between the oligophagous mite Panonychus citri McGregor (Acari: Tetranychidae) and caterpillars of the swallowtail Papilio xuthus L. (Papilionidae) that share citrus plants as their main food source. Although all T. kanzawai and some active stage P. citri tried to escape from the coincidental IGP, some were consumed together with eggs, quiescent mites, and host plant leaves, suggesting that coincidental IGP occurs on spider mites in the wild. Moreover, neither hornworms nor swallowtail caterpillars distinguished between spider mite-infested and uninfested leaves, suggesting that the mite-infested leaves do not discourage caterpillar feeding. The reasons that the mites have no effective defense against coincidental IGP other than escaping are discussed.     

Multi-trophic effects of ungulate intraguild predation on acorn weevils

Predators and parasitoids may contribute to controlling the population sizes of phytophagous insects, and this has been shown to benefit plants. Phytophagous insects may also be killed by other herbivores (intraguild predation), usually larger-sized vertebrates that ingest insects accidentally while feeding on common food sources. We studied the intraguild predation on acorn weevils by ungulates and assessed the consequences for weevil populations. Infested acorns are prematurely abscised and the weevil larvae finish their development inside the acorns after being dropped. Our results show that weevil larvae were killed by ungulates eating the infested acorns on the ground. Ungulates did not discriminate between infested and sound acorns, and the probability of a larva being incidentally eaten was inversely related to acorn availability. Thus, predation risk was enhanced by the premature drop of infested acorns when acorn availability on the ground was low. Predation rates on infested acorns were much higher where ungulates were present, and acorn infestation rates were significantly lower. However, ungulates did not provide the oaks any net benefit, since the reduction of infestation rates was not enough to compensate for the large amounts of sound acorns eaten by ungulates. Seed predation is usually studied as a progressive loss of seeds by pre- and post-dispersal predators, but the interactions between them are usually not considered. We show that intraguild predation on insects by large ungulates had an effect on the structure of the foraging guild, as the proportion of acorns predated by insects decreased; however, replicating the same experimental design in different ecological scenarios would increase the strength of these results. In conclusion, the present study shows the importance of considering the multi-trophic interactions between seed predators in order to have a complete picture of granivory.     

Egg-hatch phenology and intraguild predation between two mantid species

Relative timing of egg hatch between two cooccurring, congeneric mantids, Tenodera angustipennis and T. sinensis, was experimentally manipulated in replicated field enclosures to test the importance of intraguild predation to survivorship and development of T. angustipennis. T. angustipennis is normally smaller than its congener because of later egg-hatch. Delaying introduction of T. sinensis relative to normal egg hatch phenology reduced mortality for T. angustipennis, but did not affect its rate of development. The results indicate that intraguild predation by normally earlierhatching T. sinensis can be an important factor in the early life history of T. angustipennis, but that interspecific competition is not a strong selective factor in developmental asynchrony between these two species.     

Size structure and substitutability in an odonate intraguild predation system

Interactions between different size classes of predator species have the potential to influence survival of prey species in intraguild predation (IGP) systems, but few studies test for these effects. Using a substitutive design in a field setting, I measured the effects of two size classes of IG predators (large and small larvae of the dragonfly Anax junius) on the mortality of IG prey (larvae of the dragonfly Pachydiplax longipennis). I also examined whether combinations of large A. junius and P. longipennis and small A. junius and P. longipennis had substitutable effects on shared prey (larvae of the damselfly Ischnura verticalis). The presence of both size classes of A. junius, when alone and in combination with P. longipennis, significantly increased mortality of I. verticalis. In the presence of P. longipennis, large and small A. junius had similar effects on the mortality of I. verticalis, and effects of size-structured assemblages of A. junius were similar to the effects of each size class alone at the same density. The effects of the two size classes of A. junius on P. longipennis differed, and P. longipennis mortality was lower when exposed to size structured assemblages of A. junius than when exposed to only large A. junius at the same density. Results were similar to those in a laboratory study, although the effect of P. longipennis on I. verticalis was much lower in the field setting. These results demonstrate that interactions between different size classes of IG predators promote the survival of IG prey and highlight the importance of within-species size structure as a characteristic that may promote the coexistence of predators in IGP systems.     

Compensatory growth following transient intraguild predation risk in predatory mites

Compensatory or catch‐up growth following growth impairment caused by transient environmental stress, due to adverse abiotic factors or food, is widespread in animals. Such growth strategies commonly balance retarded development and reduced growth. They depend on the type of stressor but are unknown for predation risk, a prime selective force shaping life history. Anti‐predator behaviours by immature prey typically come at the cost of reduced growth rates with potential negative consequences on age and size at maturity. Here, we investigated the hypothesis that transient intraguild predation (IGP) risk induces compensatory or catch‐up growth in the plant‐inhabiting predatory mite Phytoseiulus persimilis. Immature P. persimilis were exposed in the larval stage to no, low or high IGP risk, and kept under benign conditions in the next developmental stage, the protonymph. High but not low IGP risk prolonged development of P. persimilis larvae, which was compensated in the protonymphal stage by increased foraging activity and accelerated development, resulting in optimal age and size at maturity. Our study provides the first experimental evidence that prey may balance developmental costs accruing from anti‐predator behaviour by compensatory growth.