Intraguild Predation among the Hoverfly Episyrphus balteatus de Geer (Diptera: Syrphidae) and Other Aphidophagous Predators

Aphidophagous predators compete for the same prey species. During their foraging activity they frequently encounter heterospecific aphid predators. These situations can lead to intraguild predation and may disrupt biological control efforts against aphids where more than one predator species is present. We investigated the behavior of larvae of the hoverfly Episyrphus balteatus de Geer and its interaction with three other aphid predators: the ladybird Coccinella septempunctata L., the lacewing Chrysoperla carnea Stephens, and the gall midge Aphidoletes aphidimyza (Rondani). Interspecific interactions between predators were examined in arenas of different sizes and in the presence of extraguild prey. The outcome of interactions between E. balteatus larvae and the other predators depended predominantly on the relative body size of the competitors. Relatively large individuals acted as intraguild predators, while relatively smaller individuals became intraguild prey. Eggs and first- as well as second-instar larvae of E. balteatus were highly susceptible to predation by all other predators, whereas pupae of E. balteatus were preyed upon only by the larvae of C. carnea. Interactions between A. aphidimyza and E. balteatus were asymmetric and always favored the latter. Eggs and first- as well as second-instar larvae of E. balteatus sustained intraguild predation irrespective of the size of the arena or the presence of extraguild prey. However, the frequency of predation on third-instar larvae of E. balteatus was significantly reduced. This study indicated that the same species can be both intraguild predator and intraguild prey. It is suggested that combinations of predators must be carefully chosen for success in biological control of aphids.     

Intraguild predation promotes complex alternative states along a productivity gradient

Intraguild predation is the simplest, ubiquitous form of trophic omnivory, known to greatly influence the structure and functioning of natural and managed food webs. Although alternative states are fundamental to intraguild predation dynamics, only necessary conditions for alternative states have been previously reported. Using simple models, we found complex but systematic patterns in which different alternative states occur along a productivity gradient, and clarified the sufficient conditions to separate these patterns. We found that two quantities known to control the necessary conditions also determine the sufficient conditions: (1) relative energy transfer efficiency through alternative trophic pathways to an intraguild predator, and (2) relative resource exploitation ability between intraguild prey and predator. These governing quantities suggest how body size and stoichiometric relations between intraguild prey and predators can influence the possibility of alternative states. Our results indicate that food webs involving intraguild predation have a high potential of complex alternative states, and their management can be highly precarious.     

Spatial refuge from intraguild predation: implications for prey suppression and trophic cascades

The ability of predators to elicit a trophic cascade with positive impacts on primary productivity may depend on the complexity of the habitat where the players interact. In structurally-simple habitats, trophic interactions among predators, such as intraguild predation, can diminish the cascading effects of a predator community on herbivore suppression and plant biomass. However, complex habitats may provide a spatial refuge for predators from intraguild predation, enhance the collective ability of multiple predator species to limit herbivore populations, and thus increase the overall strength of a trophic cascade on plant productivity. Using the community of terrestrial arthropods inhabiting Atlantic coastal salt marshes, this study examined the impact of predation by an assemblage of predators containing Pardosa wolf spiders, Grammonota web-building spiders, and Tytthus mirid bugs on herbivore populations (Prokelisia planthoppers) and on the biomass of Spartina cordgrass in simple (thatch-free) and complex (thatch-rich) vegetation. We found that complex-structured habitats enhanced planthopper suppression by the predator assemblage because habitats with thatch provided a refuge for predators from intraguild predation including cannibalism. The ultimate result of reduced antagonistic interactions among predator species and increased prey suppression was enhanced conductance of predator effects through the food web to positively impact primary producers. Behavioral observations in the laboratory confirmed that intraguild predation occurred in the simple, thatch-free habitat, and that the encounter and capture rates of intraguild prey by intraguild predators was diminished in the presence of thatch. On the other hand, there was no effect of thatch on the encounter and capture rates of herbivores by predators. The differential impact of thatch on the susceptibility of intraguild and herbivorous prey resulted in enhanced top-down effects in the thatch-rich habitat. Therefore, changes in habitat complexity can enhance trophic cascades by predator communities and positively impact productivity by moderating negative interactions among predators.     

Intraguild predation among larval plethodontid salamanders: a field experiment in artificial stream pools

Intraguild predation can be important in determining community structure and dynamics. Artificial stream pools were used to test for the impacts of intraguild predation among three species of larval plethodontid salamanders. Intraguild predators (large Gyrinophilus porphyriticus and Pseudotriton ruber) significantly decreased the survival of small Pseudotriton ruber. There was a trend toward reduced growth of Pseudotriton and Eurycea cirrigera in the presence of intraguild predators. The presence of large Gyrinophilus significantly reduced the growth rate of large Pseudotriton, both in the absence and presence of intraguild prey. The presence of intraguild prey did not significantly increase the growth rates of the intraguild predators. Intraguild predation is likely to be an important force shaping the evolution and ecology of these salamanders.     

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.     

Trophic structure of the spider community of a Mediterranean citrus grove: A stable isotope analysis

Spiders are dominant terrestrial predators that consume a large variety of prey and engage in intraguild predation. Although the feeding habits of certain species are well known, the trophic structure of spider assemblages still needs to be investigated. Stable isotope analysis enables characterisation of trophic relationships between organisms because it tracks the energy flow in food webs and indicates the average number of trophic transfers between a given species and the base of the web, thus being a useful tool to estimate the magnitude of intraguild predation in food webs. Using this technique, we studied the trophic groups of spiders and their links within the arthropod food web of a Mediterranean organic citrus grove. We assessed the trophic positions of the 25 most common spider species relative to other arthropod predators and potential prey in the four seasons of the year, both in the canopy and on the ground. The analyses showed great seasonal variation in the isotopic signatures of some arthropod species, as well as the existence of various trophic groups and a wide range of trophic levels among spiders, even in species belonging to the same family. Differences in δ¹⁵N between spiders and the most abundant prey in the grove usually spanned two trophic levels or more. Our findings provide field evidence of widespread intraguild predation in the food web and caution against using spider families or guilds instead of individual species when studying spider trophic interactions.     

Intraguild Interactions Between the Predatory Mites Neoseiulus californicus and Phytoseiulus persimilis

Species at the same trophic level may interact through competition for food, but can also interact through intraguild predation. Intraguild predation is widespread at the second and third trophic level and the effects may cascade down to the plant level. The effects of intraguild predation can be modified by antipredator behaviour in the intraguild prey. We studied intraguild predation and antipredator behaviour in two species of predatory mite, Neoseiulus californicus and Phytoseiulus persimilis, which are both used for control of the two-spotted spider mite in greenhouse and outdoor crops. Using a Y-tube olfactometer, we assessed in particular whether each of the two predators avoids odours emanating from prey patches occupied by the heterospecific predator. Furthermore, we measured the occurrence and rate of intraguild predation of different developmental stages of P. persimilis and N. californicus on bean leaves in absence or in presence of the shared prey. Neither of the two predator species avoided prey patches with the heterospecific competitor, both when inexperienced with the other predator and when experienced with prey patches occupied by the heterospecific predator. Intraguild experiments showed that N. californicus is a potential intraguild predator of P. persimilis. However, P. persimilis did not suffer much from intraguild predation as long as the shared prey was present. This is probably because N. californicus prefers to feed on two-spotted spider mites rather than on its intraguild prey.     

不同猎物及密度对巴氏新小绥螨和拉戈钝绥螨同类相残和集团内捕食作用的影响

明确不同猎物及密度下巴氏新小绥螨Neoseiulus barkeri与拉戈钝绥螨Amblyseius largoensis(Muma)的同类相残和集团内捕食作用,为其协同应用控制橡胶树害螨提供依据.在室温27±1℃、湿度75％±5％、光周期12 L∶12D 条件下,以六点始叶螨 Eotetranvchus sexmac...     

Tracking the role of alternative prey in soybean aphid predation by Orius insidiosus: a molecular approach

The soybean aphid, Aphis glycines (Hemiptera: Aphididae), is a pest of soybeans in Asia, and in recent years has caused extensive damage to soybeans in North America. Within these agroecosystems, generalist predators form an important component of the assemblage of natural enemies, and can exert significant pressure on prey populations. These food webs are complex and molecular gut-content analyses offer nondisruptive approaches for examining trophic linkages in the field. We describe the development of a molecular detection system to examine the feeding behaviour of Orius insidiosus (Hemiptera: Anthocoridae) upon soybean aphids, an alternative prey item, Neohydatothrips variabilis (Thysanoptera: Thripidae), and an intraguild prey species, Harmonia axyridis (Coleoptera: Coccinellidae). Specific primer pairs were designed to target prey and were used to examine key trophic connections within this soybean food web. In total, 32% of O. insidiosus were found to have preyed upon A. glycines, but disproportionately high consumption occurred early in the season, when aphid densities were low. The intensity of early season predation indicates that O. insidiosus are important biological control agents of A. glycines, although data suggest that N. variabilis constitute a significant proportion of the diet of these generalist predators. No Orius were found to contain DNA of H. axyridis, suggesting intraguild predation upon these important late-season predators during 2005 was low. In their entirety, these results implicate O. insidiosus as a valuable natural enemy of A. glycines in this soybean agroecosystem.     

Natural enemy diversity and biological control: Making sense of the context-dependency

Numerous studies have demonstrated that diverse predator assemblages can be more effective at controlling prey populations. Yet, other studies have shown no effect of predator diversity on prey mortality, or even negative effects (for example due to intraguild predation or interference). Much research emphasis has been placed on the traits of predators that maximise functional complementarity. However, comparatively less attention has been paid to the traits of the prey or habitat that may maximise predator diversity effects, even though there must be a variety of prey niches available to be partitioned in order for niche complementarity to occur. Following this logic, we review six hypotheses for when diverse enemy assemblages should be most effective: when 1) prey communities are diverse; 2) prey have complex life cycles; 3) prey are patchily distributed in space or time; 4) studies are conducted at larger spatial and temporal scales; 5) plant structures are complex; 6) prey are abundant. Many of these hypotheses lack direct tests, particularly in agricultural systems, but we find little or no direct or indirect support for hypotheses 1, 4, 5 and 6. However, previous work does provide some support for hypotheses 2 and 3. We discuss methods to test these hypotheses directly, and suggest that natural enemy diversity may only benefit the biological control of arthropods in heterogeneous systems.     

Dragonfly larvae and tadpole frog space use games in varied light conditions

Predators and prey often engage in a game where predators attemptto be in areas with higher prey densities and prey attempt tobe in areas with lower predator densities. A few models havepredicted the resulting distributions of predators and prey,but little empirical data exist to test these predictions andto examine how abiotic and biotic factors shape the distributions.Thus, we observed how Anax dragonfly nymphs and Pacific treefrog tadpoles (Pseudacris regilla) either together or separatelydistributed themselves in an arena with a high- and a low-preyresource patch. Trials were conducted in high- and low-lightconditions to manipulate predation risk and to view the effectsof this abiotic factor. Counter to the model predictions, wefound that predators were not more abundant in high-resource(HR) patches, and they thus did not force prey toward beinguniformly distributed. Using a model selection approach to assesswhat factors affected predator and prey patch-switching movement,we found that prey more often left patches that had more predatorspresent, but predators surprisingly more often left patcheswith more prey present. Light levels did not affect predationrisk; however, in the dark with the associated reduction invisual information predators preferred HR patches. This causeda lower coincidence of prey and predators in patches. Predatorsalso switched patches less often when they occupied the samepatch as the other predator. This suggests that predator distributions,and indirectly prey distributions, are affected by the riskof intraguild predation.     

Intraguild predation between the aphidophagous ladybird beetles Harmonia axyridis and Coccinella undecimpunctata (Coleoptera: Coccinellidae): The role of intra and extraguild prey densities

Laboratory cages were used to evaluate the influence of extraguild (EGprey) and intraguild prey (IGprey) densities on the direction, symmetry and magnitude of the intraguild predation (IGP) of the aphidophagous Harmonia axyridis Pallas on Coccinella undecimpunctata L. and vice versa. In order to understand the role of competition between IGprey, the experiments included treatments with one IGpredator, with one or four IGprey and EGprey (Aphis fabae Scopoli) ranging from zero to sufficient aphids to satiate the predators for 12, 24 or 48 h. Increases in EGprey and IGprey densities did not alter the direction, but decreased the magnitude and symmetry of IGP. Predation on one individual of IGprey decreased from more than 80%, in the absence of EGprey, to from 6% to 53%, at higher EGprey densities. Decrease in IGP was less when H. axyridis was the IGpredator. Even at high EGprey densities, eggs and 2nd larval stages of C. undecimpunctata were vulnerable to IGP and the level of predation was 40% and 53%. The presence of more than one IGprey increased the magnitude of IGP mainly at EGprey densities sufficient to satiate the predators for 12 and 24 h, suggesting that competition between the IGpredator and IGprey may be one of the processes promoting IGP. These results and those of other authors suggest that H. axyridis has the potential to be an IGpredator, mainly of the most vulnerable stages of IGprey. Thus, H. axyridis may negatively affect the survival of C. undecimpunctata, when these two species exploit the same resources.     

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.     

Impact of plant architecture and extraguild prey density on intraguild predation in an agroecosystem

Several models and experimental studies conducted in confined environments have shown that intraguild predation (IGP) can modulate population abundances and structure communities. A number of ecological and abiotic factors determine the nature and frequency of IGP. This study examined the effect of plant architecture and extraguild prey density, and their interactions, on the occurrence of IGP between two species of ladybird, Harmonia axyridis (Pallas) and Propylea quatuordecimpunctata L. (both Coleoptera: Coccinellidae). Theoretical concepts predict that IGP levels would increase with a decrease of both extraguild prey density and plant structural complexity. We conducted a factorial experiment in an open soybean field into which coccinellid larvae were introduced in experimental plots for a period of 5 days. We tested two levels of soybean aphid [Aphis glycines Matsumara (Hemiptera: Aphididae)] density, low and high (100 and 1 000 aphids per plot, respectively), and two levels of plant complexity, low (by removing half of the branches from the soybean plants) and high (by leaving plants intact). We used species‐specific molecular markers to detect the presence of P. quatuordecimpunctata in the digestive tract of H. axyridis. Molecular gut‐content analysis of H. axyridis revealed that rates of IGP were higher (20%) at low aphid density than at high aphid density (<6%). Decreased plant complexity did not impact the frequency of IGP. In accordance with existing literature, this study demonstrates that IGP is amplified at low extraguild prey density. We conclude that considering environmental factors, such as extraguild prey density, is crucial to improve our ability to predict the impact of intraguild predation on community structure and, from an applied perspective, biological control.     

The influence of generalist predators in spatially extended predator–prey systems

The presence of generalist predators is known to have important ecological impacts in several fields. They have wide applicability in the field of biological control. However, their role in the spatial distribution of predator and prey populations is still not clear. In this paper, the spatial dynamics of a predator–prey system is investigated by considering two different types of generalist predators. In one case, it is considered that the predator population has an additional food source and can survive in the absence of the prey population. In the other case, the predator population is involved in intraguild predation, i.e., the source of the additional food of the predator coincides with the food source of the prey population and thus both prey and predator populations compete for the same resource. The conditions for linear stability and Turing instability are analyzed for both the cases. In the presence of generalist predators, the system shows different pattern formations and spatiotemporal chaos which has important implications for ecosystem functioning not only in terms of their predictability, but also in influencing species persistence and ecosystem stability in response to abrupt environmental changes. This study establishes the importance of the consideration of spatial dynamics while determining optimal strategies for biological control through generalist predators.     

Diet of intraguild predators affects antipredator behavior in intraguild prey

In two-predator, one-prey systems with intraguild predationand patchily distributed prey, the intraguild prey may facea choice between prey patches with and without intraguild predators.To minimize falling victim to intraguild predation, intraguildprey are expected to perceive cues specifically associated withthe presence of intraguild predators. We investigate whetherintraguild prey avoided intraguild predators and which cuestriggered this behavior in a system composed of plant-inhabitingarthropods. We found that intraguild prey recognized intraguildpredators from a distance, based on their diet: they avoidedodors of intraguild predators that had consumed shared preybut did not avoid odors of intraguild predators that had fedon other diets, including a diet of conspecifics. When intraguildprey were foraging on a patch, detection of intraguild predatorsled to longer periods of immobility and to fewer captures ofthe shared prey. However, intraguild predators that were eitherstarved or had previously consumed intraguild prey posed a higherrisk to intraguild prey than did intraguild predators that hadconsumed the shared prey. We conclude that the cues used byintraguild prey to avoid intraguild predators are associatedwith the circumstances under which they encounter intraguildpredators in the field and not to different degrees of danger.     

An emerging infectious disease triggering large-scale hyperpredation

Hyperpredation refers to an enhanced predation pressure on a secondary prey due to either an increase in the abundance of a predator population or a sudden drop in the abundance of the main prey. This scarcely documented mechanism has been previously studied in scenarios in which the introduction of a feral prey caused overexploitation of native prey. Here we provide evidence of a previously unreported link between Emergent Infectious Diseases (EIDs) and hyperpredation on a predator-prey community. We show how a viral outbreak caused the population collapse of a host prey at a large spatial scale, which subsequently promoted higher-than-normal predation intensity on a second prey from shared predators. Thus, the disease left a population dynamic fingerprint both in the primary host prey, through direct mortality from the disease, and indirectly in the secondary prey, through hyperpredation. This resulted in synchronized prey population dynamics at a large spatio-temporal scale. We therefore provide evidence for a novel mechanism by which EIDs can disrupt a predator-prey interaction from the individual behavior to the population dynamics. This mechanism can pose a further threat to biodiversity through the human-aided disruption of ecological interactions at large spatial and temporal scales.     

Intraguild predation and cannibalism between the predatory mites Neoseiulus neobaraki and N. paspalivorus, natural enemies of the coconut mite Aceria guerreronis

Neoseiulus neobaraki and N. paspalivorus are amongst the most common phytoseiid predators of coconut mite, Aceria guerreronis, found in the spatial niche beneath coconut fruit bracts. Both predators may occur on the same coconut palms in Benin and Tanzania and are therefore likely to interact with each other. Here, we assessed cannibalism and intraguild predation (IGP) of the two predators in the absence and presence of their primary prey A. guerreronis. In the absence of the shared extraguild prey, A. guerreronis, N. neobaraki killed 19 larvae of N. paspalivorus per day and produced 0.36?eggs/female/day, while the latter species killed only 7 larvae of the former and produced 0.35?eggs/female/day. Presence of A. guerreronis only slightly decreased IGP by N. neobaraki but strongly decreased IGP by N. paspalivorus, which consumed 4-7 times less IG prey than N. neobaraki. Resulting predator offspring to IG prey ratios were, however, 4-5 times higher in N. paspalivorus than N. neobaraki. Overall, provision of A. guerreronis increased oviposition in both species. In the cannibalism tests, in the absence of A. guerreronis, N. neobaraki and N. paspalivorus consumed 1.8 and 1.2 conspecific larvae and produced almost no eggs. In the presence of abundant herbivorous prey, cannibalism dramatically decreased but oviposition increased in both N. neobaraki and N. paspalivorus. In summary, we conclude that (1) N. neobaraki is a much stronger intraguild predator than N. paspalivorus, (2) cannibalism is very limited in both species, and (3) both IGP and cannibalism are reduced in the presence of the common herbivorous prey with the exception of IGP by N. neobaraki, which remained at high levels despite presence of herbivorous prey. We discuss the implications of cannibalism and IGP on the population dynamics of A. guerreronis and the predators in view of their geographic and within-palm distribution patterns.     

Resource quality,resource availability,and intraguild predation among omnivorous mirids

Intraguild predation (IGP) among predatory species can influence many plant-arthropod associations. However, the relevance of IGP is poorly understood for truly omnivorous species such as those that can complete development on both animal and plant diets. Here we test the hypothesis that IGP among two omnivorous mirids is more common when extraguild food is either absent or not suitable. Laboratory experiments were performed in experimental cages in order to determine the effect of intraguild prey densities and diet availability on direction and intensity of IGP between Dicyphus tamaninii and Macrolophus caliginosus (Heteroptera: Miridae). Intraguild predation was symmetrical between the two mirid species in the absence of alternative food. Increasing densities of intraguild prey enhanced drastically the incidence of IGP. Intraguild predation was reduced when mirids were in the presence of green or red tomato fruits, but the presence of any other extraguild resources had no impact on IGP level. However, when given before the experiments, all resources with the exception of tomato leaves significantly reduced IGP. A second experiment was performed on live plants to compare the results of the previous trials with that obtained in a more natural setting. No IGP was observed when both mirid species were present on a plant. However, development of the intraguild prey (the more vulnerable stage) was hindered by the presence of the intraguild predator. The potential of such results is discussed from community ecology and biological control perspective.     

Increased control of thrips and aphids in greenhouses with two species of generalist predatory bugs involved in intraguild predation

The combined release of species of generalist predators can enhance multiple pest control when the predators feed on different prey, but, in theory, predators may be excluded through predation on each other. This study evaluated the co-occurrence of the generalist predators Macrolophus pygmaeus Rambur and Orius laevigatus (Fieber) and their control of two pests in a sweet pepper crop. Both predators consume pollen and nectar in sweet pepper flowers, prey on thrips and aphids, and O. laevigatus is an intraguild predator of M. pygmaeus. Observations in a commercial sweet pepper crop in a greenhouse with low densities of pests showed that the two predator species coexisted for 8 months. Moreover, their distributions in flowers suggested that they were neither attracted to each other, nor avoided or excluded each other. A greenhouse experiment showed that the predators together clearly controlled thrips and aphids better than each of them separately. Thrips control was significantly better in the presence of O. laevigatus and aphid control was significantly better in the presence of M. pygmaeus. Hence, combined inoculative releases of M. pygmaeus and O. laevigatus seem to be a good solution for controlling both thrips and aphids in greenhouse-grown sweet pepper. The predators are able to persist in one crop for a sufficiently long period and they complement each other in the control of both pests. This study also provides further evidence that intraguild predation does not necessarily have negative effects on biological control.