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.     

Species coexistence of communities with intraguild predation: The role of refuges used by the resource and the intraguild prey

In this paper, we develop a three-species intraguild predation model which incorporates refuges used by the resource and the intraguild prey, and focus on the effects of refuges on the three species coexistence. The invasion condition and parameter region for coexistence are obtained using invasion analysis. The new invasion condition requires that all boundary states with one missing species can be invaded by the missing species. Numerical simulations show that refuges have a major influence on species coexistence of intraguild predation system, and the results strongly depend on the types of refuges introduced into the model. Our study also shows that prey's refuges are detrimental to species coexistence except the resource using refuges. In contrast to previous research, we find that spatial structure may play an important role in effects of refuges on species coexistence of intraguild predation systems. Our results may shed new light on understanding the mechanisms and the persistence of multi-species predators-prey system.     

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.     

Emergent impacts of cannibalism and size refuges in prey on intraguild predation systems

Many organisms undergo ontogenetic niche shifts due to considerable changes in size during their development. These ontogenetic shifts can alter the trophic position of individuals, the type and strength of ecological interactions across species, and allow for cannibalism within species. In this study we ask if and how the interaction of a size refuge and cannibalism in the prey alters the dynamics of intraguild predation (IGP) systems. By manipulating the composition of large cannibalistic (Aeshna umbrosa) and predatory (Anax junius) dragonfly larvae in mesocosms we show that the interaction of cannibals and predators was non-linear and increased the survival of prey. The structure of the final resource community shared by prey and predator differed between small and large dragonfly treatments but not within size classes across species. In general, the small prey stage showed similar shifts in microhabitat use and refuge use when exposed to either conspecific cannibals or predators, while large cannibals showed no clear anti-predator response. However, further behavioral experiments revealed that specific behavioral components, such as distances between individuals or number of movements, differed when individuals were exposed to either cannibals or predators. This indicates that individuals discriminated between conspecific or heterospecific predators. Furthermore, in similar experiments large cannibals and predators showed different behaviors when exposed to conspecifics rather than to each other. These changes in behavior are consistent with the observed increase in prey survival. In general, the results indicate that cannibalism and ontogenetic niche shifts can result in behavior-mediated indirect interactions that reduce the impact of the predator on the mortality of its prey and alter the interactions of IGP systems. However, they also indicate that size is not the sole determinant and that we also need to account for the species identity when predicting the dynamics of communities.     

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.     

Interactions between a hunting spider and a web-builder: consequences of intraguild predation and cannibalism for prey suppression

Abstract. 1. Antagonistic interactions among invertebrate predators such as intraguild predation and cannibalism have the potential to dampen top‐down impacts on shared prey at lower trophic levels. Two abundant spider predators, the large wolf spider Pardosa littoralis and the small sheet‐web builder Grammonota trivitatta co‐occur on the salt marshes of eastern North America where they both attack planthoppers (Prokelisia spp.), the dominant herbivores on the marsh. Experiments both in the laboratory and field were used to assess the incidence of intraguild predation and cannibalism in these spiders and elucidate how such antagonistic interactions influence planthopper suppression. 2. Functional response experiments showed that with an increase in planthopper prey density, Grammonota captured more prey but not a higher proportion of that offered. Pardosa exhibited the same response when Grammonota were offered as intraguild prey. Both functional responses were type I over the range of prey densities offered. 3. Grammonota is moderately cannibalistic, and the presence of planthopper prey reduced the incidence of cannibalism. 4. Factorial experiments in the laboratory showed that Pardosa but not Grammonota reduced planthopper prey populations when prey density was low. By contrast, at high prey densities, both Pardosa and Grammonota had significant adverse effects on planthopper populations. Moreover, there was an interactive effect such that Grammonota reduced planthopper populations relatively more when Pardosa was absent than when it was present. 5. There was direct evidence for the intraguild predation of Grammonota by Pardosa such that fewer Grammonota survived in the presence of Pardosa than when it was absent. This result occurred whether planthopper prey were abundant or not. 6. Field releases of Grammonota in open plots resulted in significant but small decreases in the density of planthopper prey, both nymphs and adults. 7. Enhancing densities of Pardosa in open plots resulted in Grammonota suppression. The intraguild predation of Grammonota at this enhanced Pardosa density, however, did not preclude Pardosa from significantly reducing planthopper populations. 8. Although there was evidence that Grammonota reduced planthopper populations and that the intraguild predation of Grammonota by Pardosa occurred, the strength of these interactions was relatively weak given the low consumption rate of planthoppers by Grammonota (< 3 day^–1) and Grammonota by Pardosa (≈ 2 day^?1). Thus, weak asymmetric intraguild predation among spiders on the marsh likely dampens but does not eliminate the ability of Pardosa to exert significant top‐down control on planthopper populations.     

Spatial and temporal habitat use patterns for salt marsh nekton: implications for ecological functions

We synthesized information on temporal and spatial patterns of salt marsh habitat use by nekton in order to infer the importance of five main types of marsh function: reproduction, foraging, refuge from predation, refuge from stressful environmental conditions and environmental enhancement of physiology. We then extended the concept that intertidal gradients regulate habitat use patterns of nekton to a more universal concept that applies to all salt marsh habitats. We contend that all marsh habitats are linked to each other and to adjacent estuarine habitats along a depth gradient that mediates gradients in abiotic and biotic conditions. Tidal, diel and seasonal shifts in the magnitude and direction of these gradients result in gradients in tidal, diel and seasonal variation in biotic and abiotic conditions within the salt marsh. Collectively these gradients form the `marsh gradient'. We propose that patterns of marsh use and ecological function for nekton result primarily from physiological and behavioral responses to this marsh gradient. A comparison of habitat use patterns in the context of the marsh gradient is an important – and underutilized – method to study marsh function and essential fish habitat. We note that our limited insight into the function of the marsh habitat results from a significant lack of information on the occurrence and causes of tidal, diel and ontogenetic marsh use patterns by nekton; this is particularly relevant with respect to data on the variation in environmental conditions along marsh gradients over tidal, diel and seasonal cycles and on how environmental variation on these scales influences nekton behavior, growth and survival.     

Density of an intraguild predator mediates feeding group size, intraguild egg predation, and intra- and interspecific competition

Intraguild predation (IGP) is common in most communities, but many aspects of density-dependent interactions of IG predators with IG prey are poorly resolved. Here, we examine how the density of an IG predator can affect feeding group size, IG egg predation, and the growth responses of IG prey. We used laboratory feeding trials and outdoor mesocosm experiments to study interactions between a social intraguild predator (larvae of the wood frog; Rana sylvatica) and its prey (spotted salamander; Ambystoma maculatum). Larvae of R. sylvatica could potentially affect A. maculatum by consuming shared larval food resources or by consuming eggs and hatchlings. However, successful egg predation requires group feeding by schooling tadpoles. We established from five to 1,190 hatchlings of R. sylvatica in mesocosms, then added either 20 A. maculatum hatchlings to study interspecific competition, or a single egg mass to examine IGP. Crowding strongly suppressed the growth of R. sylvatica, and IGP was restricted to the egg stage. In the larval competition experiment, growth of A. maculatum was inversely proportional to R. sylvatica density. In the predation experiment, embryonic mortality of A. maculatum was directly proportional to the initial density of R. sylvatica and the mean number of tadpoles foraging on egg masses. IGP on eggs reduced A. maculatum hatchling density, which accelerated larval growth. Surprisingly, the density of R. sylvatica had no overall effect on A. maculatum growth because release from intraspecific competition via egg predation was balanced by increased interspecific competition. Our results demonstrate that the density of a social IG predator can strongly influence the nature and intensity of interactions with a second guild member by simultaneously altering the intensity of IGP and intra- and interspecific competition.L . A. Burley and A. T. Moyer contributed equally to this work.     

Intraguild predation, cannibalism, and microhabitat use in Calopteryx virgo and Somatochlora metallica larvae: a laboratory experiment

Intraguild predation (IGP) and cannibalism among co-occurring lotic odonate species was studied in Central Finland. A laboratory experiment was performed to assess the microhabitat use and cannibalism between intermediate and late instars of Calopteryx virgo larvae and predation by larger Somatochlora metallica larvae on the intermediate C. virgo instars. The experiment was run in small running-water aquaria where the larvae were able to divide their mutual habitat vertically by clinging onto artificial perches or crawling on the bottom. Life span of the small C. virgo larvae and attack rate on them were compared between the cannibalism and IGP treatments. The effect of predation on the activity, habitat use and spatial distribution of the small C. virgo larvae was examined. The IGP rate was 36%. The prey larvae spent the most of their time on the perches, whereas the S. metallica preferred the substrate. The large C.␣virgo larvae did not cannibalise smaller conspecifics. The presence of a predator (S. metallica) had no effect on the habitat use or activity of the prey (C. virgo) larvae. Habitat use differed more between those species than between conspecifics of different size classes of C. virgo. The spatial distribution between S.␣metallica and C. virgo showed a completely random pattern, whereas the two size classes of C. virgo aggregated in the vegetation. Absence of cannibalism and behavioural observations indicate that C. virgo may have a low tendency for intraspecific aggressions.     

The enemy of my enemy is my friend: intraguild predation between invaders and natives facilitates coexistence with shared invasive prey

Understanding and predicting the outcomes of biological invasions is challenging where multiple invader and native species interact. We hypothesize that antagonistic interactions between invaders and natives could divert their impact on subsequent invasive species, thus facilitating coexistence. From field data, we found that, when existing together in freshwater sites, the native amphipod Gammarus duebeni celticus and a previous invader G. pulex appear to facilitate the establishment of a second invader, their shared prey Crangonyx pseudogracilis. Indeed, the latter species was rarely found at sites where each Gammarus species was present on its own. Experiments indicated that this may be the result of G. d. celticus and G. pulex engaging in more intraguild predation (IGP) than cannibalism; when the ‘enemy’ of either Gammarus species was present, that is, the other Gammarus species, C. pseudogracilis significantly more often escaped predation. Thus, the presence of mutual enemies and the stronger inter- than intraspecific interactions they engage in can facilitate other invaders. With some invasive species such as C. pseudogracilis having no known detrimental effects on native species, and indeed having some positive ecological effects, we also conclude that some invasions could promote biodiversity and ecosystem functioning.     

Prey DNA detection success following digestion by intraguild predators: influence of prey and predator species

Intraguild predation (IGP) has been increasingly recognized as an important interaction in ecological systems over the past two decades, and remarkable insights have been gained into its nature and prevalence. We have developed a technique using molecular gut-content analysis to compare the rate of IGP between closely related species of coccinellid beetles (lady beetles or ladybirds), which had been previously known to prey upon one another. We first developed PCR primers for each of four lady beetle species: Harmonia axyridis, Coccinella septempunctata, Coleomegilla maculata and Propylea quatuordecimpunctata. We next determined the prey DNA detection success over time (DS(50) ) for each combination of interacting species following a meal. We found that DS(50) values varied greatly between predator-prey combinations, ranging from 5.2 to 19.3 h. As a result, general patterns of detection times based upon predator or prey species alone are not discernable. We used the DS(50) values to correct field data to demonstrate the importance of compensation for detection times that are specific to particular predator-prey combinations.     

Spatial distribution of interacting insect predators: Possible roles of intraguild predation and the surrounding habitat

Predator foraging behaviour affects the outcome of enemy–enemy interactions. Using a combination of fieldwork and laboratory experiments, we show that intraguild predation may be important in the field distribution of generalist predators that share a common prey: the eggs (and larvae) of the leaf beetle Phratora vulgatissima, a major insect pest in coppicing willow plantations. We focused on a species from the hoverfly genus Parasyrphus (Syrphidae), which may exhibit large temporal and spatial variation in density. Predator and prey densities were quantified in 40 field plots in willow plantations. The likelihood of finding hoverfly eggs declined with increasing densities of two predatory mirids, Orthotylus marginalis and Closterotomus fulvomaculatus, which exhibit less mobile behaviour similar to that of hoverfly larvae. The density of a more mobile predatory bug species, the anthocorid Anthocoris nemorum, was not associated with hoverfly occurrence. These results corroborate the hypothesis that less mobile predators should be stronger intraguild predators than mobilepredators. Further partial support for this hypothesis was obtained in the laboratory study where individual predators were presented with clutches of P. vulgatissima eggs containing one hoverfly egg: the less mobile C. fulvomaculatus and O. marginalis tended to consume the hoverfly egg more readily than the more mobile A. nemorum. However, most individuals of all three bug species consumed the egg of the potential competitor – the syrphid – within 24 h. The field study also showed that hoverfly occurrence was positively associated with the density of their prey and with the presence of nearby forests. We conclude that intraguild predation, abundance of prey and the surrounding habitat affect the distribution of hoverflies in this system and should be considered when developing biological control methods.     

Predator-induced changes in morphology of a prey fish: the effects of food level and temporal frequency of predation risk

In a series of experiments, we investigated the effects of food availability and risk frequency on the dynamics of predator-induced changes in growth and morphology of prey fish using goldfish (Carassius auratus) as our test species. In experiment 1, we fed goldfish high or low food rations and exposed them to either alarm cues from conspecifics, cues from swordtails or a water control. After 60 days, goldfish in the alarm cue treatment significantly increased their body depth and body weight but had smaller body length than goldfish exposed to swordtails cues or water, likely reducing their vulnerability to gape-limited predators. Importantly, food level had an impact on the amplitude of the morphological changes. In experiment 2, goldfish were exposed to two different frequencies of predation cues or a water control for 50 days. The cues were either continued or discontinued from day 51 to 100, and all cues were resumed from day 101 to 150. We found that goldfish exposed to predation cues increased their depth and weight at a faster rate than did the goldfish exposed to water, and of particular significance was the fact that frequency of risk had an effect on the amplitude of the change. When the cues were interrupted, the increase in growth rate parameters was reduced to the level of the goldfish exposed to water. However, when the cues were resumed, the rate increased to match the growth rate of the goldfish that were continuously exposed to the cues. Finally, we staged encounters between goldfish of differing morphologies and yellow perch (Perca flavescens) and found that deep-bodied goldfish had better survival than the shallow-bodied ones. These experiments illustrate the dynamic nature of inducible morphological defences.     

Evidence for intraguild predation by Podisus maculiventris on a ladybeetle, Coleomegilla maculata: Implications for biological control of Colorado potato beetle, Leptinotarsa decemlineata

The potential for intraguild predation (IGP) between larval and adult life stages of twopolyphagous arthropod predators common in NorthAmerican agroecosystems was studied in thelaboratory. Predators examined were the spinedsoldier bug, Podisus maculiventris Say,and the twelve-spotted ladybeetle, Coleomegilla maculata Lengi. A shared preyitem, eggs of the Colorado potato beetle (CPB),Leptinotarsa decemlineata Say, was alsoprovided to the predators, both to provide analternate food source and to quantify theimpact of IGP on the potential for pestsuppression by these two predators. Experimentswere conducted on single potato leaves inplastic cup arenas, and, subsequently, in cagesenclosing whole potato plants. IGP occurredasymmetrically, with P. maculiventrisadults and nymphs only attacking C. maculata larvae. Even though ladybeetle adultswere generally smaller than soldier bug adults,they were never preyed upon. This appears to bethe first documented case of a coccinellidshowing differential larval and adult immunityto attack by a larger invertebrate predator.The impact of IGP, when it did occur, on CPBegg consumption was equivocal. IGP did notconsistently influence levels of predation onthe eggs. Conversely, even when IGP did notoccur, predation on CPB eggs by both predatorstogether did not increase significantly overlevels inflicted by either predator alone. Theimplications for biological control of CPB bythese predators, which are being considered foraugmentative release in potato and tomato cropsin the United States, are discussed.     

Opposite latitudinal patterns for bird and arthropod predation revealed in experiments with differently colored artificial prey

The strength of biotic interactions is generally thought to increase toward the equator, but support for this hypothesis is contradictory. We explored whether predator attacks on artificial prey of eight different colors vary among climates and whether this variation affects the detection of latitudinal patterns in predation. Bird attack rates negatively correlated with model luminance in cold and temperate environments, but not in tropical environments. Bird predation on black and on white (extremes in luminance) models demonstrated different latitudinal patterns, presumably due to differences in prey conspicuousness between habitats with different light regimes. When attacks on models of all colors were combined, arthropod predation decreased, whereas bird predation increased with increasing latitude. We conclude that selection for prey coloration may vary geographically and according to predator identity, and that the importance of different predators may show contrasting patterns, thus weakening the overall latitudinal trend in top‐down control of herbivorous insects.     

Rethinking trophic niches: Speed and body mass colimit prey space of mammalian predators

1. Realized trophic niches of predators are often characterized along a one‐dimensional range in predator–prey body mass ratios. This prey range is constrained by an “energy limit” and a “subdue limit” toward small and large prey, respectively. Besides these body mass ratios, maximum speed is an additional key component in most predator–prey interactions.
2. Here, we extend the concept of a one‐dimensional prey range to a two‐dimensional prey space by incorporating a hump‐shaped speed‐body mass relation. This new “speed limit” additionally constrains trophic niches of predators toward fast prey.
3. To test this concept of two‐dimensional prey spaces for different hunting strategies (pursuit, group, and ambush predation), we synthesized data on 63 terrestrial mammalian predator–prey interactions, their body masses, and maximum speeds.
4. We found that pursuit predators hunt smaller and slower prey, whereas group hunters focus on larger but mostly slower prey and ambushers are more flexible. Group hunters and ambushers have evolved different strategies to occupy a similar trophic niche that avoids competition with pursuit predators. Moreover, our concept suggests energetic optima of these hunting strategies along a body mass axis and thereby provides mechanistic explanations for why there are no small group hunters (referred to as “micro‐lions”) or mega‐carnivores (referred to as “mega‐cheetahs”).
5. Our results demonstrate that advancing the concept of prey ranges to prey spaces by adding the new dimension of speed will foster a new and mechanistic understanding of predator trophic niches and improve our predictions of predator–prey interactions, food web structure, and ecosystem functions.

     

Plant versus prey resources: Influence on omnivore behavior and herbivore suppression

Conservation biological control tactics, such as beetle banks, that increase habitat complexity generally increase epigeal predator abundance. Habitat complexity also increases alternative food which can attract and sustain predators but may reduce predation of target pests. Our goal was to determine how alternative food from different trophic levels (fly pupae and seeds) affects behavior and biological control efficacy of omnivorous carabid beetles. Seed subsidies increased omnivorous carabid abundance more than pupae by increasing aggregation and reducing emigration. Laboratory experiment demonstrated that both omnivorous carabid species preferred seeds and pupae over cutworms. However, in field cages seeds but not pupae resulted in greater cutworm damage to corn seedlings. Our results indicate that omnivorous carabids have a stronger behavioral response to seeds than prey such that only seeds influence aggregation, emigration, and crop damage. Interestingly, whereas seeds increased omnivorous carabid abundance, pupae had no affect on carnivore abundance. Thus, carabid guild composition is skewed in favor of omnivores when seed density increases. An important finding was that the effect of seeds on behavior, predation, and crop damage was consistent among replicate carabid species suggesting our results pertain to other omnivorous species in resource diverse habitats.Our results provide insight into the mechanisms underlying the unpredictable benefit of conservation biological control tactics that alter habitat complexity.     

The roles of top and intermediate predators in herbivore suppression: contrasting results from the field and laboratory

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Effect of intraguild predation on the survival and development of three species of aphidophagous ladybirds: consequences for invasive species

Abstract 1 Survival and development of hatchling larvae of three aphidophagous ladybirds (Coleoptera: Coccinellidae), Harmonia axyridis Pallas, Coccinella septempunctata brucki Mulsant and Adalia bipunctata Linnaeus, when fed their own and the other species eggs were recorded. 2 In all three species, the larvae survived when fed conspecific eggs. 3 The percentage of larvae of H. axyridis that survived decreased to 35% and 85% when fed eggs of A. bipunctata and C. s. brucki, respectively. All the larvae of A. bipunctata and C. s. brucki died after eating eggs of H. axyridis. None of the larvae of C. s. brucki died after eating eggs of A. bipunctata, whereas 46% of those of A. bipunctata died after eating eggs of C. s. brucki. 4 In general, larvae were reluctant to eat the eggs of other species. However, larvae of C. s. brucki showed less reluctance than H. axyridis to eat the eggs of A. bipunctata. 5 The consequence of this for invasive species of ladybird is discussed.