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.     

Cues of intraguild predators affect the distribution of intraguild prey

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

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.     

Productivity, dispersal and the coexistence of intraguild predators and prey

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

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

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

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.     

Visual predators impose correlational selection on prey color pattern and behavior

Several lines of indirect evidence suggest that selection imposedby predators may favor certain combinations of prey colorationand behavior at the expense of other combinations, but thishypothesis has never been tested experimentally. We manipulatedcolor pattern and behavior of pygmy grasshoppers (Tetrix subulata)and exposed them to predation from domestic chickens. We paintedgrasshoppers either uniformly black or striped and manipulatedtheir behavior by changing the ambient temperature. We foundthat the striped pattern enhanced grasshopper survival whenreaction distance was short and jumping performance poor, butit decreased survival when reaction, distance was long and performancehigh, relative to uniformly black individuals. To our knowledge,this is the first experimental demonstration that selectionmediated by visual predators acts on the combination of preycolor pattern and behavior. Further studies are necessary, however,to clarify how widespread correlalional selection is in coevolvedpredator-prey relationships. Correlational selection may resultin genetic coupling between traits, influence the dynamics ofpolymorphisms, and promote the evolution of sexual dichromatismin animals exhibiting sexual differences in behavior. Our resultsalso illustrate the potential importance of visual illusionscreated by moving objects and suggest that it may be dangerousto make inferences about the relative survival value of differentcolor patterns from the outcome of experiments that do not takeinto account prey behavior.     

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.     

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

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

Frequency-dependent selection by predators

Sometimes predators tend to concentrate on common varieties of prey and overlook rare ones. Within prey species, this could result in the fitness of each variety being inversely related to its frequency in the population. Such frequency-dependent or 'apostatic' selection by predators hunting by sight could maintain polymorphism for colour pattern, and much of the supporting evidence for this idea has come from work on birds and artificial prey. These and other studies have shown that the strength of the observed selection is affected by prey density, palatability, coloration and conspicuousness. When the prey density is very high, selection becomes 'anti-apostatic': predators preferentially remove rare prey. There is still much to be learned about frequency-dependent selection by predators on artificial prey: work on natural polymorphic prey has hardly begun.     

Evolutionary ecology of movement by predators and prey

An essential key to explaining the mechanistic basis of ecological patterns lies in understanding the consequences of adaptive behavior for distributions and abundances of organisms. We developed a model that simultaneously incorporates (a) ecological dynamics across three trophic levels and (b) evolution of behaviors via the processes of mutation, selection, and drift in populations of variable, unique individuals. Using this model to study adaptive movements of predators and prey in a spatially explicit environment produced a number of unexpected results. First, even though predators and prey had limited information and sometimes moved in the “wrong” direction, evolved movement mechanisms allowed them to achieve average spatial distributions approximating optimal, ideal free distributions. Second, predators’ demographic parameters had marked, nonlinear effects on the evolution of movement mechanisms in the prey: As the predator mortality rate was increased past a critical point, prey abruptly shifted from making very frequent movements away from predators to making infrequent movements mainly in response to resources. Third, time series analyses revealed that adaptive, conditional movements coupled ecological dynamics across species and space. Our results provide general predictions, heretofore lacking, about how predators and prey should respond to one another on both ecological and evolutionary time scales.     

Microcosm studies on control of aphids by generalist arthropod predators: Effects of alternative prey

Generalist predators are potential controlagents of aphids in cereal fields. Becauseaphids are low-quality prey for most generalistpredators, the availability of alternativehigh-quality prey may influence theinteractions between aphids and their predatorsby reducing the predation rate due to loweredpreference for aphids. We analysed this bytesting the ability of six generalist predators(the spiders Erigone atra (Bl.), Clubiona lutescens (Westr.)/reclusaO.P.-C., Pachygnatha degeeri Sundevall,Pardosa prativaga (L.Koch), the carabidbeetle Bembidion lampros (Herbst), andthe harvestman Oligolophus tridens (C.L.Koch)) to suppress Rhopalosiphum padi(Linné) populations in the presence orabsence of alternative prey types (fruit fliesDrosophila melanogaster (Meigen) or thecollembolan Tomocerus bidentatus(Folsom)). Experiments of 10 days duration werecarried out in a microcosm set-up. Withoutalternative prey all predators except B.lampros were able to reduce aphid populationdevelopment significantly relative topredator-free controls. The harvest spider O. tridens was the most efficient predator(<90% reduction). Presence of alternativeprey (fruit flies) had a significant negativeeffect on aphid limitation by P. prativagaand a weak positive effect in B. lampros, but did not influence the ability to reduce aphids in E. atra, Clubiona, P. degeeri and O. tridens. In addition, 24-hours' consumption experiments with adult P. degeeri and subadult C. lutescens/reclusa, using R. padi and D. melanogaster as prey types, showed markedly lower consumption rates of aphid than of fruit fly prey. The microcosm arrangement is a simple way to partly simulate the habitat complexity of an agricultural field under laboratory conditions and proved to be a useful tool for investigating complex predator-prey interactions.     

Behavioral linkage of pelagic prey and littoral predators: microhabitat selection by Daphnia induced by damselfly larvae

Only recently ecologists started treating the previously separately considered benthic, littoral and pelagic zones of lake ecosystems as closely connected compartments. Here we study a link between organisms belonging to a different compartment – namely the pelagic and the littoral – through behavior in a series of laboratory experiments. Waterfleas of the genus Daphnia are inhabitants of the pelagic zone and suffer a high predation pressure from syntopic vertebrate predators (mainly fish). Presumably to escape this predation, they sometimes migrate in the day to the littoral to seek refuge within macrophytes and return to the pelagic at night. Zygopterans from the genus Ischnura do commonly co-occur in ponds with Daphnia and are known as opportunistic predators of Daphnia . In two initial experiments in microcosms in the lab we showed that Ischnura larvae are littoral predators strongly associated with macrophytes. Although we found that predation rates of individual Ischnura larvae on Daphnia are approximately 1.5 fold lower in macrophytes compared to open water, total predation from Ischnura on Daphnia per unit area is tenfold higher within macrophytes than in open water, making the open water a safer place for Daphnia with regard to Ischnura predation. In a third microcosm experiment we monitored horizontal distribution of Daphnia in the absence, presence and odor only of Ischnura larvae. After 2 hours, on average 10% less Daphnia remained within the vegetation when Ischnura larvae or only their odor were present compared to when Ischnura or their odor were absent. We interpret this as a behavioral anti-predation response of Daphnia to the presence of Ischnura larvae that seems primarily chemically mediated. The observed horizontal migration of the pelagic prey driven by the littoral predator may couple both lake compartments and may interact with the predator–prey relationships within the pelagic.     

Emergent impacts of multiple predators on prey

Although almost all prey live with many types of predator, most experimental studies of predation have examined the effects of only one predator at a time. Recent work has revealed new insights into the emergent impacts of multiple predators on prey and experimental studies have identified statistical methods for evaluating them. These studies suggest two main types of emergent effect-risk reduction caused by predator-predator interactions and risk enhancement caused by conflicting prey responses to multiple predators. Some theory and generalities are beginning to emerge concerning the conditions that tend to produce these two outcomes.     

Energetic conditions promoting top-down control of prey by predators

Humans remove large amounts of biomass from natural ecosystems, and large bodied high trophic level animals are especially sensitive and vulnerable to exploitation. The effects of removing top-predators on food webs are often difficult to predict because of limited information on species interaction strengths. Here we used a three species predator-prey model to explore relationships between energetic properties of trophodynamic linkages and interaction strengths to provide heuristic rules that indicate observable energetic conditions that are most likely to lead to stable and strong top-down control of prey by predator species. We found that strong top-down interaction strengths resulted from low levels of energy flow from prey to predators. Strong interactions are more stable when they are a consequence of low per capita predation and when predators are subsidized by recruitment. Diet composition also affects stability, but the relationship depends on the form of the functional response. Our results imply that for generalist satiating predators, strong top-down control on prey is most likely for prey items that occupy a small portion of the diet and when density dependent recruitment is moderately high.     

Impact of intraguild predators on survival of a forest-floor wolf spider

We investigated the impact of variation in densities of a guild of generalist predators on survival of young wolf spiders of the genus Schizocosa. Numbers of other spiders and centipedes were reduced by >80% in fenced 4-m² plots in an experiment that was replicated twice in each of three forest locations. Schizocosa survival during the 1st month was low (<50%) in all three locations, but did not differ between predator-reduction and control plots. By the end of the 1st month, densities of the manipulated predators had converged in control and perturbed treatments, most likely because of reduced per capita mortality from lowered rates of intraguild predation and cannibalism in the experimental treatment. During the 2nd month of the experiment, centipedes and spiders other than Schizocosa again were removed from the experimental plots and, unlike the earlier period, numbers of intraguild predators in the predator-removal treatment remained lower than in control plots. Reducing densities of intraguild predators during the 2nd month improved survival of older juvenile Schizocosa by 75% in two of three locations on the forest floor. In addition to this evidence that intraguild predation can affect older juvenile Schizocosa, survival of Schizocosa during the last half of the experiment was negatively correlated with spatial variation in densities of gnaphosid and ctenid spiders. These two abundant families of cursorial spiders preyed on Schizocosa at a high rate in laboratory trials. Thus, variation in densities of intraguild predators did not influence the youngest Schizocosa, but did influence the survival of older juveniles, most likely due to variations in densities of other cursorial spiders. Received: 21 October 1998 / Accepted: 14 May 1999     

大鸨的巢位选择研究

20 0 0年和 2 0 0 1年的 4～ 7月连续两年 ,在内蒙古自治区科尔沁右翼前旗东南部草原上采用野外直接观测和样方法对繁殖期大鸨 (Otistarda)的巢位选择进行了研究 .结果表明 ,大鸨是一种营地面松散型群巢的大型鸟类 ,最近巢间距为 9m .大鸨在繁殖期对巢位具有明显的选择性 :首先表现在景观尺度上的选择 ,大鸨巢多筑在海拔 190～ 2 30m的草原岗坡的坡腰上 ,以偏南向的朝阳缓坡的坡腰上为多 ,最大坡度不超过 8° ,而且巢均筑在距车道不远的地方 ;其次表现在植被结构上的选择 ,大鸨倾向于选择枯草较厚、植被密度较高且多数植物高度在 15～ 35cm的地方营巢 ,但植被密度过高处却并不选择 .     

Generalist predators disrupt parasitoid aphid control by direct and coincidental intraguild predation

Generalist predators and parasitoids are considered to be important regulators of aphids. The former not only feed on these pests, but might also consume parasitoids at all stages of development. This direct or coincidental interference affects the natural control of aphids, the scale of which is largely unknown, and it has rarely been examined under natural conditions. Here, molecular diagnostics were used to track trophic interactions in an aphid-parasitoid-generalist predator community during the build-up of a cereal aphid population. We found that generalist predators, principally carabid and staphylinid beetles as well as linyphiid spiders, had strong trophic links to both parasitoids and aphids. Remarkably, more than 50% of the parasitoid DNA detected in predators stems from direct predation on adult parasitoids. The data also suggest that coincidental intraguild predation is common too. Generalist predators, hence, disrupt parasitoid aphid control, although the levels at which the predators feed on pests and parasitoids seem to vary significantly between predator taxa. Our results suggest that taxon-specific trophic interactions between natural enemies need to be considered to obtain a more complete understanding of the route to effective conservation biological control.