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.     

Density-dependent effects of multiple predators sharing a common prey in an endophytic habitat

Multiple predator species feeding on a common prey can lead to higher or lower predation than would be expected by simply combining their individual effects. Such emergent multiple predator effects may be especially prevalent if predators share feeding habitat. Despite the prevalence of endophagous insects, no studies have examined how multiple predators sharing an endophytic habitat affect prey or predator reproduction. We investigated density-dependent predation of Thanasimus dubius (Coleoptera: Cleridae) and Platysoma cylindrica (Coleoptera: Histeridae) on a bark beetle prey, Ips pini (Coleoptera: Scolytidae), in a laboratory assay. I. pini utilize aggregation pheromones to group-colonize and reproduce within the stems of conifers. T. dubius and P. cylindrica exploit these aggregation pheromones to arrive simultaneously with the herbivore. Adult T. dubius prey exophytically, while P. cylindrica adults enter and prey within the bark beetle galleries. Larvae of both predators prey endophytically. We used a multiple regression analysis, which avoids confounding predator composition with density, to examine the effects of varying predator densities alone and in combination on herbivore establishment, herbivore reproduction, and predator reproduction. Predators reduced colonization success by both sexes, and decreased I. pini reproduction on a per male and per female basis. The combined effects of these predators did not enhance or reduce prey establishment or reproduction in unexpected manners, and these predators were entirely substitutable. The herbivores net replacement rate was never reduced significantly below one at prey and predator densities emulating field conditions. Similar numbers of each predator species emerged from the logs, but predator reproduction suffered from high intraspecific interference. The net replacement rate of P. cylindrica was not affected by conspecifics or T. dubius. In contrast, the net replacement rate of T. dubius decreased with the presence of conspecifics or P. cylindrica. Combinations of both predators led to an emergent effect, a slightly increased net replacement rate of T. dubius. This may have been due to predation by larval T. dubius on pupal P. cylindrica, as P. cylindrica develops more rapidly than T. dubius within this shared habitat.     

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.     

Habitat complexity reduces prey vulnerability: An experimental analysis using aquatic insect predators and immature dipteran prey

The effects of alternative prey and structural complexity of habitat on the selection of mosquito larvae by aquatic insect predators were evaluated in the laboratory. The water bugs Anisops bouvieri, Diplonychus (= Sphaerodema) rusticus, and D. annulatus, and the odonate nymphs, Ceriagrion coromandelianum and Brachydiplax chalybea chalybea, selected mosquito larvae based on their abundance relative to chironomid larvae and on the levels of habitat complexity. The effect of one prey species on the other was asymmetrical, as indicated through prey selectivity values. Compared to open habitat, the presence of macrophytes reduced the vulnerability of mosquito larvae while the effect was reverse in the presence of sediments. When both sediment and macrophytes were present in habitats, all the predators except D. annulatus consumed more mosquito larvae than chironomid larvae. The clearance rate, an indicator of predatory efficiency, varied among the predator species and habitat types. The results suggest that the outcome of the interactions between insect predators and mosquito immatures was context-dependent and that it was mediated by the presence of alternative controphic species and the habitat complexity.     

Non-lethal effects of predators on prey growth rates depend on prey density and nutrient additions

A number of studies show that predators can depress prey growth rates by inducing reductions in foraging activity, but the size of this non-lethal effect is quite variable. Here I investigate how prey density and resource productivity may alter the extent to which predators depress the growth rates of their prey. Theory predicts that when resources are overgrazed, an increase in predation risk will have little net effect on individual food intake because the decline in foraging effort will be offset by an increase in resource level. Thus, the non-lethal effects of predators on prey growth rates should depend upon prey density and resource productivity in a predictable manner, with the growth penalty imposed by predators being strongest when resources are undergrazed and weakest when resources are overgrazed. I tested this hypothesis by manipulating predation risk, prey density, and nutrient additions in a mesocosm experiment with the pulmonate snail Helisoma trivolvis . Refuge use by snails was 45% higher in the presence of caged crayfish than in their absence. Snail growth rates were reduced, on average, by 24% in the presence of caged crayfish. However, the magnitude of the growth penalty exacted by crayfish depended on snail density and nutrient additions. When snails were stocked at high density and nutrient additions were low, growth suppression was just 2.6%. At the other extreme, when snails were at low density and nutrient additions were high, growth suppression was 44.6%. Thus, the non-lethal effects of predators on prey growth depend on environmental context, illustrating an important link between individual traits and system-level properties.     

Habitat destruction in a simple predator-prey patch model: how predators enhance prey persistence and abundance

We model a metapopulation of predator-prey patches using both spatially implicit or mean-field (MF) and spatially explicit (SE) approaches. We show that in the MF model there are parameter regimes for which prey cannot persist in the absence of predators, but can in their presence. In addition, there are parameter regimes for which prey may persist in isolation, but the presence of predators will increase prey patch density. Predators may thus enhance prey persistence and overall abundance. The key mechanism responsible for this effect is the occurrence of prey dispersal from patches that are occupied by both prey and predators. In addition, these patches should be either long-lived, such as that occurs when predators keep prey from overexploiting its local resource, or the presence of a predator on a patch should significantly enhance the prey dispersal out of that patch. In the SE approach these positive effects of predators on prey persistence and abundance occur for even larger parameter ranges than in the MF model. Prey dispersal from predator-prey patches may thus be important for persistence of both species as a community, independent of the modeling framework studied. Comparison of the MF and SE approaches shows that local dispersal constraints can have the edge over global dispersal for the persistence of the metapopulation in regimes where the two species have a beneficial effect on each other. In general, our model provides an example of feedback in multiple-species metapopulations that can make the implementation of conservation schemes based on single-species arguments very risky.     

Emergent Allee effects in top predators feeding on structured prey populations

Top predators that forage in a purely exploitative manner on smaller stages of a size-structured prey population have been shown to exhibit an Allee effect. This Allee effect emerges from the changes that predators induce in the prey-population size distribution and represents a feedback of predator density on its own performance, in which the feedback operates through and is modified by the life history of the prey. We demonstrate that these emergent Allee effects will occur only if the prey, in the absence of predators, is regulated by density dependence in development through one of its juvenile stages, as opposed to regulation through adult fecundity. In particular, for an emergent Allee effect to occur, over-compensation is required in the maturation rate out of the regulating juvenile stage, such that a decrease in juvenile density will increase the total maturation rate to larger/older stages. If this condition is satisfied, predators with negative size selection, which forage on small prey, exhibit an emergent Allee effect, as do predators with positive size selection, which forage on large adult prey. By contrast, predators that forage on juveniles in the regulating stage never exhibit emergent Allee effects. We conclude that the basic life-history characteristics of many species make them prone to exhibiting emergent Allee effects, resulting in an increased likelihood that communities possess alternative stable states or exhibit catastrophic shifts in structure and dynamics.     

Test for predation effects of single versus multiple species of generalist predators: spiders and their insect prey

The prediction that single spider species (as exemplary generalist predators) limit associated prey populations to the same extent that species assemblages do was tested in a well controlled and replicated old field experiment involving the following treatments: (1) the natural spider assemblage (2) a numerically prominent web building spider, (3) a numerically prominent wandering spider, (4) a biomass prominent web-builder, and (5) a biomass prominent wandering spider. Pest insect numbers were significantly higher in spider removal controls than in any spider treament over the four month period of the study, both in terms of total numbers and per spider effects. The individual spider species, in general, showed reduced prey limitation effects relative to that of the spider assemblage, though the magnitudes of these differences were small when compared to those exhibited between the various treatments and the spider removal control. When insect numbers were partitioned according to taxa, no treatment was found to have limited the predaceous insects nor the phytophagous hemipterans. All treatments, however, showed significant limiting effects on the phytophagous homopterans, coleopterans, and dipterans in the old field system, and other taxa were significantly reduced in at least one treatment in addition to the spider assemblage as a whole.     

Partitioning the non-consumptive effects of predators on prey with complex life histories

Non-consumptive effects (NCEs) of predators on prey can be as strong as consumptive effects (CEs) and may be driven by numerous mechanisms, including predator characteristics. Previous work has highlighted the importance of predator characteristics in predicting NCEs, but has not addressed how complex life histories of prey could mediate predator NCEs. We conducted a meta-analysis to compare the effects of predator gape limitation (gape limited or not) and hunting mode (active or sit-and-pursue) on the activity, larval period, and size at metamorphosis of larval aquatic amphibians and invertebrates. Larval prey tended to reduce their activity and require more time to reach metamorphosis in the presence of all predator functional groups, but the responses did not differ from zero. Prey metamorphosed at smaller size in response to non-gape-limited, active predators, but counter to expectations, prey metamorphosed larger when confronted by non-gape-limited, sit-and-pursue predators. These results indicate NCEs on larval prey life history can be strongly influenced by predator functional characteristics. More broadly, our results suggest that understanding predator NCEs would benefit from greater consideration of how prey life history attributes mediate population and community-level outcomes.     

Response of predators to prey abundance: separating the effects of prey density and patch size

We tested the relative and combined effects of prey density and patch size on the functional response (number of attacks per unit time and duration of attacks) of a predatory reef fish (Cheilodactylus nigripes (Richardson)) to their invertebrate prey. Fish attacked prey at a greater rate and for longer time in large than small patches of prey, but large patches had naturally greater densities of prey. We isolated the effects of patch size and prey density by reducing the density of prey in larger patches to equal that of small patches; thereby controlling for prey density. We found that the intensity at which fish attacked prey (combination of attack rate and duration) was primarily a response to prey density rather than the size of patch they occupied. However, there was evidence that fish spent more time foraging in larger than smaller patches independent of prey density; presumably because of the greater total number of prey available. These experimental observations suggest that fish can distinguish between different notions of prey abundance in ways that enhance their rate of consumption. Although fish may feed in a density dependent manner, a critical issue is whether their rate of consumption outstrips the rate of increase in prey abundance to cause density dependent mortality of prey.     

Synergistic effects of multiple mechanisms drive priority effects within a tadpole assemblage

Mounting evidence suggests that the history of species arrival to a locality can have important effects on species performance but the mechanism(s) through which priority effects are produced is not always clear. Differences in the developmental time of frog tadpoles provide an opportunity to examine mechanisms through which priority effects may influence fitness components of a late arriving taxon. Specifically, tadpoles of the southern leopard frog (Rana) can often require more than a year to complete metamorphosis so they overwinter in a pond and compete with newly deposited tadpoles in the spring. We conducted an experiment in artificial ponds to evaluate mechanisms through which overwintering Rana tadpoles influence fitness components of southern toad (Bufo) tadpoles deposited into ponds during the spring. We found that overwintered Rana reduced Bufo performance while newly hatched Rana that enter a pond simultaneously with Bufo did not. The production of this priority effect was primarily the result of Rana depleting algal resources in a pond during the winter prior to Bufo arrival. The performance of Bufo did not correspond with variation in the abundance of algae present in a pond during the spring and we found evidence to indicate that, in the absence of resource exploitation during the winter, overwintered Rana do not compete strongly with Bufo during the spring when both species co‐occur. When Rana deplete algal resources during the winter, however, interactions between Rana and Bufo during the spring became much more important as both the development rate and survival of Bufo was reduced to a greater extent than what would have been predicted by resource exploitation alone. Our results demonstrate that priority effects can result from early colonists depleting resource availability prior to the arrival of other species which can intensify behavioral/physical interactions between species when they co‐occur.     

On competition of predators and prey infection

A class of prey–predator models with infected prey is investigated. Predation terms are either of Holling type II or III, infection is either modelled by mass action or standard incidence. It is shown that the key for understanding the model behaviour is the competition of predators versus infection. In the presented models the predator is not susceptible to the infection and the infection of the prey has no influence on the ability of the predator of catching the prey. However, the prey population can be seen as a resource which both the predators and the infection depend on. The competition for this resource is strong—the principle of competitive exclusion holds for biologically meaningful choices of parameters as long as there is no destabilisation by a Hopf bifurcation. The representation of models in competition diagrams which are introduced in this article can be used for a wide range of competition models which seems to be a promising method with many potential applications.     

Adaptation of prey and predators between patches

Mathematical models are proposed to simulate migrations of prey and predators between patches. In the absence of predators, it is shown that the adaptation of prey leads to an ideal spatial distribution in the sense that the maximal capacity of each patch is achieved. With the introduction of co-adaptation of predators, it is proved that both prey and predators achieve ideal spatial distributions when the adaptations are weak. Further, it is shown that the adaptation of prey and predators increases the survival probability of predators from the extinction in both patches to the persistence in one patch. It is also demonstrated that there exists a pattern that prey and predators cooperate well through adaptations such that predators are permanent in every patch in the case that predators become extinct in each patch in the absence of adaptations. For strong adaptations, it is proved that the model admits periodic cycles and multiple stability transitions.     

Temporally fluctuating prey and interfering predators: a positive feedback

Prey densities often show fluctuating patterns over various timescales. Focusing on short-term, within-generation fluctuating patterns of local prey availability, we suggest that prey that show synchronized and high-amplitude fluctuations in availability experience decreased risks of predation, but also enhance the maintenance of predator interference hierarchies by affecting the relative foraging success of unequal conspecific interferers. When predators interfere with each other, they forage less intensely on prey, which benefits prey in terms of decreased predation risk. The system hence involves a positive feedback. We thus argue that short-term temporal fluctuations in local prey availability could be an important mechanism behind how interference-structured social predator systems are developed and sustained. The temporal fluctuations also have implications for the phenotypic diversity of predators, and may be involved in speciation processes.     

Microcrustacean prey and macroinvertebrate predators in a stream food web

1. The consumption of microcrustacea by two polyphagous predators, larvae of the caddisfly Plectrocnemia conspersa (Curtis) and the alderfly Sialis fuliginosa Pictet, was investigated in an English stream with a well-known macro- and microinvertebrate fauna. Benthic samples were collected in August, November, December and April, and the gut contents of all individuals of both predators were examined. 2. All the microcrustacean groups (Cyclopoida, Harpacticoida, Chydoridae and Ostracoda) were identified in gut contents. Of the ten taxa present in the benthos, all occurred in the diet of P. conspersa; nine were found in S. fuliginosa. 3. Ontogenetic shifts in the diets of both predators were found, and microcrustacea were consumed more frequently by small than large instars. 4. There was little evidence of selective feeding by P. conspersa, whereas ostracods were over-represented in the diet of S. fuliginosa, compared with benthic relative densities. The Chydoridae were under-represented in the diet of both predators. 5. The food web of Broadstone Stream is perhaps the most detailed web available for any running water habitat. Increased taxonomic resolution produced marked changes in values of connectance and predator-prey ratios. Linkage density remained fairly constant at different levels of resolution and were high, indicative of a web of generalist species. Omnivory was pronounced and may be characteristic of donor-controlled systems where organic detritus is the primary energy base.     

Habitat and food specificity in aphidophagous predators

Current knowledge of the processes underlying prey location and choice by aphidophagous predators is reviewed by considering the succession of behavioural mechanisms required for the predator to obtain prey. The predator may locate areas where prey are likely to be found by responding to physical aspects of the habitat, or to semiochemicals produced by the host plant. The predator may then respond to visual or olfactory cues to locate the aphid prey. The predator's readiness to attack and consume aphids is influenced by any behavioural or chemical defence strategies, and by the palatability or nutrient value of the aphids. Toxic allelochemicals ingested by aphids from their host plant may have a detrimental effect on predators.     

Observation of epigeic predators and predation on artificial prey in a cereal field

Predation activity of different epigeic predators on artificially supplied prey was studied in a cereal field during several 24 h periods from spring to early summer 1993. Carabids were the most frequently observed predators. Among themPoecilus cupreus was the most voracious species during day-time, andAgonum muelleri during night-time. Predation rates were highest between 10.00 and 18.00 h and lowest between 02.00 and 10.00 h. Linear regressions showed significantly positive relations between temperature and predation rates, and between predation and activity density of epigeic predators. The latter relation was stronger when only activity density of predators which were observed to consume baits was included. Quadrat sampling and pitfall sampling showed that with the former only a small proportion of bait-consuming predators were caught whereas with the latter method this proportion was high.     

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.