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.     

Salamander evolution across a latitudinal cline in gape-limited predation risk

General predictions of community dynamics require that insights derived from local habitats can be scaled up to explain phenomena across geographic scales. Across these larger spatial extents, adaptation can play an increasing role in determining the outcome of species interactions. If local adaptation is common, then our ability to generalize measures of species interaction strength across communities will be limited without an additional understanding of the genetic variation underlying interaction traits. In the context of predator–prey interactions, prey individuals commonly are expected to reduce risky foraging behaviors and subsequent growth under predation threat. However, rapid growth into a large body size can defend against gape-limited predators, creating a tradeoff between increased predation risk due to elevated foraging activity and decreased predation risk due to large size. Here I combine field observations, natural selection experiments, and common garden assays to understand potential adaptations of spotted salamander Ambystoma maculatum larvae to gape-limited and gape-unconstrained predators. Field observations and natural selection trials suggested antagonistic selection on prey body size among ponds dominated by gape-limited predator salamanders A. opacum and gape-unconstrained beetle larvae Dytiscus . In common garden experiments, prey from sites with high gape-limited predation risk grew larger than those from other sites, suggesting the evolution of rapid growth into a prey size refuge. Larvae from all sites grew to a large size when exposed to the gape-limited N. viridescens predator's kairomones. Hence, induced rapid growth into a size refuge may be an adaptive response to gape-limited predation risk. Results point to an important role for cross-community generalizations based on functional classifications of predators by their gape constraints and inter-site genetic variation in prey growth rates and behaviors.     

Non-lethal effects of predation in birds

Predators can affect individual fitness and population and community processes through lethal effects (direct consumption or ‘density’ effects), where prey is consumed, or through non‐lethal effects (trait‐mediated effects or interactions), where behavioural compensation to predation risk occurs, such as animals avoiding areas of high predation risk. Studies of invertebrates, fish and amphibians have shown that non‐lethal effects may be larger than lethal effects in determining the behaviour, condition, density and distribution of animals over a range of trophic levels. Although non‐lethal effects have been well described in the behavioural ecology of birds (and also mammals) within the context of anti‐predation behaviour, their role relative to lethal effects is probably underestimated. Birds show many behavioural and physiological changes to reduce direct mortality from predation and these are likely to have negative effects on other aspects of their fitness and population dynamics, as well as affecting the ecology of their own prey and their predators. As a consequence, the effects of predation in birds are best measured by trade‐offs between maximizing instantaneous survival in the presence of predators and acquiring or maintaining resources for long‐term survival or reproduction. Because avoiding predation imposes foraging costs, and foraging behaviour is relatively easy to measure in birds, the foraging–predation risk trade‐off is probably an effective framework for understanding the importance of non‐lethal effects, and so the population and community effects of predation risk in birds and other animals. Using a trade‐off approach allows us to predict better how changes in predator density will impact on population and community dynamics, and how animals perceive and respond to predation risk, when non‐lethal effects decouple the relationship between predator density and direct mortality rate. The trade‐off approach also allows us to identify where predation risk is structuring communities because of avoidance of predators, even when this results in no observable direct mortality rate.     

Estimating predation risk in zooplankton communities: the importance of vertical overlap

In order to estimate predation risk in nature, two basic components of predation need to be quantified: prey vulnerability, and density risk. Prey vulnerability can be estimated from clearance rates obtained from enclosure experiments with and without predators. Density risk is a function of predator density, and the spatial and temporal overlap of the predator and prey populations. In the current study we examine the importance of the vertical component of overlap in making accurate estimates of predation risk from the invertebrate predator Mesocyclops edax on rotifer versus crustacean prey. The results indicate that assumptions of uniform predator and prey densities cause a significant underestimation of predation risk for many crustacean prey due to the coincident vertical migration of these prey with the predator. The assumption of uniformity is more reasonable for estimating predation risk for most rotifer prey.     

Evaluating the effects of large marine predators on mobile prey behavior across subtropical reef ecosystems

The indirect effect of predators on prey behavior, recruitment, and spatial relationships continues to attract considerable attention. However, top predators like sharks or large, mobile teleosts, which can have substantial top–down effects in ecosystems, are often difficult to study due to their large size and mobility. This has created a knowledge gap in understanding how they affect their prey through nonconsumptive effects. Here, we investigated how different functional groups of predators affected potential prey fish populations across various habitats within Biscayne Bay, FL. Using baited remote underwater videos (BRUVs), we quantified predator abundance and activity as a rough proxy for predation risk and analyzed key prey behaviors across coral reef, sea fan, seagrass, and sandy habitats. Both predator abundance and prey arrival times to the bait were strongly influenced by habitat type, with open homogenous habitats receiving faster arrival times by prey. Other prey behaviors, such as residency and risk‐associated behaviors, were potentially driven by predator interaction. Our data suggest that small predators across functional groups do not have large controlling effects on prey behavior or stress responses over short temporal scales; however, habitats where predators are more unpredictable in their occurrence (i.e., open areas) may trigger risk‐associated behaviors such as avoidance and vigilance. Our data shed new light on the importance of habitat and context for understanding how marine predators may influence prey behaviors in marine ecosystems.     

Are Infaunal Predators Important in Structuring Marine Soft-Bottom Communities?

The role of infaunal predators in structuring marine soft-bottomcommunities was evaluated according to these predators': 1)effects on prey density based on manipulative field experiments,2) feeding rates, 3) effects on prey distribution, 4) effectson species diversity, and 5) interactions with their prey. Estimatesof feeding rates indicate that many predatory taxa have thepotential to reduce the size of prey populations and suggestthat nemerteans are likely to have a larger impact on infaunalabundances than polychaetes. Infaunal predators have been demonstratedto have a significant effect on infaunal densities and to affectthe spatial and temporal distribution of their prey. The effectsof these predators on species diversity apparently depend onthe predator and the diversity of the system. These conclusionsmay not be applicable to all soft-bottom habitats or all groupsof infaunal predators because they are based on studies of veryfew taxa conducted almost exclusively in intertidal, unvegetated,mud habitats. Additional studies are needed on the effects ofpredation by infauna on infaunal population dynamics and onthe mechanisms of interactions between predator and prey. Furtherinvestigation will probably reveal that different groups ofinfaunal predators play different roles in structuring soft-bottomcommunities.     

Inside‐container effects drive mosquito community structure in Brazilian Atlantic forest

Metacommunity theory is a convenient framework in which to investigate how local communities linked by dispersal influence patterns of species distribution and abundance across large spatial scales. For organisms with complex life cycles, such as mosquitoes, different pressures are expected to act on communities due to behavioral and ecological partitioning of life stages. Adult females select habitats for oviposition, and resulting offspring are confined to that habitat until reaching adult stages capable of flight; outside‐container effects (OCE) (i.e., spatial factors) are thus expected to act more strongly on species distributions as a function of adult dispersal capability, which should be limited by geographic distances between sites. However, larval community dynamics within a habitat are influenced by inside‐container effects (ICE), mainly interactions with conspecifics and heterospecifics (e.g., through effects of competition and predation). We used a field experiment in a mainland‐island scenario to assess whether environmental, spatial, and temporal factors influence mosquito prey and predator distributions and abundances across spatial scales: within‐site, between‐site, and mainland‐island. We also evaluated whether predator abundances inside containers play a stronger role in shaping mosquito prey community structure than do OCE (e.g., spatial and environmental factors). Temporal influence was more important for predators than for prey mosquito community structure, and the changes in prey mosquito species composition over time appear to be driven by changes in predator abundances. There was a negligible effect of spatial and environmental factors on mosquito community structure, and temporal effects on mosquito abundances and distributions appear to be driven by changes in abundance of the dominant predator, perhaps because ICE are stronger than OCE due to larval habitat restriction, or because adult dispersal is not limited at the chosen spatial scales.     

Birds of prey as limiting factors of gamebird populations in Europe: a review

Whether predators can limit their prey has been a topic of scientific debate for decades. Traditionally it was believed that predators take only wounded, sick, old or otherwise low-quality individuals, and thus have little impact on prey populations. However, there is increasing evidence that, at least under certain circumstances, vertebrate predators may indeed limit prey numbers. This potential role of predators as limiting factors of prey populations has created conflicts between predators and human hunters, because the hunters may see predators as competitors for the same resources. A particularly acute conflict has emerged over the past few decades between gamebird hunters and birds of prey in Europe. As a part of a European-wide research project, we reviewed literature on the relationships between birds of prey and gamebirds. We start by analysing available data on the diets of 52 European raptor and owl species. There are some 32 species, mostly specialist predators feeding on small mammals, small passerine birds or insects, which never or very rarely include game animals (e.g. hares, rabbits, gamebirds) in their diet. A second group (20 species) consists of medium-sized and large raptors which prey on game, but for which the proportion in the diet varies temporally and spatially. Only three raptor species can have rather large proportions of gamebirds in their diet, and another seven species may utilise gamebirds locally to a great extent. We point out that the percentage of a given prey species in the diet of an avian predator does not necessarily reflect the impact of that predator on densities of prey populations. Next, we summarise available data on the numerical responses of avian predators to changing gamebird numbers. In half of these studies, no numerical response was found, while in the remainder a response was detected such that either raptor density or breeding success increased with density of gamebirds. Data on the functional responses of raptors were scarce. Most studies of the interaction between raptors and gamebird populations give some estimate of the predation rate (per cent of prey population taken by predator), but less often do they evaluate the subsequent reduction in the pre-harvest population or the potential limiting effect on breeding numbers. The few existing studies indicate that, under certain conditions, raptor predation may limit gamebird populations and reduce gamebird harvests. However, the number and extent of such studies are too modest to draw firm conclusions. Furthermore, their geographical bias to northern Europe, where predator-prey communities are typically simpler than in the south, precludes extrapolation to more diverse southern European ecosystems. There is an urgent need to develop further studies, particularly in southern Europe, to determine the functional and numerical responses of raptors to gamebird populations in species and environments other than those already evaluated in existing studies. Furthermore, additional field experiments are needed in which raptor and possibly also mammalian predator numbers are manipulated on a sufficiently large spatial and temporal scale. Other aspects that have been little studied are the role of predation by the non-breeding part of the raptor population, or floaters, on the breeding success and survival of gamebirds, as well as the effect of intra-guild predation. Finally there is a need for further research on practical methods to reduce raptor predation on gamebirds and thus reduce conflict between raptor conservation and gamebird management.     

Predation risk in tadpole populations shapes behavioural responses of prey but not strength of trait‐mediated indirect interactions

Prey animals often respond to predators by reducing activity levels. This can produce a trait‐mediated indirect interaction (TMII) between predators and prey resources, whereby reduced foraging by prey in the presence of a predator causes an increase in prey resources. TMIIs play important roles in structuring communities, and it is important to understand factors that determine their strength. One such influence may be behavioural variation in the prey species, with indirect effects of predators being stronger within populations that are more responsive to the presence of a predator. We tested 1) whether the behavioural responsiveness of populations of wood frog tadpoles to predator cues was related to the predation risk in their native ponds, and 2) whether more responsive tadpoles yielded stronger TMIIs. To do this, we 1) measured the activity of tadpoles from 18 populations in mesocosms with and without caged predators, and 2) measured changes in the biomass of periphyton (the tadpoles’ diet) between predator treatments for each population. We found that tadpoles from higher predation risk ponds reduced their time outside refuges more in the presence of predators and tended to move less when visible, suggesting possible local adaptation to predation regimes. Though the presence of predators generally resulted in higher periphyton biomass – a TMII – there was no evidence that the strength of this TMII was affected by variation in tadpole behaviour. Foraging activity and general activity may be decoupled to some extent, enabling high predation risk‐adapted tadpoles to limit the fitness costs of reduced foraging when predators are present.     

Dying from the lesser of three evils: facilitation and non‐consumptive effects emerge in a model with multiple predators

Prey modify their behaviour to avoid predation, but dilemmas arise when predators vary in hunting style. Behaviours that successfully evade one predator sometimes facilitate exposure to another predator, forcing the prey to choose the lesser of two evils. In such cases, we need to quantify behavioural strategies in a mix of predators. We model optimal behaviour of Atlantic cod Gadus morhua larvae in a water column, and find the minimal vulnerability from three common predator groups with different hunting modes; 1) ambush predators that sit‐and‐wait for approaching fish larvae; 2) cruising invertebrates that eat larvae in their path; and 3) fish which are visually hunting predators. We use a state‐dependent model to find optimal behaviours (vertical position and swimming speed over a diel light cycle) under any given exposure to the three distinct modes of predation. We then vary abundance of each predator and quantify direct and indirect effects of predation. The nature and strength of direct and indirect effects varied with predator type and abundance. Larvae escaped about half the mortality from fish by swimming deeper to avoid light, but their activity level and cumulative predation from ambush predators increased. When ambush invertebrates dominated, it was optimal to be less active but in more lit habitats, and predation from fish increased. Against cruising predators, there was no remedy. In all cases, the shift in behaviour allowed growth to remain almost the same, while total predation were cut by one third. In early life stages with high and size‐dependent mortality rates, growth rate can be a poor measure of the importance of behavioural strategies.     

Predation across spatial scales in heterogeneous environments

A hierarchy of scales is introduced to the spatially heterogeneous Lotka-Volterra predator-prey diffusion model, and its effects on the model's spatial and temporal behavior are studied. When predators move on a large scale relative to prey, local coupling of the predator-prey interaction is replaced by global coupling. Prey with low dispersal ability become narrowly confined to the most productive habitats, strongly amplifying the underlying spatial pattern of the environment. As prey diffusion rate increases, the prey distribution spreads out and predator abundance declines. The model retains neutrally stable Lotka-Volterra temporal dynamics: different scales of predator and prey dispersal do not stabilize the interaction. The model predicts that, for prey populations that are limited by widely ranging predators, species with low dispersal ability should be restricted to discrete high density patches, and those with greater mobility should be more uniformly distributed at lower density.     

Experimental studies of evolution in guppies: a model for understanding the evolutionary consequences of predator removal in natural communities

Guppies (Poecilia reticulata) in Trinidadian streams are found with a diversity of predators in the lower reaches of streams, but few predators in the headwaters. These differences have caused the adaptive evolution of guppy behaviour, morphology, male colouration and life history. Waterfalls often serve as barriers to the upstream distribution of predators and/or guppies. Such discontinuities make it possible to treat streams like giant test tubes by introducing guppies or predators to small segments of streams from which they were previously excluded. Such experiments enable us to document how fast evolution can occur and the fine spatial scales over which adaptation is possible. They also demonstrate that the role predators play in structuring this ecosystem resembles many others studied from a more purely ecological perspective; in these streams, as elsewhere, predators depress the numbers of individuals in prey species which in turn reduces the effects of the prey species on other trophic levels and hence the structure of the ecosystem. A focus on predators is important in conservation biology because predators are often the organisms that are most susceptible to local extinction. Their selective loss occurs because large predators have been deliberately exterminated and/or are more susceptible to environmental disturbances. Furthermore, we will argue that predator re-introductions might be destabilizing if, in the absence of predators, their prey have evolved in a fashion that makes them highly susceptible to predation, even after time intervals as short as 50-100 years. A better understanding of the evolutionary impacts of top predators will be critical goal for the policy and practice of large carnivore restoration in the future.     

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.     

Mechanisms of coexistence in diverse herbivore–carnivore assemblages: demographic,temporal and spatial heterogeneities affecting prey vulnerability

Simple models coupling the dynamics of single predators to single prey populations tend to generate oscillatory dynamics of both predator and prey, or extirpation of the prey followed by that of the predator. In reality, such oscillatory dynamics may be counteracted by prey refugia or by opportunities for prey switching by the predator in multi‐prey assemblages. How these mechanisms operate depends on relative prey vulnerability, a factor ignored in simple interactive models. I outline how compositional, temporal, demographic and spatial heterogeneities help explain the contrasting effects of top predators on large herbivore abundance and population dynamics in species‐rich African savanna ecosystems compared with less species‐diverse northern temperate or subarctic ecosystems. Demographically, mortality inflicted by predation depends on the relative size and life history stage of the prey. Because all animals eventually die and are consumed by various carnivores, the additive component of the mortality inflicted is somewhat less than the predation rate. Prey vulnerability varies annually and seasonally, and between day and night. Spatial variation in the risk of predation depends on vegetation cover as well as on the availability of food resources. During times of food shortage, herbivores become prompted to occupy more risky habitats retaining more food. Predator concentrations dependent on the abundance of primary prey species may restrict the occurrence of other potential prey species less resistant to predation. The presence of multiple herbivore species of similar size in African savannas allows the top predator, the lion, to shift its prey selection flexibly dependent on changing prey vulnerability. Hence top–down and bottom–up influences on herbivore populations are intrinsically entangled. Models coupling the population dynamics of predators and prey need to accommodate the changing influences of prey demography, temporal variation in environmental conditions, and spatial variation in the relative vulnerability of alternative prey species to predation. Synthesis While re‐established predators have had major impacts on prey populations in northern temperate regions, multiple large herbivore species typically coexist along with diverse carnivores in African savanna ecosystems. In order to explain these contrasting outcomes, certain functional heterogeneities must be recognised, including relative vulnerability of alternative prey, temporal variation in the risk of predation, demographic differences in susceptibility to predation, and spatial contrasts in exposure to predation. Food shortfalls prompt herbivores to exploit more risky habitats, meaning that top–down and bottom–up influences on prey populations are intrinsically entangled. Models coupling the interactive dynamics of predator and prey populations need to incorporate these varying influences on relative prey vulnerability.     

The complex business of survival by aposematism

The theory of warning signals dates back to Wallace but is still confusing, controversial and complex. Because predator avoidance of warningly coloured prey (aposematism) is based upon learning and reinforcement, it is difficult to understand how initially rare conspicuous forms subsequently become common. Here, we discuss several possible resolutions to this apparent paradox. Many of these ideas have been largely ignored as a result of implicit assumptions about predator behaviour and assumed lack of variation in the predators, prey and the predation process. Considering the spatial and temporal variation in and mechanisms of behaviour of both predators and prey will make it easier to understand the process and evolution of aposematism.     

Modeling changes in predator functional response to prey across spatial scales

Extrapolation of predator functional responses from laboratory observations to the field is often necessary to predict predation rates and predator-prey dynamics at spatial and temporal scales that are difficult to observe directly. We use a spatially explicit individual-based model to explore mechanisms behind changes in functional responses when the scale of observation is increased. Model parameters were estimated from a predator-prey system consisting of the predator Delphastus catalinae (Coleoptera: Coccinellidae) and Bemisia tabaci biotype B (Hemiptera: Aleyrodidae) on tomato plants. The model explicitly incorporates prey and predator distributions within single plants, the search behavior of predators within plants, and the functional response to prey at the smallest scale of interaction (within leaflets) observed in the laboratory. Validation revealed that the model is useful in scaling up from laboratory observations to predation in whole tomato plants of varying sizes. Comparing predicted predation at the leaflet scale, as observed in laboratory experiments, with predicted predation on whole plants revealed that the predator functional response switches from type II within leaflets to type III within whole plants. We found that the magnitude of predation rates and the type of functional response at the whole plant scale are modulated by (1) the degree of alignment between predator and prey distributions and (2) predator foraging behavior, particularly the effect of area-concentrated search within plants when prey population density is relatively low. The experimental and modeling techniques we present could be applied to other systems in which active predators prey upon sessile or slow-moving species.     

Frequency-dependent predation and maintenance of prey polymorphism

In positive frequency-dependent predation, predation risk of an individual prey correlates positively with the frequency of that prey type. In a number of small-scale experiments individual predators have shown frequency-dependent behaviour, often leading to the conclusion that a population of such predators could maintain prey polymorphism. Using simulations, I studied the dynamics of frequency-dependent predation and prey polymorphism. The model suggests that persistence of prey polymorphism decreases with increasing number of predators that show frequency-dependent behaviour, questioning conclusions about polymorphism based on experiments with few predators. In addition, prey population size, prey crypsis, difference in crypsis between prey morphs and the way the behaviour was adjusted affected the persistence of polymorphism. Under some circumstances prey population remained polymorphic for a shorter time under frequency-dependent than under frequency-independent predation. This suggests that although positive frequency-dependent predator behaviour may maintain prey polymorphism, it is not a sufficient condition for persistent prey polymorphism.     

Predators alter the scaling of diversity in prey metacommunities

Although predator effects on the number of locally coexisting species are well understood, there are few formal predictions of how these local predator effects influence patterns of prey diversity at larger spatial scales. Building on the theory of island biogeography, we develop a simple model that describes how predators can alter the scaling of diversity in prey metacommunities and compares the effects of generalist and specialist predators on regional prey diversity. Generalist predators, which consume prey randomly with respect to species identity, are predicted to reduce α‐diversity and increase β‐diversity thereby maintaining regional diversity (γ‐diversity). Alternatively, specialist predators, which filter out prey species intolerant of predators, are predicted to reduce bothα‐diversity andβ‐diversity by causing the same prey species to be extirpated in each locality, resulting in regional prey species extinctions and lower γ‐diversity. These distinct effects of generalist and specialist predators on prey diversity at different spatial scales are uniquely shaped by the extent of predation within those metacommunities. Overall, our model results make general predictions for how different types of predators can differentially affect prey diversity across spatial scales, allowing a more complete understanding of the possible implications of predator eradications or introductions for biodiversity.     

Female blue tits with brighter yellow chests transfer more carotenoids to their eggs after an immune challenge

Predicting the consequences of predator biodiversity loss on prey requires an understanding of multiple predator interactions. Predators are often assumed to have independent and additive effects on shared prey survival; however, multiple predator effects can be non-additive if predators foraging together reduce prey survival (risk enhancement) or increase prey survival through interference (risk reduction). In marine communities, juvenile reef fish experience very high mortality from two predator guilds with very different hunting modes and foraging domains—benthic and pelagic predator guilds. The few previous predator manipulation studies have found or assumed that mortality is independent and additive. We tested whether interacting predator guilds result in non-additive prey mortality and whether the detection of such effects change over time as prey are depleted. To do so, we examined the roles of benthic and pelagic predators on the survival of a juvenile shoaling zooplanktivorous temperate reef fish, Trachinops caudimaculatus, on artificial patch reefs over 2 months in Port Phillip Bay, Australia. We observed risk enhancement in the first 7 days, as shoaling behaviour placed prey between predator foraging domains with no effective refuge. At day 14 we observed additive mortality, and risk enhancement was no longer detectable. By days 28 and 62, pelagic predators were no longer significant sources of mortality and additivity was trivial. We hypothesize that declines in prey density led to reduced shoaling behaviour that brought prey more often into the domain of benthic predators, resulting in limited mortality from pelagic predators. Furthermore, pelagic predators may have spent less time patrolling reefs in response to declines in prey numbers. Our observation of the changing interaction between predators and prey has important implications for assessing the role of predation in regulating populations in complex communities.     

Nonconsumptive effects in a multiple predator system reduce the foraging efficiency of a keystone predator

Many studies have demonstrated that the nonconsumptive effect (NCE) of predators on prey traits can alter prey demographics in ways that are just as strong as the consumptive effect (CE) of predators. Less well studied, however, is how the CE and NCE of multiple predator species can interact to influence the combined effect of multiple predators on prey mortality. We examined the extent to which the NCE of one predator altered the CE of another predator on a shared prey and evaluated whether we can better predict the combined impact of multiple predators on prey when accounting for this influence. We conducted a set of experiments with larval dragonflies, adult newts (a known keystone predator), and their tadpole prey. We quantified the CE and NCE of each predator, the extent to which NCEs from one predator alters the CE of the second predator, and the combined effect of both predators on prey mortality. We then compared the combined effect of both predators on prey mortality to four predictive models. Dragonflies caused more tadpoles to hide under leaf litter (a NCE), where newts spend less time foraging, which reduced the foraging success (CE) of newts. Newts altered tadpole behavior but not in a way that altered the foraging success of dragonflies. Our study suggests that we can better predict the combined effect of multiple predators on prey when we incorporate the influence of interactions between the CE and NCE of multiple predators into a predictive model. In our case, the threat of predation to prey by one predator reduced the foraging efficiency of a keystone predator. Consequently, the ability of a predator to fill a keystone role could be compromised by the presence of other predators.