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.     

Predation on elasmobranch eggs

Synopsis Predation on large, energy rich eggs is common in terrestrial and freshwater communities with the eggs of amphibians, reptiles and birds figuring as prominant prey. We might predict that predation on large eggs would also be widespread in marine communities. However, little information is available to test this prediction. We present new evidence for such predation on elasmobranch eggs based on examination of capsules held in museum collections, those collected from beaches, long-term incubations of caged egg capsules, and SCUBA observation. The principal egg predators appear to be gastropods, though vertebrates contribute to mortality of embryonic elasmobranchs. As yet we can only speculate about the effects of egg predation for populations of oviparous elasmobranchs, or about the direct and indirect consequences predation upon their energy-rich eggs may have for marine communities.     

Predator identity and consumer behavior: differential effects of fish and crayfish on the habitat use of a freshwater snail

Predators can alter the outcome of ecological interactions among other members of the food web through their effects on prey behavior. While it is well known that animals often alter their behavior with the imposition of predation risk, we know less about how other features of predators may affect prey behavior. For example, relatively few studies have addressed the effects of predator identity on prey behavior, but such knowledge is crucial to understanding food web interactions. This study contrasts the behavioral responses of the freshwater snail Physellagyrina to fish and crayfish predators. Snails were placed in experimental mesocosms containing caged fish and crayfish, so the only communication between experimental snails and their predators was via non-visual cues. The caged fish and crayfish were fed an equal number of snails, thereby simulating equal prey mortality rates. In the presence of fish, the experimental snails moved under cover, which confers safety from fish predators. However, in the presence of crayfish, snails avoided benthic cover and moved to the water surface. Thus, two species of predators, exerting the same level of mortality on prey, induced very different behavioral responses. We predict that these contrasting behavioral responses to predation risk have important consequences for the interactions between snails and their periphyton resources. Received: 1 June 1998 / Accepted: 12 October 1998     

Not worth the risk: apex predators suppress herbivory on coral reefs

Apex predators are known to exert strong ecological effects, either through direct or indirect predator–prey interactions. Indirect interactions have the potential to influence ecological communities more than direct interactions as the effects are propagated throughout the population as opposed to only one individual. Indirect effects of apex predators are well documented in terrestrial environments, however there is a paucity of information for marine environments. Furthermore, manipulative studies, as opposed to correlative observations, isolating apex predator effects are lacking. Coral reefs are one of the most diverse ecosystems, providing a useful model system for investigating the ecological role of apex predators and their influence on lower trophic levels. Using predator models and transplanted macroalgae we examined the indirect effects of predators on herbivore foraging behaviour. We show that the presence of a model reef shark or large coral‐grouper led to a substantial reduction in bite rate and species richness of herbivorous fishes and an almost absolute localized cessation of macroagal removal, due to the perceived risk of predation. A smaller‐sized coral‐grouper also reduced herbivore diversity and activity but to a lesser degree than the larger model predators. These indirect effects of apex predators on the foraging behaviour of herbivores may have flow‐on effects on the biomass and distribution of macroalgae, and the functioning of coral reef ecosystems. This highlights that the ecological interactions and processes that contribute to ecosystem resilience may be more complex than previously assumed.     

Multiple intraguild predators reduce mortality risk of a mutual agricultural pest prey in simple,but not in complex,experimental settings

Multiple predator species that coexist with each other and their mutual prey can have combined effects on prey mortality that are similar to the sum of each predator's individual impact (linear effects), greater than the sum of each predator's individual impact (risk enhancement), or less than the sum of each predator's individual impact (risk reduction). Understanding multiple predator effects is important to determine the impact of predators on pest prey in agroecosystems. If two predators share the same broad spatial domain and hunting mode and engage in intraguild predation, then their combination is expected to result in risk reduction for a mutual prey. We tested this hypothesis using both additive and replacement experimental designs on two species of generalist wolf spider predators (Tasmanicosa leuckartii and Hogna crispipes) that hunt in the same domain, and a mutual insect prey (cotton bollworm Helicoverpa armigera). We used two types of enclosures: a small simple laboratory enclosure, and a larger more complex cotton plant enclosure. We found that in the small simple laboratory enclosures, the presence of two spiders led to risk reduction of Helicoverpa larva mortality as expected, but in larger more complex cotton plant enclosures the presence of both species resulted in linear effects rather than risk reduction on Helicoverpa mortality. Furthermore, intraguild predation did not change multiple predator effects in laboratory or plant enclosures. This study has implications for managing arthropod predators in agroecosystems; contrary to predictions of ecological frameworks, coexistence of predators that share the same hunting mode and hunting domain may not lead to risk reduction on a mutual prey in more complex environments, where encounters among predators can be lower. Conservation of multiple predators of a single guild can play an essential role on biological control of insect pests.     

The long‐term impacts of predators on prey: inducible defenses,population dynamics,and indirect effects

Despite the amount of research on the inducible defenses of prey against predators, our understanding of the long‐term significance of non‐lethal predators on prey phenotypes, prey population dynamics, and community structure has rarely been explored. Our objectives were to assess the effects of predators on prey defenses, prey population dynamics, and the relative magnitude of density‐ versus trait‐mediated indirect interactions (DMIIs and TMIIs) over multiple prey generations. Using a freshwater snail and three common snail predators, we constructed a series of community treatments with pond mesocosms that manipulated trophic structure, the identity of the top predator, and whether predators were caged or uncaged. We quantified snail phenotypes, snail population size, and resource abundance over multiple snail generations. We found that snails were expressing inducible defenses in our system although the magnitude of the responses varied over time and across predator species. Despite the expression of inducible defenses, caged predators did not reduce snail population size. There also was no evidence of TMIIs throughout the experiment suggesting that TMIIs have a minimal role in the long‐term structure of our communities. The absence of TMIIs was largely driven by the lack of predator‐induced reductions in resource consumption and the lack of consistent reductions in population size with predator cues. In contrast, we detected strong DMIIs associated with lethal predators suggesting that DMIIs are the dominant long‐term mechanism influencing community structure. Our results demonstrate that although predators can have significant effects on prey phenotypes and sometimes cause short‐term TMIIs, there may be few long‐term consequences of these responses on population dynamics and indirect interactions, at least within simple food webs. Research directed towards addressing the long‐term consequences of predator–prey interactions within communities will help to reveal whether the conclusions and predictions generated from short‐term experiments are applicable over ecological and evolutionary timescales.     

Predator density and the functional responses of coral reef fish

Predation is a key process driving coral reef fish population dynamics, with higher per capita prey mortality rates on reefs with more predators. Reef predators often forage together, and at high densities, they may either cooperate or antagonize one another, thereby causing prey mortality rates to be substantially higher or lower than one would expect if predators did not interact. However, we have a limited mechanistic understanding of how prey mortality rates change with predator densities. We re-analyzed a previously published observational dataset to investigate how the foraging response of the coney grouper (Cephalopholis fulva) feeding on the bluehead wrasse (Thalassoma bifasciatum) changed with shifts in predator and prey densities. Using a model-selection approach, we found that per-predator feeding rates were most consistent with a functional response that declines as predator density increases, suggesting either antagonistic interactions among predators or a shared antipredator behavioral response by the prey. Our findings suggest that variation in predator density (natural or anthropogenic) may have substantial consequences for coral reef fish population dynamics.     

Proximate composition,energetic value,and relative abundance of prey fish from the inshore eastern Bering Sea: implications for piscivorous predators

Changing ocean conditions and subsequent shifts in forage fish communities have been linked to numerical declines of some piscivorous marine birds and mammals in the North Pacific. However, limited information about fish communities is available for some regions, including nearshore waters of the eastern Bering Sea, where many piscivores reside. We determined proximate composition and energetic value of a suite of potential forage fish collected from an estuary on the Yukon-Kuskokwim Delta, Alaska, during 2002 and 2003. Across species, energy density ranged from 14.5 to 20.7 kJ g⁻¹ dry mass and varied primarily as a function of lipid content. Total energy content was strongly influenced by body length and we provide species-specific predictive models of total energy based on this relationship; some models may be improved further by incorporating year and date effects. Based on observed energetic differences, we conclude that variation in fish size, quantity, and species composition of the prey community could have important consequences for piscivorous predators.     

Seascapes of fear: evaluating sublethal predator effects experienced and generated by marine mammals

The notion that predators can affect their prey without killing them is widely supported in the ecological literature yet rarely applied by marine mammal studies. We present three case studies in which patterns of time allocation by individual marine mammal foragers were used to index the sublethal effects of predators on bottlenose dolphins (Tursiops sp.), harbor seals (Phoca vitulina), and dugongs (Dugong dugon). In each case, foraging individuals optimized energy gain and safety from predators by spending less time in more profitable but dangerous patches or decreasing their use of risky feeding tactics that would increase net energy gain. By implication, marine mammals are subject to the non consumptive effects of their predators (i.e., to intimidation), and fear can mediate their impacts on their resources. We suggest, therefore, that future studies quantify patterns of time allocation to measure sublethal effects of predators on marine mammals, as well as the capacity of marine mammals to have sublethal effects on their own prey. We argue that such an approach is important because non consumptive effects may be of greater magnitude than lethal effects of predators, and information on sublethal effects of predators can inform conservation plans and studies of community structure.     

Mammalian mesopredators on islands directly impact both terrestrial and marine communities

Medium-sized mammalian predators (i.e. mesopredators) on islands are known to have devastating effects on the abundance and diversity of terrestrial vertebrates. Mesopredators are often highly omnivorous, and on islands, may have access not only to terrestrial prey, but to marine prey as well, though impacts of mammalian mesopredators on marine communities have rarely been considered. Large apex predators are likely to be extirpated or absent on islands, implying a lack of top-down control of mesopredators that, in combination with high food availability from terrestrial and marine sources, likely exacerbates their impacts on island prey. We exploited a natural experiment—the presence or absence of raccoons (Procyon lotor) on islands in the Gulf Islands, British Columbia, Canada—to investigate the impacts that this key mesopredator has on both terrestrial and marine prey in an island system from which all native apex predators have been extirpated. Long-term monitoring of song sparrow (Melospiza melodia) nests showed raccoons to be the predominant nest predator in the Gulf Islands. To identify their community-level impacts, we surveyed the distribution of raccoons across 44 Gulf Islands, and then compared terrestrial and marine prey abundances on six raccoon-present and six raccoon-absent islands. Our results demonstrate significant negative effects of raccoons on terrestrial, intertidal, and shallow subtidal prey abundance, and point to additional community-level effects through indirect interactions. Our findings show that mammalian mesopredators not only affect terrestrial prey, but that, on islands, their direct impacts extend to the surrounding marine community.     

Do Behavioral Foraging Responses of Prey to Predators Function Similarly in Restored and Pristine Foodwebs?

Efforts to restore top predators in human-altered systems raise the question of whether rebounds in predator populations are sufficient to restore pristine foodweb dynamics. Ocean ecosystems provide an ideal system to test this question. Removal of fishing in marine reserves often reverses declines in predator densities and size. However, whether this leads to restoration of key functional characteristics of foodwebs, especially prey foraging behavior, is unclear. The question of whether restored and pristine foodwebs function similarly is nonetheless critically important for management and restoration efforts. We explored this question in light of one important determinant of ecosystem function and structure--herbivorous prey foraging behavior. We compared these responses for two functionally distinct herbivorous prey fishes (the damselfish Plectroglyphidodon dickii and the parrotfish Chlorurus sordidus) within pairs of coral reefs in pristine and restored ecosystems in two regions of these species' biogeographic ranges, allowing us to quantify the magnitude and temporal scale of this key ecosystem variable's recovery. We demonstrate that restoration of top predator abundances also restored prey foraging excursion behaviors to a condition closely resembling those of a pristine ecosystem. Increased understanding of behavioral aspects of ecosystem change will greatly improve our ability to predict the cascading consequences of conservation tools aimed at ecological restoration, such as marine reserves.     

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.     

Eco-evolutionary trophic dynamics: loss of top predators drives trophic evolution and ecology of prey

Ecosystems are being altered on a global scale by the extirpation of top predators. The ecological effects of predator removal have been investigated widely; however, predator removal can also change natural selection acting on prey, resulting in contemporary evolution. Here we tested the role of predator removal on the contemporary evolution of trophic traits in prey. We utilized a historical introduction experiment where Trinidadian guppies (Poecilia reticulata) were relocated from a site with predatory fishes to a site lacking predators. To assess the trophic consequences of predator release, we linked individual morphology (cranial, jaw, and body) to foraging performance. Our results show that predator release caused an increase in guppy density and a "sharpening" of guppy trophic traits, which enhanced food consumption rates. Predator release appears to have shifted natural selection away from predator escape ability and towards resource acquisition ability. Related diet and mesocosm studies suggest that this shift enhances the impact of guppies on lower trophic levels in a fashion nuanced by the omnivorous feeding ecology of the species. We conclude that extirpation of top predators may commonly select for enhanced feeding performance in prey, with important cascading consequences for communities and ecosystems.     

Non‐additive effects of simulated heat waves and predators on prey phenotype and transgenerational phenotypic plasticity

Understanding the effects of extreme climatic events on species and their interactions is of paramount importance for predicting and mitigating the impacts of climate change on communities and ecosystems. However, the joint effects of extreme climatic events and species interactions on the behaviour and phenotype of organisms remain poorly understood, leaving a substantial gap in our knowledge on the impacts of climatic change on ecological communities. Using an aphid–ladybeetle system, we experimentally investigated the effects of predators and heat shocks on prey body size, microhabitat use, and transgenerational phenotypic plasticity (i.e., the asexual production of winged offspring by unwinged mothers). We found that (i) aphids were smaller in the presence of predators but larger when exposed to frequent heat shocks; (ii) frequent heat shocks shifted aphid distribution towards the plant's apex, but the presence of predators had the opposite effect and dampened the heat‐shock effects; and (iii) aphids responded to predators by producing winged offspring, but heat shocks strongly inhibited this transgenerational response to predation. Overall, our experimental results show that heat shocks inhibit phenotypic and behavioural responses to predation (and vice versa) and that such changes may alter trophic interactions, and have important consequences on the dynamics and stability of ecological communities. We conclude that the effects of extreme climatic events on the phenotype and behaviour of interacting species should be considered to understand the effects of climate change on species interactions and communities.     

Climate change enhances the negative effects of predation risk on an intermediate consumer

Predators are a major source of stress in natural systems because their prey must balance the benefits of feeding with the risk of being eaten. Although this ‘fear’ of being eaten often drives the organization and dynamics of many natural systems, we know little about how such risk effects will be altered by climate change. Here, we examined the interactive consequences of predator avoidance and projected climate warming in a three‐level rocky intertidal food chain. We found that both predation risk and increased air and sea temperatures suppressed the foraging of prey in the middle trophic level, suggesting that warming may further enhance the top‐down control of predators on communities. Prey growth efficiency, which measures the efficiency of energy transfer between trophic levels, became negative when prey were subjected to predation risk and warming. Thus, the combined effects of these stressors may represent an important tipping point for individual fitness and the efficiency of energy transfer in natural food chains. In contrast, we detected no adverse effects of warming on the top predator and the basal resources. Hence, the consequences of projected warming may be particularly challenging for intermediate consumers residing in food chains where risk dominates predator‐prey interactions.     

Comparative Feeding Ecology of Bull Sharks (Carcharhinus leucas) in the Coastal Waters of the Southwest Indian Ocean Inferred from Stable Isotope Analysis

As apex predators, sharks play an important role shaping their respective marine communities through predation and associated risk effects. Understanding the predatory dynamics of sharks within communities is, therefore, necessary to establish effective ecologically based conservation strategies. We employed non-lethal sampling methods to investigate the feeding ecology of bull sharks (Carcharhinus leucas) using stable isotope analysis within a subtropical marine community in the southwest Indian Ocean. The main objectives of this study were to investigate and compare the predatory role that sub-adult and adult bull sharks play within a top predatory teleost fish community. Bull sharks had significantly broader niche widths compared to top predatory teleost assemblages with a wide and relatively enriched range of δ¹³C values relative to the local marine community. This suggests that bull sharks forage from a more diverse range of δ¹³C sources over a wider geographical range than the predatory teleost community. Adult bull sharks appeared to exhibit a shift towards consistently higher trophic level prey from an expanded foraging range compared to sub-adults, possibly due to increased mobility linked with size. Although predatory teleost fish are also capable of substantial migrations, bull sharks may have the ability to exploit a more diverse range of habitats and appeared to prey on a wider diversity of larger prey. This suggests that bull sharks play an important predatory role within their respective marine communities and adult sharks in particular may shape and link ecological processes of a variety of marine communities over a broad range.     

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.     

Reinforcing effects of non-pathogenic bacteria and predation risk: from physiology to life history

The important ecological role of predation risk in shaping populations, communities and ecosystems is becoming increasingly clear. In this context, synergistic effects between predation risk and other natural stressors on prey organisms are gaining attention. Although non-pathogenic bacteria can be widespread in aquatic ecosystems, their role in mediating effects of predation risk has been ignored. We here address the hypothesis that non-pathogenic bacteria may reinforce the negative effects of predation risk in larvae of the damselfly Coenagrion puella. We found synergistic effects for all three life history variables studied: mortality increased, growth reductions were magnified and bacterial load was higher when both non-lethal stressors were combined. The combined exposure to the bacterium and predation risk considerably impaired the two key antipredator mechanisms of the damselfly larvae: they no longer reduced their food intake under predation risk and showed a synergistic reduction in escape swimming speed. The reinforcing negative effects on the fitness-related traits could be explained by the observed synergistic effects on food intake, swimming muscle mass, immune function and oxidative damage. These are likely widespread consequences of energetic constraints and increased metabolic rates associated with the fight-or-flight response. We therefore hypothesize that the here documented synergistic interactions with non-pathogenic bacteria may be widespread. Our results highlight the ignored ecological role of non-pathogenic bacteria in reinforcing the negative effects of predation risk on prey organisms.     

Biodiversity effects of the predation gauntlet

The ubiquity of trophic downgrading has led to interest in the consequences of mesopredator release on prey communities and ecosystems. This issue is of particular concern for reef-fish communities, where predation is a key process driving ecological and evolutionary dynamics. Here, we synthesize existing experiments that have isolated the effects of mesopredators to quantify the role of predation in driving changes in the abundance and biodiversity of recently settled reef fishes. On average, predators reduced prey abundance through generalist foraging behavior, which, through a statistical sampling artifact, caused a reduction in alpha diversity and an increase in beta diversity. Thus, the synthesized experiments provide evidence that predation reduces overall abundance within prey communities, but—after accounting for sampling effects—does not cause disproportionate effects on biodiversity.

     

Top predators provide insurance against climate change

Recent research by Wilmers et al. shows that top predators might buffer some of the ecological effects of climate change. Top predators can regulate the structure of entire communities and dampen their variability; however, in their absence, prey populations are likely to fluctuate greatly owing to bottom-up factors. Restoring top predators to their natural environment could provide insurance against undesired effects of climate change on ecological communities.