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.     

Predator dispersal determines the effect of connectivity on prey diversity

Linking local communities to a metacommunity can positively affect diversity by enabling immigration of dispersal-limited species and maintenance of sink populations. However, connectivity can also negatively affect diversity by allowing the spread of strong competitors or predators. In a microcosm experiment with five ciliate species as prey and a copepod as an efficient generalist predator, we analysed the effect of connectivity on prey species richness in metacommunities that were either unconnected, connected for the prey, or connected for both prey and predator. Presence and absence of predator dispersal was cross-classified with low and high connectivity. The effect of connectivity on local and regional richness strongly depended on whether corridors were open for the predator. Local richness was initially positively affected by connectivity through rescue of species from stochastic extinctions. With predator dispersal, however, this positive effect soon turned negative as the predator spread over the metacommunity. Regional richness was unaffected by connectivity when local communities were connected only for the prey, while predator dispersal resulted in a pronounced decrease of regional richness. The level of connectivity influenced the speed of richness decline, with regional species extinctions being delayed for one week in weakly connected metacommunities. While connectivity enabled rescue of prey species from stochastic extinctions, deterministic extinctions due to predation were not overcome through reimmigration from predator-free refuges. Prey reimmigrating into these sink habitats appeared to be directly converted into increased predator abundance. Connectivity thus had a positive effect on the predator, even when the predator was not dispersing itself. Our study illustrates that dispersal of a species with strong negative effects on other community members shapes the dispersal-diversity relationship. When connections enable the spread of a generalist predator, positive effects of connectivity on prey species richness are outweighed by regional extinctions through predation.     

Human activity helps prey win the predator-prey space race

Predator-prey interactions, including between large mammalian wildlife species, can be represented as a "space race", where prey try to minimize and predators maximize spatial overlap. Human activity can also influence the distribution of wildlife species. In particular, high-human disturbance can displace large carnivore predators, a trait-mediated direct effect. Predator displacement by humans could then indirectly benefit prey species by reducing predation risk, a trait-mediated indirect effect of humans that spatially decouples predators from prey. The purpose of this research was to test the hypothesis that high-human activity was displacing predators and thus indirectly creating spatial refuge for prey species, helping prey win the "space race". We measured the occurrence of eleven large mammal species (including humans and cattle) at 43 camera traps deployed on roads and trails in southwest Alberta, Canada. We tested species co-occurrence at camera sites using hierarchical cluster and nonmetric multidimensional scaling (NMS) analyses; and tested whether human activity, food and/or habitat influenced predator and prey species counts at camera sites using regression tree analysis. Cluster and NMS analysis indicated that at camera sites humans co-occurred with prey species more than predator species and predator species had relatively low co-occurrence with prey species. Regression tree analysis indicated that prey species were three times more abundant on roads and trails with >32 humans/day. However, predators were less abundant on roads and trails that exceeded 18 humans/day. Our results support the hypothesis that high-human activity displaced predators but not prey species, creating spatial refuge from predation. High-human activity on roads and trails (i.e., >18 humans/day) has the potential to interfere with predator-prey interactions via trait-mediated direct and indirect effects. We urge scientist and managers to carefully consider and quantify the trait-mediated indirect effects of humans, in addition to direct effects, when assessing human impacts on wildlife and ecosystems.     

A native apex predator limits an invasive mesopredator and protects native prey: Tasmanian devils protecting bandicoots from cats

Apex predators can limit the abundance and behaviour of mesopredators, thereby reducing predation on smaller species. We know less about whether native apex predators are effective in suppressing invasive mesopredators, a major global driver of vertebrate extinctions. We use the severe disease‐induced decline of an apex predator, the Tasmanian devil, as a natural experiment to test whether devils limit abundance of invasive feral cats and in turn protect smaller native prey. Cat abundance was c. 58% higher where devils had declined, which in turn negatively affected a smaller native prey species. Devils had a stronger limiting effect on cats than on a native mesopredator, suggesting apex predators may have stronger suppressive effects on evolutionarily naive species than coevolved species. Our results highlight how disease in one species can affect the broader ecosystem. We show that apex predators not only regulate native species but can also confer resistance to the impacts of invasive populations. Apex predators could therefore be a powerful but underutilised tool to prevent biodiversity loss.     

Rarity of a top predator triggers continent-wide collapse of mammal prey: dingoes and marsupials in Australia

Top predators in terrestrial ecosystems may limit populations of smaller predators that could otherwise become over abundant and cause declines and extinctions of some prey. It is therefore possible that top predators indirectly protect many species of prey from excessive predation. This effect has been demonstrated in some small-scale studies, but it is not known how general or important it is in maintaining prey biodiversity. During the last 150 years, Australia has suffered the world's highest rate of mammal decline and extinction, and most evidence points to introduced mid-sized predators (the red fox and the feral cat) as the cause. Here, we test the idea that the decline of Australia's largest native predator, the dingo, played a role in these extinctions. Dingoes were persecuted from the beginning of European settlement in Australia and have been eliminated or made rare over large parts of the continent. We show a strong positive relationship between the survival of marsupials and the geographical overlap with high-density dingo populations. Our results suggest that the rarity of dingoes was a critical factor which allowed smaller predators to overwhelm marsupial prey, triggering extinction over much of the continent. This is evidence of a crucial role of top predators in maintaining prey biodiversity at large scales in terrestrial ecosystems and suggests that many remaining Australian mammals would benefit from the positive management of dingoes.     

Predator-prey interactions in a nonequilibrium context: the metapopulation approach to modeling "hide-and-seek" dynamics in a spatially explicit tri-trophic system

Predators and prey are usually heterogeneously distributed in space so that the ability of the predators to respond to the distribution of their prey may have a profound influence on the stability and persistence of a predator‐prey system. A special type of dynamics is “hide‐and‐seek” characterized by a high turnover rate of local populations of prey and predators, because once the predators have found a patch of prey they quickly overexploit it, whereupon the starving predators either should move to better places or die. Continued persistence of prey and predators thus hinges on a long‐term balance between local extinctions and founding of new subpopulations. The colonization rate depends on the rate of emigration from occupied patches and the likelihood of successfully arriving at a suitable new patch, while extinction rate depends on the local population dynamics. Since extinctions and colonizations are both discrete probabilistic events, these phenomena are most adequately modeled by means of a stochastic model. In order to demonstrate the qualitative differences between a deterministic and stochastic approach to population dynamics, a spatially explicit tritrophic predator‐prey model is developed in a deterministic and a stochastic version. The model is parameterized using data for the two‐spotted spider mite (Tetranychus urticae) and the phytoseiid mite predator Phytoseiulus persimilis inhabiting greenhouse cucumbers.
Simulations show that the deterministic and stochastic approaches yield different results. The deterministic version predicts that the populations will exhibit violent fluctuations, implying that the system is fundamentally unstable. In contrast, the stochastic version predicts that the two species will be able to coexist in spite of frequent local extinctions of both species, provided the system consists of a sufficiently large number of local populations. This finding is in agreement with experimental results. It is therefore concluded that demographic stochasticity in combination with dispersal is capable of producing and maintaining sufficient asynchrony between local populations to ensure long‐term regional (metapopulation) persistence.     

Early onset of secondary extinctions in ecological communities following the loss of top predators

The large vulnerability of top predators to human-induced disturbances on ecosystems is a matter of growing concern. Because top predators often exert strong influence on their prey populations their extinction can have far-reaching consequences for the structure and functioning of ecosystems. It has, for example, been observed that the local loss of a predator can trigger a cascade of secondary extinctions. However, the time lags involved in such secondary extinctions remain unexplored. Here we show that the loss of a top predator leads to a significantly earlier onset of secondary extinctions in model communities than does the loss of a species from other trophic levels. Moreover, in most cases time to secondary extinction increases with increasing species richness. If local secondary extinctions occur early they are less likely to be balanced by immigration of species from local communities nearby. The implications of these results for community persistence and conservation priorities are discussed.     

Relative significance of direct and indirect effects of predation by planktivorous fish on zooplankton

One of the most obvious features of tropical lakes and reservoirs is the small body size of their zooplankton taxa. It is believed that this is the result of high and persistent predation by abundant planktivorous fish, which select large-bodied zooplankton prey thus making them more vulnerable to extinction in tropical as compared to temperate habitats. Do these extinctions result directly from fish predation? Could the high predation-induced mortality alone be responsible for an extermination of the population from a habitat? Or could indirect effects of predation be responsible? Some important indirect effects can be seen at the demographic level; these include reduced reproduction in the population resulting from higher vulnerability of ovigerous females to predation by visually oriented planktivores. Other important indirect effects can be observed at the individual level; these include shifts in behavior (from foraging to predator avoidance) and adjustments in physiology (from high to low feeding rate) in those planktonic animals which detect danger from their predators by sensing either the ‘predator odor’ or an ‘alarm substance’ originating from injured conspecific prey. Although a zooplankton species density may mostly result from the brutal force of direct predator impact on the population (mortality), it is more likely that its distribution in time and space could be attributed to a combination of indirect effects of predation on individual behavior and physiology. An example of periodicity in density and depth distribution patterns of Cahora Bassa zooplankton species and their periodic exterminations seems to confirm the role of indirect effects of predation by planktivorous fish.     

Recognition of non-native peacock bass, <Emphasis Type="Italic">Cichla kelberi</Emphasis> by native prey: testing the naiveté hypothesis

Prey naiveté is proposed as one of the main reasons behind species extinctions attributed to invasive predators. This study examined whether the naiveté hypothesis could explain extinctions after the introduction of peacock bass (Cichla kelberi) in Paraná River, Brazil. Our results show that prey responded to both visual and chemical cues of peacock bass. Displayed avoidance behaviors were equal to or greater than those observed with a native predator, Hoplias malabaricus. We conclude that lack of recognition was not responsible for the observed vulnerability of native species to this introduced predator. Finally, we discuss implications of these findings for the native biodiversity and convene other potential explanations for the observed effects of peacock bass on native prey.     

Disease in group-defending prey can benefit predators

Infectious diseases have the capacity not only to influence the host population but also to interacting species like predators. In particular, they can reduce host densities, which can have knock-on effects on predators. Here, we consider how an infectious disease in the prey affects the predator–prey relationship where the prey exhibit some kind of group defence against the predator (using a Holling type IV functional response). We find that the disease can reduce prey densities to levels where the group defence is weaker. This weakened group defence allows predators to survive in many situations where they could not without the disease.     

ORGANIZATION OF PREDATOR-PREY COMMUNITIES AS AN EVOLUTIONARY GAME

We consider a simple predator-prey model of coevolution. By allowing coevolution both within and between trophic levels the model breaks the traditional dichotomy between coevolution among competitors and coevolution between a prey and its predator. By allowing the diversity of prey and predator species to emerge as a property of the evolutionarily stable strategies (ESS), the model breaks another constraint of most approaches to coevolution that consider as fixed the number of coevolving species. The number of species comprising the ESS is influenced by a parameter that determines the predator's niche breadth. Depending upon the parameter's value the ESS may contain: 1) one prey and one predator species, 2) two prey and one predator, 3) two prey and two predators, 4) three prey and two predators, 5) three prey and three predators, etc. Evolutionarily, these different ESSs all emerge from the same model. Ecologically, however, these ESSs result in very different patterns of community organization. In some communities the predator species are ecologically keystone in that their removal results in extinctions among the prey species. In others, the removal of a predator species has no significant impact on the prey community. These varied ecological roles for the predator species contrasts sharply with the essential evolutionary role of the predators in promoting prey species diversity. The ghost of predation past in which a predator's insignificant ecological role obscures its essential evolutionary role may be a frequent property of communities of predator and prey.     

Trophic cascades: the primacy of trait-mediated indirect interactions

Trophic cascades are textbook examples of predator indirect effects on ecological systems. Yet there is considerable debate about their nature, strength and overall importance. This debate stems in part from continued uncertainty about the ultimate mechanisms driving cascading effects. We present a synthesis of empirical evidence in support of one possible ultimate mechanism: the foraging‐predation risk trade‐offs undertaken by intermediary species. We show that simple trade‐off behaviour can lead to both positive and negative indirect effects of predators on plant resources and hence can explain considerable contingency on the nature and strength of cascading effects among systems. Thus, predicting the sign and strength of indirect effect simply requires knowledge of habitat and resource use by prey with regard to predators’ presence, habitat use and hunting mode. The synthesis allows us to postulate a hypothesis for new conceptualization of trophic cascades which is to be viewed as an ultimate trade‐off between intervening species. In this context, different predators apply different rules of engagement based on their hunting mode and habitat use. These different rules then determine whether behavioural effects persist or attenuate at the level of the food chain.     

Reappraisal of the role of big,fierce predators!

The suggestion in the early 20th century that top predators were a necessary component of ecosystems because they hold herbivore populations in check and promote biodiversity was at first accepted and then largely rejected. With the advent of Evolutionary Ecology and a more full appreciation of direct and indirect effects of top predators, this role of top predators is again gaining acceptance. The previous views were predicated upon lethal effects of predators but largely overlooked their non-lethal effects. We suggest that conceptual advances coupled with an increased use of experiments have convincingly demonstrated that prey experience costs that transcend the obvious cost of death. Prey species use adaptive behaviours to avoid predators, and these behaviours are not cost-free. With predation risk, prey species greatly restrict their use of available habitats and consumption of available food resources. Effects of top predators consequently cascade down to the trophic levels below them. Top predators, the biggies, are thus both the targets of and the means for conservation at the landscape scale.     

Predator–prey naïveté, antipredator behavior,and the ecology of predator invasions

We present a framework for explaining variation in predator invasion success and predator impacts on native prey that integrates information about predator–prey naïveté, predator and prey behavioral responses to each other, consumptive and non‐consumptive effects of predators on prey, and interacting effects of multiple species interactions. We begin with the ‘naïve prey’ hypothesis that posits that naïve, native prey that lack evolutionary history with non‐native predators suffer heavy predation because they exhibit ineffective antipredator responses to novel predators. Not all naïve prey, however, show ineffective antipredator responses to novel predators. To explain variation in prey response to novel predators, we focus on the interaction between prey use of general versus specific cues and responses, and the functional similarity of non‐native and native predators. Effective antipredator responses reduce predation rates (reduce consumptive effects of predators, CEs), but often also carry costs that result in non‐consumptive effects (NCEs) of predators. We contrast expected CEs versus NCEs for non‐native versus native predators, and discuss how differences in the relative magnitudes of CEs and NCEs might influence invasion dynamics. Going beyond the effects of naïve prey, we discuss how the ‘naïve prey’, ‘enemy release’ and ‘evolution of increased competitive ability’ (EICA) hypotheses are inter‐related, and how the importance of all three might be mediated by prey and predator naïveté. These ideas hinge on the notion that non‐native predators enjoy a ‘novelty advantage’ associated with the naïveté of native prey and top predators. However, non‐native predators could instead suffer from a novelty disadvantage because they are also naïve to their new prey and potential predators. We hypothesize that patterns of community similarity and evolution might explain the variation in novelty advantage that can underlie variation in invasion outcomes. Finally, we discuss management implications of our framework, including suggestions for managing invasive predators, predator reintroductions and biological control.     

Non-interactive multiple predator effects on tadpole survival

Interactions among and within three species of predators were estimated in terms of their effects on prey survival using short-term predation experiments. The prey were tadpoles (Rana temporaria), and the predators were dragonfly larvae (Anax imperator), newts (Triturus alpestris), and backswimmers (Notonecta glauca). Mortality rate per predator imposed by Triturus and Notonecta did not decline with predator density, whereas the predation rate of Anax was strongly reduced when the number of predator individuals increased. Impacts of all three predators were not altered by the presence of other species in pairwise combinations. This system is therefore characterized by interference between individual dragonflies but relatively independent effects of predator species. These results were largely predictable based on the natural history of the predators and are encouraging for attempts to model communities as assemblages of interacting species.     

Positive indirect effects in a coral reef fish community

Indirect effects occur when two species interact through one or more intermediate species. Theoretical studies indicate that indirect interactions between two prey types that share common predators can be positive, neutral or negative. We document a positive indirect interaction between different types of prey fish on coral reefs in Australia. A high abundance of one type of prey fish (cardinalfishes: Apogonidae) resulted in higher recruitment, abundance and species richness of other prey fish. Our evidence indicates that these effects were not due to differential settlement but were instead due to differential post-settlement predation. We hypothesize that resident piscivores altered their foraging behaviour by concentrating on highly abundant cardinal-fish when they were present, leaving recruits of other species relatively unmolested. Indirect effects were evident within 48 h of settlement and persisted throughout the 42-day experiment, highlighting the importance of early post-settlement processes in these communities.     

Direct and indirect effects of an introduced piscivore, <Emphasis Type="Italic">Cichla kelberi</Emphasis> and their modification by aquatic plants

The non-native peacock bass (Cichla kelberi) is causing freshwater fish extinctions in the tropical regions around the world, but there are very few studies on its interaction with native species. This study, based on a mesocosm experiment, examined direct and indirect effects of a non-native peacock bass on the native prey in Paraná River, Brazil, and tested whether these effects were mitigated by aquatic vegetation. Feeding activity of most prey was unaffected by the presence of peacock bass. All prey were consumed in the absence of vegetation; whereas a marginally significant decrease in mortality was observed in the vegetated habitats. Overall, peacock bass had minor indirect effects on prey foraging, but very significant direct effects on prey survival. As aquatic plants provide very limited protection to native prey, vegetated habitats are unlikely to slow down the decline in biodiversity resulting from this invasive species and conservation measures may need to consider other ways to ensure survival of the source populations.     

Predicting ecological consequences of marine top predator declines

Recent studies document unprecedented declines in marine top predators that can initiate trophic cascades. Predicting the wider ecological consequences of these declines requires understanding how predators influence communities by inflicting mortality on prey and inducing behavioral modifications (risk effects). Both mechanisms are important in marine communities, and a sole focus on the effects of predator-inflicted mortality might severely underestimate the importance of predators. We outline direct and indirect consequences of marine predator declines and propose an integrated predictive framework that includes risk effects, which appear to be strongest for long-lived prey species and when resources are abundant. We conclude that marine predators should be managed for the maintenance of both density- and risk-driven ecological processes, and not demographic persistence alone.     

Multi-predator effects across life-history stages: non-additivity of egg- and larval-stage predation in an African treefrog

The effects of multiple predators on their prey are frequently non‐additive because of interactions among predators. When prey shift habitats through ontogeny, many of their predators cannot interact directly. However, predators that occur in different habitats or feed on different prey stages may still interact through indirect effects mediated by prey traits and density. We conducted an experiment to evaluate the combined effects of arboreal egg‐stage and aquatic larval‐stage predators of the African treefrog, Hyperolius spinigularis. Egg and larval predator effects were non‐additive – more Hyperolius survived both predators than predicted from their independent effects. Egg‐stage predator effects on aquatic larval density and size and age at hatching reduced the effectiveness of larval‐stage predators by 70%. Our results indicate that density‐ and trait‐mediated indirect interactions can act across life‐stages and habitats, resulting in non‐additive multi‐predator effects.     

Food web structure and the strength of transient indirect effects

The relative importance of direct and indirect effects in ecological communities remains unresolved. Indirect effects may diminish as they propagate through highly reticulate food webs. We tested this hypothesis by assembling replicate food webs of different complexity in laboratory microcosms, and comparing the transmission of indirect effects through these webs. By providing the top predator ( Didinium ) with either one ( Paramecium ) or two ( Paramecium and Colpidium ) species of protists as prey, we created linear or reticulate food webs where we could examine the transient response of predators to an indirect effect. Addition of Chlamydomonas , a small alga consumed by Paramecium , but not by Colpidium , perturbed the system and generated an indirect effect on Didinium . We expected the proportional response of Didinium to Chlamydomonas addition would be smaller in the reticulate web containing alternative, unperturbed prey ( Colpidium ). We measured predator response as predator yield, the maximum number of predators produced prior to overexploitation of prey and subsequent predator decline. The ratio of yield in perturbed bottles to yield in unperturbed bottles measures the proportional response of Didinium to Chlamydomonas addition. We expected this ratio to be smaller with Colpidium present. Contrary to expectations, alternative prey enhanced rather than diminished predator response to the perturbation. This resulted from competition between the prey species, a factor ignored in some simple verbal arguments. Food web complexity may have unanticipated consequences for the strength of indirect effects.