Amphipod (Gammarus minus) responses to predators and predator impact on amphipod density

Recent theoretical work suggests that predator impact on local prey density will be the result of interactions between prey emigration responses to predators and predator consumption of prey. Whether prey increase or decrease their movement rates in response to predators will greatly influence the impact that predators have on prey density. In stream systems the type of predator, benthic versus water-column, is expected to influence whether prey increase or decrease their movement rates. Experiments were conducted to examine the response of amphipods (Gammarus minus) to benthic and water-column predators and to examine the interplay between amphipod response to predators and predator consumption of prey in determining prey density. Amphipods did not respond to nor were they consumed by the benthic predator. Thus, this predator had no impact on amphipod density. In contrast, amphipods did respond to two species of water-column predators (the predatory fish bluegills, Lepomis macrochirus, and striped shiners, Luxilus chrysocephalus) by decreasing their activity rates. This response led to similar positive effects on amphipod density at night by both species of predatory fish. However, striped shiners did not consume many amphipods, suggesting their impact on the whole amphipod “population” was zero. In contrast, bluegills consumed a significant number of amphipods, and thus had a negative impact on the amphipod “population”. These results lend support to theoretical work which suggests that prey behavioral responses to predators can mask the true impact that predators have on prey populations when experiments are conducted at small scales. Received: 21 March 1997 / Accepted: 15 December 1997     

Overcoming prey naiveté: Free‐living marsupials develop recognition and effective behavioral responses to alien predators in Australia

Naiveté in prey arises from novel ecological mismatches in cue recognition systems and antipredator responses following the arrival of alien predators. The multilevel naiveté framework suggests that animals can progress through levels of naiveté toward predator awareness. Alternatively, native prey may be preadapted to recognize novel predators via common constituents in predator odors or familiar predator archetypes. We tested predictions of these competing hypotheses on the mechanisms driving behavioral responses of native species to alien predators by measuring responses of native free‐living northern brown bandicoots (Isoodon macrourus) to alien red fox (Vulpes vulpes) odor. We compared multiple bandicoot populations either sympatric or allopatric with foxes. Bandicoots sympatric with foxes showed recognition and appropriate antipredator behavior toward fox odor via avoidance. On the few occasions bandicoots did visit, their vigilance significantly increased, and their foraging decreased. In contrast, bandicoots allopatric with foxes showed no recognition of this predator cue. Our results suggest that vulnerable Australian mammals were likely naïve to foxes when they first arrived, which explains why so many native mammals declined soon after fox arrival. Our results also suggest such naiveté can be overcome within a relatively short time frame, driven by experience with predators, thus supporting the multilevel naiveté framework.     

Antipredator Responses by Native Mosquitofish to Non-Native Cichlids: An Examination of the Role of Prey Naiveté

The strong impact of non‐native predators in aquatic systems is thought to relate to the evolutionary naiveté of prey. Due to isolation and limited dispersal, this naiveté may be relatively high in freshwater systems. In this study, we tested this notion by examining the antipredator response of native mosquitofish, Gambusia holbrooki, to two non‐native predators found in the Everglades, the African jewelfish, Hemichromis letourneuxi, and the Mayan cichlid, Cichlasoma urophthalmus. We manipulated prey naiveté by using two mosquitofish populations that varied in their experience with the recent invader, the African jewelfish, but had similar levels of experience with the longer‐established Mayan cichlid. Specifically, we tested these predictions: (1) predator hunting modes differed between the two predators, (2) predation rates would be higher by the novel jewelfish predator, (3) particularly on the naive population living where jewelfish have not invaded yet, (4) antipredator responses would be stronger to Mayan cichlids due to greater experience and weaker and/or ineffective to jewelfish, and (5) especially weakest by the naive population. We assayed prey and predator behavior, and prey mortality in lab aquaria where both predators and prey were free‐ranging. Predator hunting modes and habitat domains differed, with jewelfish being more active search predators that used slightly higher parts of the water column and less of the habitat structure relative to Mayan cichlids. In disagreement with our predictions, predation rates were similar between the two predators, antipredator responses were stronger to African jewelfish (except for predator inspections), and there was no difference in response between jewelfish‐savvy and jewelfish‐naive populations. These results suggest that despite the novelty of introduced predators, prey may be able to respond appropriately if non‐native predator archetypes are similar enough to those of native predators, if prey rely on general antipredator responses or predation cues, and/or show neophobic responses.     

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.     

Population and behavioural responses of native prey to alien predation

The introduction of invasive alien predators often has catastrophic effects on populations of naïve native prey, but in situations where prey survive the initial impact a predator may act as a strong selective agent for prey that can discriminate and avoid it. Using two common species of Australian small mammals that have persisted in the presence of an alien predator, the European red fox Vulpes vulpes, for over a century, we hypothesised that populations of both would perform better where the activity of the predator was low than where it was high and that prey individuals would avoid signs of the predator’s presence. We found no difference in prey abundance in sites with high and low fox activity, but survival of one species—the bush rat Rattus fuscipes—was almost twofold higher where fox activity was low. Juvenile, but not adult rats, avoided fox odour on traps, as did individuals of the second prey species, the brown antechinus, Antechinus stuartii. Both species also showed reduced activity at foraging trays bearing fox odour in giving-up density (GUD) experiments, although GUDs and avoidance of fox odour declined over time. Young rats avoided fox odour more strongly where fox activity was high than where it was low, but neither adult R. fuscipes nor A. stuartii responded differently to different levels of fox activity. Conservation managers often attempt to eliminate alien predators or to protect predator-naïve prey in protected reserves. Our results suggest that, if predator pressure can be reduced, otherwise susceptible prey may survive the initial impact of an alien predator, and experience selection to discriminate cues to its presence and avoid it over the longer term. Although predator reduction is often feasible, identifying the level of reduction that will conserve prey and allow selection for avoidance remains an important challenge.     

Predator impacts on stream benthic prey

The impact that predators have on benthic, macroinvertebrate prey density in streams is unclear. While some studies show a strong effect of predators on prey density, others show little or no effect. Two factors appear to influence the detection of predator impact on prey density in streams. First, many field studies have small sample sizes and thus might be unable to detect treatment effects. Second, streams contain two broad classes of predators, invertebrates and vertebrates, which might have different impacts on prey density for a variety of reasons, including availability of refuge for prey and prey emigration responses to the two types of predators. In addition, predatory vertebrates have more complex prey communities than predatory invertebrates; this complexity might reduce the impact that predatory vertebrates have on prey because of indirect effects. I conducted a meta-analysis on the results of field studies that manipulate predator density in enclosures to determine (1) if predators have a significant impact on benthic prey density in streams, (2) if the impacts that predatory invertebrates and vertebrates have differ, and (3) if predatory vertebrates have different impacts on predatory prey versus herbivorous prey. The results of the meta-analysis suggest that on average predators have a significant negative effect on prey density, predatory invertebrates have a significantly stronger impact than predatory vertebrates, and predatory vertebrates do not differ in their impact on predatory versus herbivorous invertebrate prey. Three methodological variables (mesh size of enclosures, size of enclosures, and experimental duration) were examined to determine if cross correlations exist that may explain the differences in impact between predatory invertebrates and vertebrates. No correlation exists between mesh size and predator impact. Over all predators, no correlation exists between experimental duration and predator impact; however, within predatory invertebrates a correlation does exist between these variables. Also, a correlation was found between enclosure size and predator impact. This correlation potentially explains the difference in impact between predatory invertebrates and predatory vertebrates. Results of the meta-analysis suggest two important areas for future research: (1) manipulate both types of predators within the same system, and (2) examine their impacts on the same spatial scale.     

Match and mismatch: Integrating consumptive effects of predators,prey traits,and habitat selection in colonizing aquatic insects

Predators are a particularly critical component of habitat quality, as they affect survival, morphology, behavior, population size, and community structure through both consumptive and non‐consumptive effects. Non‐consumptive effects can often exceed consumptive effects, but their relative importance is undetermined in many systems. Our objective was to determine the consumptive and non‐consumptive effects of a predaceous aquatic insect, Notonecta irrorata, on colonizing aquatic beetles. We tested how N. irrorata affected survival and habitat selection of colonizing aquatic beetles, how beetle traits contributed to their vulnerability to predation by N. irrorata, and how combined consumptive and non‐consumptive effects affected populations and community structure. Predation vulnerabilities ranged from 0% to 95% mortality, with size, swimming, and exoskeleton traits generating species‐specific vulnerabilities. Habitat selection ranged from predator avoidance to preferentially colonizing predator patches. Attraction of Dytiscidae to N. irrorata may be a natural ecological trap given similar cues produced by these taxa. Hence, species‐specific habitat selection by prey can be either predator‐avoidance responses that reduce consumptive effects, or responses that magnify predator effects. Notonecta irrorata had both strong consumptive and non‐consumptive effects on populations and communities, while combined effects predicted even more distinct communities and populations across patches with or without predators. Our results illustrate that an aquatic invertebrate predator can have functionally unique consumptive effects on prey, attracting and repelling prey, while prey have functionally unique responses to predators. Determining species‐specific consumptive and non‐consumptive effects is important to understand patterns of species diversity across landscapes.     

Naïveté in novel ecological interactions: lessons from theory and experimental evidence

The invasion of alien species into areas beyond their native ranges is having profound effects on ecosystems around the world. In particular, novel alien predators are causing rapid extinctions or declines in many native prey species, and these impacts are generally attributed to ecological naïveté or the failure to recognise a novel enemy and respond appropriately due to a lack of experience. Despite a large body of research concerning the recognition of alien predation risk by native prey, the literature lacks an extensive review of naïveté theory that specifically asks how naïveté between novel pairings of alien predators and native prey disrupts our classical understanding of predator–prey ecological theory. Here we critically review both classic and current theory relating to predator–prey interactions between both predators and prey with shared evolutionary histories, and those that are ecologically ‘mismatched’ through the outcomes of biological invasions. The review is structured around the multiple levels of naïveté framework of Banks & Dickman (2007), and concepts and examples are discussed as they relate to each stage in the process from failure to recognise a novel predator (Level 1 naïveté), through to appropriate (Level 2) and effective (Level 3) antipredator responses. We discuss the relative contributions of recognition, cue types and the implied risk of cues used by novel alien and familiar native predators, to the probability that prey will recognise a novel predator. We then cover the antipredator response types available to prey and the factors that predict whether these responses will be appropriate or effective against novel alien and familiar native predators. In general, the level of naïveté of native prey can be predicted by the degree of novelty (in terms of appearance, behaviour or habitat use) of the alien predator compared to native predators with which prey are experienced. Appearance in this sense includes cue types, spatial distribution and implied risk of cues, whilst behaviour and habitat use include hunting modes and the habitat domain of the predator. Finally, we discuss whether the antipredator response can occur without recognition per se, for example in the case of morphological defences, and then consider a potential extension of the multiple levels of naïveté framework. The review concludes with recommendations for the design and execution of naïveté experiments incorporating the key concepts and issues covered here. This review aims to critique and combine classic ideas about predator–prey interactions with current naïveté theory, to further develop the multiple levels of naïveté framework, and to suggest the most fruitful avenues for future research.     

Multiple predators induce risk reduction in coexisting vole species

Large predators may affect the hunting efficiency of smaller ones directly by decreasing their numbers, or indirectly by altering their behaviour. Either way this may have positive effects on the density of shared prey. Using large outdoor enclosures, we experimentally studied whether the presence of the Tengmalm's owl Aegolius funereus affects the hunting efficiency of the smallest member of the vole-eating predator guild, the least weasel Mustela nivalis, as measured by population responses of coexisting prey species, the field vole Microtus agrestis and the sibling vole M. levis . We compared the density and survival probability of vole populations exposed to no predation, weasel predation or combined predation by a weasel and an owl. The combined predation of both owl and weasel did not result in obvious changes in the density of sibling and field vole populations compared to the control populations without predators, while predation by least weasel alone decreased the densities of sibling voles and induced a similar trend in field vole densities. Survival of field voles was not affected by predator treatment while sibling vole survival was lower in predator treated populations than in control populations. Our results suggest that weasels are intimidated by avian predators, but without changing the effects of predators on competitive situations between the two vole species. Non-lethal effects of intraguild predation therefore will not necessarily change competitive interactions between shared prey species.     

Exploiting predators for pest management: the need for sound ecological assessment

Most people agree that arthropod natural enemies are good for insect pest management in agriculture. However, the population suppressive effects of predators, which consume their prey and often leave no direct evidence of their activity, are more difficult to study than the effects of parasitoids, which can be sampled from host populations relatively easily. We critically reviewed field studies which investigated the relationship between lepidopteran pests and their associated predatory fauna, published in 11 leading entomology and applied ecology journals between 2003 and 2008. Each study was appraised to determine whether or not it demonstrated that predators had an impact on prey (pest) populations and, if so, whether it was conducted at an ecological scale relevant to pest management. Less than half (43%) of the 54 field studies adopted methodologies that allowed the impact of predators on target pest populations to be measured. Furthermore, 76% of the studies were conducted at the scale of experimental plots rather than at the ecological scale which determines pest and predator population dynamics or at which pest‐management decisions are made. In almost one‐third of the studies, predator abundance and/or diversity was measured, but this metric was not linked with pest suppression or mortality. We conclude that much current research does not provide evidence that predatory arthropods suppress target lepidopteran pest populations and, consequently, that it has little relevance to pest management. Well‐designed ecological experiments combined with recent advances in molecular techniques to identify predator diets and the emergence of organic agriculture provide both the mechanisms and a platform upon which many predator–prey interactions can be investigated at a scale relevant to pest management. However, benefits will only be reaped from this opportunity if current approaches to research are changed and relevant ecological data are collected at appropriate ecological scales.     

Naiveté is not forever: responses of a vulnerable native rodent to its long term alien predators

Alien predators have wreaked havoc on isolated endemic and island fauna worldwide, a phenomenon generally attributed to prey naiveté, or a failure to display effective antipredator behaviour due to a lack of experience. While the failure to recognise and/or respond to a novel predator has devastating impacts in the short term after predators are introduced, few studies have asked whether medium to long term experience with alien predators enables native species to overcome their naiveté. In Australia, introduced dogs Canis lupus familiaris, foxes Vulpes vulpes and cats Felis catus have caused rapid extinctions and declines in small–medium sized native mammals since they were introduced ～150 years ago. However, native wildlife have had ～4000 years experience with another dog – the dingo Canis lupus dingo. Native bush rats Rattus fuscipes remain common despite predation from these predators. We predicted that prior experience with dingoes would mean that bush rats recognise and respond to dogs, but suspect that hundreds of years experience may not be enough for effective responses to cats and foxes. To test these predictions, we combined the giving‐up density (GUD) with analysis of remote camera footage to measure bush rat foraging and behavioural responses to body odour from dogs, foxes, cats and native spotted‐tail quolls Dasyurus maculatus. Bush rats responded strongly to dogs with increased GUDs, increased vigilance and decreased foraging. However, mixed responses to foxes and cats suggest that at least some individuals remain naïve towards these predators. Naiveté is not necessarily forever: alien predators devastate many native prey species, but others may learn or adapt to the new threat.     

Behavioral responses of native prey to disparate predators: naiveté and predator recognition

It is widely accepted that predator recognition and avoidance are important behaviors in allowing prey to mitigate the impacts of their predators. However, while prey species generally develop anti-predator behaviors through coevolution with predators, they sometimes show accelerated adoption of these behaviors under strong selection pressure from novel species. We used a field manipulation experiment to gauge the ability of the common ringtail possum (Pseudocheirus peregrinus), a semi-arboreal Australian marsupial, to recognize and respond to olfactory cues of different predator archetypes. We predicted that ringtails would display stronger anti-predator behaviors to cues of the invasive European red fox (Vulpes vulpes) in areas where fox impacts had been greatest, and to cues of the native lace monitor (Varanus varius) in areas of sympatry compared with allopatry. We found that ringtails fled quickly and were more alert when exposed to the fecal odors of both predators compared to neutral and pungent control odors, confirming that predator odors are recognized and avoided. However, these aversive responses were similar irrespective of predator presence or level of impact. These results suggest that selection pressure from the fox has been sufficient for ringtails to develop anti-predator behaviors over the few generations since foxes have become established. In contrast, we speculate that aversive responses by ringtails to the lace monitor in areas where this predator is absent reflect recent coexistence of the two species. We conclude that rapid evolution of anti-predator behaviors may occur when selection is strong. The maintenance of these behaviors should allow re-establishment of predator–prey relationships if the interactants regain sympatry via range shifts or management actions to reintroduce them to their former ranges.     

Foraging traits of native predators determine their vulnerability to a toxic alien prey

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Comparison of susceptibility to a toxic alien toad (Bufo japonicus formosus) between predators in its native and invaded ranges

1. To manage biological invasions effectively, the impacts of alien species on the demography and traits of native species must be known, but determining those impacts can be challenging. We used a comparative approach to gain insight into the impacts that an alien toad (Bufo japonicus formosus) might have on native Japanese predatory amphibians. We compared the susceptibility of native predator species to alien toad toxins in the alien-invaded range and the susceptibility of closely related native predator species to the toxins in the alien toad's native range to investigate the impacts of an alien on a native species.
2. Bufo japonicus formosus is native to Honshu, but was recently introduced to Hokkaido and Sado. In laboratory experiments, we compared individual mortality of predators exposed to a toad hatchling between novel predators on the toad-invaded islands and ecologically similar congeneric or conspecific species on Honshu, where the toad is native. We also compared (1) the percentage of individuals that consumed a toad hatchling and (2) toxin resistance (i.e. survival and growth of individuals after toad consumption) between these two groups of predators, as mechanistic components behind the susceptibility of the predators to the toxic prey.
3. The mortality of Rana pirica from all populations after consumption of a toad hatchling was almost 100%, and that of Hynobius retardatus ranged from 14 to 90%, depending on the population. In contrast, the mortality of Rana ornativentris and Hynobius nigrescens was near 0% regardless of population. These differences between congeneric predators were mostly due to differences in their toxin resistance.
4. These results suggest that the alien toad is a potential threat to the novel amphibian predators on Hokkaido, although they also imply that the novel predators on Hokkaido have the potential to develop toxin resistance through adaptive evolution. However, this counteradaptation may have a higher chance of evolving in H. retardatus than in R. pirica because of differences in their genetic backgrounds.

     

Native predator eats invasive toxic prey: evidence for increased incidence of consumption rather than aversion-learning

Contemporary adaptation of native prey species to invasive predators has been relatively well documented, but that of native predators to invasive prey has received less attention. Because the level of impact an invasive species will have on its predators versus its prey will determine changes in community trophic structure, it is important to understand how native predators respond to novel prey. Here we examine the response of native fence lizards to the invasion of red imported fire ants, a novel toxic prey. Examining invaded and uninvaded lizard populations, we tested whether or not aversion-learning occurs in juvenile fence lizards over successive feedings (within lifetime), how previous fire ant exposure may affect avoidance behavior (over generations), and whether population differences are consistent when prey choice exists. We also examine rates of phenotypic divergence in traits associated with the native species as both predator and prey. Aversion-learning did not occur in either population. Instead, the incidence of fire ant consumption increased over both successive feedings and generations. Lizards from the fire ant invaded population had a higher propensity to eat fire ants than fire ant-naïve lizards, even when given a choice between prey items. We found greater phenotypic divergence in traits associated with the native species as predator on, versus as prey to, fire ants. Although the strategy of eating these novel toxic prey can impose survival costs in the short term, over the longer-term, eating fire ants may cost little or even benefit survivors.     

Strategies of aphidophagous predators: lessons for modelling insect predator–prey dynamics

Both theoretical and empirical evidence indicate that in systems where insect predators have longer developmental times than their prey the predators have little impact on the abundance of their prey. In assessing the 'effectiveness' of a predator for biological control one should take into account that selection maximizes predator fitness, not its effctiveness as a biocontrol agent. Therefore, predators that have a long developmental time relative to their prey are unlikely to be the best biocontrol agents. If these results can be generalized to other predator–prey systems, then it is clear that an understanding of predator–prey dynamics can only be achieved by studying predators.     

Ecological effects of invasive alien species on native communities,with particular emphasis on the interactions between aphids and ladybirds

The ecological effects of introduced species on native organisms can sometimes, but not always be significant. The risks associated with invasive alien pests are difficult to quantify. This paper concentrates on the ecological effects of invasive insect predators that feed on pest insects, because the former may potentially affect the biological control of the latter. The literature indicates that invasive predatory insects generally are resistant to changes in environmental conditions, long-lived and voracious with a high reproductive rate, high dispersal ability, able to spread very rapidly across landscapes and exhibit phenotypic plasticity. Their colonization of patches of prey may induce native predators to leave, but the evidence that invaders negatively affect the abundance of the native species is scarce and not persuasive. Insect predators do not substantially affect the abundance of their prey, if the ratio of generation time of the predator to that of the prey is large (the generation time ratio hypothesis), therefore the effect of an invasion by long-lived alien predators on systems consisting of long-lived native predators and short-lived prey on the abundance of the prey is hard to detect.     

Evidence of weaker phenotypic plasticity by prey to novel cues from non‐native predators

A central question in evolutionary biology is how coevolutionary history between predator and prey influences their interactions. Contemporary global change and range expansion of exotic organisms impose a great challenge for prey species, which are increasingly exposed to invading non‐native predators, with which they share no evolutionary history. Here, we complete a comprehensive survey of empirical studies of coevolved and naive predator?prey interactions to assess whether a shared evolutionary history with predators influences the magnitude of predator‐induced defenses mounted by prey. Using marine bivalves and gastropods as model prey, we found that coevolved prey and predator‐naive prey showed large discrepancies in magnitude of predator‐induced phenotypic plasticity. Although naive prey, predominantly among bivalve species, did exhibit some level of plasticity – prey exposed to native predators showed significantly larger amounts of phenotypic plasticity. We discuss these results and the implications they may have for native communities and ecosystems.     

Do native predators benefit from non‐native prey?

Despite knowledge on invasive species’ predatory effects, we know little of their influence as prey. Non‐native prey should have a neutral to positive effect on native predators by supplementing the prey base. However, if non‐native prey displace native prey, then an invader's net influence should depend on both its abundance and value relative to native prey. We conducted a meta‐analysis to quantify the effect of non‐native prey on native predator populations. Relative to native prey, non‐native prey similarly or negatively affect native predators, but only when studies employed a substitutive design that examined the effects of each prey species in isolation from other prey. When native predators had access to non‐native and native prey simultaneously, predator abundance increased significantly relative to pre‐invasion abundance. Although non‐native prey may have a lower per capita value than native prey, they seem to benefit native predators by serving as a supplemental prey resource.     

Interspecific infanticide deters predators

It is well known that young, small predator stages are vulnerable to predation by conspecifics, intra-guild competitors or hyperpredators. It is less known that prey can also kill vulnerable predator stages that present no danger to the prey. Since adult predators are expected to avoid places where their offspring would run a high predation risk, this opens the way for potential prey to deter dangerous predator stages by killing vulnerable predator stages. We present an example of such a complex predator–prey interaction. We show that (1) the vulnerable stage of an omnivorous arthropod prey discriminates between eggs of a harmless predator species and eggs of a dangerous species, killing more eggs of the latter; (2) prey suffer a minor predation risk from newly hatched predators; (3) adult predators avoid ovipositing near killed predator eggs, and (4) vulnerable prey near killed predator eggs experience an almost fourfold reduction of predation. Hence, by attacking the vulnerable stage of their predator, prey deter adult predators and thus reduce their own predation risk. This provides a novel explanation for the killing of vulnerable stages of predators by prey and adds a new dimension to anti-predator behaviour.