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.     

Predator Generalization Decreases the Effect of Introduced Predators in the San Marcos Salamander,Eurycea nana

The introduction of novel predators into an environment can have detrimental consequences on prey species, especially if these species lack the ability to recognize these predators. One such species that may be negatively affected by introduced predators is the federally threatened San Marcos salamander (Eurycea nana). Previous research found that predator‐naïve (captive‐hatched) salamanders showed decreased activity in response to the chemical cues of both a native fish predator (Micropterus salmoides) and an introduced fish predator (Lepomis auritus), but not to a non‐predatory fish (Gambusia geiseri). We tested the hypothesis that E. nana recognized the introduced Lepomis (and other non‐native Lepomis) because they share chemical cues with other native congeneric Lepomis predators in the San Marcos River. We examined the antipredator response of predator‐naïve E. nana to chemical cues from (1) a sympatric native sunfish (Lepomis cyanellus; Perciformes: Centrarchidae); (2) a sympatric introduced sunfish (L. auritus); (3) an allopatric sunfish (Lepomis gibbosus); (4) a sympatric non‐native, non‐centrarchid cichlid (Herichthys cyanoguttatum; Perciformes: Cichlidae); and (5) a blank water control to determine whether individuals make generalizations about novel predators within a genus and across a family. Exposure to chemical cues from all fish predator treatments caused a reduction in salamander activity (antipredator response). Additionally, there were no differences in the antipredator responses to each predatory fish treatment. The similar responses to all sunfish treatments indicate that E. nana shows predator generalization in response to novel predators that are similar to recognized predators. Additionally, the antipredator response to H. cyanoguttatum indicates that predator generalization can occur among perciform families.     

Learned Recognition of Intraspecific Predators in Larval Long-Toed Salamanders Ambystoma macrodactylum

The ability of prey to detect predators and respond accordingly is critical to their survival. The use of chemical cues by animals in predator detection has been widely documented. In many cases, predator recognition is facilitated by the release of alarm cues from conspecific victims. Alarm cues elicit anti‐predator behavior in many species, which can reduce their risk of being attacked. It has been previously demonstrated that adult long‐toed salamanders, Ambystoma macrodactylum, exhibit an alarm response to chemical cues from injured conspecifics. However, whether this response exists in the larval stage of this species and whether it is an innate or a learned condition is unknown. In the current study, we examined the alarm response of naïve (i.e. lab‐reared) larval long‐toed salamanders. We conducted a series of behavioral trials during which we quantified the level of activity and spatial avoidance of hungry and satiated focal larvae to water conditioned by an injured conspecific, a cannibal that had recently been fed a conspecific or a non‐cannibal that was recently fed a diet of Tubifex worms. Focal larvae neither reduced their activity nor spatially avoided the area of the stimulus in either treatment when satiated, and exhibited increased activity towards the cannibal stimulus when hungry. We regard this latter behavior as a feeding response. Together these results suggest that an anti‐predator response to injured conspecifics and to cannibalistic conspecifics is absent in naïve larvae. Previous studies have shown that experienced wild captured salamanders do show a response to cannibalistic conspecifics. Therefore, we conducted an additional experiment examining whether larvae can learn to exhibit anti‐predator behavior in response to cues from cannibalized conspecifics. We exposed larvae to visual, chemical and tactile cues of stimulus animals that were actively foraging on conspecifics (experienced) or a diet of Tubifex (naïve treatment). In subsequent behavioral treatments, experienced larvae significantly reduced their activity compared to naive larvae in response to chemical cues of cannibals that had recently consumed conspecifics. We suggest that this behavior is a response to alarm cues released by consumed conspecifics that may have labeled the cannibal. Furthermore, over time, interactions with cannibals may cause potential prey larvae to learn to avoid cannibals regardless of their recent diet.     

Relaxed predation theory: size,sex and brains matter

Australia's wildlife is being considerably impacted by introduced mammalian predators such as cats (Felis catus), dogs (Canis lupus familiaris), and foxes (Vulpes vulpes). This is often attributed to native wildlife being naïve to these introduced predators. A systematic review of the literature reveals that native metatherians (body mass range 0.02–25 kg) do not recognise, and show relaxed antipredator behaviours towards, native and some introduced mammalian predators. Native eutherians (all with body mass < 2 kg), however, do appear to recognise and exhibit antipredator behaviours towards both native and introduced predators. Based on our findings, we propose a novel theory, the ‘Relaxed Predation Theory’. Our new theory is based on the absence of large mammalian predators leading to reduced predation pressure in Australia during the past 40000–50000 years, and on three key differences between Australian metatherians and eutherians: size, sex, and brains. In light of this Relaxed Predation Theory, we make a number of recommendations for the conservation of Australian wildlife: (i) predator avoidance training of suitable species; (ii) exclusion fencing to exclude some, but not all, predators to facilitate the development of antipredator behaviours; (iii) captive breeding programs to prevent the extinction of some species; and (iv) reintroduction of Australia's larger predators, potentially to compete with and displace introduced predators. A more detailed understanding of the responses of Australian mammals to predators will hopefully contribute to the improved conservation of susceptible species.     

Linking Morphological and Behavioural Defences: Prey Fish Detect the Morphology of Conspecifics in the Odour Signature of their Predators

Predation is a strong selective force acting on both morphology and behaviour of prey animals. While morphological defences (e.g. crypsis, presence of armours or spines or specific body morphologies) and antipredator behaviours (e.g. change in foraging or reproductive effort, or hiding and fleeing behaviours) have been widely studied separately, few studies have considered the interplay between the two. The question raised in our study is whether antipredator behaviours of a prey fish to predator odours could be influenced by the morphology of prey conspecifics in the diet of the predator. We used goldfish (Carassius auratus) as our test species; goldfish exposed to predation risk significantly increase their body depth to length ratio, which gives them a survival advantage against gape‐limited predators. We exposed shallow‐bodied and deep‐bodied goldfish to the odour of pike (Esox lucius) fed either form of goldfish. Deep‐bodied goldfish displayed lower intensity antipredator responses than shallow‐bodied ones, consistent with the hypothesis that individuals with morphological defences should exhibit less behavioural modification than those lacking such defences. Moreover, both shallow‐ and deep‐bodied goldfish displayed their strongest antipredator responses when exposed to the odour of pike fed conspecifics of their own morphology, indicating that goldfish are able to differentiate the morphology of conspecifics through predator diet cues. For a given individual, predator threat increases as the prey become more like the individual eaten, revealing a surprising level of sophistication of chemosensory assessment by prey fish.     

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.     

Responses of naïve and experienced European rabbits to predator odour

The response of prey species to predator scent has been investigated in many mammalian species; however, there is little information about the responses of European wild rabbits at the population level. Therefore, we conducted a simple experiment to investigate the behavioural response of a rabbit population to native predator cues in the wild. We compared the response to the scent of a predator (red fox) in a wild rabbit population bred in semi-natural conditions and naïve to terrestrial predators with the response of a population in a similar environment where terrestrial predators were present. The response to predators was based on rabbit abundance, inferred from pellet counts and measured by the defecation rate per day (DRD). Our results indicate that rabbits responded to the odour of fox faeces in the treatment warrens, resulting in a lower DRD. The main anti-predator behaviour observed was spatial avoidance (warren abandonment), which seemed to be more accentuated for rabbits who had not previously had contact with foxes in the plot where terrestrial predators were excluded. In both the fenced and the unfenced plot, the differences in the effect of the predator odour between the control and treatment warrens disappeared after cessation of treatment, suggesting a flexible and adaptive behaviour of rabbits to predator cues.

     

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.     

Sex‐Specific Response of Pardosa milvina (Araneae: Lycosidae) to Experience with a Chemotactile Predation Cue

Predators frequently leave behind chemical information (i.e., semiochemicals such as pheromones or kairomones) that can be detected by their prey and used to avoid areas where predators are likely present. Prey that have interacted indirectly with predators via chemical information thus may gain insight into their risk of being consumed that naïve individuals lack. Pardosa milvina (Araneae: Lycosidae) is a chemosensitive wolf spider that shows adaptive responses to chemotactile cues deposited by the larger wolf spider Tigrosa helluo. We raised offspring from P. milvina to examine the effect of experience with a predation cue on activity, foraging, and antipredator behavior. Spiders differed in activity and foraging behavior across ontogeny and between sexes, but there was no effect of experience with a predation cue. However, a sex‐specific effect of experience was found in antipredator behavior. Male spiders, but not females, used experience with a predator cue to increase their survival in the presence of a live predator. Specifically, naïve males were attacked sooner than experienced males, indicating that prior exposure to predator cues can modify Pardosa antipredator behavior. Intersexual differences in how spiders respond to experience with a predation cue likely reflect the risk of predation faced by males and females in nature.     

Macro- and micro-habitat selection of small rodents and their predation risk perception under a novel invasive predator at the southern end of the Americas

Invasive predators are responsible for the extinction of numerous island species worldwide. The naïve prey hypothesis suggests that the lack of co-evolutionary history between native prey and introduced predators results in the absence of behavioral responses to avoid predation. The lack of terrestrial mammal predators is a core feature of islands at the southern end of the Americas. Recently, however, the American mink (Neovison vison) established as a novel terrestrial predator, where rodents became a main portion of its diet. Here, we investigated on Navarino Island, Chile, macro- and micro-habitat selection of small rodents using Sherman traps. Additionally, we experimentally tested behavioral responses of small rodents to indirect cues of native raptorial predation risk (vegetation cover) and direct cues of novel mink predation risk (gland odor) using Sherman traps and foraging trays (giving-up density (GUD)). At the macro-habitat level, we detected native rodents of the species Abrothrix xanthorhinus and Oligoryzomys longicaudatus and the exotic Mus musculus. In general, rodents preferred scrubland habitats. At the micro-habitat level, we only captured individuals of A. xanthorhinus. They preferred covered habitats with tall vegetation. GUD increased in opened areas (riskier for raptorial predation) regardless of the presence or not of mink odor. These results suggest that A. xanthorhinus can perceive predation risk by raptors, but not by mink, results that accord with the hypothesis that co-evolutionary history is important for rodents to develop antipredator behavior. Given that these rodents represent an important proportion of mink diet, the low abundances together with the apparent lack of antipredator response raise conservation concerns for the small rodent populations inhabiting the southernmost island ecosystems of the Americas.     

Do Naïve Primates Recognize the Vocalizations of Felid Predators?

Traits that were adaptive under previous conditions may no longer have fitness benefits. However, some species still retain appropriate antipredator behaviors even though they do not coexist with the predators that their ancestors once faced. Studies have examined the responses of a variety of naïve species to these predators, but none have specifically investigated whether naïve primates retain antipredator behaviors against felid predators. We studied the pig‐tailed langur (Simias concolor) to determine whether it still recognizes felids as predators even though dangerous felids do not exist on the islands on which it inhabits. The responses of the langurs to the playbacks of the vocalizations of felids (an ancestral predator), elephants (an unknown animal but not a predator), humans (a known predator) and, pigs and birds (known animals but not predators) were compared. Langurs fled more slowly and looked at the speaker less in response to the felid and elephant calls than they did in response to the human voices. Similar numbers of langurs fled in response to all playback treatments except the pig and bird. The results suggest that langurs are afraid of novel vocalizations but have not retained specific acoustic knowledge of felid predator vocalizations. For long‐lived species that have extended periods of learning, being able to modify general behavioral responses, such as antipredator behaviors, based on individual experiences may be more adaptive than having fixed behavioral strategies.     

Prey naivety in the behavioural responses of juvenile Chinook salmon (Oncorhynchus tshawytscha) to an invasive predator

1. Non‐native predators might inflict proportionally higher mortality on prey that have no previous experience of them, compared to species that have coexisted with the predator for some time. 2. We tested whether juvenile Chinook salmon (Oncorhynchus tshawytscha) were less able to recognise a non‐native than a native predator, by investigating behavioural responses to the chemical cues of the invasive smallmouth bass (Micropterus dolomieu) and the native northern pikeminnow (Ptychocheilus oregonensis) in both laboratory and field experiments. 3. Laboratory results demonstrated strong innate antipredator responses of individual juvenile Chinook salmon to northern pikeminnow; fish spent 70% of time motionless and exhibited 100% greater panic response than in controls. By contrast, antipredator responses to the chemical cues of smallmouth bass did not differ from controls. 4. These results were supported by similar differences in recognition of these predator odours by groups of juvenile Chinook salmon in fully natural conditions, though responses reflected a greater range of antipredator behaviours by individuals. In field trials, responses to northern pikeminnow odour resulted in increased flight or absence, reductions in swimming and foraging, and increased time spent near the substratum, compared to smallmouth bass odour. 5. Given that survival of juvenile fish is facilitated by predator recognition, our results support the hypothesis that naivety may be an important factor determining the effect of non‐native predators on prey populations. Efforts to manage the effect of native and non‐native predators may benefit by considering complex behavioural interactions, such as these at the individual and group levels.     

Male and Female Meadow Voles,Microtus pennsylvanicus,Differ in Their Responses to Heterospecific/Conspecific Over‐Marks

Voles use runways, paths, and trails that may also be used by rabbits and mink. These shared areas could contain the scent marks of conspecifics and heterospecifics. Thus, it is likely that the scent marks of heterospecifics may overlap or be overlapped by those of voles, forming over‐marks. Much is known about how voles respond to over‐marks of two different conspecifics. However, we do not know how they would respond to an opposite‐sex conspecific whose scent marks are in an over‐mark with the scent marks of predator or the scent marks of a non‐predator heterospecifics. We tested the hypothesis that meadow voles, Microtus pennsylvanicus, differ in their response to the scent mark of the opposite‐sex conspecific if the scent mark was overlapped by that of a mink, a vole predator, or rabbit, a vole non‐predator. We found that female but not male voles showed a preference for the scent marks of the opposite‐sex conspecifics that were part of the mink‐vole over‐mark when compared to those of opposite‐sex conspecifics that were not part of the over‐mark. This preference by female voles was independent of whether the male vole was the top‐scent donor or bottom‐scent donor of the over‐mark. Male and female voles showed no preference between the scent marks of the opposite‐sex conspecifics whose marks were part of or not part of the rabbit‐vole over‐mark. Sex differences in the manner that meadow voles respond to rabbit‐vole and mink‐vole over‐marks are discussed.     

Improving anti‐predator responses of hatchery reared salmonids by social learning

Predation shortly after release is the main source of mortality among hatchery‐reared fish used to restore or enhance endangered salmonid populations. We found, that hatchery‐reared salmonid young originating from endangered stocks have weak innate responses to their natural fish predators. The ability to avoid predation in fish can be improved through social learning from experienced to naïve individuals. Huge benefits would be achieved, if social learning processes could be successfully applied on a large scale to enhance viability of hatchery fish prior to release into the wild. By using model predators together with chemical cues from real predators we tested if social learning could be used to train hatchery‐reared salmonid young to avoid fish predators. As there are clear differences in social behaviour among the salmonid species, we first examined whether these differences affect the probability and efficiency of learning anti‐predator skills from trained demonstrators. We compared anti‐predator responses of observers (fish trained by using experienced fish as demonstrators) with those of control fish, which had been ‘trained’ by untrained naïve conspecifics. We also examined how the efficiency of social learning depends on the ratio of experienced to naïve fish involved in social transmission trials. The results of these experiments will give guidelines how social learning could be utilized in developing hatchery scale training protocols.     

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.     

Do anuran larvae respond behaviourally to chemical cues from an invasive crayfish predator? A community-wide study

Antipredator behaviour is an important fitness component in most animals. A co-evolutionary history between predator and prey is important for prey to respond adaptively to predation threats. When non-native predator species invade new areas, native prey may not recognise them or may lack effective antipredator defences. However, responses to novel predators can be facilitated by chemical cues from the predators’ diet. The red swamp crayfish Procambarus clarkii is a widespread invasive predator in the Southwest of the Iberian Peninsula, where it preys upon native anuran tadpoles. In a laboratory experiment we studied behavioural antipredator defences (alterations in activity level and spatial avoidance of predator) of nine anurans in response to P. clarkii chemical cues, and compared them with the defences towards a native predator, the larval dragonfly Aeshna sp. To investigate how chemical cues from consumed conspecifics shape the responses, we raised tadpoles with either a tadpole-fed or starved crayfish, or dragonfly larva, or in the absence of a predator. Five species significantly altered their behaviour in the presence of crayfish, and this was largely mediated by chemical cues from consumed conspecifics. In the presence of dragonflies, most species exhibited behavioural defences and often these did not require the presence of cues from predation events. Responding to cues from consumed conspecifics seems to be a critical factor in facilitating certain behavioural responses to novel exotic predators. This finding can be useful for predicting antipredator responses to invasive predators and help directing conservation efforts to the species at highest risk.     

Orientation behavior of Propylaea japonica toward visual and olfactory cues from its prey–host plant combination

The lady beetle Propylaea japonica (Thunberg) (Coleoptera: Coccinellidae) is an important predator of aphids in agroecosystems. The inundative release of coccinellid beetles can be an effective biological control strategy. An understanding of how biological control agents perceive and use stimuli from host plants is the key to successfully implement commercially produced predators. Here, we studied the relative role of visual and volatile cues. Dual‐choice assays using foraging‐naïve and foraging‐experienced P. japonica adults were conducted using cotton plants [Gossypium hirsutum L. (Malvaceae)] with or without infestation by the cotton aphid, Aphis gossypii (Glover) (Hemiptera: Aphididae). Overall, experienced beetles were more attracted than naïve beetles toward cues associated with aphid‐infested plants. Experienced beetles were also more responsive to olfactory cues compared with naïve beetles. Both foraging‐naïve and ‐experienced lady beetles integrate olfactory and visual cues from plants infested with aphids, with an apparently greater reliance on olfactory cues. The results suggest that foraging experience may increase prey location in P. japonica.     

Juvenile western toads, Bufo boreas, avoid chemical cues of snakes fed juvenile, but not larval, conspecifics

Previous investigations have demonstrated the importance of predator diet in chemically mediated antipredator behaviour. However, there are few data on responses to life-stage-specific predator diets, which could be important for animals like amphibians that undergo metamorphosis and must respond to different suites of predators at different life-history stages. In laboratory choice tests, we investigated the chemically mediated avoidance response of juvenile western toads, Bufo boreas, to four different chemical stimuli: (1) live conspecific juveniles; (2) live earthworms; (3) snakes fed juvenile conspecifics; and (4) snakes fed larval conspecifics (tadpoles). Juvenile toads avoided chemical cues from snakes that had eaten juvenile conspecifics, but did not respond to the other three stimuli, including chemical cues from snakes fed larval conspecifics. In addition, the response to cues from snakes fed juveniles differed significantly from that of snakes fed larvae. To our knowledge, this is the first study to demonstrate the importance of diet in predator avoidance of juvenile anurans and the ability of juvenile toads to distinguish between chemical cues from predators that have consumed larval versus juvenile conspecifics. Copyright 2000 The Association for the Study of Animal Behaviour.     

After the crash: How do predators adjust following the invasion of a novel toxic prey type?

The ability of a native predator to adjust to a dangerously toxic invasive species is key to avoiding an ongoing suppression of the predator's population and the trophic cascade of effects that can result. Many species of anurophagous predators have suffered population declines due to the cane toad's (Rhinella marina: Bufonidae) invasion of Australia; these predators can be fatally poisoned from attempting to consume the toxic toad. We studied one such toad‐vulnerable predator, the yellow‐spotted monitor (Varanus panoptes: Varanidae), testing whether changes to the predator's feeding behaviour could explain how the species persists following toad invasion. Wild, free‐roaming lizards from (1) toad‐naïve and (2) toad‐exposed populations were offered non‐toxic native frogs and slightly toxic cane toads (with parotoid glands removed) in standardized feeding trials. Toad‐naïve lizards readily consumed both frogs and toads, with some lizards displaying overt signs of illness after consuming toads. In contrast, lizards from toad‐exposed populations consumed frogs but avoided toads. Repeated encounters with toads did not modify feeding responses by lizards from the toad‐naïve populations, suggesting that aversion learning is limited (but may nonetheless occur). Our results suggest that this vulnerable predator can adjust to toad invasion by developing an aversion to feeding on the toxic invader, but it remains unclear as to whether the lizard's toad‐aversion arises via adaptation or learning.     

The Asian grass lizard (Takydromus sexlineatus) does not respond to the scent of a native mammalian predator

Lacertid lizards use chemical cues emitted by saurophagous snakes to evade predation. Whether these lizards can detect and respond to the chemical cues of predatory mammals has not been studied. As many mammals carry distinct body odours and/or use chemical cues for intraspecific communication, lizards can be expected to use these chemicals as early warning cues. To test this idea, we observed the behaviour of Asian grass lizards (Takydromus sexlineatus) that had been transferred to an unfamiliar test arena containing one of four scent treatments. No particular scent was applied to the arena in the control situation. Diluted aftershave served as a pungency control. In the snake treatment, scent of the Oriental whip snake (Ahaetulla prasina) was applied. We included this treatment to learn how Asian grass lizards react to predator chemical cues. Finally, in the mongoose treatment, the lizards were confronted with scent cues of several small Indian mongooses (Herpestes auropunctatus). Snake scent elicited foot shakes, startles and tail vibrations. These are behaviours that in lacertid lizards are associated with stressful situations such as predatory encounters. Surprisingly, lizards confronted with mongoose scent exhibited none of these stress-indicating behaviours. In fact, their behaviour did not differ from that of lizards subjected to an odourless control treatment. These results raise concern. Mongooses are rapidly invading ecosystems worldwide. If lizards that have co-evolved with mongooses are unable to detect these predators’ presence through chemical cues, it seems highly unlikely that evolutionary naïve lizards will develop this ability rapidly.