Friend or foe? The role of latent inhibition in predator and non-predator labelling by coral reef fishes

In communities of high biodiversity, the ability to distinguish predators from non-predators is crucial for prey success. Learning often plays a vital role in the ability to distinguish species that are threatening from those that are not. Many prey animals learn to recognise predators based on a single conditioning event whereby they are exposed to the unknown predator at the same time as alarm cues released from injured conspecifics. The remarkable efficiency of such learning means that recognition mistakes may occur if prey inadvertently learn that a species is a predator when it is not. Latent inhibition is a means by which prey that are pre-exposed to an unknown species in the absence of negative reinforcement can learn that the unknown animal is likely not a threat. Learning through latent inhibition should be conservative because mistakenly identifying predators as non-predators can have fatal consequences. In this study, we demonstrated that a common coral reef fish, lemon damselfish, Pomacentrus moluccensis can learn to recognise a predator as non-threatening through latent inhibition. Furthermore, we showed that we could override the latent inhibition effect by conditioning the prey to recognise the predator numerous times. Our results highlight the ability of prey fish to continually update the information regarding the threat posed by other fishes in their vicinity.     

Learning about non-predators and safe places: the forgotten elements of risk assessment

A fundamental prerequisite for prey to avoid being captured is the ability to distinguish dangerous stimuli such as predators and risky habitats from non-dangerous stimuli such as non-predators and safe locations. Most research to date has focused on mechanisms allowing prey to learn to recognize risky stimuli. The paradox of learned predator recognition is that its remarkable efficiency leaves room for potentially costly mistakes if prey inadvertently learn to recognize non-predatory species as dangerous. Here, we pre-exposed embryonic woodfrogs, Rana sylvatica, to the odour of a tiger salamander, Ambystoma tigrinum, without risk reinforcement, and later try to teach the tadpoles to recognize the salamander, a red-bellied newt Cynops pyrrhogaster—a closely related amphibian, or a goldfish, Carassius auratus, as a predator. Tadpoles were then tested for their responses to salamander, newt or fish odour. Pre-exposure to salamander did not affect the ability of tadpoles to learn to recognize goldfish as a predator. However, the embryonic pre-exposure to salamanders inhibited the subsequent learning of salamanders as a potential predator, through a mechanism known as latent inhibition. The embryonic pre-exposure also prevented the learned recognition of novel newts, indicating complete generalization of non-predator recognition. This pattern does not match that of generalization of predator recognition, whereby species learning to recognize a novel predator do respond, but not as strongly, to novel species closely related to the known predator. The current paper discusses the costs of making recognition mistakes within the context of generalization of predators and dangerous habitats versus generalization of non-predators and safe habitats and highlights the asymmetry in which amphibians incorporate information related to safe versus risky cues in their decision-making. Mechanisms such as latent inhibition allow a variety of prey species to collect information about non-threatening stimuli, as early as during their embryonic development, and to use this information later in life to infer the danger level associated with the stimuli.     

Temporal dynamics of information use in learning and retention of predator-related information in tadpoles

Due to the high variability in predation risk through space and time, prey have to continuously update information about the risk level posed by predators. Despite numerous studies focusing on temporal risk assessment, we know very little about how individuals deal with information regarding changes in risk level of a given predator through time. In this study, we conditioned tadpoles to recognize a predator as a high or low risk twice 2 weeks apart, in a 2 × 2 design. We tested the responses of the tadpoles 1 and 11 days after each conditioning event. Prey showed responses to the predator 1 day after the first conditioning, but the low-risk group failed to respond to the predator after 11 days. However, we found that information learned during the first conditioning affected the response to the predator after the second conditioning, indicating that prey do not ‘forget’ old information, but simply ignore it. Moreover, tadpoles were able to assess their change in vulnerability over the 2-week period and further extrapolate the risk level of the predator through time to display adaptive threat-sensitive antipredator responses. Our study highlights the complex decision-making that prey use to assess temporal fluctuation in predation risk.     

Different chemical cues originating from a shared predator induce common defense responses in two prey species

In freshwater ecosystems, inducible defenses that involve behavioral or morphological changes in response to chemical cue detection are key phenomena in prey–predator interactions. Many species with different phylogenetic and ecological traits (e.g., general activity patterns and microhabitats) use chemical cues to avoid predators. We hypothesized that prey species with a shared predator, but having different ecological traits, would be adapted to detect different chemical cues from the predator. However, the proximate mechanisms by which prey use chemical cues to avoid predation remain little known. Here, we tested our hypothesis by using fractionated chemical components from predatory dragonfly nymphs (Lesser Emperor, Anax parthenope julius) to trigger anti-predator behavioral responses in two anuran tadpoles, the wrinkled frog Glandirana (Rana) rugosa and the Japanese tree frog Hyla japonica. Glandirana rugosa detected chemical cues that had either high or low hydrophobic properties, but H. japonica responded only to chemical cues with hydrophilic properties. During the normal behaviors of these tadpole species, G. rugosa remains immobile in benthic habitats, whereas H. japonica exhibits active swimming at the surface or in the middle of the water column. As we had hypothesized, these tadpole species, which have different general activity levels and microhabitats, detected different chemical cues that were exuded by their shared predator and responded by changing their activities to avoid predation. The specific chemical cues detected by each tadpole species are likely to have characteristics that optimize effective predator detection and encounter avoidance of the shared dragonfly predator.     

Social learning and acquired recognition of a predator by a marine fish

Predation is known to influence the distribution of behavioural traits among prey individuals, populations and communities over both evolutionary and ecological time scales. Prey have evolved mechanisms of rapidly learning the identity of predators. Chemical cues are often used by prey to assess predation risk especially in aquatic systems where visual cues are unreliable. Social learning is a method of threat assessment common among a variety of freshwater fish taxa, which incorporates chemosensory information. Learning predator identities through social learning is beneficial to na?ve individuals as it eliminates the need for direct interaction with a potential threat. Although social learning is widespread throughout the animal kingdom, no research on the use of this mechanism exists for marine species. In this study, we examined the role of social learning in predator recognition for a tropical damselfish, Acanthochromis polyacanthus. This species was found to not only possess and respond to conspecific chemical alarm cues, but na?ve individuals were able to learn a predators' identity from experienced individuals, the process of social learning. Fish that learned to associate risk with the olfactory cue of a predator responded with the same intensity as conspecifics that were exposed to a chemical alarm cue from a conspecific skin extract.     

Prey behaviour across antipredator adaptation types: how does growth trajectory influence learning of predators?

Despite the fact that the ability of animals to avoid being consumed by predators is influenced by their behaviour, morphology and life history, very few studies have attempted to integrate prey responses across these adaptation types. Here, our goal was to address the link between life-history traits (size and growth trajectory) of tadpoles and behavioural responses to predators. Specifically, we wanted to determine whether information learned about predators was influenced by prey growth trajectory before and after learning. We manipulated the size/growth trajectory of tadpoles by raising them under different temperatures. Tadpoles raised on a slow-growth trajectory (under cold conditions) and taught to recognize a salamander subsequently showed stronger responses after 2 weeks than tadpoles that were raised on a fast-growth trajectory (under warm conditions). When we account for the effect of size (r ² = 0.22) on the responses of prey to predator cues, we find that the growth trajectory pre-learning but not post-learning influences the learned responses of the tadpoles. The differences in responses to predators may reflect differential memory associated with the predator. To our knowledge, this is the first study that has attempted to link life-history traits (size and growth rate) with learning of predators. In order to gain a comprehensive understanding of antipredator responses of prey animals, we call for additional integrative studies that examine prey anti-predator responses across adaptation types.     

Anuran tadpoles learn to recognize injury cues from members of the same prey guild

Recognition of predation risk from cues released from injured heterospecific could be beneficial when prey belongs to the same prey guild. Here, we performed three experiments. Experiment 1 showed that P. thaul tadpoles reduced their activity levels when exposed to conspecific injury cues, but not when exposed to amphipod injury cues. Experiment 2 tested whether P. thaul tadpoles can learn to recognize predation risk from chemical cues released from injured heterospecifics from the same prey guild (amphipod, Hyalella patagonica). A group of tadpoles were conditioned by exposing them to a specific concentration of amphipod injury cues paired with conspecific injury cues. Two days later, we evaluated changes in the activity of tadpoles when they were exposed to amphipod cues. As a control of learning, we used an unpaired group. Additionally, we used more control groups to fully investigate the learning mechanism. Our results showed that tadpoles can learn to recognize predation risk from injured amphipods and that the mechanism underlying the observed learned response could be associative. Experiment 3 replicated Experiment 2 and also showed that a low concentration of amphipod cues did not sustain that learning.     

A danger foreseen is a danger avoided: how chemical cues of different tadpoles influence parental decisions of a Neotropical poison frog

The protection of offspring against predators and competitors is especially important in organisms using spatially separated breeding resources, impeding the offspring’s chances to escape. One example of such isolated reproductive resources are phytotelmata (small water bodies in plant axils), exploited by the Neotropical poison frog Ranitomeya variabilis (Dendrobatidae) for both clutch and tadpole deposition. Because poison frog tadpoles are often cannibalistic, parents tend to avoid deposition with conspecifics. Previous studies have shown that this avoidance is based on chemical cues produced by conspecific tadpoles. Further, cues produced by phylogenetically less-related tadpoles (Bufonidae) were avoided for clutch but not tadpole depositions. We analyzed how the different responses to tadpole cues are triggered. We tested the reactions of parental R. variabilis to tadpole cues of species differing in two aspects: whether or not they are dendrobatids, and whether or not they reproduce in phytotelmata. We found that for clutch deposition, tadpole cues were always avoided, i.e., all tadpoles were treated by the frogs as if they pose a danger to the eggs. However, responses varied for tadpole depositions: while dendrobatid larvae living in phytotelmata were avoided, those breeding in streams were not. Non-poison frog tadpoles were ignored when associated with habitat other than phytotelmata, but they were preferred when living in phytotelmata. This suggests that both phylogeny and tadpole habitat are important triggers for the decisions made by R. variabilis. Only tadpoles using the same breeding resources are considered as relevant for the frog’s own larvae (i.e., as a potential danger or food resource), while further decisions are related to evolutionary relationship.     

An investigation of the alarm response in Bufo boreas and Rana cascadae tadpoles

Tadpoles of the western toad (Bufo boreas) and of the Cascades frog (Rana cascadae) show an alarm reaction to an extract containing chemical cues from damaged conspecifics. The mean time spent by individual B. boreas tadpoles in the half of the test tank to which the extract solution was added was significantly lower than expected by chance. Activity was also significantly greater in Bufo extract tests than in control tests. Tadpoles did not avoid an extract of another tadpole species (Hyla regilla). Rana cascadae tadpoles did not avoid areas containing Rana extract but did significantly increase their level of activity in response to the extract. These results suggest that the R. cascadae tadpole alarm reaction exists but differs from the B. boreas reaction.     

Understanding the role of uncertainty on learning and retention of predator information

Due to the highly variable nature of predation risk, prey animals need to continuously collect information regarding the risk posed by predators. One question that ensues is how long to use this information for? An adaptive framework of predator-related information use predicted that certainty should influence the duration for which information regarding the threatening nature of a species is used in decision-making. It predicts that uncertainty contributes to the reduction in the duration of information use, due to the cost of displaying antipredator behaviours towards non-threatening species. Here, we test this prediction using repetition of conditioning events as a way to increase the certainty associated with the predatory nature of a novel salamander for woodfrog tadpoles. Tadpoles were conditioned 1, 2 or 4 times to recognize a novel salamander as a predator and subsequently tested for their response to the salamander 1?day or 11?days post-conditioning. We found that conditioning repetition did not affect the intensity with which tadpoles learned to respond to the salamander after 1?day. However, after 11?days, tadpoles with fewer conditionings responded to the salamander with a weaker intensity than those that received more conditionings. Our results provide support for the model prediction that an increase in the certainty associated with correctly identifying a predator leads to longer retention of the threat.     

Stimulus control of predatory behavior by the Iberian wall lizard (Podarcis hispanica, Sauria, Lacertidae): effects of familiarity with prey

The authors examine the relative roles of vision and chemoreception and the influence of previous experience with prey on the predatory behavior of Iberian wall lizards (Podarcis hispanica). Experiment 1 compared the responses to visual, chemical, and a combination of visual and chemical cues of a familiar prey by 2 groups of lizards that had been kept in captivity for either 3 months or 21 days. Experiment 2 assessed the responses of lizards kept in the laboratory for more than 3 months to a novel prey species. The results reveal that feeding on a prey species affects the lizards' responses to chemical stimuli from that prey. The response to chemical cues of a novel prey requires a 1st-feeding experience with that prey. Lizards that have been fed the same prey species for several months cease responding to the chemical stimuli of that particular prey.     

Evolutionary persistence of chemically elicited ophiophagous antipredator responses in gartersnakes (Thamnophis sirtalis)

The ability to detect and respond to potential predators is key for the survival of individuals, but this ability is sometimes lost via relaxation of antipredator behavior when prey species are separated from predators. Adult and predator-na?ve neonate gartersnakes (Thamnophis sirtalis) from mainland and insular sites where they do and do not occur with ophiophagous (snake-eating) snakes were tested to determine if responses to such predators have been lost, reduced, or retained, and what might be causing differences in such responses. Our data indicate that, overall, adult snakes from populations syntopic with ophiophagous milksnakes are more responsive to chemical stimuli from milksnakes than adults from areas where they are not syntopic with milksnakes, whereas there were few differences with neonate gartersnakes. Experiments with neonates with or without periodic ophiophagous snake chemical experience over several weeks showed that gartersnakes with such experience became more responsive to ophiophagous cues rather than habituating to them. Such evidence of both genetic and experiential factors underlying the antipredator responses to ophiophagous snakes indicates that antipredator responses have persisted despite separation of predator and prey.     

The detection of certain predators via olfaction by small-mouthed salamander larvae (Ambystoma texanum)

Larvae of the small-mouthed salamander (Ambystoma texanum) showed an increase in refuge use when exposed to chemical cues from a predaceous fish. The percentage of time spent outside of refuge was significantly reduced relative to controls when larvae were exposed to chemical cues from fish, but was not different from the controls when larvae were exposed to chemical cues from three other potential predators. A. texanum larvae responded to these chemical cues via olfaction. Larvae that had their external nares plugged with a gelatinous paste did not respond to fish cues, while sham-treated larvae showed an avoidance of fish cues.     

Elasmobranch cognitive ability: using electroreceptive foraging behaviour to demonstrate learning, habituation and memory in a benthic shark

Top predators inhabiting a dynamic environment, such as coastal waters, should theoretically possess sufficient cognitive ability to allow successful foraging despite unpredictable sensory stimuli. The cognition-related hunting abilities of marine mammals have been widely demonstrated. Having been historically underestimated, teleost cognitive abilities have also now been significantly demonstrated. Conversely, the abilities of elasmobranchs have received little attention, despite many species possessing relatively large brains comparable to some mammals. The need to determine what, if any, cognitive ability these globally distributed, apex predators are endowed with has been highlighted recently by questions arising from environmental assessments, specifically whether they are able to learn to distinguish between anthropogenic electric fields and prey bioelectric fields. We therefore used electroreceptive foraging behaviour in a model species, Scyliorhinus canicula (small-spotted catshark), to determine cognitive ability by analysing whether elasmobranchs are able to learn to improve foraging efficiency and remember learned behavioural adaptations. Positive reinforcement, operant conditioning was used to study catshark foraging behaviour towards artificial, prey-type electric fields (Efields). Catsharks rewarded with food for responding to Efields throughout experimental weeks were compared with catsharks that were not rewarded for responding in order to assess behavioural adaptation via learning ability. Experiments were repeated after a 3-week interval with previously rewarded catsharks this time receiving no reward and vice versa to assess memory ability. Positive reinforcement markedly and rapidly altered catshark foraging behaviour. Rewarded catsharks exhibited significantly more interest in the electrical stimulus than unrewarded catsharks. Furthermore, they improved their foraging efficiency over time by learning to locate and bite the electrodes to gain food more quickly. In contrast, unrewarded catsharks showed some habituation, whereby their responses to the electrodes abated and eventually entirely ceased, though they generally showed no changes in most foraging parameters. Behavioural adaptations were not retained after the interval suggesting learned behaviour was not memorised beyond the interval. Sequences of individual catshark search paths clearly illustrated learning and habituation behavioural adaptation. This study demonstrated learning and habituation occurring after few foraging events and a memory window of between 12 h and 3 weeks. These cognitive abilities are discussed in relation to diet, habitat, ecology and anthropogenic Efield sources.     

Iberian rock lizards (Lacerta monticola) assess short-term changes in predation risk level when deciding refuge use

Prey might assess that risk level estimated in the first encounter with a predator was fixed in subsequent responses, whereas prey using flexible behavior would track short-term changes in risk. The authors examined, in the field, refuge use of Iberian rock lizards (Lacerta monticola) after simulated predator attacks and tested (a) how risk was assessed when multiple sources of risk were present simultaneously, (b) how short-term changes in risk level of successive attacks affected refuge use, and (c) whether the interval between attacks was important, insofar as attacks were considered to be coming from the same or different predators. Results suggest that lizards have a flexible estimate of risk that is based on multiple sources and flexibly dependent on previous estimates.     

Disturbance cues function as a background risk cue but not as an associative learning cue in tadpoles

Animal Cognition - Chemical information has an important role in the sensory ecology of aquatic species. For aquatic prey, chemical cues are a vital source of information related to predator...     

Predator videos and electric shock function as punishers for zebrafish (Danio rerio)

Zebrafish (Danio rerio) are a promising animal model for studying the effects of gene–environment interactions on behavior. Two experiments were conducted to assess punishment effects of presenting predator videos (Indian leaf fish; Nandus nandus) and electric shock on operant approach responses in zebrafish. In Experiment 1, the predator video and shock stimuli were presented upon a response maintained by a single variable‐interval schedule of food reinforcement in different groups of fish. In Experiment 2, the predator video and shock stimuli were presented upon one of two response alternatives maintain by concurrently available variable‐interval schedules of food reinforcement in different groups of fish. Responding decreased when the predator video and shock stimuli were presented relative to their absence in both experiments. Moreover, responding on an unpunished alternative did not reliably decrease in Experiment 2. These results indicate that the decrease in responding resulted from the punishment contingency rather than from elicited species‐specific defense responses or conditioned avoidance. Thus, the predator video and electric shock functioned as punishers of operant behavior for zebrafish. Identifying punishers for this species could lead to research on how gene–environment interactions influence individual differences in sensitivity to punishment.     

Sound localization in a predatory rodent, the northern grasshopper mouse (Onychomys leucogaster)

A comparison of the ability of mammals to localize sound revealed that among the animals examined to date, none of the rodents have been able to localize as accurately as the carnivores. Because all of these rodents are prey animals, the question arises as to whether their poor localization acuity is a phyletic trait of Rodentia or whether it is a trait common to prey species that may be under less selective pressure than predators to localize sound accurately. To answer this question, sound localization acuity was determined in a species that is both predatory and a rodent, the northern grasshopper mouse. Localization thresholds for a single 100-ms noise burst were determined for three grasshopper mice using a conditioned avoidance procedure. Their 50% discrimination threshold of 19 degrees is larger than that of any of the previously tested carnivores and well within the range of other rodents. However, calculations of the binaural sound localization cues available to rodents (based on their head size) suggest that the grasshopper mouse may make more efficient use of the available locus cues than other rodents. Thus, although the grasshopper mouse cannot localize as accurately as carnivores, it appears to be more accurate than predicted for a nonpredatory rodent of its size.     

Personality and the response to predation risk: effects of information quantity and quality

Within aquatic ecosystems, chemosensory cues provide valuable public information regarding the form and degree of risk, allowing prey to make informed behavioural decisions. Such cues, however, may vary in both relative concentration detected (i.e. ‘quantity’) and reliability of the information available (i.e. ‘quality’), leading to varying response patterns. Moreover, prey species are also known to exhibit consistent behavioural tactics towards managing risk (i.e. personality), possibly shaping their use of public information. Here, we present two experiments examining the potential interacting effects of personality and the quantity (Experiment 1) or quality (Experiment 2) of public information on the short-term predator avoidance responses of wild-caught Trinidadian guppies under semi-natural conditions. Our first experiment demonstrated that personality shaped responses to a high concentration of alarm cues (high risk), with shyer guppies exhibiting stronger antipredator responses than bolder guppies. When exposed to either low risk or stream water controls, personality had no effect on the intensity of response. Our second experiment demonstrated that personality again shaped the response to high concentrations of alarm cues (a known risk) but not to a novel chemosensory cue (tilapia odour). When exposed to the unknown novel cue, guppies exhibited a relatively high intensity antipredator response, regardless of personality. Combined, our results suggest that individual risk-taking tactics shape the use of public information in a context-dependent fashion.     

A cross-modal effect of noise: the disappearance of the alarm reaction of a freshwater fish

Anthropogenic noise pollution is recognized as a major global stressor of animals. While many studies have assessed the unimodal impacts of noise pollution with a focus on intraspecific acoustic communication, little is known about noise pollution on the perception of visual and chemical information. The ‘distracted prey hypothesis’ posits that processing noise interferes with processing other information in the brain. Here, we found evidence for such a cross-modal effect of noise on the antipredator behaviour of a freshwater prey fish, the fathead minnow, Pimephales promelas. In laboratory trials, exposure to noise from a motorboat caused the total absence of the classical fright reaction of minnows to conspecific alarm cues, whereas an ambient noise control had no such impact. In natural habitats, the impairment of such antipredator behaviour due to noise pollution could have major fitness consequences. We discuss how our findings translate to animal ecology and the need for future studies that target specific management decisions regarding noise pollution.