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.     

Prey positions as consumers' behavioural patterns: Exploratory evidence from an fMRI study

The present article reviews some of the tenets of the Consolidated Model of Financial Predation (CMFP). The CMFP is used to explain how investors behave as either predators or prey in the financial markets, for example, during the 2008 predatory‐mortgages crisis. The article tests one of its key assumptions: that is, that people adopt different levels of prey positions. In the last four years, a number of articles have been published on the CMFP, which states that people adopt either a predator or a prey position (PPP), or else a mixture of both. The model has emerged as a result of a five‐year study and has found various applications, in particular, in the field of behavioural finance. According to this model, consumers of financial products tend to position themselves as either predators or prey. In the latter case, this causes them to judge the relationship in negative terms and to experience it as less rewarding, if not punishing altogether. This has two effects: first, perceived predation tends to gain in power and second, purchasing decisions may not be optimal. Results from an exploratory functional magnetic resonance imaging (fMRI) study aimed at generating prey positions in minimal stress conditions are presented; they show that there is a significant difference between at least two prey positions, labelled “known predator–prey position” (KPPP) and “unknown predator–prey position” (UPPP). This means that consumers of financial products could potentially face two levels of apprehension (perceived predation): a high one under uncertainty and a lower one when conditions are volatile. Copyright © 2016 John Wiley & Sons, Ltd.     

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.     

Risk-induced neophobia: does sensory modality matter?

Recent studies have documented that exposure to high levels of background risk can induce neophobic predator avoidance in prey animals, whereby they respond to any novel cue with an anti-predator response. Such phenotypically plastic predator avoidance may allow prey to maximize anti-predator benefits in variable risk environments. It remains poorly understood whether risk assessment information from different sensory modalities can be integrated to induce generalized, cross-sensory system neophobic responses. Here, we directly test this hypothesis by exposing juvenile convict cichlids (Amatitlania nigrofasciata) to high- versus low-risk environments using either conspecific alarm cue (chemosensory risk) or a model avian predator (visual/mechanical risk) and testing their response to a novel chemosensory cue (Experiment 1) or visual cue (Experiment 2). Our results suggest that regardless of the sensory modality used to increased perceived risk, cichlids pre-exposed to high-risk conditions exhibited increased predator avoidance in response to any novel visual or chemical cue. As expected, cichlids pre-exposed to low-risk conditions did not display any neophobic responses. Our results suggest that induced neophobia is not cue specific; rather, it may function as a generalized response to perceived predation risk.     

Assessment of predation risk through conspecific cues by anuran larvae

Animal Cognition - Accurate assessment of predation risk is critical for prey survival during predator–prey interactions. Prey can assess predation risk by the presence of cues dropped by...     

Aposematic colouration and avoidance learning in chicks

Two groups of male chicks (Gallus gallus) were allowed to peck at distasteful food (chick crumbs flavoured with quinine and mustard) that either matched or contrasted with the background on which the food was presented. The experiment consisted of a series of trials, each of which was terminated when a fixed amount of food (four crumbs) had been ingested. Within-trial pecking rate was initially higher in the group given constrasting food, confirming that degree of contrast between a prey item and its background increases the likelihood of detection by a naive predator. However, during the series of training trials pecking rate declined faster, and reached a lower level, in the group given contrasting food than in the group given matching food. Thus, rate and strength of avoidance learning are affected by the degree to which distasteful food contrasts with its background. This may explain why many distasteful prey species are brightly coloured, despite the fact that bright colouration increases the likelihood of initial detection by a predator.     

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.     

Specialised use of working memory by Portia africana,a spider-eating salticid

Using expectancy–violation methods, we investigated the role of working memory in the predatory strategy of Portia africana, a salticid spider from Kenya that preys by preference on other spiders. One of this predator’s tactics is to launch opportunistic leaping attacks on to other spiders in their webs. Focussing on this particular tactic, our experiments began with a test spider on a ramp facing a lure (dead prey spider mounted on a cork disc) that could be reached by leaping. After the test spider faced the lure for 30 s, we blocked the test spider’s view of the lure by lowering an opaque shutter before the spider leapt. When the shutter was raised 90 s later, either the same lure came into view again (control) or a different lure came into view (experimental: different prey type in same orientation or same prey type in different orientation). We recorded attack frequency (number of test spiders that leapt at the lure) and attack latency (time elapsing between shutter being raised and spiders initiating a leap). Attack latencies in control trials were not significantly different from attack latencies in experimental trials, regardless of whether it was prey type or prey orientation that changed in the experimental trials. However, compared with test spiders in the no-change control trials, significantly fewer test spiders leapt when prey type changed. There was no significant effect on attack frequency when prey orientation changed. These findings suggest that this predator represents prey type independently of prey orientation.     

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 predators overcome visual illusion: dazzle coloration does not protect moving prey

Predators everywhere impose strong selection pressures on the morphology and behavior of their prey, but the resulting antipredator adaptations vary greatly among species. Studies of adaptive coloration in prey species have generally focused on cryptic or aposematic prey, with little consideration of color patterns in palatable mobile prey. Complex color patterns have been proposed to decrease the ability of visual predators to capture moving prey (motion dazzle effect). Most support for this hypothesis, however, comes from experiments with human subjects and simulated prey. We tested the motion dazzle effect using, for the first time, natural predators (cane toads, Rhinella marina) and live prey (house crickets, Acheta domesticus) with altered color patterns. We found no support for the motion dazzle effect as striped crickets did not fare better than solid colored ones. Crickets that spent more time moving, however, were more likely to be eaten. Our results suggest that motion specialized visual predators such as toads overcome the motion dazzle effect and impose stronger selection pressure on prey behavior than on coloration. These findings emphasize the importance of sensory specializations of predators in mediating antipredator strategies.     

Influence of age,breeding state and approach direction on sensitivity to human gaze: a field study on Azure-winged magpies

Animal Cognition - In predator–prey interactions, various factors affect the prey’s perception of risk and decision to flee. Gaze sensitivity, the ability to react to the presence,...     

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.     

Behavioral anatomy of a hunt

It is commonly thought that the mind constructs predictive models of the environment to plan an appropriate behavioral response. Therefore a more predictable environment should entail better performance, and prey should move in an unpredictable (random) manner to evade capture, known as protean motion. To test this, we created a novel experimental design and analysis in which human participants took the role of predator or prey. The predator was set the task of capturing the prey, while the prey was set the task of escaping. Participants performed this task standing on separate sides of a board and controlling a marker representing them. In three conditions, the prey followed a pattern of movement with varying predictability (predictable, semi-random, and random) and in one condition moved autonomously (user generated). The user-generated condition illustrated a naturalistic, dynamic environment involving a purposeful agent whose degree of predictability was not known in advance. The average distance between participants was measured through a video analysis custom-built in MATLAB. The user-generated condition had the largest average distance. This indicated that, rather than moving randomly (protean motion), humans may naturally employ a cybernetic escape strategy that dynamically maximizes perceived distance, regardless of the predictability of this strategy.

     

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.     

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...     

A chamber for separating visual and physical prey access from predators

A chamber is described that provides automated separation of various phases of depredation dynamics. Two solenoid actuated doors control visual and physical access to prey items. A lever operandum is programmable to require differential response outputs by the predator. Search lever responses open one door and allow detection which may then be followed by pursuit lever responses and ultimate access for capture. The chamber is suitable for such medium sized predators as foxes and coyotes.     

Learning, memorizing and apparent forgetting of chemical cues from new predators by Iberian green frog tadpoles

Many antipredator adaptations are induced by the prey’s ability to recognize chemical cues from predators. However, predator recognition often requires learning by prey individuals. Iberian green frog tadpoles (Pelophylax perezi) have the ability to learn new potential predators. Here, we tested the memory capabilities of Iberian green frog tadpoles. We conditioned tadpoles with chemicals cues from a non-predatory fish in conjunction with conspecific alarm cues, and examined whether tadpoles retained their conditioned response (reduction of activity level). We found that conditioned tadpoles reduced their activity levels in subsequent exposures to the non-predatory fish cues alone. Tadpoles were able to remember this association and reduced movement rate at least for 9 days after. The ability to learn and memorize potential predators may be especially important for the survivorship of prey species that are likely to find a high variety of predators. However, after those 9 days, there was a lack of response to the non-predatory fish cues alone in the absence of reinforcement. This could be explained if tadpoles behave according to the threat-sensitive predator avoidance hypothesis, and the perceived risk to the learning cue diminished over time, or it could be due to an apparent forgetting process to avoid non-adaptative responses to chemical cues of non-dangerous species that were randomly paired with alarm cues. Thus, this study demonstrates that green frog tadpoles in the absence of reinforcement remember the chemical cues of a learned predator only for a limited time that may be adaptative in a threat-sensitive context.     

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.     

Glucocorticoids are required for extinction of predator stress-induced hyperarousal

Background

The role of glucocorticoids in extinction of traumatic memories has not been fully characterized despite its potential as a therapeutic target for acquired posttraumatic stress disorder (PTSD). The predator stress paradigm allows us to determine whether glucocorticoids mediate the extinction of both context-dependent and context-independent fear memories.

Methods

Male C57BL/6J mice were exposed to a predator (cat) then repeatedly exposed to the predator stress context in the absence of the cat. Context-dependent (associative) fear memory was assessed as suppression of activity during re-exposure to the predator stress context without the cat (extinction trials). Context-independent fear (non-associative) was assessed seven days after extinction trials using measures of hyperarousal and anxiety-like behaviours in environments unlike the predator stress context. To assess the role of glucocorticoids, mice were injected with metyrapone (50 mg/kg) 90 min prior to extinction trials in predator stressed mice and context-dependent and context-independent fear memories were assessed. Finally, metyrapone-treated predator stressed mice were injected with corticosterone (5 or 10 mg/kg) immediately following extinction trials and context-dependent and context-independent fear memories were assessed.

Results

Repeated re-exposure to the predator stress context without the cat present extinguished context-dependent fear memory, and also reduced hyperarousal, a generalized, chronic PTSD-like symptom. We show that extinction of context-independent predator stress-induced hyperarousal is dependent on endogenous glucocorticoids during the extinction trials. Furthermore, the inhibition of extinction by metyrapone on startle amplitude was reduced by exogenous administration of corticosterone following extinction trials. Overall, these data implicate glucocorticoids in the extinction of hyperarousal, a core symptom of PTSD.     

Tufted titmouse (Baeolophus bicolor) calling and risk-sensitive foraging in the face of threat

Individuals often produce alarm or mobbing calls when they detect a threat such as a predator. Little is known about whether such calling is affected by the facial orientation of a potential threat, however. We tested for an effect of facial orientation of a potential threat on tufted titmice, Baeolophus bicolor, a songbird that uses chick-a-dee calls in a variety of social contexts. In two studies, a human observer wore an animal mask that either faced or faced away from the focal bird(s). In Study 1, focal birds were individual titmice captured in a walk-in trap, and the observer stood near the trapped bird. In Study 2, focal birds were titmouse flocks utilizing a feeding station and the observer stood near the station. In both studies, calling behavior was affected by mask orientation. In Study 2, foraging and agonistic behavior were also affected. Titmice can therefore perceive the facial orientation of a potential threat, and this perception affects different behavioral systems, including calling. Our results indicate sensitivity of titmice to the facial orientation of a potential predator in two quite different motivational contexts. This work suggests the possibility of strategic signaling by prey species depending upon the perceptual space of a detected predator.