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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

Comparing the effects of implicit and explicit temporal expectation on choice response time and response conflict

People can use temporally structured sensory information to anticipate future events. Temporal information can be presented implicitly through probability manipulation without participants’ awareness of the manipulation, or explicitly conveyed through instructions. We examined how implicit and explicit temporal information established temporal expectations that influenced choice response times and response conflict (measured as flanker effects). We implicitly manipulated temporal structure by block-wise varying the likely timing of a target. In the short-interval block, a target was presented frequently (80 % of trials) after a short (400 ms) cue-to-target interval and infrequently (20 % of trials) after a long (1200 ms) interval; the probability assignment was reversed in the long-interval block. Building on this baseline condition (Experiment 1), we augmented the temporal information by filling the cue-to-target intervals with tones (Experiment 2), explicitly informed participants of the prevalent time interval (Experiment 3) and provided trial-by-trial reminders of the prevalent time interval (Experiment 4). The temporal probability manipulation alone (of which participants were unaware) influenced choice response times but only when the temporal information was augmented with tones, whereas providing the explicit knowledge of the temporal manipulation, with or without trial-by-trial reminders, robustly influenced choice response times. Response conflict was unaffected by these conditions. These results suggest that temporal expectation can be established by the implicit learning of a temporal structure given that sufficiently strong temporal information is presented as well as by the explicit knowledge of the temporal structure. This established temporal expectation influences choice response times without necessarily affecting the strength of response conflict.     

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.     

Selective attention in peacocks during predator detection

Predation can exert strong selective pressure on the evolution of behavioral and morphological traits in birds. Because predator avoidance is key to survival and birds rely heavily on visual perception, predation may have shaped avian visual systems as well. To address this question, we examined the role of visual attention in antipredator behavior in peacocks (Pavo cristatus). Peacocks were exposed to a model predator while their gaze was continuously recorded with a telemetric eye-tracker. We found that peacocks spent more time looking at and made more fixations on the predator compared to the same spatial location before the predator was revealed. The duration of fixations they directed toward conspecifics and environmental features decreased after the predator was revealed, indicating that the peacocks were rapidly scanning their environment with their eyes. Maximum eye movement amplitudes and amplitudes of consecutive saccades were similar before and after the predator was revealed. In cases where conspecifics detected the predator first, peacocks appeared to learn that danger was present by observing conspecifics’ antipredator behavior. Peacocks were faster to detect the predator when they were fixating closer to the area where the predator would eventually appear. In addition, pupil size increased after predator exposure, consistent with increased physiological arousal. These findings demonstrate that peacocks selectively direct their attention toward predatory threats and suggest that predation has influenced the evolution of visual orienting systems.     

Processing of global and local information in memory

The experiments reported in this paper were designed to test how global and local information are processed by the memory system. When subjects are required to match a given letter with either a previously presented large capital letter or the small capital letters comprising it, (1) responses to the global level (i.e. the big letter) are faster than responses to the local level (i.e. the small letters), and (2) responses to the latter level only are affected by the consistency between the large and the small letters (Experiment 2), a pattern similar to that obtained in perception (Experiment 1). Such results obtain when subjects are required to attend to only one level with a short ISI between the first and second stimulus, but not when a longer ISI is used (Experiment 5) or when subjects are required to attend to both levels at the same time (Experiments 3 and 4). The results are discussed in the light of a model that postulates a temporal precedence of the global information over the local one at the perceptual level.     

Contextual Pavlovian conditioning in the crab Chasmagnathus

In contextual conditioning, a complex pattern of information is processed to associate the characteristics of a particular place with incentive or aversive reinforcements. This type of learning has been widely studied in mammals, but studies of other taxa are scarce. The context-signal memory (CSM) paradigm of the crab Chasmagnathus has been extensively used as a model of learning and memory. Although initially interpreted as habituation, some characteristics of contextual conditioning have been described. However, no anticipatory response has been detected for animals exposed to the training context. Thus, CSM could be interpreted either as an associative habituation or as contextual conditioning that occurs without a context-evoked anticipatory response. Here, we describe a training protocol developed for contextual Pavlovian conditioning (CPC). For each training trial, the context (conditioned stimulus, CS) was discretely presented and finished together with the unconditioned stimulus (US). In agreement with the CSM paradigm, a robust freezing response was acquired during the 15 training trials, and clear retention was found when tested with the US presentation after short (2 and 4 h) and long (1–4 days) delays. This CPC memory showed forward but not simultaneous presentation conditioning and was context specific and protein synthesis dependent. Additionally, a weak CPC memory was enhanced during consolidation. One day after training, CPC was extinguished by repeated CS presentation, while one presentation induced a memory labilisation–reconsolidation process. Finally, we found an anticipatory conditioned response (CR) during the CS presentation for both short-term (4 h) and long-term memory (24 h). These findings support the conditioning nature of the new paradigm.     

Information structuring improves recall of emergency discharge information: a randomized clinical trial

This article examines the extent to which structuring Emergency Department discharge information improves the ability to recall that information, and whether such benefits interact with relevant prior knowledge. Using three samples of students with different levels of prior medical knowledge, we investigated the amount of information recalled after structured vs. non-structured presentation of information. Across all student samples, the structured discharge information led to a relative increase in recalled items of 17% compared to non-structured discharge information (M = 9.70, SD = 4.96 vs. M = 8.31, SD = 4.93). In the sample with least medical knowledge, however, the structured discharge information resulted in a relative increase in recall by 42% (M = 8.12 vs. M = 5.71). These results suggest that structuring discharge information can be a useful tool to improve recall of information and is likely to be most beneficial for patient populations with lower levels of medical knowledge.     

Ontogeny of object permanence in a non-storing corvid species, the jackdaw (Corvus monedula)

The aim of the present study was to investigate the ontogeny of object permanence in a non-caching corvid species, the jackdaw (Corvus monedula). Jackdaws are often presented as typical examples of non-storing corvids, as they cache either very little or not at all. We used Uzgiris and Hunt’s Scale 1 tasks to determine the age at which the certain stages set in and the final stage of this capacity that is reached. Our results show that the lack of food-storing behaviour is not associated with inferior object permanence abilities in the jackdaw, as our subjects (N = 19) have reached stage 5 competence (to follow successive visible displacements) at the average age of 61 days post-hatch and showed some evidence of stage 6 competence (to follow advanced invisible displacements) at 81 days post-hatch and thereafter. As we appreciate that object permanence abilities have a very wide ecological significance, our positive results are probably the consequence of other, more fundamental ecological pressures, such as nest-hole reproduction or prey–predator interactions.     

Reflexive orienting in response to short- and long-duration gaze cues in young,young-old,and old-old adults

Shifting visual focus on the basis of the perceived gaze direction of another person is one form of joint attention. In the present study, we investigated whether this socially relevant form of orienting is reflexive and whether it is influenced by age. Green and Woldorff (Cognition 122:96–101, 2012) argued that rapid cueing effects (i.e., faster responses to validly than to invalidly cued targets) were limited to conditions in which a cue overlapped in time with a target. They attributed slower responses following invalid cues to the time needed to resolve the incongruent spatial information provided by the concurrently presented cue and target. In the present study, we examined the orienting responses of young (18–31 years), young-old (60–74 years), and old-old (75–91 years) adults following uninformative central gaze cues that overlapped in time with the target (Exp. 1) or that were removed prior to target presentation (Exp. 2). When the cue and target overlapped, all three groups localized validly cued targets more quickly than invalidly cued targets, and validity effects emerged earlier for the two younger groups (at 100 ms post-cue-onset) than for the old-old group (at 300 ms post-cue-onset). With a short-duration cue (Exp. 2), validity effects developed rapidly (by 100 ms) for all three groups, suggesting that validity effects resulted from reflexive orienting based on the gaze cue information rather than from cue–target conflict. Thus, although old-old adults may be slow to disengage from persistent gaze cues, attention continues to be reflexively guided by gaze cues late in life.