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Neophobia, the fear of novel stimuli, plays a major role in animal ecology. Here, we review studies on predator neophobia and explore its underlying patterns within an ecological framework. Predator neophobia is typically assessed by observing behaviours in novel areas that bring potential risk from unknown predators, or by observing behaviours towards certain kinds of objects and odours that are novel. We conducted a literature review across taxa, surveying research on baseline and induced neophobia versus controls. We calculated effect sizes for the intensity of neophobic responses, and categorized data according to six factors (taxa, age class, background type, trophic position, test cue type and experimental treatment type). While accounting for each of the other factors, we found that baseline neophobia was stronger among birds and mammals, and towards novel areas, relative to other taxa and cue types. Baseline neophobia was lower for wild-caught animals and for those that were higher in trophic position, compared with those reared in captivity and from lower trophic levels. By contrast, induced neophobia was similar in intensity across taxa, background types and testing cue types, while again being lower among upper trophic-level members and among juvenile animals. Although induced neophobia occurred across all treatment types, brain lesions induced stronger neophobia than predation risk or social isolation. We discuss potential mechanisms underlying these results and highlight gaps in the literature.

Prey face a major challenge in balancing predator avoidance with other essential activities. In environments with high risk, prey may exhibit neophobia (fear of novelty) due to the increased likelihood of novel stimuli being dangerous. The zebrafish, Danio rerio , is an established model organism for many scientific studies. Although spatial and object neophobia in zebrafish have received previous attention, little is known about the role of background risk in inducing neophobia in zebrafish. Here, we present two experiments using zebrafish to explore whether background predation risk can induce anxiety-like behaviour in a novel environment and neophobic responses when exposed to a novel odour. Over five days, we repeatedly exposed zebrafish to either high background risk in the form of chemical alarm cues (i.e., injured conspecific cues that indicate a predator attack) or a low-risk water control stimulus. In Experiment 1, when tested in a novel tank, zebrafish exposed to high predation risk displayed anxiety-like responses (reduced activity and increased bottom time spent) compared to their low-risk counterparts. Moreover, high-risk individuals showed reduced intra-session habituation to the novel tank compared to low-risk individuals. In Experiment 2, high-risk individuals exhibited fear responses toward a novel odour, unlike low-risk individuals. These results reveal that short-term repeated exposures to high risk can induce anxiety-like behaviour and predator odour neophobia in zebrafish.

Exposure to intense predation risk can induce morphological and behavioural phenotypes that prepare prey, often at young ages, for surviving attacks from unknown predators. However, previous studies revealed that this survival advantage depended on the predator species. Here, we used alarm cues from injured conspecifics to simulate a period of high predation risk for embryonic wood frogs, Lithobates sylvaticus. Two weeks post-hatching, we tested whether the embryonic risk exposure influenced survival in encounters with two novel predators: (1) a spider (Dolomedes sp.) that ambushes prey exclusively on the surface of the water, and (2) the adult predacious diving beetle (Dytiscus sp.) which displays underwater sit-and-wait posture and pursuit tactics. Tadpoles exposed to embryonic high-risk survived longer when encountering spiders, whereas background risk had no influence on survival with adult beetles. These findings, coupled with survival studies involving other predator types, indicate that a high-risk environment promotes tadpole survival in future encounters with unknown sit-and-wait predators, but at the cost of increased vulnerability to novel predators capable of active pursuit.

In the natural environment, animals can face potentially dangerous and often regular exposure to major environmental fluctuations such as flash flooding and drought, or the approach of a predator. For many aquatic species, exposure to these ecological disturbances triggers the release of “disturbance cues” – generally characterized as chemicals released when animals are startled but not injured. While the chemistry of such cues remains largely unexplored, they appear to provide early warning information to nearby individuals, potentially leading to behavioral decisions that increase overall fitness, particularly for social species that may coordinate group defense. In the literature, disturbance cues have received little attention relative to other chemical cues, such as damage-released alarm cues. However, recent advances in the study of disturbance cue communication have led an uptick in research on the subject. Here, we review the existing literature on responses to disturbance cues in aquatic systems. Although the majority of studies involve behavioral responses to a simulated predator approach, we describe various disturbance types across a broad range of taxa. We discuss the ecological implications of disturbance cues, including their role in risk assessment, signaling, learning, and species specificity. We also address several methodological challenges for this developing field of study, as well as the ethical and conservation implications of this research going forward. Future research on disturbance cues should address a number of key unknowns, including questions regarding disturbance cue chemistry, function, and generality.

Although salamanders have been shown to respond to classical conditioning, spatial learning has been largely unstudied. We tested whether salamanders could learn to locate foraging areas by using landmarks. We trained 10 salamanders Plethodon angusticlavius to use landmarks （small rocks） to locate patches within the arena containing food （blackworms Lumbriculus variegatus）. At the comers of each square testing arena were four plastic dishes, one containing blackworms and the other three empty. A rock was placed in front of the dish containing blackworms, and the location of the food-dish was randomly chosen for each training trial. A control group was also trained to feed on blackworms in the presence of a rock, but the rock was positioned randomly among the four dish locations so that the rock was not a reliable landmark for the worms. Although the length of the training period for individual salamanders varied （22-38 trainings per individual）, the mean number of trainings for salamanders in the control and experimental groups was equal （30 training trials）. During testing, no blackworms were present to eliminate any visual or chemical cues emanating directly from the prey. Individuals trained with the rock landmarks spent sig- nificantly more time in the area of the landmark than did control salamanders [Current Zoology 57 （4）： 485-490, 2011].

Decision-making among prey often involves balancing fitness-related activities, such as foraging and mating, with the need to avoid predation. These trade-offs may be influenced by sex, especially among sexually dimorphic species where males and females face different selection pressures. Consistent with the ‘Distracted Male Hypothesis’, male Trinidadian guppies ( Poecilia reticulata ), may show a reduced response to publicly available personal risk assessment cues (i.e. chemosensory predation risk cues) relative to females due to the relatively high costs associated with lost courtship and mating opportunities. Male guppies may compensate for a reduced response to personal information by increasing their use of conspecifics as a source of social information. Here, we tested this hypothesis using wild-caught male Trinidadian guppies, examining their use of visual social cues from alarmed conspecific males in the presence vs. absence of females. We found that when stimulus females were absent, focal males increased their inspection of an alarmed male stimulus shoal, suggesting the use of social information. However, when a stimulus female was present, males did not increase inspection of the male stimulus shoal. Rather, they exhibited high rates of inspection towards the female stimulus. These suggest that male guppies may adjust their antipredator behaviour depending on social context, likely reflecting underlying reproductive trade-offs.

Exposure to predation risk can induce a fearful baseline state, as well as fear reactions toward novel situations (i.e., neophobia). Some research indicates that risk exposure during sensitive periods makes adults more prone to acquiring long-term fearful phenotypes. However, chronic risk can also lead to ignoring threats in order to maintain other activities. We sought to assess how a relatively long period of low risk, experienced either early in life or by the previous generation, influences fear behaviour acquired from a short period of high risk as adults. We used fathead minnows as study subjects and simulated predation risk with repeated exposures to conspecific chemical alarm cues. The period of high risk experienced by adults induced typical fear behaviour (baseline freezing and neophobia), whereas the early-life low-risk period 1 year prior caused only a reduction in baseline foraging. We found no evidence that the early-life risk significantly altered the fear acquired from the adult-risk period. However, in a second experiment, a low-risk period during the parental generation interacted with a high-risk period experienced by the adult offspring. The combination of both risk periods heightened baseline freezing despite parental risk having little effect independently. Hence, our study provides evidence that parental risk exposure can lead to an additive intergenerational effect on fear acquisition in minnows.

Under predation threat, many species produce cues that can serve as crucial sources of information for social companions. For instance, chemical cues released when experiencing a disturbing event (i.e. ‘disturbance cues’), such as a predator chase, can lead to antipredator avoidance and increased survival for nearby individuals. These chemicals also have potential to be produced as a voluntary signal for communicating threat to others. We found evidence for this hypothesis by manipulating the shoal familiarity of guppies from populations differing in background predation risk and then presenting their disturbance cues to unfamiliar conspecifics from the same populations. Receivers from low-risk sites increased shoal cohesion and decreased area use regardless of whether the disturbance cues were produced in donor groups where members were familiar or unfamiliar with each other. However, receivers from high-risk sites showed strong antipredator reactions towards disturbance chemicals produced in familiar groups and no response towards those produced in unfamiliar groups, suggesting that donors from high-risk sites may alter the quality or quantity of their disturbance cues to influence familiar individuals to enact predator defences. Because high-risk environments strengthen guppy social networks, these environments may facilitate reliance on chemical disturbance signalling to coordinate group defences with familiar individuals.

Through time, the activity patterns, morphology, and development of both predators and prey change, which in turn alter the relative vulnerability of prey to their coexisting predators. Recognizing these changes can thus allow prey to make optimal decisions by projecting risk trends into the future. We used tadpoles ( Lithobates sylvaticus ) to test the hypothesis that tadpoles can extrapolate information about predation risk from past information. We exposed tadpoles to an odour that represented either a temporally consistent risk or an increasing risk. When tested for their response to the odour, the initial antipredator behaviour of tadpoles did not differ, appearing to approach the limit of their maximum response, but exposure to increasing risk induced longer retention of these responses. When repeating the experiment using lower risk levels, heightened responses occurred for tadpoles exposed to increasing risk, and the strongest responses were exhibited by those that received an abrupt increase compared to a steady increase. Our results indicate that tadpoles can assess risk trends through time and adjust their antipredator responses in a way consistent with an extrapolated trend. This is a sophisticated method for prey to avoid threats that are becoming more (or less) dangerous over part of their lifespan.

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.