Uncertainty about predation risk: a conceptual review.

Uncertainty has long been of interest to economists and psychologists and has more recently gained attention among ecologists. In the ecological world, animals must regularly make decisions related to finding resources and avoiding threats. Here, we describe uncertainty as a perceptual phenomenon of decision-makers, and we focus specifically on the functional ecology of such uncertainty regarding predation risk. Like all uncertainty, uncertainty about predation risk reflects informational limitations. When cues are available, they may be novel (i.e. unknown information), incomplete, unreliable, overly abundant and complex, or conflicting. We review recent studies that have used these informational limitations to induce uncertainty of predation risk. These studies have typically used either over-responses to novelty (i.e. neophobia) or memory attenuation as proxies for measuring uncertainty. Because changes in the environment, particularly unpredictable changes, drive informational limitations, we describe studies assessing unpredictable variance in spatio-temporal predation risk, intensity of predation risk, predator encounter rate, and predator diversity. We also highlight anthropogenic changes within habitats that are likely to have dramatic impacts on information availability and thus uncertainty in antipredator decisions in the modern world.

Olfaction and reaction: The role of olfactory and hypothalamic investment in the antipredator responses to chemical alarm cues by northern redbelly dace.

Neuroplasticity enables teleosts to promote or downregulate the growth of their brains regionally. To compensate for the effects of predation pressure, teleosts may alter their brain morphology and behavioral responses to mitigate its impact on individual fitness. High-predation environments often promote specific patterns of brain growth and produce bolder and more proactive populations. Owing to the expense of maintaining neural tissue, relative size indicates the regions most relied upon. In northern redbelly dace Chrosomus eos, as little as 2 weeks of elevated predation pressure, resulted in increased investment in their olfactory bulbs and optic tecta, while the imposition of captivity produced smaller, less symmetric hypothalami. Taken together, these results suggest that an individual could potentially become better able to detect a threat, and simultaneously less inclined to react to it, making the impact of either change in isolation is difficult to discern. Here, we compared interindividual variation in gross brain morphology, risk-taking tactics in a novel arena (shy-bold personality), and responding to olfactory cues (proactive/reactive stress-coping style). We hypothesized that olfactory investment would positively correlate with response intensity to predator cue concentration and respond across a wider range of cue concentrations, while hypothalamus size would correlate with shyness and reactivity. Exposure to heightened risk produced more bold/proactive individuals, with larger olfactory bulbs and smaller hypothalami. However, the direction of the correlation between hypothalamus size and behavior varied by treatment, and olfactory investment only corresponded with response intensity amongst proactive individuals. Our findings illustrate the potential pitfalls of relating gross brain morphology to complex behavior and suggest that stress-coping style is a relevant consideration in future studies.

Microhabitat conditions drive uncertainty of risk and shape neophobic responses in Trinidadian guppies, Poecilia reticulata.

In response to uncertain risks, prey may rely on neophobic phenotypes to reduce the costs associated with the lack of information regarding local conditions. Neophobia has been shown to be driven by information reliability, ambient risk and predator diversity, all of which shape uncertainty of risk. We similarly expect environmental conditions to shape uncertainty by interfering with information availability. In order to test how environmental variables might shape neophobic responses in Trinidadian guppies (Poecilia reticulata), we conducted an in situ field experiment of two high-predation risk guppy populations designed to determine how the 'average' and 'variance' of several environmental factors might influence the neophobic response to novel predator models and/or novel foraging patches. Our results suggest neophobia is shaped by water velocity, microhabitat complexity, pool width and depth, as well as substrate diversity and heterogeneity. Moreover, we found differential effects of the 'average' and 'variance' environmental variables on food- and predator-related neophobia. Our study highlights that assessment of neophobic drivers should consider predation risk, various microhabitat conditions and neophobia being tested. Neophobic phenotypes are expected to increase the probability of prey survival and reproductive success (i.e. fitness), and are therefore likely linked to population health and species survival. Understanding the drivers and consequences of uncertainty of risk is an increasingly pressing issue, as ecological uncertainty increases with the combined effects of climate change, anthropogenic disturbances and invasive species.

Disturbance cue communication is shaped by emitter diet and receiver background risk in Trinidadian guppies.

In animal communication systems, individuals that detect a cue (i.e., "receivers") are often influenced by characteristics of the cue emitter. For instance, in many species, receivers avoid chemical cues that are released by emitters experiencing disturbance. These chemical "disturbance cues" appear to benefit receivers by warning them about nearby danger, such as a predator's approach. While the active ingredients in disturbance cues have been largely unexplored, by-products of metabolized protein are thought to play a role for some species. If so, the content (quality) and volume (quantity) of the emitter's diet should affect their disturbance cues, thus altering how receivers perceive the cues and respond. Guppies Poecilia reticulata are a species known to discriminate among disturbance cues from different types of donors, but dietary variation has yet to be explored. In this study, we found evidence that diet quality and quantity can affect disturbance cues released by guppy emitters (i.e., experimental "donors"). Receivers discriminated between donor cue treatments, responding more strongly to cues from donors fed a protein-rich bloodworm diet (Experiment 1), as well as an overall larger diet (Experiment 2). We also found that receivers exposed to higher background risk were more sensitive to disturbance cue variation, with the strongest avoidance responses displayed by high-risk receivers toward disturbance cues from donors fed the high-quality diet. Therefore, diet, and perhaps protein specifically, affects either the concentration or composition of disturbance cues released by guppies. Such variation may be important in information signaling in social species like the guppy.

Assessing effects of predator density and diversity on neophobia in Trinidadian guppies.

Neophobic predator avoidance, where prey actively avoid novel stimuli, is thought to allow prey to cope with the inability to predict predation risk (i.e. uncertainty) while reducing the costs associated with learning. Recent studies suggest that neophobia is elicited as a response to unpredictable and elevated mean predation risk, and is linked to experience with diverse novel cues. However, no research has disentangled the effects of predator density and diversity on neophobia. We conditioned Trinidadian guppies (Poecilia reticulata) to high- or low-diversity predator model treatments paired with high, intermediate, or low concentrations of conspecific alarm cues as a proxy for predator density. We tested behavioural responses to a novel stimulus vs. a water control to determine differences in neophobia among treatments. We found that neophobic shoaling behaviour was shaped by mean risk (predator density). However both density and diversity shaped neophobic freezing, and to a weaker extent, neophobic area use. Our research suggests that predator diversity might elicit neophobic responses in guppies, but only when mean risk is high enough. The relationship between neophobia and components of predation risk is becoming increasingly relevant as ecological uncertainty becomes more prevalent with increasing climate change, anthropogenic impacts, and invasive species.

Exploratory decisions of Trinidadian guppies when uncertain about predation risk.

Animals can reduce their uncertainty of predation risk by gathering new information via exploration behaviour. However, a decision to explore may also be costly due to increased predator exposure. Here, we found contextual effects of predation risk on the exploratory activity of Trinidadian guppies Poecilia reticulata in a novel environment. First, guppies were exposed to a 3-day period of either high or low background predation risk in the form of repeated exposure to either injured conspecific cues (i.e. alarm cues) or control water, respectively. A day later, guppies were moved into a testing arena with limited visual information due to structural barriers and were then presented with an acute chemical stimulus, either alarm cues (a known and reliable indicator of risk), a novel odour (an ambiguous cue), or control water. In the presence of control water, guppies from high and low background risk showed a similar willingness to explore the arena. However, high-risk individuals significantly reduced their spatial evenness, although not their movement latency, in the presence of both the alarm and novel cues. When these high-risk individuals were a member of a shoal, they became willing to explore the environment more evenly in the presence of alarm cues while remaining cautious toward the novel cue, indicating an effect of the greater uncertainty associated with the novel cue. In contrast, low-risk guppies showed a willingness to explore the arena regardless of acute threat or social context. Such contextual effects of background risk and social context highlight the complexity of exploratory decisions when uncertain.

Early-life and parental predation risk shape fear acquisition in adult minnows.

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.

Exploring the threat-sensitive predator avoidance hypothesis on mate competition in two wild populations of Trinidadian guppies.

The intensity of mate competition is often influenced by predation pressure. The threat-sensitive predator avoidance hypothesis predicts that prey should precisely adjust their fitness-related activities to the level of perceived acute predation risk and this effect should be stronger under high background risk. Individuals should compensate during periods of moderate risk for lost opportunities during high risk. Our study examined the interaction between acute and background predation risk on mate competition. Under laboratory conditions, we explored the effects of acute risk (low vs. high) using chemical alarm cue (AC; control (results presented in Chuard et al. (2016)) The effects of adult sex ratio on mating competition in male and female guppies (Poecilia reticulata) in two wild populations. Behav Process 129:1-10), 25 % concentration, and 100 % concentration), and population of origin (low vs. high background risk) on mate competition in guppies (Poecilia reticulata). Surprisingly, males favored courtship over forced mating under acute predation risk irrespective of background risk, potentially benefiting from a female preference for bold males. We discuss our results in the context of chemical threat-sensitivity and resource differences in defendability (e.g. mates vs. food).

The propensity for re-triggered predation fear in a prey fish.

Variation in predation risk can drive variation in fear intensity, the length of fear retention, and whether fear returns after waning. Using Trinidadian guppies, we assessed whether a low-level predation threat could easily re-trigger fear after waning. First, we show that background risk induced neophobia after either multiple exposures to a low-level threat or a single exposure to a high-level threat. However, a single exposure to the low-level threat had no such effect. The individuals that received multiple background exposures to the low-level threat retained their neophobic phenotype over an 8-day post-risk period, and this response was intensified by a single re-exposure to the low-level threat on day 7. In contrast, the neophobia following the single high-level threat waned over the 8-day period, but the single re-exposure to the low-level threat on day 7 re-triggered the neophobic phenotype. Thus, despite the single low-level exposure being insufficient to induce neophobia, it significantly elevated existing fear and re-triggered fear that had waned. We highlight how such patterns of fear acquisition, retention, and rapid re-triggering play an important role in animal ecology and evolution and outline parallels between the neophobic phenotype in fishes and dimensions of post-traumatic stress in humans.

Sender and receiver experience alters the response of fish to disturbance cues.

Predation is a pervasive selection pressure, shaping morphological, physiological, and behavioral phenotypes of prey species. Recent studies have begun to examine how the effects of individual experience with predation risk shapes the use of publicly available risk assessment cues. Here, we investigated the effects of prior predation risk experience on disturbance cue production and use by Trinidadian guppies Poecilia reticulata under laboratory conditions. In our first experiment, we demonstrate that the response of guppies from a high predation population (Lopinot River) was dependent upon the source of disturbance cue senders (high vs. low predation populations). However, guppies collected from a low predation site (Upper Aripo River) exhibited similar responses to disturbance cues, regardless of the sender population. In our second experiment, we used laboratory strain guppies exposed to high versus low background risk conditions. Our results show an analogous response patterns as shown for our first experiment. Guppies exposed to high background risk conditions exhibited stronger responses to the disturbance cues collected from senders exposed to high (vs. low) risk conditions and guppies exposed to low risk conditions were not influenced by sender experience. Combined, our results suggest that experience with background predation risk significantly impacts both the production of and response to disturbance cues in guppies.

Short-term captivity drives hypothalamic plasticity and asymmetry in wild-caught northern red bellied dace (Chrosomus eos).

Teleost fish are neuroplastic and are known to alter their brain morphology and behaviour in response to environmental change such as an increase in predation pressure. The hypothalamus plays a key role in regulating behavioural responses to predation risk. In this study, wild-caught northern red bellied dace (Chrosomus eos) developed smaller and less symmetric hypothalami when held in captivity for 14 days; both measures correlated with boldness in a latency to emerge test. This study's results highlight the potential impact of short-term holding conditions on brains and behaviour.

High-risk environments promote chemical disturbance signalling among socially familiar Trinidadian guppies.

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.

An ecological framework of neophobia: from cells to organisms to populations.

Neophobia is the fear of novel stimuli or situations. This phenotype has recently received much ecological attention, primarily in the context of decision making. Here, we explore neophobia across biological levels of organisation, first describing types of neophobia among animals and the underlying causes of neophobia, highlighting high levels of risk and uncertainty as key drivers. We place neophobia in the framework of Error Management Theory and Signal Detection Theory, showing how increases in overall risk and uncertainty can lead to costly non-responses towards novel threats unless individuals lower their response threshold and become neophobic. We then discuss how neophobic behaviour translates into population and evolutionary consequences before introducing neophobia-like processes at the cellular level, where some phenomena such as allergy and autoimmunity can parallel neophobic behaviour. Finally, we discuss neophobia attenuation, considering how a sudden change in the environment from dangerous to safe can lead to problematic over-responses (i.e. the 'maladaptive defensive carry-over' hypothesis), and discuss treatment methods for such over-responses. We anticipate that bridging the concept of neophobia with a process-centered perspective can facilitate a transfer of insight across organisational levels.

Competition for food in 2 populations of a wild-caught fish.

Aggressive behavior when competing for resources is expected to increase as the ratio of competitors-to-resource ratio (CRR) units increases. Females are expected to be more aggressive than males when competing for food when body size is more strongly related to reproductive success in females than in males, whereas aggression is predicted to decrease under high ambient predation risk by natural selection. Under the risk allocation model, however, individuals under high ambient predation risk are expected to be more aggressive, and forage more in the absence of imminent risk than their low risk counterparts. An interaction between adult sex ratio (i.e., adult males/females), ambient predation risk (high vs. low), and sex on intrasexual competition for mates in Trinidadian guppies Poecilia reticulata has been shown. The interaction suggested an increase in aggression rates as CRR increased, except for males from the high predation population. To compare the patterns of competition for food versus mates, we replicated this study by using food patches. We allowed 4 male or 4 female guppies from high and low predation populations to compete for 5, 3, or 1 food patches. The foraging rate was higher in a high rather than low ambient predation risk population. Surprisingly, CRR, sex, and population of origin had no effect on aggression rates. Despite other environmental differences between the 2 populations, the effect of ambient predation risk may be a likely explanation for differences in foraging rates. These results highlight the importance for individuals to secure food despite the cost of competition and predation.

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.

The effects of adult sex ratio on mating competition in male and female guppies (Poecilia reticulata) in two wild populations.

When competing for mates, males typically exhibit higher rates of intrasexual aggression and courtship than females. Operational sex ratio, represented here by adult sex ratio (ASR) as a proxy, is likely the best predictor of this competition, which typically increases between members of one sex as members of the opposite sex become rarer. Moreover, in populations subject to high predation, males often decrease mating competitive behaviour due to predation risk. We explored the combined effects of ASR and population of origin (low vs. high ambient predation risk) on mating competition in male and female wild-caught Trinidadian guppies. Both male and female aggression rates increased with ASR, but the increase for males was only significant in the low-predation population. In regard to male mating tactics, courtship propensity was unaffected by ASR, while the propensity to sneak increased at male-biased ASRs. Guppies from a high predation population had lower aggression rates than their low predation counterpart, but male courtship and sneaking attempts did not differ between populations. Surprisingly, females were just as aggressive as males when competing for mates. These results highlight the trade-offs between antipredator and agonistic behaviour, which may affect sexual selection pressures in wild populations.

Interactive effects of reproductive assets and ambient predation risk on the threat-sensitive decisions of Trinidadian guppies.

Threat-sensitive behavioral trade-offs allow prey animals to balance the conflicting demands of successful predator detection and avoidance and a suite of fitness-related activities such as foraging, mating, and territorial defense. Here, we test the hypothesis that background predation level and reproductive status interact to determine the form and intensity of threat-sensitive behavioral decisions of wild-caught female Trinidadian guppies Poecilia reticulata. Gravid and nongravid guppies collected from high- and low-predation pressure populations were exposed to serial dilutions of conspecific chemical alarm cues. Our results demonstrate that there was `no effect of reproductive status on the response of females originating from a low-predation population, with both gravid and nongravid guppies exhibiting strong anti-predator responses to the lowest concentration of alarm cues tested. Increasing cue concentrations did not result in increases in response intensity. Conversely, we found a significant effect of reproductive status among guppies from a high-predation population. Nongravid females from the high-predation population exhibited a strong graded (proportional) response to increasing concentrations of alarm cue. Gravid females from the same high-predation population, however, shifted to a nongraded response. Together, these results demonstrate that accrued reproductive assets influence the threat-sensitive behavioral decisions of prey, but only under conditions of high-ambient predation risk.

Local predation risk shapes spatial and foraging neophobia patterns in Trinidadian guppies.

The "dangerous niche" hypothesis posits that neophobia functions to reduce the cost of habitat use among animals exposed to unknown risks. For example, more dangerous foraging or higher competition may lead to increased spatial neophobia. Likewise, elevated ambient predation threats have been shown to induce phenotypically plastic neophobic predator avoidance. In both cases, neophobia is argued to reduce the cost of living associated with ecological uncertainty. Here, we test the hypothesis that ambient predation shapes both neophobic predator avoidance and spatial and foraging neophobia in Trinidadian guppies. Guppies were exposed to a novel foraging arena paired with a known cue (conspecific alarm cue), a novel cue (lemon odor), or a stream water control in three streams differing in ambient predation risk. We demonstrate that guppies from a high-predation-risk stream exhibited risk-averse foraging patterns regardless of the chemical stimulus presented (high spatial neophobia) and that those from a low-predation-risk stream were only risk-averse when the foraging arenas were paired with conspecific alarm cue (lower spatial neophobia). Those tested in the intermediate-predation-risk stream were consistently intermediate to the high-risk vs. low-risk populations. Our study suggests that ambient predation risk shapes both neophobic predator avoidance and space-use patterns and that neophobia may function as a "generalized" response to ecological uncertainty.