Uncertainty about old information results in differential predator memory in tadpoles.

As information ages, it may become less accurate, resulting in increased uncertainty for decision makers. For example, chemical alarm cues (AC) are a source of public information about a nearby predator attack, and these cues can become spatially inaccurate through time. These cues can also degrade quickly under natural conditions, and cue receivers are sensitive to such degradation. Although numerous studies have documented predator-recognition learning from fresh AC, no studies have explored learning from aged AC and whether the uncertainty associated with this older information contributes to shortening the retention of learned responses (i.e. the 'memory window'). Here, we found that wood frog tadpoles, Lithobates sylvaticus, learned to recognize a novel odour as a predator when paired with AC aged under natural conditions for up to 1 h. However, only tadpoles conditioned with fresh AC were found to retain this learned response when tested 9 days after conditioning. These results support the hypothesis that the memory window is shortened by the uncertainty associated with older information, preventing the long-term costs of a learned association that was based on potentially outdated information.

Evidence for the Predator Attraction Hypothesis in an amphibian predator-prey system.

Many species possess damage-released chemical alarm cues that function in alerting nearby individuals to a predator attack. One hypothesis for the evolution and/or maintenance of such cues is the Predator Attraction Hypothesis, where predators, rather than prey, are the "intended" recipients of these cues. If a predator attack attracts additional predators, these secondary predators might interfere with the predation event, providing the prey with a better chance to escape. In this study, we conducted two experiments to explore this hypothesis in an amphibian predator/prey system. In Experiment 1, we found that tiger salamanders (Ambystoma mavortium) showed a foraging attraction to chemical cues from wood frog (Lithobates sylvaticus) tadpoles. Salamanders that were experienced with tadpole prey, in particular, were strongly attracted to tadpole alarm cues. In Experiment 2, we observed experimental encounters between a tadpole and either one or two salamanders. The presence of the second predator caused salamanders to increase attack speed at the cost of decreased attack accuracy (i.e., increasing the probability that the tadpole would escape attacks). We also found that the mere presence of visual and chemical cues from a second predator did not affect this speed/accuracy trade-off but did cause enough of a distraction to increase tadpole survival. Thus, our findings are consistent with the Predator Attraction Hypothesis for the evolution and/or maintenance of alarm cues.

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

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 avoidance and risk assessment. For instance, alarm cues are released by prey that have been injured by predators. In addition to providing accurate information about current risk, repeated exposure to alarm cues can elicit a fear response to novel stimuli (neophobia) in prey. Another source of chemical information is disturbance cues, released by prey that have been disturbed or harassed (but not injured) by a predator. While disturbance cues have received much less attention than alarm cues, they appear to be useful as an early warning signal of predation risk and have the potential to be used as a priming cue for learning. In this study, we used wood frog (Lithobates sylvaticus) tadpoles to test whether repeated exposure to disturbance cues during the embryonic stage can induce neophobic behaviour. Three weeks following repeated exposure to disturbance cues, tadpoles showed reduced activity when exposed to a novel odour, but they no longer displayed an antipredator response to disturbance cues. In a second experiment, we found that tadpoles failed to learn that a novel odour was dangerous following a pairing with disturbance cues, whereas alarm cues facilitated such learning. Our results add to the growing body of information about disturbance cues and provide evidence of their function as an embryonic risk cue but not as an associative learning cue.

Predator-induced transgenerational plasticity in animals: a meta-analysis.

There is growing evidence that the environment experienced by one generation can influence phenotypes in the next generation via transgenerational plasticity (TGP). One of the best-studied examples of TGP in animals is predator-induced transgenerational plasticity, whereby exposing parents to predation risk triggers changes in offspring phenotypes. Yet, there is a lack of general consensus synthesizing the predator-prey literature with existing theory pertaining to ecology and evolution of TGP. Here, we apply a meta-analysis to the sizable literature on predator-induced TGP (441 effect sizes from 29 species and 49 studies) to explore five hypotheses about the magnitude, form and direction of predator-induced TGP. Hypothesis #1: the strength of predator-induced TGP should vary with the number of predator cues. Hypothesis #2: the strength of predator-induced TGP should vary with reproductive mode. Hypothesis #3: the strength and direction of predator-induced TGP should vary among offspring phenotypic traits because some traits are more plastic than others. Hypothesis #4: the strength of predator-induced TGP should wane over ontogeny. Hypothesis #5: predator-induced TGP should generate adaptive phenotypes that should be more evident when offspring are themselves exposed to risk. We found strong evidence for predator-induced TGP overall, but no evidence that parental predator exposure causes offspring traits to change in a particular direction. Additionally, we found little evidence in support of any of the specific hypotheses. We infer that the failure to find consistent evidence reflects the heterogeneous nature of the phenomena, and the highly diverse experimental designs used to study it. Together, these findings set an agenda for future work in this area.

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.

Reproductive fitness of honey bee queens exposed to thiamethoxam during development.

The productivity and survival of honey bee (Apis mellifera) colonies depend on queen bee health. Colony-level neonicotinoid exposure has negative effects on reproductive fitness of honey bee queens. However, it is unclear if the observed effects are a direct outcome of neonicotinoid toxicity or result from suboptimal care of developing queens by exposed workers. The aim of this study was to evaluate larval survival, reproductive fitness, and histopathology of honey bee queens exposed to incremental doses (0, 5, 50 ng) of the neonicotinoid thiamethoxam (THI) applied directly to individual late larvae (7 days post-oviposition) of queens. The 5 ng dose represents a calculated high environmental level of exposure for honey bee queen larvae. Morphometric evaluation revealed that the total area of mandibular gland epithelium in queens exposed to 5 and 50 ng THI was reduced by 14% (P = .12) and 25% (P = .001), respectively. Decreased mandibular gland size may alter pheromone production, which could in part explain previously observed negative effects of THI on the reproductive fitness of queens. We also found that late larval exposure to THI reduced larval and pupal survival and decreased sperm viability in mated queens. These changes may interfere with queen development and reproductive longevity.

Safety Cues Can Give Prey More Valuable Information Than Danger Cues.

The ability of prey to assess predation risk is fundamental to their success. It is routinely assumed that predator cues do not vary in reliability across levels of predation risk. We propose that cues can differ in how precisely they indicate different levels of predation risk. What we call danger cues precisely indicate high risk levels, while safety cues precisely indicate low risk levels. Using optimality modeling, we find that prey fitness is increased when prey pay more attention to safety cues than to danger cues. This fitness advantage is greater when prey need to protect assets, predators are more dangerous, or predation risk increases at an accelerating rate with prey foraging efforts. Each of these conditions lead to prey foraging less when estimated predation risk is higher. Danger cues have less value than safety cues because they give precise information about risk when it is high, but prey behavior varies little when risk is high. Safety cues give precise information about levels of risk where prey behavior varies. These results highlight how our fascination with predators may have biased the way that we study predator-prey interactions and focused too exclusively on cues that clearly indicate the presence of predator rather than cues that clearly indicate their absence.

Microplastic exposure interacts with habitat degradation to affect behaviour and survival of juvenile fish in the field.

Coral reefs are degrading globally due to increased environmental stressors including warming and elevated levels of pollutants. These stressors affect not only habitat-forming organisms, such as corals, but they may also directly affect the organisms that inhabit these ecosystems. Here, we explore how the dual threat of habitat degradation and microplastic exposure may affect the behaviour and survival of coral reef fish in the field. Fish were caught prior to settlement and pulse-fed polystyrene microplastics six times over 4 days, then placed in the field on live or dead-degraded coral patches. Exposure to microplastics or dead coral led fish to be bolder, more active and stray further from shelter compared to control fish. Effect sizes indicated that plastic exposure had a greater effect on behaviour than degraded habitat, and we found no evidence of synergistic effects. This pattern was also displayed in their survival in the field. Our results highlight that attaining low concentrations of microplastic in the environment will be a useful management strategy, since minimizing microplastic intake by fishes may work concurrently with reef restoration strategies to enhance the resilience of coral reef populations.

Proportional fitness loss and the timing of defensive investment: a cohesive framework across animals and plants.

The risk of consumption is a pervasive aspect of ecology and recent work has focused on synthesis of consumer-resource interactions (e.g., enemy-victim ecology). Despite this, theories pertaining to the timing and magnitude of defenses in animals and plants have largely developed independently. However, both animals and plants share the common dilemma of uncertainty of attack, can gather information from the environment to predict future attacks and alter their defensive investment accordingly. Here, we present a novel, unifying framework based on the way an organism's ability to defend itself during an attack can shape their pre-attack investment in defense. This framework provides a useful perspective on the nature of information use and variation in defensive investment across the sequence of attack-related events, both within and among species. It predicts that organisms with greater proportional fitness loss if attacked will gather and respond to risk information earlier in the attack sequence, while those that have lower proportional fitness loss may wait until attack is underway. This framework offers a common platform to compare and discuss consumer effects and provides novel insights into the way risk information can propagate through populations, communities, and ecosystems.

A novel alarm signal in aquatic prey: Familiar minnows coordinate group defences against predators through chemical disturbance cues.

Animal signalling systems outside the realm of human perception remain largely understudied. These systems consist of four main components: a signalling context, a voluntary signal, receiver responses and resulting fitness benefits to both the signaller and receiver(s). It is often most difficult to determine incidental cues from voluntary signals. One example is chemical disturbance cues released by aquatic prey during predator encounters that may serve to alert conspecifics of nearby risk and initiate tighter shoaling. We aimed to test whether disturbance cues are released incidentally (i.e. as a cue) or are produced voluntarily depending on a specific signalling context such as the audience surrounding the individual, and thus constitute a signal. We hypothesized that if receivers use disturbance cues to communicate risk among themselves, they would produce more (or more potent) disturbance cues when present in a group of conspecifics rather than when they are isolated (presence/absence of an audience) and use disturbance cues more when present alongside familiar rather than unfamiliar conspecifics (audience composition effect). We placed fathead minnows (Pimephales promelas) in groups with familiar fish, unfamiliar fish or as isolated individuals with no audience present, and then simulated a predator chase to evoke disturbance cues. We used bioassays with independent receivers to assess whether the disturbance cues produced differed depending on the signallers' audience. We found evidence of voluntary signalling, as minnows responded to disturbance cues from groups of fish with tighter shoaling while disturbance cues from isolated minnows did not evoke a significant shoaling response (presence/absence audience effect). Receivers also increased shoaling, freezing and dashing more in response to disturbance cues from familiar groups compared to disturbance cues from unfamiliar groups or isolated minnows (audience composition effect). Together, these findings support our hypothesis that disturbance cues are used as an antipredator signal to initiate coordinated group defences among familiar conspecifics involving shoaling, freezing and dashing. This study represents the strongest evidence to date that chemicals released by aquatic prey upon disturbance by predators serve as voluntary signals rather than simply cues that prey have evolved to detect when assessing their risk of predation.

Time-dependent latent inhibition of predator-recognition learning.

To optimally manage an environment with predators, prey must correctly distinguish between cues that are risky and cues that are safe. Even a specific cue that is safe in one area or at a certain time may be dangerous in other situations, and vice versa. Latent inhibition is a cognitive mechanism by which animals fail to learn that a stimulus as risky because they have already learned it as non-threatening via previous encounters with the stimulus in the absence of negative consequences. Here, we demonstrate that latent inhibition of predator-recognition learning in wood frog tadpoles, Lithobates sylvaticus, depends on the timing of their learning opportunities. For 6 days, tadpoles were exposed daily to an initially novel stimulus (salamander odour), either in the morning (11.00-13.00 h) or evening (16.00-18.00 h). The following day, we conditioned tadpoles to recognize the salamander odour as a predator by pairing it with injured tadpole cues, either at the same time as their previous experience or at the opposite time. When tested the following day, latent inhibition occurred under each scenario where the timing of conditioning matched the timing of the pre-exposure. However, tadpoles tested in the morning showed learned fright responses when conditioned in the morning if their pre-exposure had occurred in the evening, whereas individuals tested in the evening showed learned fright responses when conditioned in the evening if their pre-exposure had occurred in the morning. This is the first report of time-dependent latent inhibition of predator-recognition learning, which is likely an important mechanism for correctly managing predation risk and safety.

The Effects of Selenomethionine on the Escape Behaviours of Fathead Minnows.

Selenium (Se) is an essential micronutrient for animals and yet becomes toxic with only a small increase in concentration. Toxicological studies have reported various effects of Se on fishes, including developmental impacts and deformities of the musculature and sensory systems. This paper investigates the impact of sublethal concentrations of Se on the ability of the Fathead Minnow (Pimephales promelas) to perform escape responses, a routine behaviour important to predator-prey dynamics. Predation is among the strongest evolutionary driving forces in nature. Changes to this dynamic can have effects that cascade through the ecosystem. We used responses to mechanical and visual stimuli to determine the impact of environmentally relevant concentrations of dietary selenomethionine on the behaviour of minnows. Latency to respond to the stimulus and kinematic performance were assessed. Our results indicated that there was no significant effect of selenomethionine on either the visual response to a threat or burst swimming behaviours of the fast-start response in minnows. Levels of Se in tissues approached that of tissue-specific guidelines set by regulatory bodies across North America. This suggests that current regulations are adequately protecting this key component of predator avoidance in Fathead Minnows.

The socially mediated recovery of a fearful fish paired with periodically replaced calm models.

Social learning is an important mechanism for acquiring knowledge about environmental risk. However, little work has explored the learning of safety and how such learning outcomes are shaped by the social environment. Here, we exposed minnows, Pimephales promelas, to a high-risk environment to induce behavioural responses associated with fear (e.g. neophobia). We then used the presence of calm conspecific models (low-risk individuals) to weaken these responses. When observers (individuals from the high-risk environment) and models were paired consistently in a one-on-one setting, the observers showed no recovery (i.e. no weakening of the fear responses), and instead the models indirectly acquired those responses (i.e. a socially transmitted state of fear). However, observers paired with models that were periodically replaced with new calm models showed a significant recovery, and each new model showed diminished socially transmitted fear. We argue that our understanding of predation-related fear and social information transfer can prove fruitful in understanding problems with fear and stress across animal taxa, including among humans who experience post-traumatic stress and secondary trauma. Our findings indicate that the periodic replacement of models can promote fear recovery in observers and reduce socially transmitted fear in models.

School is out on noisy reefs: the effect of boat noise on predator learning and survival of juvenile coral reef fishes.

Noise produced by anthropogenic activities is increasing in many marine ecosystems. We investigated the effect of playback of boat noise on fish cognition. We focused on noise from small motorboats, since its occurrence can dominate soundscapes in coastal communities, the number of noise-producing vessels is increasing rapidly and their proximity to marine life has the potential to cause deleterious effects. Cognition-or the ability of individuals to learn and remember information-is crucial, given that most species rely on learning to achieve fitness-promoting tasks, such as finding food, choosing mates and recognizing predators. The caveat with cognition is its latent effect: the individual that fails to learn an important piece of information will live normally until the moment where it needs the information to make a fitness-related decision. Such latent effects can easily be overlooked by traditional risk assessment methods. Here, we conducted three experiments to assess the effect of boat noise playbacks on the ability of fish to learn to recognize predation threats, using a common, conserved learning paradigm. We found that fish that were trained to recognize a novel predator while being exposed to 'reef + boat noise' playbacks failed to subsequently respond to the predator, while their 'reef noise' counterparts responded appropriately. We repeated the training, giving the fish three opportunities to learn three common reef predators, and released the fish in the wild. Those trained in the presence of 'reef + boat noise' playbacks survived 40% less than the 'reef noise' controls over our 72 h monitoring period, a performance equal to that of predator-naive fish. Our last experiment indicated that these results were likely due to failed learning, as opposed to stress effects from the sound exposure. Neither playbacks nor real boat noise affected survival in the absence of predator training. Our results indicate that boat noise has the potential to cause latent effects on learning long after the stressor has gone.

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

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

Maternal Exposure to Dietary Selenium Causes Dopaminergic Hyperfunction and Cognitive Impairment in Zebrafish Offspring.

Maternal exposure to environmental contaminants is a predisposing factor for neurodevelopmental disorders with associated cognitive and social deficits in offspring. In this study, we investigated the effects of maternal exposure to selenium (Se), a contaminant of potential environmental concern in aquatic ecosystems, on cognitive performance and the underlying mechanisms in F1-generation adult zebrafish. Adult female zebrafish were exposed to different concentrations of dietary Se (3.5, 11.1, or 27.4 µg Se/g dry weight) for a period of 60 days. Fish were subsequently bred, and their offspring were collected and raised for 6 months on a normal diet. Maternal exposure to all concentrations of dietary Se induced learning impairment in F1-zebrafish tested in a latent learning task. The results also showed a hyperfunctioning dopaminergic system in fish exhibiting the learning deficit. The hyperfunction of the dopaminergic system was associated with enhanced oxidative stress and alterations in the mRNA abundance of several immediate early and late response genes in the zebrafish brain. Taken together, these results suggest that maternal exposure to dietary Se via alterations in the dopaminergic system leads to persistent neurobehavioral deficits in F1-generation adult zebrafish.

Patterns of predator neophobia: a meta-analytic review.

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.

Not equal in the face of habitat change: closely related fishes differ in their ability to use predation-related information in degraded coral.

Coral reefs are biodiversity hotpots that are under significant threat due to the degradation and death of hard corals. When obligate coral-dwelling species die, the remaining species must either move or adjust to the altered conditions. Our goal was to investigate the effect of coral degradation on the ability of coral reef fishes to assess their risk of predation using alarm cues from injured conspecifics. Here, we tested the ability of six closely related species of juvenile damselfish (Pomacentridae) to respond to risk cues in both live coral or dead-degraded coral environments. Of those six species, two are exclusively associated with live coral habitats, two are found mostly on dead-degraded coral rubble, while the last two are found in both habitat types. We found that the two live coral associates failed to respond appropriately to the cues in water from degraded habitats. In contrast, the cue response of the two rubble associates was unaffected in the same degraded habitat. Interestingly, we observed a mixed response from the species found in both habitat types, with one species displaying an appropriate cue response while the other did not. Our second experiment suggested that the lack of responses stemmed from deactivation of the alarm cues, rather than the inability of the species to smell. Habitat preference (live coral versus dead coral associates) and phylogeny are good candidates for future work aimed at predicting which species are affected by coral degradation. Our results point towards a surprising level of variation in the ability of congeneric species to fare in altered habitats and hence underscores the difficulty of predicting community change in degraded habitats.

Trust thy neighbour in times of trouble: background risk alters how tadpoles release and respond to disturbance cues.

In aquatic environments, uninjured prey escaping a predator release chemical disturbance cues into the water. However, it is unknown whether these cues are a simple physiological by-product of increased activity or whether they represent a social signal that is under some control by the sender. Here, we exposed wood frog tadpoles (Lithobates sylvaticus) to either a high or low background risk environment and tested their responses to disturbance cues (or control cues) produced by tadpoles from high-risk or low-risk backgrounds. We found an interaction between risk levels associated with the cue donor and cue recipient. While disturbance cues from low-risk donors did not elicit an antipredator response in low-risk receivers, they did in high-risk receivers. In addition, disturbance cues from high-risk donors elicited a marked antipredator response in both low- and high-risk receivers. The response of high-risk receivers to disturbance cues from high-risk donors was commensurate with other treatments, indicating an all-or-nothing response. Our study provides evidence of differential production and perception of social cues and provides insights into their function and evolution in aquatic vertebrates. Given the widespread nature of disturbance cues in aquatic prey, there may exist a social signalling system that remains virtually unexplored by ecologists.

Habitat degradation disrupts neophobia in juvenile coral reef fish.

Habitat degradation not only disrupts habitat-forming species, but alters the sensory landscape within which most species must balance behavioural activities against predation risk. Rapidly developing a cautious behavioural phenotype, a condition known as neophobia, is advantageous when entering a novel risky habitat. Many aquatic organisms rely on damage-released conspecific cues (i.e. alarm cues) as an indicator of impending danger and use them to assess general risk and develop neophobia. This study tested whether settlement-stage damselfish associated with degraded coral reef habitats were able to use alarm cues as an indicator of risk and, in turn, develop a neophobic response at the end of their larval phase. Our results indicate that fish in live coral habitats that were exposed to alarm cues developed neophobia, and, in situ, were found to be more cautious, more closely associated with their coral shelters and survived four-times better than non-neophobic control fish. In contrast, fish that settled onto degraded coral habitats did not exhibit neophobia and consequently suffered much greater mortality on the reef, regardless of their history of exposure to alarm cues. Our results show that habitat degradation alters the efficacy of alarm cues with phenotypic and survival consequences for newly settled recruits.