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Determining how prey learn the identity of predators and match their vigilance with current levels of threat is central to understanding the dynamics of predator–prey systems and the determinants of fitness. Our study explores how feeding history influences the relative importance of olfactory and visual sensory modes of learning, and how the experience gained through these sensory modes influences behaviour and survival in the field for a juvenile coral reef damselfish. We collected young fish immediately prior to their settlement to benthic habitats. In the laboratory, these predator-naïve fish were exposed to a high- or low-food ration and then conditioned to recognize the olfactory cues (odours) and/or visual cues from two common benthic predators. Fish were then allowed to settle on reefs in the field, and their behaviour and survival over 70 h were recorded. Feeding history strongly influenced their willingness to take risks in the natural environment. Conditioning in the laboratory with visual, olfactory or both cues from predators led fish in the field to display risk-averse behaviour compared with fish conditioned with sea water alone. Well-fed fish that were conditioned with visual, chemical or a combination of predator cues survived eight times better over the first 48 h on reefs than those with no experience of benthic predator cues. This experiment highlights the importance of a flexible and rapid mechanism of learning the identity of predators for survival of young fish during the critical life-history transition between pelagic and benthic habitats.

Aquatic prey can gauge predation risk using chemical information, including chemical alarm cues — released when prey are injured, disturbance cues — released when prey are threatened, or the odour of the predator itself. While a lot of work has focused on alarm cues, disturbance cues remained poorly studied in freshwater systems, and has been virtually omitted in marine ones. In the current study, we document the first evidence of disturbance cue use in a marine fish. Juvenile damselfish Pomacentrus nagasakiensis were exposed to cues from undisturbed or disturbed conspecifics, a water control (negative control) and conspecific alarm cues (positive control). Juveniles displayed increased antipredator responses when exposed to alarm cues and disturbed conspecifics, but not when exposed to undisturbed ones. In addition, we demonstrated that disturbance cues, just like alarm cues, could mediate learned predator recognition, a phenomenon undemonstrated in freshwater fishes. Given disturbance cues are thought to be comprised of nitrogenous waste, it has been hypothesised that the constant and dilute release of such products in the hypotonic freshwater environment results in a high level of ‘background chemical’ noise masking subsequent releases. Extending this hypothesis, we propose that in the marine environment, disturbance cues are more easily detected due to low background noise.

Chemical information is one of the most important modes of communication among aquatic organisms. However, it remains unclear whether fish embryos are innately responsive to ecologically-related chemical cues from the cues of their cohort competitors, potential caring or risky cues from parents, or chemical alarm cues from damaged embryos, and whether these response patterns differ between species that model alternative parental care strategies. Here, we examined embryo responses in heart rate and incubation performance to different conspecific chemical cues (companion embryo odours, maternal odours, maternal + companion odours, embryonic alarm cues, or water controls) in zebrafish ( ; no parental care) and Nile tilapia ( ; high parental care). Zebrafish embryos did not respond to companion embryo odours but did respond similarly to maternal odours and alarm cues consistent with detecting elevated risk levels. In contrast, Nile tilapia embryos only demonstrated significant risk responses to embryonic alarm cues. These findings indicate that embryos of both species can innately recognize alarm cues but differ in their response patterns to conspecific odours. The results highlight that parental care strategies may influence intergenerational chemical communication in fish embryos.

Prey incorporate information about risk, safety, and the reliability of both of these cues when assessing risk of predation. Here, we report results of an experiment testing avoidance of chemical alarm cues derived from skin extract of blacknose shiners, Notropis heterolepis (BNS), attraction toward a visible shoal of five BNS, and the combination of both, on fishes in Deming Lake where BNS occur. We then repeated the experiment in nearby Budd Lake where BNS do not occur. BNS avoided traps with conspecific alarm cues but did not respond to the presence of BNS shoals. We recorded responses by similar-sized heterospecifics that share predators with BNS to see if they respond to BNS as indicators of risk and safety. Fathead minnows, Pimephales promelas (FHM) avoided traps chemically labeled with BNS alarm cue when a shoal was absent and avoided BNS shoals when traps were labeled with water (control). When both BNS alarm cue and BNS shoal were combined, FHM antipredator response to BNS alarm cue invoked a shoaling response with the BNS shoal in the trap. The more distantly related redbelly dace, Chrosomus eos (RBD), responded weakly to BNS cues in Deming Lake and ignored them in Budd Lake. Non-cyprinid species (brook stickleback Culaea inconstans and pumpkinseed sunfish, Lepomis gibbosus) did not respond to either olfactory or visual cues of BNS in Deming Lake. In Budd Lake, neither avoidance of BNS alarm cue or attraction to BNS shoals surpassed the threshold of statistical significance, indicating a role of ecological familiarity and learned recognition of risk and safety in cross-species reactions to olfactory and visual cues of heterospecifics.Significance statementSmall fish, such as minnows, avoid areas marked by injury-released chemical cues because these cues are released only in the context of predation and are attracted to groups of fish because shoals offer safety from predation. In this study fathead minnows Pimephales promelas (FHM) avoided alarm cue of blacknose shiners Notropis heterolepis (BNS) in Deming Lake where both species occur but not in Budd Lake where BNS do not occur. FHM were not attracted to BNS shoals in either lake. However, when a shoal of BNS was combined with BNS alarm cue a synergism occurred where antipredator responses to BNS alarm cue induced FHM to seek safety by shoaling with BNS shoals. The synergism occurred in Deming Lake where BNS alarm cue and shoals are ecologically familiar but not in Budd Lake where BNS do not occur. These data show that behavioral responses by prey to olfactory and visual cues are tempered by sympatry (ecological familiarity) and confidence in the reliability of those cues.

Mutualistic relationships confer selective advantages to interacting species through enhanced ecological benefits but may be functionally limited to certain life history stages. However, it is not yet known whether one party can indirectly benefit from risky cues released when the other party is threatened. Larval glochidia of the Chinese pond mussel (Anodonta woodiana) attach to fishes including the rosy bitterling (Rhodeus ocellatus) for dispersal, while reproductive-phase bitterling use the gills of adult mussels as spawning substrate, and their larvae remain inside the host mussel shells until they are capable of swimming. Here, we examined heterospecific responses to risky chemical cues by rosy bitterling as an indirect indicator of species affinity consistent with mutualism at different life history stages, to test for age-dependent response patterns indicating temporal patterning of shared predation risk. Bitterling demonstrated equivocal but similar responses to water controls and mussel odor and significant antipredator responses to bitterling chemical alarm cues (CAC) independent of life stage, while only reproductive adult bitterling demonstrated significant antipredator responses to mussel CAC. These findings suggest that the mutualistic affinity to mussels present in reproductive-phase adult rosy bitterling may result in shared predation risk and therefore provide them with additional indirect antipredator benefits. Our results revealed a life history stage-dependent mutualism in this bitterling-mussel system and describe a novel application of predation risk assays for studying temporal patterning in mutualistic relationships.Significance statementInterspecific interactions, including mutualisms, are a central component of community composition. Some freshwater fishes, including the rosy bitterling, and mussels share an interesting mutualism where each species provides early life habitat to the other. However, does mutualism provide additional indirect benefits? Here, we used responses to conspecific and Chinese pond mussel chemical cues in different life stages of bitterling to identify the occurrence of mutualistic behaviors. We demonstrated that the putative occurrence of mutualistic behaviors in rosy bitterling is not consistent over time and instead varies predictably with reproductive status of different life history stages. This study provides a novel perspective for a deeper understanding of labile interspecific relationships and provides a theoretical basis for indirectly examining mutualisms through chemical communication-based behavioral assays.

The monkey goby Neogobius fluviatilis is an invasive Ponto-Caspian fish that enters habitats of the native gudgeon Gobio gobio in European freshwaters, likely belonging to the same prey guild. Their abilities to detect and avoid predation have been poorly understood, although these traits may contribute to the competitive advantage and drive the invasion success of the goby. We tested intra- and interspecific responses of fish from sympatric populations to damage-released alarm cues (skin extract) in laboratory. Both species of fish responded to conspecific and heterospecific cues, but their responses to conspecifics were more diverse (changed social distancing among individuals, reduced vertical and horizontal movement) than those elicited by heterospecifics (changed social distancing only). Moreover, the fish differed in their anti-predation behaviour: the gudgeon increased whilst the monkey goby decreased inter-individual distances and only the gudgeon exhibited thigmotaxis and reduced mobility in response to the conspecific cues. Interspecific differences show that the species exhibit distant anti-predation strategies. This might be associated with their phylogenetic distance and/or higher differentiation of their ecological niches than commonly assumed. Besides, our results suggest that alien species be included in the interspecific exchange of information in local fish assemblages.

Plasticity in hatching time allows embryos to maximize fitness by balancing the benefits and costs of remaining bound within the chorion against the benefits and costs of emerging as a free-swimming larva. Here, in the first experiment, we exposed zebrafish (Danio rerio) embryos to either chemical cues from crushed embryos (simulating egg predation) or to blank water control. Embryos exposed to alarm cues hatched sooner, and had shorter body lengths and underdeveloped fins, relative to larvae from the water treatment. Burst swimming speed was significantly slower for larvae that hatched from the alarm cue treatment than for larvae from the water treatment. In a second 2×2 experiment, we exposed zebrafish embryos to either chemical alarm cues from conspecific embryos, mechanical disturbance (magnetic stir bar) to simulate a predator probing the substrate for developing embryos, both chemical and mechanical indicators of risk, or neither (control). We found similar effects in terms of earlier time to hatch at an earlier stage of development and poorer swimming performance of hatchling larvae. In the second experiment, these effects occurred in response to mechanical disturbance with or without the presence of chemical alarm cues. Alarm cues alone produced no effects in the second experiment. Taken together, these data indicate that zebrafish embryos demonstrate a facultative trade-off between risk of predation acting on two stages of their life history.

Habitat degradation is a global problem and one of the main causes of biodiversity loss. Though widespread, the mechanisms that underlie faunal changes are poorly understood. In tropical marine systems, corals play a crucial role in forming habitat, but coral cover on many reefs is declining sharply. Coral degradation affects the olfactory cues that provide reliable information on the presence and intensity of threat. Here, we show for the first time that the ability of a habitat generalist to learn predators using an efficient and widespread method of predator learning is compromised in degraded coral habitats. Results indicate that chemical alarm cues are no longer indicative of a local threat for the habitat generalist (the damselfish, Pomacentrus amboinensis), and these cues can no longer be used to learn the identity of novel predators in degraded habitats. By contrast, a rubble specialist and congeneric (Pomacentrus coelestis) responded to olfactory threat cues regardless of background environment and could learn the identity of a novel predator using chemical alarm cues. Understanding how some species can cope with or acclimate to the detrimental impacts of habitat degradation on risk assessment abilities will be crucial to defining the scope of resilience in threatened communities.

In aquatic environments, many prey animals possess damage-released chemical alarm cues that elicit antipredator behaviours in responsive con- and heterospecifics. Despite considerable study, the selective advantage of alarm cues remains unclear. In an attempt to investigate one of the more promising hypotheses concerning the evolution of alarm cues, we examined whether the cue functions in a fashion analogous to the distress vocalizations emitted by many terrestrial animals. Our results suggest that chemical alarm cues in damselfish (Pomacentridae) may have evolved to benefit the cue sender by attracting secondary predators who disrupt the predation event, allowing the prey a greater chance to escape. The coral reef piscivore, the dusky dottyback (Pseudochromis fuscus), chemically eavesdrops on predation events and uses chemical alarm cues from fish prey (lemon damselfish; Pomacentrus moluccensis) in an attempt to find and steal prey from primary predators. Field studies showed that Ps. fuscus aggregate at sites where prey alarm cue has been experimentally released. Furthermore, secondary predators attempted to steal captured prey of primary predators in laboratory trials and enhanced prey escape chances by 35–40%. These results are the first, to the best of our knowledge, to demonstrate a mechanism by which marine fish may benefit from the production and release of alarm cues, and highlight the complex and important role that semiochemicals play in marine predator–prey interactions.

The antipredator behaviour of prey organisms is shaped by a series of threat-sensitive trade-offs between the benefits associated with successful predator avoidance and a suite of other fitness-related behaviours such as foraging, mating and territorial defence. Recent research has shown that the overall intensity of antipredator response and the pattern of threat-sensitive trade-offs are influenced by current conditions, including variability in predation risk over a period of days to weeks. In this study, we tested the hypothesis that long-term predation pressure will likewise have shaped the nature of the threat-sensitive antipredator behaviour of wild-caught Trinidadian guppies (Poecilia reticulata). Female guppies were collected from two populations that have evolved under high- and low-predation pressure, respectively, in the Aripo River, Northern Mountain Range, Trinidad. Under laboratory conditions, we exposed shoals of three guppies to varying concentrations of conspecific damage-released chemical alarm cues. Lower Aripo (high-predation) guppies exhibited the strongest antipredator response when exposed to the highest alarm cue concentration and a graded decline in response intensity with decreasing concentrations of alarm cue. Upper Aripo (low-predation) guppies, however, exhibited a nongraded (hypersensitive) response pattern. Our results suggest that long-term predation pressure shapes not only the overall intensity of antipredator responses of Trinidadian guppies but also their threat-sensitive behavioural response patterns.