Predator Inspection Research Articles

On closer inspection: Reviewing the debate on whether fish cooperate to inspect predators

AbstractCooperative behaviours, which benefit a recipient, are widespread in the animal kingdom; yet their evolution is not straightforward. Reciprocity, i.e., cooperating with previously experienced cooperative partners, has been suggested to underly cooperation, but has been contested throughout the years. Once a textbook example of reciprocity was cooperative predator inspection, where one or several individuals leave their group to approach a potential threat. Each can at any point stop or retreat, increasing the risk for its partner. It was suggested that inspecting individuals follow a specific reciprocal strategy called tit‐for‐tat, i.e., cooperating on the first move and then copying the partner's last move. Numerous studies provide evidence to support the claim that fish cooperate to inspect predators, including three‐spined sticklebacks (Gasterosteus aculeatus), guppies (Poecilia reticulata) and minnows (Phoxinus phoxinus). However, over the past few decades some scholars have expressed scepticism whether predator inspection is indeed a cooperative behaviour or rather a case of by‐product mutualism, which describes behaviours that benefit a partner as a corollary of an otherwise selfish behaviour. For instance, it has been shown that pairs of fish moving in unfamiliar environments appear to coordinate movements even in the absence of predators. Many studies have also used coarse measures of overall approach rates towards predators rather than the fine‐grained analyses necessary to infer tit‐for‐tat in cooperative inspections. Now is the time to return to the question of cooperative predator inspection with new tools and approaches to resolve a decades‐old debate.

Evolution of schooling drives changes in neuroanatomy and motion characteristics across predation contexts in guppies

One of the most spectacular displays of social behavior is the synchronized movements that many animal groups perform to travel, forage and escape from predators. However, elucidating the neural mechanisms underlying the evolution of collective behaviors, as well as their fitness effects, remains challenging. Here, we study collective motion patterns with and without predation threat and predator inspection behavior in guppies experimentally selected for divergence in polarization, an important ecological driver of coordinated movement in fish. We find that groups from artificially selected lines remain more polarized than control groups in the presence of a threat. Neuroanatomical measurements of polarization-selected individuals indicate changes in brain regions previously suggested to be important regulators of perception, fear and attention, and motor response. Additional visual acuity and temporal resolution tests performed in polarization-selected and control individuals indicate that observed differences in predator inspection and schooling behavior should not be attributable to changes in visual perception, but rather are more likely the result of the more efficient relay of sensory input in the brain of polarization-selected fish. Our findings highlight that brain morphology may play a fundamental role in the evolution of coordinated movement and anti-predator behavior.

Guppies in large groups cooperate more frequently in an experimental test of the group size paradox.

The volunteer's dilemma, in which a single individual is required to produce a public good, predicts that individuals in larger groups will cooperate less frequently. Mechanistically, this could result from trade-offs between costs associated with volunteering and costs incurred if the public good is not produced (nobody volunteers). During predator inspection, one major contributor to the cost of volunteering is likely increased probability of predation; however, a predator also poses a risk to all individuals if nobody inspects. We tested the prediction that guppies in larger groups will inspect a predator less than those in smaller groups. We also predicted that individuals in larger groups would perceive less threat from the predator stimulus because of the protective benefits of larger groups (e.g. dilution). Contrary to prediction, we found that individuals in large groups inspected more frequently than those in smaller groups, but (as predicted) spent less time in refuges. There was evidence that individuals in intermediate-sized groups made fewest inspections and spent most time in refuges, suggesting that any link between group size, risk and cooperation is not driven by simple dilution. Extensions of theoretical models that capture these dynamics will likely be broadly applicable to risky cooperative behaviour.

Roles of the 5-HT2C receptor on zebrafish sociality

Serotonin (5-HT) receptors have been implicated in social behavior in vertebrates. Zebrafish (Danio rerio) have been increasingly being used behavioral neuroscience to study the neurobiological correlates of behavior, including sociality. Nonetheless, the role of 5-HT2C receptors in different social functions were not yet studied in this species. Zebrafish were treated with the agonist MK-212 (2 mg/kg) or the antagonist RS-102221 (2 mg/kg) and tested in the social interaction and social novelty tests, conditional approach test, or mirror-induced aggressive displays. MK-212 increased preference for an unknown conspecific in the social investigation test, but also increased preference for the known conspecific in the social novelty test; RS-102221, on the other hand, decreased preference in the social investigation test but increased preference for the novel conspecific in the social novelty test. MK-212 also decreased predator inspection in the conditional approach test. While RS-102221 decreased time in the display zone in the mirror-induced aggressive display test, it increased display duration. Overall, these results demonstrate the complex role of 5-HT2C receptors in different social contexts in zebrafish, revealing a participation in social plasticity in vertebrates.

Exploring the effects of anthropogenic disturbance on predator inspection activity in Trinidadian guppies.

Exploring the effects of anthropogenic disturbance on predator inspection activity in Trinidadian guppies.

Why are predator cues in the field not more evocative? A ‘real world’ assay elicits subtle, but meaningful, responses by wild rodents to predator scents

Mismatches between highly-standardized laboratory predatory assays and more realistic environmental conditions may lead to different outcomes. Understanding rodents’ natural responses to predator scents is important. Thus, field studies on the same and related species are essential to corroborate laboratory findings to better understand the contexts and motivational drives that affect laboratory responses to predator scents. However, there are too few field assays to enable researchers to study factors that influence these responses in genetically variable populations of wild rodents. Therefore, we placed laboratory-style chambers and remote-sensing devices near multiple colonies of two species of wild mice (Apodemus agrarius and Apodemus flavicollis) to test dual-motivational drives (appetitive and aversive) in a ‘familiar’, yet natural environment. A highly-palatable food reward was offered daily alongside scents from coyotes, lions, rabbits, and both wet and dry controls. In all but two instances (n = 264), animals entered chambers and remained inside for several minutes. Animals initiated flight twice, but they never froze. Rather, they visited chambers more often and stayed inside longer when predatory scents were deployed. The total time spent inside was highest for lion urine (380% longer than the dry control), followed by coyote scent (75% longer), dry control and lastly, herbivore scents (no difference). Once inside the chamber, animals spent more time physically interacting with predatory scents than the herbivore scent or controls. Our findings support the common assumption that rodents fail to respond as overtly to predatory scents in the field compared to what has been observed in the laboratory, possibly due to their varying motivational levels to obtain food. More time spent interacting with scents in the field was likely a function of ‘predator inspection’ (risk assessment) once subjects were in a presumed safe enclosure. We conclude this sort of chamber assay can be useful in understanding the contexts and motivational drives inherent to field studies, and may help interpret laboratory results. Our results also suggest more attention should be given to subtle behaviors such as scent inspection in order to better understand how, and when, environmental stimuli evoke fear in rodents.

Brain monoaminergic activity during predator inspection in female Trinidadian guppies (Poecilia reticulata)

To understand the processes underpinning social decision-making, we need to determine how internal states respond to information gathered from the social environment. Brain monoamine neurotransmitters are key in the appraisal of the social environment and can reflect the internal state underlying behavioural responses to social stimuli. Here we determined the effects of conspecific partner cooperativeness during predator inspection on brain monoamine metabolic activity in Trinidadian guppies (Poecilia reticulata). We quantified the concentration of dopamine, serotonin and their metabolites across brain sections sampled immediately after ostensibly experiencing cooperation or defection from social partners whilst inspecting a predator model, using a familiar object as a control condition. Our results indicate dopaminergic and serotonergic activity differs with the cooperativeness experienced; these different neurotransmission profiles are likely to affect the expression and regulation of downstream behaviours that ultimately contribute to the patterning of cooperative interactions among individuals in a population.

Neophobic behavioural responses of parasitised fish to a potential predator and baited hook

Many juvenile fish show essential avoidance of predators but are also faced with the need to show risky asset-acquiring behaviour, such as trying new food sources, many of which are known to be influenced by parasite infection. Here, we investigated the links between parasite infection, anti-predator behaviour and neophobia towards a novel food presented on a baited hook in fish. Juvenile Spangled perch (Leipotherapon unicolor) undertook two behavioural tests in our laboratory, before being dissected and examined for external and internal parasites. We used an adapted conditioned place avoidance (CPA) paradigm to examine responses to a predator fish and in a separate test, we examined neophobia of a baited hook. Of the 69 Spangled perch studied, 27% of fish were uninfected and at least one of nematodes, Protozoa/Myxozoa or Monogenea were found in the remaining fish. Fish spent less time in the side of the tank where the predator was previously encountered, than before encounters, indicating that fish can learn to avoid locations where predators were previously observed. We found that fish spent longer in the side of the tank where the predator was visible than in the same side of the tank in earlier trials without the predator, supporting previous studies showing that fish actively approach and engage in predator inspection. Fish infected with Protozoa/Myxozoa and camallanid nematodes were less likely to enter the side of the tank with the predator than uninfected fish, suggesting a reluctance to approach a predator in these infected fish. However, Protozoa/Myxozoa and camallanid infected fish bit the baited hook sooner than uninfected fish, possibly indicating less neophobia of the baited hook in fish with these infections. Avoiding to approach a predator yet reduced neophobia to novel foods in some infected fish suggest that parasites do not exert a general, overall, effect on risk aversiveness. Instead, changes in neophobic behaviour appear complex and we discuss the possibility that parasite-induced changes in fish behaviour may be modulated by altered hunger levels and reduced locomotion brought about by illness.

Preliminary evidence for one-trial social learning of vervet monkey alarm calling.

How do non-human primates learn to use their alarm calls? Social learning is a promising candidate, but its role in the acquisition of meaning and call usage has not been studied systematically, neither during ontogeny nor in adulthood. To investigate the role of social learning in alarm call comprehension and use, we exposed groups of wild vervet monkeys to two unfamiliar animal models in the presence or absence of conspecific alarm calls. To assess the learning outcome of these experiences, we then presented the models for a second time to the same monkeys, but now without additional alarm call information. In subjects previously exposed in conjunction with alarm calls, we found heightened predator inspection compared to control subjects exposed without alarm calls, indicating one-trial social learning of ‘meaning’. Moreover, some juveniles (but not adults) produced the same alarm calls they heard during the initial exposure whereas the authenticity of the models had an additional effect. Our experiment provides preliminary evidence that, in non-human primates, call meaning can be acquired by one-trail social learning but that subject age and core knowledge about predators additionally moderate the acquisition of novel call-referent associations.

Social partner cooperativeness influences brain oxytocin transcription in Trinidadian guppies (Poecilia reticulata)

For non-kin cooperation to be maintained, individuals need to respond adaptively to the cooperative behaviour of their social partners. Currently, however, little is known about the biological responses of individuals to experiencing cooperation. Here, we quantify the neuroregulatory response of Trinidadian guppies (Poecilia reticulata) experiencing cooperation or defection by examining the transcriptional response of the oxytocin gene (oxt; also known as isotocin), which has been implicated in cooperative decision-making. We exposed wild-caught females to social environments where partners either cooperated or defected during predator inspection, or to a control (non-predator inspection) context, and quantified the relative transcription of the oxt gene. We tested an experimental group, originating from a site where individuals are under high predation threat and have previous experience of large aquatic predators (HP), and a control group, where individuals are under low predation threat and naïve to large aquatic predators (LP). LP, but not HP, fish showed different behavioural responses to the behaviour of their social environment, cooperating with cooperative partners and defecting when paired with defecting ones. In HP, but not LP, fish brain mid-section oxt relative transcription varied depending on social partner behaviour. HP fish experiencing cooperation during predator inspection had lower oxt transcription than those experiencing defection. This effect was not present in the control population or in the control context, where the behaviour of social partners did not affect oxt transcription. Our findings provide insight into the neuromodulation underpinning behavioural responses to social experiences, and ultimately to the proximate mechanisms underlying social decision-making.

Long-Tailed Pygmy Rice Rats Modify Their Behavioural Response and Faecal Corticosterone Metabolites in Response to Culpeo Fox but Not to Lesser Grison.

Simple SummaryPrey species must fine-tune their antipredator responses to survive, but also to achieve a positive net energy balance which will enhance biological fitness. Given this, we investigated if Oligoryzomys longicaudatus would adapt their behavioural and physiological antipredator responses depending on their relative presence in the predator’s diet. By exposing this rodent species to culpeo fox and lesser grison faeces, we found that O. longicaudatus behavioural and physiological strategies were modulated depending on the predator’s diet. Specifically, rodents would trigger their antipredator responses in the presence of the most dangerous predator, the culpeo, which consumes a higher proportion of O. longicaudatus compared to the lesser grison. Our findings could be of importance for the development of more humane and efficient strategies to control rodent populations.Even though behavioural and physiological reactions to predation risk exhibited by prey species have received considerable attention in scientific journals, there are still many questions still unsolved. Our aim was to broaden the knowledge on one specific question: do long-tailed pygmy rice rats adapt their behavioural and physiological antipredator strategies depending on the predator species? For this question, we live-trapped in a temperate forest in Southern Chile long-tailed pygmy rice rats (Oligoryzomys longicaudatus), which were exposed to three predator odour phases (Phase 0: preliminary, no predator cues; Phase 1: one plot with culpeo fox faeces (Lycalopex culpaeus), one plot with lesser grison (Galictis cuja) faeces and one plot acting as a control with no odour; Phase 2: post treatment, no predator cues). We measured the behavioural response by the capture ratio. To assess the physiological stress response, we collected fresh faecal samples to quantify faecal corticosterone metabolites (FCM). Our results showed that O. longicaudatus increased both the capture ratio and FCM levels in the presence of culpeo cues. Culpeo foxes have higher densities in the study area than G. cuja and exhibit a higher activity pattern overlap with O. longicaudatus. Moreover, it has been also been reported in other regions that L. culpaeus consumption of O. longicaudatus is more frequent compared to G. cuja diet. The increase in capturability could be because traps can be regarded as a shelter in high-risk settings, but it can also be explained by the predator inspection behaviour. The increase in FCM concentrations during culpeo treatment can be linked to the adaptive mobilisation of energy to execute antipredator responses to increase survival chances.

Qingbo, a common cyprinid fish, responds diversely in behavior and locomotion to predators with different hunting modes.

Almost all prey live in habitats with predators with different hunting modes; however, most studies on predation have investigated the effects of only one predator at a time. In this study, we aimed to investigate whether qingbo (Spinibarbus sinensis), a common cyprinid fish, responds differently to active hunting and ambush predators and how qingbo responds when both types of predators coexist. Juvenile qingbo were subjected to catfish (Clarias fuscus, active hunter) exposure, snakehead fish (Channa argus, ambush hunter) exposure, or mixed predator exposure (catfish and snakehead coexistence) for a duration of 60days. Then, their growth, behaviors, swimming performance, and metabolism were measured. Qingbo subjected to active hunting predator exposure exhibited decreased activity and predator inspection and improved fast-start escape performance compared to those in the control group. However, none of the parameters of the fish subjected to ambush predator exposure changed significantly. Fish subjected to mixed predator exposure exhibited improved fast-start escape performance but increased maintenance energy expenditure, whereas no changes were observed in any of the behavioral variables. Qingbo showed a stronger anti-predator response to active hunting predators than to ambush predators, suggesting that the fish exhibit a stronger anti-predator response to a current direct threat than to a potential threat (a predator exists nearby but seldom presents in attack behavior). Additionally, the response of prey fish to multiple predators was quite complex, and the coexistence and interaction of multiple predator species with different hunting modes may lead to serious stress responses and confound the prey's behavioral responses to each predator.

History of canids in Chile and impacts on prey adaptations.

Artiodactyl prey species of Chile, especially guanacos (Lama guanicoe), are reported to be very susceptible to predation by pack‐hunting feral dogs. It has been previously suggested that guanacos and endemic South American deer may have evolved in the absence of pack‐hunting cursorial predators. However, the paleoecology of canid presence in southern South America and Chile is unclear. Here, we review the literature on South American and Chilean canids, their distributions, ecologies, and hunting behavior. We consider both wild and domestic canids, including Canis familiaris breeds. We establish two known antipredator defense behaviors of guanacos: predator inspection of ambush predators, for example, Puma concolor, and rushing at and kicking smaller cursorial predators, for example, Lycalopex culpaeus. We propose that since the late Pleistocene extinction of hypercarnivorous group‐hunting canids east of the Andes, there were no native species creating group‐hunting predation pressures on guanacos. Endemic deer of Chile may have never experienced group‐hunting selection pressure from native predators. Even hunting dogs (or other canids) used by indigenous groups in the far north and extreme south of Chile (and presumably the center as well) appear to have been used primarily within ambush hunting strategies. This may account for the susceptibility of guanacos and other prey species to feral dog attacks. We detail seven separate hypotheses that require further investigation in order to assess how best to respond to the threat posed by feral dogs to the conservation of native deer and camelids in Chile and other parts of South America.

Behavioural variation between piscivore and insectivore rainbow trout Oncorhynchus mykiss.

A proactive-reactive continuum integrating multiple (i.e., 3+) dimensions of animal behaviour has been reported as a major axis of behavioural differentiation, but its stability along a biological hierarchy from individuals to populations remains speculative. Piscivore and insectivore rainbow trout (Oncorhynchus mykiss) represent closely related ecotypes with strong ecological divergence driven by selection for a large-bodied piscivorous lifestyle with fast juvenile growth vs. selection for smaller adult body size and lower growth associated with an insectivorous diet. To evaluate whether differences in behaviour between ecotypes are consistent with a proactive-reactive axis and consistent along a biological hierarchy, the authors examined variation in emergence time from a shelter, exploration, activity and predator inspection among individuals, populations and ecotypes of juvenile piscivore and insectivore rainbow trout O. mykiss. As expected, the faster-growing piscivore ecotype was more proactive (i.e., shorter emergence time, exploration and predator inspection) than the more reactive insectivore ecotype. This behavioural contrast was partly maintained across populations, although activity differences were most pronounced among populations, rather than emergence time. Insectivore fry showed substantial variation in behavioural expression among individuals within populations; by contrast, piscivores showed highly similar proactive behaviours with significantly lower inter-individual variation in behavioural expression, suggesting intense selection on behaviour supporting their faster growth. This work suggests that piscivore and insectivore O. mykiss broadly differ in behaviour along a proactive vs. reactive continuum, and highlights the greater multidimensionality of behavioural expression within the insectivore ecotype. Contrasting behaviours between ecotypes may result from differential selection for slow vs. fast juvenile growth and associated metabolism, and may contribute to adult trophic specialization.

Zebrafish cooperate while inspecting predators: experimental evidence for conditional approach

Different fish species use a conditional approach strategy during predator inspection; the risk of approaching a predator is distributed across all inspectors but is not shared with the animals that keep their distance. Zebrafish, Danio rerio, a highly social fish, is increasingly being used in behavioural neuroscience, but it is not known whether it displays conditional approach. In the predator inspection task, animals are observed in a tank with a refuge in one extremity and an animated image of a predator in the other extremity, with a mirror positioned in parallel to the tank, simulating a perfectly reciprocating conspecific. In experiment 1, animals spent more time in an inspection zone when the image was turned on, but also displayed more erratic swimming, suggesting cooperation under fear. In experiment 2, animals spent more time inspecting predators when the mirror was parallel to the tank (‘cooperating mirror’) than when the mirror was at an angle (‘defecting mirror’), suggesting retaliatory behaviour; in both conditions, animals displayed more freezing and erratic swimming. In experiment 3, no changes in behaviour were observed, regardless of mirror position, when the image was turned off, suggesting that the choice of specific zones in experiment 2 was not due to shoaling tendencies. These results suggest that predator inspection is associated with conditional approach, while at the same time inducing fear-like behaviour in the animal.

Do parasites influence behavioural traits of wild and hatchery-reared Murray cod, Maccullochella peelii?

This study aimed to investigate the links between parasites and behavioural traits of juvenile Murray cod (Maccullochella peelii). The Murray cod is an endangered Australian freshwater fish for which restocking programs are in place and there is a growing human consumption market. However, little is known about the parasites of these fish and how these parasites influence their behaviour and survival. Fingerlings and yearling fish were sourced from a hatchery and the wild, and after acclimatisation in the laboratory, variation in behavioural traits was examined using emergence, exploration and predator inspection tests. The fish were then euthanised to determine their age and examined for infection with parasites. Wild fish had more camallanid nematodes and lernaeid copepods than hatchery fish. An information theoretic approach using Akaike's Information Criterion (AIC) indicated that infection with protozoan cysts was an important factor for predicting the latency to emerge and explore a new environment, which was interpreted as reduced "boldness". In contrast, the presence of lernaeid copepods was included in two of the four best models predicting predator inspection, indicating that infected fish were less likely to inspect a predator. Source of fish (wild or hatchery) was found to be a strong influence on behavioural responses in all our tests. All parasites found in the present study are known to result in clinical signs of diseases in their fish hosts, raising the possibility that responses in tests of behavioural traits reflect side effects of infection. Additionally, the effect of host adaptation to not show signs of parasite infection, or more simply that the effects on behaviour are subtle and difficult to reveal with small sample sizes, is discussed. Nonetheless, we propose that it is important that infection with parasites is considered in fish behavioural studies both to assess survival behaviour and to avoid misinterpretation of behavioural tests of animal personality.

Mate-searching context of prey influences the predator-prey space race.

Predation risk is a strong driver of prey distribution and movement. However, fitness-influencing behaviours, such as mating, can alter risk and influence predator-prey space-use dynamics. In tree crickets, Oecanthus henryi, mate searching involves acoustic signalling by immobile males and phonotactic movement by females. Space-use patterns in tree crickets relative to their primary predators, green lynx spiders (Peucetia viridans), should therefore depend on their current mate-searching state; whether males are calling or non-calling and whether females are phonotactic or non-phonotactic. We first measured the degree of spatial anchoring of crickets to specific bushes in the field and determined whether that influenced the probability of broad-scale spatial overlap with spiders. In the absence of spiders, all crickets, independent of sex or male calling status, were found to be spatially anchored to specific types of bushes and not uniformly distributed on the landscape. At the broad spatial scale, spiders were more likely to be found on bushes with female crickets and, to a lesser degree, calling male crickets. At a finer spatial scale within a bush, movement strategies of crickets not only varied depending on the presence or absence of a spider, but also on their current mate-searching state. Phonotactic females showed clear predator avoidance, whereas calling and non-calling males moved towards the spider instead of away, similar to predator inspection behaviour seen in many taxa. As the strongly selected sex, males are more likely to undertake risky mate-searching activities, which includes inspection of predator positions. Overall, we found that all crickets were predictably anchored at the landscape scale, but their sex and mate-seeking behaviour influenced the degree of overlap with predators and their antipredator movement strategies. Reproductive strategies within a prey species, therefore, can alter predator-prey space race at multiple spatial scales.

Trinidadian guppies use a social heuristic that can support cooperation among non-kin.

Cooperation among non-kin is well documented in humans and widespread in non-human animals, but explaining the occurrence of cooperation in the absence of inclusive fitness benefits has proven a significant challenge. Current theoretical explanations converge on a single point: cooperators can prevail when they cluster in social space. However, we know very little about the real-world mechanisms that drive such clustering, particularly in systems where cognitive limitations make it unlikely that mechanisms such as score keeping and reputation are at play. Here, we show that Trinidadian guppies (Poecilia reticulata) use a 'walk away' strategy, a simple social heuristic by which assortment by cooperativeness can come about among mobile agents. Guppies cooperate during predator inspection and we found that when experiencing defection in this context, individuals prefer to move to a new social environment, despite having no prior information about this new social group. Our results provide evidence in non-human animals that individuals use a simple social partner updating strategy in response to defection, supporting theoretical work applying heuristics to understanding the proximate mechanisms underpinning the evolution of cooperation among non-kin.

Disturbance cues as a source of risk assessment information under natural conditions

Abstract Disturbance cues are released by stressed or disturbed prey prior to a predator attack and convey useful risk assessment information regarding local threats. While studies have shown that disturbance cues may be important early on within the predation sequence (prior to an attack), their role in predator–prey interactions remains relatively overlooked by ecologists. Critically, experimental studies examining disturbance cues, especially among prey fishes, have been conducted primarily under laboratory or semi‐natural conditions. Here, we tested the prediction that disturbance cues function as sources of risk assessment information in situ. We exposed Trinidadian guppies, in two natural populations differing in predation risk, to a model predator paired with stream water or the disturbance cue collected from guppies from either a high‐ or low‐predation risk population. We found that the predator inspection response of guppies to disturbance cues depends on the level of risk of both the focal and the cue source population. Guppies from both populations exhibited increased latencies to inspect, lower inspection rates and reduced inspecting group sizes towards the model paired with conspecific disturbance cues versus a stream water control. Interestingly, guppies of both populations showed evidence of higher perceived predation risk towards the disturbance cues collected from high‐predation risk donors compared to low‐predation risk donors. Our results support the hypothesis that disturbance cues function as a source of information used by prey fish in the assessment of predation risk and provide the first evidence of disturbance cue function under fully natural conditions.

Cue recognition and behavioural responses in the three-spined stickleback (Gasterosteus aculeatus) under risk of fish predation

To effectively respond to predation risk, prey must assess the risk associated with different predation cues. Predation cues can stem either from the predator or from conspecifics and indicate different predation risk levels, thus eliciting different anti-predation responses. The three-spined stickleback is a well-studied fish species often found in gregarious formations. Previous studies show that sticklebacks perform a variety of anti-predation behaviours; however, little is known about how they respond to multiple simultaneous predator cues, characteristic of heterogeneous natural habitats. Here, we experimentally compare the relative importance of three types of predation cues (visual predator cue, chemical predator odour cue and chemical alarm cue from injured conspecifics) and their interactions, on anti-predation and foraging behaviour of sticklebacks. Results showed that (1) individual sticklebacks responded most strongly to visual predator cues, which resulted in reduced foraging activity, increased spine erection and increased predator inspection; (2) the presence of chemical cues (predator odour and/or conspecific alarm cues) stimulates freezing behaviour to a minor extent; and (3) anti-predation behaviour manifests as a trade-off with foraging-related activities. Overall, the results indicate that sticklebacks could assess risk and modify their behavioural responses depending on which cues are present in the environment. The experimental approach of using factorial combinations of different predatory cues can increase our understanding of the role of multimodal cues in aquatic ecosystems.