Chemically mediated predator inspection behaviour in the absence of predator visual cues by a characin fish

Animals commonly approach (i.e. 'inspect') potential predators. Glowlight tetras, Hemigrammus erythrozonus, have previously been shown to inspect the combined chemical and visual cues originating from novel predators and to modify their inspection (approach) behaviour depending upon the predator's diet. We conducted two experiments to determine whether tetras would inspect the chemical cues of injured prey or the dietary cues of a novel predator in the absence of any visual cues. Shoals of glowlight tetras were exposed to either distilled water (control) or the skin extract of swordtail (lacking ostariophysan alarm pheromones) or the skin extract of tetra (with alarm pheromones). There was no significant difference in the frequency of predator inspection behaviour towards swordtail or tetra skin extract compared to the distilled water controls. In the second experiment, we exposed shoals of tetras to either distilled water or the odour of Jack Dempsey cichlids, Cichlasoma octofasciatum, which had been food deprived, or fed a diet of swordtails or tetras. There was no significant difference in the frequency of predator inspection behaviour towards the odour of the starved cichlids and the odour of the fed cichlids in either of the two diet treatments. However, when tetras were exposed to the odour of cichlids fed tetras, they took significantly longer to initiate an inspection visit, remained further from the source of the chemical cues and inspected in smaller groups, compared with the odour of a starved cichlid or a cichlid fed swordtails. These data strongly suggest that tetras will inspect chemical cues alone, but only if the cue contains information about the predator. Copyright 2000 The Association for the Study of Animal Behaviour.     

Kinship reinforces cooperative predator inspection in a cichlid fish

Kin selection theory predicts that cooperation is facilitated between genetic relatives, as by cooperating with kin an individual might increase its inclusive fitness. Although numerous theoretical papers support Hamilton's inclusive fitness theory, experimental evidence is still underrepresented, in particular in noncooperative breeders. Cooperative predator inspection is one of the most intriguing antipredator strategies, as it implies high costs on inspectors. During an inspection event, one or more individuals leave the safety of a group and approach a potential predator to gather information about the current predation risk. We investigated the effect of genetic relatedness on cooperative predator inspection in juveniles of the cichlid fish Pelvicachromis taeniatus, a species in which juveniles live in shoals under natural conditions. We show that relatedness significantly influenced predator inspection behaviour with kin dyads being significantly more cooperative. Thus, our results indicate a higher disposition for cooperative antipredator behaviour among kin as predicted by kin selection theory.     

N-person games and the evolution of co-operation: a model based on predator inspection in fish

Two N-person game theoretical models examining the evolution of co-operation during predator inspection in fish are presented. Predator inspection occurs in small shoals of fish, in which one to a few individuals, the "inspectors" (co-operators) break away from the shoal and cautiously approach a predator to obtain information on this potential danger. In the models presented here, remaining with the shoal and not inspecting is considered an act of defection. Both model I and II produce a stable internal polymorphism of inspectors and noninspectors. While the equilibrial frequency of inspectors can be low (i.e. less than 10%) at large shoal size, the proportion of shoals containing any inspectors--and therefore exhibiting the inspection behavior--is much greater. Both models presented here, and N-person games in general are equivalent to intrademic group selection models of evolution in structured populations, in which shoals are trait groups and co-operation evolves by between-shoal selection. While the results are cast in terms of predator inspection, the model itself is general and applies to any multi-group scenario where co-operators benefit entire groups at their own expense. The results presented here add to the mounting theoretical and empirical evidence that co-operation is frequently not a pure evolutionarily stable strategy, and that many metapopulations should be polymorphic for both co-operators and defectors.     

Characterization of chemical defenses in ranid tadpoles against a fish predator

Tadpoles of some ranid species appear to possess chemical defenses against fish predators, but the chemicals have not been characterized. Here, we evaluated the vulnerability of three Japanese anuran tadpole species (Glandirana rugosa, Pelophylax nigromaculatus, and Hyla japonica) to a fish (Gnathopogon elongatus elongatus) and analyzed the defensive chemicals extracted from the unpalatable tadpoles. Additionally, we examined the defensive behavior of unpalatable tadpoles in response to fish chemical cues. The fish rejected both G. rugosa (83%) and P. nigromaculatus (48%), but not H. japonica (0%). Many of the rejected tadpoles survived (60–80%). Possible defensive chemicals were extracted by methanol from the skin of G. rugosa, but were not identifiable by gas chromatography–mass spectrometry because of small quantities. The chemicals have high polarity and non-volatility. When exposed to fish chemical cues, P. nigromaculatus decreased activity presumably as a defensive behavior, but G. rugosa did not. We demonstrated the presence of chemical defenses in at least two of these species and revealed that G. rugosa releases more effective or greater amounts of defense chemicals than P. nigromaculatus with respect to this fish predator. The increased efficacy of chemical defenses may correlate with decreasing defensive behavior.     

Exploratory behaviour and novel predator recognition: behavioural correlations across contexts

It was hypothesized that the exploratory behaviour of an individual measured in a novel environment could predict its behaviour in response to a novel predator. This study examined novel predator recognition in the western mosquitofish Gambusia affinis, a species with individual differences in risk‐taking, activity and exploration in novel environments. Prey responded with characteristic shoaling and avoidance in response to native predators, but did not show characteristic antipredator behaviour towards novel predators. Furthermore, G. affinis exhibited individual‐level behavioural correlations across contexts but only when prey were tested with native predators. This could be the result of native predatory selection on behavioural correlations in the prey species.     

Introduced predator elicits deficient brood defence behaviour in a crater lake fish

Introduced species represent one of the most serious global threats to biodiversity. In this field-based study, we assessed behavioural responses of brood tending cichlid fish to an invasive predator of their offspring. This was achieved by comparing parental defence responses of the endangered arrow cichlid (Amphilophus zaliosus), a fish species endemic to the crater lake Apoyo in Nicaragua, towards the bigmouth sleeper (Gobiomorus dormitor), a formidable predator of cichlid fry, and all other potential fish predators of offspring. The bigmouth sleeper was recently introduced into Apoyo but naturally co-exists with cichlids in a few other Nicaraguan lakes. Arrow cichlid parents allowed bigmouth sleepers to advance much closer to their fry than other predators before initiating aggressive brood defence behaviours. Interestingly, parents of a very closely related species, A. sagittae, which has coevolved with bigmouth sleepers in crater lake Xiloá, reacted to approaching bigmouth sleepers at comparable distances as to other predators of cichlid fry. These results provide a novel demonstration of the specific mechanism (i.e. naive parental behaviour) by which invasive predators may negatively affect species that lack the adequate behavioural repertoire.     

Grazing behaviour of a non‐herbivorous characin: revisiting plasticity

Feeding behaviour and diet of Bryconamericus microcephalus differed between canopy conditions. At the open canopy site, a behavioural modification, grazing on algae, was observed. This was also reflected in gut content analysis and suggests behavioural plasticity in response to resource availability.     

Antipredator behaviour and predator recognition in Belding's ground squirrels

This study evaluates whether Belding's ground squirrels (Spermophilus beldingi) recognize predators under natural conditions. I observed these squirrels for 300 h during two consecutive summers, during which I described 1029 aerial and terrestrial interactions, including 299 interactions with animals known to prey on squirrels. Squirrels responded differentially to predators and non-predators, to predators that hunt differently, and to contextually different interactions with the same predator. Responses shown in encounters with predators included Trill and Chirp vocalizing, upright Posting, crouching, running to burrow entrances, entering burrows, Approaching or chasing predators, and doubling-back on pursuing predators. Ground squirrels appear to adjust their antipredator behaviour depending on the amount and kind of danger they face during an encounter.     

Smell, learn and live: The role of chemical alarm cues in predator learning during early life history in a marine fish

The speed with which individuals can learn to identify and react appropriately to predation threats when transitioning to new life history stages and habitats will influence their survival. This study investigated the role of chemical alarm cues in both anti-predator responses and predator identification during a transitional period in a newly settled coral reef damselfish, Pomacentrus amboinensis. Individuals were tested for changes in seven behavioural traits in response to conspecific and heterospecific skin extracts. Additionally, we tested whether fish could learn to associate a previously novel chemical cue (i.e. simulated predator scent) with danger, after previously being exposed to a paired cue combining the conspecific skin extract with the novel scent. Fish exposed to conspecific skin extracts were found to significantly decreased their feeding rate whilst those exposed to heterospecific and control cues showed no change. Individuals were also able to associate a previously novel scent with danger after only a single previous exposure to the paired conspecific skin extract/novel scent cue. Our results indicate that chemical alarm cues play a large role in both threat detection and learned predator recognition during the early post-settlement period in coral reef fishes.     

Scents and scents-ability: pollution disrupts chemical social recognition and shoaling in fish

Chemical cues are of enormous importance in mediating the behaviour of animals, enabling them to navigate throughout their habitats, to detect the presence of predators or prey and for social recognition-identifying and discriminating between conspecifics. In many species of freshwater fish, social recognition is known to be based primarily on chemical cues. Such recognition mechanisms are vulnerable to disruption by the presence of anthropogenic contaminants in the aquatic environment. Here we show that acute exposure to low, environmentally relevant dosages of the ubiquitous contaminant, 4-nonylphenol, can seriously affect social recognition and ultimately social organization in fishes. A 1 hour 0.5 microgl-1 dose was sufficient to alter the response of members of a shoaling fish species (juvenile banded killifish, Fundulus diaphanus) to conspecific chemical cues. Dosages of 1-2 microgl-1 caused killifish to orient away from dosed conspecifics, in both a flow channel and an arena. Given the overall importance of shoaling as an adaptive strategy against predators and for locating food, it is likely that its disruption by anthropogenic contaminants would have serious implications for fishes' fitness.     

Genetics, behaviour and chemical recognition of the invading ant Pheidole megacephala

Introduced species often become ecologically dominant, displacing native species and posing a serious threat to ecosystem function and global biodiversity. Ants are among the most widespread and damaging alien species; introductions are often accompanied by population-level behavioural and genetic changes contributing to their success. We investigated the genetic structure, chemical profile and nestmate recognition in introduced populations of the invasive big-headed ant, Pheidole megacephala, in Australia. Behavioural analyses show that workers are not aggressive towards conspecifics from different nests, even at large geographical scales (up to 3000 km) and between populations encompassing a wide range of environmental conditions. By contrast, interactions with workers of other species invariably result in agonistic behaviours. Genetic analyses reveal that populations have low genetic diversity. No genetic differentiation occurs among nests of the same population; differentiation between populations, though significant, remains weak. Chemical analyses indicate that cuticular lipids are similar between colonies of a population, and that differentiation between populations is low. Altogether, these results indicate that the big-headed ant P. megacephala forms a large unicolonial population across northern/eastern Australia.     

The role of experience and chemical alarm signalling in predator recognition by fathead minnows, Pimephales promelas

Young-of-the-year, predator-naive fathead minnows, Pimephales promelas , from a pikesympatric population did not respond to chemical stimuli from northern pike, Esox Indus , while wild-caught fish of the same age and size did. These results suggest that chemical predator recognition is a result of previous experience and not genetic factors, Wild young-of-the-year minnows responded to pike odour with a response intensity that was similar to that of older fish, demonstrating that the ability to recognize predators is learned within the first year. The intensity of response of wild minnows which had been maintained in a predator free environment for 1 year was similar to that of recently caught minnows of the same age, suggesting that reinforcement was not required for predator recognition to be retained. Naive minnows that were exposed simultaneously to chemical stimuli from pike (a neutral stimulus) and minnow alarm substance exhibited a fright response upon subsequent exposure to the pike stimulus alone. Predator-naive minnows exposed simultaneously to chemical stimuli from pike and glass-distilled water did not exhibit a fright response to the pike stimulus alone. These results demonstrate that fathead minnows can acquire predator recognition through releaserinduced recognition learning, thus confirming a known mechanism through which alarm substance may benefit the receivers of an alarm signal.     

Prey patchiness, predator survival and fish recruitment

A simple mathematical model is presented for the population dynamics of fish larvae when the main food supply, in this case copepods, is spatially patchy in its distribution. Encounters by an individual predator (larva) with prey patches, and with individual prey within patches, are represented by Poisson processes. It is demonstrated analytically, and confirmed by numerical experiments, that prey patchiness fails to alter mean predator-prey encounter rates from their values for homogeneous prey distributions. Individual variance in encounter rate is, however, much affected. This has significant consequences for the (small) numbers of larvae surviving to metamorphosis and recruitment to the adult fish population.     

Shovelnose sturgeon exhibit predator avoidance behaviour in the presence of a hungry predator

An experiment was designed to test whether age‐0 shovelnose sturgeon (Scaphirhynchus platorynchus) exhibited predator avoidance behaviour in response to a channel catfish (Ictalurus punctatus) predator. It was hypothesized that shovelnose sturgeon would not exhibit any innate predator avoidance behaviour because previous reports have shown a congener of the shovelnose sturgeon, the pallid sturgeon (S. albus), to be an unfavourable prey item for channel catfish. The results, however, indicated that shovelnose sturgeon generally avoided space occupied by the catfish predator and spent a greater proportion of time in the predator avoidance zone within the experimental tank. Bitten fish, in particular, spent a greater period of time in the predator avoidance zone. Of all sturgeon used in this experiment (N = 30), 73% swam within the fork length (350 mm) of the catfish predator. The results seem to indicate that shovelnose sturgeon were initially oblivious to the risk of predation by the catfish predator, but after interaction (e.g. being chased or bitten) appeared to display predator avoidance behaviour. Predator avoidance behaviour in shovelnose sturgeon may thus be suggested as a learned rather than an innate behaviour.     

A native dasyurid predator (common planigale,Planigale maculata) rapidly learns to avoid a toxic invader

Abstract Interactions between invasive species and native fauna afford a unique opportunity to examine interspecific encounters as they first occur, without the complications introduced by coevolution. In northern Australia, the continuing invasion of the highly toxic cane toad Bufo marinus poses a threat to many frog‐eating predators. Can predators learn to distinguish the novel toxic prey item from native prey (and thus, avoid being poisoned), or are longer‐term genetically based changes to attack behaviour needed before predators can coexist with toads? To predict the short‐term impact of cane toads on native predators, we need to know the proportion of individuals that will attack toads, the proportion surviving the encounter, and whether surviving predators learn to avoid toads. We quantified these traits in a dasyurid (common planigale, Planigale maculata) that inhabits tropical floodplains across northern Australia. Although 90% of naïve planigales attacked cane toads, 83% of these animals survived because they either rejected the toad unharmed, or killed and consumed the prey snout‐first (thereby avoiding the toxin‐laden parotoid glands). Most planigales showed one‐trial learning and subsequently refused to attack cane toads for long time periods (up to 28 days). Toad‐exposed planigales also avoided native frogs for up to 9 days, thereby providing an immediate benefit to native anurans. However, the predators gradually learnt to use chemical cues to discriminate between frogs and toads. Collectively, our results suggest that generalist predators can learn to distinguish and avoid novel toxic prey very rapidly – and hence, that small dasyurid predators can rapidly adapt to the cane toad invasion. Indeed, it may be feasible to teach especially vulnerable predators to avoid cane toads before the toads invade, by deploying low‐toxicity baits that stimulate taste‐aversion learning.     

Nest defence,enemy recognition and nest inspection behaviour of experimentally parasitized Reed Warblers Acrocephalus scirpaceus

Capsule Reed Warblers in a regularly parasitized population do not recognize Cuckoo Cuculus canorus as a special enemy and do not change their behaviour at nest immediately after being parasitized.

Aims To assess if an intruder near the nest influences the behaviour of the Cuckoo host.

Methods Host responses to Cuckoo, control Pigeon dummies and human intruder were observed. Host behaviour at 71 nests was video-recorded for 30 minutes at four experimental groups of nests: Cuckoo dummy, Cuckoo dummy + Cuckoo egg, Pigeon dummy, human intruder.

Results Reed Warblers did not respond differently to the Cuckoo and the control species. The experimental procedure had no significant effect on the behaviour of hosts during the study period. We were unable to find any differences in the time spent at the nest, clutch inspection behaviour and nest defence behaviour between morning and afternoon experimental groups. Our results do not support the hypothesis that afternoon laying by the Cuckoo is maintained by a selection pressure from the host. We observed no ejection or egg-pecking during the 30-min period after the experimental parasitism.

Conclusions Low aggression and non-specificity of host responses in our study area are in line with the fact that the Reed Warbler is an intermediate rejecter of Cuckoo eggs as expected from the spatial habitat structure hypothesis.     

Caudal eyespots on fish predators influence the inspection behaviour of Trinidadian guppies, Poecilia reticulata

The effect of the false caudal eyespots (ocelli) of fish predators on guppy inspection behaviour was tested by use of predator ( Crenicichla ) models with and without a caudal ocellus. When a false eyespot was present, inspecting guppies spent significantly less time near the tail compared to a control model without a tail eyespot.