Social facilitation of exploration in mosquitofish (<Emphasis Type="Italic">Gambusia holbrooki</Emphasis>)

The social environment can exert a powerful influence on the expression of an individual’s behaviour patterns. For example, social facilitation occurs where individuals are more likely to express a given behaviour, or express it a greater rate, in the presence of conspecifics. Social facilitation is partly driven by an individual’s perception of risk, which is a function both of the size of its social group and the information that it gathers relating to predator activity and risk. Here I tested the effects of social group size (one, two, four, eight or 16 fish) and the presence of ‘social’, ‘predation’ or ‘neutral’ chemical cues (derived respectively from live conspecifics, injured conspecifics or a blank water control) on the exploratory behaviour of juvenile mosquitofish (Gambusia holbrooki) in a novel environment. Focal fish in larger groups explored a greater proportion of the arena during the course of the experiment, demonstrating social facilitation of exploration. After 4 h in the arena, focal fish in all group sizes showed significantly reduced swimming activity, suggesting that the initial faster swimming activity of fish on entry to the arena may be in response to the motivation to explore. The presence of predation cues in the environment had the effect of reducing exploratory behaviour across groups in a novel environment, whereas social cues had no effect on exploratory behaviour. Taken as a whole, these results suggest that there is a high degree of context dependency in the expression of exploratory behaviour, with a strong influence of both the presence of conspecifics and cues relating to potential danger.     

Chemical communication in green and golden bell frogs: do tadpoles respond to chemical cues from dead conspecifics?

Captive bred animals often lack the ability of predator recognition and predation is one of the strongest causes of failure of breed and release projects. Several tadpole and fish species respond defensively to chemical cues from injured or dead conspecifics, often referred to as alarm pheromones. In natural conditions and in species that school, the association of chemical cues from predators to alarm pheromones released by attacked conspecifics may lead to the learning of the predator-related danger without experiencing an attack. In the laboratory, this chemical communication can also be used in associative learning techniques to teach naïve tadpoles to avoid specific predators and improve survivorship of released animals. In our experimental trials, tadpoles of the threatened green and golden bell frog (Litoria aurea) did not avoid or decrease their activity when exposed to solutions of conspecific macerate, suggesting that the chemicals released into the water by dead/injured conspecifics do not function as an alarm pheromone. This non-avoidance of dead conspecific chemicals may explain why green and golden bell frog tadpoles have seemingly not developed any avoidance behaviour to the presence of introduced mosquito fish, and may render attempts to teach naïve tadpoles to avoid this novel predator more difficult.     

Experimental assessment of sensory modalities of coral-reef fish larvae in the recognition of their settlement habitat

One of the great mysteries of coral-reef fish ecology is how larvae locate the relatively rare patches of coral-reef habitat on which they settle. The present study aimed to estimate, by experiments in aquaria, the sensory modalities of coral-reef fish larvae for senses used in searching for their species settlement habitat. Larval recognition of settlement habitat can be based on the detection of conspecifics and/or of characteristics of coral habitat using visual, chemical and mechanical cues. For this study, larvae were captured with crest nets and were then introduced into experimental tanks that allowed testing of each type of cue separately (visual, chemical or mechanical cues). Among the 18 species studied, 13 chose their settlement habitat due to the presence of conspecifics and not based on the characteristics of coral habitat, and 5 species did not move toward their settlement habitat (e.g. Scorpaenodes parvipinnis, Apogon novemfasciatus). Among the different sensory cues tested, two species used the three types of cues (Parupeneus barberinus and Ctenochaetus striatus: visual, chemical and mechanical cues), six used two types (e.g. Myripristis pralinia: visual and chemical cues; Naso unicornis: visual and mechanical cues), and five used one type (e.g. Chrysiptera leucopoma: visual cues; Pomacentrus pavo: chemical cues). These results demonstrate that many coral-reef fish larvae could in practice use sensory cues for effective habitat selection at settlement, and have the ability to discriminate species-specific sensory cues.Communicated by J. Krause     

Learned recognition of novel predator odour by convict cichlid embryos

Predation exerts tremendous selection pressure on all organisms. In this study, we exposed embryos of convict cichlids (Amatitlania siquia) twice daily to one of the following: (1) chemical alarm cues of damaged conspecifics + odour of a novel predator (Polypterus endlicheri), (2) chemical alarm cues of damaged conspecifics + water or (3) blank water. No chemical cues were presented after the eggs hatched. When the larvae were 9 days old (mean total length?=?5.7 mm), they were exposed to either predator odour or water. Those larvae that had been conditioned as embryos on alarm cues + predator odour showed a significant reduction in activity (i.e. anti-predator behavioural response) to predator odour relative to the other treatments. This is the first demonstration of acquired predator recognition by fish embryos.     

Social information,conformity and the opportunity costs paid by foraging fish

Animals pay opportunity costs when pursuing one of several mutually exclusive courses of action. We quantified the opportunity costs of conforming to the behaviour of others in foraging sticklebacks (Pungitius pungitius), using an arena in which they were given the option of shoaling in one area or searching for food in another. Fish foraging in the absence of stimulus conspecifics found the prey patch sooner and spent longer exploiting it than those in trials where a stimulus shoal was present. Furthermore, in trials where the stimulus shoal exhibited feeding cues, subjects approached them sooner and spent more time shoaling with them, exploring less of the arena than in trials where the stimulus shoal exhibited no such cues. This suggests sensitivity not only to the mere presence of conspecifics, but also to the social information that they produce. We also saw that groups of focal fish, compared to single individuals, were less influenced by the stimulus shoal and explored more of the arena, a behaviour that may be attributed to facilitation, competition or both. Such opportunity costs are likely to be offset by benefits such as reduced predation risk, and we discuss this in terms of the trade-offs associated with living in groups.     

A test of the senses: fish select novel habitats by responding to multiple cues

Habitat-specific cues play an important role in orientation for animals that move through a mosaic of habitats. Environmental cues can be imprinted upon during early life stages to guide later return to adult habitats, yet many species must orient toward suitable habitats without previous experience of the habitat. It is hypothesized that multiple sensory cues may enable animals to differentiate between habitats in a sequential order relevant to the spatial scales over which the different types of information are conveyed, but previous research, especially for marine organisms, has mainly focused on the use of single cues in isolation. In this study, we investigated novel habitat selection through the use of three different sensory modalities (hearing, vision, and olfaction). Our model species, the French grunt, Haemulon flavolineatum, is a mangrove/seagrass-associated reef fish species that makes several habitat transitions during early life. Using several in situ and ex situ experiments, we tested the response of fish toward auditory, olfactory, and visual cues from four different habitats (seagrass beds, mangroves, rubble, and coral reef). We identified receptivity to multiple sensory cues during the same life phase, and found that different cues induced different reactions toward the same habitat. For example, early-juvenile fish only responded to sound from coral reefs and to chemical cues from mangroves/seagrass beds, while visual cues of conspecifics overruled olfactory cues from mangrove/seagrass water. Mapping these preferences to the ecology of ontogenetic movements, our results suggest sequential cue use would indeed aid successful orientation to novel key habitats in early life.     

Risk level of chemical cues determines retention of recognition of new predators in Iberian green frog tadpoles

In aquatic environments, many prey rely on chemosensory information from injured (alarm cues) or stressed conspecifics (disturbance cues) to assess predation risk. Alarm cues are considered as a sign of higher risk than disturbance cues. These cues could be used by prey to learn potential new predators. In this study, we tested whether Iberian green frog tadpoles (Pelophylax perezi) exhibited antipredator responses to alarm and disturbance cues of conspecifics and whether tadpoles could associate new predators with alarm or disturbance cues. Tadpoles reduced their activity in the presence of disturbance cues, but only weakly when compared with their response to alarm cues. Also, tadpoles learned to recognize new predators from association with alarm or disturbance cues. However, the period of retention of the learned association was shorter for disturbance than alarm cues. Our results indicate that tadpoles are able to modify their antipredatory behavior according to (1) the degree of risk implied by the experimental cues (2) their previous experience of chemical cues of the predator.     

Innate antipredator responses of Arctic charr (<Emphasis Type="Italic">Salvelinus alpinus</Emphasis>) depend on predator species and their diet

The ability to discriminate between more dangerous and less dangerous predators can have serious fitness advantages for fish juveniles. This is especially true for hatchery-reared fish young used for stocking, because their post-release mortality is often much higher than that of wild-born conspecifics. We tested whether two coexisting fish predators and their different diets induce innate behavioral responses in predator-naive Arctic charr (Salvelinus alpinus) young originating from an endangered hatchery-bred population used for re-introductions. We predicted the antipredator responses of charr to be stronger towards chemical cues of brown trout (Salmo trutta) and pikeperch (Stizostedion lucioperca) than towards odorless control water. More pronounced antipredator behavior was predicted in treatments with predators fed on charr than when their diet consisted of another sympatric salmonid, European grayling (Thymallus thymallus), or when they were food-deprived. The Arctic charr young showed strong antipredator responses in all brown trout treatments, whereas odors of the less likely predator pikeperch were avoided with conspecific diet only. Freezing was the most sensitive antipredator behavior, as it was completely absent in control treatments. We found considerable individual variation in the amount and strength of antipredator responses. Although almost half of the charr failed to show antipredator behavior towards the piscivores, those with the innate ability showed highly sensitive recognition of predator odors. Our results indicate that the innate antipredator behavior of the juvenile fish is already finely tuned to respond specifically to chemical cues from different fish predators and even their diets.Communicated by J. Krause     

Female association preferences based on olfactory cues in the guppy,<Emphasis Type="Italic"> Poecilia reticulata</Emphasis>

Guppies are highly sexually dimorphic. Females have been shown to mate preferentially with males with various visible traits and previous studies investigating mate choice have focussed on these visual cues. However, guppies have been shown to respond behaviourally to odour cues from conspecifics as well as from predators. Therefore, sexual selection in guppies may act on multiple sensory modalities, but so far only visual cues have been investigated. Here, we used a specially designed olfactory choice tank to determine whether females could detect other guppies on the basis of their olfactory cues only, and to determine whether females preferred to associate with males or females and whether they could distinguish between different males. We show that female guppies associated preferentially with other females when given a choice between water containing the odour cues from another fish and water containing no odour cues. When females were presented with olfactory cues from a male and a female, they investigated the female initially, but then most reversed their decision and swam to the male. Furthermore, we demonstrate that females associated preferentially with certain males based upon olfactory cues alone, but that this choice was in direct opposition to that made when the females received only visual cues from the same males.Communicated by: M. Abrahams     

Ontogenetic changes in social behaviour in the forest tent caterpillar,<Emphasis Type="Italic"> Malacosoma disstria</Emphasis>

Many animals, including gregarious caterpillars, begin life in groups and become increasingly solitary as they grow larger. These ontogenetic changes in social behaviour suggest that the costs and benefits of grouping change with increasing individual size. Forest tent caterpillar (Malacosoma disstria) colonies exhibit complex social behaviour during the early larval instars, using pheromone trails to move together between temporary bivouacs and feeding sites, and break up as the caterpillars grow. We demonstrate changes in individual responses to cues from conspecifics that explain changes in aggregation during caterpillar development. We used Markov chain analysis to test the influence of pheromone trails and colony-mates on an individual caterpillars tendency to switch between quiescence, searching, walking and spinning. Pheromone-laden silk trails increased the tendency to begin locomotion, whereas colony-mates increased switching from activity to quiescence. Trails also influenced the form taken by locomotor behaviour, and promoted directed walking over searching. Social cues thus increase the efficiency of individual locomotion. Younger larvae were more quiescent and more reluctant to walk in the absence of trails than were older insects. An increase in independent locomotion as the larvae grow provides a mechanism to explain colony break-up and points to an ontogenetic shift in the internal processes driving behaviour. Scaling relationships suggest that many of the benefits associated with group-living in caterpillars decrease as individuals grow larger, providing an adaptive explanation for observed ontogenetic changes in social behaviour.Communicated by N. Wedell     

Different antipredator behaviour in two anuran tadpoles: effects of predator diet

Recent investigations have indicated that animals are able to use chemical cues of predators to assess the magnitude of predation risk. One possible source of such cues is predator diet. Chemical cues may also be important in the development of antipredator behaviour, especially in animals that possess chemical alarm substances. Tadpoles of the common toad (Bufo bufo) are unpalatable to most vertebrate predators and have an alarm substance. Tadpoles of the common frog (Rana temporaria) lack both these characters. We experimentally studied how predator diet, previous experience of predators and body size affect antipredator behaviour in these two tadpole species. Late-instar larvae of the dragonfly Aeshna juncea were used as predators. The dragonfly larvae were fed a diet exclusively of insects, R. temporaria tadpoles or B. bufo tadpoles. R. temporaria tadpoles modified their behaviour according to the perceived predation risk. Depending on predator diet, the tadpoles responded with weak antipredatory behaviour (triggered by insect-fed predators) or strong behaviour (triggered by tadpole-fed predators) with distinct spatial avoidance and lowered activity level. The behaviour of B. bufo in predator diet treatments was indistinguishable from that in the control treatment. This lack of antipredator behaviour is probably related to the effective post-encounter defenses and more intense competitive regime experienced by B. bufo. The behaviour of both tadpole species was dependent on body size, but this was not related to predator treatments. Our results also indicate that antipredator behaviour is largely innate in tadpoles of both species and is not modified by a brief exposure to predators. Received: 22 August 1996 / Accepted after revision: 31 January 1997     

Synergistic interactions between chemical alarm cues and the presence of conspecific and heterospecific fish shoals

Chemical and visual sources of information are used by aquatic prey during risk assessment. Here, we test the behavioral response of littoral prey fish to combinations of chemical alarm cues (skin extract) and the visual presence of a fish shoal. We scented minnow traps with either alarm cues or water (control) placed inside the trap, a jar that contained either a fish shoal or nothing (control), and recorded the number and species of fish captured. We predicted that chemical alarm cues would reduce the number of fish captured and that a fish shoal would increase the number of fish captured. The predicted effect of chemical and visual cues combined depended on the nature of the interaction. We found that the lowest catch rate was for the combination of alarm cue + no shoal, but the highest catch rate occurred for the combination of alarm cue + shoal. Fish shoal + water had the second highest catch rate and no shoal + water had the second lowest catch rate. We conclude that chemical alarm cues induce area avoidance in the absence of a shoal, but a strong behavioral proclivity to increase shoal cohesion in the presence of a shoal. The presence of a shoal in the traps induced alarmed fish to shoal with them and thus, enter the traps. This occurred even though traps were the source of the alarm cue.Communicated by A. Mathis     

Mixed-species shoaling in fish: the sensory mechanisms and costs of shoal choice

The mechanisms and functions of mixed-species shoaling were investigated in two sympatric species of cyprinids, the chub and the European minnow, from the river Wharfe where they comprised approximately 70% of all year 0+ fish over a 20-year survey. Chub preferred conspecific shoals over heterospecific ones with olfactory cues being more important than visual ones for shoal choice. This preference was consistent with measurements of length:flank area ratios and length:weight ratios which suggest that both species are similar in appearance. When presented with mixed-species shoals, chub increased the percentage time spent with stimulus shoals with increasing proportions of conspecifics. Feeding experiments suggest that the preference for conspecific shoals is driven by interspecific competition (with minnows out-competing similar-sized chub) and the oddity effect. The importance of this work in the context of species assortment in free-ranging shoals is discussed.     

Differences in olfactory species recognition in the females of two Australian songbird species

Although birds have recently been shown to possess olfactory abilities and to use chemical cues in communication, limited effort has been made to demonstrate the use of odorants in social contexts. Even less is known regarding the use of odorants in species recognition. The ability to recognize conspecifics should be more pronounced in social species. This study investigated the importance of olfactory cues in species recognition in females of two estrildid finch species with different levels of sociality. Combining odor preference tests with chemical analyses, we surveyed whether female zebra finches and diamond firetails are able to distinguish between the species based on volatile traits and whether individuals exhibit species-specific differences in body odorants. Zebra finches are more social than diamond firetails; nevertheless, both species have an overlapping distribution area. Applying an experimental Y-maze paradigm, we showed that zebra finches can use differences in their species odor fingerprints and displayed a significant preference for the odor of conspecifics over that of heterospecifics, whereas diamond firetails did not reveal a preference. Using gas chromatography and mass spectrometry, we demonstrated that body odorants of the two species were significantly different in relative composition. This finding demonstrates the potential importance of olfactory cues in species recognition, at least in social bird species. Even these two closely related species displayed remarkable differences in their responsiveness to similar chemical cues, which might be caused by species-specific differences in ecology, physiology, or evolution.     

“Armpit effect” in an African cichlid fish: self-referent kin recognition in mating decisions of male Pelvicachromis taeniatus

Kin discrimination in nepotistic as well as in sexual contexts is widespread in animals including humans. However, the underlying mechanisms of kin discrimination are assumed to vary between species and—within species—between contexts. During solitary life stages, kin recognition based on social learning is assumed to be less reliable because kin templates that are not continuously updated may get lost. Therefore, self-referent phenotype matching (“armpit effect”), i.e., the comparison of unknown phenotypes with own characteristics, should be particularly relevant when no social cues are available. However, experimental evidence for this mechanism is scarce. Here, we examine self-referent kin recognition in a mate-choice context in adult male Pelvicachromis taeniatus, a socially monogamous cichlid fish from West Africa with biparental brood care and pronounced kin-mating preferences. Juvenile P. taeniatus live in groups, whereas adult males compete for access to breeding sites which they aggressively defend against rivals. Using computer-animated females as standardized visual stimuli in combination with olfactory cues of related and unrelated females, we show that adult males reared isolated from kin since egg stage were able to discriminate sisters from unrelated females. As males could have learned kin cues only from themselves, our study provides evidence for self-referent kin recognition and indicates that the observed inbreeding preferences are mediated by self-derived olfactory cues. Male preferences for sisters were correlated with male body size. We discuss the implications of quality-related mate choice for the evolution of kin-mating preferences.     

Adaptive behaviour of chironomid larvae (Chironomus riparius) in response to chemical stimuli from predators and resource density

Chemical-mediated effects of predatory fish on chironomid larvae behaviour have been ignored so far. Sediment-dwelling chironomid larvae inhabit protective burrows from which they extend their bodies only to feed on deposited detritus and microalgae from the surrounding sediment. Here, we performed factorial laboratory experiments to study whether fish-borne chemical cues (kairomones) are responsible for behavioural trait changes of chironomid larvae, and whether chironomid larvae are able to assess the densities of fish predators and food resources and the trade-off between them. We exposed naïve Chironomus riparius larvae to the chemical presence of zero, one, and ten predator fish (Rutilus rutilus) and offered two resource levels (low food, high food) for each treatment. Kairomones induced significant inherent behavioural trait changes in chironomid larvae. During the first 120 min after exposing chironomids to fish-conditioned water, we found a significant increase in digging activity with increasing predator density. After 3 days of exposure, the deepest chironomid burrows were found in treatments with the highest predator density. Chironomid larvae were significantly able to adjust their foraging behaviour to different predator densities and food concentrations and trade off between them; that is, when fish predators were more abundant or when more food resources were available, the foraging activities of larvae were significantly reduced. Our data suggest that chemically mediated trait changes (burrowing and foraging behaviour) may cascade through the littoral food web.     

Sensory complementation and the acquisition of predator recognition by salmonid fishes

Following disturbance, some aquatic prey species release chemicals that act as a warning cue and increase vigilance in nearby conspecifics. Such disturbance cues evoke consistent low intensity anti-predator responses. In contrast, alarm cues from injured conspecifics often evoke stronger intensity responses in prey animals. In this study, we test the sensory complement hypothesis, which suggests that multiple cues act in an additive or synergistic fashion to provide additional information for risk assessment by prey. In the first experiment, we showed that juvenile rainbow trout pre-exposed to disturbance cues respond to a given concentration of damage-released alarm cues with a higher intensity of response than the trout that were pre-exposed to cues from undisturbed conspecifics. The two cues acted in an additive fashion. In the second experiment, we demonstrated that disturbance cues alone were not enough to elicit a conditioned response to the odour of a novel predator. We also showed that while disturbance cues elicit an increase in the response of trout to alarm cues, this increase does not translate into a stronger learned response to the predator when the predator odour is paired with alarm cues. Future studies should take into account sensory complementation to avoid underestimating the responses of prey to predators.     

The lexicon of love: what cues cause size-assortative courtship by male garter snakes?

Cues that females use to select potential mates have attracted substantial research effort, but the criteria for male mate choice remain very poorly known. Red-sided garter snakes ( Thamnophis sirtalis parietalis) court and mate in large aggregations around overwintering dens in southern Manitoba, Canada. Both courtship and mating are size-assortative: small male snakes court small as well as large females, whereas larger males court only large females. This system provides a unique opportunity to assess the cues that males use in selecting mates, and in particular the mechanisms that generate a size-related shift in mate preference. Experiments in which we manipulated body sizes and scents showed that both vision and scent (sex pheromones) were important. Large males directed intense courtship only when the stimulus provided both visual and chemical (skin lipid) evidence of large body size. Small males were much less discriminating in both respects. Thus, size-assortative mating in this system is generated not by larger males excluding their smaller rivals from the largest females (as has been reported in other reptile species), but by a size-related shift in the visual and pheromonal cues that elicit courtship. Males of some species may thus show complex patterns of mate choice, with the cues that stimulate courtship differing even among males within a single population based on traits such as age or body size.     

Chemosensory assessment of rival body size is based on chemosignal concentration in male Spanish terrapins

Assessment of the fighting ability of potential opponents is an essential skill to minimize the costs of agonistic interactions between males. Previous research showed that chemical cues released in the water by male turtles may convey information about body size, which is important for intrasexual competition. However, the mechanistic basis of such chemical signaling of body size remains poorly understood. Here, we aimed to experimentally examine whether the release of chemosignals is quantitatively or qualitatively dependent on body size in male Spanish terrapins Mauremys leprosa. We compared the time that turtles spent in a pool with clean water versus water containing chemical stimuli of conspecific males of different body sizes at two different concentrations (“diluted” or “undiluted”). Male terrapins avoided water with chemicals secreted by relatively larger males when these chemicals were undiluted, but not after the chemical stimuli were diluted. In contrast, male terrapins did not avoid chemicals of relatively smaller males in any treatment. Thus, male M. leprosa may assess the size of their rivals on the basis of the concentration or the amounts of their chemical cues released into the water and consequently avoid occupying these ponds with higher concentrations of chemicals. This study gives important hints about the mechanism of chemical signaling in freshwater turtles and demonstrates that male turtles may discriminate different concentrations of chemosignals of conspecifics and modify their behavior accordingly. Likewise, our results support the notion that relative body size is a key factor during male interactions in Spanish terrapins.     

Sexual selection and species recognition in the pygmy swordtail, Xiphophorus pygmaeus: conflicting preferences

Sexual selection and species recognition play important roles in mate choice; however, sexual selection preferences may overlap with traits found in heterospecifics, producing a conflict between sexual selection and species recognition. We examined female preferences in Xiphophorus pygmaeus for male traits that could provide both types of information to determine how females use multiple cues when preferences for these cues would conflict. We also examined X. pygmaeus behavior in the field to determine if females have the opportunity to choose mates. As no male-male competition was observed in the field, and females occasionally chased males from feeding areas, females apparently have the opportunity to exercise mate choice in their natural habitat. In the laboratory, female X. pygmaeus used body size as a sexual selection cue, preferring large heterospecifics (X. cortezi) to small conspecifics. Females also preferred barless X. cortezi over barred X. cortezi when males were size matched. Because X. pygmaeus males do not have bars, this preference suggests that X. pygmaeus females use vertical bars in species recognition, and that large body size and vertical bars are conflicting cues. However, X. pygmaeus females did not have a preference for males of either species when sexual selection and species recognition cues were presented concurrently. This result was surprising, because preferences for species recognition cues are often assumed to be stronger than sexual selection cues. We suggest that females may be using additional species-specific cues in mate choice to prevent hybridization.