Combined effects of flow condition and parasitism on shoaling behaviour of female guppies Poecilia reticulata

Group living in fish can provide benefits of protection from predators and some parasites, more efficient foraging for food, increased mating opportunities and enhanced energetic benefit when swimming. For riverine species, shoaling behaviour can be influenced by various environmental stressors, yet little is known how flow rate might influence the shoaling of diseased fish shoals. In view of the increasingly unpredictable flow rates in streams and rivers, this study aimed to assess the combined effect of flow condition and parasitism on the shoaling behaviour of a model fish species. Shoal size, shoal cohesion and time spent shoaling of female guppies Poecilia reticulata were compared when infected with the directly transmitted ectoparasite Gyrodactylus turnbulli under flow and static conditions. Flow condition was an important factor in influencing shoaling behaviour of guppies with the fish forming larger shoals in the absence of flow. When a shoal member was infected with G. turnbulli, shoal cohesion was reduced, but the magnitude of this effect was dependent on flow condition. In both flow and static conditions, bigger fish formed larger shoals than smaller counterparts. Future changes to stream hydrology with more frequent flooding and drought events will affect the shoaling tendency of fish. During high-flow events, diseased fish may not be able to keep up with shoal mates and therefore have a higher risk of predation. Additionally, these findings may be important for aquaria and farmed species where an increase in flow rate may reduce aggregation in fish.     

Performance level and efficiency of two differing predator-avoidance strategies depend on nutritional state of the prey fish

Animal prey has developed a variety of behavioural strategies to avoid predation. Many fish species form shoals in the open water or seek refuge in structurally complex habitats. Since anti-predator strategies bear costs and are energy-demanding, we hypothesised that the nutritional state of prey should modify the performance level and efficiency of such strategies. In aquaria either containing or lacking a structured refuge habitat, well-fed or food-deprived juvenile roach (Rutilus rutilus) were exposed to an open-water predator (pikeperch, Sander lucioperca). Controls were run without predators. In the presence of the predator, roach enhanced the performance of the anti-predator strategy and increased the use of the refuge habitat whereby food-deprived roach were encountered more often in the structure than well-fed roach. Nonetheless more starved than well-fed roach were fed upon by the predator. In the treatments offering only open-water areas, roach always formed dense shoals in the presence of the predator. The shoal density, however, was lower in starved roach. Starving fish in shoals experienced the highest predation mortality across all experimental treatments. The experiment confirmed the plasticity of the anti-predator behaviour in roach and demonstrated that food deprivation diminished the efficiency of shoaling more strongly than the efficiency of hiding. The findings may be relevant to spatial distribution of prey and predator–prey interactions under natural conditions because when prey are confronted with phases of reduced resource availability, flexible anti-predator strategies may lead to dynamic habitat use patterns.     

Size-assorted fish shoals and the majority's choice

Similarity among group members may serve as a defence against visually hunting predators that preferentially attack individuals who are phenotypically different from the group majority. The presence of such odd individuals in an otherwise homogeneous group may, however, increase the vulnerability of the other group members as well. Individuals might thus be expected to form uniform groups in order to decrease predation risk, not only in trying to avoid being odd in a group, but also when attempting to avoid being accompanied by odd individuals. This hypothesis was tested with small and large three-spined sticklebacks, Gasterosteus aculeatus. Focal fish were offered the choice between a shoal consisting of conspecifics that were all similar in body length to the focal fish (matching shoal) and a shoal in which one or a few individuals differed in body length from the focal fish (non-matching shoal). In the control experiment, all individuals in the non-matching shoal differed in size from the focal fish. The control confirmed that individuals preferably joined the matching shoal when the alternative option was to be odd in another one. However, when the alternative for size-assortative shoaling was to belong to the majority in a mixed shoal, the shoal choice of individuals appeared on average to be random. Visual contact with a live pike, Esox lucius, did not affect the shoal choice pattern. Furthermore, despite the frequency-dependent nature of the oddity effect, varying the number of odd individuals in the non-matching shoal did not have a significant effect on individual's shoaling decisions. These results suggest that size-assortativeness in fish shoals is not a result of individuals avoiding being among the majority in a mixed group. Received: 2 September 1998 / Received in revised form: 12 May 1999 / Accepted: 29 May 1999     

Shoaling decisions in three-spined sticklebacks (<Emphasis Type="Italic">Gasterosteus aculeatus</Emphasis>)—familiarity,kinship and inbreeding

Shoaling with familiar kin is a well-known phenomenon. It has been described both for adult and for fry of three-spined sticklebacks (Gasterosteus aculeatus). However, evidence of preference for kin independent of familiarity is scarce. Furthermore, inbreeding effects have not been studied for shoaling preferences and there is a lack of studies about changes in individuals’ ability to recognise kin during different phases of life history. We gave inbred and outbred, nonreproductive sticklebacks of different age the choice to shoal with a group of familiar siblings vs unfamiliar non-siblings and with unfamiliar siblings vs unfamiliar non-siblings. Subadult sticklebacks preferred to shoal with familiar kin over unfamiliar non-kin, but inbred and outbred individuals had similar preferences. When given the choice between unfamiliar siblings and unfamiliar non-sibs, adult outbred fish preferred the shoal of kin, while inbred fish behaved indifferently. Body characteristics of the group such as body mass, standard length and condition of its members did not significantly explain the shoaling preferences for kin. Thus, sticklebacks were capable of recognising familiar and unfamiliar kin. The latter capability was lost by inbreeding.     

Shoal composition, body size and foraging in sticklebacks

Individuals which deviate from the majority in groups are likely to be most vulnerable to predation. This oddity effect, by definition, is frequency dependent, eventually fading at equal frequencies of the phenotypes in a group. It has been hypothesized that the increased predation risk of odd individuals may play an important role in the formation of phenotypically uniform shoals of fish. However, recent work has indicated that individuals may experience, or value, their predation hazard differently depending on their own size in relation to that of other group members: single large fish, but not small ones, appear concerned about their oddity in a shoal. Here I show that the apparent wariness of large fish is also expressed in a frequency-dependent manner, closely conforming to what is predicted if the oddity effect is responsible for their behavior. Using foraging activity of individuals as a means to evaluate their predation risk, I demonstrate with shoals comprising 12 threespine sticklebacks (Gasterosteus aculeatus) that large fish forage least actively when in a shoal consisting of 2 large and 10 small fish. An increase in the number of large fish to 4 among 8 small individuals clearly results in an increase in their foraging activity. However, having reached an equal frequency with small fish in a shoal, large fish do not seem to change their foraging activity much even when their number in a shoal increases further. In contrast, foraging activity of small sticklebacks remains fairly constant throughout the entire range of tested shoal compositions, providing further evidence that small and large fish respond to their oddity differently. Received: 12 February 1998 / Accepted after revision: 7 May 1998     

Eutrophication alters social preferences in three-spined sticklebacks (Gasterosteus aculeatus)

Algae blooms, which can be caused by eutrophication, drastically influence the ecology and behaviour of aquatic organisms. Such impact is often demonstrated in the context of mate choice and predator–prey interactions. In contrast, the influence of increased turbidity on social behaviour is less well understood, although it may have strong influence, at both the level of the individual and the population. We aimed to address this gap in our knowledge by using the well-described preference of three-spined sticklebacks (Gasterosteus aculeatus) to shoal with the larger of two shoals as model behaviour. In our experiments focal fish had the choice between two shoals of different sizes, either in clear or in turbid water containing green algae. Fish in clear water spent significantly more time near the larger shoal, while fish in algae water showed no significant preferences. Furthermore, fish tested in clear water changed more often between the shoals than fish tested in algae water. These results indicate that eutrophication-induced algae blooms have the potential to alter social decisions of sticklebacks. Such changes of social decisions do not only influence the behaviour of individuals, furthermore it might influence entire populations. This might eventually lead to changes of the structure of the social system.     

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.     

Hunger-dependent predator inspection and foraging behaviours in the threespine stickleback (Gasterosteus aculeatus) under predation risk

Individual fish commonly leave the relative safety of the shoal to approach potential predators at a distance. Not all members of a shoal are equally likely to initiate such predator inspection visits. Here, we show for the first time that the current hunger state of individual fish strongly influences their predator inspection behaviour, as well as their foraging rate, in the face of predation hazard. When all members of threespine stickleback (Gasterosteus aculeatus) test shoals were in a similar hunger state, they were equally likely to inspect a trout predator model alone and did not differ in the frequency of their inspection visits or foraging rate. However, when individual sticklebacks in a shoal differed in their hunger state, the food-deprived (i.e. hungrier) member of the shoal fed at a higher rate, was significantly more likely to initiate solitary predator inspection visits, and inspected the predator model significantly more often than its less hungry (i.e. well-fed) shoal mates. Individual fish which inspected the predator model more frequently also tended to have higher feeding rates. The results indicate that the hungrier fish in a shoal are more willing to take greater risks to inspect a potential threat at a distance, compared with their well-fed shoal mates, and suggest that they may gain a foraging benefit in doing so. If marked asymmetries in hunger state exist among members of fish shoals, then mutual cooperation during predator inspection visits may be difficult to achieve because well-fed individuals are not as likely to initiate or participate in inspection visits as are hungry individuals.Correspondence to: J.-G.J. Godin     

Sensory ecology in a changing world: salinity alters conspecific recognition in an amphidromous fish, Pseudomugil signifer

Group fission and fusion processes are driven by state dependence, risk and the availability of information from others. Yet the availability of information changes under different environmental conditions, thus aiding or inhibiting group formation and maintenance. Chemical cues provide information on the location of individuals and can act as a mechanism for individuals to group together, although they can be greatly affected by environmental conditions. Using a flow channel, we studied how one shoaling fish species, the Pacific blue-eye (Pseudomugil signifer), responds to conspecific chemical cues (CCCs) in different environmental conditions (salinities). This species lives in estuarine environments, ranging in salinity from fresh to fully marine. P. signifer responded to CCCs in freshwater but not in saltwater. Furthermore, P. signifer did not respond to saltwater with CCCs added from freshwater. It took significantly longer for fish in saltwater, than in freshwater, to locate and join a shoal when only CCCs from the shoal were present. Finally, fish formed more cohesive shoals in freshwater than in brackish or saltwater. These results suggest that these fish do not rely on chemical cues in saltwater to locate conspecific shoals. Furthermore, the reduced amounts of these cues in saltwater may inhibit the maintenance of tight shoal structures. We suggest that fish utilise different sensory modalities in fresh or saltwater in order to locate one another, or the social structure of these groups is fundamentally different between these two water types. The importance of this study in relation to understanding how animals utilise and change different sensory modalities in varying environmental conditions is discussed.     

Shoaling as an anti-ectoparasite mechanism in juvenile sticklebacks (Gasterosteus spp.)

Summary In laboratory experiments, we tested the hypothesis that by living in larger shoals, juvenile threespine (Gasterosteus aculeatus) and blackspotted (G. wheatlandi) sticklebacks lower their risk of being parasitized by the crustacean ectoparasite Argulus canadensis. An increase in shoal size resulted in a lower average number of attacks received by individual fish, but had no negative effect on the attack performance (attack rate and attack success) of the parasites. In addition, more fish formed shoals and shoal sizes were larger in the presence of parasites. We conclude that ectoparasitism may have been a strong selective factor in the evolution of social behaviour in juvenile sticklebacks.     

Predator shoaling moderates the confusion effect in blue-green chromis,Chromis viridis

Summary In experiments, blue-green chromis [Chromis viridis (Cuvier 1830)] were fed on either scattered or aggregated swarms of brine shrimp (Artemia sp.). Ten runs with each prey dispersion treatment were performed with shoals of one, two, five and ten chromis. The mean lag in reaching peak feeding rate for fish fed on aggregated prey was significantly shorter in the larger chromis shoals. In contrast, with the scattered treatment all such lags were similar and very short. As foraging proceeded, higher feeding rates were observed in the larger feeding shoals, regardless of prey dispersion. Prey capture success (i.e. the rate of retention of intercepted prey) declined with time, but was significantly higher in groups of ten fish. Two main conclusions emerge. Firstly, grouping facilitated initiation of feeding by individuals preying on concentrated swarms and reduced the delay in reaching a maximum feeding level. This may have been due to a suppression of the confusion effect through reduced reliance upon vigilance. Secondly, reduced vigilance allowed larger shoals of chromis to feed effectively over more extended periods. Trends of increasing shoal cohesion and decreasing prey retention rate with time were consistent with a postulated increase in antipredator vigilance with declining feeding motivation.     

Predator choice in the field; grouping guppies, Poecilia reticulata, receive more attacks

Capture success of many predator species has been shown to decrease with increasing prey group size and it is therefore suggested that predators should choose to attack stragglers and/or small groups. Predator choice in the laboratory has shown mixed results with some species preferentially attacking large groups and others preferring to attack stragglers over groups. Such predator choices have not been tested in the field. In our study we presented a binary choice between a shoal of guppies and a single guppy to predators in pools in the Arima river, Trinidad. We observed attacks in 11 different pools from a total of 53 predators (20 acara cichlids, Aequidens pulcher, 32 pike cichlids, Crenicichla frenata, and one wolf-fish, Hoplias malabaricus) and found that all predators showed a strong preference for the shoal of guppies in terms of both first choice and total number of attacks. We discuss the implications of these preferences with regards to predator–prey interactions.     

Shoaling fish can size-assort by chemical cues alone

Animals that form groups are typically assorted by phenotype. For example, fish shoals are notably composed of closely size-matched individuals, yet the sensory mechanisms that promote this behaviour have not been fully determined. Here, we show that two freshwater shoaling fish species, three-spined stickleback and banded killifish, have a greater preference for the chemical cues of conspecifics that are the same size as themselves than for those of larger or smaller conspecifics. We suggest that this ability to determine their own size relative to conspecifics may be based on chemical self-referencing. This provides a novel insight to the mechanisms underlying a widespread phenomenon in social behaviour, and provides further evidence of the crucial role played by chemical cues in structuring the interactions of fishes.     

Association patterns of sailfin mollies (Poecilia latipinna): alternative hypotheses

Individuals may associate with each other due to a variety of selective forces, such as intra- and intersexual selection, and conspecific recognition. Previous studies have concluded that mate choice governs association behavior in polygynous species of fish. I examined whether mate choice underlies the preference for larger individuals by examining preference for association (time spent in proximity to a fish) not only between opposite-sex individuals but also between same-sex individuals of the live-bearing sailfin molly (Poecilia latipinna). Males and females from three size classes were tested with a large and a small object fish of the same and opposite sex. Females preferred to associate with larger over smaller males. Males also preferred to associate with larger over smaller females, as expected. The same female and male test fish also preferred to associate with larger over smaller fish of the same sex. Moreover, females demonstrated no significant difference in their strength of preference (large–small) when offered males or females. The same held true for males. When males and females were subsequently tested with one large male and one large female, females tended to prefer large males while males showed no significant preference for association based on sex. In another experiment, females were tested with a large female and a small male, and significantly preferred the former. These findings suggest that association patterns may have arisen under a variety of conditions, such as predation pressures, shoaling behavior, and associative preference behavior. The assumption that association behavior is a uniformly sufficient predictor of mate choice in fish needs to be re-examined for P. latipinna and other species. Received: 6 November 1998 / Received in revised form: 12 May 1999 / Accepted: 12 May 1999     

Fish in larger shoals find food faster

Summary Experiments on shoaling cyprinids hunting for food on patches in tanks demonstrate and advantage of foraging in a group. Individual goldfish (Carassius auratus) and minnows (Phoxinus phoxinus) in a shoal of conspecifics located food more rapidly as shoal size increased from 2 to 20. although shoaling minnows form polarised schools more readily than goldfish, which rarely do so, both species benefited from the trend of speedier food location with increasing group size.     

Innate responses to male sexual harassment in female mosquitofish

Male mosquitofish are very persistent in their sexual activity and harass any female they encounter. Gravid females pay a large tribute to this intense male sexual activity in terms of reduced foraging efficiency. Previous observations have demonstrated that gravid females, when chased by a male, dilute male harassment by moving closer to other females to form shoals. They also approach other males to promote male competition, and when males differ in size, they preferentially target large males, whose harassment is less intense. In this study, we tested whether the modulation of females’ social preferences in response to male harassment is innate or learned. We tested social preference in three groups of females that differed in experience of sexual harassment and in the factors affecting it. Females of the first group were reared without any sexual experience, and pregnancy was induced through artificial insemination. The second group was composed of naive females kept singly with a male; these females experienced sexual harassment but were prevented from experiencing the effects of male–male competition and shoaling on the amount of male sexual harassment. In the third group (controls), females were reared in multi-male, multi-female groups and could experience the modulating effects of social interactions on sexual harassment. When exposed to a harassing male, females of the three groups immediately reduced their distance from another female, approached a group of males or moved toward the larger of two available males. Moreover, the results for these three groups of females were similar to those obtained in wild-caught females that were tested in the same three tests in a previous study (Dadda et al. An. Behav., 70:463–471, 2005). This suggests that the strategies adopted by females in response to male sexual harassment do not need to be learned through specific experience of the social contexts.     

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.     

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.     

Predator evasion in a fish school: test of a model for the fountain effect

A model to explain the behavioural mechanisms underlying the fountain manoeuvre, a predator-evasion response shown by fish shoals is tested. It is proposed that the responses of individual fish are constrained by requirements to (1) visually monitor the predator's behaviour, (2) minimise the energetic cost of escape, and (3) maximise the rate of passage around the predator. The model predicts that individuals will swim away from the threat at a constant angle determined by the rear limit of the visual field and that the range of reaction will be constrained by water visibility. The model's predictions were upheld in tests conducted in 1984 using a shoal of juvenile whiting, Merlangius merlangus (L.). It is concluded that the principal determinant of the fountain manoeuvre is the visual field of the fish.     

Predator inspection behaviour in three-spined sticklebacks (<Emphasis Type="Italic">Gasterosteus aculeatus</Emphasis>): body size,local predation pressure and cooperation

The apparently maladaptive tendency of fish to approach and inspect potential predators has been explained in terms of useful information gathering or as a signal to the predator that it has been seen. We examined this behaviour in 16 populations of wild-caught stickleback (Gasterosteus aculeatus) from ponds with and without predatory perch (Perca fluviatilis). Three large and three small individuals per population were each exposed to three model predators differing in realism. A final cooperative treatment entailed pairing subjects with a second individual from the same population, but of the alternative size class, during predator presentation. As might be expected, predator inspection behaviour was much greater in the predator-sympatric populations, and only these fish increased their level of inspection as the models became incrementally more realistic. This suggests that reductions occur in the level of costly inspection behaviour in populations without predators. Subject body size had no effect on inspection effort, which suggests a limited role for experience (we assumed larger fish to be older than smaller fish), at least over the relative age differences utilized. However, small predator-sympatric fish were the only subjects to increase inspection significantly when in a cooperative context, perhaps reflecting the inherent value of a relatively larger partner in this context. These results confirm that levels of predator inspection are both population- and situation-dependent, suggesting a trade-off in the potential costs and benefits of this behaviour.Communicated by C. St. Mary