Disentangling the effects of group size and density on shoaling decisions of three-spined sticklebacks (<Emphasis Type="Italic">Gasterosteus aculeatus</Emphasis>)

Many animals live in groups most of their life. One function of this behaviour is an increased predator protection whereas larger groups provide better protection than smaller ones. A causal explanation is that due to a higher number of shoal members the individual risk of being predated will decrease (“dilution effect”). Additionally, shoaling leads to increased predator confusion. This “confusion effect” can be strengthened by an increased group density, which often correlates with group size. Many studies found that individuals prefer the larger of two groups. However, whether this preference is due to a larger group size or because of an increased density of the larger group remained unclear. To disentangle these factors we gave three-spined sticklebacks (Gasterosteus aculeatus) the choice between shoals of (1) different group size and density, (2) different group size, but equal density and (3) equal group sizes, but different densities. As expected, test fish preferred the larger and denser shoal over the smaller, less dense one. This preference was lost when shoal size differed but density was kept constant. When shoal size was equal but density differed, test fish preferred the less dense shoal. However, this was only the case when test fish chose between two relatively dense shoals. On the other hand, when overall density was low, test fish did not discriminate between shoals of different densities. This result may be explained in terms of predator avoidance. The results show that shoaling preferences might not always be influenced by a higher number of group members but also by the density and cohesiveness of the respective groups. An erratum to this article can be found at     

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.     

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.     

Effect of gyrodactylid ectoparasites on host behaviour and social network structure in guppies <Emphasis Type="Italic">Poecilia reticulata</Emphasis>

Understanding how individuals modify their social interactions in response to infectious disease is of central importance for our comprehension of how disease dynamics operate in real-world populations. Whilst a significant amount of theoretical work has modelled disease transmission using network models, we have comparatively little understanding of how infectious disease impacts on the social behaviour of individuals and how these effects scale up to the level of the population. We experimentally manipulated the parasite load of female guppies (Poecilia reticulata) and introduced fish either infected with the ectoparasites Gyrodactylus spp. (experimental) or uninfected (control) into replicated semi-natural populations of eight size-matched female guppies. We quantified the behaviour and social associations of both the introduced fish and the population fish. We found that infected experimental fish spent less time associating with the population fish than the uninfected control fish. Using information on which fish initiated shoal fission (splitting) events, our results demonstrate that the population fish actively avoided infected experimental fish. We also found that the presence of an infected individual resulted in a continued decline in social network clustering up to at least 24 h after the introduction of the infected fish, whereas in the control treatment, the clustering coefficient showed an increase at this time point. These results demonstrate that the presence of a disease has implications for both the social associations of infected individuals and for the social network structure of the population, which we predict will have consequences for infectious disease transmission.     

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.     

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     

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.     

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.     

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     

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.     

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.     

Habitat-specific chemical cues influence association preferences and shoal cohesion in fish

The structure of social animal groups can be dynamic, characterized by high rates of group fission and fusion. Despite this, group composition is often well ordered by factors such as species, body size and by numerous other phenotypic traits. Research in shoaling fishes has revealed that individuals refine group membership decisions still further and are capable of assimilating chemical cues pertaining to recent habitat and prey use by prospective group mates, preferring to associate with others whose recent resource use history closely matches their own. In this study, we firstly examined the dynamics of the formation and breakdown of these preferences, revealing that they can be acquired and replaced in a matter of just a few hours. Using such cues enables individuals to accurately assess the resource use of conspecifics, allowing them to indirectly sample the local environment while reducing the chances of acquiring outdated information that can precipitate maladaptive behaviors. Secondly, we found that shoals composed of individuals with shared recent habitat use history were more cohesive compared to those where the constituent individuals differed in recent habitat use. Increased shoal cohesion may reduce predation risk, and could enhance the ability of individuals to detect and use social information.     

Effects of relaxed predation pressure on visual predator recognition in the guppy

Many prey species have a genetic predisposition to recognise and respond to predators and can fine-tune their anti-predator behaviour following appropriate experience. Although the Trinidadian guppy ( Poecilia reticulata) has become a model species for the investigation of adaptive behaviour, the extent to which experience mediates predator recognition remains unclear. In this study, we examined the effects of relaxed predation pressure on patterns of anti-predator behaviour in populations differing in evolutionary history. The anti-predator behaviour of wild- and laboratory-born guppies from high- and low-predation localities in Trinidad were compared using three models resembling Crenicichla alta, a dangerous guppy predator, Aequidens pulcher, a less dangerous piscivore, and a snake. Snakes are not known to prey on guppies in Trinidad. Specifically, the following predictions were tested: (1) wild caught fish from the high-predation localities (where guppies co-occur with C. alta and A. pulcher) would respond to the three models according to their perceived level of threat, whereas guppies from the low-predation site would show a reduced response to all of the predator models; (2) high-predation laboratory-reared fish would display a reduced but qualitatively similar response to their wild counterparts; and (3) there would be no behavioural differences between wild- and laboratory-reared low-predation fish. In accordance with these predictions, the results revealed that wild fish originating from high-predation sites responded more strongly to the models than fish from low-predation sites. When reared in the laboratory, guppies from the high-predation population showed a reduced response compared to their wild-caught counterparts, but there was no difference in the behaviour of wild- and laboratory-reared low-predation fish. Model type affected predator inspection behaviour but not schooling tendency, and both wild- and laboratory-reared guppies were more wary of the fish models than the snake. These results suggest that early experience differentially mediates the anti-predator responses of fish from high-risk localities.     

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     

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     

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.     

Predation risk reduces male-male sexual competition in the Trinidadian guppy (Poecilia reticulata)

Because agonistic behaviour can increase an individual's risk of predation, natural selection should favour individuals that modify their behaviour in the face of predation hazard in ways that maximise fitness. We investigated experimentally the effects of an increase in the apparent risk of predation on male-male competition within mixed-sex shoals of the Trinidadian guppy (Poecilia reticulata). We show that males engaged in significantly fewer aggressive interactions with conspecific males in the presence of a fish predator. However, they continued to court and attempt copulations with females at the same rate irrespective of the level of predation risk. In comparison, under predation hazard, female guppies were less responsive sexually and avoided fewer male copulation attempts. Such predator-mediated changes in male-male agonistic interactions and female sexual responsiveness towards males have important implications for the mode and intensity of sexual selection within populations.     

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.     

Settlement patterns and presettlement behavior of the naked goby,Gobiosoma bosci,a temperate oyster reef fish

Dispersion, distribution, development and feeding incidence of larvae of the naked goby,Gobiosoma bosci (Lacepéde), were examined for linkages between larval behavior while near the reef surface and later patterns of settlement and recruitment. Field sampling and experiments were conducted during the summers of 1988 and 1989 in the Flag Pond oyster reef along the western shore of the Chesapeake Bay near Camp Conoy, Maryland, USA. Results indicated that prior to settlement most demersal larvae aggregate in shoals and exhibit distinct microhabitat preferences on the reef. In a field experiment, larvae settled both during the day and at night. Dispersion at settlement was aggregated, suggesting that demersal shoaling influences settlement patterns in this species. The distribution of demersal larvae also indicated that larval swimming behavior is sufficiently strong to permit active control of position on reefs. Large demersal larvae settled rapidly when brought to the laboratory, but small larvae in demersal shoals appeared to require additional growth and morphological development prior to settlement. Development of the pelvic fins, used by juveniles and adults for perching on the substrate, may be a good indicator of competence to settle in this species. The adaptive significance of demersal shoaling by small larvae of the naked goby, and the fate of these larvae, remains perplexing because the low feeding rates found for larvae shoaling near the reef surface should slow or prevent the growth and development required prior to settlement. Observations made by other authors indicate that demersal shoaling and the use of water directly overlying reefs may be common behaviors of temperate and tropical reef fishes.