The social organization of free-ranging fish shoals

The phenotypic composition of social groups can affect the foraging efficiency and predation risk of their individual members. In shoaling fishes, active choice of shoal companions on the basis of phenotypic characters such as body length has been reported. In this study, we investigated the phenotypic composition of free-ranging, multi-species fish shoals in a temperate freshwater lake. We collected 21 entire shoals, each consisting of up to four species and comprising 3622 fish in total. Shoals were strongly assorted by species, body length, parasite prevalence and parasite load. Using a mark-recapture procedure involving 785 banded killifish ( Fundulus diaphanus ), we found no evidence for shoal fidelity or site fidelity, as individuals from different shoals mixed extensively after just 24 h and ranged all over the study site irrespective of initial capture locations. Killifish showed strong changes in shoal-size choice over 24 h, and no evidence was found that shoals might break up into sub-units of individuals that are more phenotypically assorted than their original shoals. The mechanisms by which assortative groups may arise and the consequences of low group fidelity for the evolution of cooperative behaviour are discussed.     

Shoal choice and ultraviolet reflections in stickleback populations from different photic habitats

Grouping is a widespread phenomenon in the animal kingdom and the decision to join a group is a function of individual and environmental conditions, meaning that any advantages and disadvantages have to be pondered constantly. Shoaling decisions in fishes are communicated via a variety of factors, such as colour signals, amongst other ultraviolet (UV) signals. The sensitivity for ultraviolet signals is assumed to be costly and a function of the predominant ecological conditions. The island of North Uist, Scotland, comprises bodies of water that possess great variation in their spectral distribution, especially in the UV spectral range. We examined different populations of three‐spined stickleback (Gasterosteus aculeatus L.), which is known to use UV for visual tasks, consisting of three populations from tea‐stained lakes and four from clear‐water lakes, concerning their preferences to join a shoal viewed under UV‐present and UV‐absent conditions. Nonreproductively active sticklebacks from tea‐stained lakes significantly preferred the shoal under UV‐absent conditions, whereas sticklebacks from clear‐water lakes did not show a significant preference. Reflection measurements showed that the UV chroma (intensity) of sticklebacks from tea‐stained lakes was higher than that of sticklebacks from clear‐water, most likely contrasting maximally against the UV‐poor background or compensating for a stronger attenuation of the signal.     

Cross-species familiarity in shoaling fishes

Preferential association with familiar shoal mates confers a number of potentially important benefits to individuals, including improved anti-predator effects and the reduction of aggression in competitive interactions. Until now, however, familiarity has been demonstrated purely between conspecifics. Here, we present evidence that familiarity preferences can override natural preferences for conspecifics. Individual focal fishes (chub, Leuciscus cephalus) were given a choice of two stimulus shoals of the same size composed of conspecifics or of heterospecifics (minnows, Phoxinus phoxinus) in a flow tank. A series of four treatments was carried out to investigate the effects of familiarity, induced by a 15 day association between the focal fish and the stimulus fishes, on the choices made by the focal fish. Focal fishes showed a significant preference for conspecifics over heterospecifics when both stimulus shoals were composed of non-familiar individuals. Focal fishes also showed a significant preference for stimulus shoals composed of familiar fishes over stimulus shoals composed of non-familiar fishes when both shoals were conspecific and when both shoals were heterospecific. Finally, the preference of focal fishes for conspecifics disappeared when the alternative, a shoal of heterospecifics, was composed of familiar individuals. The importance of this work is discussed in the context of species interactions in free-ranging shoals.     

Familiarity affects social network structure and discovery of prey patch locations in foraging stickleback shoals

Numerous factors affect the fine-scale social structure of animal groups, but it is unclear how important such factors are in determining how individuals encounter resources. Familiarity affects shoal choice and structure in many social fishes. Here, we show that familiarity between shoal members of sticklebacks (Gasterosteus aculeatus) affects both fine-scale social organization and the discovery of resources. Social network analysis revealed that sticklebacks remained closer to familiar than to unfamiliar individuals within the same shoal. Network-based diffusion analysis revealed that there was a strong untransmitted social effect on patch discovery, with individuals tending to discover a task sooner if a familiar individual from their group had previously done so than if an unfamiliar fish had done so. However, in contrast to the effect of familiarity, the frequency with which individuals had previously associated with one another had no effect upon the likelihood of prey patch discovery. This may have been due to the influence of fish on one another''s movements; the effect of familiarity on discovery of an empty ‘control’ patch was as strong as for discovery of an actual prey patch. Our results demonstrate that factors affecting fine-scale social interactions can also influence how individuals encounter and exploit resources.     

Parasitism, oddity and the mechanism of shoal choice

When choosing between shoals differing in Schistocephalus solidus infection status, uninfected test sticklebacks Gasterosteus aculeatus showed a preference for joining uninfected conspecifics when shoal sizes were equal, but reversed this preference when the relative size of the infected shoal was increased by a factor of 3. When given a choice between a shoal composed of size-matched minnows Phoxinus phoxinus and a shoal composed of the same number of all uninfected or all S. solidus -infected sticklebacks, test fish always preferred the sticklebacks, regardless of their infection status, over the minnow shoal. These observations suggest that species, parasite status and shoal size are all of importance when fish decide which shoal to join.     

Group Choice as a Function of Group Size Differences and Assessment Time in Fish: The Influence of Species Vulnerability to Predation

The shoal-choice behaviour of two species of fish that differ in their vulnerability to predation was compared. Individuals of threespine stickleback, Gasterosteus aculeatus, and creek chub, Semotilus atromaculatus, were presented with a simultaneous choice of two equidistant stimulus shoals of conspecifics that differed in membership size (5 vs. 6 fish, 5 vs. 7, 5 vs. 8, 5 vs. 9 and 5 vs. 10). Test fish were allowed to view the stimulus shoals from a standard distance for either 10–20 or 120–150s before being frightened with a stimulus from an overhead light and released to join either shoal. We observed which shoal (the smaller or the larger one) the test fish approached. Preference for the larger stimulus shoal generally increased with increasing shoal size difference and with the duration of the assessment period, and was more pronounced in chub (the more vulnerable of the two species). For the short assessment period, chub showed a significantly stronger preference for the larger stimulus shoal than sticklebacks, whereas there was no significant difference between species for the long assessment period. Furthermore, chub responded more readily to small differences in shoal size (of 1–3 fish) than sticklebacks, for both short and long assessment periods. The above results are consistent with the hypothesis that chub, as the more vulnerable of the two species (in terms of predation), should be able to identify the larger of two shoals more quickly and should be more sensitive to small differences in shoal size than sticklebacks.     

Shoal and prey patch choice by co-occurring fishes and prawns: inter-taxa use of socially transmitted cues

Animals can use socially transmitted information to learn about the distribution and quality of resources without incurring the costs associated with having to search for and sample them first hand. Recently, it has been shown that the use of chemical social information specific to patterns of diet and habitat use is an important mechanism underpinning recognition and social organization in shoaling fishes. In this study we revealed that the use of resource-specific chemical information is not limited to conspecifics, or even members of the same taxon. In a series of laboratory experiments, we showed that threespine sticklebacks (Gasterosteus aculeatus) could recognize similar patterns of habitat use in common prawns (Leander serratus), preferentially orientating towards groups of prawns exposed to the same habitats as themselves, and even selecting foraging patches located close to them. Prawns were seen to use habitat-specific cues generated by conspecifics, but not by sticklebacks, suggesting that the benefits of forming these heterospecific social association patterns may be unequal for prawns and fishes. Our findings suggest that some species might use co-occurring, unrelated species as information centres in order to orient and locate resources within their surroundings.     

Shoaling behaviour of sticklebacks infected with the microsporidian parasite, <Emphasis Type="Italic">Glugea anomala</Emphasis>

We compared the shoaling behaviour of three-spined sticklebacks, Gasterosteus aculeatus, infected with the microsporidian, Glugea anomala, to that of non-infected conspecifics. Infected fish lost significantly more weight than non-infected fish during a period of food deprivation, suggesting a metabolic cost to parasitism. In binary shoal choice tests, non-infected test fish showed an association preference for a shoal of non-infected over a shoal of infected conspecifics; infected test fish displayed no preference. Infected fish, however, showed a higher overall tendency to shoal than non-parasitised fish. Furthermore, infected fish occupied front positions within a mixed school. We consider the behavioural differences between infected and uninfected fish in the context of their potential benefits to the fish hosts and the parasites.     

Environmental habituation and sexual composition affect juveniles' shoaling activity in a cichlid fish (Pelvicachromis taeniatus)

Group living is widespread in animals, and many fishes form shoals. Examining within-group interactions in fishes may contribute to the general understanding of dynamic social structures in animals. The sex ratio of a group has been shown to influence grouping decisions of fishes and can be expected to affect behaviour at group level. Behavioural experiments usually involve relatively short acclimatisation times, although the establishment of environmental habituation in fishes is understudied. This study tests whether the sex ratio and long-term habituation to experimental conditions influence general shoal performance (activity parameters, density) and responses of shoals to an acoustic-mechanical disturbance cue in juveniles of the cichlid fish Pelvicachromis taeniatus via individual tracking. The disturbance consisted of a defined hit against the experimental tank, which caused sudden noise and water movement. We found that a higher proportion of females increases shoal activity (swimming speed and distance covered), suggesting that female P. taeniatus are more active than males. Furthermore, shoal activity declined when shoals habituated to the experimental settings and with the time that the shoals were grouped together, which may reflect intensified group member familiarity. Moreover, behavioural changes after disturbance were weaker when individuals were kept with their group longer and more familiar to the experimental conditions. For prey species, lower activity might be beneficial under natural conditions due to lower conspicuousness of the group. We did not find any significant effects of the investigated factors on shoal density (mean interindividual distance) and speed synchronisation. The results indicate that sexual composition, familiarity between shoal members and habituation to the experimental environment affect shoal performance in a cichlid fish.     

No sibling odor preference in juvenile three-spined sticklebacks

Laboratory-bred juvenile three-spined sticklebacks from 11 sibshipsdid not prefer to shoal with their siblings when they were offeredthe choice between odor from unfamiliar siblings and non-kinin a fluviarium, although the power for finding a significantpreference was very high (0.99). The test fish preferred theside where odor from the heavier shoal was supplied; this shows thatthey could appreciate odor cues from conspecifics in our apparatusand should have preferred their siblings if such a preferenceexists. Our results are compatible with theoretical predictionsbut are at variance with previous findings by other authors.We used independent replicates in a blind protocol with strictrandomization of fish and procedures.     

Asymmetric introgression between fishes in the Red River basin of Texas is associated with variation in water quality

When ecologically divergent taxa encounter one another, hybrid zones can form when reproductive isolation is incomplete. The location of such hybrid zones can be influenced by environmental variables, and an ecological context can provide unique insights into the mechanisms by which species diverge and are maintained. Two ecologically differentiated species of small benthic fishes, the endemic and imperiled prairie chub, Macrhybopsis australis, and the shoal chub, Macrhybopsis hyostoma, are locally sympatric within the upper Red River Basin of Texas. We integrated population genomic data and environmental data to investigate species divergence and the maintenance of species boundaries in these two species. We found evidence of advanced‐generation asymmetric hybridization and introgression, with shoal chub alleles introgressing more frequently into prairie chubs than the reciprocal. Using a Bayesian Genomic Cline framework, patterns of genomic introgression were revealed to be quite heterogeneous, yet shoal chub alleles were found to have likely selectively introgressed across species boundaries significantly more often than prairie chub alleles, potentially explaining some of the observed asymmetry in hybridization. These patterns were remarkably consistent across two sampled geographic regions of hybridization. Several environmental variables were found to significantly predict individual admixture, suggesting ecological isolation might maintain species boundaries.     

Kin discrimination in sticklebacks is mediated by social learning rather than innate recognition

Theory predicts several advantages for animals to recognize kin. These include inbreeding avoidance and an increase in inclusive fitness. In shoaling species, kin recognition may lead to an increased amount of altruism among shoal members. Adult, non‐reproductive three‐spined sticklebacks, Gasterosteus aculeatus, prefer to shoal with kin. This preference was shown for familiar as well as for unfamiliar individuals. However, whether it is based on learned cues of familiar individuals or on innate mechanisms like self‐referent phenotype matching or ‘true’ kin recognition through recognition alleles remains unknown. In our experiments, juvenile fish were given the choice between shoals that differed in relatedness and familiarity. The number of testfish who joined each group indicated that sticklebacks prefer to shoal with familiar kin when the alternative shoal was composed of unfamiliar non‐kin. When one shoal consisted of familiar kin while the second consisted of familiar non‐kin testfish did not show any preference. Kin recognition in sticklebacks is thus most likely mediated by social learning.     

Shoaling Decisions in Angelfish: The Roles of Social Status and Familiarity

Abstract Past research has shown that angelfish, Pterophyllum scalare , are capable of discriminating between shoals composed of familiar dominant and subordinate companions, whereas they show no preference for shoals of unfamiliar conspecifics. In this study, the relative importance of familiarity and social status (shoal factors) on the shoaling decision of juvenile angelfish, which also differed in social status (individual factor), was investigated as very little is known about such tradeoffs in fishes. Dominant and subordinate individuals were given the choice to shoal with a group of conspecifics composed of familiar dominants vs. unfamiliar dominants and composed of familiar subordinates vs. unfamiliar subordinates. The findings demonstrate that fish with different social status differed in their shoaling preference. Subordinate test fish showed a preferential association with familiar subordinates over unfamiliar subordinates, but preferred the unfamiliar shoal over the familiar one when both shoals were constituted by dominant individuals. The shoaling behaviour shown by dominant test fish, on the other hand, indicated no significant preference for any of the shoals regardless of their composition. A replicate preference test carried out 2 h 30 min after the first one indicated that the association pattern was relatively consistent. Results suggest that angelfish are able to differentiate between the stimulus shoals and demonstrate that the pervasive influence of familiarity on the shoaling decision may be restrained or overridden by the composition of the familiar shoals and the social status of the test fish.     

UV matters in shoaling decisions

Shoaling behaviour in fish is influenced by numerous factors, such as familiarity, kinship, group size and shoal composition. Grouping decisions are based on both olfactory and visual cues. The visual system of many vertebrates is extended into the ultraviolet (UV) wave range as in three-spined sticklebacks (Gasterosteus aculeatus, L.). We investigated whether the presence or absence of UV wavelengths has an influence on shoaling behaviour in this species. Reproductively non-active three-spined sticklebacks were given the choice between two shoals, equal in numbers of individuals, which could be seen either through a UV-transmitting [UV(+)] or a UV-blocking [UV(-)] filter. Test fish preferred to join the shoal seen under UV(+) conditions. Due to differences in quantal flux between the UV(+) and UV(-) filters used, control experiments with neutral-density optical filters were performed in order to clarify the role of luminance. Here, test fish spent significantly more time near shoals that were seen in a darker environment, suggesting a potential trade-off between UV radiation and lower brightness during shoal choice.To our knowledge, these results demonstrate for the first time that shoaling decisions are influenced by UV wavelengths.     

Nutritional state influences shoaling preference for familiars

Preferences for grouping with familiar individuals are shown in many animal species, including the three-spined stickleback (Gasterosteus aculeatus). Shoaling with familiars is advantageous because of more precise anti-predator behaviours or more stable dominance hierarchies. Additionally, associations with familiar individuals facilitate the evolution of altruistic behaviour. Thus, in situations of increased competition one might expect an increased preference for familiar fish. We gave single juvenile sticklebacks of different nutritional state the choice between shoals composed either of familiar or unfamiliar individuals. Satiated fish preferred to shoal with familiar individuals. A comparative analysis of 8 stickleback studies with 15 different tests using familiars showed that all tests gave similar results, i.e. sticklebacks of all age classes preferred to shoal with familiars in a non-sexual context. In contrast, hungry test fish did not prefer to shoal with familiar fish, but even showed a preference for the unfamiliar group. Because sticklebacks use early-life familiarity to recognize kin, the results suggest the avoidance of competition with relatives. To our knowledge, this is the first study showing an impact of nutritional state on social interactions with familiar individuals.     

Parasitism and Shoal Size in Juvenile Sticklebacks: Conflicting Selection Pressures from Different Ectoparasites?

In gregarious animals, group size correlates negatively with infection levels by some kinds of parasites and positively with infection by others. Conflicting selection pressures can be exerted simultaneously on a host species by different parasite species. Among stationary, mixed-species shoals of juvenile threespine sticklebacks, Gasterosteus aculeatus , and blackspotted sticklebacks, Gasterosteus wheatlandi , shoal size correlated differently with levels of infection by two species of ectoparasites. Stickleback shoal size correlated positively with infection levels by the copepod Thersitina gasterostei , which is transmitted among fish by short-lived planktonic larvae. In contrast, infection levels by the highly mobile crustacean parasite Argulus funduli did not decrease as shoal size increased, as predicted from an earlier laboratory experiment. The species composition of the different stickleback shoals also had an influence on some aspects of infection by these two parasite species. The contrasting mode of transmission of the two parasites results in one parasite species having a higher transmission rate among fish within large shoals, whereas the success of the other parasite species is independent of fish shoal size. The two ectoparasites may thus exert different selection pressures on stickleback shoal sizes.     

The effect of hunger and cestode parasitism on the shoaling decisions of small freshwater fish

Individual minnows Phoxinus phoxinus and three-spined sticklebacks Gasterosteus aculeatus were provided with a mutually exclusive choice between joining a shoal of conspecifics and foraging alone in a maze. The shoaling decisions and foraging behaviour of individual fish were studied when the fish were satiated and after 24- and 48-h periods of food deprivation. Hunger level was found to have a significant effect on shoaling behaviour. When satiated, fish of both species spent a greater proportion of time within one body length of the shoal and spent less time out of visual contact with the shoal than after periods of food deprivation. The effect of the cestode parasite Schistocephalus solidus on the shoaling behaviour of stickleback hosts was complex. When satiated, infected fish spent less time than uninfected fish within one body length of the shoal, preferring to remain outside the shoal, yet within visual contact, although when food deprived there was no difference in the proportion of time spent by infected and uninfected fish close to the shoal. The possible ecological significance of this change in behaviour is discussed with reference to the manipulation hypothesis of host-parasite interactions.     

Fathead minnows avoid conspedfic and heterospedfic alarm pheromones in the faeces of northern pike

Groups of fathead minnows Pimephales promelas were tested to determine if they avoided areas of a test tank labelled with the faeces of a predator (northern pike, Esox lucius ) which had recently been fed minnows, brook sticklebacks Culaea inconstans , or swordtails Xiphophorus helleri. Minnows exhibited a fright reaction upon presentation of sponges labelled with faeces, when the pike had consumed minnows or sticklebacks, but not swordtails (which lack alarm pheromones). The fright reaction was characterized by increased shoal cohesiveness and increased dashing and freezing behaviour. Minnows avoided the area of the tank containing the faeces from pike on diets of minnows or sticklebacks, but not from pike fed a diet of swordtails. These data demonstrate that: (1) minnows actively avoid the faeces of pike fed minnows or brook sticklebacks, and (2) minnows exhibit a fright reaction to the faeces of a pike fed brook sticklebacks.     

Influence of lighting environment on social preferences in sticklebacks from two different photic habitats. II. Shoaling and mate preferences of lab-bred fishes

Different environmental conditions may lead to diverse morphological, behavioral, and physiological adaptations of different populations of the same species. Lighting conditions, for example, vary vastly especially between aquatic habitats, and have been shown to elicit adaptations. The availability of short-wave ultraviolet (UV) light is especially fluctuating, as UV wavelengths are attenuated strongly depending on water properties. The island of North Uist, Scotland, comprises 2 differential habitat types, tea-stained and clear-water lakes, varying considerably in UV transmission. In previous studies, wild-caught 3-spined stickleback Gasterosteus aculeatus populations (3 populations of each habitat type) were tested with respect to their shoaling and mate preferences for fish viewed under UV-present and UV-absent conditions. The results revealed a habitat-dependent preference of UV cues during shoal choice (tea-stained populations: preference for UV-absent condition in tea-stained water; clear-water populations: no preference in clear-water) but an overall preference for UV-present conditions during mate choice. To assess genetic influences on these behavioral patterns, similar experiments were conducted with lab-bred F1-generations of the same stickleback populations that were raised in a common environment (i.e. standardized clear-water conditions). Offspring of sticklebacks from tea-stained lakes tended to prefer shoals viewed under UV-absent conditions (only in tea-stained water), while sticklebacks from clear-water lakes showed a significant preference for the shoal viewed under UV-present conditions in clear-water but not in tea-stained water. Mate-preference experiments demonstrated that females from the tea-stained lakes significantly preferred and females from the clear-water lakes preferred by trend the male viewed under UV-present conditions in the clear-water treatment. The results for both shoaling- and mate-preference tests were largely similar for wild-caught and lab-bred sticklebacks, thus hinting at a genetic basis for the preference patterns.