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.     

Fish shoal composition: mechanisms and constraints

Observations were made on three fish species (banded killifish (Fundulus diaphanus), golden shiner (Notemigonus crysoleucas) and white sucker (Catostomus commersoni)) in a temperate lake (New Brunswick, Canada) in order to investigate the relationship between shoal choice behaviour of individual fishes and shoal composition. Encounters between shoals were observed to take place every 1.1 min per shoal and an encounter lasted 3.7 s on average. The duration of shoal encounters was influenced by shoal size but not by differences between shoals in either body length or species. Conversely, the outcome of shoal encounters (i.e. ences between shoals in either body length or species. Conversely, the outcome of shoal encounters (i.e. whether or not an individual changes shoal) was influenced by body length and species differences but not by shoal size. Together, these results suggest that encounter duration itself is unlikely to have an important influence on encounter outcome. The collection of ten entire fish shoals showed that they were assorted by species and body length. A simulation model demonstrated that individual shoal choice behaviour alone could account for the generation and maintenance of the observed levels of size assortedness of shoals without invoking the existence of other sorting mechanisms such as differential swimming speeds. However, the generation of species assortedness was not predicted by the model. Furthermore, our data suggest that fish density acts as a constraint on shoal choice, influencing both shoal size and composition. This work has implications for studies on information transfer and reciprocal altruism within populations.     

Body length variation within multi-species fish shoals: the effects of shoal size and number of species

Theory predicts that selection should favour phenotypic homogeneity in fish shoals, and field studies have indeed confirmed that variation in body length within fish shoals is significantly lower than expected from a random distribution of fish among shoals. We investigated the extent to which variation in fish body length within shoals is determined by the shoal mean of body length, the number of species in a shoal, and the overall shoal size. We collected 34 fish shoals, ranging in size from 6 to 776 individuals, from the littoral zone of a Canadian lake. Shoals consisted of up to four different species, with multi-species shoals being larger and more frequent than single-species ones. The strongest determinant of body length variation within shoals was the shoal mean of body length, followed by the number of fish species in a shoal; i.e. multi-species shoals were less size-assorted than single-species ones. A more detailed analysis showed that the higher body length variation observed in multi-species shoals was due to increased body length variation both within and between component species. Shoal size had no significant effect on body length variation within shoals. Potential explanations of the positive relationship between body length variation and the number of species in a shoal are suggested. The implications of the above results for the evolution of multi-species shoals are discussed. Received: 6 May 1997 / Accepted: 14 October 1997     

Juvenile convict cichlids shoaling decisions in relation to shoal size and age

Many animals form groups and socialize in response to evolutionary pressures such as predation, food availability, and mate acquisition. Evidence of social choice based on various phenotypic characters (Group Phenotypic Composition [GPC]) has been observed in several animal species. In addition to the physical characteristics of the social group, it is also interesting to consider how decisions of who to socialize with might be expected to change for an individual over time. Younger individuals with limited life experience may discriminate differently between social groups than older conspecifics who have had the opportunity to learn and who may be faced with different ecological or environmental pressures. Here, we used a traditional two‐choice design to explore the shoaling behavior of juvenile convict cichlids and determine whether the number of fish and/or the size/life stage of the individuals within a shoal influenced social choices. We found that juvenile convict cichlids spent more time shoaling with similarly sized juvenile individuals and also preferred to shoal with larger shoals, but not when shoals were comprised of adult fish. The size of the individuals in a shoal was a more influential factor than the size of the shoal itself. Size of individual juveniles was correlated with tendency to visit shoals, but was not correlated with overall time spent shoaling, regardless of shoal composition. As juveniles, convict cichlids can make discriminatory choices that are influenced by specific aspects of shoal composition.     

Mechanisms underlying shoal composition in the Trinidadian guppy, Poecilia reticulata

Free-ranging groups are frequently assorted by phenotypic characters. However, very little is known about the underlying processes that determine this structuring. In this study, we investigate the mechanisms underlying the phenotypic composition of shoals of guppies ( Poecilia reticulata ) in a high-predation stream in Trinidad's Northern Mountain Range. We collected 57 entire wild shoals, which were strongly assorted by body length. Shoal encounters staged within an experimental arena showed shoal fission (but not fusion) events to be an important mechanism in generating phenotypic assortment. In the wild, fission and fusion between guppy shoals occurred extremely frequently and thus are unlikely to constrain the opportunities for shoal assortment. However, fission and fusion processes occur under the restrictions imposed by the distribution of individuals within the environment. We observed size specific segregation within the habitat in three dimensions, providing a passive mechanism that contributes to the maintenance of the observed homogeneity of group composition. Furthermore sex differences were found in social behaviour. Individual male guppies switched between shoals more frequently than females and left a shoal more often than females. We argue that shoal composition is determined by habitat segregation on a medium spatial scale and by fission/fusion processes on a small spatial scale (with sex-specific shoal dynamics adding a additional layer of complexity).     

Shoal Choice in the Banded Killifish (Fundulus diaphanus,Teleostei, Cyprinodontidae): Effects of Predation Risk,Fish Size,Species Composition and Size of Shoals

Banded killifish (Fundulus diaphanus) were presented individually with a choice of shoaling with either of two stimulus shoals which differed in shoal size, species composition, and fish body size, before and after a simulated avian predator attack. When threatened, test fish preferred to shoal with the larger of two conspecific shoals, but only if members of both stimulus shoals were of the same size class as the test fish. Otherwise, they preferred to shoal with similarly sized fish irrespective of shoal size; threat of predation increased the magnitude of this preference. Furthermore, test fish preferred a shoal of similarly sized shiners (Notemigonus crysoleucas) over larger killifish, when shoal sizes were identical. This indicates that body size plays a key role in shoal choice, overriding the effects of shoal size and species preference. Notwithstanding the above, shoal choice was affected by predator threat only when differences between shoal size or body size of stimulus fish were large.     

Shoaling in juvenile guppies: the effects of body size and shoal size

While factors affecting shoal mate choice have been examined extensively in adult guppies (Poecilia reticulata), few studies have focused on the shoaling behavior of juveniles. In this study, juvenile guppies were tested for their ability to shoal as well as their response to shoal mates of different body size and to shoals with different numbers of individuals. In dichotomous choice tests, 10-day-old guppies (mean body length=8.83 mm), 30-day-old guppies (13.17 mm) and 50-day-old guppies (18.6mm) were given the opportunity to swim near shoals of five fish or an empty chamber. In most cases, the juvenile fish demonstrated shoaling behavior, swimming near a group of fish rather than an empty chamber, regardless of the age of the stimulus shoal. When presented with two shoals, one of similar age and body size and one of dissimilar age and body size, only the 50-day-old guppies showed a significant preference for the age-matched shoal. Similarly, when choosing between a large shoal and a small shoal, only the 50-day-old guppies spent significantly more time near the larger shoal. Thus, while juveniles at each age shoaled, only 50-day-old fish demonstrated the shoal mate discrimination seen in adult fish.     

The effect of shoal size on patterns of body colour segregation in mollies

Individual white and black mollies Poecilia latipinna spent significantly more time near the larger group when given the choice between two shoals of similar colouration to themselves. When given the choice between a large and a small shoal of dissimilar colouration to themselves, black test fish spent significantly more time with the larger shoal while white test fish showed no preference for either group. Both white and black mollies chose the smaller of two shoals when given the choice between a large dissimilarly coloured shoal and a small similarly coloured shoal. The results indicate that mollies actively discriminate between shoals on the basis of both body colour and shoal size. However, body colour segregation appears to have a stronger influence on shoal choice.     

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.     

The Effect of Hunger on Shoal Choice in Golden Shiners (Pisces: Cyprinidae,Notemigonus crysoleucas)

When an animal has a choice of joining one group over another, its decision may depend on its relative vulnerabilities to predation and starvation. For example, a well-fed animal may choose a large group of individuals with body size matching its own because this gives good protection against predators, but a hungry animal may prefer smaller groups made up of smaller individuals because this decreases food competition. To test this idea, a choice between various shoals was given to golden shiners, Notemigonus crysoleucas, that were either well fed or deprived of food for 48 h. In a choice of 10 vs. 3 shoalmates, both well-fed and hungry shiners spent more time near the shoal of 10. In a choice of 20 vs. 3 shoalmates, both well-fed and hungry shiners again preferred the larger shoal, but in one replicate this preference was significantly weaker in the hungry fish. This reduced preference did not appear to be an artefact of increased mobility by hungry fish searching for food. In a choice between shoals of small vs. large conspecifics, small well-fed shiners, small hungry shiners, and large well-fed shiners preferred shoalmates with body size matching their own, but large hungry shiners preferred smaller individuals. These results are consistent with the hypothesis that hungry fish sacrifice safety from predation in their shoaling behaviour (by avoiding larger groups to a certain extent and by risking the oddity effect) so as to decrease food competition.     

Effects of fasting on collective movement and fission–fusion dynamics in both homogeneous and heterogeneous shoals of a group-living cyprinid fish species

The present study aimed to reveal the effect of fasting (21 days) on collective movement and interaction dynamics in both homogeneous (eight members fed a commercial diet or deprived of food) and heterogeneous (four fed + four starved members) shoals of juvenile qingbo (Spinibarbus sinensis). The authors of this study measured the shoaling behaviour in both a commonly used rectangular open arena with no spatial complexity and a radial arm maze. When measured in the open arena, the starved shoals had a faster swimming speed and acceleration rate and a longer interindividual distance than the fed shoals, possibly because of the elevated foraging motivation. Nonetheless, the values of the heterogeneous groups were similar to those of the fed groups. Furthermore, in contrast to the fish in homogeneous shoals, the starved fish in heterogeneous shoals showed a slower acceleration rate and speed than fed members in heterogeneous shoals. These results, combined with the relationships of variables at the among- and within-shoal levels, suggested that starved fish limited their motion in heterogeneous shoals to maintain group cohesion but that the fed fish contributed more to maintaining shoal structure, possibly because of the higher energy expenditure required for movement changes. When monitored in a radial arm maze, starved shoals showed more fission–fusion episodes without sacrificing group cohesion, as they adaptively adjusted the frequency and duration of each majority choice. The among-shoal variation revealed that the heterogeneous groups showed less variation in the open arena but more variation in the radius maze than did the homogeneous groups. This difference might arise because dominant members have opposite effects on shoal behaviour and consensus decisions. In conclusion, the present study showed opposite effects of feeding states on collective behaviour between homogeneous and heterogeneous shoals, possibly because of the complicated interactions among members with different energy storage levels and foraging motivations. Furthermore, the heterogeneous groups showed a difference between shoal behaviour in the open area and exploration in the radial arm maze. Future studies manipulating the personality composition of starved and fed members of heterogeneous groups might yield interesting results.     

Effects of nutritional state on the shoaling tendency of banded killifish, Fundulus diaphanus, in the field

Although group living can confer benefits to individuals in terms of reduced predation risk and enhanced foraging success, it may also be associated with costs, such as increased competition for food. The nutritional state of an individual could therefore affect its readiness to join or remain in groups. We investigated the shoaling behaviour of banded killifish by following marked individuals, whose nutritional state had been experimentally manipulated, and recording their shoaling behaviour in a field enclosure containing unmarked conspecifics. Overall, food-deprived fish spent more time alone, and therefore less time shoaling, than well-fed individuals. When shoaling, however, food-deprived fish were not found in smaller shoals than well-fed conspecifics. Furthermore, they did not show a greater latency to shoal initially. Having joined a shoal, however, food-deprived fish left shoals more frequently to be alone than fed fish. Rates of change in the membership size of shoals occupied by either well-fed or food-deprived fish did not differ. We conclude that nutritional state seems to affect an individual's decision to continue shoaling once an association has been made. This study is the first to investigate experimentally state-dependent changes in the size of social groups in fish under field conditions. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

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.     

The Influence of Food Competition and Prédation Risk on Size-assortative Shoaling in Juvenile Chub (Leuciscus cephalus)

Size-assortative shoaling is a widespread phenomenon potentially linked to competition for resources among shoal members and anti-predator benefits gained from living in shoals. This paper investigates the influence of both factors on size-assortative shoaling in chub (Leuciscus cephalus). In a first experiment food competition was studied by manipulating the proportions of small and large chub in shoals of 20 fish. Large fish were generally more competitive than small ones. However, the competitive effect of large fish was strongly dependent on their number in the shoal. This has important consequences for the theory of competition because it makes it difficult to predict stable combinations of different phenotypes when foragers divide between food patches. Despite the strong effects of food competition no significant trend for size-assortativeness was observed in free-swimming shoals when undisturbed. This changed after the shoal had been frightened by introducing Schreckstoff (an alarm substance) to the test tank. Large and small fish still remained in the same shoal but showed a strong preference to be close to neighbours of their own size class. Large fish were observed mainly in the centre of the shoal and small fish were found more in the periphery. It is unclear whether these position differences are due to aggressive behaviour of large fish towards small fish which excludes them from the potentially safe centre of the shoal. These results indicate that prédation plays a more important role than food competition for size-assortative shoaling in chub.     

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.     

The effect of sex and shoal size on shoaling behaviour in Danio rerio

Male and female zebra fish Danio rerio were given choices of shoals that differed in sex and size. Male zebra fish preferred to associate with female shoals over male shoals, but had no preference when given a choice between a mixed‐sex shoal and either a male or female shoal. Female zebra fish showed no significant preference when given a choice between male and females shoals, nor between mixed‐sex shoals and either male or female shoals. When given choices between shoals of differing size, females preferred to associate with the larger shoal, whether or not they were composed of males or females. Males, however, had no preference for larger shoals over smaller shoals, whether or not they were composed of males or females. These results showed that male zebra fish were capable of distinguishing between males and females solely on the basis of visual cues. Furthermore, these results demonstrated a significant difference between the shoaling choices of male and female zebra fish, which may indicate a difference in the function of shoaling for the two sexes.     

Balancing the dilution and oddity effects: decisions depend on body size

Background

Grouping behaviour, common across the animal kingdom, is known to reduce an individual''s risk of predation; particularly through dilution of individual risk and predator confusion (predator inability to single out an individual for attack). Theory predicts greater risk of predation to individuals more conspicuous to predators by difference in appearance from the group (the ‘oddity’ effect). Thus, animals should choose group mates close in appearance to themselves (eg. similar size), whilst also choosing a large group.

Methodology and Principal Findings

We used the Trinidadian guppy (Poecilia reticulata), a well known model species of group-living freshwater fish, in a series of binary choice trials investigating the outcome of conflict between preferences for large and phenotypically matched groups along a predation risk gradient. We found body-size dependent differences in the resultant social decisions. Large fish preferred shoaling with size-matched individuals, while small fish demonstrated no preference. There was a trend towards reduced preferences for the matched shoal under increased predation risk. Small fish were more active than large fish, moving between shoals more frequently. Activity levels increased as predation risk decreased. We found no effect of unmatched shoal size on preferences or activity.

Conclusions and Significance

Our results suggest that predation risk and individual body size act together to influence shoaling decisions. Oddity was more important for large than small fish, reducing in importance at higher predation risks. Dilution was potentially of limited importance at these shoal sizes. Activity levels may relate to how much sampling of each shoal was needed by the test fish during decision making. Predation pressure may select for better decision makers to survive to larger size, or that older, larger fish have learned to make shoaling decisions more efficiently, and this, combined with their size relative to shoal-mates, and attractiveness as prey items influences shoaling decisions.     

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.     

Kin assortment in juvenile shoals in wild guppy populations

Grouping provides many potential benefits to individuals in terms of foraging and anti-predator protection. However, it has been suggested that individuals could gain additional benefits in terms of indirect fitness by grouping with kin. Surprisingly, the genetic composition of wild fish shoals and the importance of kin-associated shoaling remain poorly understood. The Trinidadian guppy (Poecilia reticulata) has life history traits that might promote kin structure of shoals such as internal fertilisation and small brood size in contrast to many other fish species. Even though previous studies did not find any indication of kin structure in shoals of adult guppies, it is possible that related juveniles remain together in shoals, partly because of lower mobility and because the advantages of kin association may change with age. Using 10 microsatellite markers, we conducted a genetic analysis on 40 shoals from four populations. Pair-wise relatedness was inferred using a modified version of the software package COLONY and permutation tests were conducted to test the hypothesis that kin occur together in juvenile shoals more often than expected by chance. The frequency of sib dyads among juveniles within shoals was significantly larger than that between shoals in two high predation populations but not in two low predation populations. This finding contributes to the understanding of factors underlying shoal composition and highlights the potential of recent methodological advances for detecting such relationships.     

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.