Recent social environment affects colour-assortative shoaling in juvenile angelfish (Pterophyllum scalare)

Theory predicts that fish should show colour-assortative shoaling in order to avoid the oddity effect whereby individuals that differ in some feature from the group majority appear to incur increased risk of predation. It has also been shown that early experience plays an important role in affecting social preferences in some fish species. In this study, the importance of colour phenotype in promoting assortative shoaling and the role played by the recent social environment on its expression were investigated in juvenile angelfish, Pterophyllum scalare. Individuals of the uniformly black and golden colour morphs were housed in a group with conspecifics of like and unlike body colour to themselves, as well as in mixed-colour groups for 4 weeks. Subsequently, they were subjected to a binary choice to shoal with a group of conspecifics composed of unfamiliar fish of either a like or unlike colour phenotype to themselves. The response of the individuals to the colour attributes of the shoals was related to their recent social environment. Fish in like- and mixed-colour previous treatments showed a preferential association with like colour conspecifics. In contrast, the shoaling behaviour exhibited by fish previously maintained with a group of unlike-coloured conspecifics (cross-housed treatment) indicated no significant preference for any of the shoals. The results suggest that angelfish use body colouration as an intraspecific shoaling cue and that learning, in the form of recent familiarisation with a specific colour phenotype of conspecifics, can affect colour-assortative shoaling preferences in this species. This learning component of the choice need not be restricted to early developmental stages.     

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.     

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.     

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.     

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.     

Effect of the Presence of Subordinates on Dominant Female Behaviour and Fitness in Hierarchies of the Dwarf Angelfish Centropyge bicolor

In many hierarchical animal societies, dominant individuals control group membership owing to their power to evict subordinates. In such groups, the presence of subordinates, and therefore group stability, is continually dependent on subordinates being tolerated by dominants. The dominant decision to tolerate or evict is, in turn, dependent on the costs and benefits to dominants of subordinate presence. We investigated the effect of subordinate presence on dominants in the female dominance hierarchy of the dwarf angelfish Centropyge bicolor, using both observations of natural groups and experimental removals of subordinates. We found that the presence of subordinates had no effect on dominant access to resources, as measured by dominant foraging rates and home range areas, nor on dominant fitness, as measured by growth rates and spawning frequencies. Our results suggest that the presence of subordinates has a neutral effect on the current fitness of dominants, so that dominants have no great incentive to evict subordinates. We discuss the possibility that tolerance of subordinates might be further explained by considering future fitness, as dominant females in these haremic protogynous angelfish stand to inherit the male position, whereupon subordinate females change from potential competition to useful mates.     

Investigating the Effect of Familiarity on Kin Recognition of Three‐Spined Stickleback (Gasterosteus aculeatus)

The ability to discriminate between related and unrelated individuals has been demonstrated in many species. The mechanisms behind this ability might be manifold and depend on the ecological context in which the species lives. In brood‐caring species, both familiarity and phenotype matching are known to be used in kin recognition. However, results of studies disentangling these two phenomena have proved contradictory. We aimed to broaden our knowledge about the mechanisms of kin recognition using shoaling preferences of three‐spined stickleback (Gasterosteus aculeatus) as a model behavior. In our first experiment, focal fish had the choice to shoal either with kin or unfamiliar non‐kin. In half of the trials, kin groups were composed of familiar individuals, while they were unfamiliar in the other half. Focal fish significantly preferred kin as shoaling partner, a result which was not reinforced by familiarity. In our second experiment, focal fish were given the choice between a shoal of familiar kin and a shoal of unfamiliar kin. Here, focal fish did not show any significant preference. These results indicate that familiarity does not impact stickleback's ability to recognize kin. Furthermore, they show that familiarity does not overrule recognition based on phenotype matching or innate recognition, underlining the importance of these mechanisms. Finally, our results lead to the assumption that individual recognition might play a minor role also in non‐kin‐based preferences for familiars.     

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 Role of Body Surface Area in Quantity Discrimination in Angelfish (Pterophyllum scalare)

Although some fish species have been shown to be able to discriminate between two groups (shoals) of conspecifics differing in the number of members, most studies have not controlled for continuous variables that covary with number. Previously, using angelfish (Pterophyllum scalare) we started the systematic analysis of the potential influence of such continuous variables, and found that they play different roles in shoal discrimination depending on whether large (≥4 fish) or small (<4 fish) shoals were contrasted. Here, we examine the potential role of the overall body surface area of stimulus fish in shoal preference, a prominent variable not yet examined in angelfish. We report that both when numerically large (5 versus 10 fish) and when small (2 versus 3 fish) shoals were contrasted, angelfish were unable to discriminate the numerically different shoals as long as the surface area of the contrasted shoals was equated. Thus, we conclude that body surface may be an important continuous variable in shoal discrimination. This conclusion was further supported by the analysis of preference when shoals of the same numerical size but different body surface area were contrasted. We found subjects to spend significantly more time close to the shoals with the greater overall surface area. Last, we conducted an experiment in which we simultaneously controlled a set of continuous variables, including overall surface area, and found angelfish to use the number of shoal members as a cue only in large shoal contrasts but not in small shoal contrasts. This result suggests the potential existence of different processing systems for large and small numbers in fish.     

The differential responses to the odor of unfamiliar male conspecifics in dominant,subordinate, and isolated mice

Male ddY mice were used to investigate the responses toward the odor of unfamiliar male mice. They were reared either in isolation from 3 weeks of age or in pairs. At 10 weeks of age, they went through a 4-day test period, in which the responses of the mice toward the odor of unfamiliar dominant and subordinate mice were investigated by differentiating the responses into the time to investigate the odor and the final decision of avoidance or preference. All the mice went through the encounter tests after this odor test in order to investigate the relationship between the responses toward the odor and the behavior toward the odor donor. The pair-reared dominants and the subordinates responded to the odor of the dominant and subordinate mice differentially. This indicated that they could discriminate the dominance status of unfamiliar mice by odor. Isolated mice did not respond to the odor of the dominant and subordinate mice differentially. Social experiences were concluded to be necessary to discriminate the dominance status of unfamiliar mice through odor. The length of the investigation time and the final decision of avoidance or preference did not correlate in pair-reared or isolated mice, and these 2 scales were concluded to be different. But the dominant mice that investigated the odor for longer periods tended to show aggression in the later encounter test.     

Olfactory cues in discrimination among individuals in dominance hierarchies in the cockroach, Nauphoeta cinerea

ABSTRACT. The purpose of this study was to explore the olfactory recognition mechanisms used by individual subordinate male cockroaches, Nauphoeta cinerea (Olivier), in a dominance hierarchy. Results of two independent sets of experiments, one using an olfactometer and the other using an arena, suggest that olfactory cues are important to males. Subordinate males did not avoid dominant male odour in an olfactometer but could discriminate between the odours of familiar and unfamiliar individual dominant males, preferring the odour of the dominant male with which they had previous social contact. Since test subordinates did not avoid dominant male odours in the olfactometer, it is possible that the distance an individual remains from a dominant is important. To test this, individual dominant and subordinate males were tethered in the centre of an arena. Subordinate males were introduced into the arena and allowed to approach the tethered male. They approached tethered dominants and subordinates differently, and tended to keep away from the dominants. Tethered males unfamiliar to the test animals were avoided as well.     

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.     

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.      

The importance of stable schooling: do familiar sticklebacks stick together?

Preferences for rejoining shoals composed of familiar individuals have recently been documented in a variety of small, shallow-water fish species. Such preferences are assumed to be adaptive, since familiar groups have improved anti-predator defences and more stable dominance hierarchies. However, the design of these studies may have created conditions that elevate preferences for familiar individuals. Furthermore, in natural habitats, where significant opportunities for inter-shoal transfer may exist, it is unclear whether shoals stay together long enough for such preferences to develop. Here we present the results of a laboratory study examining whether prior familiarity influences the subsequent shoal composition of sticklebacks (Gasterosteus aculeatus) allowed to re-assort freely in a large arena tank. We show that fish from different familiarity groups associate with familiar conspecifics significantly more than predicted by a model of random assortment, suggesting that even when there is ample opportunity for inter-group transfer, shoal composition can remain stable. We discuss the phenomena that may lead to the formation of familiar groups in natural habitats. In addition, we suggest that familiarity benefits may reduce the relative value of transferring to otherwise more attractive (e.g. larger or more phenotypically matched) groups, and thereby stabilize shoal structure.     

The influence of social rank in the angelfish,Pterophyllum scalare,on locomotor and feeding activities in a novel environment

To investigate differences in behaviour associated with social rank and environmental conditions, a comparison was made between swimming and feeding activities of dominant and subordinate angelfish, housed in groups of six, with those of angelfish housed singly in identical laboratory aquaria. Subordinate individuals were less active, less ready to feed and consumed less food items than dominants, but their feeding and activity levels were still greater than those displayed by isolated fish used as controls. When fish from each of the above categories were transferred to a novel, identical tank to be tested individually for a 6-day period, little change was observed in previously isolated fish. In contrast, the previous social experience had a marked influence on the behaviour of the other individuals, the effects being related to the social status. The strongest initial response to the new environment was shown by subordinate individuals, with a significant increase in swimming and a significant decrease in feeding compared to the group situation. Subordinates were significantly more active than dominants, who in turn moved more than previously isolated fish. Dominants and subordinates were now similarly reluctant to feed, and their food consumption was less than that of previously isolated fish. With time in the novel environment a significant reduction of swimming activity and a recovery of feeding measures were detected, but levels were still depressed in relation to the group condition, and lower in subordinates than in dominants, indicating the long-lasting effects of the previous social interactions. The results have clear implications for laboratory studies using groups of fish in which social hierarchies may be established prior to individuals being tested singly in a novel environment.     

Social familiarity and shoal formation in juvenile fishes

The potential influence of social familiarity in shoal‐choice decisions was investigated in two sympatric species of north temperate fishes, juvenile banded killifish Fundulus diaphanus and juvenile bluegill sunfish Lepomis macrochirus. Groups of socially familiar and unfamiliar conspecifics were formed in the laboratory using wild‐caught fishes. Juvenile F. diaphanus demonstrated a strong preference for familiar conspecific shoalmates, whereas juvenile L. macrochirus exhibited no preference for either unfamiliar or familiar conspecific shoalmates. The differential influence of familiarity on shoalmate choice in juveniles of these two species could be due to their different ecologies, local population densities and life histories.     

Social interactions modulate the virulence of avian malaria infection

There is an increasing understanding of the context-dependent nature of parasite virulence. Variation in parasite virulence can occur when infected individuals compete with conspecifics that vary in infection status; virulence may be higher when competing with uninfected competitors. In vertebrates with social hierarchies, we propose that these competition-mediated costs of infection may also vary with social status. Dominant individuals have greater competitive ability than competing subordinates, and consequently may pay a lower prevalence-mediated cost of infection. In this study we investigated whether costs of malarial infection were affected by the occurrence of the parasite in competitors and social status in domestic canaries (Serinus canaria). We predicted that infected subordinates competing with non-infected dominants would pay higher costs than infected subordinates competing with infected dominants. We also predicted that these occurrence-mediated costs of infection would be ameliorated in infected dominant birds. We found that social status and the occurrence of parasites in competitors significantly interacted to change haematocrit in infected birds. Namely, subordinate and dominant infected birds differed in haematocrit depending on the infection status of their competitors. However, in contrast to our prediction, dominants fared better with infected subordinates, whereas subordinates fared better with uninfected dominants. Moreover, we found additional effects of parasite occurrence on mortality in canaries. Ultimately, we provide evidence for costs of parasitism mediated by social rank and the occurrence of parasites in competitors in a vertebrate species. This has important implications for our understanding of the evolutionary processes that shape parasite virulence and group living.     

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.     

Timing and plasticity of shoaling behaviour in the zebrafish, Danio rerio

The zebrafish has become a major model system for biomedical research and is an emerging model for the study of behaviour. While adult zebrafish express a visually mediated shoaling preference, the onset of shoaling behaviour and of this preference is unknown. To assess the onset of these behaviours, we first manipulated the early social environment of larval zebrafish subjects, giving them three model shoaling partners of the same pigment phenotype. We then assayed the subjects' preferences using binary preference tests in which we presented subjects with two shoals, one shoal of fish exhibiting the same pigment pattern phenotype as their models and another shoal with a radically different pigment pattern. To determine whether or not the visually mediated preference could be altered once it was established, we further manipulated the social environment of a number of subjects, rearing them with one model shoal and testing them, then changing their social consorts and retesting them. Our results demonstrate that larval zebrafish shoal early in their development, but do not exhibit a shoaling preference until they are juveniles. Moreover, we find that the shoaling preference is stable, as changing the social environment of fish after they had acquired a preference did not change their preference. These data will facilitate investigations into the mechanisms underlying social behaviour in this vertebrate model system.