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.     

Social familiarity relaxes the constraints of limited attention and enhances reproduction of group‐living predatory mites

In many group‐living animals, within‐group associations are determined by familiarity, i.e. familiar individuals, independent of genetic relatedness, preferentially associate with each other. The ultimate causes of this behaviour are poorly understood and rigorous documentation of its adaptive significance is scarce. Limited attention theory states that focusing on a given task has interrelated cognitive, behavioural and physiological costs with respect to the attention paid to other tasks. In multiple signal environments attention has thus to be shared among signals. Assuming that familiar neighbours require less attention than unfamiliar ones, associating with familiar individuals should increase the efficiency in other tasks and ultimately increase fitness. We tested this prediction in adult females of the group‐living, plant‐inhabiting predatory mite Phytoseiulus persimilis. We evaluated the influence of social familiarity on within‐group association behaviour, activity, predation and reproduction. In mixed groups (familiar and unfamiliar), familiar predator females preferentially associated with each other. In pure groups (either familiar or unfamiliar), familiar predator females produced more eggs than unfamiliar females at similar predation rates. Higher egg production was correlated with lower activity levels, indicating decreased restlessness. In light of limited attention theory, we argue that the ability to discriminate between familiar and unfamiliar individuals and preferential association with familiar individuals confers a selective advantage because familiar social environments are cognitively and physiologically less taxing than unfamiliar social environments.     

The effect of familiarity on aggregation and social behaviour in juvenile small spotted catsharks Scyliorhinus canicula

This study was designed to address whether juvenile small spotted catsharks Scyliorhinus canicula aggregate and to determine whether potential aggregation is underpinned by social preferences for conspecifics. Using controlled and replicated experiments, the role of familiarity as a potential mechanism driving aggregation and social behaviour in this species was considered. Observed S. canicula association data compared to null model simulations of random distributions revealed differences in aggregation under different social contexts. Only familiar juvenile S. canicula aggregated more than would be expected from random distribution across their habitat. Familiarity increased the mean number of groups but did not significantly affect mean group size. Significant preference and avoidance behaviour across all groups were also observed. Furthermore, the strength of social attraction, quantified by the mean association index, was significantly higher in groups containing familiar individuals. Mixed familiar and unfamiliar treatments were also conducted to test for within‐ and between‐group effects, finding high variation across replicates with some groups assorting by familiarity and others not. It is believed that this study is the first to examine experimentally the influence of conspecific familiarity on aggregation behaviour in sharks. These results not only imply a functional benefit to aggregation, but also suggest that persistent social affiliation is likely to influence dispersal following hatching in this small benthic elasmobranch.     

Shoaling preference and evidence for maintenance of sibling groups by juvenile black perch Embiotoca jacksoni

Group sizes in free‐living juvenile black perch Embiotoca jacksoni were quantified and predictions of the hypothesis that such groups comprise sibling brood‐mates were tested. Group sizes in the field were within the range of female brood sizes and often occurred close to each other but did not merge. In captivity, juveniles formed groups immediately after birth. In laboratory experiments, they also associated significantly more with chambers containing familiar members of their own brood than empty chambers but did not associate more with chambers containing similar‐sized juveniles from a different brood. Juvenile E. jacksoni also associated significantly more with chambers containing familiar brood‐mates than with chambers containing unfamiliar members of a different brood. The strength of this preference increased with the number of days fish had been together since birth. When two broods were placed in a large outdoor tank, all individuals from both broods directed significantly more aggressive acts towards members of the other brood than towards members of their own brood. While the relative effects of familiarity and relatedness cannot be completely separated in this viviparous species, associating with familiar individuals would facilitate the maintenance of sibling groups in the field.     

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.     

Lack of social preference between unfamiliar and familiar juvenile Port Jackson sharks Heterodontus portusjacksoni

This study investigated whether captive-reared juvenile Port Jackson sharks Heterodontus portusjacksoni choose to aggregate and if familiarity is one of the mechanisms driving social preference. In a controlled binary-choice experiment, juvenile sharks were given the option to associate or not with unfamiliar conspecifics, or to associate or not with familiar conspecifics. In neither group did juvenile H. portusjacksoni actively choose to associate with conspecifics, but familiarity decreased the proportion of time spent near a conspecific only during the initial phase of the experiment. Treatment (1 or 3 shoal mates), sex and size had no effect on aggregation behaviour. These findings suggest that familiarity is not a driver of social preferences in juvenile H. portusjacksoni, contrary to results in another shark species. Additionally, adult H. portusjacksoni form large aggregations during the breeding season and actively associate with familiar sex and size-matched individuals, thus our results suggest the species undergoes an ontogenetic shift in social behaviour.     

Chemosensory Recognition of Familiar and Unfamiliar Conspecifics by Juveniles of the Iberian Wall Lizard Podarcis hispanica

Chemosensory recognition of familiar conspecifics has been reported in studies with members of several lizard families and may be advantageous to distinguish between intruders and neighbors or group members. However, few species have been studied and information on the ability to discriminate between familiar and unfamiliar conspecifics by chemosensory means is lacking for most lizard families. In this paper we ask whether juveniles of the Iberian wall lizard Podarcis hispanica (Lacertidae), can discriminate between chemical signals from familiar conspecifics with whom they have shared a terrarium for several months and those from unfamiliar conspecifics housed in a different terrarium. Experimental trials were conducted by transferring juveniles to a test terrarium with a filter paper substrate. We tested the responses of lizards to paper substrates labeled by familiar cage-mates, unfamiliar conspecifics, or unlabeled. Tongue-flicks and other behaviors in response to pheromonal stimuli were recorded for 10 min Juveniles directed more chemosensory behavior towards paper substrates bearing chemicals from familiar conspecifics than towards similar paper substrates labeled by unfamiliar conspecifics. These results indicate that juveniles in this lizard species can recognize familiar conspecifics and discriminate between familiar and unfamiliar individuals using only chemical stimuli. We discuss the role of habituation in familiar conspecific recognition and review possible explanations of the functional significance of this type of discrimination in lizards.     

The effect of ration level and social rank on the development of fin damage in juvenile rainbow trout

The development and severity of fin damage was examined in groups of juvenile rainbow trout Oncorhynchus mykiss of different strength of feeding hierarchies. The development of dorsal and caudal fin damage over time was compared between four groups fed different ration levels (0·25, 0·5, 1·0 and 1·5% body weight day⁻¹) and between individuals of different feeding rank within each group. Dominance hierarchies were assessed from repeated daily measurements of food consumption of individuals using radiography. The feeding and growth data indicated that the strength of the social hierarchy weakened with increasing ration. Caudal fin damage developed with time in all groups whereas dorsal fin damage developed only under limited rations. The severity of both dorsal and caudal fin damage was significantly dependent on the ration size fed to the group, with lower ration groups sustaining more fin damage. The severity of dorsal fin erosion was greater than for the caudal fin. Within the two lower ration groups, subordinate fish suffered the most dorsal fin damage. The results suggested that the severity of dorsal fin damage within groups of juvenile rainbow trout can be used as an indicator of hierarchy Strength.     

Kin and familiarity influence association preferences and aggression in the mangrove killifish Kryptolebias marmoratus

Association preferences and aggression intensity were investigated in relation to kin and familiarity in the self-fertilizing, clonal vertebrate, the mangrove killifish Kryptolebias marmoratus. Results indicated that fish preferentially associated with and exhibited less intense aggression towards members of their own genotype (kin), compared to members of a different genotype (non-kin). Furthermore, when fish were presented with stimulus groups of the same genotype that were familiar or unfamiliar, fish preferentially associated with and exhibited lower aggression intensity directed towards familiar groups. These results indicate that this species prefer to associate with both kin and familiar individuals and modulate aggression accordingly. These results are discussed with reference to the adaptive benefits of kin recognition and preferences for familiars, and place results within the context of current knowledge of the ecology of K. marmoratus.     

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.     

Social preferences in farmed silver fox females (Vulpes vulpes): Does it change with age?

Determining foxes’ social preference, and how this influences their social behaviour towards different conspecifics at different ages may give us a better understanding of how to prevent foxes from exposure of possible social stressors when housed in groups. Here, we investigated the effect of familiarity on social preferences in silver fox females and their motives for seeking social contact at two different ages. Fourteen silver fox females conducted two preference tests, first at the age of 9 weeks and the second at the age of 24 weeks, where they could choose between an empty cage, a familiar female or an unfamiliar female at their own age. The position and behaviour of the females were recorded using instantaneous sampling every tenth minute for 26 h. There was a clear preference to seek contact with a conspecific at 9 weeks of age (p < 0.01). The cubs did not differentiate between a familiar or unfamiliar stimulus animal (p > 0.05), however there was a tendency to play more in front of the unfamiliar stimulus animal (p = 0.07). No preference was seen for either the familiar, unfamiliar or empty cage stimulus when the females were 24 weeks old (p > 0.05), however they were more aggressive towards the unfamiliar stimulus animal (p < 0.01). Thus, there was no effect of familiarity in time spent with a social stimulus at either age, however these results suggest that the motives for seeking contact as cubs were non-aggressive and possibly play related, whereas the aggressive behaviour displayed by juveniles towards the unfamiliar female indicates an increased competitive motivation.     

The Effect of Familiarity with Demonstrators on Social Learning in Three‐Spined Sticklebacks (Gasterosteus aculeatus)

Social learning is an important process in the spread of information, especially in changing environments where inherited behaviors may not remain relevant. In many species, the decision of whom to trust to have reliable information depends on the relationship between individuals. Many fish species, including three‐spined sticklebacks, preferentially associate with familiar individuals. Previous studies in three‐spined sticklebacks have provided mixed evidence about the effect of familiarity on social learning in this species. Therefore, this study further explores familiarity and social learning in sticklebacks, specifically from a demonstrator‐focused perspective. We found that in a food patch discrimination task, individuals with unfamiliar demonstrators performed significantly better than those with familiar demonstrators. In a problem‐solving task, we found that focal fish attended to the behavior of demonstrators, but we did not detect an effect of familiarity on performance, and indeed the proportion of individuals to solve the task after observing demonstrators was low. These results suggest that sticklebacks have a preference for unfamiliar demonstrators, but that the use of social information varies depending on context.     

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.     

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.     

Schooling preferences for familiar fish vary with group size in a wild guppy population

The ability of fish to recognize and preferentially associate with familiar conspecifics has been well documented in a series of laboratory experiments. In this paper we investigate the schooling preferences of wild female guppies, Poecilia reticulata, in the Upper Tunapuna River in Trinidad and confirm that they do indeed prefer to associate with familiar individuals. The guppies in this river occur in a series of pools that become isolated during the dry season. These fish interact solely with other individuals in their pool for periods of several months at a time and thus have ample opportunity to become accustomed to one another. Our study also reveals that the tendency of female guppies to school with familiar fish declines as the group size in which they naturally live increases. Preferences are strong when there are small numbers of females in a pool, but diminish thereafter. This indicates that the expression of familiarity is constrained by group size. The basis of recognition and the consequences of schooling preferences for familiar individuals are discussed.     

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.     

Size-Dependent Chemosensory Responses to Familiar and Unfamiliar Conspecific Faecal Pellets by the Iberian Rock-Lizard, Lacerta monticola

We conducted a field study to analyse the social relationships between males of the Iberian rock lizard (Lacerta monticola). The degree of familiarity was determined based on the degree of overlap between their home ranges. We then designed a laboratory experiment to test whether the same males were able to discriminate between familiar and unfamiliar conspecifics using faecal pellet odours. Differential tongue‐flick rates suggest that large males (snout‐to‐vent length, SVL > 75 mm), at least, may discriminate between odours of familiar and unfamiliar males. The behavioural responses were dependent on relative differences in body size between the responding male and the male that donated the faecal pellet. Thus, as responding small males increased in size relative to their corresponding familiar male, their rate of tongue‐flicking significantly decreased; this was not the case in response to unfamiliar males. In contrast, there were no significant correlations between the response of large males to familiar or unfamiliar male stimuli, regardless of size differences. These results suggest that chemical cues contained in faecal pellets allow individual recognition in male L. monticola, and that the response depends on body size. We suggest that faecal pellets might be used to scent‐mark home ranges, which would contribute to lowering the costs of aggressive interactions.     

The effects of familiarity and social hierarchy on group membership decisions in a social fish

Members of animal groups face a trade-off between the benefits of remaining with a familiar group and the potential benefits of dispersing into a new group. Here, we examined the group membership decisions of Neolamprologus pulcher, a group-living cichlid. We found that subordinate helpers showed a preference for joining familiar groups, but when choosing between two unfamiliar groups, helpers did not preferentially join groups that maximized their social rank. Rather, helpers preferred groups containing larger, more dominant individuals, despite receiving significantly more aggression within these groups, possibly owing to increased protection from predation in such groups. These results suggest a complex decision process in N. pulcher when choosing among groups, dependent not only on familiarity but also on the social and life-history consequences of joining new groups.     

Effects of familiarity on the behaviour towards intruders in captive common marmosets (Callithrix jacchus)

A study on the behaviour of a group of common marmosets (Callithrix jacchus) towards unrelated intruding conspecifics (juvenile male twins) was performed. The group members' proximity to the intruders during two consecutive study periods was analyzed. During the first period in which the experimental conditions as well as the intruders were unfamiliar, all but one group member were equally likely to stay near the intruders and usually more than three individuals were present simultaneously. During the second period the group members showed different scores of proximity towards the intruders. One individual, an adult male, was in close proximity nearly the whole time. Additionally, the number of individuals simultaneously staying near the intruders was clearly reduced. It is argued that (1) the change in behaviour of the group members was affected by the increasing familiarity and (2) intruder experiments with unfamiliar conspecifics are only of partial value for clarification of the process of immigration.     

The effect of familiarity on social interactions in meadow voles,Microtus pennsylvanicus: a laboratory and field study

The role of familiarity in affecting the outcome of social interactions among meadow voles was investigated in both a laboratory and a field experiment. In the laboratory, captive meadow voles, Microtus pennsylvanicus, were exposed to a conspecific's odour. The voles were then placed into two groups: familiar and unfamiliar. Familiar voles were individuals who underwent staged dyadic encounters with the conspecific to whose odours they had been exposed. Unfamiliar voles were individuals who underwent paired encounters with conspecifics to whose odours they had not been exposed. In the field experiment, familiar voles were neighbours that were trapped within each other's home ranges over two consecutive bi-weekly trapping sessions. Unfamiliar voles were individuals that were trapped on different trapping grids. The results of the laboratory and field studies were similar. Encounters between familiar females resulted in less agonistic behaviour and more amicable acts than encounters between unfamiliar females. In contrast, encounters between familiar males resulted in more agonistic behaviour than encounters between unfamiliar males. Familiarity did not affect the outcome of male-female interactions. These results are discussed in the framework of the social system of the meadow vole.