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.     

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.     

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.     

Social Familiarity Governs Prey Patch-Exploitation, - Leaving and Inter-Patch Distribution of the Group-Living Predatory Mite Phytoseiulus persimilis

Background

In group-living animals, social interactions and their effects on other life activities such as foraging are commonly determined by discrimination among group members. Accordingly, many group-living species evolved sophisticated social recognition abilities such as the ability to recognize familiar individuals, i.e. individuals encountered before. Social familiarity may affect within-group interactions and between-group movements. In environments with patchily distributed prey, group-living predators must repeatedly decide whether to stay with the group in a given prey patch or to leave and search for new prey patches and groups.

Methodology/Principal Findings

Based on the assumption that in group-living animals social familiarity allows to optimize the performance in other tasks, as for example predicted by limited attention theory, we assessed the influence of social familiarity on prey patch exploitation, patch-leaving, and inter-patch distribution of the group-living, plant-inhabiting predatory mite Phytoseiulus persimilis. P. persimilis is highly specialized on herbivorous spider mite prey such as the two-spotted spider mite Tetranychus urticae, which is patchily distributed on its host plants. We conducted two experiments with (1) groups of juvenile P. persimilis under limited food on interconnected detached leaflets, and (2) groups of adult P. persimilis females under limited food on whole plants. Familiar individuals of both juvenile and adult predator groups were more exploratory and dispersed earlier from a given spider mite patch, occupied more leaves and depleted prey more quickly than individuals of unfamiliar groups. Moreover, familiar juvenile predators had higher survival chances than unfamiliar juveniles.

Conclusions/Significance

We argue that patch-exploitation and -leaving, and inter-patch dispersion were more favorably coordinated in groups of familiar than unfamiliar predators, alleviating intraspecific competition and improving prey utilization and suppression.     

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.     

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.     

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.     

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.     

Effects of Familiarity and Population Density on Competitive Interactions and Growth: An Experimental Study on a Territorial Salmonid Fish

The deleterious effect of competition for space and food in animals increases with increasing population density. In contrast, familiarity towards conspecifics can relax the intensity of interference competition. Here, we hypothesized that familiarity towards conspecifics mitigates the effect of density‐dependent growth and dispersal behaviour in territorial animals. To test this, wild‐captured juvenile brown trout were subjected to two consecutive laboratory experiments. First, growth and fin erosion were measured for 40 d in a 2 × 2 factorial design manipulating density and familiarity. The density was manipulated via size of experimental tanks, while per capita food abundance and fish number was constant. All fish were subsequently exposed to an emergence test, giving them the option to leave their group and disperse to a novel unoccupied environment. The results show that familiarity increases growth and decreases the level of fin erosion (i.e. proxy of intensity of aggressive interactions). We found no significant effect of population density on growth rate. However, there was a tendency towards higher fin erosion in fish kept under high density. The growth of individuals was also affected by their size rank within the group, with the largest individuals in each group growing disproportionally faster than the rest of the group, probably due to their high social rank. However, the second and third fish in the size rank did not grow significantly faster and tended to suffer higher mortality than the rest of the group. During the emergence test, the largest individuals in the familiar groups left the shelter either as the first (six of 12 groups) or last (five of 12 groups) individual in the group, while no such pattern was observed in unfamiliar groups. Our results suggest that individuals in familiar groups receive less aggression and stress (i.e. fin damage) and grow faster than fish in unfamiliar groups. The mechanisms indicated in this laboratory study may be especially important in highly fecund organisms like fish which undergo density‐dependent bottlenecks during early life.     

Phenotype Matching and Early Social Conditions Affect Shoaling and Exploration Decisions

Early social conditions are vital for the establishment of future social interactions. Less, however, is known about how differences in early social conditions contribute to the process of individual recognition and subsequently in the decision of associating and exploring behaviours. In this study, we address this gap in the Trinidadian guppy Poecilia reticulata and test the prediction that fish would show a higher tendency to recognize and associate with individuals of similar phenotype. This prediction was tested by comparing the likelihood of association and latency to explore a novel area in males and females when in the presence of individuals that were familiar (reared together but from different populations), from the same population of origin (from the same population but deprived of interaction with each other), or were unfamiliar (different population and have never interacted). Both early social conditions and population of origin (phenotype matching) affected the tendency to shoal and explore. Females, but not males, exhibited identical preference to associate either with unfamiliar females as with familiar females from a different population. Importantly, female preference did not occur with unfamiliar individuals from a different population. In contrast with our prediction, tendency to shoal did not predict exploration propensity. Males always start exploration before the group whenever unfamiliar males composed the group. Females on the other hand only moved to the novel area after seeing the group doing so, revealing sexual dimorphism in exploratory behaviour. Our results provide evidence for a familiarity and phenotypic matching recognition mechanism at the population level and also highlight the importance of accounting for differences between sexes when investigating the effects of early social conditions.     

Benefits of familiarity persist after prolonged isolation in guppies

The persistence of familiarity in the Trinidadian guppy Poecilia reticulata , reunited after prolonged periods of separation, was studied and benefits of this association were tested. Choice experiments following 5 weeks of isolation confirmed that the fish continued to prefer familiar group mates. Furthermore, guppies emerged more rapidly from a shelter in the presence of a familiar individual from which they had been isolated, as opposed to a completely unfamiliar individual. This experiment indicated that the benefits associated with the exploration of new surroundings in the presence of familiar fish were not transitory, and could persist over time periods that allow for shoal mixing and re‐assembly, or movement out of the home range.     

Retention of social recognition after hibernation in Belding's ground squirrels

The retention of social memory during long periods of separation, such as hibernation or migration, has not been well documented, despite evidence for long-term social relationships in migrating species or in long-lived sedentary species. We investigated the ability of captive Belding's ground squirrels, Spermophilus beldingi, to remember previously familiar individuals as well as littermates after 9 months of isolation. Before hibernation, young ground squirrels discriminated between odours of familiar and unfamiliar individuals, as shown by greater investigation of a novel individual's odour. The following spring, these yearlings did not respond differentially to odours of previously familiar and unfamiliar individuals, suggesting that memory for familiar conspecifics was lost during hibernation. In contrast, both female and male yearlings continued to discriminate between odours of littermates and previously familiar nonlittermates. Thus, recognition of close kin was maintained during prolonged social isolation, but recognition of familiar, unrelated individuals was not. If re-establishment of familiarity is not costly or if adults rarely interact with the same individuals in successive years, then selection may not favour retention of individual memories of particular conspecifics over the winter. Even though males rarely encounter kin after dispersal, yearling males did recognize their siblings, suggesting that the relative costs of maintaining kin-recognition abilities year-round may be low. Possible mechanisms underlying the formation and maintenance of individual and kin recognition are discussed. Copyright 2000 The Association for the Study of Animal Behaviour.     

Domestication‐related variation in social preferences in chickens is affected by genotype on a growth QTL

A growth‐related QTL on chicken chromosome 1 has previously been shown to influence domestication behaviour in chickens. In this study, we used Red Junglefowl (RJF) and White Leghorn (WL) as well as the intercross between them to investigate whether stress affects the way birds allocate their time between familiar and unfamiliar conspecifics in a social preference test (‘social support seeking’), and how this is related to genotype at specific loci within the growth QTL. Red Junglefowl males spent more time with unfamiliar chickens before the stressful event compared to the other birds, whereas all birds except WL males tended to spend less time with unfamiliar ones after stress. A significant QTL locus was found to influence both social preference under undisturbed circumstances and social support seeking. The WL allele at this QTL was associated not only with a preference for unfamiliar individuals but also with a shift towards familiar ones in response to stress (social support seeking). A second, suggestive QTL also affected social support seeking, but in the opposite direction; the WL allele was associated with increased time spent with unfamiliar individuals. The region contains several possible candidate genes, and gene expression analysis of a number of them showed differential expression between RJF and WL of AVPR2 (receptor for vasotocin), and possibly AVPR1a (another vasotocin receptor) and NRCAM (involved in neural development) in the lower frontal lobes of the brains of RJF and WL animals. These three genes continue to be interesting candidates for the observed behavioural effects .     

Familiarity adds to attractiveness in matters of siskin mate choice

There is currently considerable controversy in evolutionary ecology revolving around whether social familiarity brings attraction when a female chooses a mate. The topic of familiarity is significant because by avoiding or preferring familiar individuals as mates, the potential for local adaptation may be reduced or favoured. The topic becomes even more interesting if we simultaneously analyse preferences for familiarity and sexual ornaments, because when familiarity influences female mating preferences, this could very significantly affect the strength of sexual selection on male ornamentation. Here, we have used mate-choice experiments in siskins Carduelis spinus to analyse how familiarity and patterns of ornamentation (i.e. the size of wing patches) interact to influence mating success. Our results show that females clearly prefer familiar individuals when choosing between familiar and unfamiliar males with similar-sized wing patches. Furthermore, when females were given the choice between a highly ornamented unfamiliar male and a less ornamented familiar male, half of the females still preferred the socially familiar birds as mates. Our finding suggests that male familiarity may be as important as sexual ornaments in affecting female behaviour in mate choice. Given that the potential for local adaptation may be favoured by preferring familiar individuals as mates, social familiarity as a mate-choice criterion may become a potential area of fruitful research on sympatric speciation processes.     

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.     

The effects of habitat‐ and diet‐based cues on association preferences in the three‐spined stickleback (Gasterosteus aculeatus)

A number of recent papers have investigated the potential of familiarity to organize the distributions of free‐ranging animals. It is not clear, however, to which extent individual recognition or a more general recognition of a group odour is responsible for familiarity preferences. First, we tested the sensory basis of the recognition of familiars in three‐spined stickleback ( Gasterosteus aculeatus ). When allowed to choose between a familiar and an unfamiliar stimulus shoal on the basis of both visual and chemical communication, visual communication only and chemical communication only, the preference of focal fish for familiars was shown to be dependent on the presence of chemical cues. We subsequently investigated the mechanisms underlying such association preferences, specifically the effects of recent habitat and diet on preferences. Experimental fish were divided into four treatment groups consisting of two environment treatments (saline and freshwater) and two diet treatments ( Daphnia spp. and chironimid larvae). Focal fish subsequently showed significant association preferences for groups of unfamiliar fish that had undergone the same environment or diet treatment as themselves, suggesting self‐referent matching. These data indicate that individual recognition is not a pre‐requisite for the expression of familiarity preferences.     

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.     

Information flow through threespine stickleback networks without social transmission

Social networks can result in directed social transmission of learned information, thus influencing how innovations spread through populations. Here we presented shoals of threespine sticklebacks (Gasterosteous aculeatus) with two identical foraging tasks and applied network-based diffusion analysis (NBDA) to determine whether the order in which individuals in a social group contacted and solved the tasks was affected by the group's network structure. We found strong evidence for a social effect on discovery of the foraging tasks with individuals tending to discover a task sooner when others in their group had previously done so, and with the spread of discovery of the foraging tasks influenced by groups' social networks. However, the same patterns of association did not reliably predict spread of solution to the tasks, suggesting that social interactions affected the time at which the tasks were discovered, but not the latency to its solution following discovery. The present analysis, one of the first applications of NBDA to a natural animal system, illustrates how NBDA can lead to insight into the mechanisms supporting behaviour acquisition that more conventional statistical approaches might miss. Importantly, we provide the first compelling evidence that the spread of novel behaviours can result from social learning in the absence of social transmission, a phenomenon that we refer to as an untransmitted social effect on learning.     

Foraging nine-spined sticklebacks prefer to rely on public information over simpler social cues

Social animals can observe others' behavior and in the processacquire information of varying quality about a given resource.Theoretical models predict that blind copying of others' behavioris more likely when individuals are only able to observe thedecisions (here "social cues") of others rather than the cues(here "public information") on which such decisions are based.We investigated information use by nine-spined sticklebacks(Pungitius pungitius) in a two-patch foraging context. Socialcues were provided by the number of demonstrator fish presentat each patch (two versus six), which either conflicted withthe demonstrators' observed feeding rate at each patch (publicinformation) or was the only information available. Consistentwith predictions, observers preferred the patch previously associatedwith six demonstrators when social cues were the only availablesource of information but preferred the patch previously associatedwith two demonstrators ("rich" patch) when also provided withpublic information. On the bases of these experiments, we arguethat it is because these fish preferentially base decisionson public information rather than social cues that they canpotentially avoid engaging in erroneous informational cascades.Thus, the availability of public information can help socialanimals make adaptive decisions.