Long-term effects of adolescent stress on neophobic behaviors in zebra finches are modulated by social context when in adulthood

Experiencing stress during adolescence can increase neophobic behaviors in adulthood, but most tests have been conducted in the absence of conspecifics. Conspecifics can modulate responses to stressors, for example by acting as ‘social buffers’ to attenuate the aversive appraisal of stressors. Here, we investigate the long-term effects of adolescent stress on the behavioral responses to novel stimuli (a mild stressor) across social contexts in an affiliative passerine bird, the zebra finch. During early (days 40–60) or late (days 65–85) adolescence the birds (n = 66) were dosed with either saline or the hormone corticosterone (CORT). CORT was given in order to mimic a physiological stress response and saline was given as a control. In adulthood, the birds' behavioral responses to a novel environment were recorded in both the presence and absence of conspecifics. An acute CORT response was also quantified in adolescence and adulthood. Our findings show clear evidence of social context mediating any long-term effects of adolescent stress. In the presence of familiar conspecifics no treatment effects were detected. Individually, birds dosed with CORT in early adolescence were slower to enter a novel environment, spent more time perching in the same novel environment, and, if female, engaged in more risk assessment. Birds dosed in late adolescence were unaffected. No treatment effects were detected on CORT, but adolescents had a higher CORT concentration than adults. Our results are the first to suggest that familiar conspecifics in adulthood can buffer the long-term effects of stress that occurred during early adolescence.     

Effects of gonadectomy on prolactin and LH secretion and the pituitary-thyroid axis in male dogs

The effects of gonadectomy on the secretion of prolactin, LH, TSH, and thyroxine were investigated. Blood serum hormone concentrations were analysed before and at 20, 120, and 180 min after a single iv TRH injection in each of eight healthy intact and castrated male beagle dogs before (control) and after 4-week treatment with the dopamine-2 receptor agonist cabergoline. Under control conditions the mean prolactin, TSH, and thyroxine concentrations were similar in intact and gonadectomised dogs, and administration of TRH provoked a significant (p < 0.01) increase in concentrations of the three hormones. The overall inhibitory effect of cabergoline treatment on prolactin secretion was more pronounced in the castrated dogs compared with the intact group. Cabergoline significantly suppressed the TRH-induced prolactin increase in each group (p < 0.01). Corresponding TRH-stimulated TSH concentrations were not affected by cabergoline. In the gonadectomised dogs, thyroxine concentrations before and at 120 and 180 min after TRH injection were significantly lower than under control conditions. LH concentrations were always higher (p < 0.01) in gonadectomised dogs compared with the intact dogs, but appeared to be affected neither by TRH nor by cabergoline administration. It can thus be concluded from the results, that gonadectomy does not result in hyperprolactinaemia in male dogs, while LH concentrations are significantly increased due to missing androgen feedback. Thyroid function remains unaffected by gonadectomy. Testicular steroids appear to interact with central dopaminergic and probably other neuroendocrine mechanisms regulating the secretion of prolactin, TSH, and thyroxine. Thus, long-term dopamine-2 receptor agonistic treatment may lead to a hypothyroid condition in castrated male dogs.     

Peripheral administration of oxytocin increases social affiliation in the naked mole-rat (Heterocephalus glaber)

The neuropeptide oxytocin regulates a wide variety of social behaviors across diverse species. However, the types of behaviors that are influenced by this hormone are constrained by the species in question and the social organization that a particular species exhibits. Therefore, the present experiments investigated behaviors regulated by oxytocin in a eusocial mammalian species by using the naked mole-rat (Heterocephalus glaber). In Experiment 1, adult non-breeding mole-rats were given intraperitoneal injections of either oxytocin (1 mg/kg or 10 mg/kg) or saline on alternate days. Animals were then returned to their colony and behavior was recorded for minutes 15–30 post-injection. Both doses of oxytocin increased huddling behavior during this time period. In Experiment 2, animals received intraperitoneal injections of either oxytocin (1 mg/kg), an oxytocin-receptor antagonist (0.1 mg/kg), a cocktail of oxytocin and the antagonist, or saline across 4 testing days in a counterbalanced design. Animals were placed in either a 2-chamber arena with a familiar conspecific or in a small chamber with 1 week old pups from their home colony and behaviors were recorded for minutes 15–30 post-injection. Oxytocin increased investigation of, and time spent in close proximity to, a familiar conspecific; these effects were blocked by the oxytocin antagonist. No effects were seen on pup-directed behavior. These data suggest that oxytocin is capable of modulating affiliative-like behavior in this eusocial species.     

Effect of testosterone and melatonin on social dominance and agonistic behavior in male Tscheskia triton

Social dominance and agonistic behavior play important roles in animal societies. Melatonin and testosterone are closely related to social dominance and agonistic behavior in rodents, but interactions between both of them remain unknown. In this study we investigated the effects of testosterone and melatonin by manipulating photoperiod and castration on social dominance and agonistic behavior in male Tscheskia triton. Castration significantly decreases social dominance of both short- and long-day males, suggesting that testosterone benefits social dominance of males in both breeding and non-breeding seasons. In intact conditions, long-day males tended to dominate short-day males, suggesting that the effect of testosterone on social dominance was a little stronger than melatonin. However, castrated short-day males became dominant over their castrated long-day opponents meaning that high melatonin levels obviously benefit social dominance in males. Hormone implantation indicated that testosterone had no effect on non-breeding condition, but that melatonin was important during the breeding season. Our results indicate that both testosterone and melatonin are important in determining social dominance in male hamsters, and the effect of testosterone appears to be stronger than melatonin. Testosterone is responsible for aggression and social dominance in male hamsters during the breeding season, while melatonin regulates behavior during non-breeding, probably due to the different seasonal secretory patterns of the hormones.     

Effect of prenatal androgens on click-evoked otoacoustic emissions in male and female sheep (Ovis aries)

Otoacoustic emissions (OAEs) were measured in male and female Suffolk sheep (Ovis aries). Some sheep had been administered androgens or estrogens during prenatal development, some were gonadectomized after birth, and some were allowed to develop normally. As previously reported for spotted hyenas, gonadectomy did not alter the OAEs for either sex; accordingly, the untreated/intact and the untreated/gonadectomized animals were pooled to form the control groups. The click-evoked otoacoustic emissions (CEOAEs) exhibited by the female control group (N = 12) were slightly stronger (effect size = 0.42) than those in the male control group (N = 15), which is the same direction of effect reported for humans and rhesus monkeys. Females administered testosterone prenatally (N = 16) had substantially weaker (masculinized) CEOAEs than control females (effect size = 1.15). Both of these outcomes are in accord with the idea that prenatal exposure to androgens weakens the cochlear mechanisms that underlie the production of OAEs. The CEOAEs of males administered testosterone prenatally (N = 5) were not different from those of control males, an outcome also seen in similarly treated rhesus monkeys. Males administered dihydrotestosterone (DHT) prenatally (N = 3) had slightly stronger (hypo-masculinized) CEOAEs than control males. No spontaneous otoacoustic emissions (SOAEs) were found in any ears, a common finding in non-human species. To our knowledge, this is the first ruminant species measured for OAEs.     

Rival imprinting: interspecifically cross-fostered tits defend their territories against heterospecific intruders

Failure to recognize conspecifics in social interactions such as mate choice and aggressive encounters will often result in reduced fitness. Studies on mate choice show that the ability to recognize conspecifics as mates is not universally present at birth, but often needs to be learned. In contrast, little is known about the ontogeny of intrasexual species recognition. To test whether learning influences the recognition of sexual rivals, we compared the aggressive response towards intruders of interspecifically cross-fostered individuals and controls reared by conspecific parents. We simulated territorial intrusion by presenting either a caged individual or playback song near the nest of breeding pairs of great tits, Parus major, and blue tits, P. caeruleus. Great tits reared by blue tit parents responded much more to blue tit stimuli than did great tit controls, and furthermore showed stronger responses to blue tit stimuli than to those of their own species. Blue tits reared by great tits responded much more to great tit stimuli than did blue tit controls. In contrast, blue tits cross-fostered to coal tits, P. ater, did not respond more to coal tits than did blue tit controls. There was a species difference in the response to conspecifics: blue tits cross-fostered to great tits responded more to conspecifics than did cross-fostered great tits. The results were similar for males and females. We conclude that learning influences intrasexual species recognition in these tits. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Testosterone reactivity to facial display of emotions in men and women

Previous studies have examined testosterone's role in regulating the processing of facial displays of emotions (FDEs). However, the reciprocal process – the influence of FDEs, an evolutionarily ancient and potent class of social signals, on the secretion of testosterone – has not yet been studied. To address this gap, we examined the effects of emotional content and sex of facial stimuli in modulating endogenous testosterone fluctuations, as well as sex differences in the endocrine responses to faces. One hundred and sixty-four young healthy men and women were exposed, in a between-subjects design, to happy or angry same-sex or opposite-sex facial expressions. Results showed that in both men (n = 85) and women (n = 79), extended exposure to faces of the opposite sex, regardless of their apparent emotional content, was accompanied by an accumulation in salivary testosterone when compared to exposure to faces of the same sex. Furthermore, testosterone change in women exposed to angry expressions was greater than testosterone change in women exposed to happy expressions. These results add emotional facial stimuli to the collection of social signals that modulate endocrine status, and are discussed with regard to the evolutionary roles of testosterone.     

Social influences on plasma testosterone levels in male talapoin monkeys

Three social groups of laboratory-housed talapoin monkeys (Miopithecus talapoin) consisting of four adult males and four or five adult females, were observed over a 4-year period. All females were ovariectomized and given estradiol implants at intervals to render them sexually attractive; except for two castrated males with testosterone implants, all males were intact. Sexual and aggressive interactions were recorded, and testosterone levels were measured in plasma taken from males twice weekly. In each group males formed a linear dominance order, defined in terms of the direction of aggression between animals. The hormonal responses of intact males were monitored with respect to the presence of attractive females, access to these females, and transfer from the social group to isolation. In all groups the behavioral and endocrine responses of males to these treatments were rank related. In some instances, rising in rank was associated with elevated testosterone and falling in rank with decreased testosterone; these hormonal changes were associated with changes in sexual and aggressive interactions. The effects of sexual and aggressive behavior on plasma testosterone titers are discussed.     

Pre-pubertal gonadectomy and the social consequences of acute ethanol in adolescent male and female rats

It has previously been shown that pre-pubertal or adult gonadectomy (GX) increases ethanol intake in male rats. This study examined whether this sex-selective increase reflects a GX-induced maintenance in males of more adolescent-typical responsiveness to ethanol characterized by enhanced sensitivity to positive (e.g., socially facilitating) and a decreased sensitivity to adverse (e.g., socially inhibitory) effects of ethanol. Male and female Sprague-Dawley rats were pre-pubertally GX, sham (SH)-operated, or non-manipulated (NM) at postnatal day (P) 25. During the late adolescent transition into adulthood (P48 — baseline day), rats were given a saline injection, placed alone into a familiar test apparatus for 30 min and then exposed for 10 min to an unfamiliar partner of the same age and sex. On the following day (P49), similar testing occurred after administration of 0.5, 0.75, 1.0 or 1.25 g/kg ethanol. At baseline, GX males and females displayed higher levels of social activity (especially adolescent-typical play and contact behavior) than SH and NM animals, with GX females displaying greater social activity than GX males. Neither males nor females demonstrated social facilitation at lower ethanol doses, regardless of hormonal status. Whereas the social inhibitory effects of higher doses of ethanol were similar across groups among females, SH males were less sensitive than both GX and NM males to ethanol-induced social inhibition. These results suggest that enhanced ethanol intake in GX males is not related to alterations in sensitivity to ethanol's social inhibitory effects. GX, however, results in retention of adolescent-typical social behaviors, with older GX adolescent rats resembling early adolescents in exhibiting elevated social activity—particularly play and contact behavior.     

Sexual preferences of male hamsters (Mesocricetus auratus) for conspecifics in different endocrine conditions

The behavioral responses of sexually experienced male hamsters toward a pair of anesthetized conspecifics were investigated. Males spent significantly more time licking, sniffing, and mounting neonatally and adult castrated males than intact males. Adult castrated males receiving oil injections were preferred over castrates receiving exogenous testosterone propionate (TP). Ovariectomized females were preferred over intact males, adult castrated males, or spayed females receiving exogenous TP. It was concluded that the absence of an androgen-dependent factor(s) renders an animal more sexually attractive.     

Sex differences in olfactory social recognition memory in meadow voles,Microtus pennsylvanicus

Terrestrial mammals, like rodents, use odors, and scent marks to indicate their presence in an area to conspecifics. These odors convey information about the scent donor's genotype, sex, condition, and age. The ability to discriminate among the scent marks of conspecifics and later recollect the identity of the donor is essential for choosing between familiar and unfamiliar mates. We tested the hypothesis that the promiscuous meadow vole (Microtus pennsylvanicus) can recollect the odor of a familiar, opposite-sex conspecific and distinguish it from that of an unfamiliar, opposite-sex conspecific. We also hypothesized that because reproductive success is highly skewed among male meadow voles and competition for mates is intense, males will be more likely than females to recollect the odor of a familiar, opposite-sex conspecific and distinguish it from that of an unfamiliar, opposite-sex conspecific, for a longer period of time. Using a habituation task, we first exposed the voles, 4 times successively, to the anogenital area scent of an opposite-sex conspecific. Then, 1 hr, 24 hrs, 72 hrs, or 96 hrs after the fourth exposure, voles were presented with the odor of the donor from the exposure phase (familiar donor) and that of an unfamiliar, opposite-sex conspecific. Female meadow voles spent similar amounts of time investigating the scent of the familiar male donor and that of an unfamiliar male donor after the 1-hr and 24-hr intervals. Male meadow voles, however, spent more time with the scent of an unfamiliar female donor than that of the familiar female donor after the 1-hr, 24-hr, and 72-hr intervals, suggesting that male voles could recollect the scent mark of a familiar female for at least three days. The implications of these sex differences in social memory may reflect the different strategies male and female meadow voles use in the recognition of previous and potential mates. Recognition of an individual's scents may enhance fitness by allowing animals to direct appropriate behaviors toward those individuals.     

Investigating social discrimination of group members by laying hens

Social relationships in domestic fowl are commonly assumed to rely on social recognition and its pre-requisite, discrimination of group-mates. If this is true, then the unnatural physical and social environments in which commercial laying hens are typically housed, when compared with those in which their progenitor species evolved, may compromise social function with consequent implications for welfare. Our aims were to determine whether adult hens can discriminate between unique pairs of familiar conspecifics, and to establish the most appropriate method for assessing this social discrimination. We investigated group-mate discrimination using two learning tasks in which there was bi-directional exchange of visual, auditory and olfactory information. Learning occurred in a Y-maze task (p < 0.003; n = 7/8) but not in an operant key-pecking task (p = 0.001; n = 1/10). A further experiment with the operant-trained hens examined whether failure was specific to the group-mate social discrimination or to the response task. Learning also failed to occur in this familiar/unfamiliar social discrimination task (p = 0.001; n = 1/10). Our findings demonstrate unequivocally that adult laying hens kept in small groups, under environmental conditions more consistent with those in which sensory capacities evolved, can discriminate group members: however, appropriate methods to demonstrate discrimination are crucial.     

Testicular hormone exposure during adolescence organizes flank-marking behavior and vasopressin receptor binding in the lateral septum

Adolescence is a period during which many social behaviors emerge. One such behavior, flank marking, is a testosterone-modulated scent marking behavior that communicates dominance status between adult male Syrian hamsters. Testosterone modulates flank-marking behavior by altering neural transmission of vasopressin within a forebrain circuit. This study tested whether testicular hormones secreted during adolescence play purely a transient activational role in the display of flank-marking behavior, or whether adolescent steroid hormone secretions also cause long-term organizational changes in vasopressin binding within brain regions underlying flank-marking behavior. We tested this hypothesis by manipulating whether testicular secretions were present during adolescent development and then tested for flank-marking behavior and vasopressin receptor binding within the flank-marking neural circuit in young adulthood. Specifically, males were gonadectomized immediately before or after adolescence, replaced with testosterone 6 weeks following gonadectomy in young adulthood, and behavior tested 1 week later. Adult testosterone treatment activated flank-marking behavior only in males that were exposed to testicular hormones during adolescence. In addition, males exposed to testicular hormones during adolescence exhibited significantly less vasopressin receptor binding within the lateral septum than males deprived of adolescent hormones, suggesting that hormone-dependent remodeling of synapses normally occurs in the lateral septum during adolescence. These data highlight the importance of gonadal steroid hormone exposure during adolescence for the organization of neural circuits and social behavior.     

Rhesus monkeys see who they hear: spontaneous cross-modal memory for familiar conspecifics

Rhesus monkeys gather much of their knowledge of the social world through visual input and may preferentially represent this knowledge in the visual modality. Recognition of familiar faces is clearly advantageous, and the flexibility and utility of primate social memory would be greatly enhanced if visual memories could be accessed cross-modally either by visual or auditory stimulation. Such cross-modal access to visual memory would facilitate flexible retrieval of the knowledge necessary for adaptive social behavior. We tested whether rhesus monkeys have cross-modal access to visual memory for familiar conspecifics using a delayed matching-to-sample procedure. Monkeys learned visual matching of video clips of familiar individuals to photographs of those individuals, and generalized performance to novel videos. In crossmodal probe trials, coo-calls were played during the memory interval. The calls were either from the monkey just seen in the sample video clip or from a different familiar monkey. Even though the monkeys were trained exclusively in visual matching, the calls influenced choice by causing an increase in the proportion of errors to the picture of the monkey whose voice was heard on incongruent trials. This result demonstrates spontaneous cross-modal recognition. It also shows that viewing videos of familiar monkeys activates naturally formed memories of real monkeys, validating the use of video stimuli in studies of social cognition in monkeys.     

Impaired social contacts with familiar anesthetized conspecific in CA3‐restricted brain‐derived neurotrophic factor knockout mice

Familiarity is conveyed by social cues and determines behaviors toward conspecifics. Here, we characterize a novel assay for social behaviors in mice—contacts with anesthetized conspecific—which eliminates reciprocal interactions, including intermale aggression and shows behaviors that are independent of the demonstrator's activity. During the initial 10 minutes (phase‐1), the wild‐type (WT) subjects contacted the anesthetized conspecifics vigorously regardless of familiarity. During the subsequent 80 minutes (phase‐2), however, they contacted more with familiar than unfamiliar conspecifics. We then applied this test to highly aggressive mice with a hippocampal CA3‐restricted knockout (KO) of brain‐derived neurotrophic factor (BDNF), in which aggression may mask other social behaviors. The KO mice showed less preference for contacting familiar conspecifics than did WT mice during phase‐2 but no differences during phase‐1. Among nonsocial behaviors, WT mice also spent less time eating in the presence of familiar than with unfamiliar conspecifics, which was not seen in KO mice. In addition, KO mice exhibited reduced pain sensitization. Altogether, these findings suggest that CA3‐specific deletion of BDNF results in deficits in circuits that process social cues from familiar conspecifics as well as pain and may underlie empathy‐like behaviors.     

Temperament moderates the influence of periadolescent social experience on behavior and adrenocortical activity in adult male rats

Adolescence is a period of significant behavioral and physiological maturation, particularly related to stress responses. Animal studies that have tested the influence of adolescent social experiences on stress-related behavioral and physiological development have led to complex results. We used a rodent model of neophobia to test the hypothesis that the influence of adolescent social experience on adult behavior and adrenocortical function is modulated by pre-adolescent temperament. Exploratory activity was assessed in 53 male Sprague–Dawley rats to classify temperament and then they were housed in one of the three conditions during postnatal days (PND) 28–46: (1) with familiar kin, (2) with novel social partners, or (3) individually with no social partners. Effects on adult adrenocortical function were evaluated from fecal samples collected while rats were individually-housed and exposed to a 1-hour novel social challenge during PND 110–114. Adolescent-housing with novel or no social partners led to reduced adult glucocorticoid production compared to adolescent-housing with familiar littermates. Additionally, highly-exploratory pre-weanling rats that were housed with novel social partners during adolescence exhibited increased exploratory behavior and a more rapid return to basal glucocorticoid production in adulthood compared to those housed with familiar or no social partners during adolescence and compared to low-exploratory rats exposed to novel social partners. In sum, relatively short-term adolescent social experiences can cause transient changes in temperament and potentially longer-term changes in recovery of glucocorticoid production in response to adult social challenges. Furthermore, early temperament may modulate the influence of adolescent experiences on adult behavioral and adrenocortical function.     

Effects of sociosexual environment on serum testosterone in captive male African rhinoceros

The relationships between testosterone concentrations in male African rhinoceros and the presence of conspecific males and females were investigated. Serum testosterone concentrations were measured using enzyme-linked immunoassay (EIA) in 37 male black rhinoceros (Diceros bicornis) and 21 male white rhinoceros (Ceratotherium simum) housed at 37 institutions in the USA. Testosterone concentrations in both black (n = 37) and white (n = 21) rhinoceros males rose with increasing numbers of females present (P < 0.05). Average testosterone concentrations also rose with an increased number of conspecific males (n = 34) in black rhinoceros (P < 0.05). However, no specific pattern was found among male white rhinoceros housed with other males. We inferred that introduction of females to a male may play an important role in stimulating libido and spermatogenesis. The similar response of black rhinoceros and white rhinoceros to increased numbers of females suggested that, at least historically, herd structure for blacks may have been more similar to whites than previously realized, and should be investigated further.     

Olfactory Experience Affects the Response of Meadow Voles to the Opposite‐Sex Scent Donor of Mixed‐Sex Over‐Marks

Scent marking and over‐marking are important forms of communication between the sexes for many terrestrial mammals. Over the course of three experiments, we determined whether the amount of time individuals investigate the scent marks of opposite‐sex conspecifics is affected by 4 d of olfactory experience with those conspecifics. In Experiment 1, female meadow voles, Microtus pennsylvanicus, spent more time investigating the scent mark of the novel male conspecific than that of the familiar male donor, whereas male voles spent similar amounts of time investigating the scent mark of the familiar female and a novel female conspecific. In Experiment 2, voles were exposed to a mixed‐sex over‐mark in which subjects did not have 4 d of olfactory experience with either the top‐scent donor or the bottom‐scent donor. During the test phase, male and female voles spent more time investigating the scent mark of the opposite‐sex conspecific that provided the top‐scent mark than that of a novel, opposite‐sex conspecific. Male and female voles spent similar amounts of time investigating the scent mark of the bottom‐scent donor and that of a novel opposite‐sex conspecific. In Experiment 3, voles were exposed to a mixed‐sex over‐mark that contained the scent mark of an opposite‐sex conspecific with which they had 4 d of olfactory experience. During the test phase, male voles spent more time investigating the mark of the familiar, top‐scent female than the scent mark of a novel female donor but spent similar amounts of time investigating the mark of the familiar, bottom‐scent female and that of a novel female donor. In contrast, female voles spent more time investigating the mark of a novel male donor than that of either the familiar, top‐scent male or that of the familiar, bottom‐scent male. The sex differences in the responses of voles to scent marks and mixed‐sex over‐marks are discussed in relation to the natural history and non‐monogamous mating system of meadow voles.     

Hormones,behavior, and social network analysis: Exploring associations between cortisol,testosterone, and network structure

We used a new interdisciplinary paradigm of social network analysis (SNA) to investigate associations between hormones and social network structures. We examine these biobehavioral processes and test hypotheses about how hormones are associated with social network structures using exponential random graph modeling (ERGM) in a cohort of first-year students (n = 74; 93% female; M age = 27 years) from a highly competitive, accelerated nursing program. Participants completed friendship nominations and as a group simultaneously donated saliva (later assayed for cortisol and testosterone). ERGM analyses revealed that salivary cortisol levels were inversely associated with the number of outgoing ties (i.e., network activity). By contrast, testosterone was not related to friendship network structure. Integration of SNA and salivary bioscience creates a novel approach to understanding hormone–behavior relationships within the context of human social ecologies.     

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.