Early life maternal sociality predicts juvenile sociality in blue monkeys

Maternal effects are widespread in living organisms though little is known about whether they shape individual affiliative social behavior in primates. Further, it remains a question whether maternal effects on affiliative behavior differ by offspring sex, as they do in other physiological systems, especially in species with high levels of adult sexual dimorphism and divergence in social niches. We explored how direct and indirect experiences of maternal affiliative behavior during infancy predicted affiliative behavior approximately 1–6 years later during the juvenile period, using behavioral data from 41 wild blue monkey juveniles and their 29 mothers, and controlling for individual age, sex, and maternal rank. Female juveniles spent less time grooming with any partner and with peers the more maternal grooming they received during infancy, whereas males groomed more with any partner and with peers. Similarly, the more that mothers groomed with other adult females during subjects’ infancy, female subjects played less with peers, and male subjects played more as juveniles. Further, this maternal effect on social behavior appears specific to early life, as the same aspects of mothers’ sociality measured throughout subjects’ development did not predict juvenile behavior. Overall, our results suggest that both direct and indirect experience of mother's affiliative behavior during infancy influence an individual's affiliation later in life that sexes respond differently to the maternal affiliation, and that the first year of life is a critical window.     

Olfactory communication and the importance of different odour sources in the ferret (Mustela putorius f. furo)

Olfactory communication has a major role in solitary carnivores, particularly during the breeding season. Scent-marking behaviour in ferret (Mustela putorius f. furo) has been well studied, but not the significance of the deposited odours for the animal. We compared the interest in urogenital, anal and body odours of opposite-sex conspecifics between male and female ferrets and investigated both sexes’ discrimination ability (familiar vs. unfamiliar) for these three opposite-sex odours and the use of its ability by females during the breeding season. Males are more interested than females in the urogenital odour of the opposite sex. Male body odour probably did not interest females and males are somewhat interested in the female one. However, anal odour of the opposite sex is as interesting for males as for females and both sexes are able to discriminate familiar anal odour from an unfamiliar one. Moreover, females could use this ability when they must choose to have some sensory contact between olfactory familiar and unfamiliar males since they prefer to be in contact with the former. These results are coherent with behavioural differences observed between male and female solitary mustelids in the field and in captivity, and the consortship success of resident males compared to roaming males.     

Chemosensory Recognition of Familiar and Unfamiliar Conspecifics by the Scincid Lizard Eumeces laticeps

The ability of broad-headed skinks (Eumeces laticeps) to distinguish familiar from unfamiliar individuals of the opposite sex and themselves from other individuals of the same sex using only chemical stimuli was examined experimentally. Cloacal chemical stimuli were presented to lizards on moistened cotton swabs and numbers of tongue-flicks performed in 60 s were recorded. Males emitted significantly greater numbers of tongue-flicks in response to chemical cues from unfamiliar females than of female cagemates. Response rates of males housed with females and males housed alone to chemical stimuli from unfamiliar females did not differ. Chemical stimuli from unfamiliar males elicited significantly more tongue flicks from males than their own or deionized water, but their own stimuli elicited no more than the odourless control. Females tongue-flicked significantly more in response to cloacal chemical stimuli from unfamiliar males than from male cagemates. The findings indicate that both sexes of broad-headed skinks can discriminate between chemical stimuli of familiar and unfamiliar individuals of the opposite sex and that males can distinguish their own cloacal chemicals from those of unfamiliar males. The possible functions of these chemosensory capacities, including location of mates by scent-trailing and assessment of the presence of sexual competitors, are discussed in relation to the social behaviour of E. laticeps.     

Post‐birth separation affects the affiliative behaviour of kin in a pitviper with maternal attendance

The relatedness of individuals can have pronounced effects on behavioural interactions, as engaging in mutually beneficial behaviours with kin can increase inclusive fitness. Parental care can be particularly important for kin discrimination in birds and mammals, but similar studies have not been conducted on species exhibiting more rudimentary forms of care. Maternal attendance of young is ubiquitous among viviparous temperate pitvipers, but the adaptive value of this behaviour has received little attention. We sought to determine if being deprived of a maternal attendance period as neonates altered how cottonmouths (Agkistrodon piscivorus Lacépède), a common North American pitviper, responded to kin vs. non‐kin. We measured the affiliative behaviour of related and unrelated juvenile–juvenile and mother–juvenile pairs that had been allowed a maternal attendance period or had been separated since birth. We found that maternal attendance was not required for sibling or mother–offspring recognition, but did enhance female affiliative behaviour overall, and particularly that of sisters. In contrast, related juveniles that were separated at birth showed a reversal of the sex‐specific affiliative behaviour observed in maternally attended juveniles. Post‐birth separation had only a modest effect on mother–juvenile affiliative behaviour, and no effect on the strong affiliation between mothers and daughters. The patterns of affiliative behaviour observed in maternally attended snakes corresponded to patterns that have emerged from previous captive and field studies of pitvipers; however, the behaviour of juveniles separated at birth was atypical. Thus, it is possible that maternal attendance plays some role in the development of adaptive sex‐specific and kin‐directed affiliative behaviour in pitvipers.     

Sex differences in cortisol's regulation of affiliative behavior

A contribution to a special issue on Hormones and Human Competition.A stress perspective is used to illuminate how competitive defeat and victory shape biology and behavior. We report a field study examining how change in cortisol following perceived defeat (vs. victory) in a competition—in this case, a dog agility competition—relates to affiliative behavior. Following competition, we measured cortisol change and the extent to which dog handlers directed affiliative behaviors toward their dogs. We found striking sex differences in affiliation. First, men were more affiliative toward their dogs after victory, whereas women were more affiliative after defeat. Second, the greater a female competitor's increase in cortisol, the more time she spent affiliating with her dog, whereas for men, the pattern was the exact opposite: the greater a male competitor's increase in cortisol, the less time he spent affiliating with his dog. This pattern suggests that, in the wake of competition, men and women's affiliative behavior may serve different functions—shared celebration for men; shared consolation for women. These sex differences show not only that men and women react very differently to victory and defeat, but also that equivalent changes in cortisol across the sexes are associated with strikingly different behavioral consequences for men and women.     

Vasopressin regulates social recognition in juvenile and adult rats of both sexes, but in sex- and age-specific ways

In adult male rats, vasopressin (AVP) facilitates social recognition via activation of V1a receptors within the lateral septum. Much less is known about how AVP affects social recognition in adult females or in juvenile animals of either sex. We found that administration of the specific V1a receptor antagonist d(CH(2))(5)[Tyr(Me)(2)]AVP into the lateral septum of adult rats impaired, whereas AVP extended, social discrimination in both sexes. In juveniles, however, we detected a sex difference, such that males but not females showed social discrimination. Interestingly, administration of the V1a receptor antagonist to juveniles (either intracerebroventricularly or locally in the lateral septum) did not prevent social discrimination, but instead significantly decreased the investigation of a novel as opposed to a familiar animal in both sexes, with stronger effects in males. V1a receptors were found to be abundantly expressed in the lateral septum with higher binding density in females than in males. These findings demonstrate that activation of V1a receptors in the lateral septum is important for social recognition in both sexes, and that the roles of septal V1a receptors in social recognition change during development.     

Developmental changes in responsiveness to parents and unfamiliar adults in a monogamous monkey (Callicebus moloch)

Titi monkeys (Callicebus moloch) are monogamous New World primates that are characteristically found in family-type groups consisting of a mated adult pair and one or two young. The factors maintaining the small size of these groups are not known. Based on observations of free-ranging and captive families, parental aggression toward older offspring seems unlikely to play a significant role. Maturing individuals themselves, however, could undergo behavioral changes that weaken ties to their natal group. These might include waning of affiliative relations with parents, or subtle forms of aversion. Independent of such changes, increasing interest in unfamiliar conspecifics could be a factor. We examined these possibilities in the present study by assessing changes in social behavior and social preferences from initial ambulatory independence (6 months) through reproductive maturity (24 months) in a combined cross-sectional/longitudinal study of 21 captive titi monkeys living with their parents. Responses to both parents and to an unfamiliar adult heterosexual pair, a single unfamiliar adult male, and a single unfamiliar adult female were observed when subjects were given a choice between parents and strangers presented simultaneously or as the only social incentive. Social stimuli were at opposite ends of a 16.8-m-long test corridor. Subjects could move freely about the corridor for 5 min with each configuration of social stimuli. They stayed closer to parents than to strangers at all ages. Responsiveness to strangers increased with age and suggested growing ambivalence, particularly toward the male stranger. As they approached 24 months of age, male subjects showed a dramatic increase in the frequency and intensity of agonistic behaviors toward male strangers, behaviors that were rarely directed toward female strangers or parents. Waning of attraction to parents may be less important in dispersal from the natal group than changing reactions to strangers.     

The influence of sex and body size on nestling survival and recruitment in the house sparrow

Differences in the survival rates of males and females over the period from hatching to recruitment can have important impacts on individual fitness and population demographics. However, whilst the influence of an individual's sex on nestling growth and survival has been well studied, less is known about sex‐specific survival over the period between fledging and recruitment. Here, we analyse nestling survival and recruitment in an isolated, island population of house sparrows (Passer domesticus), using data collected over a 4‐year period. Nestlings that had a greater mass at 1 day old were more likely to fledge. Recruitment was also positively associated with day 11 mass. The positive influence of nestling mass on survival to fledging also increased as brood size increased. There was no difference in the survival of male and female individuals prior to fledging. In contrast, over the period from fledging to recruitment, females had significantly less mortality than males. Recruitment was also positively associated with 11‐day‐old mass. Neither the nestling sex ratio nor the fledging sex ratio deviated from 0.5, but the sex ratio amongst recruits was female biased. Our study shows that sex can influence juvenile survival, but also shows that its effect varies between different life‐history stages; therefore, these stages should be considered separately if we want to understand at what point sex‐specific differences in juvenile survival occur. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 680–688.     

Affiliation in Four Echimyid Rodent Species based on Intrasexual Dyadic Encounters: Evolutionary Implications

In this work we explored the evolution of sociality in cursorial echimyids by comparing affiliation among three species of Trinomys and one species of Thrichomys. We captured specimens of Trinomys yonenagae, Trinomys albispinus minor, and Thrichomys apereoides in areas of the Brazilian semiarid Caatinga, and Trinomys iheringi denigratus in one area of Atlantic Forest. For each species, we recorded 12 intra‐sexual dyadic encounters in a neutral arena (six between males and six between females) in order to test the hypothesis that species and sex influence level of affiliation. This response variable was assessed based on an affiliation index, calculated as the proportion of the total number of affiliative behaviors to the total number of social behaviors exhibited by the dyad during each encounter. Hypothesis test was performed by means of a parametric two‐way anova . The test was able to detect significant differences only among species, not among sexes. Trinomys yonenagae was the most affiliative species, while T. apereoides and T. albispinus minor were the most agonistic ones. Trinomys iheringi denigratus showed an intermediate pattern. We suggest, based on out‐group comparison, that affiliation in Trinomys increased in the lineage containing T. iheringi denigratus and T. yonenagae and that higher affiliation in the last species can be adaptive to the life in the desert‐like habitat where it lives.     

A competitive drive? Same‐sex attentional preferences in capuchins

In primates, faces provide information about several characteristics of social significance, including age, physical health, and biological sex. However, despite a growing literature on face processing and visual attention in a number of primate species, preferences for same‐ or opposite‐sex faces have not yet been examined. In the current study, we explore the role of conspecific sex on visual attention in two groups of capuchin monkeys. Subjects were shown a series of image pairs on a Tobii Pro TX300 eye tracker, each depicting an unfamiliar male and an unfamiliar female face. Given the behavioral evidence of mate choice in both sexes, we hypothesized that capuchins would preferentially attend to images of unfamiliar conspecifics of the opposite sex. Our alternative hypothesis was that capuchins would preferentially attend to same‐sex individuals to assess potential competitors. Our results provide support for our alternative hypothesis. When comparing attention to each stimuli type across sexes, females spent significantly larger percentages of time than males looking at female photos, whereas males spent significantly larger percentages of time than females looking at male photos. Within each sex, females looked for significantly larger percentages of time to female versus male images. Males also looked for larger percentages of time to same‐sex images, though not significantly. To our knowledge, these data are the first to demonstrate significant sex‐biased attentional preferences in adult primates of any species, and suggest that, for capuchins, potential competitors garner more attention than potential mates. In addition, our findings have implications for studies of visual attention and face processing across the primate order, and suggest that researchers need to control for these demographic factors in their experimental designs.     

Effects of Pair-Bond and Social Context on Male–Female Interactions in Captive Titi Monkeys (Callicebus moloch, Primates: Cebidae)

In monogamous species, an abiding relationship between a specific adult male and a specific adult female is a defining feature of the social system. The interactions between these individuals are influenced by many factors, including not only the history of their relationship (for example, development of a mutual bond), but also the immediate effects of the prevailing social context (for example, presence and sex of extra‐pair conspecifics). In this study we examined the effects of an existing bond and of social context on interactions between adult heterosexual pairs of the monogamous titi monkeys (Callicebus moloch). Twelve adult males and 12 adult females were tested with their cagemates and with an unfamiliar partner of the opposite sex in five social contexts: (1) mated male–female pair; (2) unfamiliar pair; (3) single female; (4) single male; and (5) empty stimulus cage. Results show that mated pairs were more affiliative than unfamiliar pairs and differentiated social contexts more sharply. Males were more responsive to context than females. Distance between mates was less and physical contact was more frequent in the presence of male–female pairs or a single male, than in the presence of a single female or an empty cage. These findings suggest that the presence and sex of strangers have a stronger influence on male–female interactions when the pair has an existing relationship.     

Affiliative behavior of adult female sooty mangabeys (Cercocebus atys)

A 14-month study of 30 adult female members of a captive group of sooty mangabeys investigated their affiliative interactions with group members of varying age and sex. The adult females preferentially affiliated with other adults and interacted less than expected with immature group members. Dyadic frequencies suggested especially frequent affiliation with the three resident adult males, although the pattern of interaction with each male was distinct and apparently was related to age and dominance status of the males. Females of the alpha matriline showed significantly greater affiliation with the males than did those of other matrilines, but this preference was not reciprocated by the males. A preference for grooming older group members (some of the matriarchs and the oldest adult male) was also suggested. In consideration of the taxonomic distinctness of the sooty mangabey from the gray-cheeked mangabey, comparison of these results with those available for albigena were made. Few differences were apparent. Comparisons with the affiliative behavior of Papio females also suggested limited differences, despite the apparently isolated position of the sooty mangabey within the tribe Papionini.     

Inter-Annual Variability of Fledgling Sex Ratio in King Penguins

As the number of breeding pairs depends on the adult sex ratio in a monogamous species with biparental care, investigating sex-ratio variability in natural populations is essential to understand population dynamics. Using 10 years of data (2000–2009) in a seasonally monogamous seabird, the king penguin (Aptenodytes patagonicus), we investigated the annual sex ratio at fledging, and the potential environmental causes for its variation. Over more than 4000 birds, the annual sex ratio at fledging was highly variable (ranging from 44.4% to 58.3% of males), and on average slightly biased towards males (51.6%). Yearly variation in sex-ratio bias was neither related to density within the colony, nor to global or local oceanographic conditions known to affect both the productivity and accessibility of penguin foraging areas. However, rising sea surface temperature coincided with an increase in fledging sex-ratio variability. Fledging sex ratio was also correlated with difference in body condition between male and female fledglings. When more males were produced in a given year, their body condition was higher (and reciprocally), suggesting that parents might adopt a sex-biased allocation strategy depending on yearly environmental conditions and/or that the effect of environmental parameters on chick condition and survival may be sex-dependent. The initial bias in sex ratio observed at the juvenile stage tended to return to 1∶1 equilibrium upon first breeding attempts, as would be expected from Fisher’s classic theory of offspring sex-ratio variation.     

Sons do not take advantage of a head start: parity in herring gull offspring sex ratios despite greater initial investment in males

Skewed adult sex ratios sometimes occur in populations of free‐living animals yet the proximate mechanisms, timing of sex‐biases, and the selective agents contributing to skew remain a source of debate with contradictory evidence from different systems. We investigated potential mechanisms contributing to sex biases in a population of herring gulls with an apparent female skew in the adult population. Theory predicts that skewed adult sex ratios will adaptively lead to skewed offspring sex ratios to restore balance in the effective breeding population. Parents may also adaptively bias offspring sex ratios to increase their own fitness in response to environmental factors. Therefore, we expected to detect skewed sex ratios either at hatching or at fledging as parents invest differentially in offspring of different sexes. We sampled complete clutches (n = 336 chicks) at hatching to quantify potential skews in sex ratios by position in the hatch order, time of season, year, and nesting context (nest density), finding no departure from equal sex ratios at hatching related to any of these factors. Further, we sampled 258 chicks at near‐fledging to investigate potential sex biases in survival at the chick stage. Again, no biases in sex ratios were recorded. Male offspring were favored in this population via greater maternal investment in eggs carrying male embryos and greater parental provisioning of male offspring which reached greater sizes by fledging. Despite the advantages realized by male offspring, females were equally as likely to fledge as males. Thus, biased adult sex ratios apparently arise in the post‐fledging and pre‐recruitment stage in our population.     

Aggressive behaviour of male mice (Mus musculus) towards familiar and unfamiliar opponents.

Two types of colonies of laboratory mice were employed; hierarchically organized ones formed by placing five unfamiliar 8-week-old mice in a cage together and amicably organized colonies in which four male litter mates were kept together throughout the whole period of the experiment. During a 21-day pre-experimental period intra-colony aggressive behaviour was recorded. A dominant animal and ranked subordinates occurred in every hierarchical colony, whilst no aggression was recorded in any of the amicable colonies. During a 25-day period unfamiliar adult male or female mice were introduced daily into the amicable or hierarchical colonies for 10 min. In a third experiment juvenile mice 17, 24, 31 or 38 days old were introduced into hierarchically organized colonies during a 20-day period. In all hierarchical colonies the stranger was attacked irrespective of sex and age; the majority of attacks were carried out by the dominant mouse. Aggression by the dominant declined exponentially throughout the experimental period and regression analyses compared the different data. Unfamiliar adult females were the recipients of fewer attacks than unfamiliar adult males and the age of juvenile strangers was found to be an important factor. Amicably organized mice initially did not attack strangers, but over a period of 25 days the number of attacks on unfamiliar males gradually increased.     

Canine Reconciliation and Third‐Party‐Initiated Postconflict Affiliation: Do Peacemaking Social Mechanisms in Dogs Rival Those of Higher Primates?

Conflicts over food, access to mates, or other limited resources can sometimes escalate into aggression. In species that form social groups, these aggressive conflicts can jeopardize the benefits of group living, such as enhanced access to valued resources, necessitating the development of behavioural mechanisms that either mitigate conflicts, prevent aggressive escalation or resolve disputes. Two important mechanisms for managing the effects of disputes involve postconflict (PC) affiliative behaviour, either between the former opponents (called ‘reconciliation’) or between one opponent and a third party. Even though numerous studies have tested reconciliatory and third‐party affiliation tendencies in primates, for non‐primate animals little systematic data are available. We performed behavioural observations on three groups of captive domestic dogs (Canis familiaris) and used a PC/MC method to test the existence of reconciliation and third‐party affiliation in this species. The results of this study clearly indicate that both reconciliation and third‐party PC interactions are present in the domestic dog, and form important social mechanisms of the domestic dog. Furthermore, familiar individuals showed a significantly higher proportion of reconciled conflicts than did unfamiliar individuals, and also displayed fewer conflicts. Finally, we show that most of the third‐party affiliations involve the victim of a conflict and that victim‐directed affiliation outweighs victim‐initiated third‐party affiliation in these PC interactions.     

Acoustical variations in sexually dimorphic features of distance calls in domesticated zebra finches (Taeniopygia guttata castanotis)

Species-specific distance calls (DCs) were recorded from Zebra finches (Taeniopygia guttata castanotis) obtained from three different breeding stocks: Japanese breeders that use Bengalese finches as fostering parents, and Japanese and American breeders that let natural parents rear Zebra finches. These calls were analyzed for five acoustic parameters that were shown to be sexually dimorphic in wild Zebra finches. Male Zebra finches had DCs that were variable among breeding stocks and among individuals. Female DCs recorded from Bengalese-fostered birds were generally longer in duration and higher in pitch than those recorded from Zebra-finch-reared birds, males and females in each breeding stock differed in at least one acoustic parameter, but that parameter was unique in each of the breeding stocks. These results suggest that although sexual dimorphism in Zebra finch DCs has gradually disappeared during the process of domestication, at least one acoustic attribute which allows discrimination between the calls of the sexes has been preserved.     

Postconflict Affiliation Between Former Opponents in Macaca thibetana on Mt. Huangshan, China

We describe basic patterns of postconflict affiliation between former opponents within a group of wild, provisioned Tibetan macaques Macaca thibetana on Mt. Huangshan, China. Like most primates studied to date, Tibetan macaques reconciled, i.e., overall they engaged in affiliative interaction with opponents at higher rates immediately after an aggressive conflict than at other times. Probabilities of affiliation were enhanced ≤30 s after the end of hostilities. However when we examined sex partner combinations separately, we found unequivocal evidence for reconciliation only for male-male dyads. Tolerant interaction among other partner combinations apparently was not disrupted after a conflict, presumably obviating the need to reconcile. One aspect of reconciliation among males was consistent with other indications of a despotic dominance style: aggressors initiated a higher proportion of affiliative interactions after a conflict than at other times. Another aspect of reconciliation was more typical of relaxed dominance styles: males used specialized behaviors (embraces and same-sex mounts) disproportionately to reconcile. We also found inconsistent evidence for the valuable relationship hypothesis; probabilities of reconciliation were enhanced for male-male dyads with the closest affiliative relationships, but not for those that displayed the most tolerance or mutual agonistic support. We discuss reconciliation and other aspects of conflict management among males in the context of a group with nearly even sex ratios and high male-male mating competition.     

Differences between the sexes in direction and duration of response to seeing a potential sex partner mate with another

We have shown previously that: (1) female Japanese quail, Coturnix japonica, increase and male Japanese quail decrease their tendencies to affiliate with potential sex partners after seeing them mate, and (2) in both sexes of quail, affiliative preferences and choice of a sex partner are highly correlated. Here we predict that because effects of a prior male's sperm on a second male's probability of fertilizing a female are relatively brief, a male's avoidance of whichever member of a pair of females he has seen mating should be transitory. Conversely, because female quail seek high-quality males as mates and quality is a relatively permanent characteristic, females' preferences between males should remain constant over time. We found, as predicted, that the durations of effects on affiliation of seeing a potential sex partner mate differed in male and female quail. Forty-eight hours after male quail saw a female mate, they no longer avoided her, whereas 48 h after female quail saw a male mate, his attractiveness remained enhanced. We conclude by suggesting that both the direction and the duration of responses of male and female Japanese quail to seeing a member of the other sex mating enhance the fitness of members of each sex. Copyright 2000 The Association for the Study of Animal Behaviour.     

Vasotocin treatment inhibits courtship in male zebra finches; concomitant androgen treatment inhibits this effect

Zebra finches evolved in arid areas of Australia. Their reproduction is stimulated by water availability, which is unpredictable. Cheng (Poult. Sci. Rev. 5 (1993) 37) hypothesized that the primary mechanism controlling reproduction in species relying on unpredictable cues should be inhibitory. The onset of stimulatory environmental conditions terminates the inhibition, allowing rapid initiation of reproduction. As the primary hormone regulating water balance in birds, arginine vasotocin (AVT) appears a likely candidate to modulate reproduction in finches. Drought conditions cause sustained AVT release, which in other species inhibits androgen production. To determine whether increased AVT inhibits reproductive behavior, intact males were tested with females and divided into three groups matched for courtship behavior. Osmotic minipumps containing (a) saline, (b) 264 ng AVT, or (c) 1320 ng AVT in saline were implanted subcutaneously and males tested 48 h later. AVT-treated males socialized with females, but the high dose significantly reduced singing and courtship displays. To determine whether AVT acted by depressing androgen secretion, additional males were given subcutaneous androgen implants and divided into two groups matched for courtship behavior. Males were then implanted with minipumps containing (a) saline or (b) the high AVT dose. Males treated with AVT plus androgen showed no deficits in courtship behavior. These data suggest that AVT secretion during periods of drought may inhibit reproduction by inhibiting androgen production. Inhibition of reproductive behavior by AVT may be a more general phenomenon. Large quantities of AVT or, in mammals the closely-related peptide vasopressin (VP), are released when animals are stressed, and high levels of AVT/VP may inhibit reproductive behavior. The extremely short half-life of these peptides means that once proximal factors become more favorable, the gonads should rapidly be released from the peptides' inhibitory actions.