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Ostner, J.

Publications and source records attributed to Ostner, J..

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Testosterone and cortisol are negatively associated with ritualized bonding behavior in male macaques

Neuroendocrine research on the formation of social bonds has primarily focused on the role of nonapeptides. However, steroid hormones often act simultaneously to either inhibit or facilitate bonding. Testosterone is proposed to mediate a trade-off between male mating effort and nurturing behavior; therefore, low levels are predicted during periods of nurturing infant care and social bonding. In species where social bonding and support regulates hypothalamic-pituitary-adrenal axis activity, we also expect glucocorticoid levels to be low during bonding periods. We investigated how immunoreactive urinary testosterone (iuT) and cortisol (iuC) were related to triadic male-infant-male interactions - a ritualized male bonding behavior - as well as infant care in male Barbary macaques (Macaca sylvanus). We collected >3000 hours of behavioral observation data during full-day focal animal follows from 14 adult males and quantified iuT and iuC from 650 urine samples. As predicted, both iuT and iuC were negatively correlated with rates of triadic interactions within-subjects in the hours preceding urination. We found no relationship between iuT and iuC with triadic interactions between-subjects. Infant care was weakly positively correlated to iuT and iuC within-subjects, but not between-subjects. The observed negative relationship between iuT and triadic interactions may be beneficial to lower competitive tendencies between adult males and to not inhibit bond formation. Lowered iuC could reflect increased bonding and perceived social support as triadic interactions predict future coalition formation in this species. Additionally, lowered iuC may be reflective of buffered tensions between males. The positive relationship of iuT and iuC with infant care suggests that the handling of infants in may be less nurturing but rather protective or competitive in this species. Measuring steroid hormones in relation to bonding and nurturing can help us interpret behaviors within the ecological contexts that they occur.

animal behavior and cognition

Female Assamese macaques bias their affiliation to paternal and maternal kin

Forming strong social bonds leads to higher reproductive success, increased longevity and/or increased infant survival in several mammal species. Given these adaptive benefits, understanding what determines partner preferences in social bonding is important. Maternal relatedness strongly predicts partner preference across many mammalian taxa. Although paternal and maternal kin share the same number of genes, and theoretically similar preferences would therefore be expected for paternal kin, the role of paternal relatedness has received relatively little attention. Here, we investigate the role of maternal and paternal relatedness for female bonding in Assamese macaques (Macaca assamensis), a species characterized by a relatively low male reproductive skew. We studied a wild population under natural conditions using extensive behavioural data and relatedness analyses based on pedigree reconstruction. We found stronger social bonds and more time spent grooming between maternal kin and paternal half-sisters compared to non-kin, with no preference of maternal over paternal kin. Paternally related and non-related dyads did not form stronger bonds when they had less close maternal kin available, however we would need a bigger sample size to confirm this. As expected given the low reproductive skew, bonds between paternal half-sisters closer in age were not stronger than between paternal half-sisters with larger age differences, suggesting that age similarity was not the mechanism by which paternally related individuals recognized each other. An alternative way through which paternal kin could get familiarized is mother- and/or father-mediated familiarity.

animal behavior and cognition

Oxytocin increases after affiliative interactions in male Barbary macaques

Mammals living in stable social groups often mitigate the costs of group living through the formation of social bonds and cooperative relationships. The neuropeptide hormone oxytocin (OT) has been proposed to promote both bonding and cooperation although only a limited number of studies have investigated this under natural conditions. Our aim was to assess the role of OT in bonding and cooperation in male Barbary macaques (Macaca sylvanus). First we tested for an effect of affiliation - grooming and triadic male-infant-male interactions - with bond and non-bond partners on urinary OT levels. Secondly we aimed to test whether grooming interactions (and thus increased OT levels) increase a males general propensity to cooperate in polyadic conflicts. We collected behavioral data via full-day focal animal protocols on 14 adult males and measured endogenous OT levels from 139 urine samples collected after affiliation and non-social control periods. Urinary OT levels were higher after grooming with any partner. By contrast, OT levels after male-infant-male interactions with any partner or with bond partners were not different from controls but were higher after interactions with non-bond partners. Previous grooming did not increase the likelihood of males to support others in conflicts. Collectively, our results support research indicating that OT is involved in the regulation of adult social bonds, including in non-reproductive contexts. However, our male-infant-male interaction results go against previous studies suggesting that it is affiliation with bond rather than non-bond partners that trigger the release of OT. Alternatively, OT levels may have been elevated prior to male-infant-male interactions thus facilitating interaction between non-bond partners. The lack of an association of grooming (and by extension increased OT levels) and subsequent support speaks against an OT linked increase in the general propensity to cooperate, yet further studies are needed for a more direct test including the possibility of partner-specific contingent cooperation.

animal behavior and cognition

Personality homophily affects male social bonding in wild Assamese macaques (Macaca assamensis)

Animal social bonds are defined as stable, equitable and strong affiliative and cooperative relationships similar to human friendships. Just as human friendships, social bonds are thought to function as alliances that generate adaptive benefits via support in critical situations. In humans, similarity in many sociodemographic, behavioural and intrapersonal characteristics leads to trust and is predictive of friendships. Specifically, personality homophily, that is the tendency of individuals to form social bonds with others who have a similar personality, may increase predictability and facilitate trust and reciprocity among partners with compatible behavioural tendencies. While evidence for social bonding in nonhumans is accumulating, far less is known about its predictors. Here, personality homophily effects on the formation and maintenance of social bonds are shown in twenty-four wild male Assamese macaques (Macaca assamensis), at Phu Khieo Wildlife Sanctuary, Thailand. Dyadic bond strength increased with increased similarity in the trait Connectedness (i.e. frequent and diverse neighbours in 5m proximity and pronounced social tolerance, as high rates of friendly approaches to and by others). To differentiate whether homophily indeed predicted bond formation or whether bonded males personalities became more similar over time, we tested the stability of the connectedness traits in a subset of immigrating males that had to form new bonds. Connectedness in these males remained stable suggesting that males do not adapt their personality to their partner. Our results support the idea of a shared evolutionary origin of homophily as a partner choice strategy in human and non-human animals. The main selective advantage of personality similarity in animal social bonds may result from a more reliable cooperation among individuals with similar cooperative behavioural tendencies.

animal behavior and cognition

Measuring urinary cortisol and testosterone levels in male Barbary macaques: A comparison of EIA and LC-MS

The development of methods to quantify hormones from non-invasively collected samples such as urine or feces has facilitated endocrinology research on wild-living animals. To ensure that hormone measurements are biologically meaningful, method validations are highly recommended for each new species or sample matrix. Our aim was to validate three commonly used enzyme immunoassays (EIA), one for analysis of cortisol and two for analysis of testosterone, to assess adrenocortical and gonadal activity, respectively, from the urine of male Barbary macaques. We compared EIA and liquid chromatography-mass spectrometry (LC-MS) results to determine if the EIA measurements truly reflect levels of the target hormone and to determine if cross-reactivities with other steroids were potentially confounding results. Furthermore, we conducted a biological validation of testosterone to ensure that both EIA and LC-MS were able to capture physiologically meaningful differences in hormone levels. We found that cortisol measured by EIA correlated strongly with cortisol measured by LC-MS in both adult and immature males, without the need for deconjugation of steroids in the urine. Both testosterone EIAs correlated strongly with LC-MS in adult males, but only if steroids in the urine were deconjugated by enzymatic hydrolysis prior to analysis. However, in immature males, EIA and LC-MS results did not correlate significantly. Further correlation analyses suggest this is likely due to cross-reactivity of the testosterone antibody with other adrenal steroids such as cortisol, DHEA, and likely others, which are present at much higher concentrations relative to testosterone in immature males. Testosterone levels were significantly higher in adult compared to immature males as measured by LC-MS but not as measured by EIA. Taken together, our results suggest that the testosterone EIAs are suitable to assess gonadal activity in adult but not immature males, and only if a hydrolysis of the urine is conducted prior to analysis.

physiology