Gabriele Schino

A modest proposal: displacement activities as an indicator of emotions in primates

Abstract Displacement activities are behaviour patterns (mostly body care activities) characterized by their apparent irrelevance to the situation in which they appear. Scratching, autogrooming, yawning and body shaking are among the most commonly reported displacement activities in non-human primates. A review of the primate literature indicates that displacement activities tend to occur in situations of psychosocial stress and that their frequency of occurrence is affected by anxiogenic and anxiolytic drugs. In the light of this evidence, it is suggested that displacement activities can be used as indicators of emotional states arising in a variety of primate social interactions. Methodological problems associated with such a use are discussed. The hypothesis that displacement activities may also have a communicative function in non-human primates is not supported adequately by available data.

Grooming, competition and social rank among female primates: a meta-analysis

Abstract Seyfarth (1977, Journal of Theoretical Biology,65, 671–698) proposed a model of social grooming among female monkeys that has had an enormous influence in the primatological literature. To test this model, I reviewed published data on primate grooming behaviour, using meta-analytical techniques. An analysis of grooming behaviour in 27 different social groups belonging to 14 different species revealed that a significant role in the distribution of grooming was played by attraction to high-ranking animals, attraction to kin and competition for grooming partners. These results confirm the majority of the predictions of the model. The need for more observational data on grooming (and other affiliative interactions) in New World monkeys, and experimental data on the relations between the exchange of grooming and the formation of agonistic alliances, is emphasized.

Primate displacement activities as an ethopharmacological model of anxiety

Using a within-subject cross-over, vehicle-controlled design, we investigated the acute effects of benzodiazepine receptor ligands with different mechanisms of action on the displacement activities (scratching, self-grooming, and body shake) of seven male macaques living in social groups. Our aim was to test the discriminative validity of displacement activities as an ethopharmacological model of anxiety. Subjects were given i.m. lorazepam (0.10, 0.20, 0.25 mg/ kg) and FG 7142 (0.1, 0.3, 1.0 mg/kg). The frequency of displacement activities was decreased by the anxiolytic lorazepam and increased by the anxiogenic FG 7142 in a dose-dependent manner. Displacement activities were apparently more sensitive to anxiolytic treatment than other behavior patterns indicative of an anxiety state (i.e., visual scanning of the social environment and fear responses directed to dominant males). These results suggest that primate displacement activities are a valid ethopharmacological model of anxiety.

Grooming reciprocation among female primates: a meta-analysis

The theory of reciprocal altruism offers an explanation for the evolution of altruistic behaviours among unrelated animals. Among primates, grooming is one of the most common altruistic behaviours. Primates have been suggested to exchange grooming both for itself and for rank-related benefits. While previous meta-analyses have shown that they direct their grooming up the hierarchy and exchange it for agonistic support, no comprehensive evaluation of grooming reciprocation has been made. Here we report on a meta-analysis of grooming reciprocation among female primates based on 48 social groups belonging to 22 different species and 12 genera. The results of this meta-analysis showed that female primates groom preferentially those group mates that groom them most. To the extent allowed by the availability of kinship data, this result holds true when controlling for maternal kinship. These results, together with previous findings, suggest that primates are indeed able to exchange grooming both for itself and for different rank-related benefits.

The relative roles of kinship and reciprocity in explaining primate altruism

Several hypotheses have been proposed to explain the evolution of altruistic behaviours. Their relative roles in explaining actual cases of animal altruism are, however, unclear. In particular, while kin selection is widely believed to have a pervasive influence on animal behaviour, reciprocity is generally thought to be rare. Despite this general agreement, there has been no direct test comparing the relative roles of kinship and reciprocity in explaining animal altruism. In this paper, we report on the results of such a test based on a meta-analysis of allogrooming in primates, grooming being probably the most common altruistic behaviour among mammals. In direct contrast to the prevailing view, reciprocity played a much larger role than kinship in explaining primate allogrooming. These results point to a more significant role of reciprocity in the evolution of animal altruism than is generally acknowledged.

Fitness‐related benefits of dominance in primates

Dominance hierarchies are thought to provide various fitness-related benefits to dominant individuals (e.g., preferential access to food or mating partners). Remarkably, however, different studies on this topic have produced contradictory results, with some showing strong positive association between rank and fitness (i.e., dominants gain benefits over subordinates), others weak associations, and some others even revealing negative associations. Here, we investigate dominance-related benefits across primate species while controlling for phylogenetic effects. We extracted data from 94 published studies, representing 25 primate species (2 lemur species, 4 New World monkeys, 16 Old World monkeys, and 3 apes), to assess how dominance affects life-history and behavior. We used standard and phylogenetic meta-analyses to analyze the benefits of dominance in primates. Dominant females had higher infant survival to first year, although we found no significant effect of dominance on female feeding success. Results for female fecundity differed between the two meta-analytical approaches, with no effect of dominance on female fecundity after controlling for phylogeny. Dominant males had a higher fecundity and mating success than subordinate males. Finally, the benefits of dominance for female fecundity were stronger in species with a longer lifespan. Our study supports the view that dominance hierarchies are a key aspect of primate societies as they indeed provide a number of fitness-related benefits to individuals.

MEASURING ANXIETY IN NONHUMAN PRIMATES : EFFECT OF LORAZEPAM ON MACAQUE SCRATCHING

Lorazepam (0.2 mg/kg IM) was given to group-living female macaques to assess the effect of anxiolytic treatment on scratching, a behavior pattern referred to as a displacement activity in the primate literature. Lorazepam selectively diminished scratching behavior. The drug effect was status-dependent: especially low-ranking animals showed a marked reduction in scratching. Lorazepam exerted a direct effect on scratching, that is the effect was not due to sedation or mediated by the influence of the drug on other behaviors. These results provide pharmacological validation to the ethological finding that scratching may be a manifestation of anxiety in monkeys. In addition, they suggest to use scratching as a behavioral measure in studies investigating nonhuman primate models of anxiety.

Scratching as a behavioral index of anxiety in macaque mothers

The aim of this study was to assess the validity of the notion that anxiety influences maternal style in monkeys. To this end, we investigated the correlations between measures of the quality of mother-infant relationship and scratching, a behavior pattern that reflects a state of anxiety. The subjects were seven group-living macaque mothers and their infants observed during the first 12 weeks postpartum. Postpartum scratching by the mothers was positively correlated with both maternal possessiveness and maternal warmth, two composite measures of the quality of mother-infant relationship that reflect a possessive and attentive maternal style. Evaluation of the correlations between maternal rank and scratching before and after parturition indicated that interactions with their infants, not those with other group companions, were the main source of anxiety for the mothers. These results support the notion that anxiety influences maternal style in monkeys and suggest that studies aimed at investigating physiological and social correlates of maternal emotionality in nonhuman primates could use scratching as a useful and simple behavioral measure.

Intragroup Variation in Conciliatory Tendencies in Captive Japanese Macaques

Nonhuman primates have been observed to exchange friendly gestures soon after an agonistic episode, a behaviour labelled reconciliation. Frequency of reconciliation has been shown to vary both within and between primate groups. This study used both univariate and multivariate analyses to investigate intragroup variation in the frequency of reconciliation in captive Japanese macaques (Macaca fuscata). Frequency of reconciliation was lower during the mating season, and was also affected by the intensity of aggression and by the sex and age combination of the opponents. On the contrary, outcome of aggression and number of aggressors did not influence the frequency of reconciliation. Kin reconciled more than nonkin, and individuals with a good social relationship reconciled more than those with a bad or weak relationship. The effects of kinship and relationship quality appeared to be independent since among individuals with a good relationship, kin reconciled more than nonkin, while among nonkin, individuals with a good relationship reconciled more than those with a bad or weak relationship. Our results show that Japanese macaques are highly flexible in their conciliatory behaviour, and highlight a possible role of reconciliation in the negotiation and management of primate social relationships.

Primate Reciprocity and Its Cognitive Requirements

Humans can engage in relatively indiscriminate altruistic behaviors such as donating money to charities, giving blood, and volunteering to review scientific papers. They also live in societies characterized by examples of cooperation of unmatched complexity, such as organized armies, the cooperative building of infrastructures such as roads and railways, and tax‐paying, among others. (We exclude, of course, the “anonymous” societies of some social insects in which the animals themselves are not aware of the cooperative roles they play.) The emphasis on these unique aspects of our behavior 1 has sometimes distracted scientists from paying attention to the more common aspects of our daily lives, which share characteristics with those of our fellow primates. We invite friends for dinner, console others after a loss, intervene in ongoing fights, and even groom others. 2–4 These small acts of altruism, which constitute a large part of our daily social life, tend to resemble those of nonhuman primates.