Evidence of social learning in black-and-white ruffed lemurs (Varecia variegata).

Although many studies have examined social learning capabilities in apes and monkeys, experiments involving prosimians remain largely absent. We investigated the potential for social learning in black-and-white ruffed lemurs using a two-action foraging task. Eight individuals were divided into two experimental groups and exposed to conspecifics using one of two techniques to access food. Subjects were then given access to the apparatus and their retrieval techniques were recorded and compared. All subjects made their first retrieval using the technique they observed being demonstrated, and there were significant differences between the two groups in their overall response patterns. These results suggest that prosimians are capable of social learning and that additional long-term field studies may reveal the presence of behavioural traditions similar to those found in other primates.

Male-immature relationships in multi-male groups of mountain gorillas (Gorilla beringei beringei).

We examined the pattern and possible functions of social interactions between adult males and immatures in three free-ranging, multi-male groups of mountain gorillas (Gorilla beringei beringei). Previous studies conducted during the 1970s when groups contained one to three adult males concluded that male-immature relationships were likely to be a form of low-cost paternal investment [Stewart, Mountain gorillas: three decades of research at Karisoke. Cambridge, UK: Cambridge University Press, 2001]. We evaluated whether this hypothesis still held in groups containing six to nine adult males, or if male-immature relationships might serve other functions (e.g. mating effort, kin selection, or alliance building). Overall, we found that immatures spent the most time near, and interacted most with, the alpha silverback. These behaviors peaked during the period when infants were still quite vulnerable but increasing their independence from their mothers. Such findings suggest that parenting effort remains the primary function of male-immature relationships; however, there is some evidence for the mating effort hypothesis as well.

Group structure predicts variation in proximity relationships between male-female and male-infant pairs of mountain gorillas (Gorilla beringei beringei).

Relationships between conspecifics are influenced by both ecological factors and the social organization they live in. Systematic variation of both--consistent with predictions derived from socioecology models--is well documented, but there is considerable variation within species and populations that is poorly understood. The mountain gorilla (Gorilla beringei) is unusual because, despite possessing morphology associated with male contest competition (e.g., extreme sexual dimorphism), they are regularly observed in both single-male and multimale groups. Both male-female and male-infant bonds are strong because males provide protection against infanticide and/or predation. Risk of these threats varies with social structure, which may influence the strength of social relationships among group members (including females and offspring, if females with lower infant mortality risk are less protective of infants). Here, we investigate the relationship between group structure and the strength of proximity relationships between males and females, males and infants, and females and offspring. Data come from 10 social groups containing 1-7 adult males, monitored by the Dian Fossey Gorilla Fund's Karisoke Research Center in Volcanoes National Park, Rwanda. After controlling for group size and infant age, association strength was similar for male-female pairs across group types with both dominant and nondominant males, but male-infant relationships were strongest in single-male groups where paternity certainty was high and animals had fewer social partners to choose from. The male:female and male:infant ratios better predicted both male-female and male-infant associations than the absolute number of males, females, or infants did. The fewer the number of males per female or infant, the more both pair types associated. Dominant males in groups containing fewer males had higher eigenvector centrality (a measure of importance in a social network) than dominant males in groups with more males. Results indicate that nondominant males are an important influence on relationships between dominant males and females/infants despite their peripheral social positions, and that relationships between males and infants must be considered an important foundation of gorilla social structure.

Validating faecal glucocorticoid metabolite analysis in the Virunga mountain gorilla using a natural biological stressor.

The continued degradation of primate habitat worldwide is forcing many primate populations into small protected forest islands surrounded by high-density human populations. One well-studied example is the critically endangered mountain gorilla (Gorilla beringei beringei). Decades of monitoring and research on Rwanda's mountain gorillas offer a unique opportunity to use non-invasive endocrine analysis to address pressing questions about the conservation of this endangered population. The aims of our study were as follows: (i) to validate field and laboratory methods for assessing stress through faecal glucocorticoid metabolite (FGM) analysis using inter-social unit interactions as a natural stressor; (ii) to determine the excretion lag times between interactions and detectable stress response in faeces; and (iii) to determine whether there are circadian patterns of FGM excretion. We collected ~6000 faecal samples from 127 known gorillas in 10 habituated groups, monitored by the Dian Fossey Gorilla Fund's Karisoke Research Center over 21 months in 2011 and 2012. Extracted FGMs were measured using a cortisol enzyme immunoassay (R4866; C. J. Munro). Results revealed cause-effect relationships between inter-unit interactions and increased FGMs (relative to individual pre-event samples) between 20 and 140 h after interactions, with the peak most often occurring on day 3. There was no evidence of circadian patterns in FGM concentrations, as previously shown in many species with long gut passage times. However, baseline FGM concentrations were lower in adult males than in adult females, and variation was associated with the collection month, indicating possible seasonal variation. This study provides a biologically validated, field-friendly faecal hormone metabolite extraction and laboratory enzyme immunoassay analysis method for non-invasive monitoring of adrenocortical activity in Virunga mountain gorillas. The methods are useful for future evaluation of a variety of environmental and human-induced potential stressors in this critically endangered population.

Imitative learning by captive western lowland gorillas (Gorilla gorilla gorilla) in a simulated food-processing task.

Although field studies have suggested the existence of cultural transmission of foraging techniques in primates, identification of transmission mechanisms has remained elusive. To test experimentally for evidence of imitation in the current study, we exposed gorillas (Gorilla gorilla gorilla) to an artificial fruit foraging task designed by A. Whiten and D. M. Custance (1996). Gorillas (n=6) watched a human model remove a series of 3 defenses around a fruit. Each of the defenses was removed using 1 of 2 alternative techniques. Subsequent video analysis of gorillas' behavior showed a significant tendency to copy the observed technique on 1 of the individual defenses and the direction of removal on another defense. This is the first statistically reliable evidence of imitation in gorillas. Sequence of defense removal was not replicated. The gorillas' responses were most similar to those of chimpanzees.

A preliminary study of the behavioral effects of feeding enrichment on African elephants.

Although commonly practiced with many species, feeding enrichment in elephants is understudied. The behavioral effects of feeding enrichment were tested in three African elephants by substituting an equal dry weight of browse for hay in an ABA design. The results showed a significant increase in feeding and significant decreases in drinking and inactivity when the browse was present. Additionally, changes in feeding, inactivity, and time spent in contact were observed outside the time the browse was actually presented, although the relationship of these changes to the experimental methodology is unknown. A significant increase in visibility to zoo visitors during the browse conditions demonstrates that browse is an effective, naturalistic method for increasing visibility as well as species-typical behaviors. Managers of captive elephants should consult with a nutritionist to address issues of energetics, nutritional content, and secondary compounds when using browse as feeding enrichment. Zoo Biol 19:485-493, 2000. Copyright 2000 Wiley-Liss, Inc.

A preliminary behavioral comparison of two captive all-male gorilla groups.

Gorillas live in polygamous harem groups, generally composed of one male, several adult females, and their offspring. With an equal numbers of male and female gorillas born in captivity, however, housing gorillas in social breeding units inevitably means that some males will not have access to female social partners. Thus, the future of the captive gorilla population depends on the collective ability of zoos to house equal numbers of males and females. This study examined the behavioral profiles of two all-male groups of captive lowland gorillas (Gorilla gorilla gorilla) to provide information on this type of housing situation. One group consisted of three subadult individuals, while the other consisted of two subadults and a silverback. Data were collected during two 6-month intervals, for a total of 284 hr. The behavioral profiles of the animals were stable over the course of the study but proximity patterns changed. Differences in feeding, solitary play, and object-directed behavior were found between groups, while no significant differences were observed in affiliative or agonistic social behavior. At both institutions, group cohesion appeared to be high, particularly between subadults; these individuals spent approximately 10% of their time engaging in social behavior and 25-50% of their time in close proximity (within 5 m). However, the Zoo Atlanta males spent significantly more time within 1 m and 5 m of each other than the Santa Barbara males, which may reflect a higher level of cohesiveness among members of the Zoo Atlanta group. The behavioral profiles of the animals in this study were similar to those found in bachelor groups of wild mountain gorillas. One notable exception was the absence of homosexual behavior between the silverback and subadults in Santa Barbara and the low frequency of this behavior between subadults in both groups. Although more longitudinal data are needed, these data suggest that all-male groups can be a feasible housing strategy for males at certain periods of their life span. Zoo Biol 20:27-40, 2001. Copyright 2001 Wiley-Liss, Inc.

Postconflict behavior in captive western lowland gorillas (Gorilla gorilla gorilla).

Postconflict (PC) behaviors, including reconciliation and consolation, have been observed in many primate and several nonprimate species. Using the PC-matched control (MC) method, PC behavior was examined in two groups (n=13) of captive western lowland gorillas, a species for which no conflict resolution data have been published. Analyses of 223 conflicts showed significantly more affiliation between former opponents after a conflict when compared to control periods, indicating reconciliation. Results also showed significantly more affiliation between the victim and a third-party after a conflict, indicating consolation. Both solicited and unsolicited consolation were observed. The majority of the affiliative interactions observed for both reconciliation and consolation were social proximity, which suggests that unlike most nonhuman primates, proximity, rather than physical contact, may be the main mechanism for resolving conflicts in western lowland gorillas. PC behavior was not uniform throughout the groups, but rather varied according to dyad type.

Changes in locomotor and foraging skills in captive-born, reintroduced golden lion tamarins (Leontopithecus rosalia rosalia).

The behavior of reintroduced, captive-born animals is understudied, limiting the scientific understanding and utility of reintroduction as a conservation tool. This work describes changes in locomotor and foraging behaviors in captive-born golden lion tamarins over the first 18 months after their release into the wild. The subjects included 73 individuals living in and around the Poco das Antas Biological Reserve in Brazil between 1984 and 1996. The differences between animals that survived 6 months after release and those that did not indicate that initial deficiencies in locomotor and foraging abilities are related to survival. Behavioral changes in both juvenile and adult individuals during the first 6 and 18 months after release appear to be primarily related to locomotor abilities; however, the effect of provisioning on foraging abilities is unknown. Juvenile animals showed a larger number of changes relative to adults during the first 6 and 18 months, suggesting that placing tamarins into complex environments early in development may promote the expression of natural behaviors and increase survival opportunities after their release. However, when this is not possible, the best mechanism for reintroducing adult members of this species involves intensive post-release support rather than pre-release training, which confers few behavioral advantages. Recommendations for future reintroductions with this and other species include introducing animals to complex environments early in development, and collecting data systematically.

Proximity patterns of female western lowland gorillas (Gorilla gorilla gorilla) during the six months after parturition.

Studies of wild mountain gorillas have demonstrated strong preferences among new mothers for the silverback. Protection against infanticide has been theorized to be the primary cause for this attraction. We examined social partner preferences in captive western lowland mothers during the 6 mo after parturition and found that juveniles and females were the primary members of the new mothers' social network. Mothers spent significantly more time in close proximity with both of these subgroups than with the silverback. Proximity patterns changed over time: new mothers spent more time near females in the month after parturition than in the month prior to parturition, and spatial proximity increased again in months 2-6 postparturition. These findings differ from those reported for wild mountain gorillas, which may reflect the lack of infanticide risk in captivity. Given current hypotheses that infanticide may be a limited in western lowland gorillas, the social partner preferences observed here may be indicative of patterns in wild populations.