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Coleman, K., Tully, L. A., & McMillan, J. L. (2005). Temperament correlates with training success in adult rhesus macaques. Am. J. Primatol., 65(1), 63–71.
Abstract: In recent years there has been a marked increase in awareness of issues involving the psychological well-being of nonhuman primates (NHPs) used in biomedical research. As a result, many facilities are starting to train primates to voluntarily cooperate with veterinary, husbandry, and research procedures, such as remaining still for blood draws or injections. Such training generally reduces the stress associated with these procedures, resulting in calmer animals and, ultimately, better research models. However, such training requires great investments in time, and there can be vast individual differences in training success. Some animals learn tasks quickly, while others make slower progress in training. In this study, we examined whether temperament, as measured by response to a novel food object, correlated with the amount of time it took to train 20 adult female rhesus macaques to perform a simple task. The monkeys were categorized as “exploratory” (i.e., inspected a novel object placed in the home cage within 10 sec), “moderate” (i.e., inspected the object within 10-180 sec), or “inhibited” (i.e., did not inspect the object within 3 min). We utilized positive reinforcement techniques to train the monkeys to touch a target (PVC pipe shaped like an elbow) hung on their cage. Temperament correlated with training success in this study (Pearson chi2=7.22, df=2, P=0.03). We easily trained over 75% of the animals that inspected the novel food (i.e., exploratory or moderate individuals) to touch the target. However, only 22% of the inhibited monkeys performed the task. By knowing which animals may not respond to conventional training methods, we may be able to develop alternate training techniques to address their specific needs. In addition, these results will allow us to screen monkeys to be assigned to research projects in which they will be trained, with the goal of obtaining the best candidates for those studies.
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Dindo, M., & De Waal, F. B. M. (2007). Partner effects on food consumption in brown capuchin monkeys. Am. J. Primatol., 69(4), 448–456.
Abstract: It has been claimed that capuchin monkeys (Cebus apella) show inequity aversion in relation to food rewards for a simple exchange task. However, other factors may affect the willingness of a monkey to consume foods of high or low value in the presence of a conspecific. In this study, pairs of monkeys were presented with unequally valued foods, but without any task-performance: they simply received the food under four experimental conditions. By looking at the rate of collection and consumption of low-valued cucumber slices we expected to see variation dependent on whether the partner either had 1) cucumber (equity), 2) grape (inequity), 3) inaccessible cucumber or 4) inaccessible grape. Testing 12 adult capuchin monkeys, our findings differed from those of other authors in that the monkeys failed to show negative reactions to inequity, but rather responded with scramble competition (i.e., fast food collection) in the presence of a conspecific without access to food. They also showed facilitated consumption in the presence of a conspecific consuming high-valued food. Possibly, (in)equity plays a different role if food serves as a reward for a task rather than if it is simply made available for consumption. Am. J. Primatol. 69:1-9, 2007. (c) 2006 Wiley-Liss, Inc.
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Brosnan, S. F., Freeman, C., & De Waal, F. B. M. (2006). Partner's behavior, not reward distribution, determines success in an unequal cooperative task in capuchin monkeys. Am. J. Primatol., 68(7), 713–724.
Abstract: It was recently demonstrated that capuchin monkeys notice and respond to distributional inequity, a trait that has been proposed to support the evolution of cooperation in the human species. However, it is unknown how capuchins react to inequitable rewards in an unrestricted cooperative paradigm in which they may freely choose both whether to participate and, within the bounds of their partner's behavior, which reward they will receive for their participation. We tested capuchin monkeys with such a design, using a cooperative barpull, which has been used with great success in the past. Contrary to our expectations, the equity of the reward distribution did not affect success or pulling behavior. However, the behavior of the partner in an unequal situation did affect overall success rates: pairs that had a tendency to alternate which individual received the higher-value food in unequal reward situations were more than twice as successful in obtaining rewards than pairs in which one individual dominated the higher-value food. This ability to equitably distribute rewards in inherently biased cooperative situations has profound implications for activities such as group hunts, in which multiple individuals work together for a single, monopolizable reward.
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Baker, K. C., Seres, E., Aureli, F., & De Waal, F. B. (2000). Injury risks among chimpanzees in three housing conditions. Am. J. Primatol., 51(3), 161–175.
Abstract: Meeting the psychological needs of chimpanzees (Pan troglodytes) can be a challenge given their aggressiveness on the one hand and the complexity of their social lives on the other. It is unclear how to balance the need to provide opportunities for species-appropriate behavior against potential risks of injury chimpanzees may inflict on each other. This study evaluates the suggestion that simpler social environments protect chimpanzees from wounding. Over a two-year period all visible injuries to 46 adult males, 64 adult females, and 25 immature chimpanzees were recorded at the Yerkes Regional Primate Research Center. Approximately half of the subjects were mother-reared, and the rest were nursery-reared. Housing included compounds containing about 20 chimpanzees, interconnected indoor-outdoor runs for groups of up to 12 individuals, and smaller indoor-outdoor runs for pairs and trios. Annual wounding rates were calculated for serious wounds (extensive injuries and all those requiring veterinary intervention) as well as for minor wounds. Compound-housed chimpanzees incurred the highest level of minor wounding, but serious wounding levels were not affected by housing condition. Even with a period of dominance instability and elevated levels of wounding in one compound, compound chimpanzees were not injured more than those in smaller social groups over the long term. Nursery-reared females in moderate-sized groups were wounded more than mother-reared females. Also, nursery-reared males and females were wounded less often when paired with mother-reared companions. Overall, this study indicates that maintaining chimpanzees in pairs and trios would not be an effective means for reducing injuries. The management of wounding in chimpanzee colonies is influenced more by the sex and rearing composition of a colony.
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Izar, P., Ferreira, R. G., & Sato, T. (2006). Describing the organization of dominance relationships by dominance-directed tree method. Am. J. Primatol., 68(2), 189–207.
Abstract: Methods to describe dominance hierarchies are a key tool in primatology studies. Most current methods are appropriate for analyzing linear and near-linear hierarchies; however, more complex structures are common in primate groups. We propose a method termed “dominance-directed tree.” This method is based on graph theory and set theory to analyze dominance relationships in social groups. The method constructs a transitive matrix by imposing transitivity to the dominance matrix and produces a graphical representation of the dominance relationships, which allows an easy visualization of the hierarchical position of the individuals, or subsets of individuals. The method is also able to detect partial and complete hierarchies, and to describe situations in which hierarchical and nonhierarchical principles operate. To illustrate the method, we apply a dominance tree analysis to artificial data and empirical data from a group of Cebus apella.
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Heistermann, M., Palme, R., & Ganswindt, A. (2006). Comparison of different enzyme-immunoassays for assessment of adrenocortical activity in primates based on fecal analysis. Am. J. Primatol., 68(3), 257–273.
Abstract: Most studies published to date that used fecal glucocorticoid measurements to assess adrenocortical activity in primate (and many nonprimate) species applied a specific cortisol or corticosterone assay. However, since these native glucocorticoids are virtually absent in the feces of most vertebrates, including primates, the validity of this approach has recently been questioned. Therefore, the overall aim of the present study was to assess the validity of four enzyme-immunoassays (EIAs) using antibodies raised against cortisol, corticosterone, and reduced cortisol metabolites (two group-specific antibodies) for assessing adrenocortical activity using fecal glucocorticoid metabolite (GCM) measurements in selected primate species (marmoset, long-tailed macaque, Barbary macaque, chimpanzee, and gorilla). Using physiological stimulation of the hypothalamo-pituitary-adrenocortical (HPA) axis by administering exogenous ACTH or anesthesia, we demonstrated that at least two assays detected the predicted increase in fecal GCM levels in response to treatment in each species. However, the magnitude of response varied between assays and species, and no one assay was applicable to all species. While the corticosterone assay generally was of only limited suitability for assessing glucocorticoid output, the specific cortisol assay was valuable for those species that (according to high-performance liquid chromatography (HPLC) analysis data) excreted clearly detectable amounts of authentic cortisol into the feces. In contrast, in species in which cortisol was virtually absent in the feces, group-specific assays provided a much stronger signal, and these assays also performed well in the other primate species tested (except the marmoset). Collectively, the data suggest that the reliability of a given fecal glucocorticoid assay in reflecting activity of the HPA axis in primates clearly depends on the species in question. Although to date there is no single assay system that can be used successfully across species, our data suggest that group-specific assays have a high potential for cross-species application. Nevertheless, regardless of which GC antibody is chosen, our study clearly reinforces the necessity of appropriately validating the respective assay system before it is used.
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Cooper, M. A., & Bernstein, I. S. (2002). Counter aggression and reconciliation in Assamese macaques (Macaca assamensis). Am. J. Primatol., 56(4), 215–230.
Abstract: Patterns of aggressive and affiliative behavior, such as counter aggression and reconciliation, are said to covary in the genus Macaca; this is referred to as the systematic variation hypothesis. These behavior patterns constitute a species dominance style. Van Schaik's [1989] socioecological model explains dominance style in macaques in terms of within- and between-group contest competition. Dominance style is also said to correlate with phylogeny in macaques. The present study was undertaken to examine phylogenetic and socioecological explanations of dominance style, as well as the systematic variation hypothesis. We collected data on counter aggression and reconciliation from a habituated group of Assamese macaques (Macaca assamensis) at the Tukeswari Temple in Assam, India. The proportion of agonistic episodes that involved counter aggression was relatively low. Counter aggression, however, occurred more often among males than among females, and it was most common when females initiated aggression against males. The conciliatory tendency for this group of Assamese macaques was 11.2%. The frequency of reconciliation was low for fights among males and for fights among females, but reconciliation was particularly rare for opposite-sexed opponents. Female social relationships were consistent with the systematic variation hypothesis, and suggest a despotic dominance style. A despotic dominance style in Assamese macaques weakens the correlation between dominance style and phylogeny in macaques, but it is not inconsistent with the socioecological model. Male-female relationships were not well explained by the despotic-egalitarian framework, and males may well have more tolerant social relationships than do females. Sex differences need to be considered when categorizing species according to dominance style.
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Mallavarapu, S., Stoinski, T. S., Bloomsmith, M. A., & Maple, T. L. (2006). Postconflict behavior in captive western lowland gorillas (Gorilla gorilla gorilla). Am. J. Primatol., 68(8), 789–801.
Abstract: 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.
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Maninger, N., Capitanio, J. P., Mendoza, S. P., & Mason, W. A. (2003). Personality influences tetanus-specific antibody response in adult male rhesus macaques after removal from natal group and housing relocation. Am. J. Primatol., 61(2), 73–83.
Abstract: Previous research has suggested that personality is related to immune function in macaques. Using a prospective design, we examined whether variation in the personality dimension “Sociability” in adult male rhesus macaques (Macaca mulatta) was related to the in vivo secondary antibody response to a tetanus toxoid booster immunization following removal from natal groups and relocation to individual housing. We also explored whether the timing of the immunization following relocation had an impact on the immune response. Blood was sampled at the time of booster immunization, at 14 and 28 days post-immunization, and approximately 9 months post-immunization. Plasma was assayed for tetanus-specific IgG by enzyme-linked immunoassay (ELISA). There was no difference between High- and Low-Sociable animals in antibody levels at the time of the booster immunization. Multivariate analysis of variance (MANOVA) revealed that High-Sociable animals had a significantly higher antibody response following relocation and immunization compared to Low-Sociable animals. There was no effect of timing of the immunization on the immune response. The results confirm that personality factors can affect animals' immune responses, and that the dimension Sociability may be influential in a male's response to social separation and relocation.
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Koski, S. E., Koops, K., & Sterck, E. H. M. (2007). Reconciliation, relationship quality, and postconflict anxiety: testing the integrated hypothesis in captive chimpanzees. Am. J. Primatol., 69(2), 158–172.
Abstract: Reconciliation is a conflict resolution mechanism that is common to many gregarious species with individualized societies. Reconciliation repairs the damaged relationship between the opponents and decreases postconflict (PC) anxiety. The “integrated hypothesis” links the quality of the opponents' relationship to PC anxiety, since it proposes that conflicts among partners with high relationship quality will yield high levels of PC anxiety, which in turn will lead to an increased likelihood of reconciliation. We tested the integrated hypothesis in captive chimpanzees (Pan troglodytes) in the Arnhem Zoo, The Netherlands. We applied the standard PC/matched control (MC) method. Our results mostly support the integrated hypothesis, in that more valuable and compatible partners (i.e., males and frequent groomers) reconciled more often than less valuable and weakly compatible partners (i.e., females and infrequent groomers). In addition, PC anxiety was higher after conflicts among males than among females. Emotional arousal thus appears to be a mediator facilitating reconciliation. However, in contrast to the predictions derived from the integrated hypothesis, PC anxiety appeared only in aggressees, and not in aggressors, of conflicts. This suggests that while relationship quality determines PC anxiety, it is dependent on the role of the participants in the conflict.
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