Effects of Tourist and Researcher Presence on Fecal Glucocorticoid Metabolite Levels in Wild, Habituated Sulawesi Crested Macaques (Macaca nigra).

Ecotourism managers and researchers often assume that apparently habituated primate groups no longer experience adverse consequences of prolonged exposure to tourists or researchers. We examined the effects of tourists and researchers on fecal glucocorticoid metabolite output (FGCM) in three critically endangered, wild crested macaque (Macaca nigra) groups in Tangkoko Nature Reserve, Sulawesi, Indonesia. We assayed FGCM from 456 fecal samples collected from thirty-three adults. Tourists can walk through and among macaque groups freely. Hence, we examined the possible effects of tourists both (1) in the reserve when away and not interacting with the study groups and (2) when they were present within the macaque groups. Generalized Linear Mixed Model (GLMM) analysis indicated that when tourists were present in the forest, but not directly among the macaques, FGCM levels in the macaque tourism groups were higher in months with more tourists. When tourists were among the macaque groups, some female macaques experienced rises and subsequent postexposure decreases in FGCM levels, consistent with predictions for acute stress. Male FGCM levels increased with tourist numbers within the group. Nevertheless, they were not significantly different from levels during undisturbed or postexposure conditions. FGCM responses related to researchers in groups varied by group, sex, and tourist presence. However, the temporal patterning of FGCM responses showed little evidence of chronic stress from tourism at this site.

Monkey business: A girl's once strange dream.

For close to 50 years, my research has focused on social relationships and social structure, particularly in macaques, and has been marked by a gradual broadening of scope. Supported by open-minded parents, I followed a once unconventional path into field primatology largely by ignoring distinct gender-based ideas about appropriate occupations for women that were prevalent when I was a child. Later, as Robert Hinde's PhD advisee, I benefited enormously from his mentoring and from the transformative experience he provided. I began by examining infant social development in free-ranging rhesus monkeys and the integration of infants into the kinship and dominance structures of their groups. I gradually branched out to look at (1) kinship and dominance in additional age classes and macaque species, (2) additional aspects of social structure (reciprocity, agonistic support, tolerance, cooperation, conflict management), (3) mechanisms and organizing principles (e.g., attraction to kin and high rank, intergenerational transmission, demography, reciprocity, social style, time constraints) and (4) evolutionary underpinnings of social relationships and structure (e.g., parental investment, kin selection, socioecology, phylogeny, biological markets). For much of this journey, I have been accompanied by talented PhD students who have enriched my experience and whom I am now proud to call colleagues and friends. It is gratifying to realize that my career choice is no longer considered as unconventional as it once was.

Cortisol metabolites vary with environmental conditions, predation risk, and human shields in a wild primate, Cercopithecus albogularis.

Environmental challenges are often associated with physiological changes in wildlife that allow animals to maintain homeostasis. Among these, scarcity in resources, and risks from predators, competitors, and humans can all result in psychological and physiological stress. Yet, for habituated species, it is not clear whether this relationship with humans still holds to a lesser degree or is outweighed by the benefits of human presence - such as serving as a buffer from competitors or predators. We investigated how human presence and environmental challenges such as resource availability, weather, predation, and competition may be associated with variation in fecal cortisol metabolite levels (FCMs) in a group of samango monkeys (Cercopithecus albogularis) in the Soutpansberg Mountains, South Africa. FCMs can often broadly track environmental challenges and perturbations. Initially, we employed an exploratory analysis comparing candidate models representing biological hypotheses and found that those incorporating information on human presence had less weight than models for food availability, thermoregulation, and water scarcity. When we examined a subset of the data that included information on intergroup competition and predator alarm calls, we found that FCMs were higher on the day following potential predator encounters but not competitive interactions. As observer numbers increased, responses to predators flattened, indicating that the presence of several humans might deter predators and/or affect samangos' perception of danger - yet we could not distinguish between these possibilities. Together, these results suggest that ecological perturbations track with FCMs in this study population and challenge long-held assumptions that human presence has negligible effects on habituated study animals.

Female preferences for male golden snub-nosed monkeys vary with male age and social context.

Age is a key factor affecting sexual selection, as many physical and social traits are age-related. Although studies of primate mate choice often consider particular age-related traits, few consider the collective effects of male age. We tested the hypothesis that female golden snub-nosed monkeys Rhinopithecus roxellana prefer prime aged males (10-15 years) over younger and older males. We examined a habituated, provisioned troop during a 3-year study in the Qinling Mountains, China. Prime age males were more likely to be resident males of 1-male units (OMUs) than males of other ages. Since females are free to transfer between OMUs, the number of females per OMU can be indicative of female preferences. We examined the number of females per OMU, and found that it increased with resident male age up to 7-8 years, and declined after 12 years, such that prime age resident males had more females than other resident males. Females also initiated extra-unit copulations with high-ranking prime age males at significantly higher rates than with other males. Nevertheless, females tended to transfer from OMUs with high-ranking, older resident males to those with low-ranking, younger resident males. Thus, females appear to use different strategies when choosing social mates and extra-unit mates (i.e., different social contexts). We speculate that females may perceive early signs of aging in males and trade off the benefits and costs of high rank versus male senescence. This study lays the groundwork for future studies that examine possible direct and indirect benefits of such strategies.

Anthropogenic influences on primate antipredator behavior and implications for research and conservation.

Predation risk affects prey species' behavior, even in the absence of a direct threat, but human-induced environmental change may disturb ecologically significant predator-prey interactions. Here, we propose various ways in which knowledge of antipredator tactics, behavioral risk effects, and primate-predator interactions could assist in identifying human-caused disruption to natural systems. Using behavior to evaluate primate responses to the ongoing environmental change should be a potentially effective way to make species conservation more predictive by identifying issues before a more dramatic population declines. A key challenge here is that studies of predation on primates often use data collected via direct observations of habituated animals and human presence can deter carnivores and influence subjects' perception of risk. Hence, we also review various indirect data collection methods to evaluate their effectiveness in identifying where environmental change threatens wild species, while also minimizing observer bias.

Time matching between grooming partners: Do methodological distinctions between short versus long-term reciprocation matter?

Primatologists have long focused on grooming exchanges to examine aspects of social relationships, co-operation, and social cognition. One particular interest is the extent to which reciprocating grooming partners time match, and the time frame over which they do so. Conclusions about time matching vary across species. Generally, researchers focus on the duration of pauses between grooming episodes that involve a switch in partner roles and choose a cut-off point to distinguish short from longer-term reciprocation. Problematically, researchers have made inconsistent choices about cut-offs. Such methodological variations are potentially concerning, as it is unclear whether inconsistent conclusions about short-term time matching are attributable to species/ecological differences, or are due in part to methodological inconsistency. We ask whether various criteria for separating short versus long-term reciprocation influence conclusions about short-term time matching using data from free-ranging rhesus ( Macaca mulatta) and captive-crested macaques ( Macaca nigra). We compare several commonly used cut-offs to ones generated by the currently preferred approach-survival analysis. Crested macaques displayed a mild degree of time matching regardless of the cutoff used. For rhesus macaques, whereas most cut-offs yielded similar degrees of time matching as the one derived from survival analysis, very short ones significantly underestimated both the degree of time matching and the influence of rank distance on time matching. Although researchers may have some flexibility in their choice of cut-offs, we suggest that they employ caution by using survival analysis when possible, and when not possible, by avoiding very short time windows.

The influence of phylogeny, social style, and sociodemographic factors on macaque social network structure.

Among nonhuman primates, the evolutionary underpinnings of variation in social structure remain debated, with both ancestral relationships and adaptation to current conditions hypothesized to play determining roles. Here we assess whether interspecific variation in higher-order aspects of female macaque (genus: Macaca) dominance and grooming social structure show phylogenetic signals, that is, greater similarity among more closely-related species. We use a social network approach to describe higher-order characteristics of social structure, based on both direct interactions and secondary pathways that connect group members. We also ask whether network traits covary with each other, with species-typical social style grades, and/or with sociodemographic characteristics, specifically group size, sex-ratio, and current living condition (captive vs. free-living). We assembled 34-38 datasets of female-female dyadic aggression and allogrooming among captive and free-living macaques representing 10 species. We calculated dominance (transitivity, certainty), and grooming (centrality coefficient, Newman's modularity, clustering coefficient) network traits as aspects of social structure. Computations of K statistics and randomization tests on multiple phylogenies revealed moderate-strong phylogenetic signals in dominance traits, but moderate-weak signals in grooming traits. GLMMs showed that grooming traits did not covary with dominance traits and/or social style grade. Rather, modularity and clustering coefficient, but not centrality coefficient, were strongly predicted by group size and current living condition. Specifically, larger groups showed more modular networks with sparsely-connected clusters than smaller groups. Further, this effect was independent of variation in living condition, and/or sampling effort. In summary, our results reveal that female dominance networks were more phylogenetically conserved across macaque species than grooming networks, which were more labile to sociodemographic factors. Such findings narrow down the processes that influence interspecific variation in two core aspects of macaque social structure. Future directions should include using phylogeographic approaches, and addressing challenges in examining the effects of socioecological factors on primate social structure.

Body signals used during social play in captive immature western lowland gorillas.

The play face is a well-established play signal in nonhuman primates that functions to invite play and convey a playful intent. However, recent evidence indicates that some species display repertoires of play signals that may have more specific meanings related to particular aspects of play. Furthermore, previous studies have inconsistently categorized gorilla behaviors as play signals versus actual play. Here we aim to identify behaviors displayed by two immature captive western lowland gorillas (Gorilla gorilla gorilla) at the Buffalo Zoo that meet three necessary criteria to be considered play signals. Specifically, we (1) investigate whether 21 candidate signals are significantly different from actual play behaviors, (2) and from similar signals used in non-play contexts, and (3) determine whether they predict the occurrence of social play. The results indicate that at least 18 of the 21 candidate signals have strong support for classification as play signals. These findings represent first steps in determining the function of multiple play signals in gorillas.

Primate Kinship: Contributions from Cayo Santiago.

Research on Cayo Santiago and Japan deserves credit for launching the study of primate kinship and for continuing to help shape it in important ways. This review describes the origins of kinship research on Cayo Santiago, beginning with Donald Sade's pioneering work establishing the concepts of kin preferences, matrilineal dominance systems and incest avoidance. It then reviews subsequent research by later Cayo Santiago researchers and alumni, focusing primarily on maternal kinship. Together these researchers have greatly expanded our knowledge of kin preferences in rhesus in terms of (i) what age-sex classes, behaviors and types of kin show them, (ii) the ways in which kinship interfaces with rank, sex, age, and dispersal patterns, and (iii) the graded and variably limited nature of kin preferences in terms of degree of relatedness. Second, the argument for kin selection at least for some types of behavior has survived challenges posed by several alternative explanations, and has been both strengthened by recent findings of paternal kin preferences and narrowed by studies showing that unilateral altruism may extend only to very close kin. Third, work on Cayo Santiago has contributed to an appreciation that both current conditions and inherent social characteristics may influence the strength of kin preferences, and fourth, it has contributed to an understanding of the possible origins of our own species' family systems. Cayo Santiago became a leader in kinship research in large part because of management practices that produce known extended lineages. These lineages have promoted and accelerated research on kinship, prompting other researchers to investigate its importance in other groups and species, where its effects only then became clear. The extended lineages remain valuable tools for research on a species that lives in a broad range of environments in the wild, including those with key parallels to Cayo Santiago.

Body signals during social play in free-ranging rhesus macaques (Macaca mulatta): A systematic analysis.

Social play involves one of the most sophisticated types of communication, that is, the use of play signals. Most primate research on play signals has focused on the use of the play face. However, some species appear to exhibit a variety of play signals. For example, rhesus monkeys (Macaca mulatta) have been reported to use body movements or postures that might have signal value during social play, in addition to the play face. However, it is not clear whether these body signals actually meet several criteria necessary to label them as "play signals." Here we examine the forms and possible functions of seven candidate signals that we observed exclusively during social play contexts among free-ranging rhesus monkeys on Cayo Santiago. We aim to (1) distinguish them from actual play behavior (play involving contact or chasing) using loglinear analysis and (2) determine whether they predict playful behavior using modified PC-MC methods. Two candidate signals did not resemble any behaviors used in actual play. The other five signals contained elements that lasted longer or increased their conspicuousness over similar play behaviors, suggesting ritualized characteristics. Youngsters were likely to initiate contact or chasing play significantly sooner after candidate signals than in their absence. Thus, these candidate signals appear to meet critical criteria of signals that promote, moderate or facilitate play. As such, these findings open the door to questions about why multiple play signals have evolved.

Hierarchical steepness, counter-aggression, and macaque social style scale.

Nonhuman primates show remarkable variation in several aspects of social structure. One way to characterize this variation in the genus Macaca is through the concept of social style, which is based on the observation that several social traits appear to covary with one another in a linear or at least continuous manner. In practice, macaques are more simply characterized as fitting a four-grade scale in which species range from extremely despotic (grade 1) to extremely tolerant (grade 4). Here, we examine the fit of three core measures of social style-two measures of dominance gradients (hierarchical steepness) and another closely related measure (counter-aggression)-to this scale, controlling for phylogenetic relationships. Although raw scores for both steepness and counter-aggression correlated with social scale in predicted directions, the distributions appeared to vary by measure. Counter-aggression appeared to vary dichotomously with scale, with grade 4 species being distinct from all other grades. Steepness measures appeared more continuous. Species in grades 1 and 4 were distinct from one another on all measures, but those in the intermediate grades varied inconsistently. This confirms previous indications that covariation is more readily observable when comparing species at the extreme ends of the scale than those in intermediate positions. When behavioral measures were mapped onto phylogenetic trees, independent contrasts showed no significant consistent directional changes at nodes below which there were evolutionary changes in scale. Further, contrasts were no greater at these nodes than at neutral nodes. This suggests that correlations with the scale can be attributed largely to species' phylogenetic relationships. This could be due in turn to a structural linkage of social traits based on adaptation to similar ecological conditions in the distant past, or simply to unlinked phylogenetic closeness.

Control of postpartum mating behavior in free-ranging rhesus monkeys.

This paper explores the effect that a dependent rhesus macaque infant (Macaca mulatta) has on the timing of its mother's resumption of mating. Toward this end, behavioral data from the rhesus populations at Tughlaqabad, India, and Cayo Santiago, Puerto Rico, are compared. Specifically, the intervals between parturition and subsequent resumption of mating for individual parous females are examined in order to shed light on the relative importance of environmental and internal factors (such as lactational infertility) in the control of rhesus mating behvior. At both study sites it was found that the later a given female gave birth during a birth season the shorter was her parturition-mating interval and the younger was her infant when she resumed mating activity. It is suggested that this finding is the result of an interaction of environmental and internal factors; both act in concert to determine how soon after parturition a particular rhesus female will resume mating activity.

Consistency in maternal behavior within families of free-ranging rhesus monkeys: An extension of the concept of maternal style.

This paper assesses the extent to which free-ranging rhesus monkeys (Macaca mulatta) on Cayo Santiago show consistent mother-infant interaction with individual infants over time and consistent maternal styles from one infant to another. Inter-pair differences in several measures of mother-infant interaction related to proximity and contact were correlated positively and highly significantly between 6-week age periods. Analysis of variance methods were used to show that, after the first 6 weeks, these measures of interaction were also more similar among pairs with the same mother (i.e., families) than among pairs with different mothers. Differences between families were also consistent between age periods, and appeared to be due primarily to differences between mothers rather than to differences between sets of infant siblings. The results suggest that the concept of maternal style can be used to describe variation between both individual Cayo Santiago mother-infant pairs and between individual Cayo Santiago mothers.

A nonintrusive method for determining relative body fat in free-ranging monkeys.

A procedure is described for designing simple obesity rating scales for use with free-ranging rhesus monkeys (Macaca mulatta). Ratings are based on observers' judgments of degree of overall obesity of individual monkeys. The procedure was tested separately on samples of males and females over 2 successive years. Within each of these four samples, observers' judgments were both highly reliable and highly correlated with actual measures of body weight and with estimates of body fat based on morphometric measures, including the Quetelet index. To test the degree to which scores from different applications of the scale could be compared with one another, regression functions were calculated for scale vs. the Quetelet index and for scale vs. body weight for each application. No significant differences were found among the four regression functions for scale vs. the Quetelet index for fully grown adult monkeys. This suggested that observers' judgment criteria with regard to this measure were sufficiently stable across the four test applications to allow meaningful comparison of scores. Comparable analyses for body weight suggested that observers' judgment criteria were stable over time but not between sexes. These data suggest that observers had been successful in attending more closely to obesity than to body weight. Obesity scales have many potential uses both in the field and in captivity provided they are adequately tested before use.