Consistency of dominance rank order: a comparison of David's Scores with I&SI and Bayesian methods in macaques.

In nonhuman primate social groups, dominance ranks are usually assigned to individuals based on outcomes of dyadic agonistic encounters. Multiple approaches have been used, but currently there is no consensus. One approach, David's Scores (DS), offers dual advantages of yielding cardinal scores that may in turn be used to compute hierarchical steepness. Here we correlate rank orders yielded by DS with those yielded by both the traditionally used I&SI approach and the recently proposed parametric Bayesian approach. We use six datasets for female macaques (three despotic and three tolerant groups), and 90 artificially generated datasets modeling macaque groups. We also use the artificial datasets to determine the impact of three characteristics (group size, interaction frequency, and directional asymmetry of aggression) on the magnitude of correlation coefficients, and assess the relative utility of two indices used to compute DS: Dij versus Pij. DS-based rank orders were strongly positively correlated with those yielded by the other two approaches for five out of the six macaque datasets, and for the majority of artificial datasets. Magnitudes of correlation coefficients were unrelated to group size or interaction frequency, but increased with directional asymmetry, suggesting methodological inconsistencies were more likely when dyads had more frequent reversals in directions of aggression. Finally, rank orders calculated using the Dij and Pij indices were similarly consistent with orders from other methods. We conclude that DS offers consistent estimates of rank orders, except perhaps in groups with very low levels of aggression asymmetry. In such "tolerant" groups, we suggest that the relatively greater methodological variability in rank orders may reflect behavioral characteristics of tolerant groups rather than computational inconsistencies between methods. We hypothesize that this quality may be quantified using posterior probability scores of Bayesian rank orders and may also index macaque social styles.

Using biological markets principles to examine patterns of grooming exchange in Macaca thibetana.

Biological markets principles offer testable hypotheses to explain variation in grooming exchange patterns among nonhuman primates. They predict that when within-group contest competition (WGC) is high and dominance hierarchies steep, grooming interchange with other "commodity" behaviors (such as agonistic support) should prevail. In contrast, when WGC is low and gradients shallow, market theory predicts that grooming reciprocity should prevail. We tested these predictions in a wild, provisioned Tibetan macaque (Macaca thibetana) group across six time periods during which the group had been subjected to varying degrees of range restriction. Data on female-female aggression, grooming, and support were collected using all-occurrences and focal animal sampling techniques, and analyzed using ANCOVA methods and correlation analyses. We found that hierarchical steepness varied significantly across periods, but did not correlate with two indirect indicators of WGC (group size and range restriction) in predicted directions. Contrary to expectations, we found a negative correlation between steepness and group size, perhaps because the responses of group members to external risks (i.e. prolonged and unavoidable exposure to humans) may have overshadowed the effects of WGC. As predicted, grooming reciprocity was significant in each period and negatively correlated with steepness, even after we controlled group size, kinship, rank differences, and proximity. In contrast, there was no evidence for grooming interchange with agonistic support or for a positive relationship between interchange and steepness. We hypothesize that stressful conditions and/or the presence of stable hierarchies during each period may have led to a greater market demand for grooming than support. We suggest that future studies testing these predictions consider more direct measures of WGC and commodities in addition to support, such as feeding tolerance and access to infants.

Changes in yearling rhesus monkeys' relationships with their mothers after sibling birth.

The birth of a new sibling is believed to signify an abrupt and important transition in a young primate's relationship with its mother-one that is of potential importance from at least three theoretical perspectives: attachment theory, parent-offspring conflict theory, and dynamic assessment models. This study examines changes in relationships between free-ranging yearling rhesus monkeys (Macaca mulatta) and their mothers concomitant with the birth of the mother's next infant, and tests predictions derived from each theoretical perspective. We observed 31 yearling rhesus on Cayo Santiago, Puerto Rico, 3 months before and 3 months after their siblings' births, using focal animal sampling methods. Changes in measures related to mother-yearling interaction and yearling distress were examined using repeated-measures analysis of variance. After sibling birth, mothers and yearlings abruptly reduced amounts of time in contact and increased amounts of time at a distance and out of sight of one another. Mothers and yearlings played approximately equal roles in bringing about decreases in proximity, and yearlings took the primary roles in bringing about decreases in contact. Rates of maternal aggression toward yearlings increased immediately and markedly after birth, possibly providing yearlings with early cues regarding subsequent decreased levels of maternal care. There were no marked increases in overt signs of yearling distress (e.g., vocalizations or tantrums) following the births. We conclude that yearlings generally acquiesced to reduced levels of care, responding behaviorally with increased independence and maturity. In this sense, our study provides preliminary support for dynamic assessment models over attachment theory and parent-offspring conflict theory models.

A preliminary description of responses of free-ranging rhesus monkeys to brief capture experiences: behavior, endocrine, immune, and health relationships.

A cohort of free-ranging rhesus monkeys has been followed since birth in 1994 on the island of Cayo Santiago, Puerto Rico. At 3 years of age, subjects were trapped and blood samples were collected after capture and prior to release the following day. Blood samples were processed for natural cytotoxicity toward xenogeneic tumors, phenotyping, and plasma hormones. Intestinal parasites were determined from fresh stool samples collected during trapping. Data were also available from the previous year for antibody titers to latent viruses prevalent in this population. Behavioral traits of each monkey were characterized using a previously developed trait scale for rhesus monkeys. Natural cytotoxicity toward both K562 and Raji targets declined from capture until release the following day. Plasma cortisol rose and plasma prolactin and growth hormone fell during the period of captivity; a rise in insulin was significant. It was expected that individual differences in behavioral traits might predict immune and hormone levels at the time of capture or changes in these parameters during the capture period. Although behavioral adjectives tended to cluster along three orthogonal dimensions (Insecurity, Irritability, and Sociability), they bore no relationship to the physiological parameters collected acutely (in vitro immune and endocrine parameters). The individual difference markers of gender and maternal rank were not related to the magnitude of the observed changes in these in vitro parameters, either. However, an in vivo measure (CMV titer) was related to individual differences in Irritability. It was concluded that the magnitude of the stress associated with capture overwhelmed the individual difference effects.

On the quantification of suckling intensity in primates.

The inhibitory effect that suckling has on the reproductive function of primate mothers varies as a function of the intensity with which they are suckled. Here we present an easily computed index of one parameter of suckling intensity, namely the temporal patterning of suckling bouts. High intensity suckling is characterized by frequent nursing bouts demarcated by short interbout intervals. Therefore, our suckling index is based on the brevity of observed interbout intervals, more specifically the proportion of such intervals that fail to exceed a criterion length. The index is an appropriate means of making interspecific comparisons of the development of infant suckling and is well suited for application to field data that include interbout intervals that were not observed in their entirety. To demonstrate its utility, we apply the index to field data collected on the suckling behavior of free-ranging rhesus monkey (Macaca mulatta) infants in India. In this context, we demonstrate that, in rhesus, between-infant differences in suckling intensity manifest themselves early in the postpartum period and contribute to between-female differences in the timing of first mating postpartum.

Responses of free-ranging rhesus monkeys to a natural form of social separation. I. Parallels with mother-infant separation in captivity.

Observations of 23 free-ranging rhesus monkey infants on Cayo Santiago, Puerto Rico, indicated that mothers' first postpartum estrous periods were marked by large increases in the amount of time infants were separated from their mothers, by disturbances in mother-infant relationships, and by increases in infant distress behavior. When their mothers resumed mating, most infants showed signs of agitation; a few briefly showed indications of depression. Male infants responded to their mothers' resumption of mating by playing more, whereas females engaged in less play and more allogrooming. The results suggest (a) that basic parallels exist between the behavioral responses of rhesus infants to their mothers' resumption of mating in the field and to forcible separation from their mothers in captivity and (b) that early separation experiences may play a role in the normal development or manifestation of sex differences in behavior.

Specific antibody levels in free-ranging rhesus monkeys: relationships to plasma hormones, cardiac parameters, and early behavior.

Levels of tetanus-specific antibodies were assessed in free-ranging, yearling rhesus monkeys following prophylactic immunization with tetanus toxoid. Each subject's behavior had been observed between 11 and 25 weeks of age and approximately 2 months later during its mother's first concentrated mating period as a part of another study. Prior to immunization, at approximately 1 year of age, cardiovascular parameters, and several plasma parameters [cortisol, adrenocorticotrophic hormone (ACTH), growth hormone (GH), interleukin-2 (IL-2), and total plasma immunoglobulin G (IgG)] were measured during a brief period of captivity. Antibody titers noted approximately 2 weeks after immunization were related to cardiovascular parameters. Thus, yearlings with high heart rates and low heart rate variability during captivity had the highest tetanus-specific serum IgG. Levels of plasma cortisol, ACTH, total IgG, and IL-2 noted at the time of capture were unrelated to subsequent antibody levels. Antibody titers were, however, positively correlated with GH noted immediately following capture on the day prior to immunization. Antibody titers were also related to the infants' behavior observed during their mother's first concentrated mating period. Infants who were most distressed (high levels of distress vocalization) when their mother resumed mating (a time particularly stressful for free-ranging rhesus infants) showed lower antibody titers to tetanus immunization as a yearling. The present observations add support to the existence of a relationship between behavior during exposure to an early stressor and later immune regulation and that certain cardiovascular parameters may be related to certain indicators of immunoregulation.

Trapping activities and mother-infant relationships on Cayo Santiago: a cautionary tale.

Trapping activities in the Cayo Santiago rhesus monkey colony are normally limited to January and February of each year. The year 1984 was exceptional in that the trapping period was extended until early May. This paper examines the effects of the extended trapping period on mothers and infants who observed trapping activities but were not directly involved in them. Mother-infant pairs exposed to extended trapping activities spent significantly more time in contact and less time at a distance from each other than those not exposed, both during the time of exposure and for several weeks afterward. There were also consistent nonsignificant tendencies for exposed mothers to reject their infants less, to initiate a higher proportion of their contact and to play a larger role in maintaining proximity. This pattern of differences is consistent with the suggestion that mothers reacted to the extended trapping period by protecting their infants more and by encouraging independence less. The results demonstrate the sensitivity of mothers to human disturbance and illustrate the value of management policies like those on Cayo Santiago, that minimize human disturbance and restrict trapping to a consistent and limited period each year.

The social development of an orphaned rhesus infant on Cayo Santiago: Male care, foster mother-orphan interaction and peer interaction.

The social development of a free-ranging male rhesus (Macaca mulatta) infant is described qualitatively and quantitatively from birth to orphaning at nearly 11 weeks of age, and then to 30 weeks of age. Initially the orphan was cared for by four males, but was subsequently adopted by his nulliparous sister. Measures of foster mother-orphan interaction were compared with measures of mother-infant interaction for a control sample of 20 mother-infant pais within the same group. Signs of depression, decreases in play, and atypical patterns of interaction with caretakers gradually diminished over a period of two to three months following orphaning. Through adjustments on the part of both the foster mother and the orphan, their patterns of interaction gradually came to resemble those of mothers and infants of the same age.