Performance correlates of social behavior and organization: Effects of group formation on operant performance in rhesus monkeys (M. mulatta)

The performance of six adult rhesus monkeys on a fixed interval 1-min reinforcement schedule was examined under conditions where the reinforcement probabilities were either 1.00 or .80. The animals were tested with a reinforcement probability of 1.00 immediately after removal from their social group, tested again several months later with reinforcement probabilities of 1.00 and .80, and then retested with a reinforcement probability of .80 before, during, and after the formation of a new social group with the six monkeys. The results supported an earlier report in which it was found that high ranking animals responded at a lower rate under a reinforcement probability of 1.00 than did low ranking animals and that the former also had a higher ratio of nonreinforced to reinforced responses than the lower ranked animals. These relationships were present in five of the six animals immediately after removal of the animals from their original group and during and after formation of the new group. They did not appear on tests conducted after the animals had been out of a social group for several months. A third result was a suppression of operant performance which appeared in all animals following group formation. The magnitude and duration of this effect was inversely related to social rank and the time the animal had been a member of the group. The data are discussed in terms of a carry-over of the effects of recent social experience on two factors: a more deliberate rate of response by higher ranking animals under 100% reinforcement and an inhibition of response bursting following omission of reinforcement by the lower ranking monkeys. Supported by USAMRDC Contract No. DADA 17-73-C-3007.     

Performance correlates of social behavior and organization: Social rank and reversal learning in crab-eating macaques (M. fascicularis)

Seventeen male crab-eating macaques drawn from two captive troops, were tested on a brightness discrimination, reversal learning task. Fourteen of these animals completed ten reversals. It was found that the performance of the three highest ranking animals from each troop, taken together, was poorer than that of the lower ranking animals that were tested. The high ranking animals made more errors before reaching criterion on both initial learning and the reversal problems. Analysis of error patterns revealed that, while the high ranking animals had no more difficulty than the others in withholding their responses to the previously correct stimulus following reversals, they did not adopt the correct strategy as soon as the low ranking animals. The results have been interpreted in terms of a carry-over of a hypothetical factor or factors resulting from pressures created by the ongoing social dynamics involved in establishing and maintaining a given social rank at the time laboratory testing occurred. Supported by USAMRDC Contract No. DADA 17-73-C-3007.     

Performance correlates of social behavior and organization: Social rank and complex problem solving in crab-eating macaques (M. fascicularis)

Seventeen male crab-eating macaques, drawn from two captive troops, were tested on a series of complex problem solving tasks in a Wisconsin General Test Apparatus (wgta). The animals were trained on a series of 6-trial object quality learning set problems followed by a series of 10-trial object quality learning set problems. They were then given problems in which the correct stimulus object was reversed part way through the problem. After the animals reached criterion on this task, the reversal learning set was then extinguished. High ranking animals made more intraproblem errors than low ranking animals on the 6-trial problems, but there was no relationship between social status and the rapidity with which the object quality learning set was established. Animals that received overtraining on the 6-trial problems transferred their learning virtually intact to the 10-trial problems; however, high ranking animals without overtraining made more errors than low ranking animals. On reversal learning and reversal extinction, high ranking animals made more errors on critical trials, indicating that they formed and extinguished the reversal set more slowly than low ranking animals. Object quality sets, as measured by trial-2 performance, were not affected by the reversal conditions. Supported by USAMRDC Contract No. DADA 17-73-C-3007.     

Female dominance rank and behavior during artificial menstrual cycles in social groups of rhesus monkeys (Macaca mulatta)

We recently reported (Michael & Zumpe: American Journal of Primatology 15:157–170, 1988) evidence for the hypothesis that copulations by pairs of rhesus monkeys are linked more closely to the ovulatory phase of the female's menstrual cycle when a male has access to several females in different cycle phases rather than access to females in the same cycle phase. We have now used data from this earlier study to assess the role of female dominance. Artificial menstrual cycles were induced with hormone injections in two of four ovariectomized females in eight social groups (each consisting of one male and four females). The artificial cycles were either synchronized or offset by 7-day increments. There were differences in the behavioral interactions of the higher-ranking (dominant) and lower-ranking (subordinate) hormone-treated females in each group. The amount of male sexual activity received by dominant and subordinate females differed little, but dominant females initiated significantly more sexual activity (P<.0001) than did subordinate females. Dominant females were significantly more aggressive (P<.0001) toward other females and received more direct and redirected aggression from males. Males generally initiated and maintained more social contacts with dominant than with subordinate females, and dominant females were less active than subordinates in initiating and maintaining social interactions with males. The findings provide new evidence for both female mate competition and mate choice by males for higher-ranking females.     

Birth sex ratios and maternal social rank in a captive colony of rhesus monkeys (Macaca mulatta)

Data from a 35-year study of rhesus macaques (Macaca mulatta) at Madingley, Cambridge, were used to investigate sex ratio biases associated with maternal rank. Data were available from two colonies, the Old colony (1960–81) and New colony (1982–93). Overall, top-ranking mothers gave birth to 30.9% sons, while non-top mothers gave birth to 58.4% sons. Among non-top mothers, middle- and bottom-ranking ones had 59.0 and 55.0% sons, respectively. Top mothers' daughter biases were strongest in matrilines with two adult females in the year the infants were conceived (15.4 sons and 14.3% sons in Old and New colonies). Non-top mothers' son biases (88.9 and 71.0% in Old and New colonies) were strongest in matrilines with 3 females. The findings are discussed in relation to the colonies' small matriline sizes and data on breeding performance and infant survival, which indicate the costs to mothers of different rank of having different sex infants. Overall, top-ranking mothers were more likely to breed in two successive years (78.6%) than non-top mothers (56.7%). Infant survival to 7 days was significantly higher in the New colony (89.0%) than the Old colony (75.3%), with daughters born to Old colony mothers doing especially poorly. We point out that between-group and between-species comparisons of sex ratio effects depend critically on how females are assigned to rank categories, and require information about divergences of sex ratios from 50:50 in each category. © 1996 Wiley-Liss, Inc.     

Estrous behavior of free-ranging rhesus monkeys (Macaca mulatta)

The sexual behavior of a group of free-ranging rhesus monkeys (Macaca mulatta) was studied for 13 consecutive months in an attempt to determine whether or not sexual activity occurred year-round, and the importance of sexual attraction to rhesus monkey social organization.Estrous behavior was seen both inter-menstrually and peri-menstrually, producing a shorter mean estrous cycle length than reported by other workers. New data was gathered on the interrelationships among age, dominance rank, and sexual activity; son-mother and brothersister matings; and sexual favoritism among free-ranging rhesus monkeys.A few females who failed to conceive during the fall breeding season showed cyclic estrous behavior throughout the entire annual cycle. Hypotheses are given as to possible physiological bases for birth season sexual cycles.Several forms of inter-animal bonding, including sexual bonding, are enumerated, and their importance to rhesus monkey social organization discussed.     

Social rank and cortisol among female rhesus macaques (Macaca mulatta)

In animal societies, some stressful events can lead to higher levels of physiological stress. Such stressors, like social rank, also predict an increased vulnerability to an array of diseases. However, the physiological relationship between social rank and stress varies between different species, as well as within groups of a single species. For example, dominant individuals are more socially stressed at times, while at other times it is the subordinate ones who experience this stress. Together, these variations make it difficult to assess disease vulnerability as connected to social interactions. In order to learn more about how physiological rank relationships vary between groups of a single species, cortisol measurements from hair samples were used to evaluate the effects of dominance rank on long-term stress levels in despotic and less stringent female rhesus macaque hierarchal groups. In despotic groups, cortisol levels were found not to be correlated with social rank, but a negative correlation was found between social rank and cortisol levels in less stringent hierarchies. Low ranking monkeys in less stringent groups secreted elevated levels of cortisol compared to higher ranking animals. These data suggest that variations in the strictness of the dominance hierarchy are determining factors in rank related stress physiology. The further consideration of nonhuman primate social system diversity and the linear degree of their hierarchies may allow for the development of valid rank-related stress models that will help increase our understanding and guide the development of new therapeutics for diseases related to human socioeconomic status.     

Computer-task testing of rhesus monkeys (Macaca mulatta) in the social milieu

Previous research has demonstrated that a behavior and performance testing paradigm, in which rhesus monkeys (Macaca mulatta) manipulate a joystick to respond to computer-generated stimuli, provides environmental enrichment and supports the psychological well-being of captive research animals. The present study was designed to determine whether computer-task activity would be affected by pair-housing animals that had previously been tested only in their single-animal home cages. No differences were observed in productivity or performance levels as a function of housing condition, even when the animals were required to “self-identify” prior to performing each trial. The data indicate that cognitive challenge and control are as preferred by the animals as social opportunities, and that, together with comfort/health considerations, each must be addressed for the assurance of psychological well-being.     

Parturition in rhesus monkeys (Macaca mulatta)

During five years of birth season fieldwork, we observed two births and three peri-birth instances of behavior of free-ranging rhesus living in Kathmandu, Nepal. These constitute the first two recorded free-ranging rhesus births, and we compare them to the behavior which has been observed in captivity and expected in the wild. The free-ranging parturition behavior was characterized by a general lack of contact with other troop members and by overall inconspicuousness. In the first birth we observed, the troop moved about 70 m up the hill, leaving the laboring female behind on an open hillside. Two males, a female and a juvenile returned and rested about 20 m from the delivering female. During the second delivery, the female stayed with the troop and seemed to participate normally in most troop interactions, although she avoided physical contact with other troop members. We propose that this near-normal behavior may help to assure successful parturition by allowing the female the needed social isolation and inconspicuousness without any loss of troop protection. It may also partly explain why births have not been observed during previous studies. Observations of rhesus parturition behavior reported from studies of captive monkeys and reports from other free-ranging primate studies are compared with our data.     

Interactions of social,spatial and hormonal factors on the behavior of rhesus monkeys (Macaca mulatta)

In a three year study, the interactions of social, spatial and hormonal variables on the behavior of rhesus monkeys were investigated. Observations were made on (1) an oppositelysexed pair alone in a cage; (2) the pair alone in a large room; and (3) the pair together with three ovariectomized females in the same large room. Each of four males was tested with the same group of four ovariectomized females (16 pairs, 480 1-hr tests). Each female served in turn as the focal female, namely, the hormone-treated one, and received first estradiol benzoate (EB) alone and then in combination with progesterone (P). The presence of three other females (the social variable) had a marked effect on all aspects of the behavior of the focal pair, and reduced the male's ejaculations as well as other sexual and affiliative interactions with the focal female. This was due to an inhibitory influence exerted by the dominant female on the interactions of subordinate females with the male. Comparing data from two groups of females showed that female dominance rank, and not male sexual preference, was the critical factor, and that mate competition between female rhesus monkeys was operating. Decreasing the space available for the interactions of the pair appeared to imitate a bonding effect in the male, increasing male grooming and tending to increase male sexual activity. In the group setting, treating the female with EB increased sexual activity, and additional progesterone decreased it in all three test settings. The effects of progesterone were most clearly apparent when the pair was tested alone in a large area.     

Kinship,association, and social relationships in rhesus monkeys (Macaca mulatta)

Data on social interactions with matrilineal kin were collected from two groups of rhesus monkeys for 6 years. All behavioral states, including time within one meter of another, involved kin more often than would be expected by chance. Significant associations were also found between kinship and the frequencies of various forms of agonistic as well as affiliative acts. Frequency of social interaction, however, was not a simple function of time in proximity. Although animals spent more time with kin than nonkin they had more aggressive interactions with kin. Moreover, aggression was biased toward the more serious forms of expression in interactions with kin. Time spent in association was neither predictive of the rate of aggressive interaction nor reduced by high rates of aggressive interaction. Rather than association time influencing rates of interaction, association time may be the consequence of a history of aggressive and affiliative exchanges. Preferential association and high rates of aggressive interaction with kin may be possible due to the existence of compensating social mechanisms nullifying the negative influence of specific aggressive encounters. © 1993 Wiley-Liss, Inc.     

Hydranencephaly in two rhesus monkeys (Macaca mulatta)

Spontaneously occurring hydranencephaly was diagnosed at necropsy and confirmed histologically in two stillborn fetuses that were delivered from young female rhesus macaques (Macaca mulatta).     

Skeptical responding in rhesus monkeys (Macaca mulatta)

Signalers that misinform sufficiently open may become devalued as sources of information; however, “skepticism” and any comparison involved in testing reliability entail a cost that involves delays and energy expenditure. Skepticism may be less costly though, if, as a rule, animals are not equally skeptical of the signals of all conspecifics. Animals with the ability to recognize individual conspecifics and to recall past encounters with them may have the capacity to restrict skepticism to subsets of animals that are most likely to benefit from deception. We played tape-recorded alarm calls of high- and low-ranking rhesus monkeys(Macaca mulatta) to their groups in a feeding context once daily over 8 consecutive days at the Yerkes Primate Center Field Station. Over the sequence of playbacks, response was greater to the calls of high-ranking monkeys, adult response patterns were different from those of juveniles, and for adults especially, decline in responsiveness was punctuated by partial resurgences of response. These differences may be the consequence of the adults’ more extensive histories of interaction with group members that, though generally reliable, vary with respect to the potential benefits of deceptive signaling.     

Feeding tactics in juvenile rhesus monkeys (Macaca mulatta)

In a group of rhesus monkeys, feeding tactics of juveniles were studied in a competitive situation in which food presentation had been modified, and where food was supplied in a feeding trough six times a day. Juvenile offspring of high-ranking mothers remained longer in the feeding area gathering food. In contrast, juvenile offspring of low-ranking mothers went less often to the feeding area, primarily to collect food. Low-ranking juveniles also gathered the food faster than did dominants and used longer feeding bouts. High-ranking juveniles interrupted their feeding more spontaneously than did subordinate ones. Low-ranking juveniles did so more often as a result of avoiding and being startled. Juvenile males entered the feeding area to satisfy their food requirements more often than females, but were also aggressively expelled more than females. No relation was found between age in months of juveniles and any feeding parameters or causes of interruption. Nor were significant differences found between young and old juveniles. Juvenile rhesus appear to use different tactics in accessing food according to their sex and to their mothers' dominance rank.