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.     

Mating patterns,mate choice,and birth season heterosexual relationships in free-ranging rhesus macaques

Birth season adult heterosexual nonkin relationships of 50 free-ranging female rhesus macaques (Macaca mulatta) in two social groups at Cayo Santiago, Puerto Rico were examined using focal follow (289 hr) and ad lib data. Eighty-eight percent of subjects had at least one relationship characterized by particularly high frequencies of spatial proximity, grooming, or both. These were designated “friendships.” Males intervened in aggressive interactions more frequently on behalf of Friends than non-Friends. Female aggressive support of males was extremely rare. Higher-ranking males experienced more friendships than lower-ranking males. High-ranking females had higher-ranking Friends than low-ranking females. Older females had higher-ranking Friends than younger females. Females groomed high-ranking Friends more than they were groomed by them, whereas they groomed low-ranking Friends less than they were groomed by them. In one social group, high-ranking females were more likely than low-ranking females to groom their Friends more than they were groomed by them. Males were more responsible than females for spatial proximity maintenance in 9 of 14 Friend dyads for which sufficient data were available. Neither male nor female dominance rank affected responsibility for proximity maintenance in Friend dyads. Eight of 24 females had friendships with males with whom they had completed copulations during their conception peri-ovulatory period of the preceding mating season. Two of 19 females completed peri-ovulatory copulations with Friends during the following mating season. Friendship was not correlated with either of two demonstrated female mate choice indicators: (1) proximity maintenance during estrus; or (2) cooperation with male “hip-grasp” courtship attempts. Males directed “muzzle-up” courtship signals at lower rates toward Friends than toward non-Friends. These and other investigators' results indicate that (1) protection from aggression is the primary benefit to female rhesus macaques of birth season heterosexual relationships; (2) the most effective protectors are in greatest demand as Friends; and (3) friendship has no effect or an inhibitory effect on mate choice in this species. Benefits to males of friendships were not apparent from this study but may include coalitional support against lower-ranking males.     

Effects of early experience on the behaviour of yearling rhesus monkeys (Macaca mulatta) in the presence of a strange object: classification and correlation approaches

Special techniques are needed to help us understand the long-term effects of infants' experiences of their relationships with their mothers, especially when direct experimental control of the interaction between mother and young is impossible, or could distort their relationship. A classification approach is developed to show how outcomes in individuals can be predicted from their earlier experiences and characteristics. Four-week-old rhesus monkey infants' characteristic levels of enterprise persisted through their first year, but could be reduced in certain individuals who had been kept off their mothers by high rates of early maternal rejection. Correlational approaches are difficult to interpret when they fail to confirm simple effects of experience or of individual characteristics, because they are based on groups not individuals, and because certain individuals can affect the values of correlation coefficients in ways that cannot be specified without using a classification approach. The possible effects on correlation coefficients of inconsistent individuals, and of being unable to specify which infants respond in which ways to relevant variables were discussed.     

Effects of social and inanimate enrichment on the behavior of yearling rhesus monkeys

Certain types of inanimate environmental enrichment have been shown to positively affect the behavior of laboratory primates, as has housing them in appropriate social conditions. While social housing is generally advocated as an important environmental enhancement, few studies have attempted to measure the influence of social conditions on the effects of inanimate enrichment or to compare the relative merits of social and inanimate enhancements. In the present study, inanimate enrichment (predominately physical and feeding enhancements) resulted in increased species-typical behavior for socially restricted subjects. However, social enrichment (living in groups) appeared to be more beneficial for young rhesus monkeys, leading to increased species-typical activities and decreased abnormal activities. The behavior of one cohort of yearling rhesus monkeys (Macaca mulatta) housed in small peer groups was compared with the behavior of four yearling cohorts housed in single cages. Half the animals in each cohort received a three-phase enrichment program and the rest served as controls. Group-housed yearlings spent significantly more time feeding and exploring and significantly less time behaving abnormally, self-grooming, and drinking than did singly housed yearlings. Enriched subjects spent significantly more time playing by themselves, and significantly less time self-grooming and exploring than did controls. Among group-housed subjects only, there were no differences between enriched and control monkeys. Captive primates should be housed socially, whenever appropriate, as the first and most important step in an enrichment program, with the provision of inanimate enhancements being considerably less important. Limited resources for inanimate enrichment programs instead should be focused on those individuals who can not be housed socially. © 1996 Wiley-Liss, Inc.     

Responses of foster-mothers and troop members to adopted newborns in a captive group of rhesus monkeys

Two rhesus monkey males and two females, born to females caged singly, were exchanged with same-sex infants born to females in a large troop which was held in an enclosure in a different building. The ages of the infants were between 24 and 120 hr. The selected foster mothers (FMs) immediately accepted the foreign infants, allowed them to suckle and treated them as their own offspring. Compared with interactions with previous offspring, the FMs initially tended to be more possessive and restrictive of their foster infants: generally they took longer before they allowed the infants to sit at a distance from them and more readily retrieved them. The foster infants tended to be more active (‘fidgety’) than natural (control) offspring born to the troop. Non-related members of the troop, differentiated between foster and control groups. These troop animals more frequently approached and sat in proximity, often in fur-contact with, touched, groomed, and lipsmacked to, foster infants than control infants. The attractiveness of the fostered infants seemed to be slightly associated with the FMs' dominance rank. The foster infants were therefore viewed by others as having assumed the role afforded by the FMs' rank. Thus both FMs and other troop members recognized the unfamiliarity and novelty of the foster infant but the infants were still accepted into the group. We suggest that the different treatment of the foster infants by the troop may have consequences on the infants' future social development.     

Subjective assessment of reactivity level and personality traits of rhesus monkeys

The purposes of this study are to determine whether subjective assessment of reactivity level in rhesus macaques, between 1 and 14 years old, is related to assessment of personality traits and whether a configuration of personality traits most salient for assessment of reactivity can be defined. Results indicate that subjective assessment of reactivity is complementary to that of personality traits. Interrater reliability and convergent validity are established. Principal-component and discriminant analyses of the present data show that 10 personality traits can assign all' subjects to reactivity level, but as few as 3 traits may be sufficient.     

Gestation length in rhesus macaques (Macaca mulatta)

We describe some of the sources of variation in gestation length among rhesus macaques. the data were obtained from the timed-mating breeding program at the California Regional Primate Research Center (CRPRC). Information about approximately 700 pregnancies that resulted in spontaneous vaginal deliveries of liveborn young is presented. The average length of these pregnancies was 166.5 days. In this population, older females with higher parities had significantly longer pregnancies and significantly heavier infants than other females did. Other factors, including infant sex, month of conception, maternal reproductive history, and paternal identity, had no consistent effect upon gestation length.     

Group fission in free-ranging rhesus monkeys of Tughlaqabad,Northern India

A population of rhesus monkeys (Macaca mulatta)at Tughlaqabad on the southeastern outskirts of New Delhi has grown rapidly in the past 4 years, and the largest group (Group A) has given rise to three smaller groups. Fissioning, or new group formation, was not consistently associated with any particular season of the year or stage of the reproductive cycle, but it did occur in each case when the parent group reached approximately 120 monkeys. The fissioning process was not preceded or accompanied by unusual aggressive behavior. It occurred quietly and appeared to be a loss of cohesion within the large group by which a subgroup achieved behavioral and spatial independence. Some aggressive interactions did occur following each fission when the new group approached or attempted to reenter the parent group. Each newly formed group was subordinate to the parent group and all other groups in the population.     

Varying responses to feeding competition in a group of rhesus monkeys (Macaca mulatta)

The behaviour of members of a group of rhesus monkeys was observed in experimentally created, competitive feeding situations. Socially dominant members of the group tended to start eating before lower-ranking subjects, and generally ate more. Dominants sometimes used aggression to control access to food, but overall, intermediate-ranking monkeys were involved in most agonistic episodes. Non-dominant subjects improved their feeding performance when food was presented in three piles rather than one pile, often by snatching food and consuming it away from the pile. These general patterns were less evident when realistic snake models were placed on some of the food piles. Feeding was disrupted by the presence of snakes, but notably, subordinates risked feeding in these conditions. Piles containing preferred foods and snakes were eaten from, but a low-preference food (carrot) under snakes went untouched by all subjects. The results suggest that group-members evaluate potential risks and benefits of competing for a restricted resource, and that dominance status, while an important factor, is only one element in the equation.     

Calcium,magnesium, and phosphorus content of hair from two populations of rhesus monkeys

The use of hair for the assessment of human mineral nutritional status is controversial, yet has potential because of the ease of collection and storage, and the high concentration of minerals in hair. This study generated baseline values for hair macromineral content in the most commonly used primate model for human nutrition and disease, the rhesus monkey. Hair digests from monkeys in Maryland (n=98) and Puerto Rico (n=208) were analyzed by inductively coupled plasma atomic emission spectrometry (ICP-AES). Significant differences existed between the two populations for hair calcium (Ca), magnesium (Mg), and phosphorus (P) (P<0.01,P<0.001,P<0.02). Male hair had higher concentrations of Mg in specimens from the Puerto Rican population (P<0.001), whereas hair phosphorus was higher in female hair (P<0.02). There were no significant differences attributable to pregnancy status. Differences in hair content attributable to categorical age were found for Ca and Mg (P<0.001,P<0.01). Significant location differences paralleled dietary differences. These values therefore can be considered reference ranges for hair Ca, Mg, and P for free-ranging and caged rhesus monkeys. Preliminary reports of portions of these data were presented at the 69th Annual Meeting of the Federation of American Societies for Experimental Biology, April 1982, New Orleans, LA (B. M. Marriott, J. C. Smith, R. Jacobs, A. O. Jones, M. J. Kessler, and R. Rawlins,Fed. Proc. 41:770 [1982]) and in a symposium at the 6th Annual Meeting of the American Society of Primatologists, 1983, East Lansing, MI (B. Marriott, J. C. Smith, R. Jacobs, A. O. Lee Jones, R. Rawlins, and M. J. Kessler,Am. J. Primatol. 4(3):157 [1983]; B. Marriott, J. C. Smith, Jr., R. M. Jacobs, A. O. Lee Jones, R. Rawlins, and M. J. Kessler, inThe Cayo Santiago Macaques, R. Rawlins and M. J. Kessler, eds., SUNY Press, Albany, NY, pp. 219–231 [1986]).     

Early life maternal sociality predicts juvenile sociality in blue monkeys

Maternal effects are widespread in living organisms though little is known about whether they shape individual affiliative social behavior in primates. Further, it remains a question whether maternal effects on affiliative behavior differ by offspring sex, as they do in other physiological systems, especially in species with high levels of adult sexual dimorphism and divergence in social niches. We explored how direct and indirect experiences of maternal affiliative behavior during infancy predicted affiliative behavior approximately 1–6 years later during the juvenile period, using behavioral data from 41 wild blue monkey juveniles and their 29 mothers, and controlling for individual age, sex, and maternal rank. Female juveniles spent less time grooming with any partner and with peers the more maternal grooming they received during infancy, whereas males groomed more with any partner and with peers. Similarly, the more that mothers groomed with other adult females during subjects’ infancy, female subjects played less with peers, and male subjects played more as juveniles. Further, this maternal effect on social behavior appears specific to early life, as the same aspects of mothers’ sociality measured throughout subjects’ development did not predict juvenile behavior. Overall, our results suggest that both direct and indirect experience of mother's affiliative behavior during infancy influence an individual's affiliation later in life that sexes respond differently to the maternal affiliation, and that the first year of life is a critical window.     

Climate and reproductive seasonality in two free-ranging island populations of rhesus macaques (Macaca mulatto)

We gathered data over a 3-year period (1988–1990) on two free-ranging, island populations of rhesus macaques (Macaca mulatta)to test hypotheses concerning birth seasonal asynchrony and the relationship between climate and reproductive seasonality. Rhesus macaques from Kashmir, India, were translocated to Key Lois in 1973 and from Key Lois to Raccoon Key in 1978. Both sites are low-lying mangrove islands in the Florida Keys. Floral diversity and abundance are greater on Raccoon Key than on Key Lois. Average maximal and minimal temperatures per month did not vary significantly between Raccoon Key and Key Lois over the 3-year period. Average minimal temperatures per month on Key Lois, but not Raccoon Key, varied significantly between years. There were no significant variations in either the amount or the dates of rainfall over the 3-year period for the study area. A combined total of 1524 births was recorded for Raccoon Key (N = 879) and Key Lois (N =645). The birth season on Raccoon Key began 6 weeks earlier than on Key Lois. Births were associated with warmer, rainier months on both islands. Conceptions were associated with cooler, drier months at both study sites. No significant correlations were found between the date of the onset of the summer rains and either median conception or median birth dates on Raccoon Key or Key Lois. Our results do not substantiate the hypothesis that the onset of rainfall, within the temporal period set by photoperiod, regulates seasonal reproduction in rhesus macaques. We suggest that reproductive seasonality in the study populations may be influenced by a variety of factors.     

Feeding habits of the rhesus monkeys (Macaca mulatta) of Jaipur and Galta,India

Between September 1987 and May 1988, the time budgets of two groups of rhesus monkeys were investigated. One group inhabited an old Observatory which is now a tourist attraction in the center of Jaipur, India. The other group lived in a hilly forest/temple complex on the outskirts of Jaipur known as Galta. Because it was believed that the monkeys of these two different areas ate different proportions of natural and provisioned food, it was expected that they would have different time budgets. To determine differences in time budgets, a combination of census taking and 10-minute interval scan samples were used to collect comparative data. The analysis of the data revealed that there were differences in the time budgets of the two groups — the Observatory monkeys foraged more, moved less, engaged in fewer aggressive acts, and slept less during the day than the Galta group. These differences are mainly attributed to the 1984–1987 drought, site differences in the variety of natural food resources, and the manner in which the monkeys are provisioned.     

Phylogeny of rheusus monkeys (Macaca mulatta) as revealed by mitochondrial DNA restriction enzyme analysis

Mitochondrial DNA, purified from 36 samples of 23 local populations which are widely distributed in Vietnam, Burma, and 10 provinces of China, has been analyzed to model the phylogeny of rhesus monkeys. The 20 local populations of China may represent nearly all major populations in China. Using 20 restriction endonucleases of 6-bp recognition, we observed a total of 50–61 sites in the various samples. By combining the cleavage patterns for each enzyme, the 36 samples were classified into 23 restriction types, each of which was found exclusively in the respective population from which samples were obtained. By combining the earlier study of Indian rheusus monkeys, phylogenetic trees, which have been constructed on the basis of genetic distance, indicate that rhesus monkeys in China, Vietnam, India, and Burma can be divided into seven groups. Integrating morphological and geographical data, we suggest that rhesus monkeys in China, Vietnam, and Burma may be classified into six subspecies—M. m. mulatta, M. m. brevicaudus, M. m. lasiotis, M. m. littoralis, M. m. vestita, and M. m. tcheliensis-and rhesus monkeys in India may be another valid subspecies.M. m. tcheliensis is the most endangered subspecies in China. Divergence among subspecies may have begun 0.9–1.6 Ma. The radiation of rhesus monkeys in China may have spread from the southwest toward the east. The taxonomic status of the Hainan monkey and the Taiwan monkey require further investigation.     

Determination of genetic status in a closed colony of rhesus monkeys (<Emphasis Type="Italic">Macaca mulatta</Emphasis>)

The long-term management of breeding colonies requires some measure of genetic diversity in the animal population. For the maintenance of breeding colonies of monkeys used for biomedical research, known pedigrees supply precise data to determine the genetic status of colonies. We present data of genetic analyses in an old closed colony of rhesus macaques (Macaca mulatta) that was established in 1932 with 100 animals. For more than 40 years, the animals were kept on an isolated island and, in 1980, single-male breeding groups were established. A total of 333 DNA samples of these animals were typed to 20 microsatellite markers using multiplex PCR in order to verify inbreeding coefficient () and level of heterozygosity. We found an average heterozygosity of 64% and obtained =–0.03293 (±0.00573). Our results indicate that the reproductive strategy used was effective because consanguineous breeding was avoided. A continuous genetic program must be carried out in order to obtain better quality primates for biomedical research.     

Increased numbers of neuroepithelial bodies (NEB) in lungs of fetal Rhesus monkeys following maternal dexamethasone treatment

Summary Numbers of neuroepithelial bodies in the lungs of fetal Rhesus monkeys increase in a dose-dependent manner when mothers are treated antenatally with dexamethasone. Maternal doses of 15 mg/kg result in numbers of neuroepithelial bodies in lungs of fetuses of 135-day gestational age not different from those of the mature control group at 162 days. Controls at 135 days are significantly different from those at 162 days. Serotonin immunoreactive neuroepithelial bodies were localized by immunocytochemistry.     

Infant-directed behavior in young rhesus monkeys: Sex differences and effects of prenatal androgens

Young (3–4 years old) laboratory-reared rhesus monkeys were observed in five 15-minute tests with 1–15-day-old infants. Males and females were equally likely to investigate infants. Females communicated more with infants by grin-lipsmacking and gurgling–-gestures that were not shown by any males. More females presented the ventrum to infants than did males. Females contacted infants more than did males by grooming, crouching over, and having full body contact with them. To see whether prenatal androgens produced the male pattern of response, we conducted similar tests with pseudohermaphrodites (prenatally androgenized genetic females) and neonatally castrated males. On most sexually dimorphic behaviors, pseudohermaphrodites behaved more like females than like males. Castrated males, like females and pseudohermaphrodites, crouched over infants more than did intact males. Castrated males differed from females only on one infant-directed response, the grin-lipsmack. These comparisons showed that defeminization of the repertoire of infant-directed responses was measurable only in intact males. We conclude accordingly that prenatal androgens alone are not responsible for defeminization of this repertoire and that a contribution from postnatal androgens is likely to be necessary.     

Live birthrates in two free-ranging rhesus breeding colonies in the Florida keys

The present paper provides an analysis of reproductive data derived from 1,265 adult female rhesus monkeys (Macaca mulatta), including 570 animals 13 years old and older. The data were collected during a partial census of two provisioned but free-ranging rhesus populations in the Florida Keys. Within both colonies, live birthrates were found to increase sharply among females 4–7 years old and to decline linearly among females 7–17 years of age. These data do not support the suggestion byAnderson (1986) that decline in fertility among nonhuman primate females is primarily the result of deteriorating health rather than ageper se.     

Copper,iron, manganese,and zinc content of hair from two populations of rhesus monkeys

The concentrations of the elements copper (Cu), iron (Fe), manganese (Mn), and zinc (Zn) in hair of caged (in Maryland) and freeranging (in Puerto Rico) rhesus monkey populations were determined. Significant chronological age-related decreases were evident for the trace elements Mn and Zn in both populations (P<0.01) and for Cu and Fe in free-ranging monkeys (P<0.005). The only overall gender difference was higher hair Mn concentration in freeranging males than in females (P<0.03). There were no significant differences in hair Cu, Fe, or Mn related to pregnancy status. Hair Zn was lower in samples from pregnant than from nonpregnant monkeys from the caged monkeys (P≤0.05), but did not differe in the freeranging monkeys. Comparison of the two populations revealed that hair Zn levels were significantly higher in caged vs free-ranging animals (P<0.001). We attribute this higher hair Zn in the caged monkeys to contact and ingestion of Zn from their galvanized enclosures. Hair iron levels were significantly higher (P<0.001) in free-ranging monkeys, possibly as a result of Fe-rich soil ingestion from their environment. These data support continued investigation of the use of hair as an indicator of the exposure of large groups or populations to potentially high levels of specific minerals, and the use of nonhuman primates as models for the study of trace element deficiency and/or toxicity in humans. Prelliminary reports of portions of these data were presented at the 69th Annual Meeting of the Federation of American Societies for Experimental Biology, April 1982, New Orleans, LA (B. M. Marriott, J. C. Smith, R. Jacobs, A. O. Jones, M. J. Kessler, and R. Rawlins,Fed. Proc. 41:770, [1982]) and in a symposium at the 6th Annual Meeting of the American Society of Primatologists, 1983, East Lansing, MI (B. Marriott, J. C. Smith, R. Jacobs, A. O. Lee Jones, R. Rawlins, and M. J. Kessler,Am. J. Primatol. 4(3): 157 [1983]; B. Marriott, J. C. Smith, Jr., R. M. Jacobs, A. O. Lee Jones, R. Rawlins, and M. J. Kessler, inThe Cayo Santiago Macaques, R. Rawlins and M. J. Kessler, eds., SUNY Press, Albany, NY, pp. 219–231 [1986]).