Aggression in adult male primates: A comparison of confined Japanese macaques and free-ranging olive baboons

The frequencies and types of adult male aggressive behavior of confined Japanese macaques (Macaca fuscata)and free-ranging olive baboons (Papio anubis)were compared. The baboons, which do not have a mating season, were more aggressive to conspecific males than were the macaques during their nonmating season. The baboons also solicited aid during aggressive encounters more frequently than the macaques. However, during their mating season, the macaques were more aggressive to conspecific females than were the baboons. The macaques were also involved in more triadic sequences of aggression, and the frequency of occurrence of these patterns supported Chase’s theory of dominance hierarchy formation and maintenance. The differences in aggressive behavior appeared to be related to the seasonal reproductive cycle of the macaques.     

Grooming and aggression in captive Japanese macaques

This study investigated the relations between allogrooming and aggression in a captive group of Japanese macaques (Macaca fuscata). Our aim was to test whether evidence of an interchange between allogrooming and a reduction in aggression could be identified at a group level. Female Japanese macaques did not direct less aggression to those group mates that groomed them most. Although generally they did not direct more grooming to those group mates that attacked them most, they did show increased grooming towards those nonkin group mates that showed the most aggression. These results are interpreted in light of the conflicting processes that are likely to underlie macaque social choices.     

Intrasexual selection and male mating strategies in baboons and macaques

If baboon and macaque mating systems constitute a form of female defense polygyny, male mating strategies should be intrasexually selected and should vary in predictable ways with female defensibility, and demographic factors which affect the numbers of competing males per estrous female in populations. Substantial behavioral evidence exists for intrasexual selection of male mating strategies in baboons and macaques. Limited evidence also offers tentative support for theorybased predictions about the relationship between male mating strategy and female defensibility. Although male dominance rank generally predicts mating success, there are a number of factors which tend to increase the success of subordinate males above that expected from a simple dominance-based model of priority of access to mates.     

Endocrine correlates of rank,reproduction, and female-directed aggression in male Japanese macaques (Macaca fuscata)

Fecal testosterone and cortisol levels in six wild male Japanese macaques (Macaca fuscata), three of high rank and three of low, were analyzed to investigate the hormonal correlates of rank, reproduction, and female-directed aggression. The study encompassed the 6-month mating season, from October 1999 to March 2000, during which time 251 fecal samples and approximately 550 h of behavioral data were collected. Dominant males were not found to differ from subordinate males in overall rates of aggressive or copulatory behavior. Likewise, testosterone excretion, which peaked in the early part of the mating season and declined gradually thereafter, did not differ significantly by rank. High-ranking males, however, were observed to excrete significantly higher levels of cortisol than low-ranking males, suggesting that dominance may carry costs. The two hormones were found to be inversely correlated in the two most dominant males, but independent in all others. Rate of noncontact aggression was significantly correlated with testosterone, while no significant relationships were observed between testosterone and contact aggression nor any aspect of copulatory behavior. These data further support the contention that social subordinance and stress are not inexorably linked, as well as suggest that elevated glucocorticoid concentrations in high-ranking males may reflect increased metabolic costs associated with dominant male reproductive strategy.     

Use of females by male olive baboons (Papio anubis)

Wild male olive baboons (Papio anubis) used females and infants as agonistic buffers. Male residency status determined whether a male used females or whether they were used against him. The success of the strategy depended on the cooperation of the female and the context of the interaction. Female cooperation correlated with preexisting social affiliation with the male user. Male choice of female or infant buffers represented a compromise between the potential effectiveness of each in different situations and the social and spatial availability of females and infants. Nonreproductive social relationships may provide long-term strategic benefits to the individuals who invest in them.     

Characteristics of hamadryas-like male baboons living in anubis baboon troops in the Awash hybrid zone, Ethiopia.

In the twenty-two years since the Awash baboon hybrid zone was first described, about 25-30 hamadryas or hamadryas-like hybrid males have taken up residence in anubis baboon groups. Most enter as mature adults, though some may immigrate as juvenile followers. Long-term tracking of known immigrants indicates that they may reside for four years or more in their adopted troop, during which time they establish a series of comparatively short-term harems, and probably sire hybrid offspring. "Abductions" of anubis females to hamadryas troops, as postulated by early observers, were not seen, though their occurrence cannot be ruled out. Younger, more recent immigrants tend to be "purer" hamadryas in phenotype, perhaps reflecting a more distant origin, or a change in the composition of neighboring hamadryas populations. Coexisting hamadryas and anubis show no signs of reproductive isolation by behavioral barriers, and evidently belong to a single "recognition species."     

Greeting,aggression, and coalitions between male baboons: Demographic correlates

Interactions of asymmetrical, symmetrical, and unreciprocated greeting, and episodes of aggression and coalitions observed between 18 males, members of a large multi-harem colony of baboons (Papio hamadryas, P. cynocephalus, and their hybrids) housed in the Madrid Zoo, were recorded throughout 11 time blocks between January 1983 and March 1985. The major question investigated was whether the demographic characteristics of the colony affected the frequency with which males used three behavioural strategies, namely, greeting, aggression, and coalitions. It was found that under demographic conditions eliciting more intense male-male competition, for example, when the ratio of oestrous cycles per adult male was lower, males exchanged frequent greetings, especially the symmetrical form (i.e. notifying) and solicited more coalitions, but did not show any significant change in rates of dyadic aggression. Male phenotype-related effects on rates of greeting and coalitions were found as well. Results are discussed in relation with the suggested role of greeting and of coalition behaviour as strategies used in the negotiation of changes in competitive social relationship (e.g. consort changeovers). These strategies are regarded as social tactics alternative to direct aggression.     

Effects of natal male alliances on aggression and power dynamics in rhesus macaques

In the wild, male rhesus macaques disperse at sexual maturity. In captivity, however, males cannot disperse from their natal groups. Thus, the presence of natal males in captive rhesus social groups is unnatural and has the potential to negatively influence group dynamics and stability. A primary difference between natal males and non-natal (immigrant) males is that natal males have the opportunity to form long-term alliances with their maternal kin as well as nonkin. We investigated the factors associated with natal males' kin alliances and the impact of these alliances on measures of natal male behavior, group dynamics, and group stability. We found that natal males more frequently formed alliances with maternal kin when they were from high-ranking matrilines, had more siblings, and were younger. More frequent kin alliances were associated with more frequent use of intense aggression, higher individual rank, and higher degree of integration within the male displacement network. Thus, it seems that natal males use their alliances to be more active and influential in the social group, which may affect group stability. It appears that juvenile natal males from high-ranking matrilines, in particular, have the largest impact on group stability. Younger natal males from high-ranking matrilines formed alliances with kin more frequently and used intense aggression more frequently than older or lower ranking males. Furthermore, groups with a higher proportion of juvenile males from high-ranking matrilines also had higher rates of wounding. We suggest that the presence of natal males in rhesus groups may act in opposition to group stability.     

Female mating strategy in an enclosed group of Japanese macaques

Female Japanese macaques (Macaca fuscata) are noted for mating with multiple males and for their ability to exert mate choice. In a captive group of Japanese macaques housed at the Primate Research Institute of Kyoto University, Japan, behavioral and endocrine data were combined to examine female mating strategies. During one breeding season, daily behavioral observations were conducted on females who exhibited copulatory behavior. Blood was collected from females twice weekly and their ovulatory periods estimated by analyzing hormone profiles. Females began mating shortly before ovulation, peaked at ovulation, and continued receiving ejaculations for up to ten weeks after conception. Females were more responsible than males for inbreeding avoidance with matrilineal kin. Males sometimes approached females from their own matriline, but females avoided such males and expressed mate choice behavior preferentially toward non-matrilineal males. Over the entire mating season, females did not choose non-matrilineal males on the basis of displays, dominance rank, age, weight, or weight change during the mating season. When females were likely to conceive, however, they expressed mate choice behavior toward males who displayed most frequently. Female mating strategy may include both mate choice at ovulation and other, non-procreative functions.     

Female testosterone, dominance rank, and aggression in an Ethiopian population of hybrid baboons

Studies on the relationship between female testosterone (T) measures and behavior, particularly in free-ranging primate populations, remain scant. In this study we used fecal steroid analysis to examine the effects of seasonal, reproductive, and social factors on female T in a group of free-ranging hybrid baboons (Papio sp.) in the Awash National Park of Ethiopia. We collected behavioral and hormonal data from 25 adult females across an 11-month period. Solid phase extraction and radioimmunoassay (RIA) techniques were used to quantify T in 776 fecal samples collected weekly from each female. The results indicate that 1) the females had elevated T during pregnancy and during the wet season relative to other periods, 2) female dominance rank was positively related to T measures, and 3) female T and aggression were positively related within subjects but not across subjects. Higher T concentrations during pregnancy are consistent with other published profiles of pregnancy in primates. In combination with data on foraging, wet season increases in T may indicate contest competition for females. The rank-T relationship may be mediated by supplants or aggression. Finally, we discuss the different interpretations of the hormone-behavior relationship based on within- and across-subject analyses.     

Female weight and reproductive condition in a population of olive baboons (Papio anubis)

The study reported here tested Altmann's prediction [Baboon Mothers and Infants. Cambridge, Harvard University Press, 1980] that lactating female baboons endure a weight loss. Data from 64 adult female olive baboons (Papio anubis) residing in six troops in Kenya revealed that reproductive condition was related to weight. Lactating females weighed less and pregnant females weighed more than cycling females. There was a negative correlation between the weight of cycling females and the number of months postweighing to their next conception. These results indicate that lactation in wild baboons imposes energy costs that result in lost weight. It is suggested that female baboons may have to surpass a minimum weight threshold prior to resumption of postlactational cycling and that nutritional status is more influential than rank in affecting female reproductive success.     

Female transfer in baboons

Eight of 19 identified adult females transferred over 7 years in a study of intertroop relations among Papio ursinus at Suikerbosrand. Only one of the eight was cycling at the time of transfer. Five of the seven recent mothers who transferred had lost their infants shortly before transferring. Females who transferred received no more aggression before or after their transfer than females who did not transfer. The most important factors determining this extraordinarily high rate of female transfer include subtrooping and absence of predation.     

Reproduction in wild female olive baboons

The purpose of this paper is to evaluate several factors that influence female reproduction in a large troop of wild olive baboons (Papio cynocephalus anubis) based on 4 consecutive years of demographic data. Interbirth intervals were significantly shorter for females whose infants died before their next conception than for females whose infants survived. High-ranking mothers of surviving infants had significantly shorter birth intervals than comparable low-ranking mothers, independent of maternal age. This occurred mainly because the interval from resumption of cycling to conception was significantly shorter for high-vs. low-ranking females. Dominance rank did not influence sex ratio at birth, infant survival in the first 2 years, or adult female mortality. Age was also significantly related to interbirth intervals, with older females having shorter intervals. Primiparous females had consistently longer reproductive intervals than did multiparous females, but this difference reached statistical significance only for females whose infants died before the next conception. Primiparous females also experienced significantly higher infant mortality. Data on body size and estrous cycle length indicated no differences between high- and low-ranking females. Nutritional and stress-related mechanisms that may underlie the reproductive advantages of high rank are discussed.     

Life history of male Japanese macaques living on Koshima Islet

In the study of Japanese macaques, two types of male transfer between groups, defined by the age of transfer and known as bottom- or top-rank transfer, have received much attention, whereas the meaning of the period of solitary life has received very little. Male solitary life has been regarded simply as a transient state between group transfer. We found that male solitary life is restricted to a specific period in the life history of Japanese macaques living on Koshima Islet. This period started when the body weights of males and females began to diverge and ended when the body weight increase of males had stopped. Solitary lifestyle is related to the growth of adolescent and post-adolescent males. We hypothesize that a solitary lifestyle is a necessary step for adolescent and post-adolescent males to achieve their full adult growth by avoiding feeding competition with others, especially with adult females. Increments of body weight increase between 3 and 15 years were larger for the sons of lower- and middle-rank females than for those of higher-ranking females. Although the sons of lower- plus middle-ranking females grew later, they achieved a full adult body weight similar to that of sons of higher-ranking females by the age of 15. We believe that this body weight increase was achieved because of the solitary lifestyle of adolescent and post-adolescent males. Correlation between male body weight and life-span was found for body weights at 12 years, but no correlation was evident at 6 years. Electronic Publication     

Dominance, aggression and physiological stress in wild male Assamese macaques (Macaca assamensis)

In group-living animals relative rank positions are often associated with differences in glucocorticoid output. During phases of social stability, when dominance positions are clear and unchallenged, subordinates often face higher costs in terms of social stress than dominant individuals. In this study we test this prediction and examine additional potential correlates of stress, such as reproductive season, age and amount of aggression received in wild, seasonally breeding Assamese macaques (Macaca assamensis). During a mating and a non-mating season we collected 394 h of focal observational data and 440 fecal samples of six adult and six large subadult males living in a multimale–multifemale group in their natural habitat in northeastern Thailand. The mating season was characterized by a general increase in aggressive behavior and glucocorticoid excretion across all males compared to the non-mating season. Among adult males, mating season glucocorticoid levels were significantly negatively related with dominance rank and positively with the amount of aggression received. Both relationships were non-significant among large subadult males. Thus, our results suggest that in adult Assamese macaques a high dominance position is not associated with high costs. Low costs of dominance might be induced by strong social bonds among top-ranking males, which exchange frequent affiliative interactions and serve as allies in coalitionary aggression against potentially rank-challenging subordinate males.     

Genetic polymorphisms of blood proteins in the troops of Japanese macaques,Macaca fuscata: VI. Serum transferrin polymorphism

As the serum transferrin polymorphism was observed in several macaque species, we considered it as one of the best markers for the study of population genetics of Japanese macaques,Macaca fuscata. In this work the genetic variants of transferrin (Tf) of 1,451 blood samples from 37 troops of this species were tested. The troops showing the variation of Tf were Fukushima, Yugawara T, Ihama, Ryozenyama, Mikata I and II, Takahama, Takahama (Otomi), Arashiyama A, Minoh A and B, Kohchi, Mihara, Shimane, and Tomogashima. The wild-type allele of this species was Tf F, and the variant alleles detected in these troops were E, G⁻, G, and H′. The alleles E, G and H′ were probably identical with those reported in several macaque species byIshimoto (1972), but the identification of allele G⁻ could not be done.     

Distribution of transferrin phenotypes in selected troops of Kenya baboons

The distribution of transferrin alleles in a group of common baboons, Papio cynocephalus of East Africa, was determined after starch gel electrophoresis of plasma and autoradiography of electrophoretograms. Three alleles, Tf^A, Tf^B, and Tf^C, were found, in agreement with results previously reported. The frequencies of these alleles are Tf^A = 0.276, Tf^B = 0.515, Tf^c = 0.209. The difference between the frequencies reported here and those reported by Buettner-Janusch (1963 Folia Primat., 1: 73–87) for the same species (Tf^A = 0.205, Tf^B = 0.332, Tf^c = 0.463) is significant. Transferrin of P. cynocephalus contains four residues of sialic acid per molecule of transferrin, as determined by electrophoresis and autoradiography of plasma treated with neuraminidase.     

Characterization of semen from olive baboons

Electroejaculation is an accepted method of semen collection from non-human primates and is typically performed using direct penile or rectal probe electro-stimulation. Six mature male olive baboons (Papio anubis) were subjected to rectal probe electro-stimulation procedure that yielded 65 usable ejaculates in 69 attempts over a period of 16 weeks. The four non-usable ejaculates consisted of seminal fluid without sperm cells and thus were not analysed. The analysis of ejaculate volume, concentration, % motility, liquefaction times, and morphology in this study has provided information on the quality of semen samples. It is anticipated that this analysis will provide valuable information for male fertility studies and the development of an in vitro fertilization (IVF) system in the olive baboon as a model for human IVF.     

Female reproductive signaling, and male mating behavior, in the olive baboon

Baboon sexual swellings are among the largest and most colorful signals displayed by any mammal, and many baboon studies have shown an association between sexual swellings and both female and male sexual behavior. However, the extent to which female behavior and sexual swellings combine to signal the timing of ovulation and the fertile period to males, and the extent to which males use these and other signals when determining patterns of mating behavior, remain key topics of research. Here we assess the social and sexual behavior of both female and male olive baboons with respect to detailed measures of swelling size made from digital photographs, measures of fecal progestogen and estrogen levels, and estimates of the timing of ovulation and the fertile period based on those levels. Female aggression and grooming behavior were unrelated to fecal progestogen and estrogen levels, but there were some significant relationships between these hormonal measures and presenting behaviors. Measures of female behavior collected during the study did not appear to reveal the timing of ovulation or the fertile period. Male consortship behavior was closely tied to fine-scale changes in sexual swelling size, but copulation behavior was not. Copulation behavior of consorting males was, however, linked to the timing of both ovulation and the fertile period, suggesting that males did have knowledge about these timings. Together these results suggest that males used fine-scale swelling size changes when deciding when to consort, but that consorting males did not use fine-scale swelling size changes in deciding when to copulate. We propose that swelling size may advertise the period during which males should consort with females, with other signals available only from closer inspection then used by consorting males to assess the timing of the fertile period more accurately. An important implication of this interpretation is that different males may have access to different signals of ovulation at any one time. Such a system would allow females to offer different males different information simultaneously, perhaps offering a solution to the ‘female dilemma’ of how females can simultaneously assure and confuse paternity in multi-male societies.