Post-conflict behaviour among wild long-tailed macaques (Macaca fascicularis)

Summary A procedure originally developed for the study of post-conflict behaviour in captive groups was used to study a group of long-tailed macaques (Macaca fascicularis) in the wild. During 5 months, 156 post-conflict observations on victims of agonistic conflicts were collected and compared with matched-control observations. The findings reported previously for a captive group of the same species were confirmed. After a conflict victims scratched themselves more often and received more attacks than in control periods. Reconciliation and redirection were found to be characteristic of post-conflict situations. Their occurrence seemed to follow similar patterns in captivity and in the wild. The frequency of reconciliation, but not that of redirection, seemed to be lower after conflicts over food than in other situations. No evidence for consolation was found. In the wild, victims have the option of leaving the (sub)group in order to avoid the former aggressor. No evidence for this behaviour was actually found, but within the (sub)group victims tended to keep the former aggressor at a distance. Victims also seemed to suffer ecological costs in that they spent less time foraging than in control periods.     

Ecological constraints on the behaviour of mother long-tailed macaques (Macaca fascicularis)

Summary The ecological consequence of the effects of different social conditions on the behaviour of females with infants were examined in two different-sized groups of long-tailed macaques (Macaca fascicularis) that inhabited adjacent home ranges in Gunung Leuser National Park in Indonesia. This study aims to test predictions of the within-group competition/predation avoidance hypothesis of social organization. Females, particularly those carrying an infant, are considered to experience the most direct effects of environmental constraints on fitness prospects. Data on maintenance behaviour, height in canopy and spatial position were collected for five mothers in a small group and eight mothers in a large group. Comparisons were made on the basis of group size and dominance rank. Mothers from the large group spent less time feeding on clumped fruits and more time foraging on dispersed food items. Lower-ranking mothers, undergoing the highest rate of within-group competition, foraged most. For macaques in the study area, predation risk is considered to decrease with height in the canopy. Mothers in the small group, assumed to be more susceptible to predation, remained substantially higher in the canopy than mothers in the large group. In both groups, mothers adjusted their height to their spatial position in the group. Lower-ranking mothers were more often found without neighbours, presumably to avoid feeding competition. As a result they stay higher in the canopy than higher-ranking mothers. The results clearly demonstrate that individual females in the same reproductive state and living in the same area, but in different social environments, adapted their behaviour according to the hypothesis. Correspondence to: D.R. Vos     

Mate-guarding constrains feeding activity but not energetic status of wild male long-tailed macaques (Macaca fascicularis)

Mate-guarding is an important determinant of male reproductive success in a number of species. Little is known however about the constraints of this behaviour, e.g. the associated energetic costs. We investigated these costs in long-tailed macaques where alpha males mate guard females to a lesser extent than predicted by the priority of access model. The study was carried out during two mating periods on three wild groups living in the Gunung Leuser National Park, Indonesia. We combined behavioural observations on males’ locomotion and feeding activity, GPS records of distance travelled and non-invasive measurements of urinary C-peptide (UCP), a physiological indicator of male energetic status. Mate-guarding led to a decrease in feeding time and fruit consumption suggesting a reduced intake of energy. At the same time, vertical locomotion was reduced, which potentially saved energy. These findings, together with the fact that we did not find an effect of mate-guarding on UCP levels, suggest that energy intake and expenditure was balanced during mate-guarding in our study males. Mate-guarding thus seems to not be energetically costly under all circumstances. Given that in strictly seasonal rhesus macaques, high-ranking males lose physical condition over the mating period, we hypothesise that the energetic costs of mate-guarding vary inter-specifically depending on the degree of seasonality and that males of non-strictly seasonal species might be better adapted to maintain balanced energetic condition year-round. Finally, our results illustrate the importance of combining behavioural assessments of both energy intake and expenditure with physiological measures when investigating energetic costs of behavioural strategies.     

Sneak copulations in long-tailed macaques (Macaca fascicularis): no evidence for tactical deception

Sexual competition is highly prevalent within multi-male multi-female primate groups and may lead to copulations in absence of potentially interfering bystanders. Such avoidance of bystanders may result from tactical deception or from simpler mechanisms such as taking advantage of encountered situations without bystanders, operant conditioning or a peripheral positioning of non-alpha males. We investigated which individuals are avoided as bystanders, how individuals react to the presence of bystanders and whether copulation partners separate themselves from the group in a tactical way. Our observations of a group of 15 female and seven male long-tailed macaques housed in three interconnected, but visually separated compartments revealed that both males and females can interrupt sexual behaviour and that bystanders of both sexes were avoided during copulations (n?=?256). The strength of the effect of bystanders tended to decrease with the dominance rank of male bystanders, but did not depend on the dominance rank of female bystanders. The audience effects of non-alpha individuals did not depend on the strong audience effect of the alpha male in combination with proximity with the alpha male. The effects that we found for separate bystanders suggest that sexual competition concerns rank dependent male–male competition and rank independent female–female competition. Additionally, both male and female copulation partners paid attention to the presence of bystanders and conducted fewer copulation solicitations in their presence. The timing of a male and female’s separation from the group suggests that exploitation of the peripheral position of non-alpha males, and not tactical deception, may cause these audience effects.     

Determinants of male reproductive success in wild long-tailed macaques (Macaca fascicularis)—male monopolisation, female mate choice or post-copulatory mechanisms?

One of the basic principles of sexual selection is that male reproductive success should be skewed towards strong males in species with anisogamous sex. Studies on primate multi-male groups, however, suggest that other factors than male fighting ability might also affect male reproductive success. The proximate mechanisms leading to paternity in multi-male primate groups still remain largely unknown since in most primate studies mating rather than reproductive success is measured. Furthermore, little research focuses on a female’s fertile phase. The aim of this study was to investigate the relative importance of male monopolisation and female direct mate choice for paternity determination. We also investigated the extent to which paternity was decided post-copulatory, i.e. within the female reproductive tract. We used a combined approach of behavioural observations with faecal hormone and genetic analysis for assessment of female cycle stage and paternity, respectively. The study was carried out on a group of wild long-tailed macaques living around the Ketambe Research Station, Gunung Leuser National Park, Indonesia. Our results suggest that both male monopolisation and post-copulatory mechanisms are the main determinants of male reproductive success, whereas female direct mate choice and alternative male reproductive strategies appear to be of little importance in this respect. Female cooperation may, however, have facilitated male monopolisation. Since paternity was restricted to alpha and beta males even when females mated with several males during the fertile phase, it seems that not only male monopolisation but also post-copulatory mechanisms may operate in favour of high-ranking males in long-tailed macaques, thus reinforcing the reproductive skew in this species.     

Information content of female copulation calls in wild long-tailed macaques (<Emphasis Type=Italic>Macaca fascicularis</Emphasis>)

Primates are unusual in that many females display sexual signals, such as sex skin swellings/colorations and copulation calls, without any sex role reversal. The adaptive function of these signals remains largely unclear, although it has been suggested that they provide males with information on female reproductive status. For sex skin swellings, there is increasing evidence that they represent a graded signal indicating the probability of ovulation. Data on the functional significance of copulation calls are much scarcer. To clarify the information content of such calls, we recorded copulation calls in wild long-tailed macaques (Macaca fascicularis) and analysed the structure of these calls during the ovarian cycle. Specifically, we correlated selected call parameters with the female oestrogen to progestogen ratio (obtained from faecal samples), which are known to be elevated during the female's fertile phase. In addition, we ran a general linear mixed model for these call parameters, testing factors (cycle phase, occurrence/absence of ejaculation, male dominance status, occurrence/absence of mate guarding) which potentially influence female copulation calls in primates. Our results show that copulation calls of female long-tailed macaques signal mating outcome and rank of the mating partner, but not female reproductive status. They also show for the first time on primates that copulation calls can convey information on whether a female is mate guarded or not. We suspect that the function of these calls is manipulation of male mating and mate-guarding behaviour and that in this way the degree of sperm competition and ultimately male reproductive success is influenced.     

Infanticide by resident males and female counter-strategies in wild Japanese macaques (Macaca fuscata)

Infanticide was observed for the first time in a wild, non-provisioned troop of Japanese macaques on Yakushima Island, Japan. Eight adult resident males attacked unweaned infants in the pre- and early mating season, and one infanticide was observed directly. These attacks were not consistent with the social pathology, side effect of male aggression, cannibalism, or the resource defense hypothesis, but were generally consistent with the sexual-selection hypothesis. First, most male attackers had risen in dominance rank because several high-ranking males had left the troop. Second, in 78% of cases, male attackers had not previously been observed to mate with the mothers of victims. Moreover, analysis of subject animal DNA showed that males did not attack their own offspring. The two mothers who lost their unweaned infants, however, were not subsequently observed to mate. In fact, almost no mating behavior was observed in the troop. This was most likely due to a poor fruiting year. Resumption of mating by females who lost their infants may have been inhibited by an intervening environmental variable which suppressed female reproductive function. These observations contribute to a growing body of evidence which suggests that sexually selected infanticide can occur in seasonally breeding, multi-male, multi-female primate groups. Female Japanese macaques are known to mate with multiple males. We found evidence that female mating with multiple males inhibits contact aggression towards their infants. Adult males attacked infants eight times more often when they had not previously mated with the mother. Received: 2 September 1999 / Received in revised form: 27 April 2000 / Accepted: 3 May 2000     

The social behavior of Leptothorax allardycei (Hymenoptera,Formicidae): time budgets and the evolution of worker reproduction

Summary The use of time by workers of the ant Leptothorax allardycei (Mann) is examined. Theoretical predictions are developed concerning the maximal lowering in colony reproductive output that is consistent with the evolution of worker production. Measurements are made of the effect of aggression on colony efficiency. Analysis of time budgets indicate that a typical ant spends a large fraction (0.55) of its time quiescent and another large fraction of time (0.32) involved in undifferentiated activity. Dominance activity and brood care together make up about 11% of the total time. The amount of time spent on dominance activity is negatively related to the amount of time spent on brood care, but positively related to the amount of time that an ant is active. The amount of time that an ant has available for brood care which is actually spent on brood care declines with the amount of time spent on dominance activity. The amount of time that a worker spends feeding liquid food to larvae is a function of hierarchy rank; alpha spends the most time, beta less and gamma still less. The spread of the trait of worker reproduction is examined theoretically, with particular regard to the associated costs to colony reproduction. Worker reproduction can spread through a population, under a variety of formulations, provided the cost to colony reproduction is less than some critical value in the neighborhood of 0.17–0.22 of the total colony output. The cost of worker reproduction in L. allardycei is estimated in two ways: as a time cost and as a reduction in the total number of brood tended per unit time. The two estimates of cost are 0.15 and 0.13 respectively. The reproductive options of the worker caste and the division of reproductive labor vary considerably between species. Reproduction by workers yields fitness differences between workers and results in competition among workers with the result that colony efficiency is affected.     

Sex-specific reproductive behaviours and paternity in free-ranging Barbary macaques (Macaca sylvanus)

In a wide variety of species, male reproductive success is determined by contest for access to females. Among multi-male primate groups, however, factors in addition to male competitive ability may also influence paternity outcome, although their exact nature and force is still largely unclear. Here, we have investigated in a group of free-ranging Barbary macaques whether paternity is determined on the pre- or postcopulatory level and how male competitive ability and female direct mate choice during the female fertile phase are related to male reproductive success. Behavioural observations were combined with faecal hormone analysis for timing of the fertile phase (13 cycles, 8 females) and genetic paternity analysis (n = 12). During the fertile phase, complete monopolisation of females did not occur. Females were consorted for only 49% of observation time, and all females had ejaculatory copulations with several males. Thus, in all cases, paternity was determined on the postcopulatory level. More than 80% of infants were sired by high-ranking males, and this reproductive skew was related to both, male competitive ability and female direct mate choice as high-ranking males spent more time in consort with females than low-ranking males, and females solicited copulations mainly from dominant males. As most ejaculatory copulations were female-initiated, female direct mate choice appeared to have the highest impact on male reproductive success. However, female preference was not directly translated into paternity, as fathers were not preferred over non-fathers in terms of solicitation, consortship and mating behaviour. Collectively, our data show that in the Barbary macaque, both sexes significantly influence male mating success, but that sperm of several males generally compete within the female reproductive tract and that therefore paternity is determined by mechanisms operating at the postcopulatory level.     

Digit ratio (2D:4D) and dominance rank in female rhesus macaques (Macaca mulatta)

Female rhesus macaques exhibit matrilineal dominance structures, and high dominance rank confers fitness benefits across a lifetime and across generations. Rank effects are “inherited” through social processes that are well understood; however, biological mechanisms that might impact these processes are not well known. Recently, it has been shown that prenatal androgens appear to be implicated in supporting dominance rank hierarchies in some mammals. In humans, interindividual differences in the second (index) to fourth (ring) digit ratio (2D:4D) have been linked indirectly to variation in prenatal androgens, with low 2D:4D in both sexes associated with higher inferred prenatal androgen effects. 2D:4D has also been related to dominant social behavior and has been shown to co-vary with social systems across nonhuman primate species. Here, we investigate how 2D:4D co-varies with socially inherited dominance rank in female rhesus macaques. Low 2D:4D was associated with higher-ranking females, while higher 2D:4D was associated with lower-ranking females. Similar relationships were also shown between ranked families within matrilines. This is the first study to show such a relationship between 2D:4D and dominance rank in a nonhuman primate and suggests that prenatal androgen effects could be involved in the maintenance of dominance rank in female cercopithecine primates.     

Maternal investment in rhesus macaques (Macaca mulatta): reproductive costs and consequences of raising sons

Maternal investment in offspring is expected to vary according to offspring sex when the reproductive success of the progeny is a function of differential levels of parental expenditure. We conducted a longitudinal investigation of rhesus macaques to determine whether variation in male progeny production, measured with both DNA fingerprinting and short tandem repeat marker typing, could be traced back to patterns of maternal investment. Males weigh significantly more than females at birth, despite an absence of sex differences in gestation length. Size dimorphism increases during infancy, with maternal rank associated with son’s, but not daughter’s, weight at the end of the period of maternal investment. Son’s, but not daughter’s, weight at 1 year of age is significantly correlated with adult weight, and male, but not female, weight accounts for a portion of the variance in reproductive success. Variance in annual offspring output was three- to fourfold higher in males than in females. We suggest that energetic costs of rearing sons could be buffered by fetal delivery of testosterone to the mother, which is aromatized to estrogen and fosters fat accumulation during gestation. We conclude that maternal investment is only slightly greater in sons than in daughters, with mothers endowing sons with extra resources because son, but not daughter, mass has ramifications for offspring sirehood. However, male reproductive tactics supersede maternal investment patterns as fundamental regulators of male fitness. Received: 23 July 1999 / Received in revised form: 23 February 2000 / Accepted: 13 March 2000     

Paternal kin bias in the agonistic interventions of adult female rhesus macaques (Macaca mulatta)

When agonistic interventions are nepotistic, individuals are expected to side more often with kin but less often against kin in comparison with non-kin. As yet, however, few mammal studies have been in a position to test the validity of this assertion with respect to paternal relatedness. We therefore used molecular genetic kinship testing to assess whether adult female rhesus macaques (Macaca mulatta) from the free-ranging colony of Cayo Santiago (Puerto Rico) bias their interventions in ongoing dyadic aggressive interactions towards maternal and paternal half-sisters compared with unrelated females. It turned out that females supported maternal half-sisters significantly more often than paternal half-sisters or non-kin regardless of the costs associated with such interventions. Similarly, females targeted maternal half-sisters significantly less often than non-kin when this was associated with high costs. Unrelated females provided significantly higher mean rates of both high- and low-cost support to each other than did paternal half-sisters. However, females targeted paternal half-sisters significantly less often than non-kin when targeting was at low cost, suggesting that females refrain from intervening against paternal half-sisters. Our data confirm the general view that coalition formation in female mammals is a function of both the level of maternal relatedness and of the costs of intervention. The patterns of coalition formation among paternal kin were found to be more complex, and may also differ across species, but clear evidence for paternal kin discrimination was observed in female rhesus as predicted by kin selection theory.     

Adaptive significance of sex ratio adjustment in semifree-ranging Barbary macaques (Macaca sylvanus) at Salem

Summary New data on the secondary sex ratio in semi-free-ranging Barbary macaques at Salem confirm the observation that the offspring of high-ranking females in this colony are biased towards sons while the offspring of low-ranking females are biased towards daughters. Analysis of interbirth intervals yielded no consistent differences in the relative costs of rearing male and female offspring for either high- or low-ranking females. Survivorship to adulthood of male and female offspring born to mothers of all rank classes was remarkably high, and there was no indication that juvenile females of low-ranking mothers face any greater risk. Daughters of high- and low-ranking mothers showed no substantial differences in reproductive success, while mating and probably reproductive success of sons seemed to be dependent on maternal rank, at least at the beginning of their reproductive career. The results suggest that variation in sex ratio does increase parental fitness. Offprint requests to: A. Paul     

Dominance,kinship and reproductive value in female Barbary macaques (Macaca sylvanus) at Affenberg Salem

Summary In the course of a long-term study on social organization of semi-free-ranging Barbary macaques (Macaca sylvanus) at Affenberg Salem, genealogical and cross-genealogical rank relations of adult and adolescent females in three social groups were studied. Female rank was highly dependent on maternal rank, but the process of rank acquisition was also affected by age/size differences between members of different families. Mother-daughter rank reversal was rare, but all old, postreproductive matriarchs were outranked by their adult daughters. Contrary to findings of other studies on macaques, younger sisters seldom outranked older sisters. There was no genealogy with a strict age-inversed hierarchy among adult sisters as described for rhesus and Japanese macaques. Rank reversals between sisters were more frequent in genealogies with old or dead matriarchs, in large clans, and in dyads with an age difference of more than 1 year, indicating that demographic variables influence intra-genealogical dominance relations. It is suggested that close, long-lasting relationships between sisters and mothers and doughters impede rank reversals. Previous evolutionary models of female dominance relations in primates that explain rank relations among sisters as a function of their reproductive value or as a strategy of the mother to maintain her own status are not supported by the data. The results of this and other studies indicate that rank reversal between sisters is not as universal for Old World monkeys, or even macaques, as frequently proposed.     

Predation, scramble competition, and the vigilance group size effect in dark-eyed juncos (Junco hyemalis)

In socially feeding birds and mammals, as group size increases, individuals devote less time to scanning their environment and more time to feeding. This vigilance “group size effect” has long been attributed to the anti-predatory benefits of group living, but many investigators have suggested that this effect may be driven by scramble competition for limited food. We addressed this issue of causation by focusing on the way in which the scan durations of free-living dark-eyed juncos (Junco hyemalis) decrease with group size. We were particularly interested in vigilance scanning concomitant with the handling of food items, since a decrease in food handling times (i.e. scan durations) with increasing group size could theoretically be driven by scramble competition for limited food resources. However, we showed that food-handling scan durations decrease with group size in an environment with an effectively unlimited food supply. Furthermore, this food-handling effect was qualitatively similar to that observed in the duration of standard vigilance scans (scanning exclusive of food ingestion), and both responded to changes in the risk of predation (proximity of a refuge) as one might expect based upon anti-predator considerations. The group size effects in both food-handling and standard scan durations may reflect a lesser need for personal information about risk as group size increases. Scramble competition may influence vigilance in some circumstances, but demonstrating an effect of competition beyond that of predation may prove challenging. Received: 22 September 1998 / Received in revised form: 1 February 1999 / Accepted: 14 February 1999     

Maternal rank affects reproductive success of male Barbary macaques (Macaca sylvanus): evidence from DNA fingerprinting

Summary Paternity determination by oligonucleotide fingerprinting confirms that maternal rank affects the reproductive success of male Barbary macaques (Macaca sylvanus). High-born males began to reproduce significantly earlier and sired significantly more infants surviving to at least 1 year of age during the first 4 years of their reproductive career than low-born males. This relation was independent of the natal/non-natal status of the males, and was not affected by external conditions such as the level of intrasexual competition or the number of fertilizable females. Since high-ranking females in this population produced significantly more male offspring than low-ranking females, the data on sex ratio adjustment and comparative breeding success of sons and daughters are consistent with the predictions of the Trivers-Willard hypothesis. Offprint requests to: A. Paul     

Collective group movement and leadership in wild black howler monkeys (Alouatta pigra)

Maintaining social cohesion through coordinating traveling time and direction is a primary benefit of group living in mammals. During a 15-month study, we investigated socioecological factors underlying leadership of collective group movements in three multimale–multifemale groups of black howler monkeys (Alouatta pigra) at Palenque National Park (PNP), Mexico. A total of 691 independent group movements across a variety of contexts were collected. Leadership of group movements was partially shared, with adult females initiating and leading group movements significantly more often than did adult males and juveniles, an outcome that has been observed among a diverse set of group living taxa. Adult females did not lead their group more often to feeding sites nor did they lead group movements more frequently when pregnant or lactating compared to when cycling, providing little evidence that energetic demands were the primary drivers underlying female leadership in this primate species. Instead, only one adult female in each social group was identified as a habitual leader of their group. These ‘leader’ females had the highest centrality eigenvectors among the adult group members in their group, suggesting an embedded leadership with the spatially widest connected adult group member emerging as recurrent leader of collective group movements.