Seasonal and individual predictors of diet in a free‐ranging population of mandrills

Deciphering the dietary habits of a species is central to understanding its ecology, resource requirements, and the evolution of its life history traits. Detailed information on how primates use their environment to address their nutritional needs is available for many primate species. Such basic, but necessary data are, however, fragmented for secretive primates, especially regarding direct behavioral observations of individuals. In this study, we evaluated the impact of seasonality and demographic characteristics on diet and feeding habits in the only free‐ranging population of habituated mandrills (Mandrillus sphinx), a forest‐dwelling species inhabiting the dense humid forests of Central Africa. We collected fine‐grained quantitative data on feeding behavior of 57 individually‐recognized animals of both sexes and different age classes during a 17‐month period. We identified most consumed plant species and determined their abundance in the habitat of the studied mandrills. We showed that diet in this species was extremely diverse and included approximately 150 different plant species, but also mushrooms, invertebrates, and vertebrates. This omnivorous and highly diverse diet presented, however, a clear frugivorous tendency. While we identified three food items largely consumed throughout the year, we also found a strong seasonal signature on diet that was partly, but not only, related to food availability. Age and sex also influenced feeding habits with some feeding specializations according to the individual categories considered and their associated nutritional needs. Our quantitative data provide a basis for future studies examining the nutritional and mineral content of food items, which will further elucidate important aspects of the ecology of this little studied forest primate.     

Grooming Between Male Chimpanzees at Ngogo,Kibale National Park. II. Influence of Male Rank and Possible Competition for Partners

Allogrooming contributes to the development and maintenance of social relationships, including those that involve alliances, in many primate species. Variation in relatedness, dominance rank, and other factors can produce variation in the value of others as grooming partners. Several models have been developed to account for variation in the distribution of grooming in relation to dominance ranks. These start from the premise that individuals are attracted to high-ranking partners, but time limits, direct competition, and prior grooming engagement between high-ranking individuals can constrain access to them. Sambrook et al. (1995) formalized some of these models and showed the importance of taking group size variation into account when assessing them. Chimpanzees form multimale communities in which males are the philopatric sex. Males commonly associate and groom with each other; they also form dominance hierarchies and form alliances that influence dominance ranks and mating success. Both male rank and the rank distance between partners are significantly correlated with the distribution of grooming between males in an extremely large chimpanzee community at Ngogo, Kibale National Park, Uganda, that has more males than any other known community. High-ranking males had more grooming partners than mid- or low-ranking males. Grooming predominantly went up the dominance hierarchy, but was also concentrated among males that were close in rank. Rank and rank distance apparently both affected grooming independently of reciprocity in grooming and independently of the frequency with which males associated in temporary parties. However, the data do not clearly indicate how constraints on access to partners might have operated. Published data from a smaller chimpanzee community at Mahale show no rank or rank distance effect on male grooming. These results and earlier, conflicting findings on the association between dominance rank and grooming in male chimpanzees indicate that variation in group size, i.e., the number of males per community, probably influences the strength of any such effects, as happens for grooming between females in several cercopithecine species. Data on coalitions at Ngogo support the argument that high-ranking males are valuable social partners, and similarity in strategies of alliance formation may influence the distribution of grooming.     

Grooming in mandrills and the time frame of reciprocal partner choice

In this study, we examined the time frame of reciprocal partner choice in the grooming interactions of captive mandrills (Mandrillus sphinx) in order to test the hypothesis that the cognitive limitations of primates constrain the occurrence of reciprocation to short time intervals. In contrast to this hypothesis, mandrills groomed preferentially those individuals that groomed them more even when cases of immediate reciprocation were excluded from the analysis. These results show that mandrills were not limited to reciprocating grooming over short time intervals. It is proposed that a system of emotional bookkeeping may support the ability of primates to reciprocate over long time frames. Am. J. Primatol. 71:884–888, 2009. © 2009 Wiley‐Liss, Inc.     

Factors affecting fecal glucocorticoid levels in semi-free-ranging female mandrills (Mandrillus sphinx)

Subordinate female cercopithecine primates often experience decreased reproductive success in comparison with high-ranking females, with a later age at sexual maturity and first reproduction and/or longer interbirth intervals. One explanation that has traditionally been advanced to explain this is high levels of chronic social stress in subordinates, resulting from agonistic and aggressive interactions and leading to higher basal levels of glucocorticoids. We assessed the relationships among fecal cortisol levels and reproductive condition, dominance rank, degree of social support, and fertility in female mandrills (Mandrillus sphinx) living in a semi-free-ranging colony in Franceville, Gabon. Lower-ranking females in this colony have a reproductive disadvantage relative to higher-ranking females, and we were interested in determining whether this relationship between dominance rank and reproductive success is mediated through stress hormones. We analyzed 340 fecal samples from 19 females, collected over a 14-month period. We found that pregnant females experienced higher fecal cortisol levels than cycling or lactating females. This is similar to results for other primate species and is likely owing to increased metabolic demands and interactions between the hypothalamus-pituitary-adrenal axis, estrogen, and placental production of corticotrophin releasing hormones during pregnancy. There was no influence of dominance rank on fecal cortisol levels, suggesting that subordinate females do not suffer chronic stress. This may be because female mandrills have a stable social hierarchy, with low levels of aggression and high social support. However, we found no relationship between matriline size, as a measure of social support, and fecal cortisol levels. Subordinates may be able to avoid aggression from dominants in the large enclosure or may react only transiently to specific aggressive events, rather than continuously expecting them. Finally, we found no relationship between fecal cortisol levels and fertility. There was no difference in fecal cortisol levels between conceptive and nonconceptive cycles, and no significant relationship between fecal cortisol level and either the length of postpartum amenorrhea or the number of cycles before conception. This suggests that the influence of dominance rank on female reproductive success in this population is not mediated through chronic stress in subordinate females, and that alternative explanations of the relationship between social rank and reproduction should be sought.     

Rank and grooming reciprocity among females in a mixed-sex group of captive hamadryas baboons

In a mixed-sex, captive group of hamadryas baboons (Papio hamadryas hamadryas) we investigated whether female grooming relationships are affected by their dominance ranks. Seyfarth's [1977] grooming for support model and Barrett et al.'s [1999] biological market model both predict that in primate groups where competition for monopolizable resources is high, grooming among females is based, at least partly, on the interchange of grooming for rank-related benefits, and that rank thus influences the distribution of grooming in females. Contrary to this prediction, our results show that despite the existence of a linear dominance hierarchy, rather strict dominance relationships, and high food-related aggression rates, grooming among female hamadryas baboons is not affected by rank and is only exchanged for itself. This is understandable since rank differences in our study group only result in differential access to limited, preferred food items that are not actively shared. Although some females are more likely to tolerate one another at the food pile, this tolerance is not determined by their grooming efforts and interchange of grooming for rank-related benefits does not occur. We conclude that female hamadryas baboons groom others in order to be groomed by them, which is supported by our observation that grooming reciprocity within a dyad increases when more grooming occurs in this dyad. Our results indicate that grooming is indeed a valuable commodity in itself, probably because of its stress- and tension-reducing effect. Based on our findings, the existing groom trade model is extended to include circumstances in which monopolizable resources are available but are not traded for grooming.     

Social and seasonal influences on the reproductive cycle in female mandrills (Mandrillus sphinx)

We present 12 years of perineal swelling data for a semifree-ranging colony of mandrills (Mandrillus sphinx), and evaluate the influence of rank, parity, and seasonality on reproductive parameters. Female sexual swellings showed a seasonal pattern, with August the median month of ovulation. Overlapping periovulatory periods did not decrease the likelihood of conception. Females showed their first genital swelling at age 3.6 years (n = 28; range, 3.2-4.6 years), and higher-ranking females experienced their first swelling earlier than low-ranking females. Median postpartum amenorrhea (PPA) duration was 208 days (n = 92; range, 74-538 days). PPA was longer in primiparous females than in multiparous females, but PPA duration was unrelated to female rank. Median follicular phase duration was 24 days for the first cycle after parturition (n = 84; range, 12-40 days), shortening to 17 days in subsequent cycles (n = 55; range, 6-39 days). The follicular phase was longer in nulliparous females than in parous females, but was unrelated to female rank. Median cycle length (from one sexual swelling breakdown to the next) was 38 days (n = 57; range, 18-108 days). Eighty-seven percent of conceptions occurred within two cycles, and half of the nulliparous females conceived during their first swelling cycle. Lower-ranking females were more likely to require more cycles to conceive than higher-ranking females. The cycling phase was significantly longer in nulliparous females than in parous females, and was also significantly longer in lower-ranking females than in higher-ranking females. We discuss the influence of provisioning on female reproductive parameters, the influence of parity and rank on the different phases of the interbirth interval, and the evolution of long and variable follicular phases in mandrills.     

Dominance hierarchy and social grooming in female lion- tailed macaques (Macaca silenus) in the Western Ghats, India

This article reports the structure of dominance and its relationship with social grooming in wild lion-tailed macaque females. The strength of dominance hierarchy was 0.79 on a scale of 0 to 1 indicating a moderate linearity in the ranking system. Dominance scores were converted into an ordinal as well as an interval scale. Grooming scores were also converted into interval scales using standard scores. Grooming received and grooming given correlated positively and negatively respectively with dominance ranks indicating that high ranking females received more and gave less grooming. Grooming was also positively related to encounter rates for dyads of females. More grooming among adjacent ranks, and grooming being more reciprocal, occurred only in the case of dominant females. The grooming patterns, therefore, appeared to be more of despotic than egalitarian nature. While ranking macaques into different Grades of social systems ranging from despotic to egalitarian, Thierry (2004) has placed lion-tailed macaques in Grade 3 corresponding to the ‘relaxed’ social system. Our results indicate that the grooming and dominance relationships in this species are more despotic, and hence, the Grade for this species requires to be shifted toward 2 or 1.     

Reciprocity and partner preference in grooming of female blue monkeys

Grooming among adult and older juvenile females in a wild group of blue monkeys (Cercopithecus mitis stuhlmanni) is analyzed and related to agonistic behavior. Both grooming and agonistic behavior were less frequent than would be expected in baboon and macaque groups. Fair shares of grooming were given and taken, both within and between interactions, in amost dyads, and all females were seen to groom with at least half the others. The reciprovity of grooming was its most outstanding feature. There was no evidence that grooming was preferentially directed at kin. Frequent grooming partnerships fell into two clusters, one of which ranked higher than the other. We suggest that grooming throughout the group helps to establish a coherent team of females which effectively, defends its territory in daily encounters at the boundaries with neighboring groups.     

Social grooming in Tonkean macaques (Macaca tonkeana)

The distribution, form, and contexts of occurrence of social grooming were studied in two captive groups of Tonkean macaques (Macaca tonkeana), using interaction-dependent sampling. The social events surrounding grooming had little influence on its form, the participants' behavior being shaped mainly by physical constraints. Adult females were most often involved in grooming interactions. Grooming between adult females appeared more intimate than that between adult males and females. Kinship and dominance had no effect on the form or distribution of social grooming among adult females. It is concluded that social systems that are characterized by mild dominance relations allow individuals the freedom to interact in the way and with whom they wish.     

Peaceful primates: affiliation, aggression, and the question of female dominance in a nocturnal pair-living lemur (Avahi occidentalis)

Affiliation/agonism and social dominance are central factors determining social organization in primates. The aim of our study is to investigate and describe, for the first time, the intersexual relations in a nocturnal and cohesive pair‐living prosimian primate, the western woolly lemur (Avahi occidentalis), and to determine to what extent phylogeny, activity mode, or the cohesiveness of pair partners shape the quality of social interactions. Six pairs of western woolly lemurs were radio‐collared in the dry deciduous forest of northwestern Madagascar. More than 874 hr of focal animal sampling were conducted. All occurrences of social interactions involving a focal animal were recorded. The rate of affiliation between pair partners was significantly higher than the rate of agonism. Western woolly lemur pairs' interactions were extremely peaceful. All decided agonistic conflicts (N = 15) were exclusively initiated and won by the female. No female showed spontaneous submission toward her male partner. These results are in line with those of diurnal cohesive pair‐living anthropoid primates. Findings support the hypothesis that social relations in pair‐living primates are linked to the cohesiveness of pair partners in time and space irrespective of phylogeny and activity mode. Am. J. Primatol. 73:1261–1268, 2011. © 2011 Wiley Periodicals, Inc.     

Feeding Competition and Agonistic Relationships Among Bwindi <Emphasis Type="Italic">Gorilla beringei</Emphasis>

Testing predictions of socioecological models, specifically that the types of feeding competition and social relationships female primates exhibit are strongly influenced by the distribution, density, and quality of food resources, requires studies of closely related populations of subjects living under different ecological conditions. I examined feeding competition and the resulting female social relationships in mountain gorillas (Gorilla beringei beringei) of Bwindi Impenetrable National Park, Uganda, which has ecological conditions distinctive from those where other gorilla populations live. I observed 1 group of gorillas for 29 mo to examine the proportion of time spent foraging on fruit, the relationship between patch size and occupancy patterns of fruit trees, and agonistic interactions. Patch occupancy time while foraging in fruit trees decreased with increasing number of gorillas in a tree and decreasing tree size, suggesting that fruit trees represent limiting patches and can lead to intragroup scramble competition. Gorillas exhibited higher levels of aggression while feeding on fruit versus other food resources, which indicates intragroup contest competition. I observed a linear dominance hierarchy with no bidirectionality via displacements, and a similar hierarchy via aggression, though a notable proportion of the dyads contained 2-way interactions. However, most aggression was of low intensity (vocalizations) and the recipient typically ignored it. Despite differences in ecological conditions and diet between the Virunga Volcanoes and Bwindi, agonistic relationships among females are largely similar in the 2 populations and are best characterized as dispersal individualistic.     

Alpha male chimpanzee grooming patterns: implications for dominance “style”

In social primates, individuals use various tactics to compete for dominance rank. Grooming, displays and contact aggression are common components of a male chimpanzee's dominance repertoire. The optimal combination of these behaviors is likely to differ among males with individuals exhibiting a dominance “style” that reflects their tendency to use cooperative and/or agonistic dominance tactics. Here, we examine the grooming behavior of three alpha male chimpanzees at Gombe National Park, Tanzania. We found that (1) these males differed significantly in their tendency to groom with other males; (2) each male's grooming patterns remained consistent before, during and after his tenure as alpha, and (3) the three males tended to groom with high‐ middle‐ and low‐ranking partners equally. We suggest that body mass may be one possible determinant of differences in grooming behavior. The largest male exhibited the lowest overall grooming rates, whereas the smallest male spent the most time grooming others. This is probably because large males are more effective at physically intimidating subordinates. To achieve alpha status, a small male may need to compensate for reduced size by investing more time and energy in grooming, thereby ensuring coalitionary support from others. Rates of contact aggression and charging displays conformed to this prediction, suggesting that each male exhibited a different dominance “style.” Am. J. Primatol. 71:136–144, 2009. © 2008 Wiley‐Liss, Inc.     

Age-related differences in social grooming among adult female Japanese monkeys ( Macaca fuscata)

The present study investigated the influence of dominance rank in combination with kinship on age-related differences in social grooming among adult females in a free-ranging group of Japanese monkeys (Macaca fuscata). Eighty-three adult females were divided into six sub-groups according to age-class (younger: 5–9 years old; middle: 10–14 years old; older: 15–22 years old) and dominance rank (high and low rank). The ratio of the number of unrelated females that each female groomed to the total number of available unrelated females and grooming bouts which she gave to unrelated females decreased with increasing age for both high- and low-ranking females, whereas age did not appear to affect corresponding values for related females. On the other hand, compared with low-ranking females, high-ranking females of all age-classes received grooming more often from a larger number of unrelated females. Moreover, older females of low rank received grooming less often from a smaller number of unrelated females than younger females of low rank. These results indicate that with increasing age females are more likely to concentrate on related females when they have grooming interactions with other females. This tendency seems to be more apparent for low-ranking females. Moreover, the present findings also indicate that older high-ranking females could maintain their social attractiveness as high as younger high-ranking females.     

Grooming-at-a-distance by exchanging calls in non-human primates

The ‘social bonding hypothesis'' predicts that, in large social groups, functions of gestural grooming should be partially transferred to vocal interactions. Hence, vocal exchanges would have evolved in primates to play the role of grooming-at-a-distance in order to facilitate the maintenance of social cohesion. However, there are few empirical studies testing this hypothesis. To address this point, we compared the rate of contact call exchanges between females in two captive groups of Japanese macaques as a function of female age, dominance rank, genetic relatedness and social affinity measured by spatial proximity and grooming interactions. We found a significant positive relationship between the time spent on grooming by two females and the frequency with which they exchanged calls. Our results conform to the predictions of the social bonding hypothesis, i.e. vocal exchanges can be interpreted as grooming-at-a-distance.     

Arrested development of secondary sexual adornments in subordinate adult male mandrills (Mandrillus sphinx).

Previous studies of semifree-ranging mandrills identified two morphological and social variants of the adult male, based on behavioral and secondary sexual characteristics. "Fatted" males are social, with highly developed sex skin coloration, large testes, high plasma testosterone levels, and fat rumps; while "nonfatted" males are peripheral or solitary, with paler sex skin, smaller testes, lower plasma testosterone, and slimmer rumps. We present a detailed study of morphology and group association for 10 adult male mandrills, living in two semifree-ranging groups in Gabon, in order to relate differences between males to dominance rank. The results show that rather than existing as two distinct morphotypes, male mandrills represent a continuous spectrum of possibilities between social males with fully developed secondary sexual characteristics, and solitary males with muted secondary sexual characteristics. Alpha males (N = 2) had the highest testosterone levels, the most colorful sex skin, and the most active sternal glands, and were the only males to spend 100% of their time with the social group. Rank relationships between nonalpha males (N = 8) were not always clear, but all subordinate males had lower testosterone levels and less development of the secondary sexual adornments, and were less group-associated than alpha males. These findings suggest that only alpha males have sufficient testosterone to develop full secondary sexual characteristics, and we propose possible socioendocrine mechanisms underlying the suppression of testosterone and secondary sexual development in subordinate adults. We discuss differences in secondary sexual development in relation to reproductive strategies, and discuss the evolution of alternative reproductive morphs in primates.     

Competition, breeding success and ageing rates in female meerkats

Competition between females is particularly intense in cooperatively breeding mammals, where one female monopolises reproduction in each group. Chronic competition often affects stress and may therefore have long-term consequences for fitness, but no studies have yet investigated whether intrasexual competition has effects of this kind and, in particular, whether it affects rates of reproductive senescence. Here, we use long-term data from a wild population of meerkats to test whether reproductive success and senescence in dominant females are affected by the degree of intrasexual competition experienced prior to dominance acquisition. Females that experienced greater competition had lower breeding success and higher rates of reproductive senescence. Furthermore, females that were evicted from the group more frequently as subordinates had lower breeding success when dominant. We conclude that the intense intrasexual competition between females in cooperatively breeding groups may carry fitness costs over a longer period than is usually recognised.     

Competition for resources mediated by intrinsic social dominance in sympatric finches

Gouldian Erythrura gouldiae and Long‐tailed Finches Poephila acuticauda are morphologically and ecologically similar sympatric species, for which social dominance relationships are likely to determine access to critical limiting resources. Building on previous research showing that Long‐tailed Finches dominate competition for nest‐sites, I staged dyadic contests for food between the two species in captivity in order to test social dominance dynamics under controlled conditions. Long‐tailed Finches were likely to dominate interactions with Gouldian Finches and expressed higher levels of aggression while competing for access to food. These results suggest a stable dominance relationship between the two species which could be affecting Gouldian Finches' access to food resources in the wild, potentially constraining their ability to recover from recent population declines.     

Distribution of Grooming Among Adult Females in a Large,Free-Ranging Group of Japanese Macaques

We analyzed grooming episodes recorded among adult females in a large, provisioned, free-ranging group of Japanese macaques (Macaca fuscata) at an individual level. Each female groomed on average 10 of the other 84 females, and 54% of them devoted 50% of their grooming to a single female grooming partner, which indicates that most females had grooming interactions with a relatively small subset of available females. Although 65% of the total grooming bouts were between related females, 25% of females disproportionately groomed unrelated females, 22% groomed related and unrelated females equally, and grooming was kin-biased for the remaining 53%. Moreover, 11 of 16 kin-groups included at least one female that groomed unrelated females significantly more often than related females. In 18% of unrelated dyads, grooming was directed down the hierarchy, in 58%, grooming was well-balanced between the two females, and in the remaining 25%, grooming was directed up the hierarchy. The results indicate that although Japanese macaques are considered a despotic species based on their dominance style, this group included some females that showed egalitarian tendencies, i.e., grooming was directed down the hierarchy or was well-balanced, and was directed toward unrelated females as often as or more often than toward related females. The presence of egalitarian individuals might be important to maintain a well-organized, female-bonded group.