Stress, social behaviour, and secondary sexual traits in a male primate

We examined variation in glucocorticoid levels in the mandrill, a brightly coloured primate species, to identify major social influences on stress hormones, and investigate relationships among glucocorticoid levels, testosterone and secondary sexual ornamentation. We collected a total of 317 fecal samples for 16 adult male mandrills over 13 months, including mating and non-mating periods and periods of both dominance rank stability and instability, and compared fecal glucocorticoid levels with dominance rank, rank stability, presence of receptive females, gastro-intestinal parasite infection, fecal testosterone and facial red coloration. Glucocorticoid levels did not vary systematically with dominance rank, but increased when the dominance hierarchy was unstable, and increased in the presence of receptive females. The relationship between dominance rank and glucocorticoid levels changed direction according to the stability of the dominance hierarchy: glucocorticoid levels were higher in subordinate males under stable conditions, but under conditions of instability higher ranking males had higher glucocorticoid levels. The influence of dominance rank also interacted with the presence of receptive females: glucocorticoids were higher in dominant males than in subordinates, but only during mating periods, suggesting that dominant males are more stressed than subordinates during such periods. These findings support previous studies showing that the relationship between glucocorticoids and dominance rank in male baboons is dependent on the social environment. We also found that males with higher glucocorticoids suffered a higher diversity of gastrointestinal parasite infection, in line with evidence that glucocorticoids suppress the immune system in other species. However, we found no support for the stress-mediated immunocompetence handicap hypothesis for the evolution of condition-dependent ornaments: glucocorticoid and testosterone levels were positively related, rather than the negative relationship predicted by the hypothesis, and we found no relationship between red colour and glucocorticoid levels, suggesting that glucocorticoids do not play a role in translating social conditions or physical health into ornament expression in this species.     

Effects of reproductive and social variables on fecal glucocorticoid levels in a sample of adult male ring-tailed lemurs (Lemur catta) at the Beza Mahafaly Reserve, Madagascar

Glucocorticoids, a group of adrenal hormones, are secreted in response to stress. In male primates, variables such as breeding seasonality, dominance hierarchy stability, and aggressive and affiliative interactions can affect glucocorticoid levels. In this study, we examined interindividual differences in mean fecal glucocorticoid (fGC) levels among males in three groups of wild ring-tailed lemurs to better understand the physiological costs of group living for males in a female-dominant species that exhibits strict reproductive seasonality. Fecal and behavioral data samples were collected during one mating and two postmating seasons (2001 and 2003). The mean fGC levels were examined in relation to reproductive season, male rank, number of resident males, intermale and female-male agonism, and affiliative behavior with females. The mean fGC levels were not significantly elevated during mating season compared to the postmating period. During the mating season, male dominance hierarchies broke down and rank effects could not be tested; however, there was no relationship between male rank and fGC levels in the postmating periods. In 2001, males that resided in the group with the fewest males exhibited lower fGC levels during the postmating period. They also affiliated more with females than did males in the other groups. During the mating season of 2003, males engaged in more affiliative behaviors with females compared to the postmating season, but female-male agonism did not differ by season. However, rates of intermale agonism were significantly higher during mating compared to postmating periods, but such heightened agonism did not translate to a higher stress response. Thus, neither male-male competition for mates nor heightened agonism between males during the breeding season affected male fGC levels. Fewer males residing in a group, however, did have some effect on male-female affiliation and male fGC levels outside of the mating period. Males that live in a group with only a few (two or three) males may experience less physiological stress than those that live in groups with more males.     

Influence of reproductive season and rank on fecal glucocorticoid levels in free-ranging male Verreaux's sifakas (Propithecus verreauxi)

Studies in anthropoid primates and other mammals suggest that reproductive season, rank, reproductive skew, aggression received, and social support are the major factors influencing glucocorticoid output. In which way these are also affecting adrenal function in lemurid primates has been studied rarely. Here, we examine the influence of reproductive season and rank on glucocorticoid output in male sifakas (Propithecus verreauxi), a species characterized by high breeding seasonality, a hierarchy among males and extreme reproductive skew towards dominant males. We established a fecal assay for non-invasively monitoring adrenal activity and collected 315 fecal samples during the reproductive and birth season from 10 male sifakas living in 5 groups in Western Madagascar. We found a significant effect of season on glucocorticoid output, with males exhibiting higher fecal glucocorticoid levels during the reproductive compared to the birth season in conjunction with an increase in overall aggression rates during the former period. Moreover, our data indicate a significant effect of rank on adrenocortical activity with dominant males exhibiting higher glucocorticoid levels than subordinate males in the reproductive season. However, dominant males did not differ significantly in rates of initiated or received aggression and rates of affiliative behavior from subordinates but showed significantly lower rates of submission. Given their highly formalized dominance relationships, we conclude that higher glucocorticoid output in dominant males during the 4-month reproductive season is likely related to higher energetic demands necessary to cope with the challenges of male reproduction rather than to physical demands of increased fighting frequency to maintain dominance status. High rank in sifakas may thus carry high costs, which, however, may be outweighed by monopolization of almost all paternities. In sum, our data generally support the findings on the relationship between environmental and social factors and glucocorticoid output found in non-lemurid primates.     

Social correlates of testosterone and ornamentation in male mandrills

We investigated relationships between fecal androgen concentrations, facial coloration and behaviour in semi-free-ranging male mandrills. We found that fecal androgen levels were significantly positively related to dominance rank, independent of rank stability and the mating period, suggesting that male mandrills live in a permanently aggressive context in which they must actively maintain their dominance status. Facial red coloration was also significantly related to both fecal androgen levels and rank, with high ranking males having both higher androgen levels and redder faces, although dominant males did not always have the highest androgen levels or the reddest faces. Predictive relationships between androgen levels, coloration and rank were short-term. Androgen concentrations and facial redness both increased in the presence of receptive females, as did the former during periods of rank instability. We conclude that male facial redness is likely to represent an honest signal (to other males) of current androgen status, competitive ability and willingness to engage in fights and that females may also use this to assess male condition. Further, our findings provide support for the “challenge hypothesis” as originally proposed for birds by Wingfield.     

Effects of environmental conditions, human activity, reproduction, antler cycle and grouping on fecal glucocorticoids of free-ranging Pampas deer stags (Ozotoceros bezoarticus bezoarticus)

In this study, a commercial enzyme immunoassay (EIA) was validated in detecting glucocorticoids in Pampas deer feces, in order to investigate the influence of several factors on the adrenocortical function. Fecal samples, behavioral data and information concerning male grouping and antlers status were collected at a monthly basis during a 1 year period from free-ranging stags living at Emas National Park, Brazil (18 degrees S/52 degrees W). The results revealed that concentrations of fecal glucocorticoids in winter were significantly higher than those corresponding to spring and summer. In addition, dry season data presented higher levels than during the wet season. Significant difference was found between fecal levels of breeding stags in summer and nonbreeding stags, whereas no difference was observed between breeding stags in winter and nonbreeding stags. On the other hand, males from areas with frequent human disturbance exhibited higher glucocorticoid concentrations and flight distances than individuals from areas of lower human activity. Males with antlers in velvet had elevated levels compared with animals in hard antler or antler casting. Also, we found that glucocorticoid levels were higher in groups with three or more males than in groups with only one male. The flight distances showed positive correlation with fecal glucocorticoid. These data indicate that fecal glucocorticoid provides a useful approach in the evaluation of physiological effects of environment, inter-individuals relationship and human-induced stressors on free-ranging Pampas deer stags.     

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.     

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.     

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.     

Male Response to Female Ovulation in White-Faced Capuchins (Cebus capucinus): Variation in Fecal Testosterone,Dihydrotestosterone, and Glucocorticoids

Reproductive success is linked to dominance in male primates, reflecting the benefits of male competition. However, not all males compete successfully, suggesting that the costs of obtaining and maintaining high dominance status are significant. Here we examine the fecal metabolites of testosterone (fT) and dihydrotestosterone (fDHT) as bioactive androgens reflecting male reproductive effort, as well as fecal glucocorticoid (fGC) excretion as an index of stress in male white-faced capuchins (Cebus capucinus). We investigated the influence of female fertility (periovulatory vs. nonovulatory) on the hormonal responses of alpha and subordinate males. Over a 17-mo field season, we collected and analyzed weekly fecal samples (N = 992) from all 14 adult (> 10 yr) and subadult (≥ 6–10 yr) males residing in three study groups in the Santa Rosa Sector of the Área de Conservación Guanacaste, Costa Rica. Fecal samples (N > 2250) were also collected from group females (N = 28) to identify the fertile period using progesterone and estradiol assays. Alpha males had significantly higher fT, fDHT, and fGC levels than subordinate males independent of female reproductive state; further, adult subordinates had significantly higher fT, but not fDHT or fGC, than subadult subordinates. Male fT, fDHT, and fGC levels were significantly higher in the presence of fertile females, regardless of male dominance status and age. These findings indicate that the higher reproductive effort of alpha males comes with some costs (increased fGCs), and the presence of periovulatory females is associated with specific endocrine responses reflecting male reproductive effort and stress in white-faced capuchins.     

季节和等级顺位对雄性黄山短尾猴粪样皮质醇水平的影响

在长期的进化选择压力下,灵长类动物大多数群居生活,群体中的动物个体也面临来自群内成员强度不一的社会压力,压力大小的重要生理指标通常用其体内的皮质醇水平的变化来衡量。季节性繁殖的黄山短尾猴（Macaca thibetana）,群体内的个体有严格的社会等级,是研究等级顺位与社会压力水平之间关系的理想研究对象。我们采集13只野生短尾猴雄性个体的新鲜粪便样品,并测定其皮质醇水平。本研究发现,雄性短尾猴的粪便皮质醇水平表现为交配季节显著高于非交配季节。在交配季节,中等顺位雄性个体的皮质醇水平显著高于高顺位个体和低顺位个体,而在非交配季节3种等级类型的雄性个体之间则无显著差异。本研究首次测定了野生短尾猴的粪便皮质醇含量,并分析了季节、等级顺位对粪便皮质醇含量的影响。     

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.     

The Association of Intergroup Encounters,Dominance Status,and Fecal Androgen and Glucocorticoid Profiles in Wild Male White‐Faced Capuchins (Cebus capucinus)

Androgens play a role in male reproductive competition, frequently via aggression, while glucocorticoids are associated with the stress response. However, the relationships of these hormones with different sources of competition (intra‐ vs. intergroup) and dominance status are highly variable. Here, we consider the fecal androgen (fA) and glucocorticoid (fGC) profiles of alpha and subordinate male Cebus capucinus in the context of intergroup competition during a rare period of low intragroup competition (i.e. all females were either pregnant or lactating). Intergroup encounters (IGEs) are a long‐term reproductive strategy in male white‐faced capuchins, enabling them to assess the composition of neighboring groups. IGEs pose a threat to resident males as these can result in injury or death, loss of dominance rank, group eviction, and group takeovers that are frequently associated with infanticide. From February to July 2007, fecal samples were collected from eight males in three groups of white‐faced capuchins in the Santa Rosa Sector of the Área de Conservación Guanacaste, Costa Rica. IGE rate was positively associated with both fA and fGC levels, indicating that IGEs are perceived as reproductive challenges by resident males, and may be associated with elevated metabolic costs. Alpha males sire the majority of group offspring and, accordingly, the threat of IGEs to both future (via rank loss or eviction) and current (via infanticide) reproductive success is greater than for subordinate males. Consistent with this observation, alpha males had higher fA and fGC levels than subordinate males. Given that all females were either pregnant or lactating and pronounced overt intragroup competition was absent, we interpret the difference in hormone profiles of alpha and subordinate males as being primarily associated with variation in the perceived threats of IGEs according to dominance status. Future studies should focus on the interaction of intra‐ and intergroup competition by examining hormone levels in the presence of periovulatory females. Am. J. Primatol. 75:107‐115, 2013. © 2012 Wiley Periodicals, Inc.     

Female dominance status and fecal corticoids in a cooperative breeder with low reproductive skew: ring-tailed lemurs (Lemur catta)

Many studies have shown that low dominance status within a social group is associated with elevated glucocorticoid hormone production, a common index of physiological stress. However, the reverse may be true among cooperatively breeding female mammals with high reproductive skew; that is, high dominance status is associated with elevated glucocorticoid levels. Elevated glucocorticoid levels in these dominant females may be a product of their being the only breeder within a group or may result from other challenges associated with high status. To test this difference, we studied fecal corticoid levels in cooperative breeding females with low reproductive skew (i.e., where reproduction is not limited to dominant group members): ring-tailed lemurs (Lemur catta). We collected behavioral and fecal corticoid data from 39 ring-tailed lemur females from eight groups across three sites. In seven of the eight groups, either one or both of the two most dominant females (ranks 1 and 2) exhibited the highest fecal corticoid levels in the groups. The best predictor of corticoid levels in high-ranking females was the proportion of aggressive agonistic interactions they initiated. For the lower-ranking females the best predictors of elevated corticoid levels were being the recipient of aggressive attacks and being relatively close to one's nearest neighbors. These results differ from many studies of caged male mammals where subordinate individuals often exhibit the highest glucocorticoid levels of a group. Furthermore, the results indicate that reproduction itself is not the primary reason for higher glucocorticoid levels among dominant cooperative-breeding females, but that some other factor must account for these elevated levels.     

Social cues and hormone levels in male Octodon degus (Rodentia): a field test of the Challenge Hypothesis

Social interactions are important factors determining and regulating individual behaviors. Testosterone has been related to agonistic interactions, while glucocorticoids have been related to social stress, especially during interactions of dominance. We compared testosterone and cortisol concentrations in male degus (Octodon degus, Rodentia) under laboratory conditions without male social interactions, with data from wild males in nature. Under natural conditions, males should present higher levels of testosterone during the breeding season due to social interactions (Challenge Hypothesis). Alternatively, intense social instability could act as a stressing environment, raising glucocorticoids, which inhibit testosterone concentrations. Our results show a significant increase in agonistic interactions between males during the breeding season, and disappearance of non-agonistic male interactions during this period. Hormone levels in breeding season show nonsignificant differences between laboratory groups, but testosterone concentrations in field males were significantly higher than in laboratory males. Testosterone levels were similar among pre-breeding and breeding periods, but in field animals the concentration was approximately 30% higher than in laboratory degus. In field animals, we found two different mating strategies: resident males, with territorial behavior, and transient males, displayed an opportunistic approach to females. Finally, cortisol presents a similar pattern in both laboratory and field animals; pre-breeding values of cortisol are higher than during the breeding season. This suggests that social interactions in O. degus activate a rise in testosterone, supporting the Challenge Hypothesis, and could be considered as partial support of the Social Stress Hypothesis.     

Social correlates of variation in urinary cortisol in wild male bonobos (Pan paniscus)

Cortisol excretion in males of group living species is often associated with social rank and competition for oestrous females. Rank-related patterns of cortisol levels can be used to study mechanisms of rank maintenance and costs associated with mate competition. Bonobos (Pan paniscus) are interesting because males form a linear dominance hierarchy but are not dominant over females and therefore aggressive male-male competition over access to females alone is not considered to be a successful reproductive strategy. In this study on social correlates of urinary cortisol in wild male bonobos, we investigated the relationship between cortisol levels and several aspects of mate competition, including male rank, aggression rates, and association time with oestrous females. We found that cortisol levels correlated positively with dominance rank when oestrous females were present, but not when they were absent. This result is consistent with the idea that aggressive behaviour plays a minor role in maintenance of high rank. While aggression received from males and females explained within-individual variation in cortisol levels, it was the time spent in association with oestrous females that best explained between-individual variation in male cortisol levels. The observed increase in male cortisol may be associated with spatial proximity to oestrous females and could result from anticipated aggression from other group members, reduced feeding time in the males, or a combination of both.     

Coping with a challenging environment: effects of seasonal variability and reproductive status on glucocorticoid concentrations of female baboons (Papio cynocephalus)

Environmental stressors impact physiology and behavior in many species of animals. These effects are partly mediated through changing concentrations of glucocorticoids, which also vary with reproductive state and social conditions. Prior research has focused largely on seasonal breeders, but the close temporal linkage between season and reproductive state in these species hinders ability to disentangle environmental effects from those of the animal's reproductive status. Here we assessed the effects of environmental challenges on the fecal glucocorticoid (fGC) levels of non-seasonal breeders, female baboons (Papio cynocephalus) of Amboseli, Kenya. Amboseli is characterized by a long dry season, during which food and water become scarce, and by extreme temperatures above 40 °C in the shade during some months of the year. We found that after accounting for female reproductive status and individual variability, females exhibited higher fGC levels during the dry season than during the wet season. Further, during the wet season, fGC levels were higher in months of high average daily maximum temperatures. During the dry season, fGC levels were elevated both in hotter months and in months during which the baboons spent a relatively high proportion of time feeding. In spite of these stressors, female baboons reproduce during all months of the year in Amboseli, unlike most other mammals in this environment. This may be attributable to their extreme adaptability, specifically their diversified diet, and their ability to modify their behavior, including their activity profiles.     

Olfactory communication and the importance of different odour sources in the ferret (Mustela putorius f. furo)

Olfactory communication has a major role in solitary carnivores, particularly during the breeding season. Scent-marking behaviour in ferret (Mustela putorius f. furo) has been well studied, but not the significance of the deposited odours for the animal. We compared the interest in urogenital, anal and body odours of opposite-sex conspecifics between male and female ferrets and investigated both sexes’ discrimination ability (familiar vs. unfamiliar) for these three opposite-sex odours and the use of its ability by females during the breeding season. Males are more interested than females in the urogenital odour of the opposite sex. Male body odour probably did not interest females and males are somewhat interested in the female one. However, anal odour of the opposite sex is as interesting for males as for females and both sexes are able to discriminate familiar anal odour from an unfamiliar one. Moreover, females could use this ability when they must choose to have some sensory contact between olfactory familiar and unfamiliar males since they prefer to be in contact with the former. These results are coherent with behavioural differences observed between male and female solitary mustelids in the field and in captivity, and the consortship success of resident males compared to roaming males.     

Hormonal Correlates of Social Rank in an Asocial Species, the Common Brushtail Possum (Trichosurus vulpecula)

Dominance hierarchies play an important role in access to mates or resources in many species. Rank is sometimes correlated with circulating testosterone levels or morphological traits such as body weight. The relationship of glucocorticoid secretion and rank, however, is less clear. In this study, we investigated the relationship of male rank to body weight, circulating testosterone and cortisol concentrations in captive possum triads (Trichosurus vulpecula). We carried out two experiments to examine hierarchy formation and the effects of castration of the dominant male during the non‐breeding season. A third experiment measured the effects of removal of the dominant male from a stable hierarchy during the breeding season. We found that dominant male rank was significantly correlated with higher circulating testosterone levels during periods of hierarchy formation and during the breeding season but not during periods of hierarchy stability in the non‐breeding season. Lack of correlation between plasma testosterone concentration and rank after male castration suggests that stable social rank is not dependent on hormone level and may be more dependent on behavioural traits. Any biocontrol measures that rely on manipulation of hormone levels may be unreliable when applied to unstable hierarchical situations, including the establishment of territories by subadult males, and the pre‐breeding season when circulating testosterone concentrations peak in males and a period of hierarchy establishment may occur.     

Allostatic load, social status and stress hormones: the costs of social status matter

Cooperation and social support are the major advantages of living in social groups. However, there are also disadvantages arising from social conflict and competition. Social conflicts may increase allostatic load, which is reflected in increased concentrations of glucocorticoids. We applied the emerging concept of allostasis to investigate the relation between social status and glucocorticoid concentrations. Animals in a society experience different levels of allostatic load and these differences may predict relative glucocorticoid concentrations of dominant and subordinate individuals. We reviewed the available data from free-ranging animals and generated, for each sex separately, phylogenetic independent contrasts of allostatic load and relative glucocorticoid concentrations. Our results suggest that the relative allostatic load of social status predicts whether dominants or subordinates express higher or lower concentrations of glucocorticoids. There was a significant correlation between allostatic load of dominance and relative glucocorticoid concentrations in both females and males. When allostatic load was higher in dominants than in subordinates, dominants expressed higher levels of glucocorticoids; when allostatic load was similar in dominants and subordinates, there were only minor differences in glucocorticoid concentrations; and when allostatic load was lower in dominants than in subordinates, subordinates expressed higher levels of glucocorticoids than dominants. To our knowledge, this is the first model that consistently explains rank differences in glucocorticoid concentrations of different species and sexes. The heuristic concept of allostasis thus provides a testable framework for future studies of how social status is reflected in glucocorticoid concentrations.     

The costs of dominance: testosterone, cortisol and intestinal parasites in wild male chimpanzees

Background

Male members of primate species that form multi-male groups typically invest considerable effort into attaining and maintaining high dominance rank. Aggressive behaviors are frequently employed to acquire and maintain dominance status, and testosterone has been considered the quintessential physiological moderator of such behaviors. Testosterone can alter both neurological and musculoskeletal functions that may potentiate pre-existing patterns of aggression. However, elevated testosterone levels impose several costs, including increased metabolic rates and immunosuppression. Cortisol also limits immune and reproductive functions.

Methods

To improve understanding of the relationships between dominance rank, hormones and infection status in nonhuman primates, we collected and analyzed 67 fecal samples from 22 wild adult male chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda. Samples were analyzed for cortisol and testosterone levels as well as intestinal parasite prevalence and richness. 1,700 hours of observation data were used to determine dominance rank of each animal. We hypothesized that dominance rank would be directly associated with fecal testosterone and cortisol levels and intestinal parasite burden.

Results

Fecal testosterone (but not cortisol) levels were directly associated with dominance rank, and both testosterone and cortisol were directly associated with intestinal parasite richness (number of unique species recovered). Dominance rank was directly associated with helminth (but not protozoan) parasite richness, so that high ranking animals had higher testosterone levels and greater helminth burden.

Conclusions

One preliminary interpretation is that the antagonist pleiotropic effects of androgens and glucocorticoids place a cost on attaining and maintaining high dominance rank in this species. Because of the costs associated with elevated steroid levels, dominance status may be an honest signal of survivorship against helminth parasites.