Joanna M. Setchell

Senescence rates are determined by ranking on the fast-slow life-history continuum

Comparative analyses of survival senescence by using life tables have identified generalizations including the observation that mammals senesce faster than similar-sized birds. These generalizations have been challenged because of limitations of life-table approaches and the growing appreciation that senescence is more than an increasing probability of death. Without using life tables, we examine senescence rates in annual individual fitness using 20 individual-based data sets of terrestrial vertebrates with contrasting life histories and body size. We find that senescence is widespread in the wild and equally likely to occur in survival and reproduction. Additionally, mammals senesce faster than birds because they have a faster life history for a given body size. By allowing us to disentangle the effects of two major fitness components our methods allow an assessment of the robustness of the prevalent life-table approach. Focusing on one aspect of life history - survival or recruitment - can provide reliable information on overall senescence.

Mate guarding and paternity in mandrills: factors influencing alpha male monopoly

We used long-term data on mate guarding and paternity in mandrills, Mandrillus sphinx, (1) to examine cycle day and cycle selection by males; (2) to examine associations between male rank, periovulatory mate guarding and paternity outcome; (3) to test the predictions of the priority-of-access model; and (4) to investigate factors influencing the ability of alpha males to monopolize females. Males mate-guarded on periovulatory days more than on other receptive days, and during conceptive cycles more than during nonconceptive cycles. Both periovulatory mate guarding and paternity outcome correlated significantly with male rank. Alpha males accounted for 94% of periovulatory mate guarding and 69% of paternity, confirming the existence of extremely high reproductive skew in this highly sexually dimorphic species. The fit of the observed distributions of mate guarding and paternity to predictions from the priority-of-access model was good, but in both cases the alpha males accounted for a greater proportion of reproduction than predicted. Mate guarding was a good predictor of paternity, but consistently overestimated the reproductive success of the alpha male. Splitting data into group-years revealed that the percentage of mate guarding by the alpha male decreased with increasing numbers of adult males, and the percentage of paternity decreased with increasing numbers of reproductive males (all postpubertal males). Furthermore, mate guarding became less effective as the number of reproductive males increased. We attribute this to the fact that only males aged 8 years or more mate-guarded, but that all males aged at least 3.8 years may sneak copulations, reducing the effectiveness of mate guarding and therefore reducing paternity concentration in the alpha male.

Reproductive parameters and maternal investment in mandrills (Mandrillus sphinx)

We report on 14 years of reproductive data for semifree-ranging mandrills (Mandrillus sphinx) in Gabon, and we explore relationships between female rank, age and parity, and reproductive strategies. Most births (61% of 132) occurred during the wet season in Gabon, between January and March. Female rank and parity were unrelated to the timing of parturition. Gestation lengths average 175 days (SE = ±1 day; N = 61) and were similar irrespective of female rank, parity, or sex of offspring. Birth sex ratio did not differ significantly from unity (52% male), and was unrelated to maternal rank or parity. Stillbirths and neonatal mortality tended to be more common among lower-ranking females than among either mid-ranking or dominant females. Median age at first birth is 4.71 years, at a median body mass of 7.6 kg, ca 5 years before females attain their adult body mass (median 12 kg). Age at first reproduction is significantly correlated with dominance rank, with dominant females giving birth on average 1.3 years earlier than lower-ranking females do. Interbirth intervals (IBI) average 405 days (range 184–1159 days, N = 103), and are independent of the sex of the offspring. Infant death within 6 months shortened IBI to 305 days. Increasing age and parity are also associated with short IBI, as is higher rank. Maternal rank and parity appear to influence reproductive success in female mandrills, but there is no apparent differential maternal investment by sex.

Impending extinction crisis of the world's primates: why primates matter

Impending extinction of the world’s primates due to human activities; immediate global attention is needed to reverse the trend. Nonhuman primates, our closest biological relatives, play important roles in the livelihoods, cultures, and religions of many societies and offer unique insights into human evolution, biology, behavior, and the threat of emerging diseases. They are an essential component of tropical biodiversity, contributing to forest regeneration and ecosystem health. Current information shows the existence of 504 species in 79 genera distributed in the Neotropics, mainland Africa, Madagascar, and Asia. Alarmingly, ~60% of primate species are now threatened with extinction and ~75% have declining populations. This situation is the result of escalating anthropogenic pressures on primates and their habitats—mainly global and local market demands, leading to extensive habitat loss through the expansion of industrial agriculture, large-scale cattle ranching, logging, oil and gas drilling, mining, dam building, and the construction of new road networks in primate range regions. Other important drivers are increased bushmeat hunting and the illegal trade of primates as pets and primate body parts, along with emerging threats, such as climate change and anthroponotic diseases. Often, these pressures act in synergy, exacerbating primate population declines. Given that primate range regions overlap extensively with a large, and rapidly growing, human population characterized by high levels of poverty, global attention is needed immediately to reverse the looming risk of primate extinctions and to attend to local human needs in sustainable ways. Raising global scientific and public awareness of the plight of the world’s primates and the costs of their loss to ecosystem health and human society is imperative.

Signal content of red facial coloration in female mandrills (Mandrillus sphinx)

Studies of secondary sexual ornamentation and its maintenance by sexual selection tend to focus on males; however, females may also possess showy ornaments. For example, female mandrills possess facial coloration that ranges from black to bright pink. We used fortnightly photographs of 52 semi-free-ranging females aged above 3 years over 19 months to evaluate whether colour conveys information concerning female competitive ability, reproductive quality, age or reproductive status. Colour was not related to female rank or quality (body mass index, age at first birth or mean inter-birth interval); however, colour did increase significantly with age and primiparous females were darker than multiparous females. Colour may therefore signal reproductive quality, as younger females are less fertile and produce smaller offspring. Colour was brighter during the follicular phase than during the luteal phase, suggesting that it may signal fertility. Colour also varied across gestation and peaked at four and eight weeks post-parturition, suggesting that it may signal approaching parturition and lactation. Future studies should examine the relationship between colour and the menstrual cycle in more detail, the hormonal basis of female colour, and determine experimentally whether mandrills of both sexes attend to differences in colour between and within females.

Do Female Mandrills Prefer Brightly Colored Males

Although secondary sexual adornments are widespread in male primates, few studies have examined female choice for these characters. Mandrills (Mandrillus sphinx) present an extreme example of sexual dimorphism, with males exhibiting an array of striking adornments. The most dominant adult male in a group exhibits the brightest and most extensive red coloration, while the other males are less brightly colored. I examined whether female mandrills prefer brightly colored males using data on periovulatory sexual behavior during the 1996 mating season for all males 8 years old (n = 5) and all parous females (n = 9) in a semifree-ranging colony at CIRMF, Gabon. Brightness of male coloration is significantly positively correlated with time spent within 2 m of females, female responsibility for proximity, number of sexual presentations received, % approaches accepted by females, and % inspections with which females cooperated. Females also groomed only the brightest male. Behaviors indicating female preference are not correlated significantly with male dominance rank, and partial correlations confirm that the influence of male color on female behavior is stronger than that of male rank. With the influence of male dominance rank controlled, correlation coefficients between female behaviors and male mating success are high and positive. In further support of the hypothesis that females show mate choice for brightly colored males, independent of dominance rank, I report an unusual case wherein the alpha male fell in rank without loss of coloration. He experienced no significant change in female responsibility for proximity, sexual presentations received, or female reaction to approaches or inspections, though he was no longer observed to mate. Accordingly, female mandrills attend to differences in male secondary sexual characters and favor brightly colored males. As brightly colored males are also dominant this reinforces the influence of male-male competition on male reproductive success and may explain the very high reproductive skew in mandrill males and their extraordinary appearance.

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.

Odour signals major histocompatibility complex genotype in an Old World monkey

The major histocompatibility complex (MHC) is an extraordinarily diverse cluster of genes that play a key role in the immune system. MHC gene products are also found in various body secretions, leading to the suggestion that MHC genotypes are linked to unique individual odourtypes that animals use to assess the suitability of other individuals as potential mates or social partners. We investigated the relationship between chemical odour profiles and genotype in a large, naturally reproducing population of mandrills, using gas chromatography–mass spectrometry and MHC genotyping. Odour profiles were not linked to the possession of particular MHC supertypes. Sex influenced some measures of odour diversity and dominance rank influenced some measures of odour diversity in males, but not in females. Odour similarity was strongly related to similarity at the MHC, and, in some cases, to pedigree relatedness. Our results suggest that odour provides both a cue of individual genetic quality and information against which the receiver can compare its own genotype to assess genetic similarity. These findings provide a potential mechanism underlying mate choice for genetic diversity and MHC similarity as well as kin selection.

Chemical Composition of Scent-Gland Secretions in an Old World Monkey (Mandrillus sphinx): Influence of Sex, Male Status, and Individual Identity

Primates are traditionally considered to be microsmatic, with decreased reliance on olfactory senses in comparison to other sensory modalities such as vision. This is particularly the case for Old World monkeys and apes (catarrhines). However, various lines of evidence suggest that chemical communication may be important in these species, including the presence of a sternal scent-gland in the mandrill. We investigated the volatile components of mandrill odor using gas chromatography-mass spectrometry. We identified a total of 97 volatile components in 88 swabs of the sternal gland secretion and 95 samples of sternal gland hair saturated with scent-gland secretion collected from 27 males and 18 females. We compared odor profiles with features of the signaler using principle components and discriminant function analyses and found that volatile profiles convey both variable (age, dominance rank in males) and fixed (sex, possibly individual identity) information about the signaler. The combination of an odor profile that signals sex, age, and rank with increased motivation to scent-mark and increased production of secretion in high-ranking males leads to a potent signal of the presence of a dominant, adult male with high testosterone levels. This may be particularly relevant in the dense Central African rain forest which mandrills inhabit. By contrast, we were unable to differentiate between either female cycle stage or female rank based on odor profiles, which accords with behavioral studies suggesting that odor signals are not as important in female mandrills as they are in males. The similarity of our findings to those for other mammals and in primates that are more distantly related to humans suggests a broader role for odor in primate communication than is currently recognized.

Non-invasive monitoring of physiological stress in the Western lowland gorilla (Gorilla gorilla gorilla): Validation of a fecal glucocorticoid assay and methods for practical application in the field

Enzymeimmunoassays (EIAs) allow researchers to monitor stress hormone output via measurement of fecal glucocorticoid metabolites (FGCMs) in many vertebrates. They can be powerful tools which allow the acquisition of otherwise unobtainable physiological information from both captive animals and wild animals in remote forest habitats, such as great apes. However, methods for hormone measurement, extraction and preservation need to be adapted and validated for field settings. In preparation for a field study of Western lowland gorillas (Gorilla gorilla gorilla) in the Central African Republic we used samples from captive gorillas collected around opportunistic stressful situations to test whether four different glucocorticoid EIAs reflected adrenocortical activity reliably and to establish the lag-time from the stressor to peak excretion. We also validated a field extraction technique and established a simple, non-freezer-reliant method to preserve FGCMs in extracts long-term. We determined the rate of FGCM change over 28 days when samples cannot be extracted immediately and over 12h when feces cannot be preserved immediately in alcohol. Finally, we used repeat samples from identified individuals to test for diurnal variation in FGCM output. Two group-specific assays measuring major cortisol metabolites detected the predicted FGCM response to the stressor reliably, whereas more specific cortisol and corticosterone assays were distinctly less responsive and thus less useful. We detected a lag time of 2-3 days from stressor to peak FGCM excretion. Our field extraction method performed as well as an established laboratory extraction method and FGCMs in dried extracts stored at ambient temperatures were as stable as those at -20 °C over 1 yr. Hormones in non-extracted feces in alcohol were stable up to 28 days at ambient temperatures. FGCMs in un-fixed gorilla feces deteriorated to almost 50% of the original values within 6h under field conditions. We detected no diurnal variation in FGCMs in samples from wild gorillas. Our study highlights the importance of thorough biological and immunological validation of FGCM assays, and presents validated, practical methods for the application of non-invasive adrenocortical monitoring techniques to field conservation contexts where it is crucially needed.