Modulation of cell-mediated immunity during pregnancy in wild bonobos.

During pregnancy, the mammalian immune system must simultaneously protect against pathogens while being accommodating to the foreign fetal tissues. Our current understanding of this immune modulation derives predominantly from industrialized human populations and laboratory animals. However, their environments differ considerably from the pathogen-rich, resource-scarce environments in which pregnancy and the immune system co-evolved. For a better understanding of immune modulation during pregnancy in challenging environments, we measured urinary neopterin, a biomarker of cell-mediated immune responses, in 10 wild female bonobos (Pan paniscus) before, during and after pregnancy. Bonobos, sharing evolutionary roots and pregnancy characteristics with humans, serve as an ideal model for such investigation. Despite distinct environments, we hypothesized that cell-mediated immune modulation during pregnancy is similar between bonobos and humans. As predicted, neopterin levels were higher during than outside of pregnancy, and highest in the third trimester, with a significant decline post-partum. Our findings suggest shared mechanisms of cell-mediated immune modulation during pregnancy in bonobos and humans that are robust despite distinct environmental conditions. We propose that these patterns indicate shared immunological processes during pregnancy among hominins, and possibly other primates. This finding enhances our understanding of reproductive immunology.

Dental findings in wild great apes from macerated skull analysis.

Oral health is a crucial aspect of overall well-being in both humans and nonhuman primates. Understanding the oral pathologies and dental conditions in apes can provide valuable insights into their evolutionary history, dietary habits, and overall health. The present study evaluates dental findings in wild great apes from museum specimens to gain insights into the influence of natural nutrition on dental health. Complete macerated skulls of wild, adult great apes from the collection of the Museum of Natural History, Berlin, Germany, were examined. We analyzed skulls of 53 gorillas (Gorilla gorilla), 63 chimpanzees (Pan troglodytes), and 41 orangutans (Pongo spp.). For each skull, we recorded wear of dental hard tissues (Lussi and Ganss index), carious lesions, and periodontal bone loss. Incisal and occlusal dental hard tissue defects were found in all skulls, as well as considerable external staining. In all species, incisors and canines showed the greatest loss of tissue, followed by molars. The wear of molars decreased from the first to the third molars, premolars showed the least pronounced defects. Some individuals had apical osteolytic defects along with severe dental hard tissue loss with pulp involvement or after dental trauma, respectively (n = 5). Our study did not observe any carious lesions among the examined great ape skulls. However, we did find evidence for localized or generalized periodontal bone loss in a subset of the specimens (n = 3 chimpanzees, n = 7 orangutans). The natural diet and foraging behavior of great apes induces abrasion and attrition of dental hard tissue but does not yield carious lesions. The occurrence of periodontitis in individual apes indicates that the natural circumstances can induce periodontal bone loss even in the wild, despite physiological nutrition.

Traces of dietary patterns in saliva of hominids: Profiling salivary amino acid fingerprints in great apes and humans.

Herbivorous animals that regularly consume tannin-rich food are known to secrete certain tannin-binding salivary proteins (TBSPs), especially proline-rich proteins and histidine-rich proteins, as an effective measure to counteract the antinutritive effects of dietary tannins. Due to their high binding capacity, TBSPs complex with tannins in the oral cavity, and thereby protect dietary proteins and digestive enzymes. Although the natural diet of great apes (Hominidae) is biased toward ripe fruits, analyses of food plants revealed that their natural diet contains considerable amounts of tannins, which is raising the question of possible counter-measures to cope with dietary tannins. In our study, we investigated the salivary amino acid profiles of zoo-housed Pan paniscus, Pan troglodytes, Gorilla gorilla, and Pongo abelii, and compared their results with corresponding data from Homo sapiens. Individual saliva samples of 42 apes and 17 humans were collected and quantitated by amino acid analysis, using cation-exchange chromatography with postcolumn derivatization, following acid hydrolysis. We found species-specific differences in the salivary amino acid profiles with average total salivary protein concentration ranging from 308.8 mg/dL in Po. abelii to 1165.6 mg/dL in G. gorilla. Total salivary protein was consistently higher in ape than in human saliva samples (174 mg/dL). All apes had on average also higher relative proline levels than humans did. Histidine levels had the highest concentration in the samples from Po. abelii followed by P. paniscus. In all ape species, the high salivary concentrations of proline and histidine are considered to be indicative of high concentrations of TBSPs in hominids. Given that the species differences in salivary composition obtained in this study correspond with overall patterns of secondary compound content in the diet of wild populations, we assume that salivary composition is resilient to acute and long-lasting changes in diet composition in general and tannin content in particular.

Developmental and environmental modulation of fecal thyroid hormone levels in wild Assamese macaques (Macaca assamensis).

Thyroid hormones are key modulators of development, as well as mediators of environmental conditions, by regulating developmental processes and metabolism in primates. Hormone measurement in noninvasively collected samples, that is, feces and urine, is a valuable tool for studying the endocrine function of wildlife, and recent studies have demonstrated the feasibility of measuring thyroid hormones in fecal samples of zoo-housed and wild nonhuman primates. Our study aimed to (i) validate the measurement of immunoreactive fecal total triiodothyronine (IF-T3) in wild Assamese macaques (Macaca assamensis) and (ii) to investigate its developmental changes and its response to environmental changes, including stress responses, in immature individuals. Fecal samples and environmental parameters were collected from individuals of three social groups of wild Assamese macaques living at Phu Khieo Wildlife Sanctuary, Northeastern Thailand. Our study confirmed the methodological feasibility and biological validity of measuring IF-T3 in this population. Specifically, the biological validation demonstrated higher IF-T3 levels in immatures compared to adults, and higher levels in females during late gestation compared to the preconception stage. Our analysis of IF-T3 levels in developing immature macaques revealed a significant increase with age. Furthermore, we found a positive association between IF-T3 and immunoreactive fecal glucocorticoid levels, an indicator of the physiological stress response. Neither minimum temperature nor fruit abundance predicted variation in IF-T3 levels in the immatures. Our findings indicate the possibility for differing effects of climatic factors and food availability on thyroid hormone level changes in immature versus adult animals and in wild compared to experimental conditions. Overall, our study provides the basis for further investigations into the role of thyroid hormones in shaping species-specific traits, growth, and overall primate development.

Blood testosterone levels in sickness and in health: Male chimpanzee testosterone levels decrease in face of an immune challenge.

As an integral part of the immune response, testosterone secretion is inhibited when an individual is confronted with an immune challenge. Testosterone-mediated physiological, morphological, and behavioral traits are compromised at times of impaired health. Nevertheless, males of some species seem to maintain high levels of testosterone when confronted with an immune challenge, upholding competitive strength but compromising their immune response. It has been argued that this phenomenon will occur only in species living in social systems with high degrees of male-male competition over mating opportunities. Male chimpanzees contest over access to fertile females and dominants sire the majority of offspring. This male mating pattern makes chimpanzees a candidate species where we could expect males to maintain high testosterone levels, compromising their immune response, to ensure immediate reproductive success. We measured blood testosterone levels in male and female chimpanzees, who expressed clinical symptoms (symptomatic) or showed no evidence of clinical disease on assessment (asymptomatic). For females, we expected to find lower testosterone levels in symptomatic individuals than in asymptomatic subjects. In males, we would predict lower testosterone levels in symptomatic individuals than in asymptomatic males, if the immune response leads to a decrease in testosterone secretion. Alternatively, males could have equal levels of testosterone when symptomatic and asymptomatic, upholding competitive strength. Our results show that male chimpanzees exhibit lower levels of testosterone when confronted with an immune challenge than when being asymptomatic. This suggests that male testosterone secretion is suppressed as part of the immune response, which potentially increases survival and lifetime reproductive success. It will, however, negatively impact momentary competitive ability. Also, males may employ different mating strategies, some of which are less testosterone-driven (e.g., affiliative strategies). Consequently, in some individuals, the costs of maintaining high testosterone levels may not outweigh the potential gain in reproductive success.

Responsiveness of fecal immunoglobulin A to HPA-axis activation limits its use for mucosal immunity assessment.

The assessment of mucosal immunity as a component of animal health is an important aspect for the understanding of variation in host immunity, and its tradeoff against other life-history traits. We investigated immunoglobulin A (IgA), the major type of antibody associated with mucosal immunity, in relation to changes in parasitic burden following anthelminthic treatment in noninvasively collected fecal samples in a semi-free ranging group of Barbary macaques (Macaca sylvanus). We measured IgA in 340 fecal samples of fourteen females and nine males. As IgA has been found to be responsive to stressors, we also related fecal IgA (fIgA) levels to fecal glucocorticoid metabolites (fGCM) measured in the same samples as part of a previous study. We found a high variability within and between individual fIgA levels over time. Running generalized additive mixed models, we found that fIgA levels were higher in males than in females, but did not change in response to the anthelmintic treatment and the resulting reduction in worm burden. Instead, fIgA level changes were significantly correlated to changes in fGCM levels. Our findings indicate that due to the strong responsiveness of fIgA to HPA-axis activity, the measurement of fIgA may have certain limitations with respect to reflecting gastrointestinal parasitic burden. Moreover, the responsiveness of fIgA to stressors interferes with the interpretation of IgA levels in fecal samples as a measure of mucosal immunity, at least in our study population of the Barbary macaques.

Patterns of urinary cortisol levels during ontogeny appear population specific rather than species specific in wild chimpanzees and bonobos.

Compared with most mammals, postnatal development in great apes is protracted, presenting both an extended period of phenotypic plasticity to environmental conditions and the potential for sustained mother-offspring and/or sibling conflict over resources. Comparisons of cortisol levels during ontogeny can reveal physiological plasticity to species or population specific socioecological factors and in turn how these factors might ameliorate or exaggerate mother-offspring and sibling conflict. Here, we examine developmental patterns of cortisol levels in two wild chimpanzee populations (Budongo and Taï), with two and three communities each, and one wild bonobo population (LuiKotale), with two communities. Both species have similar juvenile life histories. Nonetheless, we predicted that key differences in socioecological factors, such as feeding competition, would lead to interspecific variation in mother-offspring and sibling conflict and thus variation in ontogenetic cortisol patterns. We measured urinary cortisol levels in 1394 samples collected from 37 bonobos and 100 chimpanzees aged up to 12 years. The significant differences in age-related variation in cortisol levels appeared population specific rather than species specific. Both bonobos and Taï chimpanzees had comparatively stable and gradually increasing cortisol levels throughout development; Budongo chimpanzees experienced declining cortisol levels before increases in later ontogeny. These age-related population differences in cortisol patterns were not explained by mother-offspring or sibling conflict specifically; instead, the comparatively stable cortisol patterns of bonobos and Taï chimpanzees likely reflect a consistency in experience of competition and the social environment compared with Budongo chimpanzees, where mothers may adopt more variable strategies related to infanticide risk and resource availability. The clear population-level differences within chimpanzees highlight potential intraspecific flexibility in developmental processes in apes, suggesting the flexibility and diversity in rearing strategies seen in humans may have a deep evolutionary history.

Urinary total T3 levels as a method to monitor metabolic changes in relation to variation in caloric intake in captive bonobos (Pan paniscus).

Monitoring metabolic activity in wild living animals has become of particular interest in the field of ecological research. Methods for the repeated non-invasive sampling of individuals are needed. Thyroid hormones (TH) are involved in the regulation of metabolic activity, and their measurement can be used as a proxy to monitor metabolic changes. During periods of low energy intake, serum TH levels are reduced, leading to a decrease in metabolic activity. Using urine samples collected during a food restriction experiment in captive bonobos we validated a total triiodthyronin (TT3) enzyme immunoassay (EIA) for the monitoring of metabolic changes. We found that the majority of immune reactivity of the assay in the urine samples could be explained through immunoreactivity to T3. Furthermore, urinary T3 was stable through repeated freeze-thaw cycles but prolonged exposure to room temperature lead to degradation. Most importantly, we found that for all animals urinary total T3 levels were higher when more digestible energy was consumed. We concluded that urinary total T3 measurements are a suitable method for monitoring metabolic changes in bonobos and potentially in a wide range of animal species.

Aggression by male bonobos against immature individuals does not fit with predictions of infanticide.

The selective advantage of male infanticide is enhancement of reproductive success of the aggressor. This implies that aggression is directed at individuals sired by others, infant loss shortens the mother's inter-birth interval, and the aggressor has a greater likelihood of siring the next offspring of the victims' mother. As these conditions are not always met, the occurrence of male infanticide is expected to vary, and hominoid primates offer an interesting example of variation in male infanticide. Infanticide has been reported in gorillas and chimpanzees but appears to be absent in orangutans and bonobos. One argument for the absence of infanticide in bonobos is reduction of male aggression. However, given that male aggression against immature individuals occurs and that females engage in behavior that is considered to be counterstrategy against male infanticide, the risk of male infanticide may pose a potential threat. Here, we explored whether aggression by male bonobos fits predictions of male infanticide. Male aggression toward immature individuals was rare and did not have lethal consequences, but the majority of observed cases exposed targets to risks of injury. Males did not target their own offspring less frequently than unrelated immatures, and the risk of being the target of male aggression increased with the targets' age. Overall, these results do not match the predictions of the adaptive male infanticide hypothesis. Instead, aggression by males may promote the emigration of the targets and older males may reinforce their superior status toward individuals that will soon compete for the same resources.

Non-invasive monitoring of physiological markers in primates.

The monitoring of endocrine markers that inform about an animal's physiological state has become an invaluable tool for studying the behavioral ecology of primates. While the collection of blood samples usually requires the animal to be caught and immobilized, non-invasively collected samples of saliva, urine, feces or hair can be obtained without any major disturbance of the subject of interest. Such samples enable repeated collection which is required for matching behavioral information over long time periods with detailed information on endocrine markers. We start our review by giving an overview of endocrine and immune markers that have been successfully monitored in relation to topics of interest in primate behavioral ecology. These topics include reproductive, nutritional and health status, changes during ontogeny, social behavior such as rank relationships, aggression and cooperation as well as welfare and conservation issues. We continue by explaining which hormones can be measured in which matrices, and potential problems with measurements. We then describe different methods of hormone measurements and address their advantages and disadvantages. We finally emphasize the importance of thorough validation procedures when measuring a specific hormone in a new species or matrix.

Within arm's reach: Measuring forearm length to assess growth patterns in captive bonobos and chimpanzees.

OBJECTIVES: Bonobos and chimpanzees are known to differ in various morphological traits, a dichotomy that is sometimes used as an analogy for evolutionary splits during human evolution. The aim of our study was to measure the forearm length of immature and adult bonobos and adult chimpanzees to assess the extent of age-related changes of forearm length in bonobos and sex-dimorphism in bonobos and chimpanzees. MATERIALS AND METHODS: As a proxy of somatic growth we measured forearm length of captive bonobos and chimpanzees ranging in age from 1 to 55 years. Measures were taken from subjects inserting their arms into a transparent Plexiglas® tube, a novel technique facilitating repeated measures of nonanesthetized apes in captivity. RESULTS: Measures from adult females (>12 years) showed that bonobos exceed chimpanzees in terms of forearm length and that sexual dimorphism in forearm length is pronounced in chimpanzees, but not in bonobos. Forearm length increased significantly with chronological age in bonobos. Validation tests revealed that the device generates useful data on morphometric dimensions. DISCUSSION: In most primates, sexual dimorphism in body size is male-biased and the differences in forearm length in chimpanzees follow this trend. Given that males of the two species did not differ in forearm length, the absence/presence of sexual dimorphism of this trait must be due to differences in somatic growth in females. Our novel method offers an alternative to obtain morphometric measures and facilitates longitudinal studies on somatic growth. Am J Phys Anthropol 161:37-43, 2016. © 2016 Wiley Periodicals, Inc.

Urinary C-peptide levels in male bonobos (Pan paniscus) are related to party size and rank but not to mate competition.

Within- and between-species variation in male mating strategies has been attributed to a multitude of factors including male competitive ability and the distribution of fertile females across space and time. Differences in energy balance across and within males allow for the identification of some of the trade-offs associated with certain social and mating strategies. Bonobos live in groups with a high degree of fission-fusion dynamics, there is co-dominance between the sexes and a linear dominance hierarchy among males. Males compete over access to females, breeding is aseasonal, and females exhibit sexual swellings over extended time periods. In this study we use urinary C-peptide (UCP) levels in male bonobos (Pan paniscus) obtained from 260 urine samples from a wild bonobo community, to quantify male energy balance during mate competition and levels of gregariousness in the species. Although high ranking males are more aggressive, spend more time in proximity to maximally tumescent females, and have higher mating frequencies, we found no indication that mate guarding or mate competition affected male energy balance. Our results showed a positive correlation between monthly mean UCP levels and mean party size. When traveling in large parties, high ranking males had higher UCP levels than those of the low ranking males. These results support the hypothesis that patterns of fission-fusion dynamics in bonobos are either linked to energy availability in the environment or to the energetic costs of foraging. The finding of a rank-bias in UCP levels in larger parties could also reflect an increase in contest competition among males over access to food.

Age-related changes in thyroid hormone levels of bonobos and chimpanzees indicate heterochrony in development.

We present information on age related changes of thyroid hormone levels in bonobos (N = 96) and chimpanzees (N = 100) ranging between one and 56 years of age. Fresh urine samples were used for hormone measurements with a commercial competitive total triiodothyronine (T3) ELISA. In both species, immature individuals had higher TT3 levels than adults and there was a marked decrease in TT3 levels between age classes. The two species differed in terms of the timing of TT3 level changes, with chimpanzees experiencing a significant decline in TT3 levels after 10 years of age and bonobos after 20 years of age. The decline of TT3 in chimpanzees appears to coincide with the time when somatic growth terminates while TT3 values in bonobos decrease much later. This temporal asymmetry in urinary thyroid hormone levels indicates heterochrony in the ontogenetic changes of the two sister species and developmental delay in bonobos. The prolongation of high TT3 levels in bonobos, which is characteristic of immatures of both Pan species may affect the behavior of bonobos; namely, the low intensity of aggression they display. Given that developmental studies are often based on post-mortem analyses of skeletons, measures of urinary thyroid hormones offer a non-invasive tool for exploring ontogenetic changes in living wild and captive hominoids.

Neopterin Levels in Bonobos Vary Seasonally and Reflect Symptomatic Respiratory Infections.

As environmental changes exacerbate the threat coming from infectious diseases in wild mammal species, monitoring their health and gaining a better understanding of the immune functioning at the species level have become critically important. Neopterin is a biomarker of cell-mediated immune responses to intracellular infections. We investigated the variation of urinary neopterin (uNeo) levels of wild, habituated bonobos (Pan paniscus) in relation to individual and environmental factors. We used 309 urine samples collected between 2010 and 2018 at the LuiKotale field site, DRC. Based on current knowledge on zoo-housed conspecifics and closely related species, we predicted uNeo levels to increase (1) during infections, (2) with increasing age, (3) over the gestation period and in estrous females; and (4) to vary seasonally. Our results showed uNeo levels varied over a one-year period and increased in individuals showing respiratory symptoms. Contrary to chimpanzees, uNeo levels did not vary with age or female reproductive status, possibly due to our small sample size. Our study provides a baseline for a better understanding of bonobo's immunocompetence in the context of socio-ecological pressures and for monitoring the health of wild populations.

Evidence for adolescent length growth spurts in bonobos and other primates highlights the importance of scaling laws.

Adolescent growth spurts (GSs) in body length seem to be absent in non-human primates and are considered a distinct human trait. However, this distinction between present and absent length-GSs may reflect a mathematical artefact that makes it arbitrary. We first outline how scaling issues and inappropriate comparisons between length (linear) and weight (volume) growth rates result in misleading interpretations like the absence of length-GSs in non-human primates despite pronounced weight-GSs, or temporal delays between length- and weight-GSs. We then apply a scale-corrected approach to a comprehensive dataset on 258 zoo-housed bonobos that includes weight and length growth as well as several physiological markers related to growth and adolescence. We found pronounced GSs in body weight and length in both sexes. Weight and length growth trajectories corresponded with each other and with patterns of testosterone and insulin-like growth factor-binding protein 3 levels, resembling adolescent GSs in humans. We further re-interpreted published data of non-human primates, which showed that aligned GSs in weight and length exist not only in bonobos. Altogether, our results emphasize the importance of considering scaling laws when interpreting growth curves in general, and further show that pronounced, human-like adolescent length-GSs exist in bonobos and probably also many other non-human primates.

Salivary Cortisol Reaction Norms in Zoo-Housed Great Apes: Diurnal Slopes and Intercepts as Indicators of Stress Response Quality.

Monitoring changes in cortisol levels is a widespread tool for measuring individuals' stress responses. However, an acute increase in cortisol levels does not necessarily denote an individual in distress, as increases in cortisol can be elicited by all factors that signal the need to mobilize energy. Nor are low levels of cortisol indicative for a relaxed, healthy individual. Therefore, a more fine-grained description of cortisol patterns is warranted in order to distinguish between cortisol fluctuations associated with different stress response qualities. In most species, cortisol shows a distinct diurnal pattern. Using a reaction norm approach, cortisol levels across the day can be described by the two regression coefficients: the intercept and the slope of the curve. We measured immunoreactive salivary cortisol in three zoo-housed ape species under three conditions (routine days, enrichment days, and after the move to a new house). We examined salivary cortisol intercepts (SCI) and salivary cortisol slopes (SCS) of the diurnal curves. SCI and SCS were independent from each other. SCI was highest on enrichment days and lowest on routine days. SCS was steep on routine days and blunted after the move. Only SCI was species-specific. Our study provides evidence that combining SCI and SCS measures allows us to differentiate between types of stress responses, thereby constituting a useful tool for welfare assessment.

Transition to siblinghood causes a substantial and long-lasting increase in urinary cortisol levels in wild bonobos.

In animals with slow ontogeny and long-term maternal investment, immatures are likely to experience the birth of a younger sibling before reaching maturity. In these species, the birth of a sibling marks a major event in an offspring's early life as the older siblings experience a decrease in maternal support. The transition to siblinghood (TTS) is often considered to be stressful for the older offspring, but physiological evidence is lacking. To explore the TTS in wild bonobos, we investigated physiological changes in urinary cortisol (stress response), neopterin (cell-mediated immunity), and total triiodothyronine (T3, metabolic rate), as well as changes in behaviors that reflect the mother-offspring relationship. Following a sibling's birth, urinary cortisol levels of the older offspring increased fivefold, independent of their age, and remained elevated for 7 months. The cortisol level increase was associated with declining neopterin levels; however, T3 levels and behavioral measures did not change. Our results indicate that the TTS is accompanied by elevated cortisol levels and that this change does not coincide with nutritional weaning and attainment of physical independence. Our results suggest that bonobos and humans experience TTS in similar ways and that this developmental event may have emerged in the last common ancestor.

Plasma Testosterone and Androstenedione Levels Follow the Same Sex-Specific Patterns in the Two Pan Species.

In most animals, males are considered more aggressive, in terms of frequency and intensity of aggressive behaviors, than their female peers. However, in several species this widespread male-biased aggression pattern is either extenuated, absent, or even sex-reversed. Studies investigating potential neuro-physiological mechanisms driving the selection for female aggression in these species have revealed an important, but not exclusive role of androgens in the expression of the observed sex-specific behavioral patterns. Two very closely related mammalian species that markedly differ in the expression and degree of sex-specific aggression are the two Pan species, where the chimpanzee societies are male-dominated while in bonobos sex-biased aggression patterns are alleviated. Using liquid chromatography-mass spectrometry (LC-MS) methods, we measured levels of plasma testosterone and androstenedione levels in male and female zoo-housed bonobos (N = 21; 12 females, 9 males) and chimpanzees (N = 41; 27 females, 14 males). Our results show comparable absolute and relative intersexual patterns of blood androgen levels in both species of Pan. Plasma testosterone levels were higher in males (bonobos: females: average 0.53 ± 0.30 ng/mL; males 6.70 ± 2.93 ng/mL; chimpanzees: females: average 0.40 ± 0.23 ng/mL; males 5.84 ± 3.63 ng/mL) and plasma androstenedione levels were higher in females of either species (bonobos: females: average 1.83 ± 0.87 ng/mL; males 1.13 ± 0.44 ng/mL; chimpanzees: females: average 1.84 ± 0.92 ng/mL; males 1.22 ± 0.55 ng/mL). The latter result speaks against a role of androstenedione in the mediation of heightened female aggression, as had been suggested based on studies in other mammal species where females are dominant and show high levels of female aggressiveness.

Urinary neopterin of wild chimpanzees indicates that cell-mediated immune activity varies by age, sex, and female reproductive status.

The study of free-living animal populations is necessary to understand life history trade-offs associated with immune investment. To investigate the role of life history strategies in shaping proinflammatory cell-mediated immune function, we analyzed age, sex, and reproductive status as predictors of urinary neopterin in 70 sexually mature chimpanzees (Pan troglodytes) at Ngogo, Kibale National Park, Uganda. In the absence of clinical signs of acute infectious disease, neopterin levels significantly increased with age in both male and female chimpanzees, as observed in humans and several other vertebrate species. Furthermore, males exhibited higher neopterin levels than females across adulthood. Finally, females with full sexual swellings, pregnant females, and post-reproductive females, the oldest individuals in our sample, exhibited higher neopterin levels than lactating females and cycling females without full swellings. Variation in females' neopterin levels by reproductive status is consistent with post-ovulatory and pregnancy-related immune patterns documented in humans. Together, our results provide evidence of ample variation in chimpanzee immune activity corresponding to biodemographic and physiological variation. Future studies comparing immune activity across ecological conditions and social systems are essential for understanding the life histories of primates and other mammals.

Exploring the Utility of Hair Endocannabinoids for Monitoring Homeostasis in Bonobos.

AbstractQuantifying physiological challenges has gained increasing importance in evolutionary biology, behavioral physiology, and conservation. One matrix that is particularly useful for obtaining long-term records of physiological changes in mammals is hair. Potential markers are components of the endocannabinoid (EC) system, which regulates homeostasis of the brain as well as the endocrine and immune systems. Here, we present results from the first study to measure ECs (anandamide [AEA], 2-archidonyl glycerol [2-AG]) and EC-like compounds (N-palmitoylethanolamine [PEA], N-oleoylethanolamine [OEA], N-stearoylethanolamine [SEA]) in the hair of a nonhuman primate. We found that AEA, SEA, PEA, and OEA can be reliably measured in hair samples. When comparing the measurements of hair from different body parts, we found that variations of some analytes suggest that hair location is likely to affect results. For changes in health status, measurements of ECs and EC-like compounds reflected differences at both intra- and interindividual levels. We concluded that the EC system potentially provides novel tools to assess well-being, health status, and metabolic stress-not only in the hair of humans but also in that of domestic and wild animals. Measuring changes in ECs and EC-like compounds may improve the long-term monitoring of health status in captive and wild primates and may serve as a useful measure in animal welfare programs.