Primate phageomes are structured by superhost phylogeny and environment.

Humans harbor diverse communities of microorganisms, the majority of which are bacteria in the gastrointestinal tract. These gut bacterial communities in turn host diverse bacteriophage (hereafter phage) communities that have a major impact on their structure, function, and, ultimately, human health. However, the evolutionary and ecological origins of these human-associated phage communities are poorly understood. To address this question, we examined fecal phageomes of 23 wild nonhuman primate taxa, including multiple representatives of all the major primate radiations. We find relatives of the majority of human-associated phages in wild primates. Primate taxa have distinct phageome compositions that exhibit a clear phylosymbiotic signal, and phage-superhost codivergence is often detected for individual phages. Within species, neighboring social groups harbor compositionally and evolutionarily distinct phageomes, which are structured by superhost social behavior. Captive nonhuman primate phageome composition is intermediate between that of their wild counterparts and humans. Phage phylogenies reveal replacement of wild great ape-associated phages with human-associated ones in captivity and, surprisingly, show no signal for the persistence of wild-associated phages in captivity. Together, our results suggest that potentially labile primate-phage associations have persisted across millions of years of evolution. Across primates, these phylosymbiotic and sometimes codiverging phage communities are shaped by transmission between groupmates through grooming and are dramatically modified when primates are moved into captivity.

Persistent anthrax as a major driver of wildlife mortality in a tropical rainforest.

Anthrax is a globally important animal disease and zoonosis. Despite this, our current knowledge of anthrax ecology is largely limited to arid ecosystems, where outbreaks are most commonly reported. Here we show that the dynamics of an anthrax-causing agent, Bacillus cereus biovar anthracis, in a tropical rainforest have severe consequences for local wildlife communities. Using data and samples collected over three decades, we show that rainforest anthrax is a persistent and widespread cause of death for a broad range of mammalian hosts. We predict that this pathogen will accelerate the decline and possibly result in the extirpation of local chimpanzee (Pan troglodytes verus) populations. We present the epidemiology of a cryptic pathogen and show that its presence has important implications for conservation.

Testing the role of testosterone versus estrogens in mediating reproductive transitions in female rhesus macaques.

In male vertebrates, testosterone is generally known to coordinate reproductive trade-offs, in part by promoting the transition to the next reproduction at the expense of current parental care. The role of testosterone in reproductive transitions has been little tested in female vertebrates, especially in mammals. The present study sought to fill this gap, by first undertaking an experimental study, in which we identified DHT, androstenediol, and in particular etiocholanolone, as fecal androgen metabolites which reflect serum testosterone concentration in female rhesus macaques (Macaca mulatta). Using concentrations of fecal etiocholanolone as proxy for circulating testosterone, we then conducted a field study on 46 free-ranging rhesus macaques of Cayo Santiago, Puerto Rico, to test if testosterone mediates the trade-off between reproductive transition (a higher chance of reproducing in the next year) and current reproduction (providing more care to current offspring). While the evidence for testosterone was weak, the testing of fecal immunoreactive estrogen metabolites suggested a potential role of estrogen in reproductive trade-offs. We found large individual differences in fecal etiocholanolone concentrations during the early postpartum period that were unexplained even after accounting for sociodemographic factors such as age and dominance rank. Further investigation is needed to understand this variation. Our study suggests that the actions of testosterone in females may not have evolved to fulfil the same role in primate reproductive transitions as it does in males, and we encourage more studies to consider the function of testosterone in reproductive behaviors and life history transitions in females of mammalian taxa.

Using an on-site laboratory for fecal steroid analysis in wild white-faced capuchins.

Hormone laboratories located "on-site" where field studies are being conducted have a number of advantages. On-site laboratories allow hormone analyses to proceed in near-real-time, minimize logistics of sample permits/shipping, contribute to in-country capacity-building, and (our focus here) facilitate cross-site collaboration through shared methods and a shared laboratory. Here we provide proof-of-concept that an on-site hormone laboratory (the Taboga Field Laboratory, located in the Taboga Forest Reserve, Costa Rica) can successfully run endocrine analyses in a remote location. Using fecal samples from wild white-faced capuchins (Cebus imitator) from three Costa Rican forests, we validate the extraction and analysis of four steroid hormones (glucocorticoids, testosterone, estradiol, progesterone) across six assays (DetectX® and ISWE, all from Arbor Assays). Additionally, as the first collaboration across three long-term, wild capuchin field sites (Lomas Barbudal, Santa Rosa, Taboga) involving local Costa Rican collaborators, this laboratory can serve as a future hub for collaborative exchange.

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.

Variation in aggression rates and urinary cortisol levels indicates intergroup competition in wild bonobos.

Intergroup competition is a widespread phenomenon across taxa and groups typically compete over access to limited resources, such as food and mates. Such competition may be quantified by changes in individuals' behavioral and physiological status in response to intergroup encounters (IGEs). Bonobos, one of our closest living relatives, are often regarded as xenophilic and exhibit high tolerance towards out-group individuals. This tolerance between groups may still be accompanied by intergroup competition over resources. We hereby compared variation in aggression rates and urinary cortisol levels of bonobos during and outside contexts of IGEs in the Kokolopori Bonobo Reserve and investigated whether food and mate availability influenced males' and females' aggression and cortisol levels, when controlling for dominance rank and the number of individuals present. We found that although females had higher aggression rates and urinary cortisol levels during than outside contexts of IGEs, these increases were not related to food availability or changes in between-group dynamics when maximally tumescent females were present, rather than absent. Furthermore, males showed higher aggression rates and urinary cortisol levels during than outside contexts of IGEs. However, males' responses during IGEs were not related to the presence of maximally tumescent females and food availability. Taken together, while competition intensified during seemingly tolerant IGEs in bonobos, such competition was unrelated to short-term changes in food and mate availability. Despite physical and physiological costs of aggression, bonobos associate with out-group individuals frequently and for extended periods. This suggests potential benefits of bonobo intergroup associations.

Recognizing normal reproductive biology: A comparative analysis of variability in menstrual cycle biomarkers in German and Bolivian women.

The idealized "normal" menstrual cycle typically comprises a coordinated ebb and flow of hormones over a 28-day span with ovulation invariably shown at the midpoint. It's a pretty picture-but rare. Systematic studies have debunked the myth that cycles occur regularly about every 28 days. However, assumptions persist regarding the extent and normalcy of variation in other cycle biomarkers. The processes of judging which phenotypic variants are "normal" is context dependent. In everyday life, normal is that which is most commonly seen. In biomedicine normal is often defined as an arbitrarily bounded portion of the phenotype's distribution about its statistical mean. Standards thus defined in one population are problematic when applied to other populations; population specific standards may also be suspect. Rather, recognizing normal female reproductive biology in diverse human populations requires specific knowledge of proximate mechanisms and functional context. Such efforts should be grounded in an empirical assessment of phenotypic variability. We tested hypotheses regarding cycle biomarker variability in women from a wealthy industrialized population (Germany) and a resource-limited rural agropastoral population (Bolivia). Ovulatory cycles in both samples displayed marked but nonetheless comparable variability in all cycle biomarkers and similar means/medians for cycle and phase lengths. Notably, cycle and phase lengths are poor predictors of mid-luteal progesterone concentrations. These patterns suggest that global and local statistical criteria for "normal" cycles would be difficult to define. A more productive approach involves elucidating the causes of natural variation in ovarian cycling and its consequences for reproductive success and women's health.

Quantitative estimates of glacial refugia for chimpanzees (Pan troglodytes) since the Last Interglacial (120,000 BP).

Paleoclimate reconstructions have enhanced our understanding of how past climates have shaped present-day biodiversity. We hypothesize that the geographic extent of Pleistocene forest refugia and suitable habitat fluctuated significantly in time during the late Quaternary for chimpanzees (Pan troglodytes). Using bioclimatic variables representing monthly temperature and precipitation estimates, past human population density data, and an extensive database of georeferenced presence points, we built a model of changing habitat suitability for chimpanzees at fine spatio-temporal scales dating back to the Last Interglacial (120,000 BP). Our models cover a spatial resolution of 0.0467° (approximately 5.19 km2 grid cells) and a temporal resolution of between 1000 and 4000 years. Using our model, we mapped habitat stability over time using three approaches, comparing our modeled stability estimates to existing knowledge of Afrotropical refugia, as well as contemporary patterns of major keystone tropical food resources used by chimpanzees, figs (Moraceae), and palms (Arecacae). Results show habitat stability congruent with known glacial refugia across Africa, suggesting their extents may have been underestimated for chimpanzees, with potentially up to approximately 60,000 km2 of previously unrecognized glacial refugia. The refugia we highlight coincide with higher species richness for figs and palms. Our results provide spatio-temporally explicit insights into the role of refugia across the chimpanzee range, forming the empirical foundation for developing and testing hypotheses about behavioral, ecological, and genetic diversity with additional data. This methodology can be applied to other species and geographic areas when sufficient data are available.

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.

Oxytocin increases after affiliative interactions in male Barbary macaques.

Mammals living in stable social groups often mitigate the costs of group living through the formation of social bonds and cooperative relationships. The neuropeptide hormone oxytocin (OT) is proposed to promote both bonding and cooperation although only a limited number of studies have investigated this under natural conditions. Our aim was to assess the role of OT in bonding and cooperation in male Barbary macaques (Macaca sylvanus). First, we tested for an effect of affiliation - grooming and triadic male-infant-male interactions - with bond and non-bond partners on urinary OT levels. Second, we tested whether grooming interactions (and thus increased OT levels) increase a male's general propensity to cooperate in polyadic conflicts. We collected >4000 h of behavioral data on 14 adult males and measured OT levels from 139 urine samples collected after affiliation and non-social control periods. Urinary OT levels were higher after grooming with any partner. By contrast, OT levels after male-infant-male interactions with any partner or with bond partners were not different from controls but were higher after interactions with non-bond partners. Previous grooming did not increase the likelihood of males to support others in conflicts. Collectively, our results support research indicating that OT is involved in the regulation of adult affiliative relationships. However, our male-infant-male interaction results contradict previous studies suggesting that it is affiliation with bond rather than non-bond partners that trigger the release of OT. Alternatively, OT levels were elevated prior to male-infant-male interactions thus facilitating interaction between non-bond partners. The lack of an association of grooming and subsequent support speaks against an OT linked increase in the general propensity to cooperate.

Maternal effects on offspring growth indicate post-weaning juvenile dependence in chimpanzees (Pan troglodytes verus).

BACKGROUND: In animals with altricial offspring, most growth occurs after birth and may be optimized by post-natal maternal care. Maternal effects on growth may be influenced by individual characteristics of the mothers, such as social status, individual investment strategies and the length of association with offspring. The prolonged juvenile dependence seen in humans is a distinctive life history adaptation, which may have evolved to facilitate sustained somatic and brain growth.In chimpanzees, offspring are typically weaned at approximately 4 years old, yet immature individuals continue to associate with their mothers for up to 10 years beyond weaning. Whether this lengthy association or the individual characteristics of mothers influences growth patterns in this species is not clear.The relationship between urinary creatinine and specific gravity is an established non-invasive measure of muscle mass in humans and chimpanzees. We analysed the urinary creatinine and specific gravity of 1318 urine samples from 70 wild chimpanzees from the Taï Forest, Ivory Coast aged 4 to 15 years. RESULTS: We showed a clear increase in urinary creatinine levels with age in both males and females, replicating established growth curves in this species and reaffirming this measure as a reliable proxy for lean body mass. Comparing those who experience maternal loss (orphans) with non-orphan chimpanzees, maternal presence beyond weaning age and into late juvenility positively influenced offspring muscle mass throughout ontogeny such that orphans had significantly less muscle mass than age-matched non-orphans. In age-matched offspring with mothers, those with high-ranking mothers had greater muscle mass. Accounting for variation in muscle mass attributable to maternal presence, we found no effect of maternal investment (length of inter birth interval, from own birth to birth of following sibling) on offspring muscle mass. CONCLUSION: Chimpanzee mothers have an extended and multi-faceted influence on offspring phenotypes. Our results suggest that maternal investment extends beyond lactation and into early adulthood and has clear benefits to offspring physical development. Therefore, prolonged juvenile dependence, although unique in its form in human societies, may be a trait with deeper evolutionary origins.

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.

Oxytocin reactivity during intergroup conflict in wild chimpanzees.

Intergroup conflict is evident throughout the history of our species, ubiquitous across human societies, and considered crucial for the evolution of humans' large-scale cooperative nature. Like humans, chimpanzee societies exhibit intragroup coordination and coalitionary support during violent intergroup conflicts. In both species, cooperation among group members is essential for individuals to gain access to benefits from engaging in intergroup conflict. Studies suggest that a contributive mechanism regulating in-group cooperation during intergroup conflicts in humans involves the neuropeptide hormone oxytocin, known to influence trust, coordination, and social cognition, although evidence from natural settings is lacking. Here, applying a noninvasive method, we investigate oxytocinergic system involvement during natural intergroup conflicts in wild chimpanzees. We found that chimpanzees of both sexes had significantly higher urinary oxytocin levels immediately before and during intergroup conflict compared with controls. Also, elevated hormone levels were linked with greater cohesion during intergroup conflicts, rather than with the level of potential threat posed by rival groups, intragroup affiliative social interactions, or coordinated behavior alone. Thus, the oxytocinergic system, potentially engendering cohesion and cooperation when facing an out-group threat, may not be uniquely human but rather a mechanism with evolutionary roots shared by our last common ancestor with chimpanzees, likely expediting fitness gains during intergroup conflict.

The cooperative sex: Sexual interactions among female bonobos are linked to increases in oxytocin, proximity and coalitions.

In some species habitual same-sex sexual behavior co-occurs with high levels of intra-sexual alliance formation, suggesting that these behaviors may be linked. We tested for such a link by comparing behavioral and physiological outcomes of sex with unrelated same- and opposite-sex partners in female bonobos (Pan paniscus). We analyzed behavioral outcomes following 971 sexual events involving n = 19 female and n = 8 male adult and sub-adult members of a wild, habituated bonobo community. We additionally collected n = 143 urine samples before and after sexual interactions to non-invasively measure oxytocin (OT), which modulates female sexual behavior and facilitates cooperation in other species. The majority of sexual events (65%) consisted of female same-sex genito-genital rubbing (or GG-rubbing). Female dyads engaged in significantly more sexual interactions than did inter-sexual dyads, and females were more likely to remain within close proximity to their partners following GG-rubbing. Females also exhibited greater increases in urinary OT following GG-rubbing compared with copulations, indicating a physiological basis for increased motivation to cooperate among females. The frequency of coalitionary support among non-kin was positively predicted by the frequency of sexual interactions for female as well opposite-sex dyads, although coalitionary support tended to be more frequent among females. The emergence of habitual same-sex sexual behavior may have been an important step in the evolution of cooperation outside of kinship and pair-bonds in one of our closest phylogenetic relatives.

Analytical validation of an Enzyme Immunoassay for the measurement of urinary oxytocin in dogs and wolves.

Assessing changes in oxytocin (OT) levels in response to a variety of social stimuli has become of major interest in the field of behavioral endocrinology. OT is involved in the regulation of various aspects of social behavior such as tolerance, and the formation and maintenance of social bonds but also the regulation of stress. All of these aspects have been identified as potential targets of selection during the domestication process. Therefore, comparing the role of the oxytocinergic system in various aspects of dog and wolf social behavior, might help to understand whether this system was involved in the domestication process. Studies assessing OT levels in dogs and wolves have used invasively collected plasma and serum samples and non-invasively collected urine samples. However, when using an assay system on a new species a careful and complete validation of the method is of crucial importance, and to date no proper validation, to assess urinary OT levels in dogs and wolves, has been reported. We therefore conducted an analytical validation of an Enzyme Immunoassay (EIA) for the measurement of OT in urine of dogs and wolves, using a commercially available EIA. Stability tests revealed that OT levels degrade over time when stored at 4 °C, but are little affected by repeated thawing. In addition, our results indicate that the variance in OT levels is slightly lower when phosphoric acid is added following collection to prevent OT degradation. Long term storage tests revealed that urinary OT levels are least variable when stored as extracts in ethanol at -20 °C, rather than as unextracted urine samples. Validation results were acceptable with regard to parallelism, but values for accuracy and extraction efficiency were not meeting the standard criteria usually applied to steroid EIAs, especially when assessed for the lower range of the assay. The results of this study highlight the importance of an analytical assay validation, since even if validation parameters are not optimal, if published, they allow readers to estimate the relevance of studies using the validated method.

Measuring urinary cortisol and testosterone levels in male Barbary macaques: A comparison of EIA and LC-MS.

The development of methods to quantify hormones from non-invasively collected samples such as urine or feces has facilitated endocrinology research on wild-living animals. To ensure that hormone measurements are biologically meaningful, method validations are strongly recommended for each new species or sample matrix. Our aim was to validate three commonly used enzyme immunoassays (EIA), one for analysis of cortisol and two for analysis of testosterone, to assess adrenocortical and gonadal endocrine activity, respectively, from the urine of male Barbary macaques. We compared EIA and liquid chromatography-mass spectrometry (LC-MS) results to determine if the EIA measurements truly reflect levels of the target hormone and to determine if antibody cross-reactivities with other steroids were potentially confounding results. Furthermore, we conducted a biological validation of testosterone to ensure that both EIA and LC-MS were able to capture physiologically meaningful differences in hormone levels. We found that cortisol measured by EIA correlated strongly with cortisol measured by LC-MS in both adult and immature males, without the need for deconjugation of steroids in the urine. Both testosterone EIAs correlated strongly with LC-MS in adult males, but only if steroids in the urine were deconjugated by enzymatic hydrolysis prior to analysis. However, in immature males, EIA and LC-MS results did not correlate significantly. Further correlation analyses suggest this is likely due to cross-reactivity of the testosterone antibodies with other adrenal steroids such as cortisol, DHEA, and likely others, which are present at much higher concentrations relative to testosterone in immature males. Testosterone levels were significantly higher in adult compared to immature males as measured by LC-MS but not as measured by EIA. Taken together, our results suggest that the testosterone EIAs are suitable to assess gonadal activity in adult but not immature males, and only if a hydrolysis of the urine is conducted prior to analysis.

The costs of living at the edge: Seasonal stress in wild savanna-dwelling chimpanzees.

Adaptations associated with shifting from a predominately forested habitat to a more open environment are considered a crucial step in hominin evolution. Understanding how chimpanzees, one of our closest-living relatives, are exposed to the selection pressures associated with living in a relatively sparse, hot, and dry environment can inform us about the relative importance of potential environmental stressors involved in adaptations to drier environments. We investigated the extent to which chimpanzees living in an extreme savanna habitat experience seasonal variability in either energy balance or thermoregulation (dehydration and heat exposure), as well as whether these potential environmental constraints are taxing to chimpanzee individuals. Specifically, we tested the hypothesis that savanna environments impose seasonally-relevant costs to chimpanzees. To this end, we collected 368 urine samples from one community of chimpanzees at Fongoli, Senegal, and measured c-peptide, creatinine, and cortisol as measures of physiological responses to environmental food, water, and heat constraints, respectively. We then evaluated the influence of climatic and phenological factors on these indicators. Results illustrated significant seasonal variation in all biomarkers, which corresponded to relevant ecological correlates. Furthermore, creatinine but not c-peptide correlated with cortisol levels, suggesting that chimpanzees in this environment endure periods of heat and dehydration stress, but are able to avoid stressful levels of negative energy balance. Using savanna chimpanzees as a referential model, our research lends support to the notion that thermoregulatory challenges were a significant factor in hominin evolution, and suggests these challenges may have overshadowed the challenges of maintaining adequate energetic balance during the expansion of the hominin range from wetter to drier environments.

Seasonal and inter-annual variation of malaria parasite detection in wild chimpanzees.

BACKGROUND: Cross-sectional surveys of chimpanzee (Pan troglodytes) communities across sub-Saharan Africa show large geographical variation in malaria parasite (Plasmodium spp.) prevalence. The drivers leading to this apparent spatial heterogeneity may also be temporally dynamic but data on prevalence variation over time are missing for wild great apes. This study aims to fill this fundamental gap. METHODS: Some 681 faecal samples were collected from 48 individuals of a group of habituated chimpanzees (Taï National Park, Côte d'Ivoire) across four non-consecutive sampling periods between 2005 and 2015. RESULTS: Overall, 89 samples (13%) were PCR-positive for malaria parasite DNA. The proportion of positive samples ranged from 0 to 43% per month and 4 to 27% per sampling period. Generalized Linear Mixed Models detected significant seasonal and inter-annual variation, with seasonal increases during the wet seasons and apparently stochastic inter-annual variation. Younger individuals were also significantly more likely to test positive. CONCLUSIONS: These results highlight strong temporal fluctuations of malaria parasite detection rates in wild chimpanzees. They suggest that the identification of other drivers of malaria parasite prevalence will require longitudinal approaches and caution against purely cross-sectional studies, which may oversimplify the dynamics of this host-parasite system.

Nocturnal activity in wild chimpanzees (Pan troglodytes): Evidence for flexible sleeping patterns and insights into human evolution.

OBJECTIVES: We investigated occurrences and patterns of terrestrial nocturnal activity in wild chimpanzees (Pan troglodytes) and modelled the influence of various ecological predictors on nocturnal activity. METHODS: Data were extracted from terrestrial camera-trap footage and ecological surveys from 22 chimpanzee study sites participating in the Pan African Programme: The Cultured Chimpanzee. We described videos demonstrating nocturnal activity, and we tested the effects of the percentage of forest, abundance of predators (lions, leopards and hyenas), abundance of large mammals (buffalos and elephants), average daily temperature, rainfall, human activity, and percent illumination on the probability of nocturnal activity. RESULTS: We found terrestrial nocturnal activity to occur at 18 of the 22 study sites, at an overall average proportion of 1.80% of total chimpanzee activity, and to occur during all hours of the night, but more frequently during twilight hours. We found a higher probability of nocturnal activity with lower levels of human activity, higher average daily temperature, and at sites with a larger percentage of forest. We found no effect of the abundance of predators and large mammals, rainfall, or moon illumination. DISCUSSION: Chimpanzee terrestrial nocturnal activity appears widespread yet infrequent, which suggests a consolidated sleeping pattern. Nocturnal activity may be driven by the stress of high daily temperatures and may be enabled at low levels of human activity. Human activity may exert a relatively greater influence on chimpanzee nocturnal behavior than predator presence. We suggest that chimpanzee nocturnal activity is flexible, enabling them to respond to changing environmental factors.

Male-female interactions in multimale groups of mountain gorillas.

Male-female social interactions may vary according to female receptivity, female parity, and male dominance rank. Such variation may be less apparent in species with one-male mating systems than those with multimale mating systems, as within-group male-male competition and female mate choice are absent. Examining variation in male-female interactions in multimale groups in species with a predominantly one-male mating system may help to shed light on plasticity in behavioral patterns and the evolution of mating systems. In this study, we investigated the effect of female receptivity (i.e., days when mating occurred), female parity, and male dominance rank on the patterns of spatial proximity, grooming, following, and aggression among 34 male-female dyads in four multi-male groups of Virunga mountain gorillas. In addition, as a preliminary investigation of potential physiological costs incurred by females in a mating context (coercion), we tested whether female receptivity and female parity explained variation in immunoreactive glucocorticoid (iGC) levels of females. The amount of time male-female dyads spent in close proximity was significantly higher for parous versus nulliparous females and for high- versus low-ranking males. The rate of male aggression to females did not vary significantly with female parity, male rank, or female receptivity. However, post hoc analysis showed that both proximity and aggression increased for the males that participated in the matings on days that females were receptive. Grooming and following by males occurred infrequently. Neither female receptivity nor parity influenced iGC levels in females, a finding that is more consistent with courtship than coercion of females by males. Overall, our results suggest that males advertise their ability to provide protection to females and their offspring, and females seek out males that can do so.