Single aggressive interactions increase urinary glucocorticoid levels in wild male chimpanzees

Financial support was provided by British Academy [http://www.britac.ac.uk/] (CC), Leakey Foundation [http://www.leakeyfoundation.org/] (CC, RMW, TD), Leverhulm Trust [http://www.leverhulme.ac.uk/] (KZ), Max Planck Society [http://www.eva.mpg.de/] (AW, CC, RMW, TD) and the Royal Zoological Society of Scotland [http://www.rzss.org.uk/], in providing core funding for Budongo Conservation Field Station. This project has received additional funding from the European Union’s Seventh Framework Program for research, technological development and demonstration [http://ec.europa.eu/research/fp7/index_e​n.cfm] under grant agreement no 283871.A basic premise in behavioural ecology is the cost-benefit arithmetic, which determines both behavioural decisions and evolutionary processes. Aggressive interactions can be costly on an energetic level, demanding increased energy or causing injuries, and on a psychological level, in the form of increased anxiety and damaged relationships between opponents. Here we used urinary glucocorticoid (uGC) levels to assess the costs of aggression in wild chimpanzees of Budongo Forest, Uganda. We collected 169 urine samples from nine adult male chimpanzees following 14 aggressive interactions (test condition) and 10 resting events (control condition). Subjects showed significantly higher uGC levels after single aggressive interactions compared to control conditions, likely for aggressors as well as victims. Higher ranking males had greater increases of uGC levels after aggression than lower ranking males. In contrast, uGC levels showed no significant change in relation to aggression length or intensity, indicating that psychological factors might have played a larger role than mere energetic expenditure. We concluded that aggressive behaviour is costly for both aggressors and victims and that costs seem poorly explained by energetic demands of the interaction. Our findings are relevant for studies of post-conflict interactions, since we provide evidence that both aggressors and victims experience a stress response to conflict.Publisher PDFPeer reviewe

Endogenous peripheral oxytocin measures can give insight into the dynamics of social relationships: A review

The neuropeptide, oxytocin, receives increasing attention due to its role in stress regulation and promoting affiliative social behavior. Research across mammals points to a complex pattern whereby social context and individual differences moderate the central release of oxytocin as well as moderate the effects that exogenous administration of oxytocin has on social behavior. In addition, it is becoming evident that measuring endogenous peripheral oxytocin levels is an informative tool. This is particularly so when oxytocin can be measured from non-invasively collected samples, such as in urine. Although it is still debated as to whether peripheral measures of oxytocin relate to central measures of oxytocin, anatomical and functional evidence indicate a link between the two. We argue that non-invasive measures of peripheral oxytocin hold several research and potential therapeutic advantages. Principally, study subjects can be sampled repeatedly in different social contexts where social history between interaction partners can be taken into account. Several hormones can be measured simultaneously allowing examination of the influence of oxytocin interactions with other hormones on motivational states. Valence of relationships as well as changes in relationship quality over time can be measured through endocrine responses. Also, the approach of identifying natural social contexts that are associated with endogenous oxytocin release offers the potential of behavioral therapy as an addition or alternative to chemical therapy in the field of mental health

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

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

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 aggressivenes

Home range size in central chimpanzees (Pan troglodytes troglodytes) from Loango National Park, Gabon

Ranging behavior has been studied extensively in eastern (Pan troglodytes schweinfurthii) and western (P. t. verus) chimpanzees, but relatively little is known regarding home ranges of the other two subspecies (P. t. ellioti; P. t. troglodytes). In this study, we determined the home range size and space use of a habituated community (Rekambo) of central chimpanzees living in a habitat mosaic in Loango National Park, Gabon. Data on travel routes were collected during follows between January 2017 and April 2019 (N = 670,616 relocations, collected over 640 days and 5690 h of observation). We used three methods for calculating home range size (minimum convex polygon, kernel density estimation, and biased random bridges). We compare our estimates to those obtained from prior genetic and camera trap studies of the Rekambo community and contrast them with estimates from other chimpanzee communities of the four chimpanzee subspecies. Depending on the methodology used, the home range size of the Rekambo community ranged between 27.64 and 59.03 km(2). The location of the center of the home range remained relatively stable over the last decade, while the overall size decreased. The Rekambo home range is, therefore, one of the largest documented so far for chimpanzees outside savannah-woodland habitats. We discuss several explanations, including the presence of savannah, interspecies competition, and intercommunity interactions. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s10329-021-00927-5

Intercommunity interactions and killings in central chimpanzees (Pan troglodytes troglodytes) from Loango National Park, Gabon

Intercommunity competition in chimpanzees (Pan troglodytes) has been widely studied in eastern (P. t. schweinfurthii) and western (P. t. verus) communities. Both subspecies show hostility towards neighboring communities but differ in rates of lethal attacks and female involvement. However, relatively little is known about the territorial behavior of the two other subspecies, central (P. t. troglodytes) and Nigeria-Cameroon chimpanzees (P. t. ellioti). Here, we present the first insights into intercommunity interactions of individuals of a community of central chimpanzees living in the Loango National Park in Gabon. The presence of individuals of neighboring communities in the Rekambo home range was assessed using 27 camera traps. Information was compiled on intergroup interactions recorded before (2005–2016) and after (January 2017–June 2019) the habituation of the community. Individuals from neighboring communities entered the core area, where nine out of 16 recorded intercommunity encounters occurred. Males were the main participants in territorial patrols and intercommunity aggressions. Females were part of all six territorial patrols recorded and dependent offspring participated in five patrols. Females were involved in intercommunity aggression in five out of twelve recorded encounters in which there was visual contact between communities. While the intercommunity encounter rate was lower than that reported across most other long-term chimpanzee sites, the annual intercommunity killing rate was among the highest. These results suggest that the frequency of lethal attacks at Loango is comparable to that reported for the eastern subspecies. In contrast, female involvement in intercommunity interactions mirrors that of the western subspecies

Testing the effect of medical positive reinforcement training on salivary cortisol levels in bonobos and orangutans

The management of captive animals has been improved by the establishment of positive reinforcement training as a tool to facilitate interactions between caretakers and animals. In great apes, positive reinforcement training has also been used to train individuals to participate in simple medical procedures to monitor physical health. One aim of positive reinforcement training is to establish a relaxed atmosphere for situations that, without training, might be very stressful. This is especially true for simple medical procedures that can require animals to engage in behaviours that are unusual or use unfamiliar medical devices that can be upsetting. Therefore, one cannot exclude the possibility that the training itself is a source of stress. In this study, we explored the effects of medical positive reinforcement training on salivary cortisol in two groups of captive ape species, orangutans and bonobos, which were familiar to this procedure. Furthermore, we successfully biologically validated the salivary cortisol assay, which had already been validated for bonobos, for orangutans. For the biological validation, we found that cortisol levels in orangutan saliva collected during baseline conditions were lower than in samples collected during three periods that were potentially stressful for the animals. However, we did not find significant changes in salivary cortisol during medical positive reinforcement training for either bonobos or orangutans. Therefore, for bonobos and orangutans with previous exposure to medical PRT, the procedure is not stressful. Thus, medical PRT provides a helpful tool for the captive management of the two species