Urinary Cortisol Increases During a Respiratory Outbreak in Wild Chimpanzees

Abstract

In mammals, the excretion of cortisol can provide energy toward restoring homeostasis and is a major component of the stress response. However, chronically elevated cortisol levels also have suppressive effects on immune function. As mounting an immune response is energetically costly, sick individuals may conserve energy by exhibiting certain sickness behaviors, such as declining activity levels. Due to the complex interplay between immune function and sickness behaviors, endocrinological correlates have received growing attention in the medical community, but so far, this subject was investigated rarely. Furthermore, given the complexities of studying illnesses and immunity in natural settings, correlates of sickness behaviors have yet to be studied in non-human primates in the wild. Methods: We measured urinary cortisol levels using liquid chromatography-mass spectrometry in a group of wild habituated chimpanzees in Taï National Park, Côte d'Ivoire, before, during, and after a respiratory disease outbreak (main causative pathogen: human respiratory syncytial virus A, with coinfections of Streptococcus pneumoniae). Changes in cortisol levels were then related to urinary neopterin levels, a biomarker of immune system activation. Results: Urinary cortisol levels were found to be more than 10-fold higher during the outbreak in comparison with levels before and after the outbreak period. Increasing cortisol levels were also associated with increasing neopterin levels. Interestingly, rather atypical patterns in a diurnal decline of cortisol levels were found during infection periods, such that levels remained raised throughout the day. Conclusion: In conclusion, cortisol increase was related to cellular immune response. Our results suggest that cortisol is a mediator of infectious disease pathogenicity through its impact on the immune system and that wild chimpanzees may be facing energetic stress when sick. By monitoring immune challenges in wild-living animals, our study demonstrates that immune defenses have costs and that these costs are context-specific.

Non-genetic maternal effects shape individual differences in cortisol phenotypes in wild chimpanzees

“…Circadian slopes vary with experiences of adversity, including maternal loss and illness (Behringer et al, 2020;Girard-Buttoz et al, 2021), and also change with aging and life history stages in chimpanzees (Emery Thompson et al, 2020). Therefore, our uncertain repeatability estimates for circadian slopes could be due to substantial within-individual variation.…”

“…Furthermore, injury and sickness can elevate cortisol levels in primates (Barton, 1987;Behringer et al, 2020;McIntosh, 1987;Muehlenbein and Watts, 2010) and affect circadian cortisol patterns in chimpanzees (Behringer et al, 2020). Therefore, we excluded samples from individuals that displayed symptoms of sickness or injury (determined by onsite veterinarians in each field site).…”

Early maternal loss leads to short- but not long-term effects on diurnal cortisol slopes in wild chimpanzees

“…Very low SG values are a sign of over-diluted samples that reflect potential contamination with rain water and can, in turn, inflate cortisol concentration measurements. We also excluded samples collected from individuals on days when they displayed injuries or symptoms of sickness (as assessed by the on-site veterinary staff) since injury and sickness lead to extremely elevated cortisol levels in primates (e.g., Barton 1987; Muehlenbein & Watts 2010; Behringer et al, 2020 ). Finally, since a large part of our analysis focused on circadian cortisol variation, we excluded all samples for which we did not have a precise time of collection recorded.…”

“…Furthermore, studying physiological effects using diurnal cortisol slopes is an underused paradigm in wild animal subjects despite its prevalence in the human health literature. In chimpanzees, these slopes are repeatable in adults (i.e., are consistent within a given individual over time, Sonnweber et al, 2018 ) but also show plasticity to physiological challenges such as disease outbreaks ( Behringer et al, 2020 ) or aging ( Emery Thompson et al, 2020 ).…”

Immune StimulationviaWounding Alters Chemical Profiles of AdultTribolium castaneum

“…Importantly, to enable individuals to respond to pathogenic threats and to adjust their reactions, they need to be able to detect disease cues in others. Chemical cues have been shown to allow healthy animals to identify diseased conspecifics across taxa (Behringer et al, 2020; Csata et al, 2017; Lopes, 2020; Pull et al, 2018). For example, eusocial insects can detect immunological and disease cues of other nestmates and adjust subsequent social responses towards diseased members (Pull et al, 2018; Sun et al, 2017).…”