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Volume 168, Issue 8

A comparison of faecal glucocorticoid metabolite concentration and gut microbiota diversity in bonobos () Free

Abstract

Sex, age, diet, stress and social environment have all been shown to influence the gut microbiota. In several mammals, including humans, increased stress is related to decreasing gut microbial diversity and may differentially impact specific taxa. Recent evidence from gorillas shows faecal glucocorticoid metabolite concentration (FGMC) did not significantly explain gut microbial diversity, but it was significantly associated with the abundance of the family Anaerolineaceae. These patterns have yet to be examined in other primates, like bonobos (). We compared FGMC to 16S rRNA amplicons for 202 bonobo faecal samples collected across 5 months to evaluate the impact of stress, measured with FGMC, on the gut microbiota. Alpha diversity measures (Chao’s and Shannon’s indexes) were not significantly related to FGMC. FGMC explained 0.80 % of the variation in beta diversity for Jensen–Shannon and 1.2% for weighted UniFrac but was not significant for unweighted UniFrac. We found that genus , a member of the family Anaerolinaceae had a significant positive relationship with FGMC. These results suggest that bonobos are relatively similar to gorillas in alpha diversity and family Anaerolinaceae responses to FGMC, but different from gorillas in beta diversity. Members of the family Anaerolinaceae may be differentially affected by FGMC across great apes. FGMC appears to be context dependent and may be species-specific for alpha and beta diversity but this study provides an example of consistent change in two African apes. Thus, the relationship between physiological stress and the gut microbiome may be difficult to predict, even among closely related species.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): bonobo , cortisol , faecal glucocorticoid metabolites , microbiota and stress
© 2022 The Authors
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2022-08-12
2024-04-19
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References

  1. Allaband C, McDonald D, Vázquez-Baeza Y, Minich JJ, Tripathi A et al. Microbiome 101: studying, analyzing, and interpreting gut microbiome data for clinicians. Clin Gastroenterol Hepatol 2019; 17:218–230 [View Article] [PubMed]
     [Google Scholar]
  2. Amato KR. Incorporating the gut microbiota into models of human and non-human primate ecology and evolution: gut microbiota influences host nutrition, health, and behavior. Am J Phys Anthropol 2016; 159: [View Article]
     [Google Scholar]
  3. Dantas G, Sommer MOA, Degnan PH, Goodman AL. Experimental approaches for defining functional roles of microbes in the human gut. Annu Rev Microbiol 2013; 67:459–475 [View Article] [PubMed]
     [Google Scholar]
  4. Barlow GM, Yu A, Mathur R. Role of the gut microbiome in obesity and diabetes mellitus. Nutr Clin Pract 2015; 30:787–797 [View Article] [PubMed]
     [Google Scholar]
  5. Chattopadhyay I, Dhar R, Pethusamy K, Seethy A, Srivastava T et al. Exploring the role of gut microbiome in colon cancer. Appl Biochem Biotechnol 2021; 193:1780–1799 [View Article] [PubMed]
     [Google Scholar]
  6. Franzosa EA, Sirota-Madi A, Avila-Pacheco J, Fornelos N, Haiser HJ et al. Gut microbiome structure and metabolic activity in inflammatory bowel disease. Nat Microbiol 2019; 4:293–305 [View Article] [PubMed]
     [Google Scholar]
  7. Kim YS, Milner JA. Dietary modulation of colon cancer risk. J Nutr 2007; 137:2576S–2579S [View Article] [PubMed]
     [Google Scholar]
  8. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A et al. A core gut microbiome in obese and lean twins. Nature 2009; 457:480–484 [View Article] [PubMed]
     [Google Scholar]
  9. Konturek PC, Brzozowski T, Konturek SJ. Stress and the gut: pathophysiology, clinical consequences, diagnostic approach and treatment options. J Physiol Pharmacol 2011; 62:591–599
     [Google Scholar]
  10. Bharwani A, Mian MF, Foster JA, Surette MG, Bienenstock J et al. Structural & functional consequences of chronic Psychosocial stress on the microbiome & host. Psychoneuroendocrinology 2016; 63:217–227 [View Article] [PubMed]
     [Google Scholar]
  11. Bhatia V, Tandon RK. Stress and the gastrointestinal tract. J Gastroenterol Hepatol 2005; 20:332–339 [View Article] [PubMed]
     [Google Scholar]
  12. Bailey MT. The effects of psychological stressors on the intestinal microbiota. Biosci Microflora 2009; 28:125–134 [View Article]
     [Google Scholar]
  13. Moloney RD, Desbonnet L, Clarke G, Dinan TG, Cryan JF. The microbiome: stress, health and disease. Mamm Genome 2014; 25:49–74 [View Article] [PubMed]
     [Google Scholar]
  14. Tetel MJ, de Vries GJ, Melcangi RC, Panzica G, O’Mahony SM. Steroids, stress and the gut microbiome-brain axis. J Neuroendocrinol 2018; 30: [View Article] [PubMed]
     [Google Scholar]
  15. Söderholm JD, Perdue MH. II. Stress and intestinal barrier function. Am J Physiol Gastrointest Liver Physiol 2001; 280:G7–G13 [View Article] [PubMed]
     [Google Scholar]
  16. Collins SM. Stress and the gastrointestinal tract IV. Modulation of intestinal inflammation by stress: basic mechanisms and clinical relevance. Am J Physiol Gastrointest Liver Physiol 2001; 280:G315–8 [View Article] [PubMed]
     [Google Scholar]
  17. Bailey MT, Coe CL. Maternal separation disrupts the integrity of the intestinal microflora in infant rhesus monkeys. Dev Psychobiol 1999; 35:146–155 [View Article] [PubMed]
     [Google Scholar]
  18. Keay JM, Singh J, Gaunt MC, Kaur T. Fecal glucocorticoids and their metabolites as indicators of stress in various mammalian species: a literature review. J Zoo Wildl Med 2006; 37:234–244 [View Article] [PubMed]
     [Google Scholar]
  19. Sandrini S, Aldriwesh M, Alruways M, Freestone P. Microbial endocrinology: host-bacteria communication within the gut microbiome. J Endocrinol 2015; 225:R21–34 [View Article] [PubMed]
     [Google Scholar]
  20. Foster JA, Rinaman L, Cryan JF. Stress & the gut-brain axis: regulation by the microbiome. Neurobiol Stress 2017; 7:124–136 [View Article] [PubMed]
     [Google Scholar]
  21. Moser V. Graduate research projects. The human microbiome: the brain-gut axis and its role in immunity 20147
     [Google Scholar]
  22. Crumeyrolle-Arias M, Jaglin M, Bruneau A, Vancassel S, Cardona A et al. Absence of the gut microbiota enhances anxiety-like behavior and neuroendocrine response to acute stress in rats. Psychoneuroendocrinology 2014; 42:207–217 [View Article] [PubMed]
     [Google Scholar]
  23. Hata T, Miyata N, Takakura S, Yoshihara K, Asano Y et al. The gut microbiome derived from Anorexia Nervosa patients impairs weight gain and behavioral performance in mice. SSRN Journal 2018; 3155625: [View Article]
     [Google Scholar]
  24. Li J, Sung CYJ, Lee N, Ni Y, Pihlajamäki J et al. Probiotics modulated gut microbiota suppresses hepatocellular carcinoma growth in mice. Proc Natl Acad Sci U S A 2016; 113:E1306–15 [View Article] [PubMed]
     [Google Scholar]
  25. Bravo JA, Forsythe P, Chew MV, Escaravage E, Savignac HM et al. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci U S A 2011; 108:16050–16055 [View Article] [PubMed]
     [Google Scholar]
  26. Bharwani A, Mian MF, Foster JA, Surette MG, Bienenstock J et al. Structural & functional consequences of chronic psychosocial stress on the microbiome & host. Psychoneuroendocrinology 2016; 63:217–227 [View Article] [PubMed]
     [Google Scholar]
  27. Stothart MR, Palme R, Newman AEM. It’s what’s on the inside that counts: stress physiology and the bacterial microbiome of a wild urban mammal. Proc Biol Sci 2019; 286:20192111 [View Article] [PubMed]
     [Google Scholar]
  28. Yan D, Hu D, Li K, Li B, Zeng X et al. Effects of chronic stress on the Fecal Microbiome of Malayan Pangolins (Manis javanica) rescued from the illegal wildlife trade. Curr Microbiol 2021; 78:1017–1025 [View Article] [PubMed]
     [Google Scholar]
  29. Moustafa MAM, Chel HM, Thu MJ, Bawm S, Htun LL et al. Anthropogenic interferences lead to gut microbiome dysbiosis in Asian elephants and may alter adaptation processes to surrounding environments. Sci Rep 2021; 11:741 [View Article] [PubMed]
     [Google Scholar]
  30. Antwis RE, Edwards KL, Unwin B, Walker SL, Shultz S. Rare gut microbiota associated with breeding success, hormone metabolites and ovarian cycle phase in the critically endangered eastern black rhino. Microbiome 2019; 7:27 [View Article] [PubMed]
     [Google Scholar]
  31. Surbeck M, Deschner T, Weltring A, Hohmann G. Social correlates of variation in urinary cortisol in wild male bonobos (Pan paniscus). Horm Behav 2012; 62:27–35 [View Article] [PubMed]
     [Google Scholar]
  32. Young T, Isbell L. Ecological models of female social relationships in primates: similarities, disparities, and some directions for future clarity. Behav 2002; 139:177–202 [View Article]
     [Google Scholar]
  33. Amato KR. Incorporating the gut microbiota into models of human and non-human primate ecology and evolution. Am J Phys Anthropol 2016; 159:S196–215 [View Article] [PubMed]
     [Google Scholar]
  34. Bailey MT. The contributing role of the intestinal microbiota in stressor-induced increases in susceptibility to enteric infection and systemic immunomodulation. Horm Behav 2012; 62:286–294 [View Article] [PubMed]
     [Google Scholar]
  35. Vlčková K, Shutt-Phillips K, Heistermann M, Pafčo B, Petrželková KJ et al. Impact of stress on the gut microbiome of free-ranging western lowland gorillas. Microbiology 2018; 164:40–44 [View Article] [PubMed]
     [Google Scholar]
  36. McGrew WC, Marchant LF, Nishida T, Goodall J, Itani J. Great Ape Societies Cambridge University Press; 1996 [View Article]
     [Google Scholar]
  37. Tan J, Ariely D, Hare B. Bonobos respond prosocially toward members of other groups. Sci Rep 2017; 7:14733 [View Article] [PubMed]
     [Google Scholar]
  38. White FJ. Pan paniscus 1973 to 1996: twenty-three years of field research. Evol Anthropol 1996; 5:11–17 [View Article]
     [Google Scholar]
  39. Gruber T, Clay Z. A comparison between Bonobos and Chimpanzees: a review and update. Evol Anthropol 2016; 25:239–252 [View Article] [PubMed]
     [Google Scholar]
  40. Forcina G, Vallet D, Le Gouar PJ, Bernardo-Madrid R, Illera G et al. From groups to communities in western lowland gorillas. Proc Biol Sci 2019; 286:20182019 [View Article] [PubMed]
     [Google Scholar]
  41. Parnell RJ. Group size and structure in western lowland gorillas (Gorilla gorilla gorilla) at Mbeli Bai, Republic of Congo. Am J Primatol 2002; 56:193–206 [View Article] [PubMed]
     [Google Scholar]
  42. Harcourt AH, Stewart KJ. Gorilla society: what we know and don’t know. Evol Anthropol 2007; 16:147–158 [View Article]
     [Google Scholar]
  43. Kyrou I, Tsigos C. Stress hormones: physiological stress and regulation of metabolism. Curr Opin Pharmacol 2009; 9:787–793 [View Article] [PubMed]
     [Google Scholar]
  44. Thau L, Gandhi J, Sharma S. Physiology,Cortisol StatPearls Publishing; 2021
     [Google Scholar]
  45. Tkaczynski PJ, Behringer V, Ackermann CY, Fedurek P, Fruth B et al. Patterns of urinary cortisol levels during ontogeny appear population specific rather than species specific in wild chimpanzees and bonobos. J Hum Evol 2020; 147:102869 [View Article] [PubMed]
     [Google Scholar]
  46. Fourie NH, Brown JL, Jolly CJ, Phillips-Conroy JE, Rogers J et al. Sources of variation in hair cortisol in wild and captive non-human primates. Zoology (Jena) 2016; 119:119–125 [View Article] [PubMed]
     [Google Scholar]
  47. Strier KB, Ziegler TE, Wittwer DJ. Seasonal and social correlates of fecal testosterone and cortisol levels in wild male muriquis (Brachyteles arachnoides). Horm Behav 1999; 35:125–134 [View Article] [PubMed]
     [Google Scholar]
  48. Hohmann G, Mundry R, Deschner T. The relationship between socio-sexual behavior and salivary cortisol in bonobos: tests of the tension regulation hypothesis. Am J Primatol 2009; 71:223–232 [View Article] [PubMed]
     [Google Scholar]
  49. Mason HL, Myers CS, Kendall EC. Chemical studies of the suprarenal cortex II. the identification of a substance which possesses the qualitative action of cortin; its conversion into a diketone closely related to androstenedione. J Biol Chem 1936; 116:267–276 [View Article]
     [Google Scholar]
  50. Mason HL, Hoehn WM, Kendall EC. Chemical studies of the suprarenal cortex. J Biol Chem 1938; 124:459–474 [View Article]
     [Google Scholar]
  51. Millspaugh JJ, Washburn BE. Use of fecal glucocorticoid metabolite measures in conservation biology research: considerations for application and interpretation. Gen Comp Endocrinol 2004; 138:189–199 [View Article] [PubMed]
     [Google Scholar]
  52. Davenport ER, Sanders JG, Song SJ, Amato KR, Clark AG et al. The human microbiome in evolution. BMC Biol 2017; 15:127 [View Article] [PubMed]
     [Google Scholar]
  53. Cheng L, Lucchesi S, Mundry R, Samuni L, Deschner T et al. Variation in aggression rates and urinary cortisol levels indicates intergroup competition in wild bonobos. Horm Behav 2021; 128:104914 [View Article] [PubMed]
     [Google Scholar]
  54. Cobden AK. Party Animals: Food, Sociality and Stress in Wild Bonobos (Pan paniscus) of Iyema, Lomako Forest, Democratic Republic of Congo, PhD Thesis Emory University; 2014
     [Google Scholar]
  55. Malenky RK, Wrangham RW. A quantitative comparison of terrestrial herbaceous food consumption by Pan paniscus in the Lomako Forest, Zaire, and Pan troglodytes in the Kibale Forest, Uganda. Am J Primatol 1994; 32:1–12 [View Article] [PubMed]
     [Google Scholar]
  56. Wrangham RW, White FJ. Feeding competition and patch size in the chimpanzee species Pan paniscus and Pan troglodytes. Behav 1988; 105:148–164 [View Article]
     [Google Scholar]
  57. Dupain J, Van Krunkelsven E, Van Elsacker L, Verheyen RF. Current status of the bonobo (Pan paniscus) in the proposed Lomako Reserve (Democratic Republic of Congo). Biol Conserv 2000; 94:265–272 [View Article]
     [Google Scholar]
  58. Brand CM, White FJ, Wakefield ML, Waller MT, Ruiz-Lopez MJ et al. Initiation of genetic demographic monitoring of bonobos (Pan paniscus) at Iyema, Lomako forest, DRC. Primate Conserv Newsl J IUCNSSC Primate Spec Group 2016; 30:103
     [Google Scholar]
  59. Prado-Martinez J, Sudmant PH, Kidd JM, Li H, Kelley JL et al. Great ape genetic diversity and population history. Nature 2013; 499:471–475 [View Article]
     [Google Scholar]
  60. Langergraber KE, Prüfer K, Rowney C, Boesch C, Crockford C et al. Generation times in wild chimpanzees and gorillas suggest earlier divergence times in great ape and human evolution. Proc Natl Acad Sci U S A 2012; 109:15716–15721 [View Article] [PubMed]
     [Google Scholar]
  61. Blekhman R, Tang K, Archie EA, Barreiro LB, Johnson ZP et al. Common methods for fecal sample storage in field studies yield consistent signatures of individual identity in microbiome sequencing data. Sci Rep 2016; 6:31519 [View Article] [PubMed]
     [Google Scholar]
  62. Hayakawa T, Sawada A, Tanabe AS, Fukuda S, Kishida T et al. Improving the standards for gut microbiome analysis of fecal samples: insights from the field biology of Japanese macaques on Yakushima Island. Primates 2018; 59:423–436 [View Article] [PubMed]
     [Google Scholar]
  63. Vlčková K, Mrázek J, Kopečný J, Petrželková KJ. Evaluation of different storage methods to characterize the fecal bacterial communities of captive western lowland gorillas (Gorilla gorilla gorilla). J Microbiol Methods 2012; 91:45–51 [View Article] [PubMed]
     [Google Scholar]
  64. Hale VL, Tan CL, Knight R, Amato KR. Effect of preservation method on spider monkey (Ateles geoffroyi) fecal microbiota over 8 weeks. J Microbiol Methods 2015; 113:16–26 [View Article] [PubMed]
     [Google Scholar]
  65. Gorzelak MA, Gill SK, Tasnim N, Ahmadi-Vand Z, Jay M et al. Methods for improving human gut microbiome data by reducing variability through sample processing and storage of stool. PLOS ONE 2015; 10:e0134802 [View Article] [PubMed]
     [Google Scholar]
  66. Choo JM, Leong LEX, Rogers GB. Sample storage conditions significantly influence faecal microbiome profiles. Sci Rep 2015; 5:16350 [View Article] [PubMed]
     [Google Scholar]
  67. Menke S, Gillingham MAF, Wilhelm K, Sommer S. Home-made cost effective preservation buffer is a better alternative to commercial preservation methods for microbiome research. Front Microbiol 2017; 8:102 [View Article] [PubMed]
     [Google Scholar]
  68. Midttveit E. Measuring stress in captive bonobos: a look to the past and future to improve methods; 2016Oct https://scholarsbank.uoregon.edu/xmlui/handle/1794/20464 accessed 15 January 2021
  69. Brand CM, Boose KJ, Squires EC, Marchant LF, White FJ et al. Hair plucking, stress, and urinary cortisol among captive bonobos (Pan paniscus). Zoo Biol 2016; 35:415–422 [View Article] [PubMed]
     [Google Scholar]
  70. Goodfellow CK, Whitney T, Christie DM, Sicotte P, Wikberg EC et al. Divergence in gut microbial communities mirrors a social group fission event in a black-and-white colobus monkey (Colobus vellerosus). Am J Primatol 2019; 81:e22966 [View Article] [PubMed]
     [Google Scholar]
  71. Wikberg EC, Christie D, Sicotte P, Ting N. Interactions between social groups of colobus monkeys (Colobus vellerosus) explain similarities in their gut microbiomes. Anim Behav 2020; 163:17–31 [View Article]
     [Google Scholar]
  72. Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 2019; 37:852–857 [View Article] [PubMed]
     [Google Scholar]
  73. Davis NM, Proctor DM, Holmes SP, Relman DA, Callahan BJ. Simple statistical identification and removal of contaminant sequences in marker-gene and metagenomics data. Microbiome 2018; 6:226 [View Article] [PubMed]
     [Google Scholar]
  74. Colby HD, Kitay JI. Sex and substrate effects on hepatic corticosteroid metabolism in the rat. Endocrinology 1972; 90:473–478 [View Article] [PubMed]
     [Google Scholar]
  75. Adriansjach J, Baum ST, Lefkowitz EJ, Van Der Pol WJ, Buford TW et al. Age-related differences in the gut microbiome of rhesus macaques. J Gerontol A Biol Sci Med Sci 2020; 75:1293–1298 [View Article] [PubMed]
     [Google Scholar]
  76. Aatsinki A-K, Keskitalo A, Laitinen V, Munukka E, Uusitupa H-M et al. Maternal prenatal psychological distress and hair cortisol levels associate with infant fecal microbiota composition at 2.5 months of age. Psychoneuroendocrinology 2020; 119:104754 [View Article] [PubMed]
     [Google Scholar]
  77. The R Development Core Team R: A language and environment for statistical computing; 2013
  78. Oksanen J, Guillaume FB, Roeland K, Peter RM, Gavin LS et al. Package Vegan: Community ecology package, version 2.0 10 Cran; 2013
     [Google Scholar]
  79. Anderson MJ. Permutational multivariate analysis of variance (PERMANOVA). Wiley Statsref Stat Ref Online 20141–15
     [Google Scholar]
  80. Menéndez ML, Pardo JA, Pardo L, Pardo MC. The Jensen-Shannon divergence. J Franklin Inst 1997; 334:307–318 [View Article]
     [Google Scholar]
  81. Lozupone C, Knight R. UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 2005; 71:8228–8235 [View Article] [PubMed]
     [Google Scholar]
  82. Mandal S, Van Treuren W, White RA, Eggesbø M, Knight R et al. Analysis of composition of microbiomes: a novel method for studying microbial composition. Microb Ecol Health Dis 2015; 26:27663 [View Article] [PubMed]
     [Google Scholar]
  83. McCord AI, Chapman CA, Weny G, Tumukunde A, Hyeroba D et al. Fecal microbiomes of non-human primates in Western Uganda reveal species-specific communities largely resistant to habitat perturbation. Am J Primatol 2014; 76:347–354 [View Article] [PubMed]
     [Google Scholar]
  84. Young C, Majolo B, Heistermann M, Schülke O, Ostner J. Responses to social and environmental stress are attenuated by strong male bonds in wild macaques. Proc Natl Acad Sci U S A 2014; 111:18195–18200 [View Article] [PubMed]
     [Google Scholar]
  85. Cheney DL, Seyfarth RM. Stress and coping mechanisms in female primates. In Advances in the Study of Behavior vol 39 Academic Press; 2009 pp 1–44 [View Article]
     [Google Scholar]
  86. Amato KR, Yeoman CJ, Kent A, Righini N, Carbonero F et al. Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes. ISME J 2013; 7:1344–1353 [View Article] [PubMed]
     [Google Scholar]
  87. Usui N, Matsuzaki H, Shimada S. Characterization of early life stress-affected gut microbiota. Brain Sci 2021; 11:913 [View Article] [PubMed]
     [Google Scholar]
  88. Kim Y-M, Snijders AM, Brislawn CJ, Stratton KG, Zink EM et al. Light-stress influences the composition of the murine gut microbiome, memory function, and plasma metabolome. Front Mol Biosci 2019; 6:108 [View Article] [PubMed]
     [Google Scholar]
  89. Oki K, Toyama M, Banno T, Chonan O, Benno Y et al. Comprehensive analysis of the fecal microbiota of healthy Japanese adults reveals a new bacterial lineage associated with a phenotype characterized by a high frequency of bowel movements and a lean body type. BMC Microbiol 2016; 16:284 [View Article] [PubMed]
     [Google Scholar]
  90. Rajilić-Stojanović M, de Vos WM. The first 1000 cultured species of the human gastrointestinal microbiota. FEMS Microbiol Rev 2014; 38:996–1047 [View Article] [PubMed]
     [Google Scholar]
  91. Ley RE. Prevotella in the gut: choose carefully. Nat Rev Gastroenterol Hepatol 2016; 13:69–70 [View Article] [PubMed]
     [Google Scholar]
  92. Stothart MR, Bobbie CB, Schulte-Hostedde AI, Boonstra R, Palme R et al. Stress and the microbiome: linking glucocorticoids to bacterial community dynamics in wild red squirrels. Biol Lett 2016; 12:20150875 [View Article] [PubMed]
     [Google Scholar]
  93. Shutt K, Setchell JM, Heistermann M. 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. Gen Comp Endocrinol 2012; 179:167–177 [View Article] [PubMed]
     [Google Scholar]
  94. Wheeler BC, Tiddi B, Kalbitzer U, Visalberghi E, Heistermann M. Methodological considerations in the analysis of Fecal Glucocorticoid metabolites in Tufted Capuchins (Cebus apella). Int J Primatol 2013; 34:879–898 [View Article] [PubMed]
     [Google Scholar]
  95. Touma C, Sachser N, Möstl E, Palme R. Effects of sex and time of day on metabolism and excretion of corticosterone in urine and feces of mice. Gen Comp Endocrinol 2003; 130:267–278 [View Article] [PubMed]
     [Google Scholar]
  96. Bennett G, Malone M, Sauther ML, Cuozzo FP, White B et al. Host age, social group, and habitat type influence the gut microbiota of wild ring-tailed lemurs (Lemur catta). Am J Primatol 2016; 78:883–892 [View Article] [PubMed]
     [Google Scholar]
  97. Tung J, Barreiro LB, Burns MB, Grenier J-C, Lynch J et al. Social networks predict gut microbiome composition in wild baboons. Elife 2015; 4: [View Article] [PubMed]
     [Google Scholar]
  98. Amato KR, Leigh SR, Kent A, Mackie RI, Yeoman CJ et al. The gut microbiota appears to compensate for seasonal diet variation in the wild black howler monkey (Alouatta pigra). Microb Ecol 2015; 69:434–443 [View Article] [PubMed]
     [Google Scholar]
  99. Bruorton MR, Davis CL, Perrin MR. Gut microflora of vervet and samango monkeys in relation to diet. Appl Environ Microbiol 1991; 57:573–578 [View Article] [PubMed]
     [Google Scholar]
  100. Baniel A, Amato KR, Beehner JC, Bergman TJ, Mercer A et al. Seasonal shifts in the gut microbiome indicate plastic responses to diet in wild geladas. Microbiome 2021; 9:26 [View Article] [PubMed]
     [Google Scholar]
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A comparison of faecal glucocorticoid metabolite concentration and gut microbiota diversity in bonobos (Pan paniscus)
Microbiology 168, 001226 (2022); https://doi.org/10.1099/mic.0.001226
/content/journal/micro/10.1099/mic.0.001226
/content/journal/micro/10.1099/mic.0.001226
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