Advertisement

Primates

, Volume 56, Issue 4, pp 365–373 | Cite as

Variation in vervet (Chlorocebus aethiops) hair cortisol concentrations reflects ecological disturbance by humans

  • Nicolaas H. Fourie
  • Trudy R. Turner
  • Janine L. Brown
  • James D. Pampush
  • Joseph G. Lorenz
  • Robin M. Bernstein
Original Article

Abstract

Vervet monkeys (Chlorocebus aethiops) often live in close proximity to humans. Vervets are known to raid crops, homes and gardens in suburban areas leading to human–vervet conflict. In general, primate groups with access to human foods experience increased population densities and intra-group aggression. This suggests high stress loads for vervets living in environments with high levels of human habitat disturbance and close proximity to humans. We tested the hypothesis that populations characterized by high levels of human impact are more physiologically stressed than low human impact populations, and that this increased stress would be reflected in higher concentrations of hair cortisol. We predicted that because females would be less likely to engage in high risk foraging activities, and hence keep more distance from humans than males, their hair cortisol levels should be lower than those in males. We quantified cortisol in the hair of wild caught individuals from populations that experienced different degrees of human habitat disturbance and differences in access to human food. We found that males in high human impact groups had significantly higher hair cortisol concentrations than those in low human impact groups, although this difference was not observed in female vervets. Human impacts on vervet behavioral ecology appear to be a significant source of stress for male animals in particular.

Keywords

Hair Cortisol Stress Vervets Human impact Human food 

Notes

Acknowledgments

We thank all those who have taken part in sample and data collection over the course of 2002–2009. We are also indebted to the Environmental Affairs offices in Limpopo, Mpumalanga, Kwa-Zulu Natal, Gauteng, Free State and the Eastern Cape Provinces of South Africa for their assistance. We acknowledge the Smithsonian’s Conservation Biology Institute’s Endocrinology Laboratory, in particular Nicole Presley and Sarah Putman for their friendly assistance and advice. Analyses were carried out with support from the Lewis Cotlow Fund (2008 and 2010) and the National Science Foundation Integrative Graduate Education and Research Traineeship award (NSF IGERT—Award ID: 0801634). Sampling was supported by NSF grant BCS0938969.

Supplementary material

10329_2015_486_MOESM1_ESM.docx (24 kb)
Supplementary material 1 (DOCX 23 kb)

References

  1. Alexander GM, Hines M (2002) Sex differences in response to childrenʼs toys in nonhuman primates (Cercopithecus aethiops sabaeus). Evol Human Behav 23:467–479CrossRefGoogle Scholar
  2. Altmann J, Alberts SC (2005) Growth rates in a wild primate population: ecological influences and maternal effects. Behav Ecol Sociobiol 57:490–501CrossRefGoogle Scholar
  3. Altmann J, Muruthi P (1988) Differences in daily life between semiprovisioned and wild-feeding baboons. Am J Primatol 3:213–221CrossRefGoogle Scholar
  4. Ashley NT, Barboza PS, Macbeth BJ, Janz DM, Cattet MRL, Booth RK, Wasser SK (2011) Glucocorticosteroid concentrations in feces and hair of captive caribou and reindeer following adrenocorticotropic hormone challenge. Gen Comp Endocrinol 172:382–391CrossRefPubMedGoogle Scholar
  5. Basckin DR, Krige PD (1973) Some preliminary observations of the behaviour of an urban troop of vervet monkeys (Cercopithecus aethiops) during the birth season. J Behav Sci 1:287–297Google Scholar
  6. Bechsoft TO, Sonne C, Dietz R, Born EW, Novak MA, Henchey E, Meyer JS (2011) Cortisol levels in hair of East Greenland polar bears. Sci Total Environ 409:831–834CrossRefGoogle Scholar
  7. Bennett A, Hayssen V (2010) Measuring cortisol in hair and saliva from dogs: coat color and pigment differences. Domest Anim Endocrinol 39:171–180CrossRefPubMedGoogle Scholar
  8. Brennan EJ, Else JG, Altmann J (1985) Ecology and behaviour of a pest primate: vervet monkeys in a tourist-lodge habitat. Afr J Ecol 23:35–44CrossRefGoogle Scholar
  9. Carlitz EH, Kirschbaum C, Stalder T, van Schaik CP (2014) Hair as a long-term retrospective cortisol calendar in orang-utans (Pongo spp.): new perspectives for stress monitoring in captive management and conservation. Gen Comp Endocrinol 195:151–156CrossRefPubMedGoogle Scholar
  10. Chapman CA, Saj T, Snaith TV (2007) Temporal dynamics of nutrition, parasitism and stress in colobus monkeys: implications for population regulation and conservation. Am J Phys Anthropol 134:240–250CrossRefPubMedGoogle Scholar
  11. Chrousos GP (2000) Stress, chronic inflammation, and emotional and physical well being: concurrent effects and chronic sequelae. J Allergy Clin Immunol 106:275–291CrossRefGoogle Scholar
  12. Daly M, Wilson M (1978) Sex, evolution and behavior. Duxbury Press, North ScituateGoogle Scholar
  13. Davenport MD, Tiefenbacher S, Lutz CK, Novak MA, Meyer JS (2006) Analysis of endogenous cortisol concentrations in the hair of rhesus macaques. Gen Comp Endocrinol 47:255–261CrossRefGoogle Scholar
  14. De Kloet ER, Oitzel MS, Joels M (1999) Stress and cognition: are corticosteroids good or bad guys? Trends Neurosci 22:422–426CrossRefPubMedGoogle Scholar
  15. Fa JE (1992) Visitor-directed aggression among the Gibraltar macaques. Zoo Biol 11:43–52CrossRefGoogle Scholar
  16. Fairbanks LA, Jorgensen MJ, Bailey JN, Breidenthal JN, Sherry E, Grzywa R, Laudenslager ML (2011) Heritability and genetic correlation of hair cortisol in vervet monkeys in low and higher stress environments. Psychoneuroendocrinology 36:1201–1208PubMedCentralCrossRefPubMedGoogle Scholar
  17. Fourie NH, Bernstein RM (2011a) Hair cortisol levels track phylogenetic and age related differences in hypothalamic–pituitary–adrenal (HPA) axis activity in non-human primates. Gen Comp Endocrinol 174:150–155CrossRefPubMedGoogle Scholar
  18. Fourie NH, Bernstein RM (2011b) Quantification of cortisol in wild and captive nonhuman primate hair: methodological considerations and biological validation. Am J Phys Anthropol S 52:137Google Scholar
  19. Fourie NH, Jolly CJ, Phillips-Conroy JE, Brown JL, Bernstein RM (2015) Variation of hair cortisol concentrations among wild populations of two baboon species (Papio anubis, P. hamadryas) and a population of their natural hybrids. Primates 56:259–272CrossRefPubMedGoogle Scholar
  20. Frantz AC, Schaul M, Pope LC, Fack F, Schley L, Muller CP, Roper TJ (2004) Estimating population size by genotyping remotely plucked hair: the Eurasian badger. J Appl Ecol 41:985–995CrossRefGoogle Scholar
  21. Fuentes A, Gamerl S (2005) Characterizing aggressive interactions between long-tailed macaques (Macaca fascicularis) and human tourists at Padangtegal Money Forest, Bali, Indonesia. Am J Primatol 66:197–204CrossRefPubMedGoogle Scholar
  22. Gaetono TJ, Danzy J, Ntsali MS, Theron N, Schmitt CA, Grobler JP, Nelson F, Turner TR (2014) Mapping correlates of parasitism in wild South African vervet monkeys (Chlorocebus aethiops). S Afr J Wildl Res 44:56–70CrossRefGoogle Scholar
  23. Gesquiere LR, Khan M, Shek L, Wango TL, Wango EO, Alberts SC, Altmann J (2008) Coping with a challenging environment: effects of seasonal variability and reproductive status on glucocorticoid concentrations of female baboons (Papio cynocephalus). Horm Behav 54:410–416PubMedCentralCrossRefPubMedGoogle Scholar
  24. Grobler PJ, Matlala JM (2002) Regional genetic variability among South African vervet monkey Chlorocebus aethiops populations. Acta Theriol 47:113–124CrossRefGoogle Scholar
  25. Grobler JP, Turner TR (2010) A novel trap design for the capture and sedation of vervet monkeys (Chlorocebus aethiops). S Afr J Wildl Res 40:163–168CrossRefGoogle Scholar
  26. Groves C (2001) Primate taxonomy. Smithsonian Institute Press, WashingtonGoogle Scholar
  27. Hill C (2000) Conflict of interest between people and baboons: crop raiding in Uganda. Int J Primatol 21:299–315CrossRefGoogle Scholar
  28. Hockings KJ (2007) Human–chimpanzee coexistence at Bossou, the Republic of Guinea: a chimpanzee perspective. Ph.D. Thesis, University of Stirling, StirlingGoogle Scholar
  29. Horrocks J, Baulu J (1994) Food competition between vervets (Cercopithecus aethiops sabaeus) and farmers in Barbados—implications for management. Rev Ecol 49:281–294Google Scholar
  30. Kemnitz JW, Sapolsky RM, Altmann J, Muruthi P, Mott GE, Stefanick ML (2002) Effects of food availability on serum insulin and lipid concentrations in free-ranging baboons. Am J Primatol 57:13–19CrossRefPubMedGoogle Scholar
  31. Lee PC, Priston NEC (2005) Human attitudes to primates: perceptions of pests, conflict and consequences for primate conservation. In: Norman JD, Wallis J (eds) Commensalism and conflict: the human–primate interface. American Society of Primatologists, Oklahoma, pp 1–23Google Scholar
  32. Macbeth BJ, Cattet MRL, Stenhouse GB, Gibeau ML, Janz DM (2010) Hair cortisol concentration as a noninvasive measure of long-term stress in free-ranging grizzly bears (Ursus arctos): considerations with implications for other wildlife. Can J Zool 88:935–949CrossRefGoogle Scholar
  33. Martin JGA, Réale D (2008) Animal temperament and human disturbance: implications for the response of wildlife to tourism. Behav Process 77:66–72CrossRefGoogle Scholar
  34. Munro CJ, Lasley BL (1988) Non-radiometric methods for immunoassay of steroid hormones. Prog Clin Biol Res 285:289–329PubMedGoogle Scholar
  35. Nelson R (2005) An introduction to behavioral endocrinology. Sinauer Associates, Inc., SunderlandGoogle Scholar
  36. O’Leary H, Fa JE (1993) Effects of tourists on Barbary macaques at Gibraltar. Folia Primatol 61:77–91CrossRefPubMedGoogle Scholar
  37. Pampush JD (2010) Human food access and its effects on South African vervet body mass. Masterʼs thesis, University of Wisconsin–Milwaukee, Milwaukee WIGoogle Scholar
  38. Priston NE, Wyper RM, Lee PC (2012) Buton macaques (Macaca ochreata brunnescens): crops, conflict, and behavior on farms. Am J Primatol 74:29–36CrossRefPubMedGoogle Scholar
  39. Rangel-Negrin A, Alfaro JL, Valdez RA, Romano MC, Serio-Silva JC (2009) Stress in Yucatan spider monkeys: effects of environmental conditions on fecal cortisol levels in wild captive populations. Anim Conserv 12:496–502CrossRefGoogle Scholar
  40. Riley EP (2007) The human–macaque interface: conservation implications of current and future overlap and conflict in Lore Lindu National Park, Sulawesi, Indonesia. Am Anthropol 109:473–484CrossRefGoogle Scholar
  41. Rowe N (1996) The pictorial guide to the living primates. Pogonias Press, New YorkGoogle Scholar
  42. Saj TL, Sicotte P, Paterson JD (1999) Influence of human food consumption on the time budget of vervets. Int J Primatol 20:977–994CrossRefGoogle Scholar
  43. Saj TL, Sicotte P, Paterson JD (2001) The conflict between vervet monkeys and farmers at the forest edge in Entebbe, Uganda. Afr J Ecol 39:195–199CrossRefGoogle Scholar
  44. Sapolsky RM (1986) Endocrine and behavioral correlates of drought in wild olive baboons (Papio anubis). Am J Primatol 11:217–227CrossRefGoogle Scholar
  45. Sapolsky RM (1992) Stress, the aging brain and the mechanisms of neuron death. MIT Press, CambridgeGoogle Scholar
  46. Sapolsky RM (2000) Stress hormones: good and bad. Neurobiol Dis 7:540–542CrossRefPubMedGoogle Scholar
  47. Sapolsky RM (2004) Why zebras don’t get ulcers: a guide to stress, stress related diseases and coping. W. H. Freeman, New YorkGoogle Scholar
  48. Sapolsky RM (2005) The influence of social hierarchy on primate health. Science 308:648–652CrossRefPubMedGoogle Scholar
  49. Sapolsky RM, Share LJ (2004) A pacific culture among wild baboons: its emergence and transmission. PLoS Biol 2:0534–0541CrossRefGoogle Scholar
  50. Sauve B, Koren G, Walsh G, Tokmakejian S, van Uum SHM (2007) Measurement of cortisol in human hair as a biomarker of systemic exposure. Clin Invest Med 30:E183–E191PubMedGoogle Scholar
  51. Southwick CH, Siddioi M, Farooq FM, Yahya P, Bikas C (1976) Effects of artificial feeding on aggressive behaviour of rhesus monkeys in India. Anim Behav 24:11–15CrossRefPubMedGoogle Scholar
  52. Taylor SE, Klein LC, Lewis BP, Gruenewald TL, Gurung RA, Updegraff JA (2000) Biobehavioral responses to stress in females: tend-and-befriend, not fight-or-flight. Psychol Rev 107:411–429CrossRefPubMedGoogle Scholar
  53. Turner TR, Anapol F, Jolly CJ (1997) Growth, development, and sexual dimorphism in vervet monkeys (Cercopithecus aethiops) at four sites in Kenya. Am J Phys Anthropol 103:19–35CrossRefPubMedGoogle Scholar
  54. Wallace GE, Hill CM (2012) Crop damage by primates: quantifying the key parameters of crop-raiding events. PLoS One 10:e46636CrossRefGoogle Scholar
  55. Webb E, Thomson S, Nelson A, White C, Koren G, Rieder M (2010) Assessing individual systemic stress through cortisol analysis of archaeological hair. J Arch Sci 37:807–812CrossRefGoogle Scholar
  56. Yamada J, Stevens B, De Silva N, Gibbins S, Beyene J, Taddio A, Newman C, Koren G (2007) Hair cortisol as a potential biologic marker of chronic stress in hospitalized neonates. Neonatology 92:42–49CrossRefPubMedGoogle Scholar

Copyright information

© Japan Monkey Centre and Springer Japan (outside the USA) 2015

Authors and Affiliations

  • Nicolaas H. Fourie
    • 1
  • Trudy R. Turner
    • 2
    • 3
  • Janine L. Brown
    • 4
  • James D. Pampush
    • 5
  • Joseph G. Lorenz
    • 6
  • Robin M. Bernstein
    • 7
  1. 1.Biobehavioral Branch, Division of Intramural ResearchNational Institute of Nursing Research, National Institutes of HealthBethesdaUSA
  2. 2.Department of AnthropologyUniversity of Wisconsin-MilwaukeeMilwaukeeUSA
  3. 3.Department of GeneticsUniversity of the Free StateBloemfonteinSouth Africa
  4. 4.Smithsonian Conservation Biology Institute, Center for Species SurvivalFront RoyalUSA
  5. 5.Department of Evolutionary AnthropologyDuke UniversityDurhamUSA
  6. 6.Department of Anthropology and Museum StudiesCentral Washington UniversityEllensburgUSA
  7. 7.Department of AnthropologyUniversity of Colorado BoulderBoulderUSA

Personalised recommendations