Skip to main content
SpringerLink
Log in

Response to long-distance relocation in Asian elephants (Elephas maximus): monitoring adrenocortical activity via serum, urine, and feces

  • Original Paper
  • Published:
European Journal of Wildlife Research Aims and scope Submit manuscript

Abstract

Understanding how elephants respond to potentially stressful events, such as relocation, is important for making informed management decisions. This study followed the relocation of eight Asian elephants from the Cocos (Keeling) Islands to mainland Australia. The first goal of this study was to examine patterns of adrenocortical activity as reflected in three different substrates: serum, urine, and feces. We found that the three substrates yielded very different signals of adrenocortical activity. Fecal glucocorticoid metabolites (FGM) increased as predicted post-transport, but urinary glucocorticoid metabolites (UGM) were actually lower following transport. Serum cortisol levels did not change significantly. We suggest that the differences in FGM and UGM may reflect changes in steroid biosynthesis, resulting in different primary glucocorticoids being produced at different stages of the stress response. Additional studies are needed to more thoroughly understand the signals of adrenocortical activity yielded by different substrates. The second goal was to examine individual variation in patterns of adrenal response. There was a positive correlation between baseline FGM value and duration of post-transfer increase in FGM concentration. Furthermore, an individual's adrenocortical response to relocation was correlated with behavioral traits of elephants. Elephants that were described by keepers as being “curious” exhibited a more prolonged increase in FGM post-transfer, and “reclusive” elephants had a greater increase in FGM values. Future research should investigate the importance of these personality types for the management and welfare of elephants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Brown JL, Wemmer CM, Lehnhardt J (1995) Urinary cortisol analysis for monitoring adrenal activity in elephants. Zoo Biol 14:533–542

    Article  CAS  Google Scholar 

  • Brown JL, Somerville M, Riddle HS, Keele M, Duer CK, Freeman EW (2007) Comparative endocrinology of testicular, adrenal and thyroid function in captive Asian and African elephant bulls. Gen Comp Endocrinol 151:153–162

    Article  PubMed  CAS  Google Scholar 

  • Brown JL, Kersey DC, Freeman EW, Wagener T (2010) Assessment of diurnal urinary cortisol excretion in Asian and African elephants using different endocrine methods. Zoo Biol 29:274–283

    Article  PubMed  Google Scholar 

  • Carere C, Caramaschi D, Fawcett TW (2010) Covariation between personalities and individual differences in coping with stress: converging evidence and hypotheses. Curr Zool 56:728–740

    Google Scholar 

  • Collins PM, Tsang WN, Metzger JM (1984) Influence of stress on adrenocortical function in the male tree shrew (Tupaia belangeri). Gen Comp Endocrinol 55:450–457

    Article  PubMed  CAS  Google Scholar 

  • Cook K, O'Connor C, Gilmour K, Cooke S (2011) The glucocorticoid stress response is repeatable between years in a wild teleost fish. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 197(12):1189–1196

    Article  PubMed  CAS  Google Scholar 

  • Dathe HH, Kuckelkorn B, Minnemann D (1992) Salivary cortisol assessment for stress detection in the Asian elephant (Elephas maximus): a pilot study. Zoo Biol 11:285–289

    Article  CAS  Google Scholar 

  • Dehnhard M (2007) Characterisation of the sympathetic nervous system of Asian (Elephas maximus) and African (Loxodonta africana) elephants based on urinary catecholamine analyses. Gen Comp Endocrinol 151:274–284

    Article  PubMed  CAS  Google Scholar 

  • Dickens MJ, Delehanty DJ, Romero LM (2010) Stress: an inevitable component of animal translocation. Biol Conserv 143:1329–1341

    Article  Google Scholar 

  • Freeman EW, Weiss E, Brown JL (2004) Examination of the interrelationships of behavior, dominance status, and ovarian activity in captive Asian and African elephants. Zoo Biol 23:431–448

    Article  Google Scholar 

  • Freeman EW, Schulte BA, Brown JL (2010a) Investigating the impact of rank and ovarian activity on the social behavior of captive female African elephants. Zoo Biol 29:154–167

    PubMed  Google Scholar 

  • Freeman EW, Schulte BA, Brown JL (2010b) Using behavioral observations and keeper questionnaires to assess social relationships among captive female African elephants. Zoo Biol 29:140–153

    PubMed  Google Scholar 

  • Ganswindt A, Palme R, Heistermann M, Borragan S, Hodges JK (2003) Non-invasive assessment of adrenocortical function in the male African elephant (Loxodonta africana) and its relation to musth. Gen Comp Endocrinol 134:156–166

    Article  PubMed  CAS  Google Scholar 

  • Goymann W (2005) Noninvasive monitoring of hormones in bird droppings—physiological validation, sampling, extraction, sex differences, and the influence of diet on hormone metabolite levels. Ann N Y Acad Sci 1046:35–53

    Article  PubMed  CAS  Google Scholar 

  • Grand AP, Kuhar CW, Leighty KA, Bettinger TL, Laudenslager ML (2012) Using personality ratings and cortisol to characterize individual differences in African elephants (Loxodonta africana). Appl Anim Behav Sci 142:69–75

    Article  Google Scholar 

  • Hancock TM (2010) A duality in mammalian glucocorticoid signaling, Thesis, Queen's University

  • Hildebrandt TB, Göritz F, Hermes R, Reid C, Dehnhard M, Brown JL (2006) Aspects of the reproductive biology and breeding management of Asian and African elephants Elephas maximus and Loxodonta africana. Int Zoo Yearb 40:20–40

    Article  Google Scholar 

  • Kass EH, Hechteb O, Macchi IA, Mou TW (1954) Changes in patterns of secretion of corticosteroids in rabbits after prolonged treatment with ACTH. Proc Soc Exp Biol Med 85:583–587

    Article  PubMed  CAS  Google Scholar 

  • Koolhaas JM, Korte SM, De Boer SF, Van Der Vegt BJ, Van Reenen CG, Hopster H, De Jong IC, Ruis MAW, Blokhuis HJ (1999) Coping styles in animals: current status in behavior and stress-physiology. Neurosci Biobehav Rev 23:925–935

    Article  PubMed  CAS  Google Scholar 

  • Koolhaas JM, de Boer SF, Coppens CM, Buwalda B (2010) Neuroendocrinology of coping styles: towards understanding the biology of individual variation. Front Neuroendocrinol 31:307–321

    Article  PubMed  CAS  Google Scholar 

  • Koren L, Whiteside D, Fahlman Å, Ruckstuhl K, Kutz S, Checkley S, Dumond M, Wynne-Edwards K (2012) Cortisol and corticosterone independence in cortisol-dominant wildlife. Gen Comp Endocrinol 177:113–119

    Article  PubMed  CAS  Google Scholar 

  • Laws N, Ganswindt A, Heistermann M, Harris M, Harris S, Sherwin C (2007) A case study: fecal corticosteroid and behavior as indicators of welfare during relocation of an Asian elephant. J Appl Anim Welf Sci 10:349–358

    Article  PubMed  CAS  Google Scholar 

  • Llano M, Kolanowski J, Ortega N, Crabbe J (1982) Changes in corticosteroid secretory pattern induced by prolonged corticotropin treatment in the rabbit. J Steroid Biochem 17:631–638

    Article  PubMed  CAS  Google Scholar 

  • Mason GJ, Veasey JS (2010) How should the psychological well-being of zoo elephants be objectively investigated? Zoo Biol 29:237–255

    Article  PubMed  Google Scholar 

  • McCrae RR, Costa PT (1985) Updating Norman's “adequacy taxonomy”: intelligence and personality dimensions in natural language and in questionnaires. J Personal Soc Psychol 49:710

    Article  CAS  Google Scholar 

  • Menargues A, Urios V, Mauri M (2008) Welfare assessment of captive Asian elephants (Elephas maximus) and Indian rhinoceros (Rhinoceros unicornis) using salivary cortisol measurement. Anim Welf 17:305–312

    CAS  Google Scholar 

  • Menargues A, Urios V, Limiñana R, Mauri M (2012) Circadian rhythm of salivary cortisol in Asian elephants (Elephas maximus): a factor to consider during welfare assessment. J Appl Anim Welf Sci 15:383–390

    Article  PubMed  CAS  Google Scholar 

  • Millspaugh JJ, Burke T, Van Dyk G, Slotow R, Washburn BE, Woods RJ (2007) Stress response of working African elephants to transportation and safari adventures. J Wildl Manag 71:1257–1260

    Article  Google Scholar 

  • Monfort SL, Wemmer CM, Brown JL, Wildt DE (1990) Use of urinary hormone assays for evaluating endocrine patterns associated with the long-day breeding-season in Elds deer (Cervus eldi). J Exp Zool 4:215–218

    Article  CAS  Google Scholar 

  • Möstl E, Palme R (2002) Hormones as indicators of stress. Domest Anim Endocrinol 23:67–74

    Article  PubMed  Google Scholar 

  • Narayan EJ, Cockrem JF, Hero J-M (2013) Are baseline and short-term corticosterone stress responses in free-living amphibians repeatable? Comp Biochem Physiol Part A Mol Integr Physiol 164:21–28

    Article  CAS  Google Scholar 

  • Narayanan S, Appleton H (1980) Creatinine: a review. Clin Chem 26:1119–1126

    PubMed  CAS  Google Scholar 

  • Overli O, Winberg S, Pottinger TG (2005) Behavioral and neuroendocrine correlates of selection for stress responsiveness in rainbow trout—a review. Integr Comp Biol 45:463–474

    Article  PubMed  Google Scholar 

  • Overli O, Sorensen C, Pulman KGT, Pottinger TG, Korzan W, Summers CH, Nilsson GE (2007) Evolutionary background for stress-coping styles: relationships between physiological, behavioral, and cognitive traits in non-mammalian vertebrates. Neurosci Biobehav Rev 31:396–412

    Article  PubMed  CAS  Google Scholar 

  • Ozbay F, Johnson DC, Dimoulas E, Morgan C III, Charney D, Southwick S (2007) Social support and resilience to stress: from neurobiology to clinical practice. Psychiatry (Edgmont) 4:35

    Google Scholar 

  • Palme R (2005) Measuring fecal steroids—guidelines for practical application. Ann N Y Acad Sci 1046:75–80

    Article  PubMed  CAS  Google Scholar 

  • Palme R, Fischer P, Schildorfer H, Ismail MN (1996) Excretion of infused C-14-steroid hormones via faeces and urine in domestic livestock. Anim Reprod Sci 43:43–63

    Article  CAS  Google Scholar 

  • Palme R, Wetscher F, Winckler C (2003) Measuring faecal cortisol metabolites: a noninvasive tool to assess animal welfare in cattle? In: Proceedings of the IVth Central European Buiatric Congress, Lovran, pp 145–150

  • Rensel MA, Schoech SJ (2011) Repeatability of baseline and stress-induced corticosterone levels across early life stages in the Florida scrub-jay (Aphelocoma coerulescens). Horm Behav 59:497–502

    Article  PubMed  CAS  Google Scholar 

  • Rouff JH, Sussman RW, Strube MJ (2005) Personality traits in captive lion-tailed macaques (Macaca silenus). Am J Primatol 67:177–198

    Article  PubMed  Google Scholar 

  • Schmid J, Heistermann M, Ganslosser U, Hodges JK (2001) Introduction of foreign female Asian elephants (Elephas maximus) into an existing group: behavioural reactions and changes in cortisol levels. Anim Welf 10:357–372

    Google Scholar 

  • Sheriff M, Dantzer B, Delehanty B, Palme R, Boonstra R (2011) Measuring stress in wildlife: techniques for quantifying glucocorticoids. Oecologia 166:869–887

    Article  PubMed  Google Scholar 

  • Stead SK, Meltzer DGA, Palme R (2000) The measurement of glucocorticoid concentrations in the serum and faeces of captive African elephants (Loxodonta africana) after ACTH stimulation. J S Afr Vet Assoc 71:192–196

    PubMed  CAS  Google Scholar 

  • Szdzuy K, Dehnhard M, Strauss G, Eulenberger K, Hofer H (2006) Behavioural and endocrinological parameters of female African and Asian elephants Loxodonta africana and Elephas maximus in the peripartal period. Int Zoo Yearb 40:41–50

    Article  Google Scholar 

  • Touma C, Palme R (2005) Measuring fecal glucocorticoid metabolites in mammals and birds: the importance of validation. Ann N Y Acad Sci 1046:54–74

    Article  PubMed  CAS  Google Scholar 

  • Viljoen JJ, Ganswindt A, du Toit JT, Langbauer WR (2008) Translocation stress and faecal glucocorticoid metabolite levels in free-ranging African savanna elephants. S Afr J Wildl Res 38:146–152

    Article  Google Scholar 

  • Wasser SK, Papageorge S, Foley C, Brown JL (1996) Excretory fate of estradiol and progesterone in the African elephant (Loxodonata africana) and patterns of fecal steroid concentrations throughout the estrous cycle. Gen Comp Endocrinol 102:255–262

    Article  PubMed  CAS  Google Scholar 

  • Wasser SK, Hunt KE, Brown JL, Cooper K, Crockett CM, Bechert U, Millspaugh JJ, Larson S, Monfort SL (2000) A generalized fecal glucocorticoid assay for use in a diverse array of nondomestic mammalian and avian species. Gen Comp Endocrinol 120:260–275

    Article  PubMed  CAS  Google Scholar 

  • Watson R, Munro C, Edwards KL, Norton V, Brown JL, Walker SL (2013) Development of a versatile enzyme immunoassay for non-invasive assessment of glucocorticoid metabolites in a diversity of taxonomic species. Gen Comp Endocrinol 186:16–24

    Google Scholar 

  • Weiss M, Oddie CJ, McCance I (1979) Effects of ACTH on adrenal steroidogenesis and blood corticosteroid levels in the echidna (Tachyglossus aculeatus). Comp Biochem Physiol Part B Biochem Mol Biol 64:65–70

    Article  CAS  Google Scholar 

  • Whitham JC, Wielebnowski N (2009) Animal-based welfare monitoring: using keeper ratings as an assessment tool. Zoo Biol 28:545–560

    PubMed  Google Scholar 

  • Wielebnowski NC, Fletchall N, Carlstead K, Busso JM, Brown JL (2002) Noninvasive assessment of adrenal activity associated with husbandry and behavioral factors in the North American clouded leopard population. Zoo Biol 21:77–98

    Article  Google Scholar 

  • Ziegler TE, Sholl SA, Scheffler G, Haggerty MA, Lasley BL (1989) Excretion of estrone, estradiol, and progesterone in the urine and feces of the female cotton-top tamarin (Saguinus oedipus oedipus). Am J Primatol 17:185–195

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank all of the elephant keepers and staff at Melbourne Zoo, Taronga Zoo, and the Cocos (Keeling) Islands for their valued contributions to sample collection, survey completion, and assistance with the project. Thanks to Dr. Nadja Wielebnowski for helpful comments on the manuscript and to Heidi Kolkert for sample preparation.

Author information

Authors and Affiliations

  1. Wildlife Reproductive Centre, Taronga Western Plains Zoo, Dubbo, NSW, 2830, Australia

    Kerry V. Fanson & Tamara Keeley

  2. School of Life and Environmental Sciences, Deakin University, Geelong, VIC, 3216, Australia

    Kerry V. Fanson

  3. Veterinary Department, Melbourne Zoo, Melbourne, VIC, 3052, Australia

    Michael Lynch

  4. Taronga Wildlife Hospital & Elephant Division, Taronga Zoo, Sydney, NSW, 2088, Australia

    Larry Vogelnest & Gary Miller

Authors
  1. Kerry V. Fanson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michael Lynch
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Larry Vogelnest
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gary Miller
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tamara Keeley
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kerry V. Fanson.

Additional information

Communicated by Dr. Christian Gortázar

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 445 kb)

ESM 2

(PDF 394 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fanson, K.V., Lynch, M., Vogelnest, L. et al. Response to long-distance relocation in Asian elephants (Elephas maximus): monitoring adrenocortical activity via serum, urine, and feces. Eur J Wildl Res 59, 655–664 (2013). https://doi.org/10.1007/s10344-013-0718-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10344-013-0718-7

Keywords

Search

Navigation