Non-invasive monitoring of adrenocortical activity in European badgers (Meles meles) and effects of sample collection and storage on faecal cortisol metabolite concentrations

Animal Biology

Volumn 62, Issue 4, 2012, Pages 419-432

  Barja, Isabel ^a   Escribano Ávila, Gema ^b   Lara Romero, Carlos ^b   Virgós, Emilio ^b   Benito, Javier ^c   Rafart, Elena ^d  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b UNIVERSIDAD REY JUAN CARLOS   (Spain)

^c NORTH CAROLINA STATE UNIVERSITY   (United States)

^d UNIVERSITY OF BARCELONA   (Spain)

Author keywords

ACTH challenge; enzyme immunoassay; European badger; faecal cortisol metabolites; sample collection; sample storage

Indexed keywords

FECAL PELLET; HORMONE; IMMUNOASSAY; METABOLITE; MONITORING; MUSTELID; RELATIVE HUMIDITY; WILD POPULATION;

EID: 84874857390     PISSN: 15707555     EISSN: 15707563     Source Type: Journal    
DOI: 10.1163/157075612X642914     Document Type: Article

References (54)

1. Abáigar, T., Domene, M.A. & Palomares, F. (2010) Effects of fecal age and seasonality on steroid hormone concentration as a reproductive parameter in field studies. Eur. J. Wildl. Res., 56, 781-787.
2. Axelrod, J. & Reisine, T.D. (1984) Stress hormones: their interaction and regulation. Science, 224, 452-459.
3. Barja, I., Silván, G., Rosellini, S., Piñeiro, A., Martínez, M.M., Illera, M. & Illera, J.C. (2006) Influence of reproductive state and human disturbances on fecal glucocorticoid concentrations in wild population of Iberian wolves. Reprod. Domest. Anim., 41, 377.
4. Barja, I., Silván, G., Rosellini, S., Piñeiro, A., González-Gil, A., Camacho, L. & Illera, J.C. (2007) Stress physiological responses to tourist pressure in a wild population of European pine marten. J. Steroid. Biochem. Mol. Biol., 104, 136-142.
5. Barja, I., Silván, G. & Illera, J.C. (2008) Relationships between sex and stress hormone levels in feces and marking behavior in a wild population of Iberian wolves (Canis lupus signatus). J. Chem. Ecol., 34, 697-701.
6. Barja, I., Silván, G., Martínez-Fernández, L. & Illera, J.C. (2011) Physiological stress responses, faecal marking behaviour, and reproduction in wild European pine martens (Martes martes). J. Chem. Ecol., 37, 253-259.
7. Boonstra, R. (2005) Equiped for life: the adaptative role of the stress axis in male mammals. J. Mammal., 86, 236-247.
8. Boonstra, R., Hik, D., Singleton, G.R. & Tinnikov, A. (1998) The impact of predator-induced stress on the snowshoe hare cycle. Ecol. Monogr., 79, 371-394.
9. Brown, J.L., Wasser, S.K., Wildt, D.E. & Graham, L.H. (1994) Comparative aspects of steroid hormone metabolism and ovarian activity in felids, measured noninvasively in feces. Biol. Reprod., 51, 776-786.
10. Cockrem, J.F. & Rounce, R.R. (1994) Faecal measurements of oestradiol and testosterone allow the non-invasive estimation of plasma steroid concentrations in the domestic fowl. Br. Poult. Sci., 35, 433.
11. Creel, S., Fox, J.E., Hardy, A., Sands, J., Garrott, B. & Peterson, R.O. (2002) Snowmobile activity and glucocorticoid stress responses in wolves and elk. Conserv. Biol., 16, 809-814.
12. Dehnhard, M., Clauss, M., Lechner-Doll, M., Meyer, H.H.D. & Palme, R. (2001) Noninvasive monitoring of adrenocortical activity in roe deer (Capreolus capreolus) by measurement of faecal cortisol metabolites. Gen. Comp. Endocr., 123, 111-120.
13. Foley, C.A., Papageorge, S. & Wasser, S.K. (2001) Noninvasive stress and reproductive measures of social and ecological pressures in free-ranging African elephants. Conserv. Biol., 15, 1134-1142.
14. Frigerio, D., Dittami, J., Möstl, E. & Kotrschal, K. (2004) Excreted corticosterone metabolites covary with ambient temperature and air pressure in male Greylag geese (Anser anser). Gen. Comp. Endocr., 137, 29-36.
15. Goymann, W., Möstl, E., Van't Hof, T., East, M.L. & Hofer, H. (1999) Noninvasive fecal monitoring of glucocorticoids in spotted hyaenas (Crocuta crocuta). Gen. Comp. Endocr., 114, 340-348.
16. Goymann,W., East, M.L.,Wachter, B., Höner, O.P., Möstl, E., Van't Hof, T.J. & Hofer, H. (2001) Social, state-dependent and environmental modulation of faecal corticosteroid levels in free-ranging female spotted hyenas. Proc. R. Soc. Lond. B, 268, 2453-2459.
17. Graham, L.H. & Brown, J.L. (1996) Cortisol metabolism in the domestic cat and implications for non-invasive monitoring of adrenocortical function in endangered felids. Zoo Biol., 15, 71-82.
18. Harper, J.M. & Austad, S.N. (2000) Fecal glucocorticoids: a noninvasive method of measuring adrenal activity in wild and captive rodents. Physiol. Biochem. Zool., 73, 12-22.
19. Herring, G. & Gawlik, D.E. (2009) Stability of avian corticosterone metabolite levels in frozen avian feces. J. Wildlife Manage., 73, 1010-1013.
20. Jewgenow, K., Naidenko, S.V., Goeritz, F., Vargas, A. & Dehnhard, M. (2006) Monitoring testicular activity of male Eurasian (Lynx lynx) and Iberian (Lynx pardinus) lynx by fecal testosterone metabolite measurement. Gen. Comp. Endocr., 149, 151-158.
21. Khan, M.Z., Altmann, J., Isani, S.S. & Yu, J. (2002) A matter of time: evaluating the storage of fecal samples for steroid analysis. Gen. Comp. Endocr., 128, 57-64.
22. Little, R.C., Freund, R.J. & Spector, P.C. (1992) SAS Linear Systems for General Models. SAS Institute, Cary, North Carolina.
23. Lochmiller, R.L. & Deerenberg, C. (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos, 88, 87-98.
24. Mashburn, K.L. & Atkinson, S. (2004) Evaluation of adrenal function in serum and feces of Steller sea lions (Eumetopias jubatus): influences of molt, gender, sample storage, and age on glucocorticoid metabolism. Gen. Comp. Endocr., 136, 371-381.
25. Millspaugh, J.J., Woods, R.J., Hunt, K.E., Raedeke, K.J., Brundige, G.C., Washburn, B.E. & Wasser, S.K. (2001) Fecal glucocorticoid assays and the physiological stress response of elk. Wildlife Soc. Bull., 29, 899-907.
26. Millspaugh, J.J. & Warhburn, B.E. (2003) Within-sample variation of fecal glucocorticoid measurements. Gen. Comp. Endocr., 132, 21-26.
27. Millspaugh, J.J. & Warhburn, B.E. (2004) Use of fecal glucocorticoid metabolite measures in conservation biology research: considerations for application and interpretation. Gen. Comp. Endocr., 138, 189-199.
28. Monfort, S.L., Brown, J.L. & Wildt, D.E. (1993) Episodic and seasonal rhythms of cortisol secretion in male Eld's deer (Cervus eldi thamin). J. Endocrinol., 138, 41-49.
29. Monfort, S.L., Mashburn, K.L., Brewer, B.A. & Creel, S.R. (1998) Evaluating adrenal activity in African wild dogs (Lycaon pictus) by fecal corticosteroid analysis. J. Zoo Wildl. Med., 29, 129-133.
30. Neal, C.G. & Cheeseman, C.L. (1991) Badger. In: G.B. Corbet & S. Harris (Eds.) The Handbook of British Mammals, pp. 415-423. Blackweil Scientific Publications, Oxford.
31. Ohe von der, C.G., Wasser, S.K., Hunt, K.E. & Servheen, C. (2004) Factors associated with fecal glucocorticoids in Alaskan brown bears (Ursus arctos horribilis). Physiol. Biochem. Zool., 77, 313-320.
32. Palme, R. (2005) Measuring fecal steroids. Guidelines for practical application. Ann. NY Acad. Sci., 1046, 1-6.
33. Romero, L.M. & Reed, J.M. (2005) Collecting baseline corticosterone samples in the field: is under 3 min good enough? Comp. Biochem. Phys. A, 140, 73-79.
34. Sands, J. & Creel, S. (2004) Social dominance, aggression and faecal glucocorticoid levels in a wild population of wolves, Canis lupus. Anim. Behav., 67, 387-396.
35. Santymire, R.M. & Armstrong, D.M. (2010) Development of a field-friendly technique for fecal steroid extraction and storage using the African wild dog (Lycaon pictus). Zoo Biol., 29, 289-302.
36. Sapolsky, R.M. (1992) Neuroendocrinology of the stress response. In: J.B. Becker & S.M. Breedlove (Eds.) Behavioral Endocrinology, pp. 287-324. MIT Press, Cambridge.
37. Sapolsky, R.M., Romero, L.M. & Munck, A.U. (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev., 21, 55-89.
38. Schatz, S. & Palme, R. (2001) Measurement of faecal cortisol metabolites in cats and dogs: a noninvasive method for evaluating adrenocortical function. Vet. Res. Commun., 25, 271-287.
39. Schütz, K.E., Agren, E., Amundin, M., Röken, B., Palme, R. & Mörner, T. (2006) Behavioral and physiological responses of trap-induced stress in European badgers. J. Wildlife Manage., 70, 884-891.
40. Schwartz, M.K. & Monfort, S.L. (2008) Genetic and endocrine tools for carnivore surveys. In: R. Long, P. Mackay, J. Ray & W. Zielinski (Eds.) Non Invasive Survey Methods for Carnivores, pp. 238-262. Island Press, Washington, DC.
41. Sheriff, M.J., Dantzer, B., Delehanty, B., Palme, R.&Boonstra, R. (2011) Measuring stress in wildlife: techniques for quantifying glucocorticoids. Oecologia, 166, 869-887.
42. Shideler, S.E., Ortuño, A.M., Morán, F.M., Moorman, E.A. & Lasley, B.I. (1993) Simple extraction and enzyme immunoassays for estrogen and progesterone metabolites in the feces of Macaca fascicularis during non-conceptive and conceptive ovarian cycles. Biol. Reprod., 48, 1290-1298.
43. Silván, G., Barja, I., Rosellini, S., Piñeiro, A., Illera,M.J., Camacho, L. & Illera, J.C. (2006) Variations of sex reproductive hormones during the year in a wild population of European pine marten (Martes martes). Reprod. Domest. Anim., 41, 119.
44. Stewart, P.M. (2003) The adrenal cortex. In: P.R. Larsen, H.M. Kronenberg, S.Melmed & K.S. Polonsky (Eds.) Williams Textbook of Endocrinology, pp. 491-551. Saunders, Philadelphia.
45. Terio, K.A., Citino, S.B. & Brown, J.L. (1999) Fecal cortisol metabolite analysis for non invasive monitoring of adrenocortical function in the cheetah (Acinonyx jubatus). J. Zoo Wildl. Med., 30, 484-491.
46. Terlouw, E.M., Schouten,W.G.P. & Ladewig, J. (1997) Physiology. In:M.C. Appleby & B.O. Hughes (Eds.) Animal Welfare, pp. 143-158. CAB International, University Press, Cambridge.
47. Touma, C. & Palme, R. (2005) Measuring fecal glucocorticoid metabolites in mammals and birds: the importance of validation. Annals New York Acad. Sci., 1046, 54-74.
48. Van Meter, P.E., French, J.A., Dloniak, S.M., Watts, H.E., Kolowski, J.M. & Holekamp, K.E. (2009) Fecal glucocorticoids reflect socio-ecological and anthropogenic stressors in the lives of wild spotted hyenas. Horm. Behav., 55, 329-337.
49. Vargas, A., Sanchez, I.,Martinez, F., Rivas, A., Godoy, J.A., Roldán, E., Simón, M.A., Serra, R., Perez, M.J., Euseñat, C., Delibes, M., Aymerich, M., Sliwa, A. & Breitenmoser, V. (2008) The Iberian lynx Lynx pardinus conservation breeding program. The Developing Zoo World, 42, 190-198.
50. Wasser, S.K., Hunt, K.E., Brown, J.L., Cooper, K., Crockett, C.M., Bechert, U.,Millspaugh, J., Larson, J.S. & Monfort, S. (2000) A generalized fecal glucocorticoid assay for use in a diverse array of nondomestic mammalian and avian species. Gen. Comp. Endocr., 120, 260-275.
51. Wielebnowski, N. & Watters, J. (2007) Applying fecal endocrine monitoring to conservation and behavior studies of wild mammals: important considerations and preliminary tests. Israel J. Ecol. Evol., 53, 439-460.
52. Wikelski, M. & Cooke, S.J. (2006) Conservation physiology. Trends Ecol. Evol., 21, 38-46.
53. Wingfield, J.C. (2008) Comparative endocrinology, environment and global change. Gen. Comp. Endocr., 157, 207-216.
54. Young, K.M., Walker, S.L., Lanthier, C., Waddell, W.T., Monfort, S.L. & Brown, J.L. (2004) Noninvasive monitoring of adrenocortical activity in carnivores by fecal glucocorticoid analyses. Gen. Comp. Endocr., 137, 148-165.