Skip to main content Accessibility help
×
Hostname: page-component-77c89778f8-cnmwb Total loading time: 0 Render date: 2024-07-20T05:22:12.649Z Has data issue: false hasContentIssue false

10 - Non-invasive endocrine measures of reproduction and stress in wild populations

Published online by Cambridge University Press:  21 January 2010

Steven L. Monfort
Affiliation:
Conservation & Research Center, National Zoological Park, Smithsonian Institution, Front Royal, VA 22630 and Washington, DC 20008, U.S.A.
William V. Holt
Affiliation:
Zoological Society of London
Amanda R. Pickard
Affiliation:
Zoological Society of London
John C. Rodger
Affiliation:
Marsupial CRC, New South Wales
David E. Wildt
Affiliation:
Smithsonian National Zoological Park, Washington DC
Get access

Summary

INTRODUCTION AND OBJECTIVE

The evaluation of steroid metabolite content and/or profiles in either urine or faeces represents a snapshot of hormone activity and permits the long-term study of reproductive patterns in individuals, populations or species, all without perturbing the animal. By the mid-1980s, non-invasive immunoassay analysis of urine, which was pioneered in captive non-human primates (Hodges et al., 1979), had been adopted for the ex situ reproductive study of diverse primate, ungulate and avian species. Steroid monitoring in faeces was first described in the human (Adlercreutz & Martin, 1976) and then applied to the domestic mare (Bamberg et al., 1984) and cow (Möstl et al., 1984), before being used in the first non-domesticated species, the macaque (Risler et al., 1987). The non-invasive measurement of adrenal hormone metabolites was first accomplished in the bighorn sheep (Miller et al., 1991). These technological breakthroughs have revolutionised wildlife endocrinology.

Similar strategies using either urine or faeces also have application to free-living wildlife. The first study was reported in 1984 and investigated musth in male African elephants (Poole et al., 1984). Shortly thereafter, followed a study of female vervet monkeys (Andelman et al., 1985). Since then, more than 50 publications (Table 10.1) have described non-invasive endocrine monitoring of free-living mammals and birds. These studies have assessed longitudinal reproductive patterns (including seasonality, ovarian cyclicity and pregnancy), but more often have evaluated fecundity or hormonal relationships in ‘social’ species.

Type
Chapter
Information
Publisher: Cambridge University Press
Print publication year: 2002

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adlercreutz, H. & Martin, F. (1976). Oestrogen in human pregnancy faeces. Acta Endocrinologica 83, 410–419Google ScholarPubMed
Albuquerque, A. C. S. R., Sousa, M. B. C., Santos, H. M. & Ziegler, T. E. (2001). Behavioral and hormonal analysis of social relationships between oldest females in a wild monogamous group of common marmosets (Callithrix jacchus). International Journal of Primatology 22, 631–645CrossRefGoogle Scholar
Andelman, S. J., Else, J. G., Hearn, J. P. & Hodges, J. K. (1985). The non-invasive monitoring of reproductive events in wild vervet monkeys (Cercopithecus aethiops) using urinary pregnanediol glucuronide and its correlation with behavioural observation. Journal of Zoology (London) 205, 467–477CrossRefGoogle Scholar
Bamberg, E., Choi, H. S., Möstl, E., Wurm, W., Lorin, D. & Arbeiter, K. (1984). Enzymatic determination of unconjugated oestrogens in faeces for pregnancy diagnosis in mares. Equine Veterinary Journal 16, 537–539CrossRefGoogle ScholarPubMed
Berger, J., Testa, J. W., Roffe, T. & Monfort, S. L. (1999). Conservation endocrinology: a non-invasive tool to understand relationships between carnivore colonization and ecological carrying capacity. Conservation Biology 13, 980–989CrossRefGoogle Scholar
Borjesson, D., Boyce, W. B., Gardner, I. A., DeForge, J. & Lasley, B. (1996). Pregnancy detection in bighorn sheep (Ovis canadensis) using a fecal-based enzyme immunoassay. Journal of Wildlife Diseases 32, 67–74CrossRefGoogle ScholarPubMed
Brockman, D. K. & Whitten, P. L. (1996). Reproduction in free-ranging Propithecus verreauxi: estrus and the relationship between multiple partner matings and fertilization. American Journal of Physical Anthropology 100, 57–693.0.CO;2-A>CrossRefGoogle ScholarPubMed
Brockman, D. K., Whitten, P. L., Richard, A. F. & Schneider, A. (1998). Reproduction in free-ranging male Propithecus verreauxi: the hormonal correlates of mating and aggression. American Journal of Physical Anthropology 105, 137–1513.0.CO;2-S>CrossRefGoogle ScholarPubMed
Brown, J. L., Wasser, S. K., Wildt, D. E. & Graham, L. H. (1994). Measurement of fecal estrogen and progesterone metabolites for assessing ovarian activity in felids. Biology of Reproduction 51, 776–786CrossRefGoogle Scholar
Burrows, R., Hofer, H. & East, M. (1994). Demography, extinction and intervention in a small population: the case of the Serengeti wild dogs. Proceedings of the Royal Society of London B 256, 281–292CrossRefGoogle Scholar
Clarke, M. R., Zucker, E. L. & Harrison, R. M. (1991). Fecal estradiol, sexual swellings and sociosexual behavior in free-ranging howler monkeys in Costa Rica. American Journal of Primatology 24, 93Google Scholar
Clutton-Brock, T. H., Brotherton, P. N. M., Russell, A. F., O'Riain, M. J., Gaynor, D., Kansky, R., Griffin, A., Manser, M., Sharpe, L., McIlrath, G. M., Small, T., Moss, A. & Monfort, S. (2001). Cooperation, control and concession in Meerkat groups. Science 291, 478–481CrossRefGoogle ScholarPubMed
Cockrem, J. F. & Rounce, J. R. (1995). Non-invasive assessment of the annual gonadal cycle in free-living Kakapo (Strigops habroptilus) using fecal steroid measurements. Auk 112, 253–257CrossRefGoogle Scholar
Creel, S., Creel, N. M., Mills, M. G. L. & Monfort, S. L. (1997b). Rank and reproduction in co-operatively breeding African wild dogs: behavioral and endocrine correlates. Behavioral Ecology 8, 298–306CrossRefGoogle Scholar
Creel, S., Creel, N. M. & Monfort, S. L. (1997a). Radiocollaring African wild dogs (Lycaon pictus) does not cause chronic stress. Conservation Biology 11, 544–548CrossRefGoogle Scholar
Creel, S., Creel, N., Wildt, D. E. & Monfort, S. L. (1992). Behavioural and endocrine mechanisms of reproductive suppression in Serengeti dwarf mongooses. Animal Behaviour 43, 231–245CrossRefGoogle Scholar
Creel, S., Marusha-Creel, N. & Monfort, S. L. (1998). Birth order, estrogens and sex-ratio adaptation in African wild dogs (Lycaon pictus). Animal Reproduction Science 53, 315–320CrossRefGoogle Scholar
Creel, S., Monfort, S. L., Marusha-Creel, N., Wildt, D. E. & Waser, P. M. (1995). Pregnancy, oestrogens and future reproductive success in Serengeti dwarf mongooses. Animal Behaviour 50, 1132–1135CrossRefGoogle Scholar
Creel, S. R., Monfort, S. L., Wildt, D. E. & Waser, P. M. (1991). Spontaneous lactation is an adaptive result of pseudopregnancy. Nature 351, 660–662CrossRefGoogle ScholarPubMed
Creel, S. R., Wildt, D. E. & Monfort, S. L. (1993). Aggression, reproduction and androgens in wild dwarf mongooses: a test of the challenge hypothesis. American Naturalist 141, 816–825CrossRefGoogle ScholarPubMed
Curtis, D. J., Zaramody, A., Green, D. I. & Pickard, A. R. (2000). Non-invasive monitoring of reproductive status in wild mongoose lemurs (Eulemur mongoz). Reproduction, Fertility and Development 12, 21–29CrossRefGoogle Scholar
Czekala, N. M. & Sicotte, P. (2000). Reproductive monitoring of free-ranging female mountain gorillas by urinary hormone analysis. American Journal of Primatology 51, 209–2153.0.CO;2-6>CrossRefGoogle ScholarPubMed
Foley, C. A. H., Papageorge, S. & Wasser, S. K. (2001). Non-invasive stress and reproductive measures of social and ecological pressures in free-ranging African elephants. Conservation Biology 15, 134–142CrossRefGoogle Scholar
Garnier, J. N., Green, D. I., Pickard, A. R., Shaw, H. J. & Holt, W. V. (1998). Non-invasive diagnosis of pregnancy in wild black rhinoceros (Diceros bicornis minor) by faecal steroid analysis. Reproduction, Fertility and Development 10, 451–458CrossRefGoogle Scholar
Garrott, R. A., Monfort, S. L., Mashburn, K. L., White, P. J. & Cook, J. G. (1998). One-sample pregnancy diagnosis in elk using fecal steroid metabolites. Journal of Wildlife Diseases 34, 126–131CrossRefGoogle ScholarPubMed
Goymann, W., Möstl, E., Van't Hof, T., East, M. L. & Hofer, H. (1999). Non-invasive fecal monitoring of glucocorticoids in spotted hyaenas, Crocuta crocuta. General and Comparative Endocrinology 114, 340–348CrossRefGoogle Scholar
Herrick, J. R., Agoramoorthy, G., Rasanayagam, R. & Harder, J. D. (2000). Urinary progesterone in free-ranging red howler monkeys (Alouatta seniculus): preliminary observations of the estrous cycle and gestation. American Journal of Primatology 51, 257–2633.0.CO;2-6>CrossRefGoogle ScholarPubMed
Hirschenhauser, K., Möstl, E. & Kotrschal, K. (1999). Seasonal patterns of sex steroids determined from feces in different social categories of greylag geese (Anser anser). General and Comparative Endocrinology 114, 67–79CrossRefGoogle Scholar
Hodges, J. K., Czekala, N. M. & Lasley, B. L. (1979). Estrogen and luteinizing hormone secretion in diverse primate species from simplified urinary analysis. Journal of Medical Primatology 8, 349–364CrossRefGoogle ScholarPubMed
Kirkpatrick, J. F., Bancroft, K. & Kincy, V. (1992b). Pregnancy and ovulation detection in bison (Bison bison) assessed by means of urinary and fecal steroids. Journal of Wildlife Diseases 28, 590–597CrossRefGoogle Scholar
Kirkpatrick, J. F., Gudermuth, D. F., Flagan, R. L., McCarthy, J. C. & Lasley, B. L. (1993a). Remote monitoring of ovulation and pregnancy of Yellowstone bison. Journal of Wildlife Management 57, 407–412CrossRefGoogle Scholar
Kirkpatrick, J. F., Kincy, V., Bancroft, K., Shideler, S. E. & Lasley, B. L. (1991b). Oestrous cycle of the North American bison (Bison bison) characterised by urinary pregnanediol-3-glucuronide. Journal of Reproduction and Fertility 93, 541–547CrossRefGoogle Scholar
Kirkpatrick, J. F., Lasley, B. L., Shideler, S. E., Roser, J. F. & Turner, J. W. (1993b). Non-instrumented immunoassay field tests for pregnancy detection in free-roaming feral horses. Journal of Wildlife Management 57, 168–173CrossRefGoogle Scholar
Kirkpatrick, J. F., Liu, I. K. M., Turner, J. W., Naugle, R. & Keiper, R. (1992a). Long-term effects of porcine zonae pellucidae immunocontraception on ovarian function in feral horses (Equus caballus). Journal of Reproduction and Fertility 94, 437–444CrossRefGoogle Scholar
Kirkpatrick, J. F., McCarthy, J. C., Gudermuth, D. F., Shideler, S. E. & Lasley, B. L. (1996). An assessment of the reproductive biology of Yellowstone bison (Bison bison) subpopulations using non-capture methods. Canadian Journal of Zoology 74, 8–14CrossRefGoogle Scholar
Kirkpatrick, J. F., Naugle, R., Liu, I. K. M., Bernoco, M. & Turner, J. W. (1995). Effects of seven consecutive years of porcine zona pellucida contraception on ovarian function in feral mares. Biology of Reproduction Monographs 1, 411–418Google Scholar
Kirkpatrick, J. F., Shideler, S. E., Lasley, B. L. & Turner, J. W. (1991a). Pregnancy determination in uncaptured feral horses by means of fecal steroid conjugates. Theriogenology 35, 753–759CrossRefGoogle Scholar
Kirkpatrick, J. F., Shideler, S. E. & Turner, J. W. (1990). Pregnancy determination in uncaptured feral horses based on free steroids in feces and steroid metabolites in urine-soaked snow. Canadian Journal of Zoology 68, 2576–2579CrossRefGoogle Scholar
Knott, C. D. (1993). Monitoring of hormonal profiles of free-ranging chimpanzees (Pan troglodytes) and orangutans (Pongo pygmaeus). Bulletin of the Ecological Society of America, Suppl. 74, 314Google Scholar
Kofuji, H., Kanda, M. & Oishi, T. (1993). Breeding cycles and fecal gonadal steroids in the Brown Dipper (Cinclus pallasii). General and Comparative Endocrinology 91, 216–223CrossRefGoogle Scholar
Kotrschal, K., Hirschenhauser, K. & Möstl, E. (1998). The relationship between social stress and dominance is seasonal in greylag geese. Animal Behaviour 55, 171–176CrossRefGoogle ScholarPubMed
Lasley, B. L. & Kirkpatrick, J. F. (1991). Monitoring ovarian function in captive and free-ranging wildlife by means of urinary and fecal steroids. Journal of Zoo Wildlife Medicine 22, 23–31Google Scholar
Miller, M. W., Hobbs, N. T. & Sousa, M. C. (1991). Detecting stress responses in Rocky Mountain bighorn sheep (Ovis canadensis canadensis): reliability of cortisol concentrations in urine and feces. Canadian Journal of Zoology 69, 15–24CrossRefGoogle Scholar
Millspaugh, J. J. (1999). Behavioral and physiological responses of elk to human disturbances in the southern Black Hills, South Dakota. Doctoral dissertation, University of Washington, Seattle, WA
Monfort, S. L., Arthur, N. P. & Wildt, D. E. (1991). Monitoring ovarian function and pregnancy by evaluating excretion of urinary oestrogen conjugates in semi-free-ranging Przewalski's horses (Equus przewalskii). Journal of Reproduction and Fertility 91, 155–164CrossRefGoogle Scholar
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. Journal of Zoo and Wildlife Medicine 29, 129–133Google ScholarPubMed
Monfort, S. L., Schwartz, C. C. & Wasser, S. K. (1993). Monitoring reproduction in captive moose using urinary and fecal steroid metabolites. Journal of Wildlife Management, 57, 400–407CrossRefGoogle Scholar
Monfort, S. L., Wasser, S. K., Mashburn, K. L., Burke, M., Brewer, B. A. & Creel, S. R. (1997). Steroid metabolism and validation of non invasive endocrine monitoring in the African wild dog (Lycaon pictus). Zoo Biology 16, 533–5483.0.CO;2-B>CrossRefGoogle Scholar
Morrow, C. J. & Monfort, S. L. (1998). Ovarian activity in the scimitar-horned oryx (Oryx dammah) determined by faecal steroid analysis. Animal Reproduction Science 53, 191–207CrossRefGoogle ScholarPubMed
Möstl, E., Choi, H. S., Wurm, W., Ismail, N. & Bamberg, E. (1984). Pregnancy diagnosis in cows and heifers by determination of oestradiol-17α in faeces. British Veterinary Journal 140, 287–291CrossRefGoogle Scholar
Niswender, G. D., Akbar, A. M. & Nett, T. M. (1975). Use of specific antibodies for quantification of steroid hormones. In Methods in Enzymology (Eds. B. W. O'Malley & J. G. Hardman), pp. 119–142. Academic Press, New YorkCrossRef
Palme, R., Robia, C., Messmann, S. & Möstl, E. (1998). Measuring faecal cortisol metabolites: a non-invasive tool to evaluate adrenocortical activity in mammals. Proceedings of the 2nd International Symposium of Physiology and Ethology of Wild and Zoo Animals, Berlin, Germany. Advances in Ethology 33, 27
Poole, J. H., Kasman, L. H., Ramsay, E. C. & Lasley, B. L. (1984). Musth and urinary testosterone in the African elephant (Loxodonta africana). Journal of Reproduction and Fertility 70, 255–290CrossRefGoogle Scholar
Reimers, T. J., Cowan, B. A., Davidson, H. P. & Colby, E. D. (1981). Validation of radioimmunoassays for triiodothyronine, thyroxine, and hydrocortisone (cortisol) in canine, feline, and equine sera. American Journal of Veterinary Research 42, 2016–2021Google ScholarPubMed
Risler, L., Wasser, S. K. & Sackett, G. P. (1987). Measurement of excreted steroids in Macaca nemestrina. American Journal of Primatology 12, 91–100CrossRefGoogle Scholar
Robbins, M. M. & Czekala, N. M. (1997). A preliminary investigation of urinary testosterone and cortisol levels in wild male mountain gorillas. American Journal of Primatology 43, 51–643.0.CO;2-X>CrossRefGoogle ScholarPubMed
Savage, A., Shideler, S. E., Soto, L. H., Causado, J., Giraldo, L. H., Lasley, B. L. & Snowdon, C. T. (1997). Reproductive events of wild cotton-top tamarins (S. oedipus) in Colombia. American Journal of Primatology 43, 329–3373.0.CO;2-Z>CrossRefGoogle Scholar
Schwartz, C. C., Monfort, S. L., Dennis, P. & Hundertmark, K. J. (1995). Fecal progesterone concentration as an indicator of the estrous cycle and pregnancy in moose. Journal of Wildlife Management 59, 580–583CrossRefGoogle Scholar
Stavisky, R. C., Russell, E., Stallings, J., Smith, E. O., Worthman, C. M. & Whitten, P. L. (1995). Fecal steroid analysis of ovarian cycles in free-ranging baboons. American Journal of Primatology 36, 285–297CrossRefGoogle Scholar
Stoops, M. A., Anderson, G. B., Lasley, B. L. & Shideler, S. E. (1999). Estimating the reproductive potential in a free-ranging herd of elk. Journal of Wildlife Management 63, 561–569CrossRefGoogle Scholar
Strier, K. B. & Ziegler, T. E. (1994). Insights into ovarian function in wild muriqui monkeys (Brachyteles arachnoides). American Journal of Primatology 32, 31–40CrossRefGoogle Scholar
Strier, K. B. & Ziegler, T. E. (1997). Behavioral and endocrine characteristics of the reproductive cycle in wild muriqui monkeys, Brachyteles arachnoides. American Journal of Primatology 42, 299–3103.0.CO;2-S>CrossRefGoogle ScholarPubMed
Strier, K. A., Ziegler, T. E. & Wittwer, D. J. (1999). Seasonal and social correlates of fecal testosterone and cortisol levels in wild male muriquis (Brachyteles arachnoides). Hormones and Behavior 35, 125–134CrossRefGoogle Scholar
Taussky, H. H. (1954). A microcolorimetric determination of creatine in urine by the Jaffe reaction. Journal of Biological Chemistry 208, 853–861Google ScholarPubMed
Thierry, B., Heistermann, M., Aujard, F. & Hodges, J. K. (1996). Long-term data on basic reproductive parameters and evaluation of endocrine, morphological, and behavioral measures for monitoring reproductive status in a group of semifree-ranging Tonkean macaques (Macaca tonkeana). American Journal of Primatology 39, 47–623.0.CO;2-S>CrossRefGoogle Scholar
Schaik, C. P., Noordwijk, M. A., Bragt, T. & Blakenstein, M. A. (1991). A pilot study of the social correlates of levels of urinary cortisol, prolactin, and testosterone in wild long-tailed macaques (Macaca fascicularis). Primates 32, 345–356CrossRefGoogle Scholar
Wallner, B., Möstl, E., Dittami, J. & Prossinger, H. (1999). Fecal glucocorticoids document stress in female Barbary macaques (Macaca sylvanus). General and Comparative Endocrinology 113, 80–86CrossRefGoogle Scholar
Wasser, S. K. (1996). Reproductive control in wild baboons measured by fecal steroids. Biology of Reproduction 55, 393–399CrossRefGoogle ScholarPubMed
Wasser, S. K., Bevis, K., King, G. & Hanson, E. (1997). Noninvasive physiological measures of disturbance in the Northern spotted owl. Conservation Biology 11, 1019–1022CrossRefGoogle Scholar
Wasser, S. K., Hunt, K. E., Brown, J. L., Crockett, C., Bechert, U., Millspaugh, J., Larson, S. & Monfort, S. L. (2001). A generalized fecal glucocorticoid assay for use in a diverse array of non-domestic mammalian and avian species. General and Comparative Endocrinology 120, 260–275CrossRefGoogle Scholar
Wasser, S. K., Monfort, S. L., Southers, J. & Wildt, D. E. (1994). Excretion rates and metabolites of oestradiol and progesterone in baboon (Papio cynocephalus cynocephalus). Journal of Reproduction and Fertility 101, 213–220CrossRefGoogle Scholar
Wasser, S. K., Monfort, S. L. & Wildt, D. E. (1991). Rapid extraction of steroids for measuring reproductive cyclicity and early pregnancy in free-ranging yellow baboons (Papio cynocephalus cynocephalus). Journal of Reproduction and Fertility 92, 415–423CrossRefGoogle Scholar
Wasser, S. K., Papageorge, S., Foley, C. & Brown, J. L. (1996). Excretory fate of estradiol and progesterone in the African elephant (Loxodonta africana) and pattern of fecal steroid concentrations throughout the estrous cycle. General and Comparative Endocrinology, 102, 255–262CrossRefGoogle Scholar
White, P. J., Garrott, R. A., Kirkpatrick, J. F. & Berkeley, E. V. (1995). Diagnosing pregnancy in free-ranging elk using fecal steroid metabolites. Journal of Wildlife Diseases 31, 514–522CrossRefGoogle ScholarPubMed
Whitten, P. J., Brockman, D. K. & Stavisky, R. C. (1998). Recent advances in non-invasive techniques to monitor hormone-behavior interactions. American Journal of Physical Anthropology, Suppl. 27, 1–233.0.CO;2-H>CrossRefGoogle Scholar
Ziegler, T., Hodges, K., Winkler, P. & Heistermann, M. (2000). Hormonal correlates of reproductive seasonality in wild female hanuman langurs (Presbytis entellus). American Journal of Primatology 51, 119–1343.0.CO;2-O>CrossRefGoogle Scholar
Ziegler, T. E., Santos, C. V., Pissinatti, A. & Strier, K. B. (1997a). Steroid excretion during the ovarian cycle in captive and wild muriquis, Brachyteles aracnoides. American Journal of Primatology 42, 311–3213.0.CO;2-#>CrossRefGoogle Scholar
Ziegler, T. E., Scheffler, G. & Carlson, A. A. (1997b). Methods and use of fecal steroid analyses for monitoring reproductive functioning in marmosets and tamarins. Acta Primatologia 6, 269–280Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×