Comparative endocrinology of testicular, adrenal and thyroid function in captive Asian and African elephant bulls

Brown, Janine L.; Somerville, Malia; Riddle, Heidi S.; Keele, Mike; Duer, Connie K.; Freeman, Elizabeth W.

doi:10.1016/j.ygcen.2007.01.006

Cited by 83Sperm and Testicular FunctionAnimal Behavior and Welfare StudiesAnimal Behavior and Reproduction

Comparative endocrinology of testicular, adrenal and thyroid function in captive Asian and African elephant bulls

Brown, Janine L., Somerville, Malia, Riddle, Heidi S., Keele, Mike, Duer, Connie K., Freeman, Elizabeth W.·2007·General and Comparative Endocrinology

DOI 10.1016/j.ygcen.2007.01.006

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Abstract

Concentrations of serum testosterone, cortisol, thyroxine (free and total T4), triiodothyronine (free and total T3) and thyroid stimulating hormone (TSH) were measured to assess adrenal and thyroid function as they relate to testicular activity and musth in captive elephants. Blood samples were collected approximately weekly from Asian (n=8) and African (n=12) bulls at seven facilities for periods of 4 months to 9.5 years. Age ranges at study onset were 8-50 years for Asian and 10-21 years for African elephants. Based on keeper logs, seven Asian and three African bulls exhibited behavioral and/or physical (temporal gland secretion, TGS, or urine dribbling, UD) signs of musth, which lasted 2.8+/-2.5 months in duration. Serum testosterone was elevated during musth, with concentrations often exceeding 100 ng/ml. Patterns of testosterone secretion and musth varied among bulls with no evidence of seasonality (P>0.05). Only three bulls at one facility exhibited classic, well-defined yearly musth cycles. Others exhibited more irregular cycles, with musth symptoms often occurring more than once a year. A number of bulls (1 Asian, 9 African) had consistently low testosterone (<10 ng/ml) and never exhibited significant TGS or UD. At facilities with multiple bulls (n=3), testosterone concentrations were highest in the oldest, most dominant male. There were positive correlations between testosterone and cortisol for six of seven Asian and all three African males that exhibited musth (range, r=0.23-0.52; P<0.05), but no significant correlations for bulls that did not (P>0.05). For the three bulls that exhibited yearly musth cycles, TSH was positively correlated (range, r=0.22-0.28; P<0.05) and thyroid hormones (T3, T4) were negatively correlated (range, r=-0.25 to -0.47; P<0.05) to testosterone secretion. In the remaining bulls, there were no clear relationships between thyroid activity and musth status. Overall mean testosterone and cortisol concentrations increased with age for all bulls combined, whereas thyroid activity declined. In summary, a number of bulls did not exhibit musth despite being of adequate physical maturity. Cortisol and testosterone were correlated in most bulls exhibiting musth, indicating a possible role for the adrenal gland in modulating or facilitating downstream responses. Data were generally inconclusive as to a role for thyroid hormones in male reproduction, but the finding of discrete patterns in bulls showing clear testosterone cycles suggests they may facilitate expression or control of musth in some individuals.

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Musth is associated with increased androgen production.
“and is associated with increased androgen production [60,61].”
From Socializing a group of male Asian elephants in a semi-captive facility in Lao PDR (2025) · cites this paper as [61]

The Thyroid Gland.
Ingbar, S. H. (1965) · Archives of Internal Medicine · doi:10.1001/archinte.1965.03870060154035 · Cited by 1,745 · see citing works
Encyclopedia of Reproduction
(2018) · Elsevier eBooks · doi:10.1016/c2015-1-06718-7 · Cited by 1,525 · see citing works
Thermogenic Mechanisms and Their Hormonal Regulation
Silva, J. E. (2006) · Physiological Reviews · doi:10.1152/physrev.00009.2005 · Cited by 687 · see citing works
The differences between the sexes
Colgan, P. W. (1995) · Behavioural Processes · doi:10.1016/0376-6357(95)90037-3 · Cited by 324 · see citing works
Announcing intent: the aggressive state of musth in African elephants
Poole, J. H. (1989) · Animal Behaviour · doi:10.1016/0003-3472(89)90014-6 · Cited by 240 · see citing works
Effects of endogenous testosterone and estradiol on sexual behavior in normal young men.
Bagatell, C. J., Heiman, J. R., Rivier, J., & Bremner, W. J. (1994) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.78.3.8126146 · Cited by 240 · see citing works
Biology, Medicine, and Surgery of Elephants
Fowler, M. E., & Mikota, S. K. (2006) · Wiley eBooks · doi:10.1002/9780470344484 · Cited by 237 · see citing works
Social dominance, aggression and faecal glucocorticoid levels in a wild population of wolves, Canis lupus
Sands, J. L., & Creel, S. (2004) · Animal Behaviour · doi:10.1016/j.anbehav.2003.03.019 · Cited by 235 · see citing works
The Differences between the Sexes
Short, R. V., & Balaban, E. (1994) · Medical Entomology and Zoology · Cited by 231 · see citing works
Non-invasive assessment of adrenocortical function in the male African elephant (Loxodonta africana) and its relation to musth
Ganswindt, A., Palme, R., Heistermann, M., Borragan, S., & Hodges, J. K. (2003) · General and Comparative Endocrinology · doi:10.1016/s0016-6480(03)00251-x · Cited by 213 · see citing works
The relationship between sexual and aggressive behaviour, and pituitary and testicular activity during the seasonal sexual cycle of rams, and the influence of photoperiod
Lincoln, G. A., & Davidson, W. G. (1977) · Reproduction · doi:10.1530/jrf.0.0490267 · Cited by 176 · see citing works
Effects of prolonged fasting on plasma cortisol and TH in postweaned northern elephant seal pups
Ortiz, R. M., Wade, C. E., & Ortiz, C. L. (2001) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.2001.280.3.r790 · Cited by 151 · see citing works
DOLPHIN THYROID AND ADRENAL HORMONES: CIRCULATING LEVELS IN WILD AND SEMIDOMESTICATED TURSIOPS TRUNCATUS, AND INFLUENCE OF SEX, AGE, AND SEASON
Aubin, D. J. S., Ridgway, S. H., Wells, R. S., & Rhinehart, H. L. (1996) · Marine Mammal Science · doi:10.1111/j.1748-7692.1996.tb00301.x · Cited by 142 · see citing works
Basic & Clinical Endocrinology
Melmed, S. K. (1985) · PubMed Central · Cited by 135 · see citing works
PLASMA TESTOSTERONE LEVELS IN RELATION TO MUSTH AND SEXUAL ACTIVITY IN THE MALE ASIATIC ELEPHANT, ELEPHAS MAXIMUS
Jainudeen, M. R., Katongole, C. B., & Short, R. V. (1972) · Reproduction · doi:10.1530/jrf.0.0290099 · Cited by 131 · see citing works
Basic & Clinical Endocrinology
Greenspan, F. S., & Strewler, G. J. (1990) · Medical Entomology and Zoology · Cited by 127 · see citing works
The sexually active states of free-ranging male African elephants (Loxodonta africana): defining musth and non-musth using endocrinology, physical signals, and behavior
Ganswindt, A., Rasmussen, H. B., Heistermann, M., & Hodges, J. K. (2005) · Hormones and Behavior · doi:10.1016/j.yhbeh.2004.09.002 · Cited by 115 · see citing works
Comparative endocrinology of cycling and non-cycling Asian (Elephas maximus) and African (Loxodonta africana) elephants
Brown, J. L., Walker, S. L., & Moeller, T. (2004) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2004.01.013 · Cited by 112 · see citing works
Self-citation
A comparison of the seasonal hormone changes and patterns of growth, voluntary food intake and reproduction in juvenile and adult red deer ( Cervus elaphus ) and Père David's deer ( Elaphurus davidianus ) hinds
Loudon, A. S. I., Milne, J. A., Curlewis, J. D., & McNeilly, A. S. (1989) · Journal of Endocrinology · doi:10.1677/joe.0.1220733 · Cited by 94 · see citing works
Testosterone and Dihydrotestosterone Concentrations in Elephant Serum and Temporal Gland Secretions
Rasmussen, L. E. L., Buss, I. O., Hess, D. L., & Schmidt, M. J. (1984) · Biology of Reproduction · doi:10.1095/biolreprod30.2.352 · Cited by 90 · see citing works
OBSERVATIONS ON MUSTH IN THE DOMESTICATED ASIATIC ELEPHANT (ELEPHAS MAXIMUS)
Jainudeen, M. R., McKay, G. M., & Eisenberg, J. F. (1972) · Mammalia · doi:10.1515/mamm.1972.36.2.247 · Cited by 85 · see citing works
A RELATIONSHIP BETWEEN PLASMA CONCENTRATIONS OF TESTOSTERONE AND CORTICOSTEROIDS DURING SEXUAL AND AGGRESSIVE BEHAVIOUR IN THE BOAR
Liptrap, R. M., & RAESIDE, J. I. (1978) · Journal of Endocrinology · doi:10.1677/joe.0.0760075 · Cited by 71 · see citing works
Cortisol, growth hormone, and testosterone concentrations during mating behavior in the bull and boar.
Borg, K. E., Esbenshade, K. L., & Johnson, B. H. (1991) · Journal of Animal Science · doi:10.2527/1991.6983230x · Cited by 62 · see citing works
Testosterone secretion, musth behaviour and social dominance in captive male Asian elephants living near the equator
Lincoln, G. A., & Ratnasooriya, W. D. (1996) · Reproduction · doi:10.1530/jrf.0.1080107 · Cited by 61 · see citing works
Physical, Physiological, and Behavioral Correlates of Musth in Captive African Elephants ( <i>Loxodonta africana</i> )
Ganswindt, A., Heistermann, M., & Hodges, K. (2005) · Physiological and Biochemical Zoology · doi:10.1086/430237 · Cited by 58 · see citing works
Thyroidectomy abolishes seasonal testicular cycles of Soay rams
Parkinson, T., & Follett, B. K. (1995) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1995.0001 · Cited by 58 · see citing works
Serum testosterone and musth in captive male African and Asian elephants
Cooper, K. A., Harder, J. D., Clawson, D. H., Fredrick, D. L., Lodge, G. A., Peachey, H., Spellmire, T. J., & Winstel, D. P. (1990) · Zoo Biology · doi:10.1002/zoo.1430090405 · Cited by 49 · see citing works
Changes in Serum Levels of LH, FSH, Prolactin, Testosterone, and Cortisol Associated with Season and Mating in Male Pygmy Goats
HOWLAND, B. E., Sanford, L. M., & PALMER, W. M. (1985) · Journal of Andrology · doi:10.1002/j.1939-4640.1985.tb00822.x · Cited by 46 · see citing works
Altered androstenedione to testosterone ratios and LH concentrations during musth in the captive male Asian elephant ( Elephas maximus )
Niemuller, C., & Liptrap, R. M. (1991) · Reproduction · doi:10.1530/jrf.0.0910139 · Cited by 41 · see citing works
Plasma testosterone levels in relation to musth in the male African Elephant
Hall-Martin, A. J., & van der Walt, L. A. (1984) · Koedoe · doi:10.4102/koedoe.v27i1.561 · Cited by 41 · see citing works
Seasonal variations in thyroxine and testosterone levels in relation to the moult in the adult male mink (Mustela vison Peale and Beauvois)
Boissin‐Agasse, L., Maurel, D., & Boissin, J. (1981) · Canadian Journal of Zoology · doi:10.1139/z81-147 · Cited by 41 · see citing works
Population management of zoo elephants
Wiese, R. J., & Willis, K. B. (2006) · International Zoo Yearbook · doi:10.1111/j.1748-1090.2006.00080.x · Cited by 40 · see citing works
Seasonal changes in weight gain, growth hormone, and thyroid hormones in male red deer (Cervus elaphus atlanticus)
Ryg, M. S., & Langvatn, R. (1982) · Canadian Journal of Zoology · doi:10.1139/z82-331 · Cited by 37 · see citing works
EFFECT OF CORTICOTROPHIN AND CORTICOSTEROIDS ON PLASMA INTERSTITIAL CELL-STIMULATING HORMONE AND URINARY STEROIDS IN THE BOAR
Liptrap, R. M., & RAESIDE, J. I. (1968) · Journal of Endocrinology · doi:10.1677/joe.0.0420033 · Cited by 36 · see citing works
Plasma thyroxine and testosterone levels in the red fox (Vulpes vulpes L.) during the annual cycle
Maurel, D., & Boissin, J. (1981) · General and Comparative Endocrinology · doi:10.1016/0016-6480(81)90301-4 · Cited by 34 · see citing works
Reproductive Endocrinology
Brown, J. L. (2006) · doi:10.1002/9780470344484.ch28 · Cited by 33 · see citing works
Self-citation
Effects of GnRH analogues on pituitary–testicular function in free-ranging African elephants ( Loxodonta africana )
Brown, J. L., Bush, Μ., Wildt, D. E., Raath, J. R., de Vos, V., & Howard, J. (1993) · Reproduction · doi:10.1530/jrf.0.0990627 · Cited by 32 · see citing works
Self-citation
Thyroid hormones are required for the expression of seasonal changes in red deer (Cervus elaphus) stags
Shi, Z., & Barrell, G. K. (1994) · Reproduction Fertility and Development · doi:10.1071/rd9940187 · Cited by 31 · see citing works

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Correlations of plasma cortisol levels, chaperone expression and mammalian longevity: a review of published data
Krøll, J. (2010) · Biogerontology · doi:10.1007/s10522-010-9264-9 · Cited by 10 · see citing works
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Self-citation
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Behringer, V., Heistermann, M., Malaivijitnond, S., Schülke, O., & Ostner, J. (2023) · American Journal of Primatology · doi:10.1002/ajp.23530 · Cited by 9 · see citing works
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Madsen, A. E., Minge, C., Pushpakumara, T. V., Weerathunga, U. S., Padmalal, U. K. G. K., Weerakoon, D. K., & de Silva, S. (2022) · Scientific Reports · doi:10.1038/s41598-022-22989-1 · Cited by 8 · see citing works
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Temporal gland secretion in African elephants (Loxodonta africana)
Kioko, J., Taylor, K., Milne, H. J. M., Hayes, K. Z., & Kiffner, C. (2016) · Mammalian Biology · doi:10.1016/j.mambio.2016.07.005 · Cited by 7 · see citing works
Predictors of testosterone in zoo‐managed male African elephants (Loxodonta Africana)
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Self-citation
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Kosaruk, W., Brown, J. L., Towiboon, P., Pringproa, K., Punyapornwithaya, V., Tankaew, P., Kittisirikul, N., Toonrongchang, W., Janyamathakul, T., Muanghong, P., et al. (2023) · Frontiers in Veterinary Science · doi:10.3389/fvets.2023.1263775 · Cited by 5 · see citing works
Self-citation
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Effects of Positive Reinforcement Training and Novel Object Exposure on Salivary Cortisol Levels under Consideration of Individual Variation in Captive African Elephants (Loxodonta africana)
Hambrecht, S., Oerke, A., Heistermann, M., Hartig, J., & Dierkes, P. W. (2021) · Animals · doi:10.3390/ani11123525 · Cited by 5 · see citing works
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Zheng, Y., Liu, X., Liu, H., Xu, H., Liu, Y., Li, C., Wang, B., Cui, S., Jia, T., Yang, D., et al. (2024) · Conservation Physiology · doi:10.1093/conphys/coae044 · Cited by 4 · see citing works
Multi-year profiles of T3 are positively correlated with corticosterone in male bowhead whale baleen
Hudson, J. M., Hunt, K. E., Marcoux, M., Buck, C. L., & Matthews, C. J. D. (2025) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2025.114800 · Cited by 3 · see citing works
EFFECTS OF GONADOTROPIN-RELEASING HORMONE ANTAGONIST DEGARELIX ON MUSTH AND SERUM TESTOSTERONE CONCENTRATIONS IN ASIAN ELEPHANTS (ELEPHAS MAXIMUS)
Pathirana, I., Rajapaksa, C., Kawate, N., Wimalarathne, A., Fonseka, L., Weerakoon, P. N., Hannan, M. A., Alexander, B., Pushpakumara, P. G. A., Ariyaratne, S., et al. (2018) · Journal of Zoo and Wildlife Medicine · doi:10.1638/2018-0019.1 · Cited by 3 · see citing works
Exploring seasonal variation in the faecal glucocorticoid concentrations of African elephants (
Troup, G., Heinsohn, R., King, L. E., & Edwards, K. L. (2022) · Wildlife Research · doi:10.1071/wr21003 · Cited by 3 · see citing works
Elephants
Pushpakumara, P. G. A., Thitaram, C., & Brown, J. L. (2018) · Elsevier eBooks · doi:10.1016/b978-0-7020-7233-8.00042-2 · Cited by 3 · see citing works
Self-citation
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Jelincic, J., Dillon, D. M., Reed, J., Rogers, M. C., de Mello, D. M. D., Fleming, A. H., Lysiak, N. S. J., New, L., Buck, C. L., & Hunt, K. E. (2026) · Conservation Physiology · doi:10.1093/conphys/coag020 · Cited by 2 · see citing works
The hormone-emotion-behavioural gene-neuromessenger labyrinth: Pertinent questions
Adamafio, N. A. (2009) · Cited by 2 · see citing works
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López Pérez, A. B., Brown, J. L., Goldenberg, S. Z., Rey, A., & Khonmee, J. (2025) · PLOS One · doi:10.1371/journal.pone.0332944 · Cited by 2 · see citing works
“Musth, a phenomenon unique to African and Asian elephants, is typically observed in sexually mature males in good physical condition [22,59] and is associated with increased androgen production [60,61].”
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Shatab, M. S., Kumar, A., Honparkhe, M., Singhal, S., Kaur, S., & Brar, P. S. (2016) · Journal of animal research · doi:10.5958/2277-940x.2016.00158.3 · Cited by 1 · see citing works
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Self-citation
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Negus, C. (2021) · The Sydney eScholarship Repository (The University of Sydney) · Cited by 1 · see citing works
Creating a 21 st Century Darwinian Paradigm
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Glaeser, S. S. (2000) · doi:10.15760/etd.7419
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Keady, M. (2021) · doi:10.13021/mars/7465
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Dow, T. L. (2012) · doi:10.33915/etd.4849
Current World Literature
(2008) · Current Opinion in Endocrinology Diabetes and Obesity · doi:10.1097/med.0b013e3283040e80
References
(2020) · Elsevier eBooks · doi:10.1016/b978-0-12-816208-8.00022-1
Elephants
Brown, J. L. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-809633-8.20654-7
Self-citation
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Hambrecht, S. (2020) · doi:10.21248/gups.56647
Relationship between insulin-like growth factor-1 and semen quality in Asian elephants (elephas maximus)
Yang, Y. (2020) · doi:10.58837/chula.the.2020.476
Elephant Reproduction
Brown, J. L. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-21477-6.00115-2
Self-citation
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Campbell, K. M., Marolf, C. J., Buss, P. E., & Morfeld, K. A. (2025) · Animals · doi:10.3390/ani15131863
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Hyatt, M. W., Penfold, L. M., Mone, A. J., Newton, A. L., & Davis, M. R. (2026) · Journal of Zoo and Wildlife Medicine · doi:10.1638/2025-0039
Influence of intrinsic and extrinsic factors on quality of Asian elephant semen – Current knowledge and new research directions
Yang, Y., Thongthip, N., Angkawanish, T., Comizzoli, P., & Chatdarong, K. (2026) · Animal Reproduction Science · doi:10.1016/j.anireprosci.2026.108122
BLOOD ANALYTE CHANGES ASSOCIATED WITH MUSTH IN TWO CAPTIVE ASIAN ELEPHANT (ELEPHAS MAXIMUS) BULLS
Minor, R. L., Edes, A. N., Kanarr, M. L., Cannizzo, S. A., Griffioen, J. A., Stacy, N. I., Cray, C., Paris, S., Brown, J. L., & Rainwater, K. L. (2026) · Journal of Zoo and Wildlife Medicine · doi:10.1638/2025-0064
Self-citation

Serum testosterone and musth in captive male African and Asian elephants
Cooper, K. A., Harder, J. D., Clawson, D. H., Fredrick, D. L., Lodge, G. A., Peachey, H., Spellmire, T. J., & Winstel, D. P. (1990) · Zoo Biology · doi:10.1002/zoo.1430090405 · Cited by 49 · see citing works
Variation in metabolic factors and gonadal, pituitary, thyroid, and adrenal hormones in association with musth in African and Asian elephant bulls
Chave, E., Edwards, K. L., Paris, S., Prado, N. A., Morfeld, K. A., & Brown, J. L. (2019) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2019.02.005 · Cited by 30 · see citing works
Self-citation
Testosterone secretion, musth behaviour and social dominance in captive male Asian elephants living near the equator
Lincoln, G. A., & Ratnasooriya, W. D. (1996) · Reproduction · doi:10.1530/jrf.0.1080107 · Cited by 61 · see citing works
Reproductive endocrinology of bull elephants
Somerville, M. (2023) · American University Research Archive · doi:10.57912/23878995
Self-citation
A cross-sectional study on serum testosterone and cortisol concentrations in pre-musth and non-musth Asian bull elephants (Elephas maximus) using radioimmunoassay (RIA) in Assam, India
Mahato, G., Sarma, K. K., Sharma, A. K., Arif, S. A., Das, T., & Deka, D. (2025) · Indian Journal of Animal Health · doi:10.36062/ijah.2025.07724

Authors: Brown, J. L., Somerville, M., Riddle, H. S., Keele, M., Duer, C. K., & Freeman, E. W.
Affiliations: Smithsonian Institution (US)
Oregon Zoo (US)
Oklahoma State University (US)
Corresponding author: Brown, Janine L.
ORCID: Brown, Janine L.
Freeman, Elizabeth W.
Venue: General and Comparative Endocrinology
Publisher: Elsevier BV
Published: 2007-04
Volume: 151
Issue: 2
Pages: 153-162
ISSN: 0016-6480 (ISSN-L)
DOI: 10.1016/j.ygcen.2007.01.006
OpenAlex: W1991510594
Cited by: 83
References: 38
Citations by year: 2026: 6 · 2025: 4 · 2024: 6 · 2023: 5 · 2022: 8 · 2021: 7 · 2020: 7 · 2019: 6 · 2018: 7 · 2016: 6 · 2015: 3 · 2014: 2 · 2013: 3 · 2012: 1
FWCI: 3.32
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: General and Comparative Endocrinology (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Reproductive Medicine › Sperm and Testicular Function
Health Sciences › Veterinary › Small Animals › Animal Behavior and Welfare Studies
Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
Keywords: Asian elephant, Loxodonta africana, musth, captive elephants, bull reproduction, testosterone, cortisol, thyroxine, triiodothyronine, thyroid-stimulating hormone, adrenal function, thyroid function, age-related hormonal changes, comparative endocrinology
MeSH terms: Adrenal Glands, Africa, Aging, Animals, Asia, Elephants, Hydrocortisone, Male, Seasons, Testis, Testosterone, Thyroid Gland, Thyroid Hormones, Thyrotropin

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Comparative endocrinology of testicular, adrenal and thyroid function in captive Asian and African elephant bulls

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