Reproductive health assessment of female elephants in north American zoos and association of husbandry practices with reproductive dysfunction in African elephants (Loxodonta africana)
Open accessAbstract
As part of a multi-institutional study of zoo elephant welfare, we evaluated female elephants managed by zoos accredited by the Association of Zoos and Aquariums and applied epidemiological methods to determine what factors in the zoo environment are associated with reproductive problems, including ovarian acyclicity and hyperprolactinemia. Bi-weekly blood samples were collected from 95 African (Loxodonta africana) and 75 Asian (Elephas maximus) (8-55 years of age) elephants over a 12-month period for analysis of serum progestogens and prolactin. Females were categorized as normal cycling (regular 13- to 17-week cycles), irregular cycling (cycles longer or shorter than normal) or acyclic (baseline progestogens, <0.1 ng/ml throughout), and having Low/Normal (<14 or 18 ng/ml) or High (≥14 or 18 ng/ml) prolactin for Asian and African elephants, respectively. Rates of normal cycling, acyclicity and irregular cycling were 73.2, 22.5 and 4.2% for Asian, and 48.4, 37.9 and 13.7% for African elephants, respectively, all of which differed between species (P < 0.05). For African elephants, univariate assessment found that social isolation decreased and higher enrichment diversity increased the chance a female would cycle normally. The strongest multi-variable models included Age (positive) and Enrichment Diversity (negative) as important factors of acyclicity among African elephants. The Asian elephant data set was not robust enough to support multi-variable analyses of cyclicity status. Additionally, only 3% of Asian elephants were found to be hyperprolactinemic as compared to 28% of Africans, so predictive analyses of prolactin status were conducted on African elephants only. The strongest multi-variable model included Age (positive), Enrichment Diversity (negative), Alternate Feeding Methods (negative) and Social Group Contact (positive) as predictors of hyperprolactinemia. In summary, the incidence of ovarian cycle problems and hyperprolactinemia predominantly affects African elephants, and increases in social stability and feeding and enrichment diversity may have positive influences on hormone status.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In 2016, a series of epidemiological studies of elephants in North American zoos revealed problems associated with ovarian acyclicity, health and musculoskeletal function, stereotypic behaviors, and high body condition scores.
“In 2016, a series of epidemiological studies of elephants in North American zoos revealed problems associated with ovarian acyclicity (45), health and musculoskeletal function (46), stereotypic behaviors (35), and high body condition scores (47).”
From Comparison of animal welfare assessment tools and methodologies: need for an effective approach for captive elephants in Asia (2024) · cites this paper as [45]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Applied Multiple Regression/Correlation Analysis for the Behavioral Sciences
Cohen, P., Cohen, P., West, S. G., & Aiken, L. S. (2014) · Psychology Press eBooks · doi:10.4324/9781410606266 · Cited by 20,819 · see citing works
Social Relationships and Mortality Risk: A Meta-analytic Review
Holt-Lunstad, J., Smith, T. B., & Layton, J. B. (2010) · PLoS Medicine · doi:10.1371/journal.pmed.1000316 · Cited by 7,272 · cited 1× · see citing works
“Among social species, the benefits of communal connections, even if individuals are unrelated, include reduced morbidity and mortality [76,77], better physiological function and fitness [78–81] and specifically reproduction [82,83].”
BackgroundSocial Relationships and Health
House, J. S., Landis, K. R., & Umberson, D. (1988) · Science · doi:10.1126/science.3399889 · Cited by 7,073 · see citing works
Akaike's Information Criterion in Generalized Estimating Equations
Pan, W. (2001) · Biometrics · doi:10.1111/j.0006-341x.2001.00120.x · Cited by 2,507 · see citing works
Prolactin: structure, function, and regulation of secretion
Freeman, M. E., Kanyicska, B., Lerant, A., & Nagy, G. (2000) · Physiological Reviews · doi:10.1152/physrev.2000.80.4.1523 · Cited by 2,457 · see citing works
The Prudent Parent: Energetic Adjustments in Avian Breeding1)
Drent, R. H., & Daan, S. (2002) · Ardea · doi:10.5253/arde.v68.p225 · Cited by 2,046 · see citing works
Cacioppo, J. T., Hawkley, L. C., & Thisted, R. A. (2010) · Psychology and Aging · doi:10.1037/a0017216 · Cited by 1,757 · see citing works
(2018) · Elsevier eBooks · doi:10.1016/c2015-1-06718-7 · Cited by 1,525 · see citing works
Environmental enrichment: Increasing the biological relevance of captive environments
Newberry, R. C. (1995) · Applied Animal Behaviour Science · doi:10.1016/0168-1591(95)00616-z · Cited by 1,057 · see citing works
The prudent parent. Energetic adjustments in avian breeding
Drent, R. H., & Daan, S. (1980) · Cited by 806 · see citing works
Strong and Consistent Social Bonds Enhance the Longevity of Female Baboons
Silk, J. B., Beehner, J. C., Bergman, T. J., Crockford, C., Engh, A. L., Moscovice, L. R., Wittig, R. M., Seyfarth, R. M., & Cheney, D. L. (2010) · Current Biology · doi:10.1016/j.cub.2010.05.067 · Cited by 802 · see citing works
The benefits of social capital: close social bonds among female baboons enhance offspring survival
Silk, J. B., Beehner, J. C., Bergman, T. J., Crockford, C., Engh, A. L., Moscovice, L. R., Wittig, R. M., Seyfarth, R. M., & Cheney, D. L. (2009) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2009.0681 · Cited by 717 · see citing works
Chamaillé‐Jammes, S., Fritz, H., Valeix, M., Murindagomo, F., & Clobert, J. (2008) · Journal of Animal Ecology · doi:10.1111/j.1365-2656.2007.01307.x · Cited by 596 · see citing works
Cacioppo, J. T., Hawkley, L. C., Norman, G. J., & Berntson, G. G. (2011) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2011.06028.x · Cited by 554 · see citing works
Social bonds between unrelated females increase reproductive success in feral horses
Cameron, E. Z., Setsaas, T. H., & Linklater, W. L. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0900639106 · Cited by 547 · see citing works
Mechanisms for pituitary tumorigenesis: the plastic pituitary
Melmed, S. K. (2003) · Journal of Clinical Investigation · doi:10.1172/jci20401 · Cited by 458 · see citing works
Estrous cycle influences the response of female rats in the elevated plus-maze test
Marcondes, F. K., Miguel, K. J., Melo, L. L., & Spadari-Bratfisch, R. C. (2001) · Physiology & Behavior · doi:10.1016/s0031-9384(01)00593-5 · Cited by 449 · see citing works
Behavioral Ecology and Conservation Biology
(1998) · doi:10.1093/oso/9780195104899.001.0001 · Cited by 390 · see citing works
Archie, E. A., Moss, C. J., & Alberts, S. C. (2005) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2005.3361 · Cited by 388 · see citing works
Natural Selection of Optimal Reproductive Tactics
Pianka, E. R. (1976) · American Zoologist · doi:10.1093/icb/16.4.775 · Cited by 363 · see citing works
Creative Conservation: Interactive Management of Wild and Captive Animals
Thorne, E. T., Olney, P., Mace, G. M., & Feistner, A. T. C. (1996) · Journal of Wildlife Management · doi:10.2307/3802403 · Cited by 348 · see citing works
Wielebnowski, N. C., Fletchall, N., Carlstead, K., Busso, J. M., & Brown, J. L. (2002) · Zoo Biology · doi:10.1002/zoo.10005 · Cited by 344 · see citing works
Self-citationRico, C., Fabre, S., Medigue, C., di Clemente, N., Clément, F., Bontoux, M., Touzé, J.-L., Dupont, M., Briant, E., Rémy, B., et al. (2008) · Biology of Reproduction · doi:10.1095/biolreprod.108.072157 · Cited by 276 · see citing works
Assessing Animal Welfare at the Farm and Group Level: The Interplay of Science and Values
Fraser, D. J. (2003) · Animal Welfare · doi:10.1017/s0962728600026038 · Cited by 243 · see citing works
Reproductive role of prolactin
Bachelot, A., & Binart, N. (2007) · Reproduction · doi:10.1530/rep-06-0299 · Cited by 224 · see citing works
Cameron, J. L. (1982) · General and Comparative Endocrinology · doi:10.1016/0016-6480(82)90190-3 · Cited by 213 · see citing works
Neuroendocrine responses to stress.
Matteri, R. L., Carroll, J. A., & Dyer, C. J. (2000) · CABI Publishing eBooks · doi:10.1079/9780851993591.0043 · Cited by 213 · see citing works
Effects of environmental enrichment on reproduction
Carlstead, K., & Shepherdson, D. (1994) · Zoo Biology · doi:10.1002/zoo.1430130507 · Cited by 202 · see citing works
Self-citationMellen, J. D. (1991) · Zoo Biology · doi:10.1002/zoo.1430100202 · Cited by 194 · see citing works
Pharmacological causes of hyperprolactinemia.
Torre, D. L., & Falorni, A. (2007) · PubMed Central · Cited by 183 · see citing works
GOBUSH, K. S., MUTAYOBA, B. M., & WASSER, S. K. (2008) · Conservation Biology · doi:10.1111/j.1523-1739.2008.01035.x · Cited by 180 · see citing works
Female post‐reproductive lifespan: a general mammalian trait
Cohen, A. A. (2004) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1017/s1464793103006432 · Cited by 180 · see citing works
Diagnosis and Management of Hyperprolactinemia
Serri, O., Chik, C. L., Ur, E., & Ezzat, S. (2022) · Topics in Obstetrics & Gynecology · doi:10.1097/01.pgo.0000873452.09562.77 · Cited by 171 · see citing works
Persistent Associations between Maternal Prenatal Exposure to Phthalates on Child IQ at Age 7 Years
Factor-Litvak, P. R., Insel, B. J., Calafat, A. M., Liu, X., Perera, F. P., Rauh, V., & Whyatt, R. M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0114003 · Cited by 167 · see citing works
The Brain Prolactin System: Involvement in Stress Response Adaptations in Lactation
Torner, L., & Neumann, I. D. (2002) · Stress · doi:10.1080/1025389021000048638 · Cited by 159 · see citing works
Shepherdson, D. J. (1994) · Springer eBooks · doi:10.1007/978-94-011-0721-1_8 · Cited by 141 · see citing works
Schuff, K. G., Hentges, S. T., Kelly, M. A., Binart, N., Kelly, P. A., Iuvone, P. M., Asa, S. L., & Low, M. J. (2002) · Journal of Clinical Investigation · doi:10.1172/jci15912 · Cited by 133 · see citing works
Diagnosis and Management of Hyperprolactinemia
Wand, G. S. (2003) · The Endocrinologist · doi:10.1097/00019616-200301000-00010 · Cited by 127 · see citing works
Wielebnowski, N. C., Ziegler, K., Wildt, D. E., Lukas, J., & Brown, J. L. (2002) · Animal Conservation · doi:10.1017/s1367943002004043 · Cited by 124 · see citing works
Breeding phenology in relation to NDVI variability in free-ranging African elephant
Wittemyer, G., Rasmussen, H. B., & Douglas‐Hamilton, I. (2007) · Ecography · doi:10.1111/j.0906-7590.2007.04900.x · Cited by 123 · see citing works
Brown, J. L., Schmitt, D. L., Bellem, A. C., Graham, L. H., & Lehnhardt, J. (1999) · Biology of Reproduction · doi:10.1095/biolreprod61.5.1294 · Cited by 121 · see citing works
Prolactin Secretion in Healthy Adults Is Determined by Gender, Age and Body Mass Index
Roelfsema, F., Pijl, H., Keenan, D. M., & Veldhuis, J. D. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031305 · Cited by 117 · see citing works
Social factors influence ovarian acyclicity in captive African elephants (Loxodonta africana)
Freeman, E. W., Guagnano, G., Olson, D., Keele, M., & Brown, J. L. (2008) · Zoo Biology · doi:10.1002/zoo.20187 · Cited by 117 · see citing works
Prolactin regulation of estrogen receptor expression
Frasor, J. M., & Gibori, G. (2003) · Trends in Endocrinology and Metabolism · doi:10.1016/s1043-2760(03)00030-4 · Cited by 114 · see citing works
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
The role of anti‐Müllerian hormone in female fertility and infertility – an overview
Grynnerup, A. G.-A., Lindhard, A., & Sørensen, S. (2012) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.1111/j.1600-0412.2012.01471.x · Cited by 101 · see citing works
Prolactin, Psychological Stress and Environment in Humans: Adaptation and Maladaptation
Sobrinho, L. G. (2003) · Pituitary · doi:10.1023/a:1026229810876 · Cited by 101 · see citing works
Fecal corticoid metabolite measurement in the cheetah (Acinonyx jubatus)
Jurke, M. H., Czekala, N. M., Lindburg, D. G., & Millard, S. E. (1997) · Zoo Biology · doi:10.1002/(sici)1098-2361(1997)16:2 · Cited by 94 · see citing works
Birkett, P. J., Vanak, A. T., Muggeo, V. M. R., Ferreira, S. M., & Slotow, R. (2012) · PLoS ONE · doi:10.1371/journal.pone.0038363 · Cited by 94 · see citing works
A comparative approach to the study of Keeper–Animal Relationships in the zoo
Carlstead, K. (2009) · Zoo Biology · doi:10.1002/zoo.20289 · Cited by 94 · see citing works
Reproductive cessation and post-reproductive lifespan in Asian elephants and pre-industrial humans
Lahdenperä, M., Mar, K. U., & Lummaa, V. (2014) · Frontiers in Zoology · doi:10.1186/s12983-014-0054-0 · Cited by 92 · see citing works
Brown, J. L., & Lehnhardt, J. (1995) · Zoo Biology · doi:10.1002/zoo.1430140608 · Cited by 79 · see citing works
Greco, B. J., Meehan, C. L., Miller, L. J., Shepherdson, D. J., Morfeld, K. A., Andrews, J., Baker, A. M., Carlstead, K., & Mench, J. A. (2016) · PLOS ONE · doi:10.1371/journal.pone.0152490 · Cited by 73 · see citing works
An epidemiological approach to welfare research in zoos: the elephant welfare project
Carlstead, K., Mench, J. A., Meehan, C., & Brown, J. L. (2013) · Journal of Applied Animal Welfare Science · doi:10.1080/10888705.2013.827915 · Cited by 68 · see citing works
Self-citationA preliminary study of the behavioral effects of feeding enrichment on African elephants
Stoinski, T. S., Daniel, E., & Maple, T. L. (2000) · Zoo Biology · doi:10.1002/1098-2361(2000)19:6 · Cited by 66 · see citing works
Prado-Oviedo, N. A., Bonaparte-Saller, M. K., Malloy, E. J., Meehan, C. L., Mench, J. A., Carlstead, K., & Brown, J. L. (2016) · PLoS ONE · doi:10.1371/journal.pone.0154750 · Cited by 61 · see citing works
Follicular status at the menopause*
Gosden, R. G. (1987) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a136601 · Cited by 60 · see citing works
Life events in the pathogenesis of hyperprolactinemia
Sonino, N., Navarrini, C., Ruini, C., Fallo, F., Boscaro, M., & Fava, G. A. (2004) · European Journal of Endocrinology · doi:10.1530/eje.0.1510061 · Cited by 57 · see citing works
Wittemyer, G., Ganswindt, A., & Hodges, K. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.12.013 · Cited by 52 · see citing works
Comparative Reproductive Biology of Elephants
Brown, J. L. (2014) · Advances in experimental medicine and biology · doi:10.1007/978-1-4939-0820-2_8 · Cited by 51 · see citing works
Effects of cage size and enrichment on reproductive performance and behavior in C57BL/6Tac mice
Whitaker, J., Moy, S. S., Godfrey, V., Nielsen, J. N., Bellinger, D. A., & Bradfield, J. F. (2008) · Lab Animal · doi:10.1038/laban0109-24 · Cited by 51 · see citing works
Pituitary tumors. Current concepts in diagnosis and management.
Aron, D. C., Tyrrell, J. B., & Wilson, C. B. (1995) · PubMed · Cited by 50 · see citing works
Individual differences in emotionality: social temperament and health
Capitanio, J. P. (2010) · American Journal of Primatology · doi:10.1002/ajp.20870 · Cited by 50 · see citing works
Influence of the estrous cycle on the behavior of rats in the elevated T-maze
Gouvêia, A., dos Santos, U. D., Felisbino, F. E., Afonseca, T. L., Antunes, G., & Morato, S. (2004) · Behavioural Processes · doi:10.1016/j.beproc.2004.03.018 · Cited by 49 · see citing works
Meehan, C. L., Hogan, J. N., Bonaparte-Saller, M. K., & Mench, J. A. (2016) · PLOS ONE · doi:10.1371/journal.pone.0146703 · Cited by 45 · see citing works
Response of African Elephants (Loxodonta africana) to Seasonal Changes in Rainfall
Garstang, M., Davis, R. E. L., Leggett, K. E. A., Frauenfeld, O. W., Greco, S., Zipser, E. J., & Peterson, M. J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0108736 · Cited by 43 · see citing works
A Behavioral Taxonomy of Loneliness in Humans and Rhesus Monkeys (Macaca mulatta)
Capitanio, J. P., Hawkley, L. C., Cole, S. W., & Cacioppo, J. T. (2014) · PLoS ONE · doi:10.1371/journal.pone.0110307 · Cited by 40 · see citing works
Dow, T. L., Holásková, I., & Brown, J. L. (2011) · Zoo Biology · doi:10.1002/zoo.20377 · Cited by 38 · see citing works
Glaeser, S. S., Hunt, K. E., Martin‐Wintle, M. S., Finnegan, M., & Brown, J. L. (2012) · Theriogenology · doi:10.1016/j.theriogenology.2012.01.014 · Cited by 37 · see citing works
The naked truth: Breeding performance in nude mice with and without nesting material
Gaskill, B. N., Winnicker, C., Garner, J. P., & Pritchett‐Corning, K. R. (2012) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2012.10.009 · Cited by 36 · see citing works
Freeman, E. W., Whyte, I. J., & Brown, J. L. (2008) · African Journal of Ecology · doi:10.1111/j.1365-2028.2008.00957.x · Cited by 35 · see citing works
Food hiding and enrichment in captive Asian elephants
Wiedenmayer, C. P. (1998) · Applied Animal Behaviour Science · doi:10.1016/s0168-1591(97)00091-9 · Cited by 35 · see citing works
Meagher, R. K., Dallaire, J. A., Campbell, D. L. M., Ross, M., Møller, S. H., Hansen, S. W., Díez‐León, M., Palme, R., & Mason, G. J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0110589 · Cited by 34 · see citing works
Fanson, K., & Wielebnowski, N. (2013) · Animal Welfare · doi:10.7120/09627286.22.2.159 · Cited by 32 · see citing works
Proctor, C. M., Freeman, E. W., & Brown, J. L. (2009) · Zoo Biology · doi:10.1002/zoo.20238 · Cited by 31 · see citing works
Jahn, G. A., & Deis, R. P. (1986) · Journal of Endocrinology · doi:10.1677/joe.0.1100423 · Cited by 30 · see citing works
Hyperprolactinemia in women with paternal deprivation during childhood.
Lg, S., Mc, N., Calhaz–Jorge, C., Am, A., Mc, P., & Ma, S. (1984) · PubMed · Cited by 30 · see citing works
Dow, T. L., & Brown, J. L. (2012) · Reproduction Fertility and Development · doi:10.1071/rd11302 · Cited by 29 · see citing works
Social networks in African elephants
Vance, E. A., Archie, E. A., & Moss, C. J. (2009) · Computational and Mathematical Organization Theory · doi:10.1007/s10588-008-9045-z · Cited by 27 · see citing works
Yamamoto, Y., YAMAMOTO, T., Watanabe, G., Yuto, N., Keio, M., NARUSHIMA, E., Katayanagi, M., Nakao, R., MORIKUBO, S., Sakurai, Y., et al. (2010) · Journal of Veterinary Medical Science · doi:10.1292/jvms.09-0480 · Cited by 24 · see citing works
Psychosocial aspects of hyperprolactinemia
Assies, J., Vingerhoets, A. J. J. M., & Poppelaars, K. (1992) · Psychoneuroendocrinology · doi:10.1016/0306-4530(92)90026-4 · Cited by 23 · see citing works
Nimon, A., & Broom, D. (2001) · Animal Welfare · doi:10.1017/s0962728600024015 · Cited by 22 · see citing works
Morfeld, K. A., Ball, R. L., & Brown, J. L. (2014) · Journal of Zoo and Wildlife Medicine · doi:10.1638/2013-0254r.1 · Cited by 21 · see citing works
Dow, T. L., Roudebush, W. E., Parker, F. N., & Brown, J. L. (2010) · Theriogenology · doi:10.1016/j.theriogenology.2010.10.002 · Cited by 20 · see citing works
Freeman, E. W., Meyer, J. M., Putman, S. B., Schulte, B. A., & Brown, J. L. (2013) · Conservation Physiology · doi:10.1093/conphys/cot025 · Cited by 20 · see citing works
Mouttham, L., Buhr, M. M., Freeman, E. W., Widowski, T. M., Graham, L. H., & Brown, J. L. (2011) · Animal Reproduction Science · doi:10.1016/j.anireprosci.2011.04.006 · Cited by 18 · see citing works
Chelini, M. O. M., Palme, R., & Otta, E. (2011) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.06.006 · Cited by 18 · see citing works
Prado, N. A., Malloy, E. J., Deng, X., & Brown, J. L. (2013) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2013.03.035 · Cited by 16 · see citing works
Using a simplified field progestagen method to assess ovarian activity in female African elephants
Freeman, E. W., Meyer, J. M., Putman, S. B., Schulte, B. A., & Brown, J. L. (2011) · Biological Conservation · doi:10.1016/j.biocon.2011.04.033 · Cited by 12 · see citing works
Wittemyer, G., Ganswindt, A., & Hodges, K. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.12.014 · Cited by 7 · see citing works
Hyperprolactinemia in Women of Reproductive Age: Etiology, diagnosis, and management.
Yuen, B. H. (1992) · PubMed · Cited by 6 · see citing works
Stansfield, F. J., Nöthling, J. O., & Allen, W. R. T. (2012) · Reproduction Fertility and Development · doi:10.1071/rd12296 · Cited by 6 · see citing works
Wiese (2000) · doi:10.1002/1098-2361(2000)19:5
Flagged first, then by citations
4 of the 97 references couldn’t be matched to a known paper.
Research works printed but not linked: 5
- [4]Brown JL. Reproductive endocrine monitoring of elephants: An essential tool for assisting captive management. Zoo Biol. 2000; 19: 347– 368.
- [9]Brown JL, Citino SB, Bush M, Lehnhardt J, Phillips LG. Cyclic patterns of luteinizing hormone, follicle-stimulating hormone, inhibin, and progesterone secretion in the Asian elephant (Elephas maximus). J Zoo Wildl Med. 1991; 1: 49– 57.
- [42]Brown JL, Lehnhardt J. Secretory patterns of serum prolactin in Asian (Elephas maximus) and African (Loxodonta africana) elephants during different reproductive states: Comparison with concentrations in a non-cycling African elephant. Zoo Biol. 1997; 16: 149– 159.
- [64]Shepherdson DJ. Environmental enrichment for elephants: Current status and future directions. J Elephant Manag Assoc. 1999; 10: 69– 77.
- [65]Shepherdson DJ, Mellen JD, Hutchins M, editors. Second nature: Environmental enrichment for captive animals Washington, D.C.; Smithsonian Institution Press; 1998.
Cited by
Sorted by citations
Meehan, C. L., Mench, J. A., Carlstead, K., & Hogan, J. N. (2016) · PLOS ONE · doi:10.1371/journal.pone.0158124 · Cited by 82 · see citing works
Greco, B. J., Meehan, C. L., Miller, L. J., Shepherdson, D. J., Morfeld, K. A., Andrews, J., Baker, A. M., Carlstead, K., & Mench, J. A. (2016) · PLOS ONE · doi:10.1371/journal.pone.0152490 · Cited by 73 · see citing works
Elephant tourism in Thailand: a review of animal welfare practices and needs
Bansiddhi, P., Brown, J. L., Thitaram, C., Punyapornwithaya, V., & Nganvongpanit, K. (2020) · Journal of Applied Animal Welfare Science · doi:10.1080/10888705.2019.1569522 · Cited by 65 · see citing works
Holdgate, M. R., Meehan, C. L., Hogan, J. N., Miller, L. J., Soltis, J., Andrews, J., & Shepherdson, D. J. (2016) · PLoS ONE · doi:10.1371/journal.pone.0150331 · Cited by 65 · see citing works
Prado-Oviedo, N. A., Bonaparte-Saller, M. K., Malloy, E. J., Meehan, C. L., Mench, J. A., Carlstead, K., & Brown, J. L. (2016) · PLoS ONE · doi:10.1371/journal.pone.0154750 · Cited by 61 · see citing works
Greco, B. J., Meehan, C. L., Heinsius, J. L., & Mench, J. A. (2017) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2017.05.003 · Cited by 56 · see citing works
Comparative ovarian function and reproductive monitoring of endangered mammals
Brown, J. L. (2017) · Theriogenology · doi:10.1016/j.theriogenology.2017.12.004 · Cited by 50 · see citing works
Bansiddhi, P., Brown, J. L., Khonmee, J., Norkaew, T., Nganvongpanit, K., Punyapornwithaya, V., Angkawanish, T., Somgird, C., & Thitaram, C. (2019) · PLoS ONE · doi:10.1371/journal.pone.0221537 · Cited by 46 · see citing works
Brown, J. L., Carlstead, K., Bray, J. D., Dickey, D., Farin, C., & Ange-van Heugten, K. (2019) · PLOS ONE · doi:10.1371/journal.pone.0217326 · Cited by 46 · see citing works
Self-citationMeehan, C. L., Hogan, J. N., Bonaparte-Saller, M. K., & Mench, J. A. (2016) · PLOS ONE · doi:10.1371/journal.pone.0146703 · Cited by 45 · see citing works
Edwards, K. L., Miller, M. A., Carlstead, K., & Brown, J. L. (2019) · PLoS ONE · doi:10.1371/journal.pone.0217774 · Cited by 45 · see citing works
Stress, Well-Being and Reproductive Success
Edwards, K. L., Edes, A. N., & Brown, J. L. (2019) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-23633-5_5 · Cited by 43 · see citing works
Keady, M., Prado, N. A., Lim, H. C., Brown, J. L., Paris, S., & Muletz‐Wolz, C. R. (2021) · Animal Microbiome · doi:10.1186/s42523-021-00146-9 · Cited by 41 · see citing works
Edwards, K. L., Bansiddhi, P., Paris, S., Galloway, M., & Brown, J. L. (2019) · Conservation Physiology · doi:10.1093/conphys/coy077 · Cited by 36 · see citing works
Waste to Carbon: Biocoal from Elephant Dung as New Cooking Fuel
Stępień, P., Świechowski, K., Hnat, M., Kugler, S., Stegenta-Dąbrowska, S., Koziel, J. A., Manczarski, P., & Białowiec, A. (2019) · Energies · doi:10.3390/en12224344 · Cited by 36 · see citing works
Scott, N. L., & LaDue, C. A. (2019) · Zoo Biology · doi:10.1002/zoo.21506 · Cited by 30 · see citing works
Evolutionary significance of maternal kinship in a long-lived mammal
Lynch, E. C., Lummaa, V., Htut, W., & Lahdenperä, M. (2019) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2018.0067 · Cited by 27 · see citing works
Glaeser, S. S., Edwards, K. L., Wielebnowski, N. C., & Brown, J. L. (2020) · PLoS ONE · doi:10.1371/journal.pone.0241910 · Cited by 28 · see citing works
Brown, J. L., Bansiddhi, P., Khonmee, J., & Thitaram, C. (2020) · Animals · doi:10.3390/ani10040737 · Cited by 26 · see citing works
Kosaruk, W., Brown, J. L., Plangsangmas, T., Towiboon, P., Punyapornwithaya, V., Silva-Fletcher, A., Thitaram, C., Khonmee, J., Edwards, K. L., & Somgird, C. (2020) · Animals · doi:10.3390/ani10101928 · Cited by 24 · see citing works
Glaeser, S. S., Shepherdson, D., Lewis, K., Prado, N., Brown, J. L., Lee, B., & Wielebnowski, N. (2021) · Animals · doi:10.3390/ani11092566 · Cited by 24 · see citing works
Incorporating stakeholder perspectives into the assessment and provision of captive elephant welfare
Chadwick, C. L., Williams, E., Asher, L., & Yon, L. (2017) · Animal Welfare · doi:10.7120/09627286.26.4.461 · Cited by 24 · see citing works
The Chemical Ecology of Elephants: 21st Century Additions to Our Understanding and Future Outlooks
Schulte, B. A., & LaDue, C. A. (2021) · Animals · doi:10.3390/ani11102860 · Cited by 24 · see citing works
Update on Comparative Biology of Elephants: Factors Affecting Reproduction, Health and Welfare
Brown, J. L. (2019) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-23633-5_9 · Cited by 22 · see citing works
Miller, L. J., Lauderdale, L. K., Mellen, J. D., Walsh, M. T., & Granger, D. A. (2021) · PLoS ONE · doi:10.1371/journal.pone.0252861 · Cited by 23 · see citing works
A Systematic Review on the Link between Animal Welfare and Antimicrobial Use in Captive Animals
da Costa, M. R., & Diana, A. (2022) · Animals · doi:10.3390/ani12081025 · Cited by 23 · see citing works
Morfeld, K. A., & Brown, J. L. (2017) · PLOS ONE · doi:10.1371/journal.pone.0188701 · Cited by 22 · see citing works
Self-citationAdiposity and Reproductive Cycling Status in Zoo African Elephants
Chusyd, D. E., Brown, J. L., Hambly, C., Johnson, M. S., Morfeld, K. A., Patki, A., Speakman, J. R., Allison, D. B., & Nagy, T. R. (2017) · Obesity · doi:10.1002/oby.22046 · Cited by 21 · see citing works
Zoo elephant research: contributions to conservation of captive and free‐ranging species
Bechert, U. S., Brown, J. L., Dierenfeld, E. S., Ling, P. D., Molter, C. M., & Schulte, B. A. (2019) · International Zoo Yearbook · doi:10.1111/izy.12211 · Cited by 21 · see citing works
LaDue, C. A., Hunt, K. E., Kiso, W. K., & Freeman, E. W. (2023) · Conservation Physiology · doi:10.1093/conphys/coad019 · Cited by 16 · see citing works
The historical development of zoo elephant survivorship
Scherer, L., Bingaman Lackey, L., Clauss, M., Gries, K., Hagan, D., Lawrenz, A., Müller, D. W. H., Roller, M., Schiffmann, C., & Oerke, A. (2023) · Zoo Biology · doi:10.1002/zoo.21733 · Cited by 15 · see citing works
“For female African elephants, a higher sensitivity for ovarian cycle problems than in Asian elephants was detected (Brown et al., 2016; Oerke et al., 2002), pointing toward a generally more sensitive nature of this species.”
BackgroundPrado, N. A., Keady, M., Oestmann, A., Steinbeiser, C. M., & Brown, J. L. (2019) · Biology of Reproduction · doi:10.1093/biolre/ioz036 · Cited by 15 · see citing works
Chusyd, D. E., Nagy, T. R., Golzarri‐Arroyo, L., Dickinson, S., Speakman, J. R., Hambly, C., Johnson, M. S., Allison, D. B., & Brown, J. L. (2021) · Journal of Experimental Biology · doi:10.1242/jeb.219543 · Cited by 13 · see citing works
Hufenus, R., Schiffmann, C. L., Hatt, J., Müller, D. W. H., Lackey, L. B., Clauß, M., & Zerbe, P. (2018) · Mammal Review · doi:10.1111/mam.12133 · Cited by 14 · see citing works
Feng, X., Hua, R., Zhang, W., Liu, Y., Luo, C., Li, T., Chen, X., Zhu, H., Wang, Y., & Lu, Y. (2023) · Frontiers in Veterinary Science · doi:10.3389/fvets.2023.986382 · Cited by 13 · see citing works
Meehan, C., Greco, B., Lynn, B., Morfeld, K., Vicino, G., Orban, D., Gorsuch, C., Quick, M., Ripple, L., Fournier, K., et al. (2019) · International Zoo Yearbook · doi:10.1111/izy.12222 · Cited by 12 · see citing works
Prado, N. A., Paris, S., & Brown, J. L. (2018) · Zoo Biology · doi:10.1002/zoo.21464 · Cited by 13 · see citing works
Cameron, E. Z., & Ryan, S. J. (2016) · PLoS ONE · doi:10.1371/journal.pone.0158701 · Cited by 12 · see citing works
Monitoring and controlling ovarian activity in elephants
Thitaram, C., & Brown, J. L. (2017) · Theriogenology · doi:10.1016/j.theriogenology.2017.12.009 · Cited by 12 · see citing works
Hacker, C., Miller, L., & Schulte, B. (2018) · Animal Welfare · doi:10.7120/09627286.27.1.055 · Cited by 14 · see citing works
Flacke, G. L., Schwarzenberger, F., Penfold, L. M., Walker, S. L., Martin, G. B., Millar, R. P., & Paris, M. C. J. (2017) · Theriogenology · doi:10.1016/j.theriogenology.2017.07.017 · Cited by 11 · see citing works
Prado, N. A., Carlstead, K., Malloy, E. J., Paris, S., Wielebnowski, N. C., Rockwood, L. L., & Brown, J. L. (2020) · Hormones and Behavior · doi:10.1016/j.yhbeh.2020.104804 · Cited by 11 · see citing works
Kosaruk, W., Brown, J. L., Towiboon, P., Punyapornwithaya, V., Pringproa, K., & Thitaram, C. (2023) · Animals · doi:10.3390/ani13091548 · Cited by 10 · see citing works
Boonprasert, K., Yun, Y., Kosaruk, W., Towiboon, P., Tankaew, P., Punyapornwithaya, V., Janyamathakul, T., Muanghong, P., Brown, J. L., Thitaram, C., et al. (2021) · Animals · doi:10.3390/ani11092530 · Cited by 10 · see citing works
Immunoglobulin A and Physiologic Correlates of Well-Being in Asian Elephants
Moresco, A., Prado, N. A., Davis, M., Schreier, A. L., Readyhough, T. S., Joseph, S., Gray, C., & Brown, J. L. (2022) · Journal of Zoological and Botanical Gardens · doi:10.3390/jzbg3040050 · Cited by 9 · see citing works
Ghimire, R., Brown, J. L., Thitaram, C., & Bansiddhi, P. (2024) · Frontiers in Veterinary Science · doi:10.3389/fvets.2024.1370909 · Cited by 8 · see citing works
The elusive role of prolactin in the sociality of the naked mole-rat
Gilbert, J. D., Rossiter, S. J., Bennett, N. C., & Faulkes, C. G. (2022) · Hormones and Behavior · doi:10.1016/j.yhbeh.2022.105196 · Cited by 7 · see citing works
de Mori, B., Stagni, E., Ferrante, L., Vogt, G., Ramsay, K., & Normando, S. (2019) · Animals · doi:10.3390/ani9100831 · Cited by 7 · see citing works
Predictors of testosterone in zoo‐managed male African elephants (Loxodonta Africana)
Campbell, K. M., Wilson, J. A., & Morfeld, K. A. (2022) · Zoo Biology · doi:10.1002/zoo.21737 · Cited by 7 · see citing works
Male elephant management in AZA institutions: Current status and priorities for the future
LaDue, C. A., Davis, M., Emory, R., & Snyder, R. J. (2024) · Zoo Biology · doi:10.1002/zoo.21835 · Cited by 6 · see citing works
A zoo animal's neighbourhood: how conspecific neighbours impact welfare
Whitham, J. C., & Miller, L. J. (2019) · Animal Welfare · doi:10.7120/09627286.28.2.127 · Cited by 6 · see citing works
Prado, N. A., Krcmarik, M. D., Paris, S., Larry, L., & Brown, J. L. (2023) · Theriogenology Wild · doi:10.1016/j.therwi.2023.100062 · Cited by 7 · see citing works
Bechert, U. S., Hixon, S., & Schmitt, D. L. (2021) · Zoo Biology · doi:10.1002/zoo.21619 · Cited by 6 · see citing works
Development of a welfare assessment tool for tourist camp elephants in Asia
Ghimire, R., Brown, J. L., Thitaram, C., Glaeser, S. S., Lampang, K. N., Kulnanan, P., & Bansiddhi, P. (2024) · PeerJ · doi:10.7717/peerj.18370 · Cited by 6 · see citing works
Edes, A. N., Brown, J. L., & Edwards, K. L. (2022) · American Journal of Primatology · doi:10.1002/ajp.23457 · Cited by 6 · see citing works
Trask, A. E., Carraro, C., Kock, R. A., McCrea, R. S., Newland, S., Royer, E., Medina, S., Fontenot, D. K., & Ewen, J. G. (2023) · Animal Conservation · doi:10.1111/acv.12895 · Cited by 5 · see citing works
The African Elephant (Loxodonta africana): Mini-Review of an Endangered Species
de Sales, A. R., Anastácio, R. S. S., & Pereira, M. J. (2020) · Natural Resources · doi:10.4236/nr.2020.118019 · Cited by 5 · see citing works
Elwell, E. J., & Vaglio, S. (2023) · Animals · doi:10.3390/ani13101617 · Cited by 6 · see citing works
Dow, T. L., Cross, D. L., & Brown, J. L. (2020) · Journal of Zoo and Wildlife Medicine · doi:10.1638/2019-0017 · Cited by 4 · see citing works
Pontzer, H., Rimbach, R., Paltan, J., Ivory, E. L., & Kendall, C. J. (2020) · Royal Society Open Science · doi:10.1098/rsos.201155 · Cited by 4 · see citing works
Abegglen, L. M., Harrison, T. M., Moresco, A., Fowles, J. S., Troan, B. V., Kiso, W. K., Schmitt, D. L., Boddy, A. M., & Schiffman, J. D. (2022) · Animals · doi:10.3390/ani12152005 · Cited by 5 · see citing works
Saito, M. H., Matsunaga, M., Fukuizumi, H., Nakamichi, M., & Kinoshita, K. (2023) · Zoo Biology · doi:10.1002/zoo.21774 · Cited by 3 · see citing works
Roth, T. L., Donelan, E. M., Rispoli, L. A., & Reilly, T. (2023) · Theriogenology Wild · doi:10.1016/j.therwi.2023.100035 · Cited by 3 · see citing works
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
Review: The role of prolactin in the maternal investment-survival balance
Huijsmans, T. E. R. G., Soom, A. V., Smits, K., Wauters, J., & Hildebrandt, T. B. (2024) · Theriogenology Wild · doi:10.1016/j.therwi.2024.100109 · Cited by 3 · see citing works
Yang, Y., Kittisirikul, N., Langkaphin, W., Angkawanish, T., Comizzoli, P., & Chatdarong, K. (2025) · The Veterinary Journal · doi:10.1016/j.tvjl.2025.106324 · Cited by 2 · see citing works
Rose, J. B., Leeds, A., LeMont, R., Yang, L. M., Fayette, M. A., Proudfoot, J. S., Bowman, M. R., Woody, A., Oosterhuis, J. E., & Fagan, D. A. (2022) · Journal of Zoological and Botanical Gardens · doi:10.3390/jzbg3010008 · Cited by 1 · see citing works
Chapter 11. Mahout-elephant relationships
Crawley, J. A. H. (2023) · IRD Éditions eBooks · doi:10.4000/books.irdeditions.47365 · Cited by 1 · see citing works
Flacke, G. L. (2017) · UWA Profiles and Research Repository (UWA) · doi:10.4225/23/5953425346527 · Cited by 1 · see citing works
(2020) · Elsevier eBooks · doi:10.1016/b978-0-12-816208-8.00022-1
Brown, J. L. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-809633-8.20654-7
Chusyd, D. E., Brown, J. L., Golzarri‐Arroyo, L., Dickinson, S., Kraus, V. B., Siegal-Willott, J. L., Griffin, T. M., Huebner, J. L., Edwards, K. L., Allison, D. B., et al. (2023) · Journal of Zoo and Wildlife Medicine · doi:10.1638/2021-0080
Brown, J. L. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-21477-6.00115-2
Watters, D. J. V., & Krebs, D. B. L. (2025) · Wiley eBooks · doi:10.1002/9781118884836.ch11
Psychological Well-being of Animals in Zoos and Aquariums
Allard, S. M., Shepherdson, D. J., & Carlstead, K. (2025) · CABI eBooks · doi:10.1079/9781800624313.0020
Mosleh, G., & Nimrouzi, M. (2025) · The Journal of Obstetrics and Gynecology of India · doi:10.1007/s13224-025-02182-w
Metabolic profiles of captive Asian elephants (Elephas maximus) in Lao PDR and Thailand
Pérez, A. B. L., Brown, J. L., Punyapornwithaya, V., Thitaram, C., Pongsumpan, J., Supanta, J., Tocharoennirattisai, W., & Khonmee, J. (2025) · PLoS ONE · doi:10.1371/journal.pone.0334550
Prado, N. A., & Brown, J. L. (2026) · Advances in experimental medicine and biology · doi:10.1007/978-3-031-87707-0_15
Sayuti, A., Fahrimal, Y., Sutriana, A., Stremme, C. R., Ferdian, R., Ridwan, R., Nugraha, T. P., Semiadi, G., & Gholib, G. (2026) · Veterinary Medicine International · doi:10.1155/vmi/1184315
Gregory, J. T., Maldonado, J. E., Brown, J. L., McInerney, N. R., Rogers, R., Campana, M. G., & Prado, N. A. (2026) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2026.115017
- Authors
- Brown, J. L., Paris, S., Prado-Oviedo, N. A., Meehan, C. L., Hogan, J. N., Morfeld, K. A., & Carlstead, K.
- Affiliations
- Smithsonian Conservation Biology Institute (US)
- Corresponding author
- Brown, Janine L.
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2016-07-14
- Volume
- 11
- Issue
- 7
- Pages
- e0145673
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC4945061
- OpenAlex
- W2472595233
- Cited by
- 83
- References
- 97
- Citations by year
- 2026: 4 · 2025: 5 · 2024: 5 · 2023: 10 · 2022: 8 · 2021: 8 · 2020: 8 · 2019: 15 · 2018: 5 · 2017: 8 · 2016: 6
- FWCI
- 17.44
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- public-domain
- creativecommons.org/publicdomain/zero/1.0/ (vor)
- Locations
- PLoS ONE (publishedVersion, public-domain)
- Europe PMC (PubMed Central) (publishedVersion, public-domain)
- PubMed Central (publishedVersion, public-domain)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Institute of Museum and Library Services
- Topics
- Health Sciences › Veterinary › Small Animals › Animal Behavior and Welfare Studies
- Life Sciences › Agricultural and Biological Sciences › Agronomy and Crop Science › Reproductive Physiology in Livestock
- Health Sciences › Veterinary › Small Animals › Veterinary Medicine and Surgery
- Keywords
- zoo elephants, Loxodonta africana, Asian elephant, reproductive disorders, hyperprolactinemia, prolactin, progestogens, reproductive cycle, husbandry practices, social isolation, feeding methods, captive animal welfare, zoo animal health
- MeSH terms
- Age Factors, Animals, Animal Husbandry, Animal Welfare, Animals, Zoo, Elephants, Female, Housing, Animal, Progestins, Prolactin, Reproduction, Social Environment, Social Isolation, United States, Estrous Cycle
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review