Abstract
Asian (Elephas maximus) and African (Loxodonta africana) elephants serve as important keystone, umbrella and flagship species. Despite that, population numbers are declining, due mainly to poachingĀ and habitat destruction. Understanding reproductive mechanisms is vital to effective management, particularly insurance populations in captivity, and to that end, long-term biological databases are key to understanding how intrinsic and extrinsic factors affect reproductive function at individual and population levels. Through decades of hormonal and ultrasonographic monitoring, many unique aspects of zoo elephant reproduction have been identified, including differences in luteal steroidogenic activity, follicular maturation, pituitary gonadotropin secretion, fetal development and reproductive tract anatomy. Reproductive problems also hamper captive propagation efforts, particularly those related to abnormal or lack of ovarian cyclicity. Recent large-scale, multi-institutional studies and use of epidemiological approaches have identified factors important for good welfare and reproduction, which include enrichment, feeding diversity, good elephant-keeper relations, social compatibility, exercise, and not being obese. There are notable differences in reproductive mechanisms between Asian and African elephants, as well as the factors that influence reproduction and welfare, suggesting species-targeted management approaches are needed to maximize fitness. In the first edition, we discussed reproductive function in male and female elephants. Since then, a number of significant advances have been made primarily in female elephants, which will be the focus of this updated review.
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References
Ahlers MJ, Ganswindt A, MĆ¼nscher S, Bertschinger HJ. Fecal 20-oxo-pregnane concentrations in free-ranging African elephants (Loxodonta africana) treated with porcine zona pellucida vaccine. Theriogenology. 2012;78:77ā85.
Allen WR. Ovulation, pregnancy, placentation and husbandry in the African elephant (Loxodonta africana). Philos Trans R Soc B. 2006;361:821ā34.
Allen WR, Mathias SS, Wooding FBP, Skidmore JA, van Aarde RJ. Placentation in the African elephant, Loxodonta africana. I. Endocrinological aspects. Reprod Suppl. 2002;60:105ā16.
Allen WR, Mathias S, Ford M. Placentation in the African elephant, Loxodonta africana. IV. Growth and function of the fetal gonads. Reproduction. 2005;130:713ā20.
Ange K, Crissey SD, Doyle C, Lance K, Hintz H. A survey of African (Loxodonta afriana) and Asian (Elephas maximus) elephant diets and measured body dimensions compared to their estimated nutrient requirements. Proc Nutr Advisory Group Conf. 2001;4:5ā14.
Angkawanish T, Thitaram C. Behavioral study and monitoring of Asian elephant (Elephas maximus) reintroduction under the Queenās initiative. In: Aranovich M, Dufresne O, editors. Elephants: ecology, behavior and conservation. New York: Nova Science; 2012. p. 133ā44.
Aron DC, Tyrrell JB, Wilson CB. Pituitary tumors: current concepts in diagnosis and management. West J Med. 1985;162:340ā52.
Assies J, Vingerhoets JJM, Poppelaars K. Psychosocial aspects of hyperprolactinemia. Psychoneuroendocrinology. 1992;17:673ā9.
Bachelot A, Binart N. Reproductive role of prolactin. Reproduction. 2007;113:361ā9.
Bechert US, Swanson L, Wasser SK, Hess DL, Stormshak F. Serum prolactin concentrations in the captive female African elephant (Loxodonta africana): potential effects of season and steroid hormone interactions. Gen Comp Endocrinol. 1999;114:269ā78.
Bertschinger H, Sills ES. Contraceptive applications of GnRH-analogs and vaccines for wildlife mammals of southern Africa: current experience and future challenges. In: Sills EC, editor. Gonadotropin-releasing hormone (GnRH): production, structure and function. 1st ed. New York: Nova Science; 2013. p. 85ā108.
Bertschinger HJ, Lueders I. Use of anti-gonadotropin-releasing hormone vaccines in African elephants (Loxodonta africana): a review. Bothalia. 2018;48:a2320.
Bertschinger HJ, Delsink A, van Altena JJ, Kirkpatrick JF. Porcine zona pellucida vaccine immunocontraception of African elephant (Loxodonta africana). A review of 22 years of research. Bothalia Afr Biodivers Conserv. 2018;48(2):a2324.
Boedeker NC, Hayek LC, Murray S, de Avila DM, Brown JL. Effects of a gonadotropin-releasing hormone vaccine on ovarian cyclicity and uterine morphology of an Asian elephant (Elephas maximus). J Zoo Wildl Med. 2012;43:603ā14.
Brown JL. Reproductive endocrine monitoring of elephants: an essential tool for assisting captive management. Zoo Biol. 2000;19:347ā67.
Brown JL. Reproductive endocrinology. In: Fowler ME, Mikota SK, editors. Biology, medicine and surgery of elephants. Ames: Blackwell; 2006. p. 377ā88.
Brown JL. Comparative reproductive biology of elephants. In: Holt WV, Brown JL, Comizzoli P, editors. Reproductive sciences in animal conservationāprogress and prospects, Advances in experimental medicine and biology. New York: Springer; 2014. p. 135ā69.
Brown JL, Lehnhardt J. Serum and urinary hormones during pregnancy and the peri- and postpartum period in an Asian elephant (Elephas maximus). Zoo Biol. 1995;14:555ā64.
Brown JL, Citino SB, Bush M, Lehnhardt J, Phillips LG. Cyclic patterns of luteinizing hormone, follicle stimulating hormone, inhibin, and progesterone in the Asian elephant (Elephas maximus). J Zoo Wildl Med. 1991;22:49ā57.
Brown JL, Schmitt DL, Bellem A, Graham LH, Lehnhardt J. Hormone secretion in the Asian elephant (Elephas maximus): characterization of ovulatory and anovulatory luteinizing hormone surges. Biol Reprod. 1999;61:1294ā9.
Brown JL, Walker SL, Moeller T. Comparative endocrinology of cycling and noncycling Asian (Elephas maximus) and African (Loxodonta africana) elephants. Gen Comp Endocrinol. 2004a;136:360ā70.
Brown JL, Goritz F, Pratt-Hawkes N, Hermes R, Galloway M, Graham LH, Gray C, Walker SL, Gomez A, Moreland R, Murray S, Schmitt DL, Howard J, Lehnhardt J, Beck B, Bellem A, Montali R, Hildebrandt TB. Successful artificial insemination of an Asian elephant at the National Zoological Park. Zoo Biol. 2004b;23:45ā63.
Brown JL, Paris S, Prado-Oviedo NA, Meehan C, Hogan J, Carlstead K. Reproductive health assessment of female elephants in North American zoos and association of husbandry practices with reproductive dysfunction in African elephants (Loxodonta africana). PLoS One. 2016;11(7):e0145673.
Calogero AE, Badgy G, DāAgata R. Mechanisms of stress on reproductionāevidence for a complex intra-hypothalamic circuit. Ann N Y Acad Sci. 1998;1:364ā70.
Carlstead K. A comparative approach to the study of keeper-animal relationships in the zoo. Zoo Biol. 2009;8:589ā608.
Castracane VD, Stewart DR, Gimpel T, Overstreet JW, Lasley BL. Maternal serum androgens in human pregnancy: early increases within the cycle of conception. Hum Reprod. 1998;13:460ā4.
Chase MJ, Schlossberg S, Griffin CR, Bouche PJC, Djene SW, Elkan PW, Ferreira S, Grossman F, Kohi EM, Landen K, Omondi P, Peltier A, Selier SAJ, Sutcliffe R. Continent-wide survey reveals massive decline in African savannah elephants. PeerJ. 2016;4:e2354.
Che-Castaldo JP, Grow SA, Faust LJ. Evaluating the contribution of North American zoos and aquariums to endangered species recovery. Sci Rep. 2018;8:9789.
Clubb R, Rowcliffe M, Lee P, Mar KU, Moss C, Mason GF. Fecundity and population viability in female zoo elephants: problems and possible solutions. Anim Welfare. 2009;18:237ā47.
Cocchi D, Locatelli V, Carminati R, Muller EE. Mechanisms underlying the prolactin-lowering effect of metergoline in the rat. Life Sci. 1978;23:927ā36.
Conde DA, Flesness N, Colchero F, Jones OR, Scheuerlein A. An emerging role of zoos to conservation biodiversity. Science. 2011;331:1390ā1.
Creel S, MacDonald D. Sociality, group size, and reproductive suppression among carnivores. Adv Study Behav. 1995;24:203ā57.
Czekala NM, MacDonald EA, Steinman K, Walker S, Garrigues NW II, Olson D, Brown JL. Estrogen and LH dynamics during the follicular phase of the estrous cycle in the Asian elephant. Zoo Biol. 2003;22:443ā54.
Dale RH. Birth statistics for African (Loxodonta africana) and Asian (Elephas maximus) elephants in human care: history and implications for elephant welfare. Zoo Biol. 2010;29:87ā103.
de Silva S, Webber CE, Weerathunga US, Pushpakumara TV, Weerakoon DK, Wittemyer G. Demographic variables for wild Asian elephants using longitudinal observations. PLoS One. 2013;8(12):e82788.
Delsink AK, Kirkpatrick JF. Free-ranging African elephant immunocontraception. A new paradigm for elephant management. Cape Town: Trident Press; 2012. p. 36.
Delsink AK, van Altena JJ, Kirkpatrick J, Grobler D, Fayrer-Hosken RA. Field applications of immunocontraception in African elephants (Loxodonta africana). Reprod Suppl. 2002;60:117ā24.
Delsink AK, van Altena JJ, Kirkpatrick J, Grobler D, Bertschinger H, Kirkpatrick J, Slotow R. Regulation of a small, discrete African elephant population through immunocontraception in the Makalali conservancy, Limpopo, South Africa. South Afr J Sci. 2006;102:403ā5.
Delsink AK, van Altena JJ, Grobler D, Bertschinger HJ, Kirkpatrick JF, Slotow R. Implementing immunocontraception in free-ranging African elephants at Makalali conservancy. J S Afr Vet Assoc. 2007;78:25ā30.
Delsink AK, Kirkpatrick J, van Altena JJ, Bertschinger HJ, Ferreira SM, Slotow R. Lack of spatial and behavioral responses to immunocontraception application in African elephants (Loxodonta africana). J Zoo Wildl Med. 2013;44:52ā74.
Dow TL, Brown JL. Evidence that hyperprolactinemia is associated with ovarian acyclicity in female zoo African elephants (Loxondonta africana). Reprod Fertil Dev. 2012;24:1019ā27.
Dow TL, Holaskova I, Brown JL. Results of the third reproductive assessment survey of North American Asian (Elephas maximus) and African (Loxodonta africana) female elephants. Zoo Biol. 2011a;30:699ā711.
Dow TL, Roudebush W, Parker FN, Brown JL. Influence of age and gender on secretion of anti-MĆ¼llerian hormone in Asian (Elephas maximus) and African (Loxodonta africana) elephants. Theriogenology. 2011b;75:620ā7.
Drews B, Hermes R, Gƶritz F, Gray C, Kurz J, Lueders I, Hildebrandt TB. Early embryo development in the elephant assessed by serial ultrasound examinations. Theriogenology. 2008;69:1120ā8.
Duer C, Carden M, Schmitt D, Tomasi T. Utility of maternal serum testosterone analysis for fetal gender determination in Asian elephants (Elephas maximus). Anim Reprod Sci. 2002;69:47ā52.
Edwards KL, Trotter J, Jones M, Brown JL, Steinmetz HW, Walker SL. Investigating temporary acyclicity in a captive group of Asian elephants (Elephas maximus): relationship between management, adrenal activity and social factors. Gen Comp Endocrinol. 2016;225:104ā16.
Edwards KL, Edes A, Brown JL. Stress, well-being and reproductive success. In: Holt WV, Brown JL, Comizzoli P, editors. Reproductive sciences in animal conservationāprogress and prospects, Advances in experimental medicine and biology. 2nd ed. New York: Springer; this volume.
Emiliano ABF, Fudge JL. From galactorrhea to osteopenia: rethinking serotonin-prolactin interactions. Neuropsychopharmacology. 2004;29:833ā46.
Fanson KV, Keeley T, Fanson BG. Cyclic changes in cortisol across the estrous cycle in parous and nulliparous Asian elephants. Endocr Connect. 2014;3:57ā66.
Faust L, Marti K. Technical report on zoo risk modeling of the North American Asian elephant population, AZA TAG/SSP. Chicago: Lincoln Park Zoo; 2011a.
Faust L, Marti K. Technical report on zoo risk modeling of the North American African elephant population, AZA TAG/SSP. Chicago: Lincoln Park Zoo; 2011b.
Fayrer-Hosken RA, Bertschinger HJ, Kirkpatrick JF, Grobler D, Lamberski N, Honneyman G, Ulrich T. Contraceptive potential of the porcine zona pellucidavaccine in the African elephant (Loxodonta africana). Theriogenology. 1999;52:835ā46.
Ferrari C, Caldara R, Rampini P, Telloli P, Romussi M, Bertazzoni A, Polloni G, Mattei A, Crosignani PG. Inhibition of prolactin release by serotonin antagonists in hyperprolactinemic subjects. Metabolism. 1978;127:1499ā504.
Florio P, Gabbanini M, Borges LE, Bonaccorsi L, Pinzauti S, Reis FM, Boy Torres P, Rago G, Litta P, Petraglia F. Activins and related proteins in the establishment of pregnancy. Reprod Sci. 2010;17:320ā30.
Forsyth IA, Wallis M. Growth hormone and prolactināmolecular and functional evolution. J Mammary Gland Biol Neoplasia. 2002;7:291ā312.
Frasor J, Gibori G. Prolactin regulation of estrogen receptor expression. Trends Endocrinol Metab. 2003;14:118ā23.
Freeman ME, Kanyicska B, Lerant A, Nagy G. Prolactin: structure, function and regulation of secretion. Physiol Rev. 2000;80:1524ā631.
Freeman EW, Weiss E, Brown JL. Examination of the interrelationships of behavior, dominance status, and ovarian activity in captive Asian and African elephants. Zoo Biol. 2004;23:431ā48.
Freeman EW, Whyte I, Brown JL. Reproductive evaluation of elephants culled in Kruger National Park, South Africa between 1976 and 1995. Afr J Ecol. 2008;47:192ā201.
Freeman EW, Guagnano G, Olson D, Keele M, Brown JL. Social factors influence ovarian acyclicity in captive African elephants (Loxodonta africana). Zoo Biol. 2009;28:1ā15.
Freeman EW, Schulte BA, Brown JL. Investigating the impact of rank and ovarian activity on the social behavior of captive female African elephants. Zoo Biol. 2010;29:154ā67.
Freeman EW, Meyer JM, Putman S, Schulte BA, Brown JL. Using a simplified field progestagen method to assess ovarian activity in female African elephants. Biol Conserv. 2011;44:2105ā11.
Freeman EW, Meyer JM, Putman S, Schulte BA, Brown JL. Ovarian cycle status varies with respect to age and social status in free-ranging elephants in Addo Elephant National Park, South Africa. Cons Physiol. 2013;1:cot025.
Glaeser SS, Hunt KE, Martin MS, Finnegan M, Brown JL. Investigation of individual and group variability in estrous cycle characteristics in female Asian elephants (Elephas maximus) at the Oregon Zoo. Theriogenology. 2012;78:285ā96.
Grattan DR, Kokay IC. Prolactin: a pleiotropic neuroendocrine hormone. J Neuroendocrinol. 2008;20:752ā63.
Grynnerup AG, Lindhard A, Sorensen S. The role of anti-MĆ¼llerian hormone in female fertility and infertilityāan overview. Acta Obstet Gynecol Scand. 2012;91:1252ā60.
Harris M, Sherwin C, Harris S. The welfare, housing and husbandry of elephants in UK zoos. Final report. Bristol: University of Bristol; 2008.
Hartley M, Stanley CR. Survey of reproduction and calf rearing in Asian and African elephants in European zoos. J Zoo Aquar Res. 2016;4:139ā46.
Hayward AD, Mar KU, Lahdenpera M, Lummaa V. Early reproductive investment, senescence and lifetime reproductive success in female Asian elephants. J Evol Biol. 2014;27:7772ā83.
Hermes R, Olson D, Gƶritz F, Brown JL, Schmitt DL, Hagan D, Peterson JS, Fritsch G, Hildebrandt TB. Ultrasonography of the estrous cycle of female African elephants (Loxodonta africana). Zoo Biol. 2000;19:369ā82.
Hermes R, Hildebrandt TB, Gƶritz F. Reproductive problems directly attributable to long-term captivity: asymmetric reproductive aging. Anim Reprod Sci. 2004;82ā83:49ā60.
Hermes R, Sargusty J, Schaftenaar W, Goeritz F, Schmitt DL, Hildebrandt TB. Obstetrics in elephants. Theriogenology. 2008;70:131ā44.
Hermes R, Behr B, Hildebrandt TB, Blottner S, Sieg B, Frenzel A, Knieriem A, Saragusty J, Rath D. Sperm sex-sorting in the Asian elephant (Elephas maximus). Anim Reprod Sci. 2009;112:390ā6.
Hermes R, Saragusty J, Gƶritz F, Bartels P, Potier R, Baker B, Streich JW, Hildebrandt TB. Freezing African elephant semen as a new population management tool. PLoS One. 2013;8:e57616.
Hildebrandt TB, Gƶritz F, Hermes R, Reid C, Dehnhard M, Brown JL. Aspects of the reproductive biology and breeding management of Asian and African elephants. Int Zoo Yearb. 2006;40:20ā40.
Hildebrandt TB, Lueders I, Hermes R, Gƶritz F, Sargusty J. Reproductive cycle of the elephant. Anim Reprod Sci. 2011;124:176ā83.
Hildebrandt TB, Hermes R, Saragusty J, Potier R, Schwammer HM, Balfanz F, Vielgrader H, Baker B, Bartels P, Gƶritz F. Enriching the captive elephant population genetic pool through artificial insemination with frozen-thawed semen collected in the wild. Theriogenology. 2012;78:1398ā404.
Holdgate MR, Meehan CL, Hogan JN, Miller LJ, Soltis J, Andrews J, Shepherdson DJ. Walking behavior of zoo elephants: associations between GPS-measured daily walking distances and environmental factors, social factors, and welfare indicators. PLoS One. 2016;11(7):e0150331.
Hufenus R, Schiffmann C, Hatt JM, Muller DWH, Lackey LB, Clauss M, Zerbe P. Seasonality of reproduction in Asian elephants Elephas maximus and African elephants Loxodonta africana: underlying photoperiodic cueing? Mammal Rev. 2018;48:261ā76.
Illera JC, SilvĆ”n G, CĆ”ceres S, Carbonell MD, Gerique C, Martinez-FernĆ”ndez L, Munro C, Cesares M. Assessment of ovarian cycles in the African elephant (Loxodonta africana) by measurement of salivary progesterone metabolites. Zoo Biol. 2014;33:245ā9.
IUCN Red List of Threatened Species. 2018. Version 2018-2. www.iucnredlist.org.
Jorgensen HS. Studies on the neuroendocrine role of serotonin. Dan Med J. 2007;54:266ā88.
Jungheim ES, Moley KH. Current knowledge of obesityās effects in the pre- and periconceptional periods and avenues for future research. Am J Obstet Gynecol. 2010;203:525ā30.
Kaewmanee S, Watanabe G, Kishimoto M, Zhu Jin W, Yamamoto Y, Yamamoto T, Nagaoka K, Narushima E, Komiya T, Taya K. Secretion of inhibin during the estrous cycle in the female Asian elephant (Elephas maximus). J Vet Med Sci. 2011;73:77ā82.
Kajaysri J, Nokkaew W. Assessment of pregnancy status of Asian elephants (Elephas maximus) by measurement of progestagen and glucocorticoid and their metabolite concentrations in serum and feces, using enzyme immunoassay (EIA). J Vet Med Sci. 2013;76:363ā8.
Kaplowitz PB. Link between body fat and the timing of puberty. Pediatrics. 2008;121:S208ā17.
Kapustin N, Critser JK, Olson D, Malven PV. Nonluteal estrous cycles of 3-week duration are initiated by anovulatory luteinizing hormone peaks in African elephants. Biol Reprod. 1996;55:1147ā54.
Keele M, Lewis K, Owens T. Asian elephant (Elephas maximus) North American Regional Studbook. Portland: Oregon Zoo; 2014.
Kirkpatrick JF, Turner JW Jr, Liu IK, Fayrer-Hosken R. Applications of pig zona pellucida immunocontraception to wildlife fertility control. J Reprod Fertil Suppl. 1996;50:183ā9.
Kiso W, Brown JL, Siewerdt SDL, Olson D, Crichton EG, Pukazhenthi BS. Liquid semen storage in elephants (Elephas maximus and Loxodonta africana): species differences and storage optimization. J Androl. 2011;21:420ā31.
Kiso WK, Asano A, Travis AJ, Schmitt DL, Brown JL, Pukazhenthi BS. Pretreatment of Asian elephant (Elephas maximus) spermatozoa with cholesterol-loaded cyclodextrins and glycerol addition at 4Ā°C improves cryosurvival. Reprod Fertil Dev. 2012;24:1134ā42.
Kiso WK, Selvaraj V, Nagashima J, Asano A, Brown JL, Schmitt DL, Leszyk J, Travis AJ, Pukazhenthi BS. Lactotransferrin in Asian elephant (Elephas maximus) seminal plasma correlates with semen quality. PLoS One. 2013;8:e71033.
Kiso W, Wiedner E, Isaza R, Lindsay W, Aria J, Jacobson G, Jacobson K, Schmitt S. Reproductive parameters and birth statistics for a herd of Asian elephants (Elephas maximus) in North America over a 20-year period. J Zoo Wildl Med. 2017;48:987ā97.
Knight PG. Roles of inhibins, activins, and follistatin in the female reproductive system. Front Neuroendocrinol. 1996;17:476ā509.
LahdenperƤ M, Mar KU, Lummaa V. Reproductive cessation and post-reproductive lifespan in Asian elephants and pre-industrial humans. Front Zool. 2014;11:54ā68.
LahdenperƤ M, Mar KU, Lummaa V. Nearby grandmother enhances calf survival and reproduction in Asian elephants. Sci Rep. 2016;6:27213.
Lamberts SWJ, Macleod RM. Regulation of prolactin secretion at the level of the lactotroph. Physiol Rev. 1990;70:279ā98.
Lee PC, Fishlock V, Webber CE, Moss CJ. The reproductive advantages of a long life: longevity and senescence in wild female African elephants. Behav Ecol Sociobiol. 2016;70:337ā45.
Lueders I, Niemuller C, Gray C, Rich P, Hildebrandt TB. Luteogenesis during the estrous cycle in Asian elephants (Elephas maximus). Reproduction. 2010;140:777ā86.
Lueders I, Taya K, Watanabe G, Yamamoto Y, Yamamoto T, Kaewmanee S, Niemuller C, Gray C, Streich W, Hildebrandt TB. Role of the double luteinizing hormone peak, luteinizing follicles, and the secretion of inhibin for dominant follicle selection in Asian elephants (Elephas maximus). Biol Reprod. 2011;85:714ā20.
Lueders I, Niemuller C, Rich P, Gray C, Hermes R, Gƶritz F, Hildebrandt TB. Gestation for 22 months: luteal development and pregnancy maintenance in elephants. Proc R Soc B. 2012;279:3687ā96.
Lueders I, Hildebrandt T, Gray C, Botha S, Rich P, Niemuller C. Suppression of testicular function in a male Asian elephant (Elephas maximus) treated with gonadotropin-releasing hormone vaccines. J Zoo Wildl Med. 2014;45:611ā9.
Lueders I, Young D, Maree L, van der Horst G, Luther I, Botha S, Tindall B, Fosgate G, Ganswindt A, Bertschinger HJ. Effects of GnRH vaccination in wild and captive African elephant bulls (Loxodonta africana) on reproductive organs and semen quality. PLoS One. 2017;12:e0178270.
Lueders I, Niemuller C, Steinmetz HW, Bouts T, Gray C, Knauf-Witzens T, Taya K, Watanabe G, Yamamoto Y, Oerke AK. Prolonged luteal lifespan and pseudopregnancy in Asian elephants (Elephas maximus). Anim Reprod Sci. 2018;197:58ā66.
Mar KU. The demography and life-history strategies of timber elephants in Myanmar. PhD thesis. London: University College; 2007.
Mar KU, Lahdenpera M, Lummaa V. Causes and correlates of calf mortality in captive Asian elephants (Elephas maximus). PLoS One. 2012;7(3):e32335.
Mason GJ, Veasey JS. What do population-level welfare indices suggest about the well-being of zoo elephants? Zoo Biol. 2010;29:256ā73.
Melmed S. Mechanisms for pituitary tumorigenesis: the plastic pituitary. J Clin Invest. 2003;112:1603ā18.
Mellen JD. Factors influencing reproductive success in small captive exotic felids (Felis spp.): a multiple regression analysis. Zoo Biol. 2005;10:95ā110.
Mendis S, Jayasekera NK, Rajapakse RC, Brown JL. Endocrine correlates of puberty in female Asian elephants (Elephas maximus) at the Pinnawala Elephant Orphanage, Sri Lanka. BMC Zool. 2017;2:1. https://doi.org/10.1186/s40850-016-0012-8.
Meyer JM, Walker SL, Freeman EW, Steinetz BG, Brown JL. Species and fetal gender effects on the endocrinology of pregnancy in elephants. Gen Comp Endocrinol. 2004;138:263ā70.
Miller PB, Forstein DA, Styles S. Effect of short-term diet and exercise on hormone levels and menses in obese, infertile women. J Reprod Med. 2008;53:315ā9.
Morfeld KA, Brown JL. High body condition scores and elevated insulin and leptin are associated with ovarian acyclicity in zoo African elephants (Loxodonta africana). Reprod Fertil Dev. 2014;28:640ā7.
Morfeld K, Brown JL. Metabolic health assessment of zoo elephants: management factors predicting leptin levels and the glucose-to-insulin ratio and their associations with health parameters. PLoS One. 2017;12(11):e0188701.
Morfeld KA, Ball RL, Brown JL. Recurrence of hyperprolactinemia and continuation of ovarian acyclicity in captive African elephants (Loxodonta africana) treated with cabergoline. J Zoo Wildl Med. 2014;45:569ā76.
Morfeld KA, Meehan C, Hogan J, Brown JL. Assessment of body condition in African (Loxodonta africana) and Asian (Elephas maximus) elephants in North American zoos and management practices associated with high body condition scores. PLoS One. 2016;11(7):e0155146.
Mouttham L, Buhr M, Brown JL. Ovarian acyclicity and dominance status of African elephants in zoos is not associated with increased serum testosterone production. Zoo Biol. 2011;126:115ā21.
Mumby HS, Mar KU, Thitaram C, Courtiol A, Towiboon P, Min-Oo Z, Htut-Aung Y, Brown JL, Lummaa V. Stress and body condition are associated with climate and demography in Asian elephants. Conserv Physiol. 2015; https://doi.org/10.1093/conphys/cov030.
Niemuller CA, Gray C, Cummings E, Liptrap RM. Plasma concentrations of immunoreactive relaxin activity and progesterone in the pregnant Asian elephant (Elephas maximus). Anim Reprod Sci. 1998;53:119ā31.
Nilsson EM, Fainberg HP, Choong SS, Giles TC, Sells J, May S, Stansfield FJ, Allen WR, Emes RD, Mostyn A, Mongan NP, Yon L. Molecular characterization of adipose tissue in the African elephant (Loxodonta africana). PLoS One. 2014;9(3):e91717.
Norkaew T, Brown JL, Bansiddhi P, Somgird C, Thitaram C, Punyapornwithaya V, Punturee KK, Vongchan P, Nopphamas S, Khonmee J. Body condition and adrenal glucocorticoid activity affects metabolic marker and lipid profiles in working female tourist elephants in Thailand. PLoS One. 2018;13(10):e0204965.
Olive A, Jansen K. The contribution of zoos and aquaria to Aichi Biodiversity Target 12: a case study of Canadian Zoos. Glob Ecol Conserv. 2017;10:103ā13.
Olson D. North American Region Studbook for the African elephant (Loxodonta africana). Azle: International Elephant Foundation; 2014. p. 1ā71.
Prado NA, Keady M, Oestmann A, Steinbeiser C, Brown JL. Hyperprolactinemic African elephant (Loxodonta africana) females exhibit elevated dopamine, oxytocin and serotonin concentrations compared to normal cycling and non-cycling, low prolactin elephants. Biol Reprod. 2019a;100:1549ā60.
Prado NA, Paris SW, Brown JL. Prolonged ovarian acyclicity is associated with a higher likelihood of developing hyperprolactinemia in captive female African elephants (Loxodonta africana). Zoo Biol. 2019b; https://doi.org/10.1002/zoo.21464.
Prado-Oviedo NA. Hyperprolactinemia and ovarian acyclicity in captive African elephant females (Loxodonta africana). George Mason University, College of Science Archival Resources; 2015.
Prado-Oviedo NA, Mallow EJ, Deng X, Brown JL. Hyperprolactinemia is not associated with hyperestrogenism in noncycling African elephants (Loxodonta africana). Gen Comp Endocrinol. 2013;89C:7ā14.
Pushpakumara PGA, Rajapakse RC, Perera BMAO, Brown JL. Reproductive performance of the largest captive Asian elephant (Elephas maximus) population in Sri Lanka. Anim Reprod Sci. 2016;174:93ā9.
Richard P, Moos F, Freund-Mercier MJ. Central effects of oxytocin. Physiol Rev. 1991;71:331ā55.
Rico C, Fabre S, Medigue C, di Clemente N, Clement F, Bontoux M, Touze JL, Dupont M, Briant E, Remy B, Beckers JF, Monniaux D. Anti-MĆ¼llerian hormone is an endocrine marker of ovarian gonadotropin-responsive follicles and can help to predict superovulatory responses in the cow. Biol Reprod. 2009;80:50ā9.
Robinson MR, Mar KU, Lummaa V. Senescence and age-specific trade-offs between reproduction and survival in female Asian elephants. Ecol Lett. 2012;15:260ā6.
Saragusty J, Hermes R, Gƶritz F, Schmitt DL, Hildebrandt TB. Skewed birth sex ratio and premature mortality in elephants. Anim Reprod Sci. 2009;115:247ā54.
Sarkar DK, Gottschall PE, Meites J. Decline of tuberoinfundibular dopaminergic function resulting from chronic hyperprolactinemia in rats. Endocrinology. 1984;115:1269ā74.
Sarkar DK, Frautschy SA, Mitsugi N. Pituitary portal plasma levels of oxytocin during the estrous cycle, lactation and hyperprolactinemia. Ann N Y Acad Sci. 1992;652:397ā410.
Schiffmann C, Clauss M, Fernando P, Pastorini J, Wendler P, Ertl N, Hoby S, Hatt JM. Body condition scores of European zoo elephants (Elephas maximus and Loxodonta africana): status quo and influencing factors. J Zoo Aquar Res. 2018;6:91ā103.
Schuff KG, Hentges ST, Kelly MA, Binart N, Kelly PA, Iuvone PM, Asa SL, Low MJ. Lack of prolactin receptor signaling in mice results in lactotroph proliferation and prolactinomas by dopamine dependent and independent mechanisms. J Clin Invest. 2002;110:973ā81.
Schulte BA, Feldman E, Lambert R, Oliver R, Hess DL. Temporary ovarian inactivity in elephants: relationship to status and time outside. Physiol Behav. 2000;71:123ā31.
Serri O, Chik CL, Ur E, Ezzat S. Diagnosis and management of hyperprolactinemia. Can Med Assoc J. 2003;169:575ā81.
Sobrinho LG. Prolactin, psychological stress and environment in humans: adaptation and maladaptation. Pituitary. 2003;6:35ā9.
Sobrinho LG, Nunes MCP, Calhaz-Jorge C, Afonso AM, Pereira MC, Santos MA. Hyperprolactinemia in women with paternal deprivation during childhood. Obstet Gynecol. 1984;64:465ā8.
Somgird C, Homkong P, Sripiboon S, Brown JL, Stout TA, Colenbrander B, Mahasawangkul S, Thitaram C. Potential of a gonadotropin-releasing hormone vaccine to suppress musth in captive male Asian elephants (Elephas maximus). Anim Reprod Sci. 2016;164:111ā20.
Sonino N, Navarrini C, Ruini C, Fallo F, Boscaro M, Fava GA. Life events in the pathogenesis of hyperprolactinemia. Eur J Endocrinol. 2004;151:61ā5.
Squires EL, Ginther OJ. Follicular and luteal development in pregnant mares. J Reprod Fertil Suppl. 1975;23:429ā33.
Stansfield FJ, Allen WR. Luteal maintenance of pregnancy in the African elephant (Loxodonta africana). Reproduction. 2012;143:845ā54.
Sukumar R, editor. The living elephants: evolution, ecology, behavior and conservation. Oxford: Oxford University Press; 2003. p. 478.
Tabak J, Gonzalez-Iglesias AE, Toporikova N, Bertram R, Freeman ME. Variations in the response of pituitary lactotrophs to oxytocin during the rat estrous cycle. Neuroendocrinology. 2010;151:1806ā13.
Takahashi T. Biology of the prolactin family in bovine placenta. I. Bovine placental lactogen: expression, structure and proposed roles. Anim Sci J. 2006;77:10ā7.
Thitaram C. Breeding management of captive Asian elephant (Elephas maximus) in range countries and zoos. Jpn J Zoo Wildl Med. 2012;17:91ā6.
Thitaram C, Brown JL. Control and monitoring of ovarian function in elephants. Theriogenology. 2018;109:42ā7.
Thitaram C, Brown JL, Pongsopawijit P, Chansitthiwet S, Wongkalasin W, Daram P, Roongsri R, Kulmapijit A, Mahasawangkul S, Rojanasathien S, Colenbrander B, van der Weijden GC, van Eerdenburg FJCM. Seasonal effects on the endocrine pattern of the semi-captive female Asian elephant (Elephas maximus): timing of the luteinizing hormone surge determines the length of the estrous cycle. Theriogenology. 2008;69:237ā44.
Thitaram C, Pongsopawijit P, Chansitthiwet S, Brown JL, Nimtragul N, Boonprasert K, Homkong P, Mahasawangkul S, Rojanasthien S, Colenbrander B, van der Weijden GC, van Eerdenburg FJ. Induction of the ovulatory LH surge in Asian elephants (Elephas maximus): a novel aid in captive breeding management of an endangered species. Reprod Fertil Dev. 2009;21:672ā8.
Thongtip N, Mahasawangkul S, Thitaram C, Pongsopavijitr P, Kornkaewrat K, Pinyopummin A, Angkawanish T, Jansittiwate S, Rungsri R, Boonprasert K, Songkalasin W, Homkong P, Dejchaisri S, Wajjwalku W, Saikhun K. Successful artificial insemination in the Asian elephant (Elephas maximus) using chilled and frozen-thawed semen. Reprod Biol Endocrinol. 2009;7:75ā81.
Urwin VE, Allen WR. Pituitary and chorionic gonadotrophin control of ovarian function during early pregnancy in equids. J Reprod Fertil Suppl. 1982;32:371ā82.
Valades G, Ganswindt A, Annandale H, Schulman M, Bertschinger H. Non-invasive assessment of the reproductive cycle in free-ranging female African elephants (Loxodonta africana) treated with a gonadotropin-releasing hormone (GnRH) vaccine for inducing anoestrus. Reprod Biol Endocrinol. 2012;10:63.
Verhelst J, Abs R, Maiter D, van den Bruel A, Vandeweghe M, Velkeniers B, Mockel J, Lamberigts G, Petrossians P, Coremans P, Mahler C, Stevenaert A, Verlooy J, Raftopoulos C, Beckers A. Cabergoline in the treatment of hyperprolactinemia: a study in 455 patients. J Clin Endocrinol Metab. 1999;84:2518ā22.
Vick MM, Sessions DR, Murphy BA, Kennedy EL, Reedy SE, Fitzgerald BP. Obesity is associated with altered metabolic and reproductive activity in the mare: effects of metformin on insulin sensitivity and reproductive cyclicity. Reprod Fertil Dev. 2006;18:609ā17.
Wang AT, Mullan RJ, Lane MA, Hazem A, Prasad C, Gathaiya NW, Fernandez-Balsells MM, Bagatto A, Coto-Yglesias F, Carey J, Elraiyah TA, Erwin PJ, Gandhi GY, montori VM, Murad MH. Treatment of hyperprolactinemia: a systematic review and meta-analysis. Syst Rev. 2012; https://doi.org/10.1186/2046-4053-1-33.
Wasser SL, Barash DP. Reproductive suppression among female mammals: implications for biomedicine and sexual selection theory. Q Rev Biol. 1983;58:513ā38.
Wasser SL, Papageorge S, Foley C, Brown JL. Excretory fate of estradiol and progesterone in the African elephant (Loxodonta africana) and pattern of fecal steroid concentrations throughout the estrous cycle. Gen Comp Endocrinol. 1996;102:255ā62.
Weissenbock NM, Schwammer HM, Ruf T. Estrous synchrony in a group of African elephants (Loxodonta africana) under human care. Anim Reprod Sci. 2009;113:322ā7.
Wielebnowski N. Contribution of behavioral studies to captive management and breeding of rare and endangered animals. In: Caro T, editor. Behavioral ecology and conservation biology. New York: Oxford University Press; 1998. p. 130ā62.
Wielebnowski NC, Fletchall N, Carlstead K, Busso JM, Brown JL. Non-invasive assessment of adrenal activity associated with husbandry and behavioral factors in the North American clouded leopard population. Zoo Biol. 2002a;21:77ā98.
Wielebnowski NC, Ziegler K, Wildt DE, Lukas J, Brown JL. Impact of social management on reproductive, adrenal and behavioural activity in the cheetah (Acinonyx jubatus). Anim Conserv. 2002b;5:291ā301.
Wittemyer G, Northrup JM, Blanc J, Douglas-Hamilton I, Omondi P, Burnham KP. Illegal killing for ivory drives global decline in African elephants. Proc Natl Acad Sci. 2014;111(36):13117ā21.
Yamamoto Y, Yamamoto T, Watanabe G, Yuto N, Keio M, Narushima E, Katayanagi M, Nakao R, Morikubo S, Sakurai Y, Kaneko M, Kaewmanee S, Taya K. Prolactin secretion and ovarian function in cycling and non-cycling African female elephants (Loxodonta africana). J Vet Med Sci. 2010;72:845ā52.
Yamamoto Y, Yamamoto T, Taya K, Watanabe G, Stansfield FJ, Allen WR. Placentation in the African elephant (Loxodonta africana). V. The trophoblast secretes placental lactogen. Placenta. 2011;32:506ā10.
Yamamoto Y, Yuto N, Yamamoto T, Kaewmanee S, Shiina O, Mouri Y, Narushima E, Katayanagi M, Sugimura K, Nagaoka K, Watanabe G, Taya K. Secretory pattern of inhibin during the estrous cycle and pregnancy in African (Loxodonta africana) and Asian (Elephas maximus) elephants. Zoo Biol. 2012a;31:511ā22.
Yamamoto Y, Yamamoto T, Yuto N, Hildebrandt TB, Lueders I, Wibbelt G, Shiina O, Mouri Y, Sugimura K, Sakamoto S, Kaewmanee S, Nagoaka K, Watanabe G, Taya K. The secretory pattern and source of immunoreactive prolactin in pregnant African (Loxodonta africana) and Asian (Elephas maximus) elephants. J Reprod Dev. 2012b;58:105ā11.
Yamamoto Y, Nagaoka K, Kamite Y, Watanabe G, Allen T, Stansfield F, Taya K. Different origins of two corpora lutea recovered from a pregnant African elephant (Loxodonta africana). Reprod Domest Anim. 2017;52(6):1138ā41.
Yuen BH. Hyperprolactinemia in women of reproductive age: etiology, diagnosis and management. Can Fam Physician. 1992;38:367ā79.
Zacur HA. Hyperprolactinemia. In: Knobil E, Neill J, editors. Encyclopedia of reproduction, vol. 2. New York: Academic Press; 1998. p. 725ā35.
Acknowledgments
We thank all of the technical, veterinary, zoo and research staff who contributed to the reproductive work described herein, and all participating elephants. This work was funded or supplied with in-kind donations by the Abbott Fund, Anela Kolohe Foundation, AZA Conservation Endowment Fund, Friends of the National Zoo, Institute of Museum and Library Services, International Elephant Foundation, Morris Animal Foundation, Pfizer Corporation, Siemens Medical Solutions Diagnostics, Shared Earth Foundation, Smithsonian Competitive Grants Program, Smithsonian Scholar Studies Program, Smithsonian Womenās Committee, Susan Fulton and FBB Capital Partners, and the Wolcott Fund.
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Brown, J.L. (2019). Update on Comparative Biology of Elephants: Factors Affecting Reproduction, Health and Welfare. In: Comizzoli, P., Brown, J., Holt, W. (eds) Reproductive Sciences in Animal Conservation. Advances in Experimental Medicine and Biology, vol 1200. Springer, Cham. https://doi.org/10.1007/978-3-030-23633-5_9
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