Ovulation, pregnancy, placentation and husbandry in the African elephant (Loxodonta africana)

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 361, Issue 1469, 2006, Pages 821-834

  Allen, W R ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

African elephant; Foetal gonads; Placenta; Progestagens

Indexed keywords

ANIMAL HUSBANDRY; ELEPHANT; POPULATION DENSITY; PREGNANCY;

AFRICA; BOTSWANA; SOUTH AFRICA; SOUTHERN AFRICA; SUB-SAHARAN AFRICA; ZIMBABWE;

LOXODONTA; LOXODONTA AFRICANA;

EID: 33845245395     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2006.1831     Document Type: Review

References (95)

1. Adams, C. E. 1982 Embryo transfer in rodents. In Mammalian egg transfer (ed. C. E. Adams), pp. 22-23. Boca Raton, FL: CRC Press.
2. Allen, W. R., Mathias, S. S., Wooding, F. B. P., Skidmore, J. A. & van Aarde, R. J. 2002a Placentation in the African elephant, Loxodonta africana. I. Endocrinological aspects. Reproduction 60, 105-116.
3. Allen, W. R., Wilsher, S., Stewart, F., Ousey, J. & Fowden, A. 2002b The influence of maternal size on placental, fetal and postnatal growth in the horse. II Endocrinology of pregnancy. J. Endocrinol. 172, 237-246. (doi:10.1677/joe. 0.1720237)
4. Allen, W. R., Mathias, S., Wooding, F. B. P. & van Aarde, R. J. 2003 Placentation in the African elephant (Loxodonta africana). II. Morphological changes in the uterus and placenta throughout gestation. Placenta 24, 598-617. (doi:10.1016/S0143-4004(03)00102-4)
5. Allen, W. R., Stout, S. & Ford, M. 2005 Placentation in the African elephant, Loxodonta africana. IV. Growth and organisation of the fetal gonads. Reproduction 130, 713-720. (doi:10.1530/rep.1.00696)
6. Amoroso, E. C. & Perry, J. S. 1964 The foetal membranes and placenta of the African elephant (Loxodonta africana). Proc. R. Soc. B 248, 1-34.
7. Amoroso, E. C. & Rowlands, I. W. 1951 Hormonal effects in the pregnant mare and foetal foal. J. Endocrinol. 7, 50-52.
8. 3H-dehydroisoandrosterone injected into the fetal circulation. Endocrinology 92, 657-666.
9. 3H-dehydroisoandrosterone injected into the fetal circulation. Endocrinology 92, 1397-1404.
10. 14C-androstenedione injected into the umbilical vein. Endocrinology 85, 1172-1179.
11. 3H-cholesterol injected into the fetal circulation. Endocrinology 89, 1152-1157.
12. Brannian, J. D., Griffin, F., Papkoff, H. & Terranova, P. F. 1988 Short and long phases of progesterone secretion during the oestrous cycle of the African elephant (Loxodonta africana). J. Reprod. Fertil. 84, 357-365.
13. Brown, J. L. 2000 Reproductive endocrine monitoring of elephants: an essential tool for assisting captive management. Zoo Biol. 19, 347-367. (doi:10.1002/1098-2361 (2000)19:5 〈347::AID-ZOO6〉 3.0.CO;2-V)
14. Brown, J. L. & Lehnhardt, J. 1995 Serum and urinary hormones during pregnancy and the peri- and postpartum period in an Asian elephant (Elephas maximus). Zoo Biol. 14, 555-564. (doi:10.1002/zoo.1430140608)
15. Brown, J. L., Citino, S. C., Bush, M., Lehnhardt, J. & Phillips, L. G. 1991 Cyclic patterns of luteinising hormone, follicle-stimulation hormone, inhibin, and progesterone secretion in the Asian elephant (Elephas maximus). J. Zoo Wildl. Med. 22, 49-57.
16. Buss, I. O. & Johnson, O. W. 1967 Relationships of Leydig cell characteristics and intratesticular testosterone levels to sexual activity in the African elephant. Anat. Rec. 157, 191-210. (doi:10.1002/ar.1091570210)
17. Buss, I. O. & Savidge, J. M. 1966 Change in population number and reproduction rates of elephants in Uganda. J. Wildl. Manage. 30, 791-799.
18. Buss, I. O. & Smith, N. R. 1966 Observations on reproduction and breeding behaviour of the African elephant. J. Wildl. Manage. 30, 375-387.
19. Cole, H. H., Hart, G. H., Lyons, W. R. & Catchpole, H. R. 1933 The development and hormonal content of fetal horse gonads. Anat. Rec. 56, 275-293. (doi:10.1002/ar.1090560308)
20. Cox, J. E. 1975 Oestrone and equilin in the plasma of the pregnant mare. J. Reprod. Fertil. 23, 463-468.
21. Craig, J. C. 1984 Foetalmass and date of conception in African elephants: a revised formula. Afr. J. Sci. 80, 512-516.
22. de Villiers, D. J., Skinner, J. D. & Hall-Martin, A. J. 1989 Circulating progesterone concentrations and ovarian functional anatomy in the African elephant (Loxodonta africana). J. Reprod. Fertil. 86, 195-201.
23. Diczfalusy, E. 1964 Endocrinological functions of the human foeto-placental unit. Fed. Proc. 23, 791-798.
24. Foggin, C. M. 2003 The elephant population problem in Zimbabwe: can there by any alternative to culling? In Managing African elephant populations: live or let die. Proc. First Int. Workshop on Control of Wild Elephant Populations, pp. 17-21. University of Utrecht, The Netherlands.
25. Gaeth, A. P., Short, R. V. & Renfree, M. B. 1999 The developing renal, reproductive, and respiratory systems of the African elephant suggest an aquatic ancestry. Proc. Natl Acad. Sci. USA 96, 5555-5558. (doi:10.1073/pnas.96. 10.5555)
26. Greyling, M. D., van Aarde, R. J. & Potgieter, H. C. 1997 Ligand specifity of uterine oestrogen and progesterone receptors in the subadult African elephant, Loxodonta africana. J. Reprod. Fertil. 109, 199-204.
27. Greyling, M. D., Ford, M., Potgieter, H. C. & van Aarde, R. J. 1998 Influence of gestation on uterine endometrial steroid receptor concentrations in the African elephant, Loxodonta africana. Biol. Reprod. 58, 60-64. (doi:10.1095/biolreprod58.1.60)
28. Hamon, M., Clarke, S. W., Houghton, E., Fowden, A. L., Silver, M., Rossdale, P. D., Ousey, J. C. & Heap, R. B. 1991 Production of 5α-dihydroprogesterone during late pregnancy in the mare. J. Reprod. Fertil. 44, 29-35.
29. Hanks, J. 1971 The reproductive physiology of the African elephant, Loxodonta africana. Ph.D. thesis, University of Cambridge.
30. Hanks, J. 1972 Reproduction of elephant, Loxodonta africana, in the Luangwa valley, Zambia. J. Reprod. Fertil. 30, 13-26.
31. Hanks, J. & Short, R. V. 1972 The formation and function of the corpus luteum in the African elephant (Loxodonta africana). J. Reprod. Fertil. 29, 79-89.
32. Hay, M. F. & Allen, W. R. 1975 An ultrastructural and histochemical study of the interstitial cells in the gonads of the fetal horse. J. Reprod. Fertil. 23, 557-561.
33. Heistermann, M., Trohorsch, B. & Hodges, J. K. 1997a Assessment of ovarian function in the African elephant (Loxodonta africana) by measurement of 5α-reduced progesterone metabolites in serum and urine. Zoo Biol 16, 273-284. (doi:10.1002/(SICI)1098-2361(1997)16:3 〈273::AID-ZOO7〉 3.0.CO;2-7)
34. Heistermann, M., Fieß, M. & Hodges, J. K. 1997b Patterns of excretion of faecal progesterone and 5α-reduced progestins during the ovarian cycle and early pregnancy in the African elephant (Loxodonta africana). J. Reprod. Fertil. 19, 57. (Abstract)
35. Hermes, R., Hildebrandt, T. B. & Goritz, F. 2004 Reproductive problems directly attributable to long term captivity-asymmetric reproductive ageing. Anim. Reprod. Sci. 82, 49-60. (doi:10.1016/j.anireprosci.2004.05.015)
36. Hildebrandt, T., Goritz, F., Pratt, N. C., Schmitt, D., Quandt, S., Raath, J. & Hopkins, D. T. 1998 Reproductive assessment of male elephants (Loxodonta africana and Elephas maximus) by ultrasonography. J. Zoo Wildl. Med. 29, 114-128.
37. Hildebrandt, T., Goritz, F., Pratt, N. C., Brown, J. L., Montali, R. J., Schmitt, D., Fritsch, G. & Hermes, R. 2000a Ultrasonography of the urogenital tract in elephants (Loxodonta africana and Elephas maximus): an important tool for assessing female reproductive function. Zoo Biol. 19, 321-332. (doi:10.1002/1098-2361(2000)19:5 〈321:: AID-ZOO4〉 3.0.CO;2-K)
38. Hildebrandt, T. et al. 2000b Ultrasonography of the urogenital tract in elephants (Loxodonta africana and Elephas maximus): an important tool for assessing male reproductive function. Zoo Biol. 19, 333-345. (doi:10.1002/1098-2361(2000)19:5 〈333::AID-ZOO5〉 3.0.CO;2-A)
39. Hodges, J. K. 1998 Endocrinology of the ovarian cycle and pregnancy in the Asian (Elephas maximus) and African (Loxodonta africana) elephant. Anim. Reprod. Sci. 53, 3-18. (doi:10.1016/S0378-4320(98)00123-7)
40. Hodges, J. K., McNeilly, A. S. & Hess, D. L. 1987 Circulating hormones during pregnancy in the Asian and African elephants (Elephas maximus and Loxodonta africana): a diagnostic test based on the measurement of prolactin. Int. Zoo Ybk 26, 285-289.
41. Hodges, J. K., van Aarde, M., Heistermann, M. & Hoppen, H.-O. 1994 Progestin content and biosynthetic potential of the corpus luteum of the African elephant (Loxodonta africana). J. Reprod. Fertil. 102, 163-168.
42. Hodges, J. K., Heistermann, M., Beard, A. & van Aarde, R. J. 1997 Concentrations of the 5α-reduced progestins, 5α-pregnane-3,20 dione and 5α-pregnane-3α-ol-20-one in luteal tissue and circulating blood and their relationship to luteal function in the African elephant, Loxodonta africana. Biol. Reprod. 56, 640-646. (doi:10.1095/biolreprod56.3.640)
43. Holtan, D. W., Houghton, E., Silver, M., Fowden, A. L., Ousey, J. & Rossdale, P. D. 1991 Plasma progestagens in the mare, fetus and newborn foal. J. Reprod. Fertil. 44, 517-528.
44. Johnson, O. W. & Buss, I. O. 1967a The testis of the African elephant (Loxodonta africana). I. Histological features. J. Reprod. Fertil. 13, 11-16.
45. Johnson, O. W. & Buss, I. O. 1967a The testis of the African elephant (Loxodonta africana). II. Development, puberty and weight. J. Reprod. Fertil. 13, 23-28.
46. Kapustin, N., Critser, J. K., Olson, D. & Malven, P. V. 1996 Nonluteal estrous cycles of 3-week duration are initiated by anovulatory luteinising hormone peaks in African elephants. Biol. Reprod. 55, 1147-1154. (doi:10.1095/biolreprod55.5.1147)
47. Kurt, F. & Khyne, U. 1996 Neonate mortality in captive Asian elephants. Z. Säugetierkd. 61, 155-164.
48. Laws, R. M. 1966 Age criteria for the African elephant, Loxodonta a. africana. E. Afr. Wildl. J. 4, 1-37.
49. Laws, R. M. 1967a Eye lens weight and age in African elephants. E. Afr. Wildl. J. 5, 46-52.
50. Laws, R. M. 1967b Occurrence of placental scars in the uterus of the African elephant (Loxodonta africana). J. Reprod. Fertil. 14, 445-449.
51. Laws, R. M. 1968 Interactions between elephant and hippopotamus populations and their environments. E. Afr. Agric. Forest. J. 33, 140-147.
52. Laws, R. M. 1969a Aspects of reproduction in the African elephant, Loxodonta africana. J. Reprod. Fertil. 6, 193-217.
53. Laws, R. M. 1969b The Tsavo research project. J. Reprod. Fertil. 6, 495-531.
54. Laws, R. M. & Parker, I. S. C. 1968 Recent studies on elephant populations in East Africa. Symp. Zool. Soc. Lond. 21, 349-359.
55. Maghuin-Rogister, C., Closset, J., Combarnous, Y., Hennen, G., Dechenne, C. H. & Ketelslegers, J. M. 1978 Study of follitropin receptors in testis using an homologous system. Binding of porcine follitropin to plasma membranes from immature porcine testis and correlation with adenylate cyclase stimulation. Eur. J. Biochem. 86, 121-131. (doi:10.1111/j.1432-1033.1978.tb12291.x)
56. McNeilly, A. S., Martin, R. D., Hodges, J. K. & Smuts, G. L. 1983 Blood concentrations of gonadotrophins, prolactin and gonadal steroids in males and in non-pregnant and pregnant female African elephants (Loxodonta africana). J. Reprod. Fertil. 67, 113-120.
57. Meyer, H. H. D., Jewgenow, K. & Hodges, J. K. 1997 Binding activity of 5α-reduced gestagens to the progestin receptor in the African elephant. Gen. Comp. Endocrinol. 105, 164-167. (doi:10.1006/gcen.1996.6813)
58. Meyer, J. M., Walker, S. L., Freeman, E. W., Steinetz, B. & Brown, J. L. 2004 Species and fetal gender effects on the endocrinology of pregnancy in elephants. Gen. Comp. Endocrinol. 138, 263-270. (doi:10.1016/j.ygcen.2004.06. 010)
59. Montali, R. J., Hildebrandt, T., Goritz, F., Hermes, R., Ippen, R. & Ramsay, E. C. 1997 Ultrasonography and pathology of genital tract leiomyomas in captive Asian elephants: implications for reproductive soundness. Verh ber Erkrg Zootiere 38, 253-258.
60. Moss, C. J. 1983 Oestrous behaviour and female choice in the African elephant. Behaviour 86, 167-196.
61. Moss, C. 1988 Elephant memories. Thirteen years in the life of an elephant family. London, UK: Elm Tree Books.
62. Mossman, H. W. 1987 Vertebrate fetal membranes, ch. 12, pp. 84-87
63. Mossman, H. W. Vertebrate fetal membranes, & ch. 14, pp. 91-97. Basingstoke, UK: Macmillan Press.
64. Niemuller, C. A., Shaw, H. J. & Hodges, J. K. 1993 Noninvasive monitoring of ovarian function in Asian elephants (Elephas maximus) by measurement of urinary 5β-pregnanetriol. J. Reprod. Fertil. 99, 243-251.
65. Niemuller, C. A., Shaw, H. J. & Hodges, J. K. 1997 Pregnancy determination in the Asian elephant (Elephas maximus): a change in the plasma progesterone to 17α-hydroxy-progesterone ratio. Zoo Biol. 16, 415-426. (doi:10. 1002/(SICI)1098-2361(1997)16:5 〈415::AID-ZOO4〉 3.0.CO;2-D)
66. Olsen, J. H., Chen, C. L., Boules, M. M., Morris, L. S. & Coville, V. R. 1994 Determination of reproductive cyclicity and pregnancy in elephant: luteinising hormone and progesterone cycles in African (Loxodonta africana) and Asian (Elephas maximus) elephants. Biol. Reprod. 38, 309-334.
67. Olson, D. & Wiese, R. J. 2000 State of the North American African elephant population and projections for the future. Zoo Biol. 19, 311-320. (doi:10.1002/1098-2361(2000) 19:5 〈311::AID-ZOO3〉 3.0.CO;2-O)
68. Perry, J. S. 1953 The reproduction of the African elephant, Loxodonta africana. Proc. R. Soc. B 237, 93-153.
69. Perry, J. S. 1964 The structure and development of the reproductive organs of the female African elephant. Proc. R. Soc. B 248, 36-51.
70. Perry, J. S. 1974 Implantation, foetal membranes and early placentation of the African elephant, Loxodonta africana. Proc. R. Soc. B 269, 109-135.
71. Plotka, E. D., Seal, U. S., Zarembka, F. R., Simmons, L. G., Teare, A., Phillips, L. G., Hinshaw, K. C. & Wood, D. G. 1988 Ovarian function in the elephant: luteinising hormone and progesterone cycles in African and Asian elephants. Biol. Reprod. 38, 309-314. (doi:10.1095/biolreprod38.2.309)
72. Poole, J. H. 1989 Mate guarding, reproductive success and female choice in African elephants. Anim. Behav. 37, 842-849. (doi:10.1016/0003-3472(89)90068- 7)
73. Poole, J. 1996 Coming of age with elephants. London, UK: Hodder and Stoughton.
74. Ramsey, E. C., Lasley, B. L. & Stabenfeldt, G. H. 1981 Monitoring the estrous cycle of the Asian elephant (Elephas maximus), using urinary oestrogens. Am. J. Vet. Res. 42, 256-260.
75. Roca, A. L., Georgiadis, N., Pecon-Slattery, J. & O'Brian, S. J. 2001 Genetic evidence for two species of elephant in Africa. Science 293, 1473-1477. (doi:10.1126/science. 1059936)
76. Rogers, K. H. 2005. Report of a Science Workshop on Elephant and Biodiversity, Luiperdskloof, South Africa. Johannesburg: University of Witwatersrand.
77. Schmid, J. 1998 Hands off, hands on: some aspects of keeping elephants. Int. Zoo News 45, 478-486.
78. Schmidt, M. J. & Khyne, U. 1996 Reproductive performance of captive Asian elephants in Myanmar. Gajah 16, 23-42.
79. Short, R. V. 1962 The peculiar lungs of the elephant. New Sci. 16, 570-572.
80. Short, R. V. 1966 Oestrous behaviour, ovulation and the formation of the corpus luteum in the African elephant, Loxodonta africana. E. Afr. Wildl. J. 4, 56-68.
81. Short, R. V. & Buss, I. O. 1965 Biochemical and histological observations on the corpora lutea of the African elephant, Loxodonta africana. J. Reprod. Fertil. 9, 61-67.
82. Short, R. V., Mann, T. & Hay, M. F. 1967 Male reproductive organs of the African elephant, Loxodonta africana. J. Reprod. Fertil. 13, 517-536.
83. Smith, N. S. & Buss, I. O. 1975 Formation, function and persistence of the corpora lutea of the African elephant (Loxodonta africana). J. Mammal. 56, 30-43.
84. Smith, J. G., Hanks, J. & Short, R. V. 1969 Biochemical observations on the corpora lutea of the African elephant, Loxodonta africana. J. Reprod. Fertil. 20, 11-117.
85. Stevenson, M. 2005. Management guidelines for the welfare of zoo animals: Elephant. Report for the Federation of Zoological Gardens of Great Britain and Ireland (director@biaza.org.uk).
86. Sukumar, R. 2003. The living elephants: evolutionary ecology, behaviour and conservation. New York, NY: Oxford University Press.
87. Tait, A. D., Santikarn, L. C. & Allen, W. R. 1983 Identification of 3β-hydroxy-5,7 pregnandien-20-one and 3β-hydroxy-5,7 androstadien-17-one as endogenous steroids in the foetal horse gonad. J. Endocrinol. 99, 87-92.
88. Tait, A. D., Hodge, L. C. & Allen, W. R. 1985 The biosynthesis of 3β-hydroxy-5,7-androstadien-17-one by the horse fetal gonad. FEBS Lett. 182, 107-110. (doi:10.1016/0014-5793(85)81164-9)
89. Taya, K. et al. 1991 Concentrations of progesterone, testosterone and estradiol-17β in the serum during the estrous cycle of Asian elephants (Elephas maximus). Zoo Biol. 10, 299-307. (doi:10.1002/zoo.1430100404)
90. Taylor, V. J. & Poole, T. B. 1998 Captive breeding and infant mortality in Asian elephants: a comparison between twenty western zoos and three eastern elephant centers. Zoo Biol. 17, 311-332. (doi:10.1002/(SICI)1098-2361 (1998)17:4 〈311::AID-ZOO5〉 3.0.CO;2-C)
91. Whyte, I. J. 2001 Conservation management of the Kruger National Park elephant population. Ph.D. thesis, University of Pretoria, South Africa.
92. Whyte, I. J. 2003 The feasibility of current options for the management of wild elephant populations. In managing african elephant populations: live or let die. Proc. First Int. Workshop on Control of Wild Elephant Populations, pp. 15-16. University of Utrecht, The Netherlands.
93. Wiese, R. J. 2000 Asian elephants are not self-sustaining in North America. Zoo Biol. 19, 299-309. (doi:10.1002/1098-2361(2000)19:5 〈299::AID-ZOO2〉 3.0.CO;2-Z)
94. Wooding, F. B. P., Stewart, S., Mathias, S. & Allen, W. R. 2005 Placentation in the African elephant, Loxodonta africanus. III Ultrastructural and functional features of the placenta. Placenta 26, 449-470. (doi:10.1016/j.placenta. 2004.08.007)
95. WWF-SARPO 2003 Proc. Workshop on Parks and Wildlife Management Authority 2001 National Aerial Survey and Census. Harare, Zimbabwe.