The progression of small-follicle reserves in the ovaries of wild African elephants (Loxodonta africana) from puberty to reproductive senescence
F. J. Stansfield A B D , J. O. Nöthling B and W. R. Allen A C
+ Author Affiliations
- Author Affiliations
A The Elephant Research and Conservation Unit, Savé Valley Conservancy, c/o 490 Borrowdale Brooke, Harare, Zimbabwe.
B Department of Production Animal Studies, Faculty of Veterinary Science, University of Pretoria, Onderstepoort 0110, Republic of South Africa.
C The Paul Mellon Laboratory, ‘Brunswick’, 18 Woodditton Road, Newmarket, Suffolk, CB89BJ, UK.
D Corresponding author. Email: fjs@yoafrica.com
Reproduction, Fertility and Development 25(8) 1165-1173 https://doi.org/10.1071/RD12296
Submitted: 17 September 2012 Accepted: 8 November 2012 Published: 7 December 2012
Abstract
This study aimed to determine whether the follicle reserve in the ovary of the African elephant declines progressively after puberty and whether its depletion constrains the fertility of older females. Elephant ovaries were fixed in 4% neutral buffered formalin and small-follicle counts made using stereological protocols. Excepting a slight rise in small-follicle numbers between 16 and 25 years of age, there was a trend for follicle numbers to fall from puberty to 70 years. Reproductive status did not impact significantly on small-follicle numbers (P = 0.31). The number of early primary follicles, initially higher in number than true primary follicles, fell from post-puberty to nil at 45 years of age. Six of the seven oldest animals in the study showed signs of recent ovarian activity in the form of antral follicles, corpora lutea or large corpora nigra. The four oldest elephants (mean age 69 years) had a median small-follicle count of 11 113. In summary, it appears that the elephant ovary is capable of supplying oocytes for ovulation right up to the time of death at the age of maximum life expectancy, although the follicle reserve becomes depleted in some older elephants.
Additional keywords : oocyte, ovarian reserve, reproductive lifespan, stereology.
References
Allen, W. R., Mathias, S., and Ford, M. (2005). Placentation in the African elephant, Loxodonta africana. IV. Growth and function of the fetal gonads. Reproduction 130, 713–720.| Placentation in the African elephant, Loxodonta africana. IV. Growth and function of the fetal gonads.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1OnsLjE&md5=1fe151794d04ec16bb9e91e077763352CAS | 16264100PubMed |
Brown, J. L. (2000). Reproductive endocrine monitoring of elephants: an essential tool for assisting captive management. Zoo Biol. 19, 347–367.
| Reproductive endocrine monitoring of elephants: an essential tool for assisting captive management.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXos12gs7o%3D&md5=9a0aa1cd7c9ede734acacc972e8103afCAS |
Brown, J. L., Olson, D., Keele, M., and Freeman, E.W. (2004). Survey of the reproductive cyclicity status of Asian and African elephants in North America. Zoo Biol. 23, 309–321.
| Survey of the reproductive cyclicity status of Asian and African elephants in North America.Crossref | GoogleScholarGoogle Scholar |
Cohen, A. A. (2004). Female post-reproductive lifespan: a general mammalian trait. Biol. Rev. Camb. Philos. Soc. 79, 733–750.
| Female post-reproductive lifespan: a general mammalian trait.Crossref | GoogleScholarGoogle Scholar | 15682868PubMed |
Dohoo, I., Martin, W., and Stryhn, H. (2009) ‘Veterinary Epidemiologic Research’. (VER, Inc.: Charlottetown, Prince Edward Island, Canada.)
Dow, T., Holaskova, I., and Brown, J. (2011). Results of the third reproductive assessment survey of North American Asian (Elephas maximus) and African (Loxodonta africana) female elephants. Zoo Biol. 30, 699–711.
| Results of the third reproductive assessment survey of North American Asian (Elephas maximus) and African (Loxodonta africana) female elephants.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38%2Flt1GrsQ%3D%3D&md5=dae4589a64b5c43bb7a9b9e99c9e3e8dCAS | 21319213PubMed |
ESHRE Capri Workshop Group (2005). Fertility and ageing. Human Reproduction Update 11, 261–276.
| Fertility and ageing.Crossref | GoogleScholarGoogle Scholar | 15831503PubMed |
Faddy, M. J., and Gosden, R. G. (1996). A model conforming the decline in follicle numbers to the age of menopause in women. Hum. Reprod. 11, 1484–1486.
| A model conforming the decline in follicle numbers to the age of menopause in women.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK28zisVKqsw%3D%3D&md5=69a4920644a193ce93fed61839952c72CAS | 8671489PubMed |
Fortune, J. E., Kito, S., Wandji, S. A., and Srsen, V. (1998). Activation of bovine and baboon primordial follicles in vitro. Theriogenology 49, 441–449.
| Activation of bovine and baboon primordial follicles in vitro.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7ps1Gktg%3D%3D&md5=47bd7bd9a3f58683c45035cc7dbafb1aCAS | 10732025PubMed |
Freeman, E. W., Whyte, I. J., and Brown, E. M. (2008). Reproductive evaluation of elephants culled in Kruger National Park, South Africa between 1975 and 1995. Afr. J. Ecol. 47, 192–201.
| Reproductive evaluation of elephants culled in Kruger National Park, South Africa between 1975 and 1995.Crossref | GoogleScholarGoogle Scholar |
Freeman, E. W., Whyte, I. J., and Brown, E. M. (2009). Reproductive evaluation of elephants culled in Kruger National Park, South Africa between 1975 and 1995. Afr. J. Ecol. 47, 192–201.
| Reproductive evaluation of elephants culled in Kruger National Park, South Africa between 1975 and 1995.Crossref | GoogleScholarGoogle Scholar |
Gosden, R. G. (1987). Follicular status at menopause. Hum. Reprod. 2, 617–621.
| 1:STN:280:DyaL1c%2FlvFGnsQ%3D%3D&md5=b2b9a616db72eb84a10f7b7d661870d9CAS | 3316270PubMed |
Gougeon, A. (2010) The early stages of follicular growth. In ‘Biology and Pathology of the Oocyte’. (Eds A. O. Trounson and G. R. Gosden) pp. 29–43. (Cambridge University Press: Cambridge.)
Gundersen, H. J. G., and Jensen, E. B. (1987). The efficiency of systematic sampling in stereology and its prediction. J. Microsc. 147, 229–263.
| The efficiency of systematic sampling in stereology and its prediction.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1c7hvVyltA%3D%3D&md5=cdcc0d3a1366c77fd9c583788f15fa9aCAS |
Hanks, J. (1972). Reproduction of elephant, Loxodonta africana, in the Luangwa Valley, Zambia. J. Reprod. Fertil. 30, 13–26.
| Reproduction of elephant, Loxodonta africana, in the Luangwa Valley, Zambia.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE383htVCktw%3D%3D&md5=77b1d95d5284755b536dff2f2e9d59beCAS | 5035330PubMed |
Hansen, K. R., Knowlton, N. S., Thver, A. C., Charleston, J. S., Soules, M. R., and Klein, N. A. (2008). A new model of reproductive aging: the decline in ovarian non-growing follicle number from birth to menopause. Hum. Reprod. 23, 699–708.
| A new model of reproductive aging: the decline in ovarian non-growing follicle number from birth to menopause.Crossref | GoogleScholarGoogle Scholar | 18192670PubMed |
Hermes, R., Hildebrandt, T. B., and Goritz, F. (2004). Reproductive problems directly attributable to long-term captivity – asymmetric reproductive aging. Anim. Reprod. Sci. 82–83, 49–60.
| Reproductive problems directly attributable to long-term captivity – asymmetric reproductive aging.Crossref | GoogleScholarGoogle Scholar | 15271443PubMed |
Hirshfield, A. N. (1991). Development of follicles in the mammalian ovary. Int. Rev. Cytol. 124, 43–101.
| Development of follicles in the mammalian ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXlsFSmsr4%3D&md5=ce46e9c38971b5a49726fec940456e42CAS | 2001918PubMed |
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.
| Endocrinology of the ovarian cycle and pregnancy in the Asian (Elephas maximus) and African (Loxodonta africana) elephant.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXns1yksLs%3D&md5=77469f34397684ad46b00b8391d154b1CAS | 9835363PubMed |
Howard, C. V., and Reed, M. G. (2005) ‘Unbiased Stereology’. (BIOS Scientific Publishers: Oxford.)
Jachmann, H. (1988). Estimating age in African elephants: a revision of Laws’ molar evaluation technique. Afr. J. Ecol. 26, 51–56.
| Estimating age in African elephants: a revision of Laws’ molar evaluation technique.Crossref | GoogleScholarGoogle Scholar |
Krysko, D. V., Diez-Fraile, A., Criel, G., Svistunov, A. A., Vandenabeele, P., and D’Herde, K. (2008). Life and death of female gametes during oogenesis and folliculogenesis. Apoptosis 13, 1065–1087.
| Life and death of female gametes during oogenesis and folliculogenesis.Crossref | GoogleScholarGoogle Scholar | 18622770PubMed |
Laws, R. M. (1966). Age criteria for the African elephant. East African Wildlife Journal 4, 1–37.
Laws, R. M. (1969). Aspects of reproduction in the African Elephant, Loxodonta Africana. J. Reprod. Fertil. Suppl. 6, 193–217.
Laws, R. M., Parker, I. S. C., and Johnstone, R. C. B. (1970). Elephants and habitats in Northern Bunyoro, Uganda. East African Wildlife Journal 8, 163.
Lee, P. C., Sayialel, S., Lindsay, W. K., and Moss, C. J. (2012). African elephant age determination from teeth: validation from known individuals. Afr. J. Ecol. 50, 9–20.
| African elephant age determination from teeth: validation from known individuals.Crossref | GoogleScholarGoogle Scholar |
Mizroch, S. A. (1981). Analyses of some biological parameters in the Antarctic fin whale. International Whaling Commission 31, 425–434.
Moss, C. (2001). The demography of an African elephant (Loxodonta africana) population in Amboseli, Kenya. J. Zool. 255, 145–156.
| The demography of an African elephant (Loxodonta africana) population in Amboseli, Kenya.Crossref | GoogleScholarGoogle Scholar |
Moss, C. J., and Lee, P. C. (2011) Female reproductive strategies: individual life histories. In ‘The Amboseli Elephants: A Long-Term Perspective on a Long-Lived Mammal’. (Eds C. J. Moss, H. Croze and L. P. C. Lee) pp. 187–204. (University of Chicago Press: Chicago.)
Oktay, K., Schenken, R. S., and Nelson, J. F. (1995). Proliferating cell nuclear antigen marks the initiation of follicular growth in the rat. Biol. Reprod. 53, 295–301.
| Proliferating cell nuclear antigen marks the initiation of follicular growth in the rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXntVSmur8%3D&md5=f59cf6b48c50f18190064dfebe58106dCAS | 7492681PubMed |
Perry, J. S. (1953). The reproduction of the African elephant, Loxodonta africana. Philos. Trans. R. Soc. Lond. B Biol. Sci. 237, 93–149.
| The reproduction of the African elephant, Loxodonta africana.Crossref | GoogleScholarGoogle Scholar |
Peters, H., and McNatty, K. P. (1980) ‘The Ovary, a Correlation of Structure and Function in Mammals’. (University of California Press: Berkley.)
Picton, H. M. (2001). Activation of follicle development: the primordial follicle. Theriogenology 55, 1193–1210.
| Activation of follicle development: the primordial follicle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjsFSju7c%3D&md5=c53fcfcf4f05cd1de2107060cdd1c009CAS | 11327680PubMed |
Proctor, C. M., Freeman, E. W., and Brown, J. L. (2010). Results of a second survey to assess the reproductive status of female Asian and African elephants in North America. Zoo Biol. 29, 127–139.
| 20391465PubMed |
Sawyer, H. R., Smith, P., Heath, D. A., Juengel, J. L., Wakefield, S. J., and McNatty, K. P. (2002). Formation of ovarian follicles during fetal development in sheep. Biol. Reprod. 66, 1134–1150.
| Formation of ovarian follicles during fetal development in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XitlClu70%3D&md5=e6ed22df85bb270390bb67f37b88c686CAS | 11906935PubMed |
Sherry, B. Y. (1975). Reproduction of elephant in Gonarezhou, South-Eastern Rhodesia. Arnoldia Rhodesia 29, 7–13.
Smith, N. S., and Buss, I. O. (1975). Formation, function, and persistence of the corpora lutea of the African elephant (Loxodonta africana). J. Mammal. 56, 30–43.
| 1:STN:280:DyaE2M%2Fps1GjtQ%3D%3D&md5=a2914e12afb7fc7d1efd17f6dbfcdb4eCAS | 1113050PubMed |
Stansfield, F. J. (2006) Ovarian reserve in wild African elephant. MSc thesis, University of Leeds.
Stansfield, F. J., and Allen, W. R. (2012). Luteal maintenance of pregnancy in the African elephant (Loxodonta africana). Reproduction 143, 845–854.
| Luteal maintenance of pregnancy in the African elephant (Loxodonta africana).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XovFahsL8%3D&md5=c2766ffa48d37cd8b5718925450772c6CAS | 22457432PubMed |
Stansfield, F. J., Picton, H. M., and Nöthling, J. O. (2011a). Early primary rather than primordial follicles constitute the main follicular reserve in the African elephant (Loxodonta africana). Anim. Reprod. Sci. 123, 112–118.
| Early primary rather than primordial follicles constitute the main follicular reserve in the African elephant (Loxodonta africana).Crossref | GoogleScholarGoogle Scholar | 21126835PubMed |
Stansfield, F. J., Nöthling, J. O., and Ansari, T. (2011b). The distribution of small preantral follicles within the ovaries of prepubertal African elephants (Loxodonta africana). Anim. Reprod. Sci. 129, 96–103.
| The distribution of small preantral follicles within the ovaries of prepubertal African elephants (Loxodonta africana).Crossref | GoogleScholarGoogle Scholar | 22074896PubMed |
Stansfield, F. J., Nöthling, J. O., and Allen, W. R. (2012a). Growth and development of the ovary and small-follicle pool from mid fetal life to pre-puberty in the African elephant (Loxodonta africana). BMC Vet. Res. 8, 119.
| Growth and development of the ovary and small-follicle pool from mid fetal life to pre-puberty in the African elephant (Loxodonta africana).Crossref | GoogleScholarGoogle Scholar | 22824067PubMed |
Stansfield, F. J., Nothling, J. O., Soley, J. T., and Allen, W. R. (2012b). Development of the germinal ridge and ovary in the African elephant (Loxodonta africana). Reproduction 144, 583–593.
| Development of the germinal ridge and ovary in the African elephant (Loxodonta africana).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslClt7rO&md5=82dd87c58ccbe1c43e7d1ae6af8c0a8dCAS | 22991581PubMed |
te Velde, E. R., and Pearson, P. L. (2002). The variability of female reproductive ageing. Hum. Reprod. Update 8, 141–154.
| The variability of female reproductive ageing.Crossref | GoogleScholarGoogle Scholar | 12099629PubMed |
Tilly, J. L., and Telfer, E. E. (2009). Purification of germline stem cells from adult mammalian ovaries: a step closer towards control of the female biological clock? Mol. Hum. Reprod. 15, 393–398.
| Purification of germline stem cells from adult mammalian ovaries: a step closer towards control of the female biological clock?Crossref | GoogleScholarGoogle Scholar | 19509111PubMed |
van Noord, P. S. H., Dubas, J. S., Dorland, M., Boersma, H., and te Velde, E. (1997). Age at natural menopause in a population-based screening cohort: the role of menarch, fecundity and lifestyle factors. Fertil. Steril. 68, 95–102.
| Age at natural menopause in a population-based screening cohort: the role of menarch, fecundity and lifestyle factors.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2szltFejuw%3D%3D&md5=093b224e40bc8d124620dfb541d2b783CAS |
Wallace, W. H. B., and Kelsey, T. W. (2010). Human ovarian reserve from conception to the menopause. PLoS ONE 5, e8772.
| Human ovarian reserve from conception to the menopause.Crossref | GoogleScholarGoogle Scholar |
White, Y. A. R., Woods, D. C., Kakai, Y., Ishihara, O., Seki, H., and Tilly, J. L. (2012). Oocyte formation by mitotically active germ cells purified from ovaries of reproductive-age women. Nat. Med. 18, 413–421.
| Oocyte formation by mitotically active germ cells purified from ovaries of reproductive-age women.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xislygu7g%3D&md5=a9e6239768a6d3630a63f02ae265b3fcCAS |
Williamson, B. R. (1976). Reproduction in female African elephant in the Whankie National Park, Rhodesia. S. Afr. J. Wildl. Res 6, 89–93.
Zou, K., Yuan, Z., Yang, Z., Luo, H., Sun, K., Zhou, L., Xiang, J., Shi, L., Yu, Q., Zhang, Y., Hou, R., and Wu, J. (2009). Production of offspring from a germline stem cell line derived from neonatal ovaries. Nat. Cell Biol. 11, 631–636.
| Production of offspring from a germline stem cell line derived from neonatal ovaries.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlt1Sktrg%3D&md5=a7341c4d9c89a42f9397206fade6f801CAS | 19363485PubMed |
