The use of a synthetic progesterone, levonorgestrel (LNG), to control the oestrous cycle in the koala
K. Ballantyne A E , S. T. Anderson B , M. Pyne C , V. Nicolson D , A. Mucci D , A. Lisle A and S. D. Johnston A
+ Author Affiliations
- Author Affiliations
A School of Agriculture and Food Science, University of Queensland, Gatton, Qld 4343, Australia.
B School of Biomedical Sciences, University of Queensland, St Lucia, Qld 4072, Australia.
C Currumbin Wildlife Sanctuary, Currumbin, Qld 4223, Australia.
D Dreamworld, Dreamworld Parkway, Coomera, Qld 4209, Australia.
E Corresponding author. Email: kate_068@msn.com
Reproduction, Fertility and Development 28(10) 1526-1532 https://doi.org/10.1071/RD14387
Submitted: 12 October 2014 Accepted: 9 February 2015 Published: 1 May 2015
Abstract
This study investigated the efficacy of a synthetic progestogen, levonorgestrel (LNG), to control koala ovarian activity for the purposes of oestrous synchronisation. Captive koalas were administered either saline control or a 70-mg LNG implant on Day 2 of oestrus. Urogenital cytology, oestrous behaviour and plasma oestradiol-17β and LH concentrations were monitored over a 6-week period. After LNG implant removal females were monitored to determine if the return to oestrus was synchronised. LNG-treated koalas immediately ceased displaying oestrous behaviour, showed no evidence of cornified epithelial cells in smears of urogenital cytology and exhibited low plasma oestradiol-17β concentrations throughout the implantation period. In contrast, oestradiol-17β levels in control koalas showed evidence of continued cyclic activity associated with behavioural oestrus and increased cornified epithelial cells in urogenital smears on Days 33 to 35 after saline injection. After implant removal, LNG-treated koalas exhibited oestrus at 13, 14, 17 and 30 days after implant removal. Plasma LH concentrations varied throughout the study period with no significant time (P = 0.49) or treatment (P = 0.13) effect. Overall results from this study suggest that LNG implants in koalas can inhibit oestrous behaviour and reduce circulating oestradiol-17β levels before oestrus, most likely by preventing development of the pre-ovulatory follicle. However, there was no evidence of LH suppression by the LNG implants. Removal of LNG implants resulted in the synchronous return to oestrus in three of the four treated koalas. Further studies on a larger population are required to validate these findings.
Additional keywords: marsupial, oestrous synchronisation, phascolarctos cinereus, reproductive management.
References
Allen, C. D., Burridge, M., Chafer, M. L., Nicolson, V. N., Jago, S. C., Booth, R. J., Fraser, G., Ensabella, T. J., Zee, Y. P., Lundie-Jenkins, G., Holt, W. V., Lisle, A. T., Carrick, F. N., Curlewis, J. D., D’Occhio, M. J., and Johnston, S. D. (2008). Control of the koala (Phascolarctos cinereus) anterior pituitary–gonadal axis with analogues of GnRH. Reprod. Fertil. Dev. 20, 598–605.| Control of the koala (Phascolarctos cinereus) anterior pituitary–gonadal axis with analogues of GnRH.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmsFagu7g%3D&md5=d01b5dca54387f71b5bab6250b515ba3CAS | 18577357PubMed |
Baldwin, C. J., Peter, A. T., Bosu, W. T. K., and Dubielzig, R. R. (1994). The contraceptive effects of levonorgestrel in the domestic cat. Lab. Anim. Sci. 44, 261–269.
| 1:CAS:528:DyaK2cXlvFKiu7g%3D&md5=69d71499d2ade782d18a9414efa872b1CAS | 7933974PubMed |
Blanshard, W. H. (1994) Medicine and husbandry of koalas. In ‘Wildlife: the T.G. Hungerford Refresher Course for Veterinarians’. pp. 547–623. (University of Sydney Post-Graduate Committee in Veterinary Science: Sydney.)
Busby, E. R., Soeta, S., Sherwood, N. M., and Johnston, S. D. (2014). Molecular analysis of the reproductive axis in a marsupial (koala Phascolarctos cinereus): gonadotrophin-releasing hormone (GnRH), luteinising hormone, follicle-stimulating hormone and their receptors with localisation of GnRH. J. Neuroendocrinol. , .
| Molecular analysis of the reproductive axis in a marsupial (koala Phascolarctos cinereus): gonadotrophin-releasing hormone (GnRH), luteinising hormone, follicle-stimulating hormone and their receptors with localisation of GnRH.Crossref | GoogleScholarGoogle Scholar | 25200132PubMed |
Crawford, J. L., McLeod, B. J., and Eckery, D. C. (2011). The hypothalamic–pituitary–ovarian axis and manipulations of the oestrous cycle in the brushtail possum. Gen. Comp. Endocrinol. 170, 424–448.
| The hypothalamic–pituitary–ovarian axis and manipulations of the oestrous cycle in the brushtail possum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXntVamtQ%3D%3D&md5=7de335f03a3f79d0e8f276805ae20797CAS | 21074534PubMed |
Croxatto, H. B. (2002). Mechanisms that explain the contraceptive action of progestin implants for women. Contraception 65, 21–27.
| Mechanisms that explain the contraceptive action of progestin implants for women.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtlGgsb4%3D&md5=431c3e8d40098ac25070ebc8ce146063CAS | 11861052PubMed |
Curlewis, J. D. (1991). Seasonal changes in the reproductive organs and plasma and pituitary of the male Bennett’s wallaby (Macropus rufogriseus rufogriseus). J. Zool. (Lond.) 223, 223–231.
| Seasonal changes in the reproductive organs and plasma and pituitary of the male Bennett’s wallaby (Macropus rufogriseus rufogriseus).Crossref | GoogleScholarGoogle Scholar |
Handasyde, K. A., McDonald, I. R., Than, K. A., Michaelides, J., and Martin, R. W. (1990) Reproductive hormones and reproduction in the koala. In ‘Biology of the Koala’. (Eds A. K. Lee, K. A. Handasyde and G. D. Sanson.) pp. 203–210. (Surrey Beatty & Sons: Sydney.)
Hinds, L. A., Fletcher, T. P., and Rodger, J. C. (1996). Hormones of oestrus and ovulation and their manipulation in marsupials. Reprod. Fertil. Dev. 8, 661–672.
| Hormones of oestrus and ovulation and their manipulation in marsupials.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XlvVWksbo%3D&md5=51face9e64222be50f89b596f39923f9CAS | 8870088PubMed |
Hsueh, A. J. W., Adashi, E. Y., Jones, P. B. C., and Welsh, T. H. (1984). Hormonal regulation of the differentiation of cultured ovarian granulosa cells. Endocr. Rev. 5, 76–127.
| Hormonal regulation of the differentiation of cultured ovarian granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXhvVGrtrc%3D&md5=3b6d0f2055b1294fac7984cd2fdb7c36CAS |
Hynes, E. F., Nave, C. D., Shaw, G., and Renfree, M. B. (2007). Effects of levonorgestrel on ovulation and oestrous behaviour in the female tammar wallaby. Reprod. Fertil. Dev. 19, 335–340.
| Effects of levonorgestrel on ovulation and oestrous behaviour in the female tammar wallaby.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVeisL4%3D&md5=c165b2357e763732de02e5113ded4e96CAS | 17257519PubMed |
Hynes, E. F., Handasyde, K. A., Shaw, G., and Renfree, M. B. (2010). Levonorgestrel, not etonogestrel, provides contraception in free-ranging koalas. Reprod. Fertil. Dev. 22, 913–919.
| Levonorgestrel, not etonogestrel, provides contraception in free-ranging koalas.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXotFenu7o%3D&md5=5e8a7f597e2cfe195064f11f9805fc66CAS | 20591325PubMed |
Jabbour, H. N., Asher, G. W., Smith, J. F., and Morrow, C. J. (1992). Effect of progesterone and oestradiol benzoate on oestrous behaviour and secretion of luteinising hormone in ovariectomised fallow deer (Dama dama). J. Reprod. Fertil. 94, 353–361.
| Effect of progesterone and oestradiol benzoate on oestrous behaviour and secretion of luteinising hormone in ovariectomised fallow deer (Dama dama).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XktVWitr0%3D&md5=cb3cd66ffe660a5cb25bc025d119a870CAS | 1593538PubMed |
Johnston, S. D. (1994) The reproductive biology of the Queensland koala. BSc (Honours) Thesis, University of Queensland, Brisbane.
Johnston, S. D. (1999) Studies towards the development of an artificial insemination program in the koala (Phascolarctos cinereus). Ph.D. Thesis, The University of Queensland, Brisbane.
Johnston, S. D., and Holt, W. V. (2001) Germplasm conservation in marsupials. In ‘Cryobanking the Genetic Resource: Wildlife Conservation for the Future?’. (Eds P. F. Watson and W. V. Holt.) pp. 201–227. (Taylor and Francis: London.)
Johnston, S. D., McGowan, M. R., O’Callaghan, P., and Nicolson, V. (2000a). Studies of the oestrous cycle, oestrus and pregnancy in the koala (Phascolarctos cinereus). J. Reprod. Fertil. 120, 49–57.
| 1:CAS:528:DC%2BD3cXntlCiur8%3D&md5=a0b40927067df9d902ebb9ceba6d284aCAS | 11006145PubMed |
Johnston, S. D., McGowan, M. R., O’Callaghan, P., and Nicolson, V. (2000b). Natural and artificial methods for inducing the luteal phase in the koala (Phascolarctos cinereus). J. Reprod. Fertil. 120, 59–64.
| 1:CAS:528:DC%2BD3cXntlCiurw%3D&md5=7e0703eddc9c02cd5ed34caa646c7854CAS | 11006146PubMed |
Johnston, S. D., O’Callaghan, P., Nilsson, K., Tzipori, G., and Curlewis, J. D. (2004). Semen-induced luteal phase and identification of a LH surge in the koala (Phascolarctos cinereus). Reproduction 128, 629–634.
| Semen-induced luteal phase and identification of a LH surge in the koala (Phascolarctos cinereus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVSis7nK&md5=9f45a7d28bb5aeb9fa97c020ec93f42dCAS | 15509709PubMed |
Matteri, R. L., Roser, J. F, Baldwin, D. M., Lipovetsky, V., and Papkoff, H. (1987). Characterization of a monoclonal antibody which detects luteinizing hormone from diverse mammalian species. Domest. Anim. Endocrinol. 4, 157–165.
| Characterization of a monoclonal antibody which detects luteinizing hormone from diverse mammalian species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXlt1Ogsrw%3D&md5=dea1397c1abe5e111fdc7f2cedd83a1fCAS | 3507889PubMed |
McFarlane, J. R., Rudd, C. D., Foulds, L. M., Fletcher, T. P., and Renfree, M. B. (1997). Isolation and partial characterization of tammar wallaby luteinizing hormone and development of a radioimmunoassay. Reprod. Fertil. Dev. 9, 475–480.
| Isolation and partial characterization of tammar wallaby luteinizing hormone and development of a radioimmunoassay.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXnslyksbw%3D&md5=b3c4d80b216758581c887eaacac03738CAS | 9402258PubMed |
McGowan, M. R., Tribe, A., Johnson, S. D., Carrick, F. N., and Van Hensbroek, L. (1995). The use of isofluorane to anaesthetise koalas (Phascolarctos cinereus). Aust. Vet. J. 72, 472–473.
| The use of isofluorane to anaesthetise koalas (Phascolarctos cinereus).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK28vit1Ojsg%3D%3D&md5=8211e3c9a54f45f3f39673206103ef7eCAS | 8825317PubMed |
Middleton, D. R., Walters, B., Menkhorst, P., and Wright, P. (2003). Fertility control in the koala, Phascolarctos cinereus: the impact of slow-release implants containing levonorgestrel or oestradiol on the production of pouch young. Wildl. Res. 30, 207–212.
| Fertility control in the koala, Phascolarctos cinereus: the impact of slow-release implants containing levonorgestrel or oestradiol on the production of pouch young.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntV2msbk%3D&md5=39aa5dac3d69075046aba8651011a07eCAS |
Scaramuzzi, R. J., Lindsay, D. R., and Shelton, J. N. (1972). Effect of repeated oestrogen administration on oestrous behaviour in ovariectomised ewes. J. Endocrinol. 52, 269–278.
| Effect of repeated oestrogen administration on oestrous behaviour in ovariectomised ewes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE38XhtVyntbw%3D&md5=4713cd8e07dc63d3ba9536279a4ed84eCAS | 5062726PubMed |
Shaw, G. (2006). Reproduction. In ‘Marsupials’. (Eds P. J. Armati, C. Dickman and I. Hume.) pp. 83–107. (Cambridge University Press: Cambridge.)
Sivin, I. (1988). International experience with Norplant and Norplant-2 contraceptives. Stud. Fam. Plann. 19, 81–94.
| International experience with Norplant and Norplant-2 contraceptives.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1c3kvV2rug%3D%3D&md5=17a3e1a95ee77cbecd3d7b4dcd15d3d4CAS | 3132758PubMed |
Tyndale-Biscoe, H., and Renfree, M. (1987) ‘Monographs on Marsupial Biology: Reproductive Physiology of Marsupials’. (Cambridge University Press: Cambridge.)
