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Vertebrate reproductive science and technology
RESEARCH ARTICLE

Contraceptive efficacy and dose-response effects of the gonadotrophin-releasing hormone (GnRH) agonist deslorelin in Tasmanian devils (Sarcophilus harrisii)

Holly R. Cope https://orcid.org/0000-0002-0651-5238 A , Sarah Peck B , Rebecca Hobbs C , Tamara Keeley D , Stephen Izzard B , Wei Yeen-Yap E , Peter J. White F , Carolyn J. Hogg A G and Catherine A. Herbert A H
+ Author Affiliations
- Author Affiliations

A School of Life and Environmental Sciences, Faculty of Science, The University of Sydney, J.D. Stewart Building B01, Camperdown, NSW 2006, Australia.

B Wildlife Management Branch, Department of Primary Industries, Parks, Water and Environment, Hobart, Tas. 7000, Australia.

C Taronga Institute of Science and Learning, Taronga Conservation Society, NSW 2088, Australia.

D School of Agriculture and Food Sciences, Faculty of Science, The University of Queensland, Gatton, Qld 4343, Australia.

E Hobart, Tas. 7000, Australia.

F Sydney School of Veterinary Science, Faculty of Science, The University of Sydney, R.M.C. Gunn Building B19, Camperdown, NSW 2006, Australia.

G Zoo and Aquarium Association Australasia, Mosman, NSW 2088, Australia.

H Corresponding author. Email: catherine.herbert@sydney.edu.au

Reproduction, Fertility and Development 31(9) 1473-1485 https://doi.org/10.1071/RD18407
Submitted: 8 October 2018  Accepted: 13 March 2019   Published: 3 May 2019

Abstract

Contraception is increasingly used to manage breeding opportunities in conservation-dependent species. This study aimed to determine the efficacy, duration of effect, optimal dose and potential side effects of Suprelorin contraceptive implants in Tasmanian devils, for use in the conservation breeding program. In our pilot study, Suprelorin was found to effectively suppress oestrous cycles in female devils, yet caused a paradoxical increase in testosterone in males. Therefore, we focussed on females in further trials. Females received one (n = 5), two (n = 5) or no (n = 5) Suprelorin implants, with quarterly gonadotrophin-releasing hormone (GnRH) challenges used to test pituitary responsiveness over two breeding seasons. Both Suprelorin doses suppressed pituitary responsiveness for at least one breeding season, with a reduced effect in the second. There was a dose-response effect on duration rather than magnitude of effect, with high-dose devils remaining suppressed for longer than low-dose animals. There were no apparent negative effects on general health, yet captivity and contraception together may cause weight gain. Suprelorin contraceptive implants are now routinely used in the Save the Tasmanian Devil Program insurance metapopulation to meet the aims of maintaining genetic and behavioural integrity by controlling individual reproductive contributions in group housing situations.

Additional keywords: captive breeding, DFTD, fertility control, marsupial, Suprelorin, wildlife.


References

Arlt, S., Spankowski, S., Kaufmann, T., Kostelnik, K., and Heuwieser, W. (2010). Fertility control in a male rabbit using a deslorelin implant. A case report. World Rabbit Sci. 18, 179–182.
Fertility control in a male rabbit using a deslorelin implant. A case report.Crossref | GoogleScholarGoogle Scholar |

Asa, C. S. (2005). Assessing efficacy and reversibility. In ‘Wildlife Contraception: Issues, Methods, and Application’. (Eds C. S. Asa and I. J. Porton.) pp. 53–65. (The John Hopkins University Press: Baltimore, MD, USA.)

Asa, C. S., and Porton, I. J. (Eds) (2005). ‘Wildlife Contraception: Issues, Methods, and Application’. (The John Hopkins University Press: Baltimore, MD, USA.)

AZA RMC (2016). AZA Reproductive Management Centre. https://www.stlzoo.org/animals/scienceresearch/reproductivemanagementcenter [Accessed 5 April 2016]

AZA RMC (2018). Suprelorin (deslorelin). https://www.stlzoo.org/animals/scienceresearch/reproductivemanagementcenter/contraceptionrecommendatio/contraceptionmethods/suprelorin-deslorelin [Accessed 15 March 2018]

Bergfeld, E. G., D’Occhio, M., and Kinder, J. (1996). Continued desensitization of the pituitary gland in young bulls after treatment with the luteinizing hormone-releasing hormone agonist deslorelin. Biol. Reprod. 54, 769–775.
Continued desensitization of the pituitary gland in young bulls after treatment with the luteinizing hormone-releasing hormone agonist deslorelin.Crossref | GoogleScholarGoogle Scholar | 8924495PubMed |

Cope, H. R., Hogg, C. J., Fagg, K., Barnard, O., White, P. J., and Herbert, C. A. (2018a). Effects of deslorelin implants on reproduction and feeding behavior in Tasmanian devils (Sarcophilus harrisii) housed in free-range enclosures. Theriogenology 107, 134–141.
Effects of deslorelin implants on reproduction and feeding behavior in Tasmanian devils (Sarcophilus harrisii) housed in free-range enclosures.Crossref | GoogleScholarGoogle Scholar | 29149677PubMed |

Cope, H. R., Hogg, C. J., White, P. J., and Herbert, C. A. (2018b). A role for selective contraception of individuals in conservation management programs. Conserv. Biol. 32, 546–558.
A role for selective contraception of individuals in conservation management programs.Crossref | GoogleScholarGoogle Scholar | 29080297PubMed |

Cowan, M. L., Martin, G. B., Monks, D. J., Johnston, S. D., Doneley, R. J. T., and Blackberry, M. A. (2014). Inhibition of the reproductive system by deslorelin in male and female pigeons (Columba livia). J. Avian Med. Surg. 28, 102–108.
Inhibition of the reproductive system by deslorelin in male and female pigeons (Columba livia).Crossref | GoogleScholarGoogle Scholar | 25115038PubMed |

Curtis, P. D., Richmond, M. E., Miller, L. A., and Quimby, F. W. (2007). Pathophysiology of white-tailed deer vaccinated with porcine zona pellucida immunocontraceptive. Vaccine 25, 4623–4630.
Pathophysiology of white-tailed deer vaccinated with porcine zona pellucida immunocontraceptive.Crossref | GoogleScholarGoogle Scholar | 17475371PubMed |

D’Occhio, M. J., and Aspden, W. J. (1996). Characteristics of luteinizing hormone (LH) and testosterone secretion, pituitary responses to LH-releasing hormone (LHRH), and reproductive function in young bulls receiving the LHRH agonist deslorelin: effect of castration on LH responses to LHRH. Biol. Reprod. 54, 45–52.
Characteristics of luteinizing hormone (LH) and testosterone secretion, pituitary responses to LH-releasing hormone (LHRH), and reproductive function in young bulls receiving the LHRH agonist deslorelin: effect of castration on LH responses to LHRH.Crossref | GoogleScholarGoogle Scholar | 8837999PubMed |

Delville, Y., Mansour, K. M., and Ferris, C. F. (1996). Testosterone facilitates aggression by modulating vasopressin receptors in the hypothalamus. Physiol. Behav. 60, 25–29.
Testosterone facilitates aggression by modulating vasopressin receptors in the hypothalamus.Crossref | GoogleScholarGoogle Scholar | 8804638PubMed |

Eymann, J., Herbert, C. A., Thomson, B. P., Trigg, T. E., Cooper, D. W., and Eckery, D. C. (2007). Effects of deslorelin implants on reproduction in the common brushtail possum (Trichosurus vulpecula). Reprod. Fertil. Dev. 19, 899–909.
Effects of deslorelin implants on reproduction in the common brushtail possum (Trichosurus vulpecula).Crossref | GoogleScholarGoogle Scholar | 18076822PubMed |

Farquharson, K. A., Hogg, C. J., and Grueber, C. E. (2017). Pedigree analysis reveals a generational decline in reproductive success of captive Tasmanian devil (Sarcophilus harrisii): implications for captive management of threatened species. J. Hered. 108, 488–495.
Pedigree analysis reveals a generational decline in reproductive success of captive Tasmanian devil (Sarcophilus harrisii): implications for captive management of threatened species.Crossref | GoogleScholarGoogle Scholar | 28379457PubMed |

Fontaine, C. (2015). Long-term contraception in a small implant: a review of Suprelorin (deslorelin) studies in cats. J. Feline Med. Surg. 17, 766–771.
Long-term contraception in a small implant: a review of Suprelorin (deslorelin) studies in cats.Crossref | GoogleScholarGoogle Scholar | 26323800PubMed |

Friedman, A. J., Hoffman, D. I., Comite, F., Browneller, R. W., and Miller, J. D. (1991). Treatment of leiomyomata uteri with leuprolide acetate depot: a double-blind, placebo-controlled, multicenter study. Obstet. Gynecol. 77, 720–725.
| 1901638PubMed |

Gionfriddo, J. P., Denicola, A. J., Miller, L. A., and Fagerstone, K. A. (2011). Health effects of GnRH immunocontraception of wild white-tailed deer in New Jersey. Wildl. Soc. Bull. 35, 149–160.
Health effects of GnRH immunocontraception of wild white-tailed deer in New Jersey.Crossref | GoogleScholarGoogle Scholar |

Goericke-Pesch, S., Georgiev, P., Antonov, A., Albouy, M., and Wehrend, A. (2011). Clinical efficacy of a GnRH-agonist implant containing 4.7 mg deslorelin, Suprelorin®, regarding suppression of reproductive function in tomcats. Theriogenology 75, 803–810.
Clinical efficacy of a GnRH-agonist implant containing 4.7 mg deslorelin, Suprelorin®, regarding suppression of reproductive function in tomcats.Crossref | GoogleScholarGoogle Scholar | 21196037PubMed |

Goericke-Pesch, S., Georgiev, P., Fasulkov, I., Vodenicharov, A., and Wehrend, A. (2013). Basal testosterone concentrations after the application of a slow-release GnRH agonist implant are associated with a loss of response to buserelin, a short-term GnRH agonist, in the tom cat. Theriogenology 80, 65–69.
Basal testosterone concentrations after the application of a slow-release GnRH agonist implant are associated with a loss of response to buserelin, a short-term GnRH agonist, in the tom cat.Crossref | GoogleScholarGoogle Scholar | 23622940PubMed |

Graham, L., Schwarzenberger, F., Möstl, E., Galama, W., and Savage, A. (2001). A versatile enzyme immunoassay for the determination of progestogens in feces and serum. Zoo Biol. 20, 227–236.
A versatile enzyme immunoassay for the determination of progestogens in feces and serum.Crossref | GoogleScholarGoogle Scholar |

Graham, L. H., Bolling, J., Miller, G., Pratt-Hawkes, N., and Joseph, S. (2002). Enzyme-immunoassay for the measurement of luteinizing hormone in the serum of African elephants (Loxodonta africana). Zoo Biol. 21, 403–408.
Enzyme-immunoassay for the measurement of luteinizing hormone in the serum of African elephants (Loxodonta africana).Crossref | GoogleScholarGoogle Scholar |

Guiler, E. (1970). Observations on the Tasmanian devil, Sarcophilus harrisii (Marsupialia: Dasyuridae) II. Reproduction, breeding and growth of pouch young. Aust. J. Zool. 18, 63–70.
Observations on the Tasmanian devil, Sarcophilus harrisii (Marsupialia: Dasyuridae) II. Reproduction, breeding and growth of pouch young.Crossref | GoogleScholarGoogle Scholar |

Guiler, E. R. (1978). Observations on the Tasmanian devil, Sarcophilus harrisii (Dasyuridae: Marsupialia) at Granville Harbour, 1966–75. Royal Society of Tasmania 112, 161–188.

Herbert, C. A. (2002). Contraception of marsupials using slow release implants containing the GnRH agonist deslorelin. Ph.D. Thesis, Macquarie University, Sydney.

Herbert, C. A., Trigg, T. E., Renfree, M. B., Shaw, G., Eckery, D. C., and Cooper, D. W. (2004). Effects of a gonadotropin-releasing hormone agonist implant on reproduction in a male marsupial, Macropus eugenii. Biol. Reprod. 70, 1836–1842.
Effects of a gonadotropin-releasing hormone agonist implant on reproduction in a male marsupial, Macropus eugenii.Crossref | GoogleScholarGoogle Scholar | 14973259PubMed |

Herbert, C. A., Trigg, T. E., Renfree, M. B., Shaw, G., Eckery, D. C., and Cooper, D. W. (2005). Long-term effects of deslorelin implants on reproduction in the female tammar wallaby (Macropus eugenii). Reproduction 129, 361–369.
Long-term effects of deslorelin implants on reproduction in the female tammar wallaby (Macropus eugenii).Crossref | GoogleScholarGoogle Scholar | 15749962PubMed |

Herbert, C., Trigg, T., and Cooper, D. (2006). Fertility control in female eastern grey kangaroos using the GnRH agonist deslorelin. 1. Effects on reproduction. Wildl. Res. 33, 41–46.
Fertility control in female eastern grey kangaroos using the GnRH agonist deslorelin. 1. Effects on reproduction.Crossref | GoogleScholarGoogle Scholar |

Herbert, C. A., Eckery, D., Trigg, T., and Cooper, D. (2007). Chronic treatment of male tammar wallabies with deslorelin implants during pouch life: effects on development, puberty, and reproduction in adulthood. Biol. Reprod. 76, 1054–1061.
Chronic treatment of male tammar wallabies with deslorelin implants during pouch life: effects on development, puberty, and reproduction in adulthood.Crossref | GoogleScholarGoogle Scholar | 17329593PubMed |

Herbert, C. A., Renfree, M. B., Coulson, G., Shaw, G., Trigg, T. E., and Cooper, D. W. (2010). Advances in fertility control technologies for managing overabundant macropodid populations. In ‘Macropods: the Biology of Kangaroos, Wallabies and Rat-Kangaroos’. (Eds G. Coulson and M. D. B. Eldridge.) pp. 313–324. (CSIRO Publishing: Collingwood, Vic., Australia.)

Herbert, C. A., Eckery, D. C., Trigg, T. E., and Cooper, D. W. (2013). Chronic treatment of female tammar wallabies with deslorelin implants during pouch life: effects on reproductive maturation. Reprod. Fertil. Dev. 25, 879–889.
Chronic treatment of female tammar wallabies with deslorelin implants during pouch life: effects on reproductive maturation.Crossref | GoogleScholarGoogle Scholar | 22980757PubMed |

Herrick, J. R., Bond, J. B., Campbell, M., Levens, G., Moore, T., Benson, K., D’Agostino, J., West, G., Okeson, D. M., Coke, R., Portacio, S. C., Leiske, K., Kreider, C., Polumbo, P. J., and Swanson, W. F. (2010). Fecal endocrine profiles and ejaculate traits in black-footed cats (Felis nigripes) and sand cats (Felis margarita). Gen. Comp. Endocrinol. 165, 204–214.
Fecal endocrine profiles and ejaculate traits in black-footed cats (Felis nigripes) and sand cats (Felis margarita).Crossref | GoogleScholarGoogle Scholar | 19576217PubMed |

Hesterman, H., Jones, S., and Schwarzenberger, F. (2008). Pouch appearance is a reliable indicator of the reproductive status in the Tasmanian devil and the spotted-tailed quoll. J. Zool. 275, 130–138.
Pouch appearance is a reliable indicator of the reproductive status in the Tasmanian devil and the spotted-tailed quoll.Crossref | GoogleScholarGoogle Scholar |

Hogg, C. J., Ivy, J. A., Srb, C., Hockley, J., Lees, C., Hibbard, C., and Jones, M. (2015). Influence of genetic provenance and birth origin on productivity of the Tasmanian devil insurance population. Conserv. Genet. 16, 1465–1473.
Influence of genetic provenance and birth origin on productivity of the Tasmanian devil insurance population.Crossref | GoogleScholarGoogle Scholar |

Hogg, C. J., Grueber, C. E., Pemberton, D., Fox, S., Lee, A. V., Ivy, J. A., and Belov, K. (2017a). “Devil tools & tech”: a synergy of conservation research and management practice. Conserv. Lett. 10, 133–138.
“Devil tools & tech”: a synergy of conservation research and management practice.Crossref | GoogleScholarGoogle Scholar |

Hogg, C. J., Lee, A. V., Srb, C., and Hibbard, C. (2017b). Metapopulation management of an endangered species with limited genetic diversity in the presence of disease: the Tasmanian devil Sarcophilus harrisii. Int. Zoo Yearb. 51, 137–153.
Metapopulation management of an endangered species with limited genetic diversity in the presence of disease: the Tasmanian devil Sarcophilus harrisii.Crossref | GoogleScholarGoogle Scholar |

Hope, K. L., and Peck, S. (2016). Hematological and serum biochemical values in anesthetized captive Tasmanian devils (Sarcophilus harrisii). J. Zoo Wildl. Med. 47, 564–572.
Hematological and serum biochemical values in anesthetized captive Tasmanian devils (Sarcophilus harrisii).Crossref | GoogleScholarGoogle Scholar | 27468030PubMed |

Hughes, R. L. (1982). Reproduction in the Tasmanian devil Sarcophilus harrisii (Dasyuridae, Marsupialia). In ‘Carnivorous Marsupials’. (Ed. M. Archer.) pp. 49–63. (Surrey Beatty and Sons: Sydney.)

Jones, M., Jarman, P., Lees, C., Hesterman, H., Hamede, R., Mooney, N., Mann, D., Pukk, C., Bergfeld, J., and McCallum, H. (2007). Conservation management of Tasmanian devils in the context of an emerging, extinction-threatening disease: devil facial tumor disease. EcoHealth 4, 326–337.
Conservation management of Tasmanian devils in the context of an emerging, extinction-threatening disease: devil facial tumor disease.Crossref | GoogleScholarGoogle Scholar |

Jones, M. E., Cockburn, A., Hamede, R., Hawkins, C., Hesterman, H., Lachish, S., Mann, D., McCallum, H., and Pemberton, D. (2008). Life-history change in disease-ravaged Tasmanian devil populations. Proc. Natl. Acad. Sci. USA 105, 10023–10027.
Life-history change in disease-ravaged Tasmanian devil populations.Crossref | GoogleScholarGoogle Scholar | 18626026PubMed |

Junaidi, A., Williamson, P. E., Cummins, J. M., Martin, G. B., Blackberry, M. A., and Trigg, T. E. (2003). Use of a new drug delivery formulation of the gonadotrophin-releasing hormone analogue deslorelin for reversible long-term contraception in male dogs. Reprod. Fertil. Dev. 15, 317–322.
Use of a new drug delivery formulation of the gonadotrophin-releasing hormone analogue deslorelin for reversible long-term contraception in male dogs.Crossref | GoogleScholarGoogle Scholar | 14975229PubMed |

Junaidi, A., Williamson, P. E., Martin, G. B., Blackberry, M. A., Cummins, J. M., and Trigg, T. E. (2009). Dose-response studies for pituitary and testicular function in male dogs treated with the GnRH superagonist, deslorelin. Reprod. Domest. Anim. 44, 725–734.
Dose-response studies for pituitary and testicular function in male dogs treated with the GnRH superagonist, deslorelin.Crossref | GoogleScholarGoogle Scholar | 19769638PubMed |

Kauffold, J., Rohrmann, H., Boehm, J., and Wehrend, A. (2010). Effects of long-term treatment with the GnrH agonist deslorelin (Suprelorin®) on sexual function in boars. Theriogenology 74, 733–740.
Effects of long-term treatment with the GnrH agonist deslorelin (Suprelorin®) on sexual function in boars.Crossref | GoogleScholarGoogle Scholar | 20570338PubMed |

Keeley, T., Harris, M., McGreevy, P. D., Hudson, D., and O’Brien, J. K. (2012a). Development and evaluation of electroejaculation techniques in the Tasmanian devil (Sarcophilus harrisii). Reprod. Fertil. Dev. 24, 1008–1018.
Development and evaluation of electroejaculation techniques in the Tasmanian devil (Sarcophilus harrisii).Crossref | GoogleScholarGoogle Scholar | 22935162PubMed |

Keeley, T., O’Brien, J. K., Fanson, B. G., Masters, K., and McGreevy, P. D. (2012b). The reproductive cycle of the Tasmanian devil (Sarcophilus harrisii) and factors associated with reproductive success in captivity. Gen. Comp. Endocrinol. 176, 182–191.
The reproductive cycle of the Tasmanian devil (Sarcophilus harrisii) and factors associated with reproductive success in captivity.Crossref | GoogleScholarGoogle Scholar | 22306283PubMed |

Lazenby, B. T., Tobler, M. W., Brown, W. E., Hawkins, C. E., Hocking, G. J., Hume, F., Huxtable, S., Iles, P., Jones, M. E., Lawrence, C., Thalmann, S., Wise, P., Williams, H., Fox, S., and Pemberton, D. (2018). Density trends and demographic signals uncover the long-term impact of transmissible cancer in Tasmanian devils. J. Appl. Ecol. 55, 1368–1379.
Density trends and demographic signals uncover the long-term impact of transmissible cancer in Tasmanian devils.Crossref | GoogleScholarGoogle Scholar | 30089931PubMed |

Lincoln, G. A. (1987). Long-term stimulatory effects of a continuous infusion of LHRH agonist on testicular function in male red deer (Cervus elaphus). J. Reprod. Fertil. 80, 257–261.
Long-term stimulatory effects of a continuous infusion of LHRH agonist on testicular function in male red deer (Cervus elaphus).Crossref | GoogleScholarGoogle Scholar | 3110411PubMed |

Lunn, S. F., Dixson, A., Sandow, J., and Fraser, H. (1990). Pituitary-testicular function is suppressed by an LHRH antagonist but not by an LHRH agonist in the marmoset monkey. J. Endocrinol. 125, 233–239.
Pituitary-testicular function is suppressed by an LHRH antagonist but not by an LHRH agonist in the marmoset monkey.Crossref | GoogleScholarGoogle Scholar | 2165119PubMed |

Lunn, S. F., Cowen, G., Morris, K., and Fraser, H. (1992). Influence of the gonad on the degree of suppression induced by an LHRH agonist implant in the marmoset monkey. J. Endocrinol. 132, 217–224.
Influence of the gonad on the degree of suppression induced by an LHRH agonist implant in the marmoset monkey.Crossref | GoogleScholarGoogle Scholar | 1541921PubMed |

Mason, P., and Harman, R. J. (2002). ‘Handbook of Pharmacy Healthcare: Diseases and Patient Advice’. 2nd edn. (Pharmaceutical Press: London.)

Matson, P., Mayberry, C., Willers, N., Blackberry, M. A., and Martin, G. B. (2009). The measurement of luteinising hormone in the western grey kangaroo (Macropus fuliginosus ocydromus) and the black-flanked rock wallaby (Petrogale lateralis lateralis). Aust. Mammal. 31, 61–63.
The measurement of luteinising hormone in the western grey kangaroo (Macropus fuliginosus ocydromus) and the black-flanked rock wallaby (Petrogale lateralis lateralis).Crossref | GoogleScholarGoogle Scholar |

Matteri, R. L., Roser, J., Baldwin, D., 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 | 3507889PubMed |

Mayberry, C. J. (2011). Management of isolated populations of western grey kangaroos (Macropus fuliginosus ocydromus) through fertility control, in south-western Australia. Ph.D. Thesis, University of Western Australia, Perth.

McCallum, H., Tompkins, D., Jones, M., Lachish, S., Marvanek, S., Lazenby, B., Hocking, G., Wiersma, J., and Hawkins, C. (2007). Distribution and impacts of Tasmanian devil facial tumor disease. EcoHealth 4, 318–325.
Distribution and impacts of Tasmanian devil facial tumor disease.Crossref | GoogleScholarGoogle Scholar |

Melson, B. E., Brown, J. L., Schoenemann, H. M., Tarnavsky, G. K., and Reeves, J. J. (1986). Elevation of serum testosterone during chronic LHRH agonist treatment in the bull. J. Anim. Sci. 62, 199–207.
Elevation of serum testosterone during chronic LHRH agonist treatment in the bull.Crossref | GoogleScholarGoogle Scholar | 3007418PubMed |

Melville, D. F., O’Brien, G. M., Crichton, E. G., Theilemann, P., McKinnon, A., and Johnston, S. D. (2012). Reproductive seasonality and the effect of the GnRH agonist deslorelin as a contraceptive in captive male black flying-foxes (Pteropus alecto). Theriogenology 77, 652–661.
Reproductive seasonality and the effect of the GnRH agonist deslorelin as a contraceptive in captive male black flying-foxes (Pteropus alecto).Crossref | GoogleScholarGoogle Scholar | 22115809PubMed |

Miller, L. A., Crane, K., Gaddis, S., and Killian, G. J. (2001). Porcine zona pellucida immunocontraception: long-term health effects on white-tailed deer. J. Wildl. Manage. 65, 941–945.
Porcine zona pellucida immunocontraception: long-term health effects on white-tailed deer.Crossref | GoogleScholarGoogle Scholar |

Nillius, S. J., and Wide, L. (1972). Variation in LH and FSH response to LH-releasing hormone during the menstrual cycle. J Obstet Gynaecol Br Commonw 79, 865–873.
Variation in LH and FSH response to LH-releasing hormone during the menstrual cycle.Crossref | GoogleScholarGoogle Scholar | 4563793PubMed |

Ortmann, O., Weiss, J. M., and Diedrich, K. (2002). Gonadotrophin-releasing hormone (GnRH) and GnRH agonists: mechanisms of action. Reproductive Biomedicine Online 5, 1–7.
| 12537774PubMed |

Peck, S., Corkrey, R., Hamede, R., Jones, M., and Canfield, P. (2015). Hematologic and serum biochemical reference intervals for wild Tasmanian devils (Sarcophilus harrisii). Vet. Clin. Pathol. 44, 519–529.
Hematologic and serum biochemical reference intervals for wild Tasmanian devils (Sarcophilus harrisii).Crossref | GoogleScholarGoogle Scholar | 26613213PubMed |

Pollock, K., Booth, R., Wilson, R., Keeley, T., Grogan, K., Kennerley, P., and Johnston, S. D. (2010). Oestrus in the Julia Creek dunnart (Sminthopsis douglasi) is associated with wheel running behaviour but not necessarily changes in body weight, food consumption or pouch morphology. Anim. Reprod. Sci. 117, 135–146.
Oestrus in the Julia Creek dunnart (Sminthopsis douglasi) is associated with wheel running behaviour but not necessarily changes in body weight, food consumption or pouch morphology.Crossref | GoogleScholarGoogle Scholar | 19362793PubMed |

Ronayne, E., Enright, W., and Roche, J. (1993). Effects of continuous administration of gonadotropin-releasing hormone (GnRH) or a potent GnRH analogue on blood luteinizing hormone and testosterone concentrations in prepubertal bulls. Domest. Anim. Endocrinol. 10, 179–189.
Effects of continuous administration of gonadotropin-releasing hormone (GnRH) or a potent GnRH analogue on blood luteinizing hormone and testosterone concentrations in prepubertal bulls.Crossref | GoogleScholarGoogle Scholar | 8252838PubMed |

Scheele, F., Hompes, P. G. A., Lambalk, C. B., Schoute, E., Broekmans, F. J., and Schoemaker, J. (1996). The GnRH challenge test: a quantitative measure of pituitary desensitization during GnRH agonist administration. Clin. Endocrinol. 44, 581–586.
The GnRH challenge test: a quantitative measure of pituitary desensitization during GnRH agonist administration.Crossref | GoogleScholarGoogle Scholar |

Soma, K. K. (2006). Testosterone and aggression: Berthold, birds and beyond. J. Neuroendocrinol. 18, 543–551.
Testosterone and aggression: Berthold, birds and beyond.Crossref | GoogleScholarGoogle Scholar | 16774503PubMed |

Stachenfeld, N. S. (2008). Sex hormone effects on body fluid regulation. Exerc. Sport Sci. Rev. 36, 152–159.
Sex hormone effects on body fluid regulation.Crossref | GoogleScholarGoogle Scholar | 18580296PubMed |

Stachenfeld, N. S. (2014). Hormonal changes during menopause and the impact on fluid regulation. Reprod. Sci. 21, 555–561.
Hormonal changes during menopause and the impact on fluid regulation.Crossref | GoogleScholarGoogle Scholar | 24492487PubMed |

Stewart, E. A. (2001). Uterine fibroids. Lancet 357, 293–298.
Uterine fibroids.Crossref | GoogleScholarGoogle Scholar | 11214143PubMed |

Stovall, T. G., Muneyyirci-Delale, O., Summitt, R. L., and Scialli, A. R. (1995). GnRH agonist and iron versus placebo and iron in the anemic patient before surgery for leiomyomas: a randomized controlled trial. Obstet. Gynecol. 86, 65–71.
GnRH agonist and iron versus placebo and iron in the anemic patient before surgery for leiomyomas: a randomized controlled trial.Crossref | GoogleScholarGoogle Scholar | 7784025PubMed |

Trigg, T. E., Wright, P., Armour, A., Williamson, P., Junaidi, A., Martin, G., Doyle, A., and Walsh, J. (2001). Use of a GnRH analogue implant to produce reversible long-term suppression of reproductive function in male and female domestic dogs. J. Reprod. Fertil. Suppl. 57, 255–261.
| 11787159PubMed |

Walker, S. L., Waddell, W. T., and Goodrowe, K. L. (2002). Reproductive endocrine patterns in captive female and male red wolves (Canis rufus) assessed by fecal and serum hormone analysis. Zoo Biol. 21, 321–335.
Reproductive endocrine patterns in captive female and male red wolves (Canis rufus) assessed by fecal and serum hormone analysis.Crossref | GoogleScholarGoogle Scholar |

Willers, N., Martin, G. B., Matson, P., Mawson, P. R., Morris, K., and Bencini, R. (2015). Finding the balance: fertility control for the management of fragmented populations of a threatened rock-wallaby species. Animals (Basel) 5, 1329–1344.
Finding the balance: fertility control for the management of fragmented populations of a threatened rock-wallaby species.Crossref | GoogleScholarGoogle Scholar | 26694471PubMed |

Wilson, M. E., Coulson, G., Shaw, G., and Renfree, M. B. (2013). Deslorelin implants in free-ranging female eastern grey kangaroos (Macropus giganteus): mechanism of action and contraceptive efficacy. Wildl. Res. 40, 403–412.
Deslorelin implants in free-ranging female eastern grey kangaroos (Macropus giganteus): mechanism of action and contraceptive efficacy.Crossref | GoogleScholarGoogle Scholar |

Yen, S. S. C., VandenBerg, G., Rebar, R., and Ehara, Y. (1972). Variation of pituitary responsiveness to synthetic LRF during different phases of the menstrual cycle. J. Clin. Endocrinol. Metab. 35, 931–934.
Variation of pituitary responsiveness to synthetic LRF during different phases of the menstrual cycle.Crossref | GoogleScholarGoogle Scholar |