Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Variable duration of reproductive suppression in male coyotes (Canis latrans) treated with a high dose of the gonadotrophin-releasing hormone agonist deslorelin

Marjorie J. MacGregor A E , Cheryl S. Asa B C and Donal C. Skinner A D
+ Author Affiliations
- Author Affiliations

A Department of Zoology and Physiology, University of Wyoming, Department 3166, 1000 E. University Avenue, Laramie, WY 82070, USA.

B Research Department, Saint Louis Zoo, 1 Government Drive, St. Louis, MO 63110, USA.

C AZA Wildlife Contraception Center, Saint Louis Zoo, 1 Government Drive, St. Louis, MO, USA.

D Program in Neuroscience, University of Wyoming, University of Wyoming, Department 3166, 1000 E. University Avenue, Laramie, WY 82070, USA.

E Corresponding author. Email: marjiem@uwyo.edu

Reproduction, Fertility and Development 29(7) 1271-1279 https://doi.org/10.1071/RD15253
Submitted: 25 June 2015  Accepted: 31 March 2016   Published: 10 May 2016

Abstract

Effective and humane management strategies for coyotes (Canis latrans) remain elusive. We hypothesised that exposure to a high dose of a gonadotrophin-releasing hormone (GnRH) agonist would cause prolonged suppression of the reproductive axis. Two groups of male coyotes were administered 47 mg deslorelin in the form of either five 9.4-mg controlled-release Suprelorin (Peptech Animal Health, Macquarie Park NSW, Australia) implants (n = 3) or 10 4.7-mg implants (n = 5). In the first group, deslorelin suppressed plasma LH, testosterone and testes volume in two of three coyotes for three breeding seasons. In the second group, two of five deslorelin-treated coyotes had no sperm production after 1 year and plasma LH, FSH, testosterone and testes volume were suppressed. Although plasma gonadotropins and testosterone were suppressed in three treated coyotes in group two, testes volume and sperm production were evident. Because the duration of suppression differed among individual coyotes, we further hypothesised that a variation in deslorelin release underlay the variability. To test this, we analysed in vivo plasma profiles of deslorelin concentrations. These profiles suggested that deslorelin concentrations >100 pg mL–1 are required to maintain suppression in male coyotes. For field implementation, the development of an implant capable of releasing deslorelin for the life of the coyote is necessary.

Additional keywords: contraception, fertility, neuroendocrinology, testosterone, wildlife.


References

Amoss, M. S., Jr, and Hodges, C. M. (1995). Selected parameters of the reproductive physiology and endocrinology of coyotes. In ‘Symposium Proceedings – Coyotes in the Southwest: A Compendium of our Knowledge’. (Eds D. Rollins, C. Richardson, T. Blankenship, K. Canon and S. Henke) p. 44. (University of Nebraska – Lincoln Press.)

Arslan, M., Lobo, J., Zaidi, A., Jalali, S., and Qazi, M. (1978). Annual androgen rhythm in the spiny-tailed lizard, (Uromastix hardwicki). Gen. Comp. Endocrinol. 36, 16–22.
Annual androgen rhythm in the spiny-tailed lizard, (Uromastix hardwicki).CrossRef | 1:CAS:528:DyaE1cXlvFChsL4%3D&md5=a9694a0cb9fccede7f014e412c93994aCAS | 730036PubMed |

Asa, C. S., Porton, I. J., Baker, A., and Plotka, E. D. (1993). Contraception as a management tool for controlling surplus animals. In ‘Wild Mammals in Captivity: Principles and Techniques for Zoo Management’. (Eds D. G. Kleiman, K. V. Thompson, and C. Baer.) pp. 469–482. (University of Chicago Press.)

Aspden, W. J., Rao, A., Scott, P. T., Clarke, I. J., Trigg, T. E., Walsh, J., and D’Occhio, M. J. (1996). Direct actions of the luteinizing hormone-releasing hormone agonist, deslorelin, on anterior pituitary contents of luteinizing hormone (LH) and follicle-stimulating hormone (FSH), LH and FSH subunit messenger ribonucleic acid, and plasma concentrations of LH and FSH in castrated male cattle. Biol. Reprod. 55, 386–392.
Direct actions of the luteinizing hormone-releasing hormone agonist, deslorelin, on anterior pituitary contents of luteinizing hormone (LH) and follicle-stimulating hormone (FSH), LH and FSH subunit messenger ribonucleic acid, and plasma concentrations of LH and FSH in castrated male cattle.CrossRef | 1:CAS:528:DyaK28XltlGitbY%3D&md5=963cfe60a7f37d5c17c834bc1aebec13CAS | 8828844PubMed |

Bex, F., Bartke, A., Goldman, B., and Dalterio, S. (1978). Prolactin, growth hormone, luteinizing hormone receptors and seasonal changes in testicular activity in the golden hamster. Endocrinology 103, 2069–2080.
Prolactin, growth hormone, luteinizing hormone receptors and seasonal changes in testicular activity in the golden hamster.CrossRef | 1:CAS:528:DyaE1MXosVCnsA%3D%3D&md5=9c721a3f45dafe9baf17491dbd737791CAS | 218802PubMed |

Bromley, C., and Gese, E. M. (2001a). Effects of sterilization on territory fidelity and maintenance, pair bonds, and survival rates of free-ranging coyotes. Can. J. Zool. 79, 386–392.
Effects of sterilization on territory fidelity and maintenance, pair bonds, and survival rates of free-ranging coyotes.CrossRef |

Bromley, C., and Gese, E. M. (2001b). Surgical sterilization as a method of reducing coyote predation on domestic sheep. J. Wildl. Manage. 65, 510–519.
Surgical sterilization as a method of reducing coyote predation on domestic sheep.CrossRef |

Chikamori, K., Suehiro, F., Ogawa, T., Sato, K., Mori, H., Oshima, I., and Saito, S. (1981). Distribution volume, metabolic clearance and plasma half disappearance time of exogenous luteinizing hormone releasing hormone in normal women and women with obesity and anorexia nervosa. Acta Endocrinol. (Copenh.) 96, 1–6.
| 1:STN:280:DyaL3M7gsFGhuw%3D%3D&md5=80ea6073d07de7133fd7db765922ee96CAS | 7006293PubMed |

Courty, Y., and Dufaure, J. L. (1979). Levels of testosterone in the plasma and testis of the viviparous lizard (Lacerta vivipara jacquin) during the annual cycle. Gen. Comp. Endocrinol. 39, 336–342.
Levels of testosterone in the plasma and testis of the viviparous lizard (Lacerta vivipara jacquin) during the annual cycle.CrossRef | 1:CAS:528:DyaE1MXmtVOkt78%3D&md5=7378815bad78640901700d1555584039CAS | 499760PubMed |

Cutuly, E., McCullagh, D., and Cutuly, E. (1938). Effects of androgenic steroids in hypophysectomized and in castrated rats. Am. J. Physiol. 121, 786–793.
| 1:CAS:528:DyaA1cXisVOlsw%3D%3D&md5=019db1d25f877b5b471518f346ca54bfCAS |

Edwards, B., Smith, A., and Skinner, D. C. (2013). Dose and durational effects of the gonadotropin-releasing hormone agonist, deslorelin: the male rat (Rattus norvegicus) as a model. J. Zoo Wildl. Med. 44, S97–S101.
Dose and durational effects of the gonadotropin-releasing hormone agonist, deslorelin: the male rat (Rattus norvegicus) as a model.CrossRef | 24437089PubMed |

Emons, G., Gr, C., Westphalen, S., Kavanagh, J., and Verschraegen, C. (2003). GnRH antagonists in the treatment of gynecological and breast cancers. Endocr. Relat. Cancer 10, 291–299.
GnRH antagonists in the treatment of gynecological and breast cancers.CrossRef | 1:CAS:528:DC%2BD3sXmsFCrs70%3D&md5=9fed798df54e293d9d7c8ff911101ee7CAS | 12790790PubMed |

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 | 1:CAS:528:DC%2BD2sXht1eqsrzL&md5=c5d18857cb385939e4d9fff0e60857d4CAS | 18076822PubMed |

Gentil, M., Hoffmann, B., Spang, A., Failing, K., and Goericke-Pesch, S. (2012). Restart of steroidogenesis in dogs during recrudescence of testicular function following downregulation with a GnRH-agonist implant. Cell Tissue Res. 350, 513–523.
Restart of steroidogenesis in dogs during recrudescence of testicular function following downregulation with a GnRH-agonist implant.CrossRef | 1:CAS:528:DC%2BC38Xhslaqt7jN&md5=0878a4cafb39b1f4f5a63f9751c2da02CAS | 23053053PubMed |

Green, J. S., Adair, R. A., Woodruff, R. A., and Stellflug, J. N. (1984). Seasonal variation in semen production by captive coyotes. J. Mammal. 65, 506–509.
Seasonal variation in semen production by captive coyotes.CrossRef |

Green, J. S., Knowlton, F. F., Pitt, W. C., and O’Shea, T. J. (2002). Reproduction in captive wild-caught coyotes (Canis latrans). J. Mammal. 83, 501–506.
Reproduction in captive wild-caught coyotes (Canis latrans).CrossRef |

Herbert, C. A., Trigg, T. E., and Cooper, D. W. (2004a). Effect of deslorelin implants on follicular development, parturition and post-partum oestrus in the tammar wallaby (Macropus eugenii). Reproduction 127, 265–273.
Effect of deslorelin implants on follicular development, parturition and post-partum oestrus in the tammar wallaby (Macropus eugenii).CrossRef | 1:CAS:528:DC%2BD2cXitVWrtL0%3D&md5=a49a51373ec27c6721a67e1989e271e9CAS | 15056792PubMed |

Herbert, C. A., Trigg, T. E., Renfree, M. B., Shaw, G., Eckery, D. C., and Cooper, D. W. (2004b). 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 | 1:CAS:528:DC%2BD2cXktlOmtLg%3D&md5=96db24e8565163bfa8fe0fb02a6d2c6aCAS | 14973259PubMed |

Hopkinson, C. R. N., Pant, H. C., and Fitzpatrick, R. J. (1974). Release of LH and FSH in the normal intact ram by synthetic LH-RF and the effect of pretreatment with testosterone propionate. J. Reprod. Fertil. 39, 135–139.
Release of LH and FSH in the normal intact ram by synthetic LH-RF and the effect of pretreatment with testosterone propionate.CrossRef | 1:CAS:528:DyaE2cXltlWit70%3D&md5=2e6734eca534dfb459c772066cd4bb3aCAS |

Junaidi, A., Williamson, P., Martin, G., Blackberry, M., Cummins, J., and Trigg, T. (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 | 1:CAS:528:DC%2BD1MXhtlSjt7nE&md5=6f69f895d3f7729633309dd7f3e42998CAS | 19769638PubMed |

Kaku, H., Saika, T., Tsushima, T., Ebara, S., Senoh, T., Yamato, T., Nasu, Y., and Kumon, H. (2006). Time course of serum testosterone and luteinizing hormone levels after cessation of long-term luteinizing hormone-releasing hormone agonist treatment in patients with prostate cancer. Prostate 66, 439–444.
Time course of serum testosterone and luteinizing hormone levels after cessation of long-term luteinizing hormone-releasing hormone agonist treatment in patients with prostate cancer.CrossRef | 1:CAS:528:DC%2BD28XivVCku7o%3D&md5=b4c1d13031ad7d1e93d92f483309f114CAS | 16329145PubMed |

Knowlton, F. F., Gese, E. M., and Jaeger, M. M. (1999). Coyote depredation control: an interface between biology and management. J. Range Manage. 52, 398–412.
Coyote depredation control: an interface between biology and management.CrossRef |

Labrie, F., Dupont, A., Belanger, A., St-Arnaud, R., Giguere, M., Lacourciere, Y., Emond, J., and Monfette, G. (1986). Treatment of prostate cancer with gonadotropin-releasing hormone agonists. Endocr. Rev. 7, 67–74.
Treatment of prostate cancer with gonadotropin-releasing hormone agonists.CrossRef | 1:STN:280:DyaL287msVWmtA%3D%3D&md5=1d828911ddf4e19ec966b6829fbe8d9eCAS | 3514203PubMed |

Lahlou, N., Carel, J.-C., Chaussain, J.-L., and Roger, M. (2000). Pharmacokinetics and pharmacodynamics of GnRH agonists: clinical implications in pediatrics. J. Pediatr. Endocrinol. Metab. 13, 723–738.
Pharmacokinetics and pharmacodynamics of GnRH agonists: clinical implications in pediatrics.CrossRef | 10969915PubMed |

Lincoln, G. A. (1998). Reproductive seasonality and maturation throughout the complete life-cycle in the mouflon ram (Ovis musimon). Anim. Reprod. Sci. 53, 87–105.
Reproductive seasonality and maturation throughout the complete life-cycle in the mouflon ram (Ovis musimon).CrossRef | 1:CAS:528:DyaK1cXns1yksLc%3D&md5=ff09727a09492ee5b639aa24254c9108CAS | 9835369PubMed |

Lincoln, G. A., Lincoln, C. E., and McNeilly, A. S. (1990). Seasonal cycles in the blood plasma concentration of FSH, inhibin and testosterone, and testicular size in rams of wild, feral and domesticated breeds of sheep. J. Reprod. Fertil. 88, 623–633.
Seasonal cycles in the blood plasma concentration of FSH, inhibin and testosterone, and testicular size in rams of wild, feral and domesticated breeds of sheep.CrossRef | 1:CAS:528:DyaK3cXhslaltbw%3D&md5=3af7a98b232efe797109ca79238d2a3aCAS | 2109070PubMed |

Ludwig, D. J. (1950). The effect of androgen on spermatogenesis. Endocrinology 46, 453–481.
The effect of androgen on spermatogenesis.CrossRef | 1:CAS:528:DyaG3cXksVKmsg%3D%3D&md5=956073841fbfd66d68f59e0b9c7fc776CAS | 15414821PubMed |

Lunn, S. F., Dixson, A. F., Sandow, J., and Fraser, H. M. (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 | 1:CAS:528:DyaK3cXktlCqsL0%3D&md5=7696e5deb54ec18a6a768caa6b9dd486CAS | 2165119PubMed |

MacGregor, M. J., Perkins, E. G., Asa, C., and Skinner, D. C. (2013). Contraception has gone to the coyotes. J. Zoo Wildl. Med. 44, S4–S8.
Contraception has gone to the coyotes.CrossRef | 24437078PubMed |

Marshall, G. R., Jockenhövel, F., Lüdecke, D., and Nieschlag, E. (1986). Maintenance of complete but quantitatively reduced spermatogenesis in hypophysectomized monkeys by testosterone alone. Acta Endocrinol. (Copenh.) 113, 424–431.
| 1:CAS:528:DyaL2sXhtlWgsQ%3D%3D&md5=1428cba70c61c6292fbdd4a2131e06feCAS | 3788416PubMed |

Minter, L. J., and DeLiberto, T. J. (2008). Seasonal variation in serum testosterone, testicular volume, and semen characteristics in the coyote (Canis latrans). Theriogenology 69, 946–952.
Seasonal variation in serum testosterone, testicular volume, and semen characteristics in the coyote (Canis latrans).CrossRef | 1:CAS:528:DC%2BD1cXks12gt7k%3D&md5=45e240bb7caaf8431054a3cddddd14bbCAS | 18359065PubMed |

Monfort, S., Brown, J., Wood, T., Bush, M., Williamson, L., and Wildt, D. (1995). Effects of long-term continuous GnRH administration on the pituitary–gonadal axis in Eld’s deer stags (Cervus eldi thamin). Can. J. Zool. 73, 1609–1619.
Effects of long-term continuous GnRH administration on the pituitary–gonadal axis in Eld’s deer stags (Cervus eldi thamin).CrossRef | 1:CAS:528:DyaK28Xjt1Wgsg%3D%3D&md5=ac3ee7089cabae1f041283dea37f0030CAS |

Mul, D., and Hughes, I. (2008). The use of GnRH agonists in precocious puberty. Eur. J. Endocrinol. 159, S3–S8.
The use of GnRH agonists in precocious puberty.CrossRef | 1:CAS:528:DC%2BD1MXhtFOnsLs%3D&md5=14199df521878f87a17cf6c7d28cceaeCAS | 19064674PubMed |

Oefelein, M. G. (1998). Time to normalization of serum testosterone after 3-month luteinizing hormone-releasing hormone agonist administered in the neoadjuvant setting: implications for dosing schedule and neoadjuvant study consideration. J. Urol. 160, 1685–1688.
Time to normalization of serum testosterone after 3-month luteinizing hormone-releasing hormone agonist administered in the neoadjuvant setting: implications for dosing schedule and neoadjuvant study consideration.CrossRef | 1:CAS:528:DyaK1cXmvFSmsbk%3D&md5=0675593ce809c00ad9c171b0f02bd3c3CAS | 9783932PubMed |

Patton, M. L., Bashaw, M. J., del Castillo, S. M., Jöchle, W., Lamberski, N., Rieches, R., and Bercovitch, F. B. (2006). Long-term suppression of fertility in female giraffe using the GnRH agonist deslorelin as a long-acting implant. Theriogenology 66, 431–438.
Long-term suppression of fertility in female giraffe using the GnRH agonist deslorelin as a long-acting implant.CrossRef | 1:CAS:528:DC%2BD28Xmt1Gktrw%3D&md5=cdddc1940ed163614ed83cc5f11650c5CAS | 16423382PubMed |

Pelletier, J. (1976). Influence of LH-RF on LH and FSH releases in domestic mammals. Ann. Biol. Anim. Biochim. Biophys. 16, 213–234.
Influence of LH-RF on LH and FSH releases in domestic mammals.CrossRef | 1:CAS:528:DyaE28XhsF2rt7w%3D&md5=f4ba3a4c352c8a3375a757691c29c0bcCAS |

Penfold, L., Ball, R., Burden, I., Joechle, W., Citino, S., Monfort, S., and Wielebnowski, N. (2002). Case studies in antelope aggression control using a GnRH agonist. Zoo Biol. 21, 435–448.
Case studies in antelope aggression control using a GnRH agonist.CrossRef | 1:CAS:528:DC%2BD38XovFWhtrY%3D&md5=627ae9a54d62517992df32a1ab77cd05CAS |

Rubion, S., and Driancourt, M. (2009). Controlled delivery of a GnRH agonist by a silastic implant (Gonazon) results in long-term contraception in queens. Reprod. Domest. Anim. 44, 79–82.
Controlled delivery of a GnRH agonist by a silastic implant (Gonazon) results in long-term contraception in queens.CrossRef | 19754541PubMed |

Sacks, B. N., Jaeger, M. M., Neale, J. C., and McCullough, D. R. (1999). Territoriality and breeding status of coyotes relative to sheep predation. J. Wildl. Manage. 63, 593–605.
Territoriality and breeding status of coyotes relative to sheep predation.CrossRef |

Schou, J. (1961). Absorption of drugs from subcutaneous connective tissue. Pharmacol. Rev. 13, 441–464.
| 1:CAS:528:DyaF3MXhtlyqsr4%3D&md5=a257fce611af7d6a3769a3945f392231CAS | 13748537PubMed |

Seidler, R. (2009). Surgical sterilization of coyotes to reduce predation on pronghorn fawns. MS Thesis, Utah State University, Logan, .

Seidler, R. G., and Gese, E. M. (2012). Territory fidelity, space use, and survival rates of wild coyotes following surgical sterilization. J. Ethol. 30, 1–10.
Territory fidelity, space use, and survival rates of wild coyotes following surgical sterilization.CrossRef |

Smith, A. W., Asa, C. S., Edwards, B. S., Murdoch, W. J., and Skinner, D. C. (2012). Predominant suppression of FSHβ-immunoreactivity after long-term treatment of intact and castrate adult male rats with the GnRH agonist deslorelin. J. Neuroendocrinol. 24, 737–747.
Predominant suppression of FSHβ-immunoreactivity after long-term treatment of intact and castrate adult male rats with the GnRH agonist deslorelin.CrossRef | 1:CAS:528:DC%2BC38Xmsl2htrY%3D&md5=8d65ba727882f7d18e9c166504003ab1CAS | 22172059PubMed |

Till, J. A., and Knowlton, F. F. (1983). Efficacy of denning in alleviating coyote depredations upon domestic sheep. J. Wildl. Manage. 47, 1018–1025.
Efficacy of denning in alleviating coyote depredations upon domestic sheep.CrossRef |

Trigg, T. E., Wright, P. J., Armour, A. F., Williamson, P. E., Junaidi, A., Martin, G. B., Doyle, A. G., 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.
| 1:CAS:528:DC%2BD3MXktF2qtrs%3D&md5=6d1088762f18fb66846068bcdfeab346CAS | 11787159PubMed |

Trigg, T. E., Doyle, A. G., Walsh, J. D., and Swangchan-Uthai, T. (2006). A review of advances in the use of the GnRH agonist deslorelin in control of reproduction. Theriogenology 66, 1507–1512.
A review of advances in the use of the GnRH agonist deslorelin in control of reproduction.CrossRef | 1:CAS:528:DC%2BD28Xps1Oitrc%3D&md5=8628825b27431fd07af1fa972a8e070aCAS | 16600356PubMed |

Vickery, B. H., McRae, G. I., Briones, W., Worden, A., Seidenberg, R., Schanbacher, B. D., and Falvo, R. (1984). Effects of an LHRH agonist analog upon sexual function in male dogs. J. Androl. 5, 28–42.
Effects of an LHRH agonist analog upon sexual function in male dogs.CrossRef | 1:CAS:528:DyaL2cXktVWisLs%3D&md5=fa2ae3e6c51d04f2de46b7ba870ef9c5CAS | 6231277PubMed |

Wagner, J. G. (1975). ‘Fundamentals of Clinical Pharmacokinetics.’ (Drug Intelligence Publications: Hamilton, IL.)

Wagner, F. H. (1988). ‘Predator Control and the Sheep Industry: The Role of Science in Policy Formation.’ (Regina Books: Claremont CA)

Weil, M. R. (1985). Comparison of plasma and testicular testosterone levels during the active season in the common garter snake, Thamnophis sirtalis. Comp. Biochem. Physiol. A. Comp. Physiol. 81, 585–587.
Comparison of plasma and testicular testosterone levels during the active season in the common garter snake, Thamnophis sirtalis.CrossRef | 1:STN:280:DyaL2M3otlKrsw%3D%3D&md5=14e919a52cc9912733c62bf22328a601CAS | 2863045PubMed |

Zhang, F.-P., Pakarainen, T., Poutanen, M., Toppari, J., and Huhtaniemi, I. (2003). The low gonadotropin-independent constitutive production of testicular testosterone is sufficient to maintain spermatogenesis. Proc. Natl Acad. Sci. USA 100, 13 692–13 697.
The low gonadotropin-independent constitutive production of testicular testosterone is sufficient to maintain spermatogenesis.CrossRef | 1:CAS:528:DC%2BD3sXptFOiur8%3D&md5=1cfc42d0dcb813d63a9db9e523404837CAS |



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