Hormone-induced spawning of the critically endangered northern corroboree frog Pseudophryne pengilleyi
Aimee J. Silla A C , Michael McFadden B and Phillip G. Byrne AA Centre for Sustainable Ecosystem Solutions, School of Biological Sciences, University of Wollongong, Wollongong, NSW 2522, Australia.
B Herpetofauna Department, Taronga Conservation Society Australia, PO Box 20, Mosman, NSW 2088, Australia.
C Corresponding author. Email: aimee.silla@gmx.com
Reproduction, Fertility and Development 30(10) 1352-1358 https://doi.org/10.1071/RD18011
Submitted: 9 January 2018 Accepted: 21 March 2018 Published: 26 April 2018
Abstract
Fundamental knowledge of the optimal hormone concentrations required to stimulate amplexus and spawning in breeding pairs of amphibians is currently lacking, hindering our understanding of the proximate mechanisms underpinning mating behaviour. The present study investigated the effects of: (1) the dose of a gonadotropin-releasing hormone analogue (GnRH-a) administered; (2) male–female hormone administration interval; and (3) topical application of GnRH-a, on spawning success in the northern corroboree frog. Administration of GnRH-a at doses of 0.5, 1.0 and 2.0 μg g−1 were highly successful, with a significantly greater proportion of hormone-treated pairs ovipositing (89–100%) compared with the 0 μg g−1 treatment (22%). Of the hormone-treated pairs, those receiving 0.5 μg g−1 GnRH-a exhibited the highest fertilisation success (61%). Administration of GnRH-a to males and females simultaneously (0 h) was more effective than injecting males either 48 or 24 h before the injection of females. Overall, administration of GnRH-a was highly successful at inducing spawning in northern corroboree frogs. For the first time, we also effectively induced spawning following the topical application of GnRH-a to the ventral pelvic region. Topical application of GnRH-a eliminates the need for specialised training in amphibian injection, and will allow assisted reproductive technologies to be adopted by a greater number of captive facilities globally.
Additional keywords: amphibian, assisted reproductive technologies, captive breeding, conservation, gamete release, gonadotropin-releasing hormone (GnRH), LH-releasing hormone, reproduction.
References
Bromage, N., Bruce, M., Basavaraja, N., Rana, K., Shields, R., Young, C., Dye, J., Smith, P., Gillespie, M., and Gamble, J. (1994). Egg quality determinants in finfish the role of overripening with special reference to the timing of stripping in the Atlantic halibut Hippoglossus hippoglossus. J. World Aquacult. Soc. 25, 13–21.| Egg quality determinants in finfish the role of overripening with special reference to the timing of stripping in the Atlantic halibut Hippoglossus hippoglossus.Crossref | GoogleScholarGoogle Scholar |
Browne, R. K., Seratt, J., Vance, C., and Kouba, A. (2006). Hormonal priming, induction of ovulation and in-vitro fertilization of the endangered Wyoming toad (Bufo baxteri). Reprod. Biol. Endocrinol. 4, 34.
| Hormonal priming, induction of ovulation and in-vitro fertilization of the endangered Wyoming toad (Bufo baxteri).Crossref | GoogleScholarGoogle Scholar |
Byrne, P. G., and Silla, A. J. (2010). Hormonal induction of gamete release, and in-vitro fertilisation, in the critically endangered Southern Corroboree Frog, Pseudophryne corroboree. Reprod. Biol. Endocrinol. 8, 144.
| Hormonal induction of gamete release, and in-vitro fertilisation, in the critically endangered Southern Corroboree Frog, Pseudophryne corroboree.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFelu7rE&md5=25a09ebcd669057e47088d1401085670CAS |
Calatayud, N. E., Langhorne, C. J., Mullen, A. C., Williams, C. L., Smith, T., Bullock, L., Kouba, A. J., and Willard, S. T. (2015). A hormone priming regimen and hibernation affect oviposition in the boreal toad (Anaxyrus boreas boreas). Theriogenology 84, 600–607.
| A hormone priming regimen and hibernation affect oviposition in the boreal toad (Anaxyrus boreas boreas).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXot1Wlsrg%3D&md5=dea8d7e29ead8591ecb3476ad1765bc4CAS |
Calatayud, N. E., Mullen, A. K., and Langhorne, C. J. (2017). Induction of reproductive behaviors by exogenous hormones in captive Southern Rocky Mountain boreal toads, Anaxyrus boreas boreas. bioRxiv 2017, 131–763.
| Induction of reproductive behaviors by exogenous hormones in captive Southern Rocky Mountain boreal toads, Anaxyrus boreas boreas.Crossref | GoogleScholarGoogle Scholar |
Ceballos, G., Ehrlich, P. R., Barnosky, A. D., García, A., Pringle, R. M., and Palmer, T. M. (2015). Accelerated modern human-induced species losses: entering the sixth mass extinction. Sci. Adv. 1, e1400253.
| Accelerated modern human-induced species losses: entering the sixth mass extinction.Crossref | GoogleScholarGoogle Scholar |
Conn, P. M. (1986). The molecular basis of gonadotropin-releasing hormone action. Endocr. Rev. 7, 3–10.
| The molecular basis of gonadotropin-releasing hormone action.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XitVShsbc%3D&md5=9737cf645ff064c8ba1caab2d1e98314CAS |
Della Togna, G., Trudeau, V. L., Gratwicke, B., Evans, M., Augustine, L., Chia, H., Bronikowski, E. J., Murphy, J. B., and Comizzoli, P. (2017). Effects of hormonal stimulation on the concentration and quality of excreted spermatozoa in the critically endangered Panamanian golden frog (Atelopus zeteki). Theriogenology 91, 27–35.
| Effects of hormonal stimulation on the concentration and quality of excreted spermatozoa in the critically endangered Panamanian golden frog (Atelopus zeteki).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXlt1ynuw%3D%3D&md5=1f64373bb71554c5f4e313d2d6f76352CAS |
Durrant, B. S. (2009). The importance and potential of artificial insemination in CANDES (companion animals, non-domestic, endangered species). Theriogenology 71, 113–122.
| The importance and potential of artificial insemination in CANDES (companion animals, non-domestic, endangered species).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cjnt1Snsg%3D%3D&md5=3f858c51cf6faa3ab76bc3d34aadab4eCAS |
Gore, A. C. (2002) ‘GnRH: The Master Molecule of Reproduction.’ (Springer Science & Business Media: New York.)
Jacobs, L. E., Robertson, J. M., and Kaiser, K. (2016). Variation in male spermiation response to exogenous hormones among divergent populations of red-eyed treefrogs. Reprod. Biol. Endocrinol. 14, 83.
| Variation in male spermiation response to exogenous hormones among divergent populations of red-eyed treefrogs.Crossref | GoogleScholarGoogle Scholar |
Kouba, A. J., Vance, C. K., and Willis, E. L. (2009). Artificial fertilization for amphibian conservation: current knowledge and future considerations. Theriogenology 71, 214–227.
| Artificial fertilization for amphibian conservation: current knowledge and future considerations.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cjnt1yqtg%3D%3D&md5=1c822bb0de33f3a6ca4f3f2bb3087157CAS |
Mansour, N., Lahnsteiner, F., and Patzner, R. A. (2011). Collection of gametes from live axolotl, Ambystoma mexicanum, and standardization of in vitro fertilization. Theriogenology 75, 354–361.
| Collection of gametes from live axolotl, Ambystoma mexicanum, and standardization of in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsF2isbbP&md5=91bb46ffbbc732d6d6cc13f59cbe58c8CAS |
McFadden, M., Hunter, D., Evans, M., Scheele, B., Pietsch, R., and Harlow, P. (2016). Re-introduction of the northern corroboree frog in the Northern Brindabella Mountains, New South Wales, Australia. In ‘Global Re-introduction Perspectives: 2016. Case-Studies From Around the Globe’. (Ed. P. S. Soorae.) pp. 35–39. (Gland, Switzerland: IUCN/SSC Re-introduction Specialist Group and Abu Dhabi. UAE: Environment Agency.)
Michael, S. F., Buckley, C., Toro, E., Estrada, A. R., and Vincent, S. (2004). Induced ovulation and egg deposition in the direct developing anuran Eleutherodactylus coqui. Reprod. Biol. Endocrinol. 2, 6.
| Induced ovulation and egg deposition in the direct developing anuran Eleutherodactylus coqui.Crossref | GoogleScholarGoogle Scholar |
Obringer, A. R., O’Brien, J. K., Saunders, R. L., Yamamoto, K., Kikuyama, S., and Roth, T. L. (2000). Characterization of the spermiation response, luteinizing hormone release and sperm quality in the American toad (Bufo americanus) and the endangered Wyoming toad (Bufo baxteri). Reprod. Fertil. Dev. 12, 51–58.
| Characterization of the spermiation response, luteinizing hormone release and sperm quality in the American toad (Bufo americanus) and the endangered Wyoming toad (Bufo baxteri).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhtlKlug%3D%3D&md5=630e4a76792b8d53aa2173ebb734ec6dCAS |
Osborne, W. S. (1991). The biology and management of the corroboree frog (Pseudophryne corroboree) in NSW. Species Management Report no. 8, NSW National Parks and Wildlife Service, Hurstville.
Rowson, A. D., Obringer, A. R., and Roth, T. L. (2001). Non‐invasive treatments of luteinizing hormone‐releasing hormone for inducing spermiation in American (Bufo americanus) and Gulf Coast (Bufo valliceps) toads. Zoo Biol. 20, 63–74.
| Non‐invasive treatments of luteinizing hormone‐releasing hormone for inducing spermiation in American (Bufo americanus) and Gulf Coast (Bufo valliceps) toads.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlt1Gmurc%3D&md5=fd54159560b6095cb4790507f977065fCAS |
Scheele, B. C., Hunter, D. A., Brannelly, L. A., Skerratt, L. F., and Driscoll, D. A. (2017). Reservoir-host amplification of disease impact in an endangered amphibian. Conserv. Biol. 31, 592–600.
| Reservoir-host amplification of disease impact in an endangered amphibian.Crossref | GoogleScholarGoogle Scholar |
Silla, A. J. (2010). Effects of luteinizing hormone-releasing hormone and arginine-vasotocin on the sperm-release response of Günther’s toadlet, Pseudophryne guentheri. Reprod. Biol. Endocrinol. 8, 139.
| Effects of luteinizing hormone-releasing hormone and arginine-vasotocin on the sperm-release response of Günther’s toadlet, Pseudophryne guentheri.Crossref | GoogleScholarGoogle Scholar |
Silla, A. J. (2011). Effect of priming injections of luteinizing hormone-releasing hormone on spermiation and ovulation in Günther’s toadlet, Pseudophryne guentheri. Reprod. Biol. Endocrinol. 9, 68.
| Effect of priming injections of luteinizing hormone-releasing hormone on spermiation and ovulation in Günther’s toadlet, Pseudophryne guentheri.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmvVKrt7k%3D&md5=b95bdbcda1c6e04c8a9ac836c687f654CAS |
Silla, A. J. (2013). Artificial fertilisation in a terrestrial toadlet (Pseudophryne guentheri): effect of medium osmolality, sperm concentration and gamete storage. Reprod. Fertil. Dev. 25, 1134–1141.
| Artificial fertilisation in a terrestrial toadlet (Pseudophryne guentheri): effect of medium osmolality, sperm concentration and gamete storage.Crossref | GoogleScholarGoogle Scholar |
Silla, A. J., and Roberts, J. D. (2012). Investigating patterns in the spermiation response of eight Australian frogs administered human chorionic gonadotropin (hCG) and luteinizing hormone-releasing hormone (LHRHa). Gen. Comp. Endocr. 179, 128–136.
| Investigating patterns in the spermiation response of eight Australian frogs administered human chorionic gonadotropin (hCG) and luteinizing hormone-releasing hormone (LHRHa).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtlKjsr3J&md5=26faf7e50c0ba3a2566a87c0f139bdccCAS |
Silla, A. J., Keogh, L. M., and Byrne, P. G. (2015). Antibiotics and oxygen availability affect the short-term storage of spermatozoa from the critically endangered booroolong frog, Litoria booroolongensis. Reprod. Fertil. Dev. 27, 1147–1153.
| Antibiotics and oxygen availability affect the short-term storage of spermatozoa from the critically endangered booroolong frog, Litoria booroolongensis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhs1Glu7jO&md5=711d29a1134114d6c74b33eeb850f3f9CAS |
Stuart, S. N., Chanson, J. S., Cox, N. A., Young, B. E., Rodrigues, A. S., Fischman, D. L., and Waller, R. W. (2004). Status and trends of amphibian declines and extinctions worldwide. Science 306, 1783–1786.
| Status and trends of amphibian declines and extinctions worldwide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVKitb7E&md5=6d0459f3766f5b6be79b0f6b8048de48CAS |
Toledo, R. C., and Jared, C. (1993). Cutaneous adaptations to water balance in amphibians. Comp. Biochem. Physiol. Part A. Physiol. 105, 593–608.
| Cutaneous adaptations to water balance in amphibians.Crossref | GoogleScholarGoogle Scholar |
Trudeau, V. L., Somoza, G. M., Natale, G. S., Pauli, B., Wignall, J., Jackman, P., Doe, K., and Schueler, F. W. (2010). Hormonal induction of spawning in 4 species of frogs by coinjection with a gonadotropin-releasing hormone agonist and a dopamine antagonist. Reprod. Biol. Endocrinol. 8, 36.
| Hormonal induction of spawning in 4 species of frogs by coinjection with a gonadotropin-releasing hormone agonist and a dopamine antagonist.Crossref | GoogleScholarGoogle Scholar |
Trudeau, V. L., Schueler, F. W., Navarro-Martin, L., Hamilton, C. K., Bulaeva, E., Bennett, A., Fletcher, W., and Taylor, L. (2013). Efficient induction of spawning of northern leopard frogs (Lithobates pipiens) during and outside the natural breeding season. Reprod. Biol. Endocrinol. 11, 14.
| Efficient induction of spawning of northern leopard frogs (Lithobates pipiens) during and outside the natural breeding season.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXksFGjt74%3D&md5=e480c6e7bfbb973cb31734c2cb00c291CAS |
Uteshev, V., Kaurova, S., Shishova, N., Stolyarov, S., Browne, R., and Gakhova, E. (2015). in vitro fertilization with hormonally induced sperm and eggs from sharp-ribbed newts Pleurodeles waltl. Russ. J. Herpetol. 22, .
Vu, M., and Trudeau, V. L. (2016). Neuroendocrine control of spawning in amphibians and its practical applications. Gen. Comp. Endocrinol. 234, 28–39.
| Neuroendocrine control of spawning in amphibians and its practical applications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XkvFGgsLw%3D&md5=d7b1407a4212da4b4c1eca64e90e666eCAS |
Watson, G. F., and Martin, A. A. (1973). Life history, larval morphology and relationships of Australian Leptodactylid frogs. Trans. R. Soc. S. Aust. 97, 33–45.