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Vertebrate reproductive science and technology
REVIEW

Applied reproductive technologies and genetic resource banking for amphibian conservation

Andrew J. Kouba A B C and Carrie K. Vance A B
+ Author Affiliations
- Author Affiliations

A Conservation and Research Department, Memphis Zoological Society, 2000 Prentiss Place, Memphis, TN 38112, USA.

B Department of Biochemistry and Molecular Cell Sciences, Mississippi State University, Mississippi State, MS 39759, USA.

C Corresponding author. Email: akouba@memphiszoo.org

Reproduction, Fertility and Development 21(6) 719-737 https://doi.org/10.1071/RD09038
Submitted: 21 February 2009  Accepted: 29 March 2009   Published: 1 July 2009

Abstract

As amphibian populations continue to decline, both government and non-government organisations are establishing captive assurance colonies to secure populations deemed at risk of extinction if left in the wild. For the most part, little is known about the nutritional ecology, reproductive biology or husbandry needs of the animals placed into captive breeding programs. Because of this lack of knowledge, conservation biologists are currently facing the difficult task of maintaining and reproducing these species. Academic and zoo scientists are beginning to examine different technologies for maintaining the genetic diversity of founder populations brought out of the wild before the animals become extinct from rapidly spreading epizootic diseases. One such technology is genetic resource banking and applied reproductive technologies for species that are difficult to reproduce reliably in captivity. Significant advances have been made in the last decade for amphibian assisted reproduction including the use of exogenous hormones for induction of spermiation and ovulation, in vitro fertilisation, short-term cold storage of gametes and long-term cryopreservation of spermatozoa. These scientific breakthroughs for a select few species will no doubt serve as models for future assisted breeding protocols and the increasing number of amphibians requiring conservation intervention. However, the development of specialised assisted breeding protocols that can be applied to many different families of amphibians will likely require species-specific modifications considering their wide range of reproductive modes. The purpose of this review is to summarise the current state of knowledge in the area of assisted reproduction technologies and gene banking for the conservation of amphibians.

Additional keywords: anuran, cryopreservation, frog, in vitro fertilisation, ovulation, reproduction, spermatozoa, toad.


Acknowledgements

Work presented by the authors was supported by the Morris Animal Foundation grant #DO1Z0–94 and the Institute of Museum and Library Services grant #IC-01–03–0199–03. We would also like to thank Dr Steve Reichling, Rachel Hansen, Deanna Lance, seasonal intern students and the herpetarium staff for their assistance with care and husbandry of research amphibians. Finally, we would like to thank Diane Barber and Bruce Foster for communications regarding the Wyoming toad and Puerto-Rican crested toad breeding programs.


References

Alexander, M. A. , and Eischeid, J. K. (2001). Climate variability in regions of amphibian declines. Conserv. Biol. 15(4), 930–942.
Crossref | GoogleScholarGoogle Scholar | Bennet P. M. (2001). Establishing animal germplasm resource banks for wildlife conservation: genetic, population and evolutionary aspects. In ‘Cryobanking the Genetic Resource: Wildlife Conservation for the Future?’. (Eds P. F. Watson and W. V. Holt.) pp. 47–67. (Taylor and Francis: London and New York.)

Biesinger, D. I. , and Miller, D. F. (1952). Seasonal and hormone-induced changes in the testes of Rana pipiens. Ohio J. Sci. 52(3), 169–175.
Blaustein A. R., and Belden L. K. (2005). Ultraviolet radiation. In ‘Amphibian Declines: Conservation Status of United States Species’. (Ed. M. Lannoo.) pp. 87–88. (University of California Press: Berkeley, LA.)

Blaustein, A. R. , Kiesecker, J. M. , Chivers, D. P. , and Anthony, R. G. (1997). Ambient UV-B radiation causes deformities in amphibian embryos. Proc. Natl. Acad. Sci. USA 94(25), 13 735–13 737.
Crossref | GoogleScholarGoogle Scholar | CAS | Bridges C. M., and Semlitsch R. D. (2005a). Xenobiotics. In ‘Amphibian Declines: Conservation Status of United States Species’. (Ed. M. Lannoo.) pp. 89–92. (University of California Press: Berkeley, LA.)

Bridges C. M., and Semlitsch R. D. (2005b). Variation in pesticide tolerance. In ‘Amphibian Declines: Conservation Status of United States Species’. (Ed. M. Lannoo.) pp. 93–95. (University of California Press: Berkeley, LA.)

Briggs, R. , and King, T. J. (1952). Transplantation of living nuclei from blastula cells into enucleated frogs eggs. Proc. Natl. Acad. Sci. USA 38, 455–463.
Crossref | GoogleScholarGoogle Scholar | CAS | Clulow J., Mahony M., Browne R., Pomering M., and Clark A. (1999). Applications of assisted reproductive technologies (ART) to endangered amphibian species. In ‘Declines and Disappearance of Australian Frogs’. (Ed. A. Campbell.) pp. 219–225. (Environment Australia: Canberra.)

Comizzoli, P. , Mermillod, P. , and Maugut, R. (2000). Reproductive biotechnologies for endangered mammalian species. Reprod. Nutr. Dev. 40, 493–504.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | Duellman W. E., and Trueb L. (1986). Enemies and defense. In ‘Biology of Amphibians’. pp. 241–260. (The Johns-Hopkins University Press: Baltimore.)

Easley, K. A. , Culley, D. D. , Horseman, N. D. , and Penkala, J. E. (1979). Environmental influences on hormonally induced spermiation of the bullfrog, Rana catesbeiana. J. Exp. Zool. 207, 407–416.
Crossref | GoogleScholarGoogle Scholar | CAS | Gascon C., Collins J. P., Moore R. D., Church D. R., McKay J. E., and Mendelson J. R.III (Eds) (2007). ‘Amphibian Conservation Action Plan.’ (IUCN/SSC Amphibian Specialist Group: Gland, Switzerland and Cambridge, UK.)

George, J. M. , Smita, M. , Kadalmani, B. , Girija, R. , Oommen, O. V. , and Akbarsha, M. A. (2005). Contribution of the secretory material of caecilian (Amphibian: Gymnophiona) male mullerian gland to motility of sperm: a study in Uraeotyphlus narayani. J. Morphol. 263, 227–237.
Crossref | GoogleScholarGoogle Scholar | PubMed | Green D. M. (2005). Biology of amphibian declines. In ‘Amphibian Declines: Conservation Status of United States Species’. (Ed. M. Lannoo.) pp. 28–33. (University of California Press: Berkeley, LA.)

Griffiths, R. A. , and Pavajeau, L. (2008). Captive breeding, reintroduction, and the conservation of amphibians. Conserv. Biol. 22(4), 852–861.
Crossref | GoogleScholarGoogle Scholar | PubMed | Hodges J. K. (2001). Reproductive technologies necessary for successful application of genetic resource banking. In ‘Cryobanking the Genetic Resource: Wildlife Conservation for the Future?’. (Eds P. F. Watson and W. V. Holt.) pp. 85–112. (Taylor and Francis: London and New York.)

Hollinger, T. G. , and Corton, G. L. (1980). Artificial fertilisation of gametes from the South African clawed frog, Xenopus laevis. Gamete Res. 3, 45–57.
Crossref | GoogleScholarGoogle Scholar | CAS | Holt W. V. (2001). Genetic resource banking and maintaining biodiversity. In ‘Cryobanking the Genetic Resource: Wildlife Conservation for the Future?’ (Eds P. F. Watson and W. V. Holt.) pp. 9–20. (Taylor and Francis: London and New York.)

Holt, W. V. , Bennett, P. M. , and Volobouev, V. (1996). Genetic resource banks in wildlife conservation. J. Zool. (Lond.) 238, 531–544.
Crossref | GoogleScholarGoogle Scholar | Howard J., Marinari P. E., and Wildt D. E. (2003). Black-footed ferret: model for assisted reproductive technologies contributing to in situ conservation. In ‘Reproductive Science and Integrated Conservation’. (Eds W. V. Holt, A. R. Pickard, J. C. Rodger and D. E. Wildt.) pp. 249–266. (Cambridge University Press: Cambridge.)

Iimori, E. , D’Occhio, M. J. , Lisle, A. T. , and Johnston, S. D. (2005). Testosterone secretion and pharmacological spermatozoal recovery in the cane toad. Anim. Reprod. Sci. 90, 163–173.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | IUCN, Conservation International, and NatureServe (2006). ‘Global Amphibian Assessment.’ Available at: www.globalamphibians.org [Accessed 4 May 2006].

Johnson C. J., Vance C. K., Roth T. L., and Kouba A. J. (2002). Oviposition and ultrasound monitoring of American toads (Bufo americanus) treated with exogenous hormones. In ‘Proceedings of the American Association of Zoo Veterinarians Meeting, Milwaukee, WI, 5–10 October’. pp. 299–301.

Kaurova, S. A. , Uteshev, V. K. , Chekurova, N. R. , and Gakhova, E. N. (1997). Cryopreservation of testis of frog Rana temporaria. Infusionsther. Transfusiosmed. 24, 378.
King T. J. (1966). Nuclear transplantation in amphibian. In ‘Methods in Cell Physiology. Vol. 2’. (Ed. D. M. Prescott.) pp. 1–36. (Academic Press: New York.)

Kleinhans, F. W. , Guenther, J. F. , Roberts, D. M. , and Mazur, P. (2006). Analysis of intracellular ice nucleation in Xenopus oocytes by differential scanning calorimetry. Cryobiology 52, 128–138.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | Lentini A. (2002). Reproduction. In ‘Puerto Rican Crested Toad Husbandry Manual.’ American Association of Zoos and Aquariums (AZA) Amphibian Taxon Advisory Group (www.aza.org).

Long, J. A. (2006). Avian semen cryopreservation: what are the biological challenges? Poult. Sci. 85(2), 232–236.
CAS | PubMed | Norris D. O. (2007). III. Tropic hormones of the adenohypophysis. In ‘Vetebrate Endocrinology’. 4th edn. (Ed. D. O. Norris.) pp. 125–140. (Academic Press: San Diego.)

Obringer, A. R. , O’Brien, J. K. , Saunders, R. L. , Yamamoto, K. , Kikuyama, S. , and Roth, T. L. (2000). Characterisation 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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | Rabb G. B. (1999). The amphibian crisis. In ‘Proceedings of the Seventh World Conference on Breeding Endangered Species: Linking Zoos and Field Research to Advance Conservation’. (Eds T. L. Roth, W. F. Swanson and L. K. Blattman.) pp. 23–30. (Cincinnati Zoo and Botanical Garden: Cincinnati.)

Reaser J. K., and Blaustein A. (2005). Repercussions of global change. In ‘Amphibian Declines: Conservation Status of United States Species’. (Ed. M. Lannoo.) pp. 60–63. (University of California Press: Berkeley, LA.)

Roth T. L., and Obringer A. R. (2003). Reproductive research and the worldwide amphibian extinction crisis. In ‘Reproductive Science and Integrated Conservation’. (Eds W. V. Holt, A. R. Pickard, J. C. Rodger and D. E. Wildt.) pp. 359–374. (Cambridge University Press: Cambridge.)

Rowson, A. D. , Obringer, A. R. , and Roth, T. L. (2001). Non-invasive treatments of lutuenizing hormone-releasing hormone for inducing spermiation in American (Bufo americanus) and Gulf coast (Bufo valliceps) toads. Zoo Biol. 20, 63–74.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | Rugh R. (1965). ‘Experimental Embryology: Techniques and Procedures.’ 3rd edn. (Burgess Publishing Co.: Minneapolis.)

Ryder, O. A. , McLaren, A. , Brenner, S. , Zhang, Y. P. , and Benirschke, K. (2000). DNA banks for endangered species. Science 288, 275–277.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | Spencer B. (2002). Reproduction. In ‘Puerto Rican Crested Toad Husbandry Manual’. American Association of Zoos and Aquariums (AZA) Amphibian Taxon Advisory Group (www.aza.org).

Stallard, R. F. (2001). Possible environmental factors underlying amphibian decline in eastern Puerto Rico: analysis of U.S. government data archives. Conserv. Biol. 15(4), 943–953.
Crossref | GoogleScholarGoogle Scholar | Subcommittee on Amphibian Standards (1996). ‘Amphibians: Guidelines for the Breeding, Care, and Management of Laboratory Animals.’ (Eds Committee on Standards, National Research Council.) (National Academy Press Inc.: Washington, DC.) Available at: http://books.nap.edu/html/amphibian.

Swanson, W. F. (2006). Application of assisted reproduction for population management in felids: the potential and reality for conservation of small cats. Theriogenology 66, 49–58.
Crossref | GoogleScholarGoogle Scholar | PubMed | Whitaker B. R. (2001). Reproduction. In ‘Amphibian Medicine and Captive Husbandry’. (Eds K. M. Wright and B. R. Whitaker.) pp. 285–299. (Krieger Publishing Co: Malabar, FL.)

Wildt, D. E. (1992). Genetic resource banks for conserving wildlife species: justifications, examples and becoming organised on a global basis. Anim. Reprod. Sci. 28, 247–257.
Crossref | GoogleScholarGoogle Scholar | Young B. E., Stuart S. N., Chanson J. S., Cox N. A., and Boucher T. M. (2004). ‘Disappearing Jewels: the Status of New World Amphibians.’ (Nature Serve: Arlington, VA.)