Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Semen and oocyte collection, sperm cryopreservation and IVF with the threatened North American giant salamander Cryptobranchus alleganiensis

Dale McGinnity https://orcid.org/0000-0002-7758-7677 A E , Sherri D. Reinsch A , Heather Schwartz B , Vance Trudeau C and Robert K. Browne https://orcid.org/0000-0002-3172-9991 D
+ Author Affiliations
- Author Affiliations

A Ectotherm Department, Nashville Zoo at Grassmere, 3777 Nolensville Rd, Nashville, TN 37211, USA.

B Veterinary Department, Nashville Zoo at Grassmere, 3777 Nolensville Rd, Nashville, TN 37211, USA.

C Department of Biology, University of Ottawa, 75 Laurier Ave East, Ottawa, ON, K1N 6N5, Canada.

D Sustainability America, La Isla Road, Sarteneja, Corozal District, Belize.

E Corresponding author. Email: dmcginnity@nashvillezoo.org

Reproduction, Fertility and Development 34(5) 470-477 https://doi.org/10.1071/RD21035
Submitted: 2 February 2021  Accepted: 27 June 2021   Published: 20 August 2021

Abstract

Semen of high to moderate quality was collected following the hormonal induction of North American giant salamanders Cryptobranchus alleganiensis. Oocytes from one female yielded the first C. alleganiensis produced while maintained in aquaria under human care and the first externally fertilising salamander produced with cryopreserved spermatozoa and IVF. Further research is needed with North American giant salamanders to establish reliable techniques to produce large numbers of viable offspring, along with the application of cryopreserved spermatozoa.

Keywords: amphibian, breeding, conservation, hellbender, hormone, induction, propagation, reproduction.


References

Baker, C. L. (1963). Spermatozoa and spermateleosis in Cryptobranchus and Necturus. J. Tennessee Acad. Sci. 38, 1.9.

Bishop, N. C. (1941). The Salamanders of New York. New York State Museum Bulletin # 324, Albany, p. 1-NY.

Browne, R. K., Janzen, P., Bagaturov, M. F., and van Houte, D. K. (2018). Amphibian keeper conservation breeding programs. J. Zoo. Res. 2, 29–46.

Browne, R. K., Silla, A. J., Upton, R., et al. (2019). Sperm collection and storage for the sustainable management of amphibian biodiversity. Theriogenology 133, 187–200.
Sperm collection and storage for the sustainable management of amphibian biodiversity.Crossref | GoogleScholarGoogle Scholar | 31155034PubMed | 31155034PubMed |

Burgmeier, N. G., Unger, S. D., Meyer, J. L., Sutton, T. M., and Williams, R. N. (2011). Health and habitat quality assessment for the eastern hellbender (Cryptobranchus alleganiensis alleganiensis) in Indiana, USA. J. Wildlife Dis. 47, 836–848.

Civiello, J. A., Timothy, J. B., Brisco, S. J., and Briggler, J. T. (2019). Propagation of Eastern hellbender (Cryptobranchus alleganiensis) in a recirculating aquaculture system at the Shepherd of the Hills State Fish Hatchery. N. Am. J. Aquaculture 81, 281–290.
Propagation of Eastern hellbender (Cryptobranchus alleganiensis) in a recirculating aquaculture system at the Shepherd of the Hills State Fish Hatchery.Crossref | GoogleScholarGoogle Scholar |

Dundee, H. A., and Dundee, D. S. (1965). Observations on the systematics and ecology of Cryptobranchus from the Ozark Plateaus of Missouri and Arkansas. Copeia 1965, 369–370.
Observations on the systematics and ecology of Cryptobranchus from the Ozark Plateaus of Missouri and Arkansas.Crossref | GoogleScholarGoogle Scholar |

Green, N. B. (1933). Cryptobranchus allegianensis in West Virginia. Proc. W. Va. Acad. Sci. 30, 300–302.

Guy, E. L., Gillisa, A. B., Kouba, A. J., Barber, D., Poole, V., Marcec-Greaves, R. M., and Kouba, C. K. (2020). Sperm collection and cryopreservation for threatened newt species. Cryobiology 94, 80–88.
Sperm collection and cryopreservation for threatened newt species.Crossref | GoogleScholarGoogle Scholar | 32437677PubMed | 32437677PubMed |

Hime, P. M. (2017). Genomic perspectives on amphibian evolution across multiple phylogenetic scales. Ph.D. Thesis, University of Kentucky, Lexington, KY, USA. Available at https://uknowledge.uky.edu/cgi/viewcontent.cgi?article=1046&context=biology_etds [verified 29 June 2021].

Hime, P. M., Briggler, J. T., Reece, J. S., and Weisrock, D. W. (2019). Genomic data reveal conserved female heterogamety in giant salamanders with gigantic nuclear genomes. G3 (Bethesda) 9, 3467–3476.
Genomic data reveal conserved female heterogamety in giant salamanders with gigantic nuclear genomes.Crossref | GoogleScholarGoogle Scholar | 31439718PubMed | 31439718PubMed |

Hime, P. M., Lemmon, A. R., Moriarty Lemmon, E. C., et al. (2021). Phylogenomics reveals ancient gene tree discordance in the amphibian tree of life. Syst. Biol. 70, 49–66.
Phylogenomics reveals ancient gene tree discordance in the amphibian tree of life.Crossref | GoogleScholarGoogle Scholar | 32359157PubMed | 32359157PubMed |

Hopkins, W. A., and DuRant, S. E. (2011). Innate immunity and stress physiology of eastern hellbenders (Cryptobranchus alleganiensis) from two stream reaches with differing habitat quality. Gen. Comp. Endocrinol. 174, 107–115.
Innate immunity and stress physiology of eastern hellbenders (Cryptobranchus alleganiensis) from two stream reaches with differing habitat quality.Crossref | GoogleScholarGoogle Scholar | 21872597PubMed | 21872597PubMed |

Howell, L. G., Frankham, R. J. C., Witt, R. R., Clulow, C., Upton, R. M. O., and Clulow, J. (2020). Integrating biobanking minimises inbreeding and produces significant cost benefits for a threatened frog captive breeding programme. Conserv. Lett. 14, e12776.

Hu, Q., Tian, H., Li, W., Meng, Y., Wang, Q., and Xiao, H. (2019). Identification of critical sex-biased genes in Andrias davidianus by de novo transcriptome. Mol. Genet. Genomics 294, 287–299.
Identification of critical sex-biased genes in Andrias davidianus by de novo transcriptome.Crossref | GoogleScholarGoogle Scholar | 30377773PubMed | 30377773PubMed |

Humphries, J. (1999). Ecology and population demography of the hellbender, Cryptobranchus alleganiensis in West Virginia. M.S. Thesis, Marshall University, Huntington, WV.

Jachowski, C. M. B., and Hopkins, W. A. (2018). Loss of catchment-wide riparian forest cover is associated with reduced recruitment in a long-lived amphibian. Biol. Conserv. 220, 215–227.
Loss of catchment-wide riparian forest cover is associated with reduced recruitment in a long-lived amphibian.Crossref | GoogleScholarGoogle Scholar |

Kern, W. H. (1986). Reproduction of the hellbender, Cryptobranchus alleganiensis, in Indiana. Proc. Indiana Acad. Sci. 95, 521.

Kikuyama, S., Okada, R., Hasunuma, I., and Nakada, T. (2019). Some aspects of the hypothalamic and pituitary development, metamorphosis, and reproductive behavior as studied in amphibians. Gen. Comp. Endocrinol. 284, 113212.
Some aspects of the hypothalamic and pituitary development, metamorphosis, and reproductive behavior as studied in amphibians.Crossref | GoogleScholarGoogle Scholar | 31238076PubMed |

Marcec, R. M. (2016). Development of assisted reproductive technologies for endangered North American salamanders. Ph.D. Thesis, Mississippi State University, Starkville, MS, USA.

Nickerson, M. A., and Mays, C. E. (2005). The Hellbenders: North American Giant Salamanders. CNAH Facsimile Reprint Series #5. Publications in Biology and Geology No. 1. pp. 1–109. (The Center for North American Herpetology.)

Nowoshilow, S., and Tanaka, E. M. (2020). Introducing www.axolotl-omics.org – an integrated -omics data portal for the axolotl research community. Exp. Cell. Res. 394, 112143.
Introducing www.axolotl-omics.org – an integrated -omics data portal for the axolotl research community.Crossref | GoogleScholarGoogle Scholar | 32540400PubMed | 32540400PubMed |

Peng, L. Y., Xiao, Y. M., and Liu, Y. (2011). Effect of cryopreservation and short-term storage of 622 Chinese giant salamander sperm. Shui Sheng Sheng Wu Hsueh Bao 35, 325–332.
Effect of cryopreservation and short-term storage of 622 Chinese giant salamander sperm.Crossref | GoogleScholarGoogle Scholar |

Schmitt, D., and Webb, G. (2002). Applications in reproductive technologies for agriculture educators. Missouri State University, Agriculture Department, Springfield, Missouri.

Smith, B. G. (1907). The life history and habits of Cryptobranchus allegheniensis. Biol. Bull. 13, 5–39.
The life history and habits of Cryptobranchus allegheniensis.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 | 23442383PubMed | 23442383PubMed |

Unger, S. (2003). Sperm production and larval development in and hellbenders (Cryptobranchus alleganiensis alleganiensis and C.a. bishopi); a comparison of declining and stable populations. M.S. Thesis, Southwest Missouri State University, Springfield, MO, USA.

Unger, S., Mathis, A., and Wilkinson, W. (2013). A comparison of sperm health in declining and stable populations of hellbenders (Cryptobranchus alleganiensis alleganiensis and C.a. bishopi) Am. Midl. Nat. 170, 382–392.
A comparison of sperm health in declining and stable populations of hellbenders (Cryptobranchus alleganiensis alleganiensis and C.a. bishopi)Crossref | GoogleScholarGoogle Scholar |

Virata, J. (2016). Hellbender salamander conceived with cryopreserved sperm hatches at Nashville Zoo. Reptiles Magazine. Available at https://www.reptilesmagazine.com/hellbender-salamander-conceived-with-cryopreserved-sperm-hatches-at-nashville-zoo/ [verified 6 January 2021].

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 | 27013378PubMed | 27013378PubMed |

Wheeler, B. A., Prosen, E., Mathis, A., and Wilkinson, R. F. (2003). Population declines of a long-lived salamander: a 20+-year study of hellbenders, Cryptobranchus alleganiensis. Biol. Conserv. 109, 151–156.
Population declines of a long-lived salamander: a 20+-year study of hellbenders, Cryptobranchus alleganiensis.Crossref | GoogleScholarGoogle Scholar |