Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
REVIEW

Reproduction technologies for the sustainable management of Caudata (salamander) and Gymnophiona (caecilian) biodiversity

Robert K. Browne https://orcid.org/0000-0002-3172-9991 A * , Svetlana A. Kaurova https://orcid.org/0000-0002-2298-1597 B , Karthikeyan Vasudevan https://orcid.org/0000-0003-2316-3382 C , Dale McGinnity https://orcid.org/0000-0002-7758-7677 D , Govindappa Venu https://orcid.org/0000-0003-4873-7418 E , Manuel Gonzalez F , Victor K. Uteshev https://orcid.org/0000-0002-4357-7577 B and Ruth Marcec-Greaves G
+ Author Affiliations
- Author Affiliations

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

B Institute of Cell Biophysics of the Russian Academy of Sciences, PSCBR RAS, Pushchino, Moscow Region 142290, Russia.

C Laboratory for the Conservation of Endangered Species, CSIR-Centre for Cellular and Molecular Biology, Hyderabad, Telangana 500048, India.

D Ectotherm Department, Nashville Zoo at Grassmere, Nashville, TN 37211, USA.

E Department of Zoology, Centre for Applied Genetics, Bangalore University, Jnana Bharathi Campus, Bengaluru, Karnataka 560056, India.

F Departamento de Produccion Animal, Universidad de Guadalajara, Guadalajara, Jalisco, Mexico.

G National Amphibian Conservation Center Detroit Zoological Society, Detroit, MI, USA. Honduras Amphibian Rescue and Conservation Center, Oak Grove Missouri 64075

* Correspondence to: robert.browne@gmail.com

Reproduction, Fertility and Development 34(6) 479-497 https://doi.org/10.1071/RD21356
Published online: 15 February 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

We review the use of reproduction technologies (RTs) to support the sustainable management of threatened Caudata (salamanders) and Gymnophiona (caecilian) biodiversity in conservation breeding programs (CBPs) or through biobanking alone. The Caudata include ∼760 species with ∼55% threatened, the Gymnophiona include ∼215 species with an undetermined but substantial number threatened, with 80% of Caudata and 65% of Gymnophiona habitat unprotected. Reproduction technologies include: (1) the exogenous hormonal induction of spermatozoa, eggs, or mating, (2) in vitro fertilisation, (3) intracytoplasmic sperm injection (ICSI), (4) the refrigerated storage of spermatozoa, (5) the cryopreservation of sperm, cell or tissues, (6) cloning, and (7) gonadal tissue or cell transplantation into living amphibians to eventually produce gametes and then individuals. Exogenous hormone regimens have been applied to 11 Caudata species to stimulate mating and to 14 species to enable the collection of spermatozoa or eggs. In vitro fertilisation has been successful in eight species, spermatozoa have been cryopreserved in seven species, and in two species in vitro fertilisation with cryopreserved spermatozoa has resulted in mature reproductive adults. However, the application of RTs to Caudata needs research and development over a broader range of species. Reproduction technologies are only now being developed for Gymnophiona, with many discoveries and pioneering achievement to be made. Species with the potential for repopulation are the focus of the few currently available amphibian CBPs. As Caudata and Gymnophiona eggs or larvae cannot be cryopreserved, and the capacity of CBPs is limited, the perpetuation of the biodiversity of an increasing number of species depends on the development of RTs to recover female individuals from cryopreserved and biobanked cells or tissues.

Keywords: ART, assisted reproduction technologies, biobanking, caecilian, Caudata, CBPs, conservation breeding programs, cryopreservation, Gymnophiona, hormones, in vitro fertilisation, repopulation, reproduction technologies, salamander, sperm cryopreservation.


References

Aglietti, GS (2020). Current challenges and opportunities for space technologies. Frontiers in Space Technologies 1, 1.
Current challenges and opportunities for space technologies.Crossref | GoogleScholarGoogle Scholar |

AmphibiaWeb (2021) Species lists. Available at https://amphibiaweb.org/lists/index.shtml. [Downloaded 1 February 2021]

Ananjeva, NB, Uteshev, VK, Orlov, NL, Ryabov, SA, Gakhova, EN, Kaurova, SA, Kramarova, LI, Shishova, NV, and Browne, RK (2017). Comparison of the modern reproductive technologies for amphibians and reptiles. Russian Journal of Herpetology 24, 275–290.
Comparison of the modern reproductive technologies for amphibians and reptiles.Crossref | GoogleScholarGoogle Scholar |

Bradshaw, CJA, Ehrlich, PR, Beattie, A, Ceballos, G, Crist, E, Diamond, J, Dirzo, R, Ehrlich, AH, Harte, J, Harte, ME, Pyke, G, Raven, PH, Ripple, WJ, Saltré, F, Turnbull, C, Wackernagel, M, and Blumstein, DT (2021). Underestimating the challenges of avoiding a ghastly future. Frontiers in Conservation Science 1, 9.
Underestimating the challenges of avoiding a ghastly future.Crossref | GoogleScholarGoogle Scholar |

Brannelly, LA, Ohmer, MEB, and Richards-Zawacki, CL (2019). Artificial reproduction using leuprolide acetate in the frog Rana pipiens. Herpetological Journal 29, 125–130.
Artificial reproduction using leuprolide acetate in the frog Rana pipiens.Crossref | GoogleScholarGoogle Scholar |

Bronson, E, Guy, EL, Murphy, KJ, Barrett, K, Kouba, AJ, Poole, V, and Kouba, CK (2021). Influence of oviposition-inducing hormone on spawning and mortality in the endangered Panamanian golden frog (Atelopus zeteki). BMC Zoology 6, 17.
Influence of oviposition-inducing hormone on spawning and mortality in the endangered Panamanian golden frog (Atelopus zeteki).Crossref | GoogleScholarGoogle Scholar |

Browne, RK, Clulow, J, Mahony, M, and Clark, A (1998). Successful recovery of motility and fertility of cryopreserved cane toad (Bufo marinus) sperm. Cryobiology 37, 339–345.
| 9917350PubMed |

Browne, RK, Clulow, J, and Mahony, M (2001). Short-term storage of cane toad (Bufo marinus) gametes. Reproduction 121, 167–173.
Short-term storage of cane toad (Bufo marinus) gametes.Crossref | GoogleScholarGoogle Scholar | 11226040PubMed |

Browne, RK, Li, H, Seratt, J, and Kouba, A (2006a). Progesterone improves the number and quality of hormone induced Fowler toad (Bufo fowleri) oocytes. Reproductive Biology and Endocrinology 4, 3.
Progesterone improves the number and quality of hormone induced Fowler toad (Bufo fowleri) oocytes.Crossref | GoogleScholarGoogle Scholar | 16451718PubMed |

Browne, RK, Seratt, J, Vance, C, and Kouba, A (2006b). Hormonal priming, induction of ovulation and in-vitro fertilization of the endangered Wyoming toad (Bufo baxteri). Reproductive Biology and Endocrinology 4, 34.
Hormonal priming, induction of ovulation and in-vitro fertilization of the endangered Wyoming toad (Bufo baxteri).Crossref | GoogleScholarGoogle Scholar | 16790071PubMed |

Browne, RK, Janzen, P, Bagaturov, MF, and van Houte, DK (2018). Amphibian keeper conservation breeding programs. Journal of Zoological Research 2, 29–46.

Browne, RK, Silla, AJ, Upton, R, Della-Togna, G, Marcec-Greaves, R, Shishova, NV, Uteshev, VK, Proaño, B, Pérez, OD, Mansour, N, Kaurova, SA, Gakhova, EN, Cosson, J, Dzyuba, B, Kramarova, LI, McGinnity, D, Gonzalez, M, Clulow, J, and Clulow, S (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 |

Browne RK, Wang Z, Okada S, McGinnity D, Luo Q, Taguchi Y, Kilpatrick D, Hardman R, Janzen P, Zhang Z, Geng Y (2020) ‘The sustainable management of giant Salamanders (Cryptobranchoidea).’ (Sustainability America: Belize)

Byrne, PG, and Silla, AJ (2010). Hormonal induction of gamete release, and in-vitro fertilisation, in the critically endangered Southern Corroboree Frog, Pseudophryne corroboree. Reproductive Biology and Endocrinology 8, 144.
Hormonal induction of gamete release, and in-vitro fertilisation, in the critically endangered Southern Corroboree Frog, Pseudophryne corroboree.Crossref | GoogleScholarGoogle Scholar | 21114857PubMed |

Calatayud, NE, Stoops, MA, and Durrant, BS (2018). Ovarian control and monitoring in amphibians. Theriogenology 109, 70–81.
Ovarian control and monitoring in amphibians.Crossref | GoogleScholarGoogle Scholar | 29325879PubMed |

Clulow J, Upton R, Trudeau VL, Clulow S (2014) Amphibian assisted reproductive technologies: moving from technology to application. In ‘Reproductive sciences in animal conservation’. (Eds P Comizzoli, JL Brown, WV Holt) pp. 413–463 (Springer)

Clulow, J, Pomering, M, Herbert, D, Upton, R, Calatayud, N, Clulow, S, Mahony, MJ, and Trudeau, VL (2018). Differential success in obtaining gametes between male and female Australian temperate frogs by hormonal induction: a review. General and Comparative Endocrinology 265, 141–148.
Differential success in obtaining gametes between male and female Australian temperate frogs by hormonal induction: a review.Crossref | GoogleScholarGoogle Scholar | 29859744PubMed |

Della Togna, G, Howell, LG, Clulow, J, Langhorne, CJ, Marcec-Greaves, R, and Calatayud, NE (2020). Evaluating amphibian biobanking and reproduction for captive breeding programs according to the Amphibian Conservation Action Plan Objectives. Theriogenology 150, 412–431.
Evaluating amphibian biobanking and reproduction for captive breeding programs according to the Amphibian Conservation Action Plan Objectives.Crossref | GoogleScholarGoogle Scholar | 32127175PubMed |

de Sa, R, and Berois, N (1986). Spermatogenesis and histology of the testes of the caecilian, Chthonerpeton indistinctum. Journal of Herpetology 20, 510–514.
Spermatogenesis and histology of the testes of the caecilian, Chthonerpeton indistinctum.Crossref | GoogleScholarGoogle Scholar |

Diwan, AD, and Harke, SN Diwan, AD, and Harke, SN Diwan, AD, and Harke, SN (2020). Cryobanking of fish and shellfish egg, embryos and larvae: an overview. Frontiers in Marine Science 7, 251.
Cryobanking of fish and shellfish egg, embryos and larvae: an overview.Crossref | GoogleScholarGoogle Scholar |

Doherty-Bone, TM, Gonwouo, NL, Hirschfeld, M, Ohst, T, Weldon, C, Perkins, M, Kouete, MT, Browne, RK, Loader, SP, Gower, DJ, Wilkinson, MW, Rödel, MO, Penner, J, Barej, MF, Schmitz, A, Plötner, J, and Cunningham, AA (2013). Batrachochytrium dendrobatidis in amphibians of Cameroon, including first records for caecilians. Diseases of Aquatic Organisms 102, 187–194.
Batrachochytrium dendrobatidis in amphibians of Cameroon, including first records for caecilians.Crossref | GoogleScholarGoogle Scholar | 23446968PubMed |

Dymek, J, Dymek, A, and Osikowski, A (2018). Anatomy of the female reproductive system and sperm storage of the viviparous caecilian Typhlonectes natans (Gymnophiona: Typhlonectidae. Acta Biologica 25, 19–31.
Anatomy of the female reproductive system and sperm storage of the viviparous caecilian Typhlonectes natans (Gymnophiona: Typhlonectidae.Crossref | GoogleScholarGoogle Scholar |

Figiel, C (2013). Cryopreservation of sperm from the axolotl Ambystoma mexicanum: implications for conservation. Herpetological Conservation and Biology 8, 748–755.

Germano, JM, Cree, A, Molinia, FC, Arregui, L, and Bishop, PJ (2021). Hormone treatment does not reliably induce spermiation or mating in Hamilton’s frog from the archaic leiopelmatid lineage. Reproduction, Fertility and Development , .
Hormone treatment does not reliably induce spermiation or mating in Hamilton’s frog from the archaic leiopelmatid lineage.Crossref | GoogleScholarGoogle Scholar |

Gillis, AB, Guy, EL, Kouba, AJ, Allen, PJ, Marcec-Greaves, RM, and Kouba, CK (2021). Short-term storage of tiger salamander (Ambystoma tigrinum) spermatozoa: the effect of collection type, temperature and time. PLoS ONE 16, e0245047.
Short-term storage of tiger salamander (Ambystoma tigrinum) spermatozoa: the effect of collection type, temperature and time.Crossref | GoogleScholarGoogle Scholar | 33428658PubMed |

Gomes, AD, Moreira, RG, Navas, CA, Antoniazzi, MM, and Jared, C (2012). Review of the reproductive biology of caecilians (Amphibia, Gymnophiona). South American Journal of Herpetology 7, 191–202.
Review of the reproductive biology of caecilians (Amphibia, Gymnophiona).Crossref | GoogleScholarGoogle Scholar |

Goncharov, BF, Shubravy, OI, Serbinova, IA, and Uteshev, VK (1989). The USSR program for breeding amphibians, including rare and endangered species. International Zoo Yearbook 28, 10–21.
The USSR program for breeding amphibians, including rare and endangered species.Crossref | GoogleScholarGoogle Scholar |

Gower, DJ, and Wilkinson, M (2002). Phallus morphology in caecilians (Amphibia, Gymnophiona) and its systematics utility. Bulletin of the Natural History Museum. Zoology Series 68, 143–154.
Phallus morphology in caecilians (Amphibia, Gymnophiona) and its systematics utility.Crossref | GoogleScholarGoogle Scholar |

Gower, DJ, and Wilkinson, M (2005). Conservation biology of caecilian amphibians. Conservation Biology 19, 45–55.
Conservation biology of caecilian amphibians.Crossref | GoogleScholarGoogle Scholar |

Groffman PM, Kareiva P, Carter S, Grimm NB, Lawler J, Mack M, Matzek V, Tallis H (2014) Ch. 8: Ecosystems, biodiversity, and ecosystem services. In ‘Climate Change Impacts in the United States: the Third National Climate Assessment’. (Eds JM Melillo, Terese (TC) Richmond, GW Yohe) pp. 195–219 (U.S. Global Change Research Program).
| Crossref |

Guy, EL, Gillis, AB, Kouba, AJ, Barber, D, Poole, V, Marcec-Greaves, RM, and Kouba, CK (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 |

Hagedorn, M, Kleinhans, FW, Wildt, DE, and Rall, WF (1997). Chill sensitivity and cryoprotectant permeability of dechorionated zebrafish embryos, Brachydanio rerio. Cryobiology 34, 251–263.
Chill sensitivity and cryoprotectant permeability of dechorionated zebrafish embryos, Brachydanio rerio.Crossref | GoogleScholarGoogle Scholar | 9160996PubMed |

Hardy, MP, and Dent, JN (1986). Transport of sperm within the cloaca of the female red-spotted newt. Journal of Morphology 190, 259–270.
Transport of sperm within the cloaca of the female red-spotted newt.Crossref | GoogleScholarGoogle Scholar | 3806681PubMed |

Herbert D (2004) Studies of assisted reproduction in the spotted grass frog Limnodynastes tasmaniensis: ovulation, early development and microinjection (ICSI). Masters by Research thesis, The University of Newcastle, Australia.

Higaki, S, Eto, Y, Kawakami, Y, Yamaha, E, Kagawa, N, Kuwayama, M, Nagano, M, Katagiri, S, and Takahashi, Y (2010). Production of fertile zebrafish (Danio rerio) possessing germ cells (gametes) originated from primordial germ cells recovered from vitrified embryos. Reproduction 139, 733–740.
Production of fertile zebrafish (Danio rerio) possessing germ cells (gametes) originated from primordial germ cells recovered from vitrified embryos.Crossref | GoogleScholarGoogle Scholar | 20154175PubMed |

Hime PM (2017) Genomic perspectives on amphibian evolution across multiple phylogenetic scales. Doctoral Dissertation, University of Kentucky, USA.

Hime, PM, Lemmon, AR, Lemmon, ECM, Prendini, E, Brown, JM, Thomson, RC, Kratovil, JD, Noonan, BP, Pyron, RA, Peloso, PLV, Kortyna, ML, Keogh, JS, Donnellan, SC, Mueller, RL, Raxworthy, CJ, Kunte, K, Ron, SR, Das, S, Gaitonde, N, Green, DM, Labisko, J, Che, J, and Weisrock, DW (2021). Phylogenomics reveals ancient gene tree discordance in the amphibian tree of life. Systematic Biology 70, 49–66.
Phylogenomics reveals ancient gene tree discordance in the amphibian tree of life.Crossref | GoogleScholarGoogle Scholar | 32359157PubMed |

Houck LD, Arnold SJ (2003) Courtship and mating behavior. In ‘Reproductive biology and phylogeny of Urodela’. (Ed. DM Sever) pp. 383–424. (Science Publishers, Inc.: Enfield, NH)

Houck LD, Watts RA, Mead LM, Palmer CA, Arnold SJ, Feldhoff PW, Feldhoff RC (2008) A candidate vertebrate pheromone, SPF, increases female receptivity in a salamander. In ‘Chemical signals in vertebrates 11’. (Eds JL Hurst, RJ Beyon, SC Roberts, TD Wyatt) pp. 213–221. (Springer, New York, NY)

Howard, SD, and Bickford, DP (2014). Amphibians over the edge: silent extinction risk of Data Deficient species. Diversity and Distributions 20, 837–846.
Amphibians over the edge: silent extinction risk of Data Deficient species.Crossref | GoogleScholarGoogle Scholar |

Howell, LG, Frankham, R, Rodger, JC, Witt, RR, Clulow, S, Upton, RMO, and Clulow, J (2020). Integrating biobanking minimises inbreeding and produces significant cost benefits for a threatened frog captive breeding programme. Conservation Letters 14, e12776.
Integrating biobanking minimises inbreeding and produces significant cost benefits for a threatened frog captive breeding programme.Crossref | GoogleScholarGoogle Scholar |

Hu, Y, Fan, H, Chen, Y, Chang, Y, Zhan, X, Wu, H, Zhang, B, Wang, M, Zhang, W, Yang, L, Hou, X, Shen, X, Pan, T, Wu, W, Li, J, Hu, H, and Wei, F (2021). Spatial patterns and conservation of genetic and phylogenetic diversity of wildlife in China. Science Advances 7, eabd5725.
Spatial patterns and conservation of genetic and phylogenetic diversity of wildlife in China.Crossref | GoogleScholarGoogle Scholar | 33523945PubMed |

Itoh, T, Kamimura, S, Watanabe, A, and Onitake, K (2002). Egg-jelly structure promotes efficiency of internal fertilization in the newt, Cynops pyrrhogaster. Journal of Experimental Zoology 292, 314–322.
Egg-jelly structure promotes efficiency of internal fertilization in the newt, Cynops pyrrhogaster.Crossref | GoogleScholarGoogle Scholar |

IUCN (2021) The IUCN Red List of threatened species. Version 2020-3. Available at https://www.iucnredlist.org. [Downloaded 1 February 2021]

Iwata, T, Toyoda, F, Yamamoto, K, and Kikuyama, S (2000). Hormonal control of urodele reproductive behavior. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 126, 221–229.
Hormonal control of urodele reproductive behavior.Crossref | GoogleScholarGoogle Scholar |

Jamieson BGM (2013) Reproductive biology and phylogeny of Anura. Vol. 2. Science Publishers Inc.: New Hampshire, USA.

Kaurova, SA, Uteshev, VK, Chekurova, NR, and Gakhova, EN (1997). Сryopreservation of testis of frog Rana temporaria. Infusionsther Trasfusionsmed 24, 379.

Khosla, K, Wang, Y, Hagedorn, M, Qin, Z, and Bischof, J (2017). Gold nanorod induced warming of embryos from the cryogenic state enhances viability. ACS Nano 11, 7869–7878.
Gold nanorod induced warming of embryos from the cryogenic state enhances viability.Crossref | GoogleScholarGoogle Scholar | 28702993PubMed |

Kidov, AA, and Nemyko, EA (2019). Captive breeding of the alpine newt, Ichthyosaura alpestris (Laurenti, 1768) (Amphibia, Caudata, Salamndridae) under hormonal stimulation. Current Studies in Herpetology 19, 31–39.
Captive breeding of the alpine newt, Ichthyosaura alpestris (Laurenti, 1768) (Amphibia, Caudata, Salamndridae) under hormonal stimulation.Crossref | GoogleScholarGoogle Scholar |

Kidov, AA, Shimanskaya, EA, Askenderov, AD, and Nemyko, EA (2019). The use of hormonal stimulation for reproduction of the Karelin’s newt, Triturus karelinii in laboratory conditions. University proceedings. Volga region. Natural Sciences 4, 50–60.
The use of hormonal stimulation for reproduction of the Karelin’s newt, Triturus karelinii in laboratory conditions. University proceedings. Volga region.Crossref | GoogleScholarGoogle Scholar |

Kuehnel, S, and Kupfer, A (2012). Sperm storage in caecilian amphibians. Frontiers in Zoology 9, 12.
Sperm storage in caecilian amphibians.Crossref | GoogleScholarGoogle Scholar | 22672478PubMed |

Kühnel, S, Reinhard, S, and Kupfer, A (2010). Evolutionary reproductive morphology of amphibians: an overview. Bonn Zoological Bulletin 57, 119–126.

Kupfer, A, Kramer, A, Himstedt, W, and Greven, H (2006a). Copulation and egg retention in an oviparous Caecilian (Amphibia: Gymnophiona). Zoologischer Anzeiger - A Journal of. Comparative Zoology 244, 223–228.
Copulation and egg retention in an oviparous Caecilian (Amphibia: Gymnophiona). Zoologischer Anzeiger - A Journal of.Crossref | GoogleScholarGoogle Scholar |

Kupfer, A, Müller, H, Antoniazzi, MM, Jared, C, Greven, H, Nussbaum, RA, and Wilkinson, M (2006b). Parental investment by skin feeding in a caecilian amphibian. Nature 440, 926–929.
Parental investment by skin feeding in a caecilian amphibian.Crossref | GoogleScholarGoogle Scholar | 16612382PubMed |

Kupfer, A, Maxwell, E, Reinhard, S, and Kuehnel, S (2016). The evolution of parental investment in caecilian amphibians: a comparative approach. Biological Journal of the Linnean Society 119, 4–14.
The evolution of parental investment in caecilian amphibians: a comparative approach.Crossref | GoogleScholarGoogle Scholar |

Lee, MSY, and Jamieson, BGM (1993). The ultrastructure of the spermatozoa of bufonid and hylid frogs (Anure, Amphibia): implications for phylogeny and fertilisation biology. Zoologica Scripta 22, 309–323.
The ultrastructure of the spermatozoa of bufonid and hylid frogs (Anure, Amphibia): implications for phylogeny and fertilisation biology.Crossref | GoogleScholarGoogle Scholar |

Lidicker, WZ (2020). A scientist’s warning to humanity on human population growth. Global Ecology and Conservation 24, e01232.
A scientist’s warning to humanity on human population growth.Crossref | GoogleScholarGoogle Scholar | 32837974PubMed |

Mansour, N, Lahnsteiner, F, and Patzner, RA (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 | 20965554PubMed |

Marcec RM (2016) Development of assisted reproductive technologies for endangered North American salamanders. PhD Thesis, Mississippi State University, Starkville, MS, USA.

Marcec, R, Langhorne, C, Vance, C, Kouba, A, and Willard, S (2014). Cryopreservation of spermic milt in the model species Ambystoma tigrinum (Tiger salamander) for application in endangered salamanders. Cryobiology 69, 515.
Cryopreservation of spermic milt in the model species Ambystoma tigrinum (Tiger salamander) for application in endangered salamanders.Crossref | GoogleScholarGoogle Scholar |

Maruska, EJ (1986). Amphibians: review of zoo breeding programmes. International Zoo Yearbook 24/25, 56–65.

McGinnity, D, Reinsch, SD, Schwartz, H, Trudeau, V, and Browne, RK (2021). Semen and oocyte collection, sperm cryopreservation and IVF with the threatened North American giant salamander (Cryptobranchus alleganiensis). Reproduction, Fertility and Development , .
Semen and oocyte collection, sperm cryopreservation and IVF with the threatened North American giant salamander (Cryptobranchus alleganiensis).Crossref | GoogleScholarGoogle Scholar |

Miyamoto, K, Simpson, D, and Gurdon, JB (2015). Manipulation and in vitro maturation of Xenopus laevis oocytes, followed by intracytoplasmic sperm injection, to study embryonic development. Journal of Visualized Experiments 96, 52496.
Manipulation and in vitro maturation of Xenopus laevis oocytes, followed by intracytoplasmic sperm injection, to study embryonic development.Crossref | GoogleScholarGoogle Scholar |

Molur, S, and Walker, S (1998). Conservation assessment of the herpeto-fauna of India – an overview. Hamadryad 23, 169–178.

Moore, FL, Boyd, SK, and Kelley, DB (2005). Historical perspecitive: hormonal regulation of behaviors in amphibians. Hormones and Behavior 48, 373–383.
Historical perspecitive: hormonal regulation of behaviors in amphibians.Crossref | GoogleScholarGoogle Scholar | 15992801PubMed |

Najbar, A, Kiełbowicz, Z, Szymczak, J, and Ogielska, M (2016). Ultrasonography: a method used for pregnancy imaging of the fire salamander (Salamandra salamandra). Polish Journal of Veterinary Sciences 19, 715–722.
Ultrasonography: a method used for pregnancy imaging of the fire salamander (Salamandra salamandra).Crossref | GoogleScholarGoogle Scholar | 28092623PubMed |

Nori, J, Villalobos, F, and Loyola, R (2018). Global priority areas for amphibian research. Journal of Biogeography 45, 2588–2594.
Global priority areas for amphibian research.Crossref | GoogleScholarGoogle Scholar |

Peng, L-Y, Xiao, Y-M, and Liu, Y (2011). Effect of cryopreservation and short-term storage of Chinese giant salamander sperm. Acta Hydrobiologica Sinica 35, 325–332.
Effect of cryopreservation and short-term storage of Chinese giant salamander sperm.Crossref | GoogleScholarGoogle Scholar |

Petranka JW (1998) ‘Salamanders of the United States and Canada.’ (Smithsonian Institution Press: Washington, DC and London)

Poo, S, and Hinkson, KM (2019). Applying cryopreservation to anuran conservation biology. Conservation Science and Practice 1, e91.
Applying cryopreservation to anuran conservation biology.Crossref | GoogleScholarGoogle Scholar |

Rivera-Pacheco, J, Herrera-Barragán, J, León-Galván, M, Ocampo-Cervantes, J, Pérez-Rivero, J, and Gual-Sill, F (2021). Ambystoma mexicanum sperm cryopreservation (Shaw & Nodder, 1798). Abanico Veterinario 11, 1–14.
Ambystoma mexicanum sperm cryopreservation (Shaw & Nodder, 1798).Crossref | GoogleScholarGoogle Scholar |

Robock, A, Oman, L, and Stenchikov, GL (2007). Nuclear winter revisited with a modern climate model and current nuclear arsenals: still catastrophic consequences. Journal of Geophysical Research: Atmospheres 112, .
Nuclear winter revisited with a modern climate model and current nuclear arsenals: still catastrophic consequences.Crossref | GoogleScholarGoogle Scholar |

Rowson, AD, Obringer, AR, and Roth, TL (2001). Non-invasive treatments of luteinizing hormone-releasing hormone for inducing spermiation in American (Bufo americanus) and Gulf Coast (Bufo valliceps) toads. Zoo Biology 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 | 11429778PubMed |

Scheltinga DM, Jamieson BGM (2006) Ultrastructure and phylogeny of caecilian spermatozoa. In ‘Reproductive biology and phylogeny of gymnophiona (Caecilians). Vol. 5’. (Ed. JM Exbrayat) pp. 247–274. (Science Publishers: Enfield, NH, USA, Jersey, Plymouth)

Seshachar, BR (1940). The apodan sperm. Current Science, Bangalore 10, 464–465.

Seshachar, BR (1943). The spermatogenesis of Ichthyophis glutinosus Linn, Part 3. Spermatelosis. Proceedings of the National Institute of Science, India 9, 271–286.

Sever, DM (2002). Female sperm storage in amphibians. Journal of Experimental Zoology 292, 165–179.
Female sperm storage in amphibians.Crossref | GoogleScholarGoogle Scholar |

Sever, DM, and Brizzi, R (1998). Comparative biology of sperm storage in female salamanders. Journal of Experimental Zoology 282, 460–476.
Comparative biology of sperm storage in female salamanders.Crossref | GoogleScholarGoogle Scholar |

Sever DM, Staub NL (2011) Hormones, sex accessory structures, and secondary sexual characteristics in amphibians. In ‘Hormones and reproduction of vertebrates’. (Eds DO Norris, KH Lopez) pp. 83–98. (Academic Press).
| Crossref |

Shishova, NR, Uteshev, VK, Kaurova, SA, Browne, RK, and Gakhova, EN (2011). Cryopreservation of hormonally induced sperm for the conservation of threatened amphibians with Rana temporaria as a model species. Theriogenology 75, 220–232.
Cryopreservation of hormonally induced sperm for the conservation of threatened amphibians with Rana temporaria as a model species.Crossref | GoogleScholarGoogle Scholar | 21040966PubMed |

Shishova, NV, Uteshev, VK, Sirota, NP, Kuznetsova, EA, Kaurova, SA, Browne, RK, and Gakhova, EN (2013). The quality and fertility of sperm collected from European common frog (Rana temporaria) carcasses refrigerated for up to 7 days. Zoo Biology 32, 400–406.
| 23609917PubMed |

Silla, AJ, and Byrne, PG (2019). The role of reproductive technologies in amphibian conservation breeding programs. Annual Review of Animal Biosciences 7, 499–519.
The role of reproductive technologies in amphibian conservation breeding programs.Crossref | GoogleScholarGoogle Scholar | 30359086PubMed |

Silla, AJ, and Roberts, JD (2012). Investigating patterns in the spermiation response of eight Australian frogs administered human chorionic gonadotropin (hCG) and luteinizing hormone-releasing hormone (LHRHa). General and Comparative Endocrinology 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 | 22909973PubMed |

Silla, AJ, Roberts, JD, and Byrne, PG (2020). The effect of injection and topical application of hCG and GnRH agonist to induce sperm-release in the roseate frog, Geocrinia rosea. Conservation Physiology 8, coaa104.
The effect of injection and topical application of hCG and GnRH agonist to induce sperm-release in the roseate frog, Geocrinia rosea.Crossref | GoogleScholarGoogle Scholar | 33304589PubMed |

Smita, M, Oommen, OV, Jancy, MG, and Akbarsha, MA (2004). Stages in spermatogenesis of two species of caecilians, Ichthyophis tricolor and Uraeotyphlus cf. narayani (Amphibia: Gymnophiona): light and electron microscopic study. Journal of Morphology 261, 92–104.
Stages in spermatogenesis of two species of caecilians, Ichthyophis tricolor and Uraeotyphlus cf. narayani (Amphibia: Gymnophiona): light and electron microscopic study.Crossref | GoogleScholarGoogle Scholar | 15164370PubMed |

Snyder, WE, Trudeau, VL, and Loskutoff, NM (2012). A noninvasive, transdermal absorbtion approach for exogenous hormone induction of spawning in the northern cricket frog, Acris crepitans: a model for small endangered amphibians. Reproduction, Fertility and Development 25, 232–233.
A noninvasive, transdermal absorbtion approach for exogenous hormone induction of spawning in the northern cricket frog, Acris crepitans: a model for small endangered amphibians.Crossref | GoogleScholarGoogle Scholar |

Steffan, SA, Chikaraishi, Y, Currie, CR, Horn, H, Gaines-Day, HR, Pauli, JN, Zalapa, JE, and Ohkouchi, N (2015). Microbes are trophic analogs of animals. Proceedings of the National Academy of Sciences of the United States of America 112, 15119–15124.
Microbes are trophic analogs of animals.Crossref | GoogleScholarGoogle Scholar | 26598691PubMed |

Stokstad, E (2019). Can a dire ecological warning lead to action? Science 364, 517–518.
Can a dire ecological warning lead to action?Crossref | GoogleScholarGoogle Scholar | 31073046PubMed |

Stoops, MA, Campbell, MK, and Dechant, CJ (2014). Successful captive breeding of Necturus beyeri through manipulation of environmental cues and exogenous hormone administration: a model for endangered Necturus. Herpetological Review 45, 251–256.

Strand, J, Thomsen, H, Jensen, JB, Marcussen, C, Nicolajsen, TB, Skriver, MB, Søgaard, IM, Ezaz, T, Purup, S, Callesen, H, and Pertoldi, C (2020). Biobanking in amphibian and reptilian conservation and management: opportunities and challenges. Conservation Genetics Resources 12, 709–725.
Biobanking in amphibian and reptilian conservation and management: opportunities and challenges.Crossref | GoogleScholarGoogle Scholar |

Taku, S, Masakazu, A, and Seiji, G (2004). A new method to extract sperm from spermatophores of the male spiny king crab Paralithodes brevipes (Anomura: Lithodidae). Crustacean Research 33, 10–14.
A new method to extract sperm from spermatophores of the male spiny king crab Paralithodes brevipes (Anomura: Lithodidae).Crossref | GoogleScholarGoogle Scholar |

Taylor EH (1968) ‘The Caecilians of the World: a taxonomic review.’ p. 848 (University of Kansas Press: Lawrence, Kansas)

Trudeau, VL, Somoza, GM, Natale, GS, Pauli, B, Wignall, J, Jackman, P, Doe, K, and Schueler, FW (2010). Hormonal induction of spawning in 4 species of frogs by coinjection with a gonadotropin-releasing hormone agonist and a dopamine antagonist. Reproductive Biology and Endocrinology 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 | 20398399PubMed |

Trudeau, VL, Schueler, FW, Navarro-Martin, L, Hamilton, CK, 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. Reproductive Biology and Endocrinology 11, 14.
Efficient induction of spawning of Northern leopard frogs (Lithobates pipiens) during and outside the natural breeding season.Crossref | GoogleScholarGoogle Scholar | 23442383PubMed |

Trumbo DR (2015) Landscape genomics and species range limit evolution of the invasive cane toad (Rhinella marina) in Australia. PhD thesis. Washington State University, Washington, USA.

Turvey, ST, Chen, S, Tapley, B, Wei, G, Xie, F, Yan, F, Yang, J, Liang, Z, Tian, H, Wu, M, Okada, S, Wang, J, Lü, J, Zhou, F, Papworth, SK, Redbond, J, Brown, T, Che, J, and Cunningham, AA (2018). Imminent extinction in the wild of the world’s largest amphibian. Current Biology 28, R592–R594.
Imminent extinction in the wild of the world’s largest amphibian.Crossref | GoogleScholarGoogle Scholar | 29787717PubMed |

Ukita, M, Itoh, T, Watanabe, T, Watanabe, A, and Onitake, K (1999). Substances for the initiation of sperm motility in egg-jelly of the Japanese newt, Cynops pyrrhogaster. Zoological Science 16, 793–802.
Substances for the initiation of sperm motility in egg-jelly of the Japanese newt, Cynops pyrrhogaster.Crossref | GoogleScholarGoogle Scholar |

UNESCO (2020) The Precautionary Principle”. United Nations Educational, Scientific and Cultural Organization (UNESCO). World Commission on the Ethics of Scientific Knowledge and Technology (COMEST). p. 8. [Retrieved 2 January 2020]

Unger, S (2013). A comparison of sperm health in declining and stable populations of hellbenders (Cryptobranchus alleganiensis alleganiensis and C.a. bishopi). The American Midland Naturalist 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 |

Upton, R, Clulow, S, Calatayud, NE, Colyvas, K, Seeto, RGY, Wong, LAM, Mahony, MJ, and Clulow, J (2021). Generation of reproductively mature offspring from the endangered green and golden bell frog Litoria aurea using cryopreserved spermatozoa. Reproduction, Fertility and Development 33, 562–572.
Generation of reproductively mature offspring from the endangered green and golden bell frog Litoria aurea using cryopreserved spermatozoa.Crossref | GoogleScholarGoogle Scholar |

Uteshev, VK, Kaurova, SA, Shishova, NV, Stolyarov, SD, Browne, RK, and Gakhova, EN (2015). In vitro fertilisation with hormonally induced sperm and eggs from sharp-ribbed newts Pleurodeles waltl. Russian Journal of Herpetology 22, 35–40.
In vitro fertilisation with hormonally induced sperm and eggs from sharp-ribbed newts Pleurodeles waltl.Crossref | GoogleScholarGoogle Scholar |

Uteshev, VK, Gakhova, EN, Kramarova, LI, Shishova, NV, Kaurova, SA, and Browne, RK (2018). Refrigerated storage of European common frog Rana temporaria oocytes. Cryobiology 83, 56–59.
Refrigerated storage of European common frog Rana temporaria oocytes.Crossref | GoogleScholarGoogle Scholar | 29886118PubMed |

Venu G, Ramakrishna S, Venkatachalaiah G (2016) ‘Sperm morphology – a novel tool for Caecilian taxonomy (Amphibia: Gymnophiona).’ (National Seminar on Science and Technology for National Development: Kanpur, India)

Vu, M, and Trudeau, VL (2016). Neuroendocrine control of spawning in amphibians and its practical applications. General and Comparative Endocrinology 234, 28–39.
Neuroendocrine control of spawning in amphibians and its practical applications.Crossref | GoogleScholarGoogle Scholar | 27013378PubMed |

Vu, M, Weiler, B, and Trudeau, VL (2017). Time- and dose-related effects of a gonadotropin-releasing hormone agonist and dopamine antagonist on reproduction in the Northern leopard frog (Lithobates pipiens). General and Comparative Endocrinology 254, 86–96.
Time- and dose-related effects of a gonadotropin-releasing hormone agonist and dopamine antagonist on reproduction in the Northern leopard frog (Lithobates pipiens).Crossref | GoogleScholarGoogle Scholar | 28964731PubMed |

Wakayama, S, Ito, D, Kamada, Y, Shimazu, T, Suzuki, T, Nagamatsu, A, Araki, R, Ishikawa, T, Kamimura, S, Hirose, N, Kazama, K, Yang, L, Inoue, R, Kikuchi, Y, Hayashi, E, Emura, R, Watanabe, R, Nagatomo, H, Suzuki, H, Yamamori, T, Tada, MN, Osada, I, Umehara, M, Sano, H, Kasahara, H, Higashibata, A, Yano, S, Abe, M, Kishigami, S, Kohda, T, Ooga, M, and Wakayama, T (2021). Evaluating the long-term effect of space radiation on the reproductive normality of mammalian sperm preserved on the International Space Station. Science Advances 7, eabg5554.
Evaluating the long-term effect of space radiation on the reproductive normality of mammalian sperm preserved on the International Space Station.Crossref | GoogleScholarGoogle Scholar | 34117068PubMed |

Wake, MH (1994). Comparative morphology of caecilian Sperm (Amphibia: Gymnophiona). Journal of Morphology 221, 261–276.
Comparative morphology of caecilian Sperm (Amphibia: Gymnophiona).Crossref | GoogleScholarGoogle Scholar | 29865407PubMed |

Watanabe, T, Itoh, T, Watanabe, A, and Onitake, K (2003). Characteristics of sperm motility induced on the egg-jelly in the internal fertilization of the newt, Cynops pyrrhogaster. Zoological Science 20, 345–352.
Characteristics of sperm motility induced on the egg-jelly in the internal fertilization of the newt, Cynops pyrrhogaster.Crossref | GoogleScholarGoogle Scholar | 12692394PubMed |

WebMD (2021) Dimethylsulfoxide (DMSO). Overview, uses, side effects. Available at https://www.webmd.com/vitamins/ai/ingredientmono-874/dimethylsulfoxide-dmso

Wilkinson M, Nussbaum RA (2006) Caecilian phylogeny and classification. In ‘Reproductive biology and phylogeny of Gymnophiona (Caecilians)’. (Ed. J Exbrayat) pp. 39–71. (Science Publishers: Enfield, NH, USA)

Wirsig-Wiechmann, CR, Colvard, J, Aston, CE, Dighe, R, Houck, LD, Feldhoff, PW, and Feldhoff, RC (2012). Gonadotropin-releasing hormone modulates vomeronasal neuron response to male salamander pheromone. Journal of Experimental Neuroscience 6, 1–10.
Gonadotropin-releasing hormone modulates vomeronasal neuron response to male salamander pheromone.Crossref | GoogleScholarGoogle Scholar |

Yan, F, Lü, J, Zhang, B, Yuan, Z, Zhao, H, Huang, S, Wei, F, Wu, M, Xiao, H, Liang, Z, Jin, J, Wu, S, Xu, C, Tapley, B, Turvey, ST, Papenfuss, TJ, Cunningham, AA, Murphy, RW, Zhang, Y, and Che, J (2018). The Chinese giant salamander exemplifies the hidden extinction of cryptic species. Current Biology 28, R590–R592.
The Chinese giant salamander exemplifies the hidden extinction of cryptic species.Crossref | GoogleScholarGoogle Scholar | 29787716PubMed |

Yongjie, W, Honglian, C, Fen, W, and Fujiang, R (2017). Improved method in breeding and artificial propagation for Chinese giant salamanders (Andrias davidianus). Journal of Marine Biology and Aquaculture 3, 1–5.
Improved method in breeding and artificial propagation for Chinese giant salamanders (Andrias davidianus).Crossref | GoogleScholarGoogle Scholar |

Zalisko, EJ, Brandon, RA, and Martan, J (1984). Microstructure and histochemistry of salamander spermatophores (Ambystomatidae, Salamandridae and Plethodontidae). Copeia 1984, 739–747.
Microstructure and histochemistry of salamander spermatophores (Ambystomatidae, Salamandridae and Plethodontidae).Crossref | GoogleScholarGoogle Scholar |

Zhang, H, Shen, J, Zhao, H, and Wang, Q (2012). Study on spawning induction and incubation technology of the giant salamander (Andrias davidianus). Qi Hubei Agricultural Sciences 2012, .

Zhang, Z, Mammola, S, Liang, Z, Capinha, C, Wei, Q, Wu, Y, Zhou, J, and Wang, C (2020). Future climate change will severely reduce habitat suitability of the Critically Endangered Chinese giant salamander. Freshwater Biology 65, 971–980.
Future climate change will severely reduce habitat suitability of the Critically Endangered Chinese giant salamander.Crossref | GoogleScholarGoogle Scholar |

Zhao, H, Zhang, H, Wang, Q, and Chen, J (2012). Preliminary study on conservation of Andrias davidanus semen in vitro. Journal of Hydroecology 33, 149–152.

Zou, K, Thébault, E, Lacroix, G, and Barot, S (2015). Interactions between the green and brown food web determine ecosystem functioning. Functional Ecology 30, 1454–1465.
Interactions between the green and brown food web determine ecosystem functioning.Crossref | GoogleScholarGoogle Scholar |