Abstract
Amphibians have experienced a catastrophic decline since the 1980s driven by disease, habitat loss, and impacts of invasive species and face ongoing threats from climate change. About 40% of extant amphibians are under threat of extinction and about 200 species have disappeared completely. Reproductive technologies and biobanking of cryopreserved materials offer technologies that could increase the efficiency and effectiveness of conservation programs involving management of captive breeding and wild populations through reduced costs, better genetic management and reduced risk of species extinctions. However, there are relatively few examples of applications of these technologies in practice in on-the-ground conservation programs, and no example that we know of where genetic diversity has been restored to a threatened amphibian species in captive breeding or in wild populations using cryopreserved genetic material. This gap in the application of technology to conservation programs needs to be addressed if assisted reproductive technologies (ARTs) and biobanking are to realise their potential in amphibian conservation. We review successful technologies including non-invasive gamete collection, IVF and sperm cryopreservation that work well enough to be applied to many current conservation programs. We consider new advances in technology (vitrification and laser warming) of cryopreservation of aquatic embryos of fish and some marine invertebrates that may help us to overcome factors limiting amphibian oocyte and embryo cryopreservation. Finally, we address two case studies that illustrate the urgent need and the opportunity to implement immediately ARTs, cryopreservation and biobanking to amphibian conservation. These are (1) managing the biosecurity (disease risk) of the frogs of New Guinea which are currently free of chytridiomycosis, but are at high risk (2) the Sehuencas water frog of Bolivia, which until recently had only one known surviving male.
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References
Acharjee S, Maiti K, Soh JM, Im W-B, Seong JY, Kwon HB. Differential desensitization and internalization of three different bullfrog gonadotropin-releasing hormone receptors. Mol Cells. 2002;14:101–7.
Adams MJ. Pond permanence and the effects of exotic vertebrates on anurans. Ecol Appl. 2000;10:559–68.
Alonso-Bedate M, Carballada R, Delgado MJ. Effects of melatonin on gonadal steroids and glucose plasma levels in frogs (Rana perezi and Rana temporaria). J Pineal Res. 1990;8:79–89.
Alroy J. Current extinction rates of reptiles and amphibians. Proc Natl Acad Sci. 2015;112(42):13003–8.
Anstis M. Tadpoles and frogs of Australia. 2nd ed. Sydney: New Holland; 2017.
Araujo MB, et al. Climate warming and the decline of amphibians and reptiles in Europe. J Biogeogr. 2006;33:1712–28.
Argyle CE, Harper JC, Davies MC. Oocyte cryopreservation: where are we now? Hum Reprod Update. 2016;22:440–9.
Arregui L, Boveda P, Gosalvez J, Kouba AJ. Seasonal effect on sperm cryopreservation in Epidalea calamita (Anura: Bufonidae). Cryobiology. 2018;85:177.
Austin C, Hayden C, Bigilale I, Dahl C, Anaminiato J. Checklist and comments on the terrestrial amphibian and reptile fauna from Utai, Northwestern Papua New Guinea. Herpetol Rev. 2008;39(1):40–6.
Balinsky BI. Cleavage. In: An introduction to embryology. 4th ed. Philadelphia: W.B. Saunders; 1975a. p. 101–47.
Balinsky BI. Morphological aspects of gastrulation and primary organ formation. In: An Introduction to embryology. 4th ed. Philadelphia: W.B. Saunders; 1975b. p. 151–88.
Banks C, Clulow S, McGeorge M, Bower D. A future-proofing plan for Papua New Guinea frogs. AArk Newslett. 2018;42:16–7.
Barton HL, Gutman SL. Low temperature preservation of toad spermatozoa (Genus Bufo). Texas J Sci. 1972;23:363–70.
Beesley SG, Costanzo JP, Lee RE. Cryopreservation of spermatozoa from freeze-tolerant and -intolerant anurans. Cryobiology. 1998;37:155–62.
Berger L, Speare R, Daszak P, Green DE, Cunningham AA, Goggin CL, et al. Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proc Natl Acad Sci. 1998;95:9031–6.
Bischof J. Nanoparticle and metal form heating for improved cryopreservation. Cryobiology. 2018;85:164.
Bishop PJ, Angulo A, Lewis JP, Moore RD, Rabb GB, Moreno JG. The amphibian extinction crisis—what will it take to put the action into the Amphibian Conservation Action Plan? SAPIENS. 2012;(5.2). http://sapiens.revues.org/1406.
Bower DS, Lips K, Schwarzkopf L, Georges A, Clulow S. Amphibians on the brink. Science. 2017;357(6350):454–5.
Bower D, Lips K, Amepou Y, Richards S, Dahl C, Nagombi E, Supuma M, Dabek L, Alford R, Schwarzkopf L, Ziembicki M, Noro J, Hamidy A, Gillespie G, Berger L, Eisemberg C, Li Y, Liu X, Jennings C, Tjaturadi B, Peters A, Krockenberger A, Nason D, Kusrini M, Webb R, Skerratt L, Banks C, Mack A, Georges A, Clulow S. Island of opportunity: can New Guinea protect amphibians from a globally emerging pathogen? Front Ecol Environ. 2019; https://doi.org/10.1002/fee.2057.
Bradford DF. Allotopic distribution of native frogs and introduced fishes in high Sierra Nevada lakes of California: implication of the negative effect of fish introductions. Copeia. 1989;1989:775–8.
Browne RK, Clulow J, Mahony M, Clark A. Successful recovery of motility and fertility of cryopreserved cane toad (Bufo marinus) sperm. Cryobiology. 1998;37:339–45.
Browne RK, Clulow J, Mahony M. Short-term storage of cane toad (Bufo marinus) gametes. Reproduction. 2001;121:167–73.
Browne RK, Clulow J, Mahony M. The effect of saccharides on the post-thaw recovery of cane toad (Bufo marinus) spermatozoa. Cryo Letters. 2002a;23:121–8.
Browne RK, Clulow J, Mahony M. The short-term storage and cryopreservation of spermatozoa from Hylid and Myobatrachid frogs. CryoLetters. 2002b;23:129–36.
Browne RK, Clulow J, Mahony M. A comparison of sucrose, saline, and saline with egg-yolk diluents on the cryopreservation of cane toad (Bufo marinus) sperm. Cryobiology. 2002c;44:251–7.
Browne RK, Davis J, Pomering M, Clulow J. Storage of cane toad (Bufo marinus) sperm for 6 days at 0 °C with subsequent cyropreservation. Reprod Fertil Dev. 2002d;14:267–73.
Browne RK, Seratt J, Vance C, Kouba A. Hormonal priming, induction of ovulation and in-vitro fertilization of the endangered Wyoming toad (Bufo baxteri). Reprod Biol Endocrinol. 2006a;4:34.
Browne RK, Li H, Seratt J, Kouba A. Progesterone improves the number and quality of hormone induced Fowler toad (Bufo fowleri) oocytes. Reprod Biol Endocrinol. 2006b;4:3.
Browne R, Gaikhorst G, Vitali S, Roberts JD, Matson P. Exogenous hormones induce poor rates of oviposition in the anurans, Litoria moorei and L. aurea. Appl Herpetol. 2008;5(1):81–6.
Browne R, Janzen P, Bagaturov M, van Houte D. Amphibian keeper conservation breeding programs. J Zool Res. 2018;2:29–46.
Browne RK, et al. Sperm collection and storage for the sustainable management of amphibian biodiversity. Theriogenology. 2019;133:187–200.
Buchholz DR, Fu L, Shi YB. Cryopreservation of Xenopus transgenic lines. Mol Reprod Dev. 2004;67:65–9.
Byrne P, Silla A. Hormonal induction of gamete release, and in-vitro fertilisation, in the critically endangered Southern Corroboree Frog, Pseudophryne corroboree. Reprod Biol Endocrinol. 2010;8:144.
Calado LL. Coleta e criopreservação do sêmen de rã-touro. Universidade Federal de Viçosa; 2009.
Calvi SL, Maisse G. Cryopreservation of Rainbow Trout (Oncorhynchus mykiss) blastomeres: influence of embryo stage on postthaw survival rate. Cryobiology. 1998;36:255–62.
Calvi SL, Maisse G. Cryopreservation of carp (Cyprinus carpio) blastomeres. Aquat Living Resour. 1999;12:71–4.
Campbell L, Bower DS, Clulow S, Stockwell M, Clulow J, Mahony M. Interaction between temperature and sublethal infection with the amphibian chytrid fungus impacts a susceptible frog species. Sci Rep. 2019;9:83.
Cardona-Costa J, García-Ximénez F. Vitrification of zebrafish embryo blastomeres in microvolumes. CryoLetters. 2007;28:303–9.
Carey C, Alexander MA. Climate change and amphibian declines: is there a link? Divers Distrib. 2003;9:111–21.
Ceballos G, Ehrlich PR, Dirzo R. Biological annihilation via the ongoing sixth mass extinction signaled by vertebrate population losses and declines. Proc Natl Acad Sci. 2017;114:E6089–96.
Chakraborty M, Burmeister SS. Estradiol induces sexual behavior in female túngara frogs. Horm Behav. 2009;55:106–12.
Chakraborty M, Burmeister SS. Effects of estradiol on neural responses to social signals in female túngara frogs. J Exp Biol. 2015;218:3671–7.
Chanson J, et al. The State of the world’s amphibians. In: Stuart SN, Hoffmann M, Chanson JS, Cox NA, Berridge RJ, Ramani P, Young BE, editors. Threatened amphibians of the world. Barcelona, Gland, and Arlington: Lynx Edicions, IUCN, and Conservation International; 2008. p. 33–52.
Clulow J, Clulow S. Cryopreservation and other assisted reproductive technologies for the conservation of threatened amphibians and reptiles: bringing the arts up to speed. Reprod Fertil Dev. 2016;28:1116–32.
Clulow S, Swan M. A complete guide to frogs of Australia. Sydney: Australian Geographic; 2018. 336 pp.
Clulow J, Mahony M, Browne R, Pomering M, Clark A. Applications of assisted reproductive technologies (ART) to endangered anuran amphibians. In: Campbell A, editor. Declines and disappearances of Australian frogs. Canberra: Environment Australia; 1999. p. 219–25.
Clulow J, Clulow S, Guo J, French AJ, Mahony MJ, Archer M. Optimisation of an oviposition protocol employing human chorionic and pregnant mare serum gonadotropins in the barred frog Mixophyes fasciolatus (Myobatrachidae). Reprod Biol Endocrinol. 2012;10(1):60.
Clulow J, Trudeau VL, Kouba AJ. Amphibian declines in the twenty-first century: why we need assisted reproductive technologies. In: Holt WV, et al., editors. Reproductive sciences in animal conservation, Advances in experimental medicine and biology 753. New York: Springer; 2014. p. 275–316. https://doi.org/10.1007/978-1-4939-0820-2_12.
Clulow J, Pomering M, Herbert D, Upton R, Calatayud N, Clulow S, Mahony M, Trudeau V. Differential success in obtaining gametes between male and female Australian temperate frogs by hormonal induction: a review. Gen Comp Endocrinol. 2018a;265:141–8.
Clulow S, Gould J, James H, Stockwell M, Clulow J, Mahony M. Elevated salinity blocks pathogen transmission and improves host survival from the global amphibian chytrid pandemic: implications for translocations. J Appl Ecol. 2018b;55:830–40.
Collin F, Chartrel N, Fasolo A, Conlon JM, Vandesande F, Vaudry H. Distribution of two molecular forms of gonadotropin-releasing hormone (GnRH) in the central nervous system of the frog Rana ridibunda. Brain Res. 1995;703:111–28.
Corley-Smith GE, Lim CJ, Brandhorst BP. Production of androgenetic zebrafish (Danio rerio). Genetics. 1996;142:1265–76.
Costanzo JP, Mugnano JA, Wehrheim HM, Lee RE. Osmotic and freezing tolerance in spermatozoa of freeze-tolerant and -intolerant frogs. Am J Physiol Regul Integr Comp Physiol. 1998;275:R713–9.
Creighton AE, Wilczynski W. Influence of dopamine D2-type receptors on motor behaviors in the green tree frog, Hyla cinerea. Physiol Behav. 2014;127:71–80.
Creighton A, Satterfield D, Chu J. Effects of dopamine agonists on calling behavior in the green tree frog, Hyla cinerea. Physiol Behav. 2013;116:54–9.
Crossland MR, Brown GP, Anstis M, Shilton CM, Shine R. Mass mortality of native anuran tadpoles in tropical Australia due to the invasive cane toad (Bufo marinus). Biol Conserv. 2008;141:2387–94.
Daly J, Zuchowicz N, Nuñez Lendo CI, Khosla K, Lager C, Henley M, Bischof J, Kleinhans FW, Lin C, Peters E, et al. Successful cryopreservation of coral larvae using vitrification and laser warming. Scientific Reports. 2018; https://doi.org/10.1038/s41598-018-34035-0.
Dash SN, Routray P, Dash C, Guru BC, Swain P, Sarangi N. Use of the nontoxic cryoprotectant trehalose enhances recovery and function of fish embryonic stem cells following cryogenic storage. Curr Stem Cell Res Ther. 2008;3:277–87.
Davis A, Abraham E, McEvoy E, Sonnenfeld S, Lewis C, Hubbard CS, Dolence EK, Rose JD, Coddington E. Corticosterone suppresses vasotocin-enhanced clasping behavior in male rough-skinned newts by novel mechanisms interfering with V1a receptor availability and receptor-mediated endocytosis. Horm Behav. 2015;69:39–49.
del Pino EM, Venegas-Ferrín M, Romero-Carvajal A, Montenegro-Larrea P, Sáenz-Ponce N, Moya IM, Alarcón I, Sudou N, Yamamoto S, Taira M. A comparative analysis of frog early development. Proc Natl Acad Sci U S A. 2007;104:11882–8.
Della Togna Nieto G. Structural and functional characterization of the Panamanian golden frog (Atelopus zeteki) spermatozoa—impact of medium osmolality and cryopreservation on motility and cell viability. Dissertation, University of Maryland. 2015.
Deng J, Carbajal L, Evaul K, Rasar M, Jamnongjit M, Hammes SR. Nongenomic steroid-triggered oocyte maturation: of mice and frogs. Steroids. 2009;74:595–601.
Derakhshan Z, Nokhbatolfoghahai M, Zahiri S. Cryopreservation of Bufotes viridis embryos by vitrification. Cryobiology. 2017;75:60–7.
Di Berardino MA. Genomic potential of differentiated cells. New York: Columbia University Press; 1997.
Diez C, Munoz M, Caamano J, Gomez E. Cryopreservation of the bovine oocyte: current status and perspectives. Reprod Domest Anim. 2012;47:76–83.
Donnelly MA, Crump ML. Potential effects of climate change on two neotropical amphibian assemblages. Clim Change. 1998;39:541–61.
Du Pasquier D, Dupré A, Jessus C. Unfertilized xenopus eggs die by bad-dependent apoptosis under the control of cdk1 and jnk. PLoS One. 2011;6:e23672.
Duellman WE, Trueb L. Biology of amphibians. Baltimore: Johns Hopkins University Press; 1994.
Dufour S, Weltzien FA, Sebert ME, Le Belle N, Vidal B, Vernier P, Pasqualini C. Dopaminergic inhibition of reproduction in teleost fishes: ecophysiological and evolutionary implications. Ann N Y Acad Sci. 2005;1040:9–21.
Edwards DL, Mahony MJ, Clulow J. Effect of sperm concentration, medium osmolality, and oocyte storage on artificial fertilisation success in a myobatrachid frog (Limnodynastes tasmaniensis). Reprod Fertil Dev. 2004;16:347–54.
Elinson RP, del Pino EM. Developmental diversity of amphibians. Wiley Interdiscip Rev Dev Biol. 2012;1:345–69.
Eroglu A, Bailey SE, Toner M, Toth TL. Successful cryopreservation of mouse oocytes by using low concentrations of trehalose and dimethylsulfoxide. Biol Reprod. 2009;80:70–8.
Evaul K, Jamnongjit M, Bhagavath B, Hammes SR. Testosterone and progesterone rapidly attenuate plasma membrane Gβγ-mediated signaling in Xenopus laevis oocytes by signaling through classical steroid receptors. Mol Endocrinol. 2007;21:186–96.
Fahy GM, MacFarlane D, Angell C, Meryman H. Vitrification as an approach to cryopreservation. Cryobiology. 1984;21:407–26.
Figiel CR. Cryopreservation of sperm from the axolotl Ambystoma mexicanum: implications for conservation. Herpetol Conserv Biol. 2013;8(3):748–55.
Fitzsimmons C, McLaughlin EA, Mahony MJ, Clulow J. Optimisation of handling, activation and assessment procedures for Bufo marinus spermatozoa. Reprod Fertil Dev. 2007;19(4):594–601.
Foden WB, Butchart SH, Stuart SN, Vié J-C, Akçakaya HR, Angulo A, DeVantier LM, Gutsche A, Turak E, Cao L. Identifying the world’s most climate change vulnerable species: a systematic trait-based assessment of all birds, amphibians and corals. PLoS One. 2013;8:e65427.
Franěk R, Marinović Z, Lujić J, Urbányi B, Fučíková M, Kašpar V, Pšenička M, Horváth Á. Cryopreservation and transplantation of common carp spermatogonia. bioRxiv. 2018:429449.
Frankham R. Challenges and opportunities of genetic approaches to biological conservation. Biol Conserv. 2010;143(9):1919–27.
Frankham R. Genetic rescue of small inbred populations: meta-analysis reveals large and consistent benefits of gene flow. Mol Ecol. 2015;24(11):2610–8.
Gibbs JP, Breisch AR. Climate warming and calling phenology of frogs near Ithaca, New York, 1900-1999. Conserv Biol. 2001;15:1175–8.
Gillespie LL, Armstrong JB. Production of androgenetic diploid axolotls by suppression of first cleavage. J Exp Zool. 1980;213:423–5.
Godoy LC, Streit DP Jr, Zampolla T, Bos-Mikich A, Zhang T. A study on the vitrification of stage III zebrafish (Danio rerio) ovarian follicles. Cryobiology. 2013;67:347–54.
Goodsell JA, Kats LB. Effect of introduced mosquitofish on Pacific treefrogs and the role of alternative prey. Conserv Biol. 1999;13:921–4.
Gordon NM, Gerhardt HC. Hormonal modulation of phonotaxis and advertisement-call preferences in the gray treefrog (Hyla versicolor). Horm Behav. 2009;55:121–7.
Guan M, Rawson DM, Zhang T. Cryopreservation of zebrafish (Danio rerio) oocytes by vitrification. Cryo Letters. 2010;31:230–8.
Guenther JF, Seki S, Kleinhans FW, Edashige K, Roberts DM, Mazur P. Extra- and intra-cellular ice formation in stage I and II Xenopus laevis oocytes. Cryobiology. 2006;52:401–16.
Günther R. Derived reproductive modes in New Guinean anuran amphibians and description of a new species with paternal care in the genus Callulops (Microhylidae). J Zool. 2006;268:153–70.
Gurdon JB. The effects of ultraviolet irradiation on uncleaved eggs of Xenopus laevis. Q J Microsc Sci. 1960;101:299–311.
Gurdon J, Byrne J. The first half-century of nuclear transplantation. Proc Natl Acad Sci U S A. 2003;100:8048–52.
Gurdon JB, Hopwood N. The introduction of Xenopus laevis into developmental biology: of empire, pregnancy testing and ribosomal genes. Int J Dev Biol. 2000;44:43–50.
Gurdon JB, Uehlinger V. “Fertile” intestine nuclei. Nature. 1966;210:1240–1.
Gurdon JB, Laskey RA, Reeves OR. The developmental capacity of nuclei transplanted from keratinized skin cells of adult frogs. J Embryol Exp Morphol. 1975;34:93–112.
Hagedorn M, Kleinhans FW. Problems and prospects in cryopreservation of fish embryos. In: Tiersch TR, Green CC, editors. Cryopreservation in aquatic species. 2nd ed. Baton Rouge: World Aquaculture Society; 2011. p. 483–502.
Hagedorn M, Hsu EW, Pilatus U, Wildt DE, Rall WF, Blackband SJ. Magnetic resonance microscopy and spectroscopy reveal kinetics of cryoprotectant permeation in a multicompartmental biological system. Proc Natl Acad Sci U S A. 1996;93:7454–9.
Hagedorn M, Hsu E, Kleinhans FW, Wildt DE. New approaches for studying the permeability of fish embryos: toward successful cryopreservation. Cryobiology. 1997a;34:335–47.
Hagedorn M, Kleinhans FW, Freitas R, Liu J, Hsu EW, Wildt DE, et al. Water distribution and permeability of zebrafish embryos, Brachydanio rerio. J Exp Zool. 1997b;278:356–71.
Hagedorn M, Kleinhans FW, Wildt DE, Rall WF. Chill sensitivity and cryoprotectant permeability of dechorionated zebrafish embryos, Brachydanio rerio. Cryobiology. 1997c;34:251–63.
Hagedorn M, Kleinhans FW, Artemov D, Pilatus U. Characterization of a major permeability barrier in the zebrafish embryo. Biol Reprod. 1998;59:1240–50.
Hagedorn M, Peterson A, Mazur P, Kleinhans FW. High ice nucleation temperature of zebrafish embryos: slow-freezing is not an option. Cryobiology. 2004;49:181–9.
Harding G, Griffiths RA, Pavajeau L. Developments in amphibian captive breeding and reintroduction programs. Conserv Biol. 2016;30:340–9.
Harvey B. Cooling of embryonic cells, isolated blastoderms, and intact embryos of the zebra fish Brachydanio rerio to -196°C. Cryobiology. 1983;20:440–7.
He X, Park EY, Fowler A, Yarmush ML, Toner M. Vitrification by ultra-fast cooling at a low concentration of cryoprotectants in a quartz micro-capillary: a study using murine embryonic stem cells. Cryobiology. 2008;56:223–32.
Hecnar SJ, M’Closkey RT. Changes in the composition of a ranid frog community following bullfrog extinction. Am Midl Nat. 1997;137:145–50.
Higaki S, Eto Y, Kawakami Y, Yamaha E, Kagawa N, Kuwayama M, et al. Production of fertile zebrafish (Danio rerio) possessing germ cells (gametes) originated from primordial germ cells recovered from vitrified embryos. Reproduction. 2010;139:733–40.
Hill JE, Kilgore KH, Pouder DB, Powell JF, Watson CA, Yanong RP. Survey of ovaprim use as a spawning aid in ornamental fishes in the United States as administered through the University of Florida Tropical Aquaculture Laboratory. N Am J Aquac. 2009;71:206–9.
Hoelker M, Schmoll F, Schneider H, Rings F, Gilles M, Tesfaye D, Jennen D, Tholen E, Griese J, Schellander K. Bovine blastocyst diameter as a morphological tool to predict embryo cell counts, embryo sex, hatching ability and developmental characteristics after transfer to recipients. Reprod Fertil Dev. 2006;18:551–7.
Hollinger T, Corton G. Artificial fertilization of gametes from the South African clawed frog, Xenopus laevis. Gamete Res. 1980;3:45–7.
Hong N, Chen S, Ge R, Song J, Yi M, Hong Y. Interordinal chimera formation between medaka and zebrafish for analyzing stem cell differentiation. Stem Cells Dev. 2012;21:2333–41.
Hopkins BK, Herr C. 78 Cryopreservation of frog (Rana pipiens) sperm cells collected by non-lethal methods. Reprod Fertil Dev. 2007;20:120.
Horseman ND, Smith CA, Culley DD Jr. Effects of age and photoperiod on ovary size and condition in bullfrogs (Rana catesbeiana, Shaw) (Amphibia, Anura, Ranidae). J Herpetol. 1978;12:287–90.
Howard JG, Marinari PE, Wildt DE. Black-footed ferret: model for assisted reproductive technologies contributing to in situ conservation. In: Holt WV, Pickard AR, Rodger JC, Wildt DE, editors. Reproductive science and integrated conservation. Cambridge: University Press; 2003. p. 249–66.
Howard JG, Lynch C, Santymire RM, Marinari PE, Wildt DE. Recovery of gene diversity using long-term cryopreserved spermatozoa and artificial insemination in the endangered black-footed ferret. Anim Conserv. 2016;19:102–11.
Hwang I-S, Hochi S. Recent progress in cryopreservation of bovine oocytes. Biomed Res Int. 2014;2014:570647.
Inoda T, Morisawa M. Effect of osmolality on the initiation of sperm motility in Xenopus laevis. Comp Biochem Physiol A Physiol. 1987;88(3):539–42.
Isayeva A, Zhang T, Rawson DM. Studies on chilling sensitivity of zebrafish (Danio rerio) oocytes. Cryobiology. 2004;49:114–22.
Ishibashi S, Kroll KL, Amaya E. Generation of transgenic Xenopus laevis: II. Sperm nuclei preparation. CSH Protoc. 2007a;2007:pdb.prot4839.
Ishibashi S, Kroll KL, Amaya E. Generation of transgenic Xenopus laevis: III. Sperm nuclear transplantation. Cold Spring Harb Protoc. 2007b;2007:pdb.prot4840.
Jin B, Kleinhans FW, Mazur P. Survivals of mouse oocytes approach 100% after vitrification in 3-fold diluted media and ultra-rapid warming by an IR laser pulse. Cryobiology. 2014;68:419–30.
Kaurova S, Chekurova N, Melnikova E, Uteshev V, Gakhova E. Cryopreservation of frog Rana temporaria sperm without loss of fertilizing capacity. In: Paper presented at genetic resource conservation proc of XIV working meeting, Pushchino, 13–15 May 1996; 1996.
Kaurova S, Uteshev V, Chekurova N, Gakhova E. Cryopreservation of testis of frog Rana temporaria. Infusionsther Transfusionsmed. 1997;24:78–9.
Keogh LM, Byrne PG, Silla AJ. The effect of gentamicin on sperm motility and bacterial abundance during chilled sperm storage in the Booroolong frog. Gen Comp Endocrinol. 2017;243:51–9.
Khalili MA, A Nottola S, Shahedi A, Macchiarelli G. Contribution of human oocyte architecture to success of in vitro maturation technology. Iranian J Reprod Med. 2013;11:1–10.
Khosla K, Wang Y, Hagedorn M, Qin Z, Bischof J. Gold nanorod induced warming of embryos from the cryogenic state enhances viability. ACS Nano. 2017;11:7869–78.
Khosla K, Zhan L, Bhati A, Carley-Clopton A, Hagedorn M, Bischof J. Characterization of laser gold nanowarming: a platform for millimeter-scale cryopreservation. Langmuir. 2018a; https://doi.org/10.1021/acs.langmuir.8b03011.
Khosla K, Zhan L, Bhati A, Carley-Clopton A, Hagedorn M, Bischof J. Physical limits of laser gold nanowarming. Cryobiology. 2018b;85:161.
Kiesecker JM, Blaustein AR, Miller CL. Transfer of a pathogen from fish to amphibians. Conserv Biol. 2001;15:1064–70.
Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF. Stages of embryonic development of the zebrafish. Dev Dyn. 1995;203:253–310.
Kleinhans FW, Guenther JF, Seki S, Edashige K, Roberts DM, Mazur P. Water Pf of Xenopus (AQP +/-) Stage I and II oocytes. Cryobiology. 2005;51:389.
Kleinhans FW, Guenther JF, Roberts DM, Mazur P. Analysis of intracellular ice nucleation in Xenopus oocytes by differential scanning calorimetry. Cryobiology. 2006;52:128–38.
Klop-Toker KL, Valdez JW, Stockwell MP, Edgar ME, Fardell L, Clulow S, Clulow J, Mahony MJ. Assessing host response to disease treatment: how chytrid-susceptible frogs react to increased water salinity. Wildl Res. 2018;44:648–59.
Knapp RA, Matthews KR. Non-native fish introductions and the decline of the mountain yellow-legged frog from within protected areas. Conserv Biol. 2000;14:1–12.
Knapp RA, Boiano DM, Vredenburg VT. Removal of nonnative fish results in population expansion of a declining amphibian (mountain yellow-legged frog, Rana muscosa). Biol Conserv. 2007;135(1):11–20.
Köseoglu M, Eroglu A, Toner M, Sadler KC. Starfish oocytes form intracellular ice at unusually high temperatures. Cryobiology. 2001;43:248–59.
Kouba AJ, Vance CK. Applied reproductive technologies and genetic resource banking for amphibian conservation. Reprod Fertil Dev. 2009;21:719–37.
Kouba AJ, Vance CK, Frommeyer MA, Roth TL. Structural and functional aspects of Bufo americanus spermatozoa: effects of inactivation and reactivation. J Exp Zool. 2003;295A:172–82.
Kouba AJ, Vance CK, Willis EL. Artificial fertilization for amphibian conservation: current knowledge and future considerations. Theriogenology. 2009;71:214–27.
Kouba A, Willis E, Vance C, Hasenstab S, Reichling S, Krebs J, Linhoff L, Snoza M, Langhorne C, Germano J. 116 development of assisted reproduction technologies for the endangered Mississippi gopher frog (Rana sevosa) and sperm transfer for in vitro fertilization. Reprod Fertil Dev. 2011;24:170.
Kouba AJ, Lloyd RE, Houck ML, Silla AJ, Calatayud N, Trudeau VL, et al. Emerging trends for biobanking amphibian genetic resources: the hope, reality and challenges for the next decade. Biol Conserv. 2013;164:10–21.
Kusuda S, Teranishi T, Koide N. Cryopreservation of chum salmon blastomeres by the straw method. Cryobiology. 2002;45:60–7.
Kusuda S, Teranishi T, Koide N, Nagai T, Arai K, Yamaha E. Pluripotency of cryopreserved blastomeres of the goldfish. J Exp Zool A Comp Exp Biol. 2004;301(2):131–8.
Kuwayama M, Vajta G, Kato O, Leibo SP. Highly efficient vitrification method for cryopreservation of human oocytes. Reprod Biomed Online. 2005;11:300–8.
Lambert MR, et al. Molecular evidence for sex reversal in wild populations of green frogs (Rana clamitans). PeerJ. 2019;7:e6449. https://doi.org/10.7717/peerj.6449.
Langhorne CJ, Calatayud NE, Kouba AJ, Feugang JM, Vance CK, Willard ST. 026 Cryoconservation: successful sperm cryopreservation and develop-mental outcomes using endangered North American amphibians. Cryobiology. 2013;67(3):405.
Lawler SP, Dritz D, Strange T, Holyoak M. Effects of introduced mosquitofish and bullfrogs on the threatened California red-legged frog. Conserv Biol. 1999;13:613–22.
Lawson B, Clulow S, Mahony MJ, Clulow J. Towards gene banking amphibian maternal germ lines: short-term incubation, cryoprotectant tolerance and cryopreservation of embryonic cells of the frog, Limnodynastes peronii. PLoS One. 2013;8(4):e60760.
Leibo S, Loskutoff N. Cryobiology of in vitro-derived bovine embryos. Theriogenology. 1993;39:81–94.
Licht P, Tsai P-S, Sotowska-Brochocka J. The nature and distribution of gonadotropin-releasing hormones in brains and plasma of ranid frogs. Gen Comp Endocrinol. 1994;94:186–98.
Liebermann J, Tucker MJ. Vitrifying and warming of human blastocysts using the Cryotop. In: Vitrification in assisted reproduction. London: CRC Press; 2007. p. 258–64.
Lin S, Long W, Chen J, Hopkins N. Production of germ-line chimeras in zebrafish by cell transplants from genetically pigmented to albino embryos. Proc Natl Acad Sci U S A. 1992;89:4519–23.
Lin C, Zhang T, Rawson DM. Cryopreservation of zebrafish (Danio rerio) blastomeres by controlled slow cooling. CryoLetters. 2009;30:132–41.
Lips KR, Brem F, Brenes R, Reeve JD, Alford RA, Voyles J, et al. Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proc Natl Acad Sci U S A. 2006;103:3165–70.
Liu X-H, Zhang T, Rawson DM. The effect of partial removal of yolk on the chilling sensitivity of zebrafish (Danio rerio) embryos. Cryobiology. 1999;39:236–42.
Liu X-H, Zhang T, Rawson DM. Differential scanning calorimetry studies of intramembrane freezing and cryoprotectant penetration in zebrafish (Danio rerio) embryos. J Exp Zool. 2001;290:299–310.
Longcore JE, Pessier AP, Nichols DK. Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia. 1999;91:219–27.
Lujić J, Franěk R, Marinović Z, Kašpar V, Pšenička M, Urbányi B, Horváth Á. Cryopreservation of common carp (Cyprinus carpio) spermatogonial stem cells. Cryobiology. 2018;85:158.
Luo T, Xu Y, Hoffman TL, Zhang T, Schilling T, Sargent TD. Inca: a novel p21-activated kinase-associated protein required for cranial neural crest development. Development. 2007;134(7):1279–89.
Luyet BJ, Hodapp EL. Revival of frog’s spermatozoa vitrified in liquid air. Proc Soc Exp Biol Med. 1938;39:433–4.
Madsen T, Shine R, Olsson M, Wittzell H. Conservation biology: restoration of an inbred adder population. Nature. 1999;402:34–5.
Mansour N, Lahnsteiner F, Patzner RA. Optimization of the cryopreservation of African clawed frog (Xenopus laevis) sperm. Theriogenology. 2009;72:1221–8.
Mansour N, Lahnsteiner F, Patzner RA. Motility and cryopreservation of spermatozoa of European common frog, Rana temporaria. Theriogenology. 2010;74:724–32.
Marcec R, Langhorne C, Vance C, Kouba A, Willard S. C-1013: cryopreservation of spermic milt in the model species Ambystoma tigrinum (Tiger salamander) for application in endangered salamanders. Cryobiology. 2014;69:515.
Marinović Z, Li Q, Lujić J, Iwasaki Y, Csenki Z, Urbányi B, Horváth Á, Yoshizaki G. Testis cryopreservation and spermatogonia transplantation as a tool for zebrafish line reconstitution. Cryobiology. 2018a;85:145–6.
Marinović Z, Lujić J, Kása E, Csenki Z, Urbányi B, Horváth Á. Cryopreservation of zebrafish spermatogonia by whole testes needle immersed ultra-rapid cooling. J Vis Exp. 2018b;133:e56118.
Masui Y. Relative roles of the pituitary, follicle cells, and progesterone in the induction of oocyte maturation in Rana pipiens. J Exp Zool. 1967;166:365–75.
Mazur P. Principles of cryobiology. In: Fuller BJ, Lane N, Benson EE, editors. Life in the frozen state. Boca Rotan: CRC Press; 2004. p. 3–65.
Mazur P, Kleinhans FW. Relationship between intracellular ice formation in oocytes of the mouse and Xenopus and the physical state of the external medium—a revisit. Cryobiology. 2008;56:22–7.
Mazur P, Seki S. Survival of mouse oocytes after being cooled in a vitrification solution to −196 °C at 95 to 70,000 °C/min and warmed at 610 to 118,000 °C/min: a new paradigm for cryopreservation by vitrification. Cryobiology. 2011;62:1–7.
Mazur P, Seki S, Pinn IL, Kleinhans FW, Edashige K. Extra- and intracellular ice formation in mouse oocytes. Cryobiology. 2005;51:29–53.
Mazzoni R, Cunningham AA, Daszak P, Apolo A, Perdomo E, et al. Emerging pathogen of wild amphibians in frogs (Rana catesbeiana) farmed for international trade. Emerg Infect Dis. 2003;9:3–30.
McKinnell RG. Cloning: nuclear transplantation in amphibia. Minneapolis: University of Minnesota Press; 1978.
McKinnell RG, Picciaano DJ, Kreig RE. Fertilization and development of frog eggs after repeated spermiation induced by human chorionic gonadotrophin. Lab Anim Sci. 1976;26:932–5.
Menzies J. The frogs of New Guinea and the Solomon Islands. Sofia: Pensoft; 2006.
Messaoud NB, Yue J, Valent D, Katzarova I, López JM. Osmostress-induced apoptosis in Xenopus oocytes: role of stress protein kinases, calpains and smac/diablo. PLoS One. 2015;10:e0124482.
Michael SF, Jones C. Cryopreservation of spermatozoa of the terrestrial Puerto Rican frog, Eleutherodactylus coqui. Cryobiology. 2004;48:90–4.
Michael S, Buckley C, Toro E, Estrada A, Vincent S. Induced ovulation and egg deposition in the direct developing anuran Eleutherodactylus coqui. Reprod Biol Endocrinol. 2004;2:6.
Mollard R. Culture, cryobanking and passaging of karyotypically validated native Australian amphibian cells. Cryobiology. 2018;81:201–5.
Monfort SL. “Mayday Mayday Mayday”, the Millenium Ark is sinking! In: Holt WV, et al., editors. Reproductive sciences in animal conservation, Advances in experimental medicine and biology 753. New York: Springer; 2014. p. 15–31. https://doi.org/10.1007/978-1-4939-0820-2_2.
Moore FL. Reproductive endocrinology of amphibians. In: Chester-Jones L, Ingleton PM, Phillips JG, editors. Fundamentals of comparative vertebrate endocrinology. New York: Springer; 1987. p. 207–21.
Morrow SG. The effects of DNA damage caused by sperm cryopreservation in Xenopus. University of Portsmouth; 2015.
Morrow S, Gosálvez J, López-Fernández C, Arroyo F, Holt WV, Guille MJ. Effects of freezing and activation on membrane quality and DNA damage in Xenopus tropicalis and Xenopus laevis spermatozoa. Reprod Fertil Dev. 2017;29:1556–66.
Moyle PB. Effects of introduced bullfrogs (Rana catesbeiana), on the native frogs of the San Joaquin Valley, California. Copeia. 1973;1:18–22.
Mugnano JA, Costanzo JP, Beesley SG, Lee RE. Evaluation of glycerol and dimethyl sulfoxide for the cryopreservation of spermatozoa from the wood frog (Rana sylvatica). CryoLetters. 1998;19:249–54.
Murray K, Retallick R, McDonald KR, Mendez D, Aplin K, Kirkpatrick P, et al. The distribution and host range of the pandemic disease chytridiomycosis in Australia spanning surveys from 1956 to 2007. Ecology. 2010;91:1557.
Nakamura M. Sex determination in amphibians. Semin Cell Dev Biol. 2009;20(3):271–82. https://doi.org/10.1016/j.semcdb.2008.10.003.
Nakano M, Hasunuma I, Okada R, Yamamoto K, Kikuyama S, Machida T, Kobayashi T. Molecular cloning of bullfrog D2 dopamine receptor cDNA: tissue distribution of three isoforms of D2 dopamine receptor mRNA. Gen Comp Endocrinol. 2010a;168:143–8.
Nakano M, Minagawa A, Hasunuma I, Okada R, Tonon M-C, Vaudry H, Yamamoto K, Kikuyama S, Machida T, Kobayashi T. D2 Dopamine receptor subtype mediates the inhibitory effect of dopamine on TRH-induced prolactin release from the bullfrog pituitary. Gen Comp Endocrinol. 2010b;168:287–92.
Narayan E, Hero J-M. Urinary corticosterone responses and haematological stress indicators in the endangered Fijian ground frog (Platymantis vitiana) during transportation and captivity. Aust J Zool. 2011;59:79–85.
Narayan EJ, Cockrem JF, Hero J-M. Urinary corticosterone metabolite responses to capture and captivity in the cane toad (Rhinella marina). Gen Comp Endocrinol. 2011;173:371–7.
Nilsson EE, Cloud JG. Rainbow trout chimeras produced by injection of blastomeres into recipient blastulae. Proc Natl Acad Sci U S A. 1992;89:9425–8.
Nilsson EE, Cloud JG. Cryopreservation of rainbow trout (Oncorhynchus mykiss) blastomeres. Aquat Living Resour. 1993;6:77–80.
O’Hanlon SJ, Rieux A, Farrer RA, Rosa GM, Waldman B, Bataille A, Kosch TA, Murray KA, Brankovics B, Fumagalli M. Recent Asian origin of chytrid fungi causing global amphibian declines. Science. 2018;360:621–7.
O’Brien ED, Salicioni AM, Cabada MO, Arranz SE. Vitellogenesis in Bufo arenarum: identification, characterization and immunolocalization of high molecular mass lipovitellin during oogenesis. Comp Biochem Physiol B Biochem Mol Biol. 2010;155:256–65.
Otoi T, Yamamoto K, Koyama N, Tachikawa S, Suzuki T. Bovine oocyte diameter in relation to developmental competence. Theriogenology. 1997;48:769–74.
Parsons JE, Thorgaard GH. Production of androgenetic diploid rainbow trout. J Hered. 1984;76:177–81.
Pearl E, Morrow S, Noble A, Lerebours A, Horb M, Guille M. An optimized method for cryogenic storage of Xenopus sperm to maximise the effectiveness of research using genetically altered frogs. Theriogenology. 2017;92:149–55.
Peng L-Y, Xiao Y-M, Liu Y. Effect of cryopreservation and short-term storage of Chinese giant salamander sperm. Acta Hydrobiol Sinica. 2011;35:325–31.
Peter RE, Lin H-R, Van Der Kraak G. Induced ovulation and spawning of cultured freshwater fish in China: advances in application of GnRH analogues and dopamine antagonists. Aquaculture. 1988;74:1–10.
Peyridieu J, Baudot A, Boutron P, Mazuer J, Odin J, Ray A, Chapelier E, Payen E, Descotes J. Critical cooling and warming rates to avoid ice crystallization in small pieces of mammalian organs permeated with cryoprotective agents. Cryobiology. 1996;33:436–46.
Popesku JT, Martyniuk CJ, Mennigen J, Xiong H, Zhang D, Xia X, Cossins AR, Trudeau VL. The goldfish (Carassius auratus) as a model for neuroendocrine signaling. Mol Cell Endocrinol. 2008;293:43–56.
Porter KR. Androgenetic development of the egg of Rana pipiens. Biol Bull. 1939;77:233–57.
Pounds JA, Crump ML. Amphibian declines and climate disturbance: the case of the golden toad and the harlequin frog. Conserv Biol. 1994;8:72–85.
Pounds JA, Fogden MPL, Campbell JH. Biological response to climate change on a tropical mountain. Nature. 1999;398:611–5.
Proaño B, Pérez OD. In vitro fertilizations with cryopreserved sperm of Rhinella marina (Anura: Bufonidae) in Ecuador. Amphibian Reptile Conserv. 2017;11:1–6.
Rall W, Fahy G. Vitrification: a new approach to embryo cryopreservation. Theriogenology. 1985a;23:220.
Rall WF, Fahy GM. Ice-free cryopreservation of mouse embryos at −196°C by vitrification. Nature. 1985b;313:573.
Rasar MA, Hammes SR. The physiology of the Xenopus laevis ovary. In: Liu XJ, editor. Xenopus protocols: cell biology and signal transduction. Totowa: Humana Press; 2006. p. 17–30.
Rienzi L, Balaban B, Ebner T, Mandelbaum J. The oocyte. Hum Reprod. 2012;27:i2–i21.
Roth TL, Szymanski DC, Keyster ED. Effects of age, weight, hormones, and hibernation on breeding success in boreal toads (Bufo boreas boreas). Theriogenology. 2010;73:501–11.
Routray P, Dash C, Dash SN, Tripathy S, Verma DK, Swain SK, et al. Cryopreservation of isolated blastomeres and embryonic stem-like cells of Leopard danio, Brachydanio frankei. Aquacult Res. 2010;41:579–89.
Rugh R. Experimental embryology techniques and procedures. Minneapolis: Burgess Publishing; 1962.
Ryder OA, Onuma M. Viable cell culture banking for biodiversity characterization and conservation. Annu Rev Anim Biosci. 2018;6:83–98.
Salgado Costa C, Trudeau VL, Ronco AE, Natale GS. Exploring antipredator mechanisms: new findings in ceratophryid tadpoles. J Herpetol. 2016;50:233–8.
Santymire R, Livieri T, Branvold-Faber H, Marinari P. The black-footed ferret: on the brink of recovery? In: Holt WV, Brown JL, Comizzoli P, editors. Reproductive sciences in animal conservation, vol. 753. New York: Springer; 2014. p. 119–34.
Sargent MG, Mohun TJ. Cryopreservation of sperm of Xenopus laevis and Xenopus tropicalis. Genesis. 2005;41:41–6.
Sarre SD, Ezaz T, Georges A. Transitions between sex-determining systems in reptiles and amphibians. Annu Rev Genomics Hum Genet. 2011;12(1):391–406. https://doi.org/10.1146/annurev-genom-082410-101518.
Scheele BC, Hunter DA, Grogan LF, Berger L, Kolby JE, McFadden MS, Marantelli G, Skerratt LF, Driscoll DA. Interventions for reducing extinction risk in chytridiomycosis-threatened amphibians. Conserv Biol. 2014;28:1195–205.
Scheele BC, Pasmans F, Skerratt LF, Berger L, Martel A, Beukema W, Acevedo AA, Burrowes PA, Carvalho T, Catenazzi A. Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity. Science. 2019;363:1459–63.
Seong JY, Wang L, Oh DY, Yun O, Maiti K, Li JH, Soh JM, Choi HS, Kim K, Vaudry H. Ala/Thr201 in extracellular loop 2 and Leu/Phe290 in transmembrane domain 6 of type 1 frog gonadotropin-releasing hormone receptor confer differential ligand sensitivity and signal transduction. Endocrinology. 2003;144:454–66.
Sherman CD, Wapstra E, Uller T, Olsson M. Male and female effects on fertilization success and offspring viability in the Peron’s tree frog, Litoria peronii. Austral Ecol. 2008;33:348–52.
Shishova NR, Uteshev VK, Kaurova SA, Browne RK, Gakhova EN. Cryopreservation of hormonally induced sperm for the conservation of threatened amphibians with Rana temporaria as a model research species. Theriogenology. 2011;75(2):220–32.
Silla A. Effect of priming injections of luteinizing hormone-releasing hormone on spermiation and ovulation in Gunther’s toadlet, Pseudophryne guentheri. Reprod Biol Endocrinol. 2011;9:68.
Silla AJ. Artificial fertilisation in a terrestrial toadlet (Pseudophryne guentherii): effect of medium osmolality, sperm concentration and gamete storage. Reprod Fertil Dev. 2012; https://doi.org/10.1071/RD12223.
Silla AJ. Artificial fertilisation in a terrestrial toadlet (Pseudophryne guentheri): effect of medium osmolality, sperm concentration and gamete storage. Reprod Fertil Dev. 2013;25:1134–41.
Silla AJ, Byrne PG. The role of reproductive technologies in amphibian conservation breeding programs. Annu Rev Anim Biosci. 2019;7:499–519.
Silla AJ, McFadden MS, Byrne PG. Hormone-induced sperm-release in the critically endangered Booroolong frog (Litoria booroolongensis): effects of gonadotropin-releasing hormone and human chorionic gonadotropin. Conserv Physiol. 2019;7:coy080.
Skerratt LF, Berger L, Speare R, Cashins S, McDonald KR, Phillott AD, et al. Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. Ecohealth. 2007;4:125–34.
Skerratt LF, McDonald KR, Hines HB, Berger L, Mendez D, Phillott AD, et al. Application of the survey protocol for chytridiomycosis to Queensland, Australia. Dis Aquat Organ. 2010;92:117–29.
Skinner DC, Robinson JE. Luteinising hormone secretion from the perifused ovine pars tuberalis and pars distalis: effects of gonadotropin-releasing hormone and melatonin. Neuroendocrinology. 1997;66:263–70.
Smith LD, Ecker RE, Subtelny S. In vitro induction of physiological maturation in Rana pipiens oocytes removed from their ovarian follicles. Dev Biol. 1968;17:627–43.
Sotowska-Brochocka J. The stimulatory and inhibitory role of the hypothalamus in the regulation of ovulation in grass frog, Rana temporaria. Gen Comp Endocrinol. 1988;70:83–90.
Sotowska-Brochocka J, Licht P. Effect of infundibular lesions on GnRH and LH release in the frog, Rana temporaria, during hibernation. Gen Comp Endocrinol. 1992;85:43–54.
Sotowska-Brochocka J, Martyńska L, Licht P. Dopaminergic inhibition of gonadotropic release in hibernating frogs, Rana temporaria. Gen Comp Endocrinol. 1994;93:192–6.
Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues AS, Fischman DL, et al. Status and trends of amphibian declines and extinctions worldwide. Science. 2004;306:1783–6.
Stuart SN, Hoffmann M, Chanson JS, Cox NA, Berridge RJ, Ramani P, Young BE. Threatened amphibians of the world. Barcelona, Gland, and Arlington: Lynx Edicions, IUCN, and Conservation International; 2008.
Thorgaard G, Wheeler P, Fields R. Utilization of androgenesis for strain recovery from cryopreserved sperm. In: Tiersch TR, Green CC, editors. Cryopreservation in aquatic species. 2nd ed. Sorrento: World Aquaculture Society; 2005. p. 732–7.
Toro E, Michael SF. In vitro fertilization and artificial activation of eggs of the direct-developing anuran Eleutherodactylus coqui. Reprod Biol Endocrinol. 2004;2:60.
Trudeau VL. Neuroendocrine regulation of gonadotrophin II release and gonadal growth in the goldfish, Carassius auratus. Rev Reprod. 1997;2:55–68.
Trudeau VL, Somoza GM, Natale GS, Pauli B, Wignall J, Jackman P, Doe K, Schueler FW. Hormonal induction of spawning in 4 species of frogs by coinjection with a gonadotropin-releasing hormone agonist and a dopamine antagonist. Reprod Biol Endocrinol. 2010;8:36.
Trudeau VL, Schueler FW, Navarro-Martin L, Hamilton CK, Bulaeva E, Bennett A, Fletcher W, Taylor L. Efficient induction of spawning of Northern leopard frogs (Lithobates pipiens) during and outside the natural breeding season. Reprod Biol Endocrinol. 2013;11:14.
Turani B, Aliko V, Jona D. In vitro fertilization and maturation of Balkan water frog (Pelophylax kurtmuelleri, Gayda, 1940)—a case study in reproductive amphibian biotechnology. Int J Ecosyst Ecol Sci. 2015;5:557–60.
Unger S, Mathis A, Wilkinson R. A comparison of sperm health in declining and stable populations of Hellbenders (Cryptobranchus alleganiensis alleganiensis and C.a. bishopi). Am Midl Nat. 2013;170:382–92.
Upton R, Clulow S, Mahony M, Clulow J. Generation of a sexually mature individual of the amphibian Litoria fallax from cryopreserved testicular macerates: proof of capacity of cryopreserved sperm derived offspring to complete development. Conserv Physiol. 2018a;6(1):coy043. https://doi.org/10.1093/conphys/coy043.
Upton R, Clulow S, Seeto R, Wong L, Mahony M, Clulow J. Successful sperm cryopreservation and generated offspring of the endangered frog, Litoria aurea. Cryobiology. 2018b;85:148–9.
Uteshev V, Gakhova E. Gene cryobanks for conservation of endangered amphibian species. Russ J Herpetol. 2005;12(Suppl):233–4.
Uteshev VK, Melnikova EV, Kaurova SA, Nikitin VA, Gakhova EN, Karnaukhov VN. Fluorescent analysis of cryopreserved totipotent cells of amphibian embryos. Biofizika. 2002;47:539–45.
Uteshev VK, Shishova N, Kaurova SA, Manohkin AA, Gakhova EN. Collection and cryopreservation of hormonally induced sperm of pool frog (Pelophylax lessonae). Russ J Herpetol. 2013;20(2):105–9.
Uteshev VK, Gakhova EN, Kramarova LI, Shishova NV, Kaurova SA, Browne RK. Refrigerated storage of European common frog Rana temporaria oocytes. Cryobiology. 2018;83:56–9.
Vajta G, Holm P, Kuwayama M, Booth PJ, Jacobsen H, Greve T, Callesen H. Open pulled straw (ops) vitrification: a new way to reduce cryoinjuries of bovine ova and embryos. Mol Reprod Dev. 1998;51:53–8.
Vance CK, Julien A, Counsell K, Marcec R, Agcanas L, Tucker A, Kouba A. Amphibian art over the generations: frozen sperm offspring produce viable F2 generation. Cryobiology. 2018;85:178.
Vanecek J. Inhibitory effect of melatonin on GnRH-induced LH release. Rev Reprod. 1999;4:67–72.
Vitt LJ, Caldwell JP. Herpetology: an introductory biology of amphibians and reptiles. San Diego: Academic Press; 2013.
Vu M, Trudeau VL. Neuroendocrine control of spawning in amphibians and its practical applications. Gen Comp Endocrinol. 2016;234:28–39.
Vu M, Weiler B, Trudeau VL. Time-and dose-related effects of a gonadotropin-releasing hormone agonist and dopamine antagonist on reproduction in the northern leopard frog (lithobates pipiens). Gen Comp Endocrinol. 2017;254:86–96.
Waggener WL, Carroll EJ. A method for hormonal induction of sperm release in anurans (eight species) and in vitro fertilization in Lepidobatrachus species. Dev Growth Differ. 1998;40:19–25.
Wake DB. Climate change implicated in amphibian and lizard declines. PNAS. 2007;104:8201–2.
Wake DB, Vredenburg VT. Are we in the midst of the sixth mass extinction? A view from the world of amphibians. Proc R Soc Lond Ser B Biol Sci. 2008;105:11466–73.
Wallace RA. Studies on amphibian yolk III. A resolution of yolk platelet components. Biochim Biophys Acta. 1963;74:494–504.
Wallace RA. Vitellogenesis and oocyte growth in nonmammalian vertebrates. In: Browder LW, editor. Oogenesis. Boston: Springer; 1985. p. 127–77.
Wang L, Bogerd J, Choi HS, Seong JY, Soh JM, Chun SY, Blomenröhr M, Troskie BE, Millar RP, Wen HY. Three distinct types of GnRH receptor characterized in the bullfrog. Proc Natl Acad Sci. 2001;98:361–6.
Wilczynski W, Lynch KS. Female sexual arousal in amphibians. Horm Behav. 2011;59:630–6.
Williams SE, Hoffman EA. Minimizing genetic adaptation in captive breeding programs: a review. Biol Conserv. 2009;142(11):2388–400.
Wolf DP, Hedrick JL. A molecular approach to fertilization: II. Viability and artificial fertilization of Xenopus laevis gametes. Dev Biol. 1971;25(3):348–59.
Wowk B, Leitl E, Rasch CM, Mesbah-Karimi N, Harris SB, Fahy GM. Vitrification enhancement by synthetic ice blocking agents. Cryobiology. 2000;40:228–36.
Wright P. Induction of ovulation in vitro in Rana pipiens with steroids. Gen Comp Endocrinol. 1961;1:20–3.
Yamaha E, Mizuno T, Hasebe Y, Yamazaki F. Chimeric fish produced by exchanging upper parts of blastoderms in goldfish blastulae. Fish Sci. 1997;63:514–9.
Yaron Z, Gur G, Melamed P, Rosenfeld H, Elizur A, Levavi-Sivan B. Regulation of fish gonadotropins. Int Rev Cytol. 2003;225:131–85.
Yasui GS, Fujimoto T, Sakao S, Yamaha E, Arai K. Production of loach (Misgurnus anguillicaudatus) germ-line chimera using transplantation of primordial germ cells isolated from cryopreserved blastomeres. J Anim Sci. 2011;89:2380–8.
Zhang T, Rawson DM. Feasibility studies on vitrification of intact zebrafish (Brachydanio rerio) embryos. Cryobiology. 1996;33:1–13.
Zhang RB, Werkman AS. Water and urea permeability properties of Xenopus oocytes: expression of mRNA from toad urinary bladder. Am J Physiol Cell Physiol. 1991;260:C26–34.
Zhang T, Isayeva A, Adams SL, Rawson DM. Studies on membrane permeability of zebrafish (Danio rerio) oocytes in the presence of different cryoprotectants. Cryobiology. 2005;50:285–93.
Zimkus B, Hassapakis C, Houck M. Integrating current methods for the preservation of amphibian genetic resources and viable tissues to achieve best practices for species conservation. Amphibian Reptile Conserv. 2018;12:1–27.
Zuccotti M, Piccinelli A, Marziliano N, Mascheretti S, Redi CA. Development and loss of the ability of mouse oolemma to fuse with spermatozoa. Zygote (Cambridge, England). 1994;2:333–9.
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The authors acknowledge funding support from the Australian Research Council, the University of Newcastle and WWF (JC); Australian Government Post-Graduate Awards (RU); University of Ottawa Research Chair Program, Natural Sciences and Engineering Research Council of Canada (VLT); Macquarie University Research Fellowship (SC).
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Clulow, J., Upton, R., Trudeau, V.L., Clulow, S. (2019). Amphibian Assisted Reproductive Technologies: Moving from Technology to Application. In: Comizzoli, P., Brown, J., Holt, W. (eds) Reproductive Sciences in Animal Conservation. Advances in Experimental Medicine and Biology, vol 1200. Springer, Cham. https://doi.org/10.1007/978-3-030-23633-5_14
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