Victor K. UTESHEV,Edith N. GAKHOVA,Ludmila I. KRAMAROVA,et al.Russian Collaborative Development of Reproduction Technologies for the Sustainable Management of Amphibian Biodiversity[J].Asian Herpetological Research(AHR),2023,14(1):103-115.[doi:10.16373/j.cnki.ahr.220043]
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Russian Collaborative Development of Reproduction Technologies for the Sustainable Management of Amphibian Biodiversity
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Asian Herpetological Research[ISSN:2095-0357/CN:51-1735/Q]

Issue:
2023 VoI.14 No.1
Page:
103-115
Research Field:
Publishing date:
2023-03-27

Info

Title:
Russian Collaborative Development of Reproduction Technologies for the Sustainable Management of Amphibian Biodiversity
Author(s):
Victor K. UTESHEV1 Edith N. GAKHOVA1 Ludmila I. KRAMAROVA2 Natalia V. SHISHOVA1 Svetlana A. KAUROVA1 Elena A. KIDOVA3 Artem A. KIDOV3 and Robert K. BROWNE4*
1 Institute of Cell Biophysics, Russian Academy of Sciences, Pushchino, Moscow 142290, Russia
2 Institute of Theoretical and Experimental Biophysics, Russian Academy of Sciences, Pushchino, Moscow 142290, Russia
3 Russian State Agrarian University - K. A. Timiryazev Agricultural Academy, Moscow 127550, Russia
4 Sustainability America, La Isla Road, Corozal District, Belize
Keywords:
artificial fertilisation assisted reproductive technologies (ART) cryopreservation gonadotropic hormones oocytes spermatozoa storage urinary spermatozoa
PACS:
-
DOI:
10.16373/j.cnki.ahr.220043
Abstract:
Reproduction technologies (RTs) can provide for the reliable reproduction of amphibians, as well as perpetuation of species genetic variation with the use of biobanks. In 1982, in anticipation of the biodiversity conservation crisis, major Russian institutions collaborated in a dynamic program to develop and implement RTs for the sustainable management of amphibian biodiversity. An initial primary focus was the captive breeding of threatened Russian endemic anuran and caudate species, using RTs that varied from environmental manipulation to the use of exogenous gonadotropic hormones to stimulate reproduction. These species were mostly from Palearctic or cool mountain regions, but also included a wide range of species from warm regions. Other early achievements included the successful cryopreservation of anuran spermatozoa and anuran diploid pluripotent cell nuclei, in order to store both the matrilineal and patrilineal genomes in biobanks, with their subsequent development to the blastula stage after implantation into enucleated oocytes. After the turn of the 21st Century, in support of the priorities of the Amphibian Conservation Action Plan (2007), we developed RTs for the refrigerated storage of testicular or urinary spermatozoa for days to weeks at 4°C, the cryopreservation of urinary spermatozoa using a novel cryoprotectant, the in vitro fertilisation of hormonally induced oocytes either fresh or after refrigerated ex situ or in situ storage, and the artificial insemination of salamanders with fresh spermatozoa. In this article, we describe previously unpublished techniques and techniques from obscure Russian sources.

References:

Ananjeva N. B., Uteshev V. K., Orlov N. L., Gakhova E. N. 2015. Strategies for conservation of endangered amphibian and reptile species. Biol Bull, 42: 432–439 (In Russian)
Ananjeva N. B., Uteshev V. K., Orlov N. L., Ryabov S. A., Gakhova E. N., Kaurova S. A., Kramarova L. I., Shishova N. V., Browne R. K. 2017. Comparison of the modern reproductive technologies for amphibians and reptiles. Russ J Herpetol, 24: 275–290 (In Russian)
Arakelyan M. S., Danielyan F. D., Corti C., Sindaco R., Leviton A. E. 2011. The Herpetofauna of Armenia and Nagorno-Karabakh. S: Contributions to Herpetology, 27. Salt Lake City: Society for the Study of Amphibians and Reptiles, 181 pp
Arregui L., Bóveda P., Gosálveza J., Kouba A. J. 2020. Effect of seasonality on hormonally induced sperm in Epidalea calamita (Amphibia, Anura, Bufonidae) and its refrigerated and cryopreserved storage. Aquaculture. 529: e735677
Arregui L., Kouba A. J., Germano J. M., Barrios L., Moore M., Kouba C. K. 2021. Fertilization potential of cold-stored Fowler’s toad (Anaxyrus fowleri) spermatozoa: temporal changes in sperm motility based on temperature and osmolality. Reprod Fert Devel, 34: 461–469
AZA. 2010. Amphibian Conservation. Highlights and Accomplishments. Association of Zoos and Aquariums
Blitz I. L., Fish M. B., Cho K. W. Y. 2016. Leapfrogging: primordial germ cell transplantation permits recovery of CRISPR/Cas9-induced mutations in essential genes. Development, 143: 2868–2875
Bolton R. L., Mooney A., Pettit M. T., Bolton A. E., Morgan L., Drake G. J., Appeltant R., Walker S. L., Gillis J. D., Hvilsom C. 2022. Resurrecting biodiversity: Advanced assisted reproductive technologies and biobanking. Reprod Fert, 3(3):121–146
Browne R. K., Clulow J., Mahony M., Clark A. 1998. Successful recovery of motility and fertility of cryopreserved cane toad (Bufo marinus) sperm. Cryobiology, 37: 339–345
Browne R. K., Clulow J., Mahony M. 2001. Short-term storage of cane toad (Bufo marinus) gametes. Reproduction, 2001: 121:167e73
Browne R. K., Clulow J., Manony M. 2002. The short-term storage and cryopreservation of spermatozoa from hylid and myobatrachid frogs. Cryo Letters, 23: 129–136
Browne R. K., Janzen P., Bagaturov M. F., van Houte D. K. 2018. Amphibian keeper conservation breeding programs. J Zoo Res, 2: 29–46
Browne R. K., Silla A. J., Upton R., Della-Togna G., Marcec-Greaves R., Shishova N. V., Uteshev V. K., Proano B., Perez, O. D., Mansour N., Kaurova S. A., Gakhova E. N., Cosson J., Dzyuba B., Kramarova L. I., McGinnity D., Gonzalez M., Clulow J., Clulow S. 2019. Sperm collection and storage for the sustainable management of amphibian biodiversity. Theriogenology, 133: 187–200
Browne R. K., 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). Review. Sustainability America, Belize
Browne R. K., Kaurova S. A., Vasudevan K., McGinnity D., Venu, G., Gonzalez M. F., Uteshev V. K., Marcec-Greaves R. 2022. Targeting and development of reproduction technologies for the sustainable management of Caudata (salamanders) and Gymnophiona (caecilians). Reprod Fertil Dev, 34: 479–497
Burger I., Julien A. R., Kouba A. J., Barber, D., Counsell K. R., Pacheco C., Krebs J., Kouba C. K. 2021. Linking in-situ and ex-situ populations of threatened amphibians through genome banking. Conserv Sci Practice, 3(11): e525
Campbell L. C., Anderson K., Marcec-Greaves R. 2021. Topical application of hormone gonadotropin‐releasing hormone (GnRH‐A) stimulates reproduction in the endangered Texas blind salamander (Eurycea rathbuni). Conserv Sci Practice, 4(3): e609
Clulow J., Pomering M., Herbert D., Upton R., Calatayud N., Clulow S., Mahony M. J., Trudeau V.L. 2018. Differential success in obtaining gametes between male and female Australian temperate frogs by hormonal induction: A review. Gen Comp Physiol, 265: 141–148
Clulow J., Upton R., Trudeau V. L., Clulow S. 2019. Amphibian assisted reproductive technologies: moving from technology to application. Adv Exp Med Biol, 1200: 413–463
Clulow J., Upton R., Clulow S. 2022. Cryopreservation of amphibian genomes: targeting the Holy Grail, cryopreservation of maternal- haploid and embryonic-diploid genomes. 147-165. In Heatwole H., Kouba A., Silla A. (Eds.). Reproductive Technologies and Biobanking for the Conservation of Amphibians. Australia: CSIRO Publishing
Della Tonga, G. 2015. Structural and Functional Characterization of the Panamanian Golden Frog (Atelopus zeteki) Spermatozoa—Impact of Medium Osmolality and Cryopreservation on Motility and Cell Viability. PhD dissertation submitted to the Faculty of the Graduate School of the University of Maryland, College Park, USA
Edwards D. L., Mahony M. J., Clulow J. 2004. Effect of sperm concentration, medium osmolality and oocyte storage on artificial fertilisation success in a myobatrachid frog (Limnodynastes tasmaniensis). Reprod Fertil Dev, 16: 347–354
Elinson, R. P. 1975 Site of sperm entry and a cortical contraction associated with egg activation in the frog Rana pipiens. Devel Biol. 47: 257–268
Gakhova E. N. 1998. Genetic cryobanks for conservation of biodiversity. The development and current status of this problem in Russia. Cryo Letters Suppl., 1: 57–64
Gascon C., Collins J. P., Moore R. D., Church D. R., McKay J. E., Mendelson J. R. III (Eds). 2007. Amphibian Conservation Action Plan. Gland, UK: IUCN/SSC Amphibian Specialist Group, Switzerland and Cambridge, 64pp
Goncharov B. F., Shubravy O. I., Serbinova I. A., Uteshev V. K. 1989. The USSR programme for breeding amphibians, including rare and endangered species. Int Zoo Yearbook, 28: 10–21
González-del-Pliego P., Freckleton R. P., Edwards D. P., Koo M. S., Scheffers B. R., Pyron R. A., Jetz W. 2019. Phylogenetic and trait-based prediction of extinction risk for data-deficient amphibians. Current Biol, 29: 1557–1563
Gosalvez J., Holt W V., Johnston S. D. 2014. Sperm DNA fragmentation and its role in wildlife conservation. Adv Exp Med Biol, 2014; 753: 357–384
Guy, E. L., Gillisa, A. B., Kouba, A. J., Barber D, Poole V, Marcec-Greaves RM, Kouba CK. 2020. Sperm collection and cryopreservation for threatened newt species. Cryobiology, 94: 80–88
Higaki S., Kawakami Y., Eto Y., Yamaha E., Nagano M., Katagiri S., Takada T., Takahashi Y. 2013. Cryopreservation of zebrafish (Danio rerio) primordial germ cells by vitrification of yolk-intact and yolk-depleted embryos using various cryoprotectant solutions. Cryobiology, 67: 374–382
Iliashenko V. Y., Iliashenko E. I. 2000. Krasnaya kniga Rossii: Pravovye akty [Red Data Book of Russia: Legislative acts]. Moscow: State committee of the Russian Federation for Environmental Protection (In Russian)
IUCN. 2021. International Union for the Conservation of Nature. https://www.iucnredlist.org
Jeuthe H., Palaiokostas C., Johannisson A. 2022. DNA fragmentation and membrane integrity in sperm of farmed Arctic charr (Salvelinus alpinus). Aquaculture, 547: e737537
Kaurova S. A., Chekurova N. R., Melnikova E. V., Uteshev V. K., Gakhova E. N. 1996. Cryopreservation of frog Rana temporaria sperm without loss of fertilizing capacity. In Gakhova E. N., Karnaukhov V. N. (Eds.), Proceedings of the 14th Working Meeting, Pushchino, 13–15 May 1996, Pushchino: Pushchino Press, 106–108 (In Russian)
Kaurova S. A., Uteshev V. K., Chekurova N. R., Gakhova E. N. 1997. Cryopreservation of testis of frog Rana temporaria. Infusionsther Transfusionsmed, 24: 379
Kaurova S. A., Vrublevskaya V. V., Uteshev V.K., Dolgacheva L.P., Gakhova E.N. 1998a. Activity of NADH- and ɑ-glycerophosphate-dehydrogenases of frog Rana temporaria spermatozoa during the process of cryopreservation. In Gakhova E. N., Karnaukhov V. N. (Eds.), Proceedings of the 15th Working Meeting, Pushchino, 13–15 October 1998, Pushchino: Pushchino Press, 79–83 (In Russian)
Kaurova S. A., Nikitina L. A., Uteshev V. K., Gakhova E. N. 1998b. Cryopreservation of totipotent embryo cells and their use in reconstruction of enucleated eggs. In Gakhova E. N., Karnaukhov V. N. (Eds.), Proceedings of the 15th Working Meeting, Pushchino, 13–15 October 1998, Pushchino: Pushchino Press, pp. 206–208 (In Russian)
Kaurova S. A., Uteshev V. K., Gapeyev A. B., Shishova N. V., Gakhova E. N., Browne R. K., Kramarova L. I. 2021. Cryopreservation of spermatozoa obtained postmortem from the European common frog Rana temporaria. Reprod Fert Dev, 33: 10.1071/RD20336
Kaurova S. A., Browne R. K., Uteshev V. K. 2022. Antibiotics for the refrigerated storage at 4°C of hormonally induced European сommon frog (Rana temporaria) spermatozoa. Theriogenology Wild, 1: e100009
Kidov A. A., Serbinova I. A. 2008. Experience of cultivation of Caucasian toad, Bufo verrucosissimus (Pallas, 1814) (Amphibia: Anura: Bufonidae) in laboratory conditions. In Chopikashvili L. V., Cherchesova S. K. (Eds.), Present Problems of Ecology and Conservation of Biodiversity. Vladikavkaz: North Ossetian State University, 49–53 (In Russian)
Kidov A. A., Matushkina K. A., Afrin K. A., Blinova S. A., Timoshina A. L., Kovrina E. G. 2014a. Captive breeding of Caucasian common toads (Bufo eichwaldi and B. verrucosissimus) without hormonal stimulations. Current Stud Herpetol, 14: 19–26 (In Russian)
Kidov A. A., Matushkina K. A., Uteshev V. K., Timoshina A. L., Kovrina, E. G. 2014b. The first captive breeding of the Eichwald’s toad (Bufo eichwaldi). Russ J Herpetol, 21: 40–46
Kidov A. A., Matushkina K. A. 2015. Female fertility of the Caucasian toad, Bufo verrucosissimus (Pallas, 1814) in artificial conditions. Vestnik Buryat State Univer, S4: 75–80 (In Russian)
Kidov A. A., Matushkina K. A., Blinova S. A., Afrin K. A., Kovrina E. G., Baksheyeva, A. A. 2015a. Reproduction of the Iranian long-legged frog (Rana macrocnemis pseudodalmatina Eiselt et Schmidtler, 1971) in laboratory conditions. Current Stud Herpetol, 15: 109–113 (In Russian)
Kidov A. A., Matushkina K. A., Afrin, K. A. 2015b. The first results of captive breeding and reintroduction of the Karelin’s newt, Triturus karelinii Strauch, 1870 from Talysh population. Vestnik Buryat State Univer, S4: 81–89 (In Russian)
Kidov A. A., Matushkina K. A., Litvinchuk S. N., Blinova S. A., Afrin K. A., Kovrina, E. G. 2016. The first case of reproduction of the Lataste’s toad, Bufotes latastii (Boulenger, 1882) in laboratory conditions. Current Stud Herpetol, 16: 20–26 (In Russian)
Kidov A. A., Matushkina K. A., Blinova S. A., Afrin K. A. 2017. Laboratory reproduction of the Cuban toad, Peltophryne empusa Cope, 1862. Curr Stud Herpetol, 17: 36–43
Kidov A. A., Nemyko E. A. 2018. Captive breeding of the Caucasian smooth newt, Lissotriton lantzi (Wolterstorff, 1914) (Salamandridae, Amphibia). Curr Studies Herpetol, 18: 125–134 (In Russian)
Kidov A. A., Nemyko, E. A. 2019. Captive breeding of the alpine newt, Ichthyosaura alpestris (Laurenti, 1768) (Amphibia, Caudata, Salamndridae) under hormonal stimulation. Curr Stud Herpetol, 19: 31–39 (In Russian)
Kidov A. A., Shimanskaya E. A., Askenderov A. D., Nemyko E. A. 2019. The use of hormonal stimulation for reproduction of the Karelin’s newt, Triturus karelinii in laboratory conditions. University proceedings. Volga region. Natur Sci, 4: 50–60 (In Russian)
Langhorne C. J. 2016. Developing Assisted Reproductive Technologies for Endangered North American Amphibians. Theses and Dissertations, 1373
Mansour N., Lahnsteiner F., and Patzner R. A. 2011. Collection of gametes from live axolotl, Ambystoma mexicanum, and standardization of in vitro fertilization. Theriogenology, 75: 354–361
Marcec R. M. 2016. Development of assisted reproductive technologies for endangered North American salamanders by Ruth Marie Marcec. Theses. Faculty of Mississippi State University, Degree of Doctor of Philosophy in Animal Physiology, Department of Biochemistry, Molecular Biology, Entomology, and Plant Pathology, Mississippi State, Mississippi, USA
Matushkina K. A., Kidov A. A., Litvinchuk S. N. 2017. The first results of captive breeding of the Batura toad, Bufotes baturae Stoeck, Schmid, Steinleinet Grosse, 1999. Tambov Univer Reports. Series: Natur Technic Sci, 22: 955–959 (In Russian)
Matushkina K. A., Kidov A. A., Litvinchuk S. N. 2020. Keeping, breeding and maintenance of zooculture of the Ladakh toad, Bufotes latastii (Boulenger, 1882). Russ J Herpetol, 27: 284–290
Mazanaeva L. F., Kidov A. A., Dzhamirzoev G. S., Askenderov A. D., Nemyko E. A., Shimanskaya E. A. 2019. The program for reintroduction of the Karelin’s newt, Triturus karelinii in the south of Daghestan. University proceedings. Volga region Natur Sci, 1: 102–112 (In Russian)
Melnikova E. V., Uteshev V. K., Pashovkin T. N., Sokolova A. A., Yashin V. N., Karnaukhov V. N., Gakhova E.N. 2005. Changes in the permeability of amphibian embryo envelope for fluorochromes under the action of ultrasound. Biophysics, 50: 441–444
Nemyko E. A., Vyatkin, Ya. A., Kidov A. A. 2019. Growing of larvae of the Caucasian smooth newt, Lissotriton lantzi (Wolterstorff, 1914) (Amphibia, Caudata) at various temperatures. Curr Stud Herpetol, 19: 125–131 (In Russian)
Nikitina L. A. 1996. Nuclear heterotransplantation in fish and amphibians. Russ J Dev Biol, 5: 267–280 (In Russian)
Nikitina L. A. 1997. Nuclear transplantation in fish and amphibians. Physiol Gen Biol Rev, 13: 35–72
Pollock, K. 2016. Amphibian sperm DNA fragmentation. MPhil Thesis, School of Agriculture and Food Sciences, The University of Queensland
Poo S., Hinkson K. M. 2019. Applying cryopreservation to anuran conservation biology. Conserv Scien Pract, 2019;1:e91.
Rivera-Pacheco J., Herrera-Barragan J., Leon-Galvan M., Ocampo-Cervantes J., Perez-Rivero J., Gual-Sill F. 2021. Ambystoma mexicanum sperm cryopreservation (Shaw & Nodder, 1798). Abanico Veterinario, 11
Rocha L. A., Aleixo A., Allen G., Almeda F., Baldwin C. C., Barclay M. V. L., Bates J. M., Bauer A. M., Benzoni F., Berns C. M., Berumen M. L., Blackburn D. C. et al. (123 authors). 2014. Specimen collection: An essential tool. Science, 344(6186): 814-815
Rowson A. D., Obringer A. R., Roth T. L. 2001. Non-invasive treatments of lutenizing hormone-releasing hormone for inducing spermiation in American (Bufo americanus) and Gulf coast (Bufo valliceps) toads. Zoo Biol, 20: 63–74
Rugh R. 1962. Induced breeding. In Experimental Embryology. Techniques and Procedures. Minneapolis: Burgess Publishing Co., pp. 91–103
Serbinova I. A., Tuniyev B. S. 1986. Keeping, captive breeding and reintroduction of northern banded newt (Triturus vittatus). In Sokolov V. E., Syroechkovskiy E. E. (Eds.), First all-Union Meeting on Problems of Zooculture, 2–4 December 1986, Moscow. Moscow, Russ: Academy of Sciences of the USSR, 147–150 (In Russian)
Serbinova I. A., Shubravy O. I., Uteshev V. K., Agasian A. L., Goncharov B. F. 1990a. Keeping, captive breeding and creation of new populations of eastern spadefoot (Pelobates syriacus Boettger). In Syroechkovskiy E. E., Salomatina N. I. (Eds.), Zooculture of Amphibians. Moscow, Russ: A. N. Severtsov Institute of Evolutionary Morphology and Ecology of Animals, 82–89 (In Russian)
Serbinova I. A., Tuniyev B. S., Uteshev V. K., Shubravy O. I., Goncharov B. F. 1990b. Creation of the population of northern banded newt (Triturus vittatus ophryticus) in artificial conditions. In Syroechkovskiy E. E., Salomatina N. I. (Eds.), Zooculture of Amphibians. Moscow, Russ: A. N. Severtsov Institute of Evolutionary Morphology and Ecology of Animals, 75–81 (In Russian)
Serbinova I. A. 2007. Reintroduction as a method of wild amphibian conservation. Sci Res Zoo Parks, 22: 113–117 (In Russian)
Shishova N. V., Uteshev V. K., Kaurova S. A., Browne R. K., Gakhova E. N. 2011. Cryopreservation of hormonally induced sperm for the conservation of threatened amphibians with Rana temporaria as a model research species. Theriogenology, 75: 220–232
Shishova N. V., Uteshev V. K., Sirota N. P., Kuznetsova E. A., Kaurova S. A., Browne R. K., Gakhova E. N. 2013. The quality and fertility of sperm collected from European common frog (Rana temporaria) carcasses refrigerated for up to 7 days. Zoo Biol, 32: 400–406
Silla A. J., McFadden M., and Byrne P.G. 2019. Hormone-induced sperm-release in the critically endangered Booroolong frog (Litoria booroolongensis): effects of gonadotropin-releasing hormone and human chorionic gonadotropin. Conserv Physiol, 7(1): coy080
Tuniyev B. S., Tuniyev S. B. 2006. Rare species of amphibians and reptiles of the Sochi National Park. In Tuniyev B. S. (Ed.), Inventory of major taxonomic groups and communities, zoological research of the Sochi national Park – first results of the first national park in Russia. Moscow, Russ: Prestige Press, 205–225 (In Russian)
Tuniyev B. S., Ostrovskikh S. V. 2017. The Karelin’s newt Triturus karelinii (Strauch, 1870). In Zamotaylov A. S. (Ed.), Red Data Book of Krasnodar Krai. Krasnodar, Russ: Center for information and economic development of the press, television and radio of the Krasnodar, 478–479 (In Russian)
Upton R., Clulow S., Calatayud N. E., Colyvas K., Seeto R. G. Y., Wong L. A. M., Mahony M. J., Clulow J. 2021. Generation of reproductively mature offspring from the endangered green and golden bell frog Litoria aurea using cryopreserved spermatozoa. Reprod Fertil Develop, 33: 562–572.
Uteshev V. K., Melnikova E. V., Kaurova S. A., Nikitin V. A., Gakhova E. N., Karnaukhov, V. N. 2002. Fluorescent analysis of cryopreserved totipotent cells of amphibian embryos. Biophysics, 47: 539–545
Uteshev V. K., Shishova N. V., Kaurova S. A., Browne R. K., Gakhova E. N. 2012. Hormonal induction of spermatozoa from amphibians with Rana temporaria and Bufo bufo as anuran models. Reprod Fertil Dev, 24: 599–607
Uteshev V. K., Shishova N. V., Kaurova, S. A., Manokhin A. A., Gakhova E. N. 2013a. Collection and cryopreservation of hormonally induced sperm of pool frog (Pelophylax lessonae). Russ J Herpetol, 20: 105–109
Uteshev V. K., Kidov A. A., Kaurova S. A., Shishova N. V., Melnikova E.V., Kovaliov, A.V. 2013b. Comparative characteristics of the urinal sperm of three species of Palearctic brown frogs. Tambov Univer Reports Series: Natur Technic Sci, 18: 3087–3089 (In Russian)
Uteshev V. K., Kidov A. A., Kaurova S. A., Shishova N. V., Melnikova E. V. 2013c. First experience of reproduction of a Karelin’s newt Ttriturus karelinii (Strauch, 1870) with urinal sperm use for eggs fertilization. Tambov Univer Reports Series: Natur Technic Sci, 18: 3090–3092 (In Russian)
Uteshev V. K., Kaurova S. A., Shishova N. V., Stolyarov S. D., Browne R. K., Gakhova, E. N. 2015a. In vitro fertilization with hormonally induced sperm and eggs from sharp-ribbed newt Pleurodeles waltl. Russ J Herpetol, 22: 35–40
Uteshev V. K., Kaurova S. A., Shishova N. V., Kramarova L. I., Browne R. K., Gakhova, E. N. 2015b. Current reproductive and cryopreservation technologies in herpetology. Russ J Herpetol, 22: 143–144
Uteshev V. K., Gakhova E. N., Kramarova L. I., Shishova N. V., Kaurova S. A., Browne R. K. 2018. Refrigerated storage of European common frog Rana temporaria oocytes. Cryobiology, 83: 56–59
Uteshev V. K., Gakhova E. N., Kramarova L. I., Shishova N. V., Kaurova S. A., Browne R. K. 2019a. Cryobanking of amphibian genetic recourses in Russia: past and future. Russ J Herpetol, 26: 319–324
Uteshev V. K., Gakhova E. N., Kramarova L. I., Shishova N. V., Kaurova S. A. 2019b. New approaches to collecting reproductive material from amphibians for its use in artificial fertilization. Current Studies Herpetol, 19: 46–55 (In Russian)
Veprintsev B. N., Rott N. N. 1979. Conserving genetic resources of animal species. Nature, 280: 633–634

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Last Update: 2023-03-25