Common goals, different stages: the state of the ARTs for reptile and amphibian conservation
Simon Clulow A , John Clulow B , Ruth Marcec-Greaves C , Gina Della Togna D E and Natalie E. Calatayud F G A *
+ Author Affiliations
- Author Affiliations
A Centre for Conservation Ecology & Genomics, Institute for Applied Ecology, University of Canberra, Bruce, ACT 2617, Australia.
B University of Newcastle, Conservation Biology Research Group, University Drive, Callaghan, NSW 2308, Australia.
C Honduras Amphibian Rescue and Conservation Center, Honduras.
D Universidad Interamericana de Panama, Direccion de Investigacion, Campus Central, Avenida Ricardo J. Alfaro, Panama City, Panama.
E Smithsonian Tropical Research Institute, Panama Amphibian Rescue and Conservation Project, Panama.
F San Diego Zoo Wildlife Alliance, Beckman Center for Conservation Research, 15600 San Pasqual valley Road, Escondido, CA 92025, USA.
G Conservation Science Network, 24 Thomas Street, Mayfield, NSW 2304, Australia.
Reproduction, Fertility and Development 34(5) i-ix https://doi.org/10.1071/RDv34n5_FO
Published online: 11 March 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Amphibians and reptiles are highly threatened vertebrate taxa with large numbers of species threatened with extinction. With so many species at risk, conservation requires the efficient and cost-effective application of all the tools available so that as many species as possible are assisted. Biobanking of genetic material in genetic resource banks (GRBs) in combination with assisted reproductive technologies (ARTs) to retrieve live animals from stored materials are two powerful, complementary tools in the conservation toolbox for arresting and reversing biodiversity decline for both amphibians and reptiles. However, the degree of development of the ARTs and cryopreservation technologies differ markedly between these two groups. These differences are explained in part by different perceptions of the taxa, but also to differing reproductive anatomy and biology between the amphibians and reptiles. Artificial fertilisation with cryopreserved sperm is becoming a more widely developed and utilised technology for amphibians. However, in contrast, artificial insemination with production of live progeny has been reported in few reptiles, and while sperm have been successfully cryopreserved, there are still no reports of the production of live offspring generated from cryopreserved sperm. In both amphibians and reptiles, a focus on sperm cryopreservation and artificial fertilisation or artificial insemination has been at the expense of the development and application of more advanced technologies such as cryopreservation of the female germline and embryonic genome, or the use of sophisticated stem cell/primordial germ cell cryopreservation and transplantation approaches. This review accompanies the publication of ten papers on amphibians and twelve papers on reptiles reporting advances in ARTs and biobanking for the herpetological taxa.
Keywords: assisted reproduction, biobanking, biodiversity, cryopreservation, gametes, genome resource banks, herpetofauna, IVF.
References
Arregui, L, Kouba, AJ, Germano, JM, Barrios, L, Moore, M, Kouba, CK, and Clulow, J (2022a). Fertilization potential of cold-stored Fowler’s toad (Anaxyrus fowleri) spermatozoa: temporal changes in sperm motility based on temperature and osmolality. Reproduction, Fertility and Development 34, 461–469.| Fertilization potential of cold-stored Fowler’s toad (Anaxyrus fowleri) spermatozoa: temporal changes in sperm motility based on temperature and osmolality.Crossref | GoogleScholarGoogle Scholar |
Arregui, L, Martinez-Pastor, F, Arroyo, F, and Gosálvez, J (2022b). Determining the effects of sperm activation in anuran cloaca on motility and DNA integrity in Epidalea calamita (Bufonidae). Reproduction, Fertility and Development 34, 438–446.
| Determining the effects of sperm activation in anuran cloaca on motility and DNA integrity in Epidalea calamita (Bufonidae).Crossref | GoogleScholarGoogle Scholar |
Berger, L, Speare, R, Daszak, P, Green, DE, Cunningham, AA, Goggin, CL, Slocombe, R, Ragan, MA, Hyatt, AD, McDonald, KR, Hines, HB, Lips, KR, Marantelli, G, and Parkes, H (1998). Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proceedings of the National Academy of Sciences of the United States of America 95, 9031–9036.
| Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America.Crossref | GoogleScholarGoogle Scholar |
Böhm, M, Collen, B, Baillie, JEM, et al. (2013). The conservation status of the world’s reptiles. Biological Conservation 157, 372–385.
| The conservation status of the world’s reptiles.Crossref | GoogleScholarGoogle Scholar |
Bower, DS, Lips, KR, Schwarzkopf, L, Georges, A, and Clulow, S (2017). Amphibians on the brink. Science 357, 454–455.
| Amphibians on the brink.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.
| Successful recovery of motility and fertility of cryopreserved cane toad (Bufo marinus) sperm.Crossref | GoogleScholarGoogle Scholar |
Browne, R, Li, H, Robertson, H, Uteshev, V, Shishova, N, McGinnity, D, Nofs, S, Figiel, C, Mansour, N, Lloyd, R, Agnew, D, Carleton, C, Wu, M, and Gakhova, E (2011). Reptile and amphibian conservation through gene banking and other reproduction technologies. Russian Journal of Herpetology 18, 165–174.
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, Dyzuba, 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 |
Burger, I, Julien, AR, Kouba, AJ, Barber, D, Counsell, KR, Pacheco, C, Krebs, J, and Kouba, CK (2021). Linking in-situ and ex-situ populations of threatened amphibians through genome banking. Conservation Science and Practice 3, e525.
| Linking in-situ and ex-situ populations of threatened amphibians through genome banking.Crossref | GoogleScholarGoogle Scholar |
Campbell, L, Cafe, SL, Upton, R, Doody, JS, Nixon, B, Clulow, J, and Clulow, S (2020). A model protocol for the cryopreservation and recovery of motile lizard sperm using the phosphodiesterase inhibitor caffeine. Conservation Physiology 8, coaa044.
| A model protocol for the cryopreservation and recovery of motile lizard sperm using the phosphodiesterase inhibitor caffeine.Crossref | GoogleScholarGoogle Scholar |
Campbell, L, Clulow, J, Doody, JS, and Clulow, S (2021a). Optimal cooling rates for sperm cryopreservation in a threatened lizard conform to two-factor hypothesis of cryo-injury. Cryobiology 103, 101–106.
| Optimal cooling rates for sperm cryopreservation in a threatened lizard conform to two-factor hypothesis of cryo-injury.Crossref | GoogleScholarGoogle Scholar |
Campbell, L, Clulow, J, Howe, B, Upton, R, Doody, S, and Clulow, S (2021b). Efficacy of short-term cold storage prior to cryopreservation of spermatozoa in a threatened lizard. Reproduction, Fertility and Development 33, 555–561.
| Efficacy of short-term cold storage prior to cryopreservation of spermatozoa in a threatened lizard.Crossref | GoogleScholarGoogle Scholar |
Chen, Q, and Holt, WV (2021). Extracellular vesicles in the male reproductive tract of the softshell turtle. Reproduction, Fertility and Development 33, 519–529.
| Extracellular vesicles in the male reproductive tract of the softshell turtle.Crossref | GoogleScholarGoogle Scholar |
Chiari, Y, Cahais, V, Galtier, N, and Delsuc, F (2012). Phylogenomic analyses support the position of turtles as the sister group of birds and crocodiles (Archosauria). BMC Biology 10, 65.
| Phylogenomic analyses support the position of turtles as the sister group of birds and crocodiles (Archosauria).Crossref | GoogleScholarGoogle Scholar |
Clulow, J, and Clulow, S (2016). Cryopreservation and other assisted reproductive technologies for the conservation of threatened amphibians and reptiles: bringing the ARTs up to speed. Reproduction, Fertility and Development 28, 1116–1132.
| Cryopreservation and other assisted reproductive technologies for the conservation of threatened amphibians and reptiles: bringing the ARTs up to speed.Crossref | GoogleScholarGoogle Scholar |
Clulow J, Mahony M, Browne R, Pomering M, Clark A (1999) Applications of assisted reproductive technologies (ART) to endangered anuran amphibians. In ‘Declines and disappearances of Australian frogs’. (Ed. A Campbell) pp. 219–225. (Environment Australia: Canberra)
Clulow, J, Clulow, S, Guo, J, French, AJ, Mahony, MJ, and Archer, M (2012). Optimisation of an oviposition protocol employing human chorionic and pregnant mare serum gonadotropins in the Barred Frog Mixophyes fasciolatus (Myobatrachidae). Reproductive Biology and Endocrinology 10, 60.
| Optimisation of an oviposition protocol employing human chorionic and pregnant mare serum gonadotropins in the Barred Frog Mixophyes fasciolatus (Myobatrachidae).Crossref | GoogleScholarGoogle Scholar |
Clulow J, Trudeau VL, Kouba AJ (2014) Amphibian declines in the twenty-first century: why we need assisted reproductive technologies. In ‘Reproductive sciences in animal conservation.’ (Eds WV Holt, JL Brown, P Comizzoli) pp. 275–316. (Springer: New York)
Clulow, J, Pomering, M, Herbert, D, Upton, R, Calatayud, N, Clulow, S, Mahony, MJ, and Trudeau, VL (2018a). 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 |
Clulow, S, Gould, J, James, H, Stockwell, M, Clulow, J, and Mahony, M (2018b). Elevated salinity blocks pathogen transmission and improves host survival from the global amphibian chytrid pandemic: implications for translocations. Journal of Applied Ecology 55, 830–840.
| Elevated salinity blocks pathogen transmission and improves host survival from the global amphibian chytrid pandemic: implications for translocations.Crossref | GoogleScholarGoogle Scholar |
Clulow J, Upton R, Trudeau VL, Clulow S (2019) Amphibian assisted reproductive technologies: moving from technology to application. In ‘Reproductive sciences in animal conservation’. 2nd edn. (Eds P Comizzoli, JL Brown, WV Holt) pp. 413–463. (Springer: Cham)
Clulow J, Upton R, Clulow S (2022) Cryopreservation of amphibian genomes: targeting the Holy Grail, cryopreservation of maternal-haploid and embryonic-diploid genomes. In ‘Reproductive technologies and biobanking as tools for the conservation of amphibians’. (Eds AJ Silla, AJ Kouba, H Heatwole) (CSIRO Publishing: Melbourne)
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 |
Doody, JS, Burghardt, GM, and Dinets, V (2013). Breaking the social–non-social dichotomy: a role for reptiles in vertebrate social behavior research? Ethology 119, 95–103.
| Breaking the social–non-social dichotomy: a role for reptiles in vertebrate social behavior research?Crossref | GoogleScholarGoogle Scholar |
Doody, JS, Soanes, R, Castellano, CM, Rhind, D, Green, B, McHenry, C, and Clulow, S (2015). Invasive toads shift predator–prey densities in animal communities by removing top predators. Ecology 96, 2544–2554.
| Invasive toads shift predator–prey densities in animal communities by removing top predators.Crossref | GoogleScholarGoogle Scholar |
Doody, JS, Rhind, D, Green, B, Castellano, C, McHenry, C, and Clulow, S (2017). Chronic effects of an invasive species on an animal community. Ecology 98, 2093–2101.
| Chronic effects of an invasive species on an animal community.Crossref | GoogleScholarGoogle Scholar |
Doody JS, Dinets V, Burghardt GM (2021a) ‘The secret social lives of reptiles.’ (JHU Press: Baltimore)
Doody, JS, Soennichsen, KF, James, H, McHenry, C, and Clulow, S (2021b). Ecosystem engineering by deep-nesting monitor lizards. Ecology 102, e03271.
| Ecosystem engineering by deep-nesting monitor lizards.Crossref | GoogleScholarGoogle Scholar |
Folch, J, Cocero, MJ, Chesné, P, Alabart, JL, Domínguez, V, Cognié, Y, Roche, A, Fernández-Arias, A, Martí, JI, Sánchez, P, Echegoyen, E, Beckers, JF, Sánchez Bonastre, A, and Vignon, X (2009). First birth of an animal from an extinct subspecies (Capra pyrenaica pyrenaica) by cloning. Theriogenology 71, 1026–1034.
| First birth of an animal from an extinct subspecies (Capra pyrenaica pyrenaica) by cloning.Crossref | GoogleScholarGoogle Scholar |
Gardner, MG, Pearson, SK, Johnston, GR, and Schwarz, MP (2016). Group living in squamate reptiles: a review of evidence for stable aggregations. Biological Reviews 91, 925–936.
| Group living in squamate reptiles: a review of evidence for stable aggregations.Crossref | GoogleScholarGoogle Scholar |
Germano, JM, Cree, A, Molinia, F, Arregui, L, and Bishop, PJ (2022). Hormone treatment does not reliably induce spermiation or mating in Hamilton’s frog from the archaic leiopelmatid lineage. Reproduction, Fertility and Development 34, 447–452.
| Hormone treatment does not reliably induce spermiation or mating in Hamilton’s frog from the archaic leiopelmatid lineage.Crossref | GoogleScholarGoogle Scholar |
González-del-Pliego, P, Freckleton, RP, Edwards, DP, Koo, MS, Scheffers, BR, Pyron, RA, and Jetz, W (2019). Phylogenetic and trait-based prediction of extinction risk for data-deficient amphibians. Current Biology 29, 1557–1563.e3.
| Phylogenetic and trait-based prediction of extinction risk for data-deficient amphibians.Crossref | GoogleScholarGoogle Scholar |
Grigg G, Kirshner D (2015) ‘Biology and evolution of crocodylians’. (CSIRO Publishing: Clayton)
Hagedorn M, Kleinhans F (2000) Problems and prospects in cryopreservation of fish embryos. In ‘Cryopreservation in aquatic species’. (Eds T Tiersch, C Green) pp. 161–178. (The World Aquaculture Society: Baton Rouge)
Hagedorn, M, Peterson, A, Mazur, P, and Kleinhans, F (2004). High ice nucleation temperature of zebrafish embryos: slow-freezing is not an option. Cryobiology 49, 181–189.
| High ice nucleation temperature of zebrafish embryos: slow-freezing is not an option.Crossref | GoogleScholarGoogle Scholar |
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 |
Higaki, S, Kawakami, Y, Eto, Y, Yamaha, E, Nagano, M, Katagiri, S, Takada, T, and 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.
| Cryopreservation of zebrafish (Danio rerio) primordial germ cells by vitrification of yolk-intact and yolk-depleted embryos using various cryoprotectant solutions.Crossref | GoogleScholarGoogle Scholar |
Hildebrandt, TB, Hermes, R, Goeritz, F, Appeltant, R, Colleoni, S, de Mori, B, Diecke, S, Drukker, M, Galli, C, Hayashi, K, Lazzari, G, Loi, P, Payne, J, Renfree, M, Seet, S, Stejskal, J, Swegen, A, Williams, SA, Zainuddin, ZZ, and Holtze, S (2021). The ART of bringing extinction to a freeze – History and future of species conservation, exemplified by rhinos. Theriogenology 169, 76–88.
| The ART of bringing extinction to a freeze – History and future of species conservation, exemplified by rhinos.Crossref | GoogleScholarGoogle Scholar |
Hobbs, RJ, Upton, R, Keogh, L, James, K, Baxter-Gilbert, J, and Whiting, MJ (2022). Sperm cryopreservation in an Australian skink (Eulamprus quoyii). Reproduction, Fertility and Development 34, 428–437.
| Sperm cryopreservation in an Australian skink (Eulamprus quoyii).Crossref | GoogleScholarGoogle Scholar |
Holt, WV, and Comizzoli, P (2021). Opportunities and limitations for reproductive science in species conservation. Annual Review of Animal Biosciences 10, 5.1–5.21.
| Opportunities and limitations for reproductive science in species conservation.Crossref | GoogleScholarGoogle Scholar |
Holt W, Abaigar T, Watson P, Wildt D (2003) Genetic resource banks for species conservation. In ‘Reproductive science and integrated conservation’. Vol. 8. (Eds W Holt, A Pickard, J Rodger, D Wildt) pp. 267–280. (Cambridge University Press: Cambridge)
Howard, JG, Lynch, C, Santymire, RM, Marinari, PE, and Wildt, DE (2016). Recovery of gene diversity using long-term cryopreserved spermatozoa and artificial insemination in the endangered black-footed ferret. Animal Conservation 19, 102–111.
| Recovery of gene diversity using long-term cryopreserved spermatozoa and artificial insemination in the endangered black-footed ferret.Crossref | GoogleScholarGoogle Scholar |
Howell, LG, Frankham, R, Rodger, JC, Witt, RR, Clulow, S, Upton, RMO, and Clulow, J (2021a). 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 |
Howell, LG, Mawson, PR, Frankham, R, Rodger, JC, Upton, RMO, Witt, RR, Calatayud, NE, Clulow, S, and Clulow, J (2021b). Integrating biobanking could produce significant cost benefits and minimise inbreeding for Australian amphibian captive breeding programs. Reproduction, Fertility and Development 33, 573–587.
| Integrating biobanking could produce significant cost benefits and minimise inbreeding for Australian amphibian captive breeding programs.Crossref | GoogleScholarGoogle Scholar |
Jacobs, LE, Hammond, TT, Gaffney, PM, Curtis, MJ, Shier, DM, Durrant, BS, Righton, A, Williams, CL, and Calatayud, NE (2021). Using reproductive technologies to assess the development of secondary sexual characteristics, ovarian senescence and hermaphroditism in the endangered mountain yellow-legged frog Rana muscosa. Reproduction, Fertility and Development 33, 610–614.
| Using reproductive technologies to assess the development of secondary sexual characteristics, ovarian senescence and hermaphroditism in the endangered mountain yellow-legged frog Rana muscosa.Crossref | GoogleScholarGoogle Scholar |
Johnson K, Mendelson JR (2022) Status of global amphibian declines and the prioritisation of species for captive breeding. In ‘Reproductive technologies and biobanking as tools for the conservation of amphibians’. (Eds AJ Silla, AJ Kouba, H Heatwole). (CSIRO Publishing: Melbourne)
Johnston, SD, Lever, J, McLeod, R, Qualischefski, E, Brabazon, S, Walton, S, and Collins, SN (2014). Extension, osmotic tolerance and cryopreservation of saltwater crocodile (Crocodylus porosus) spermatozoa. Aquaculture 426–427, 213–221.
| Extension, osmotic tolerance and cryopreservation of saltwater crocodile (Crocodylus porosus) spermatozoa.Crossref | GoogleScholarGoogle Scholar |
Johnston, SD, Qualischefski, E, Cooper, J, McLeod, R, Lever, J, Nixon, B, Anderson, AL, Hobbs, R, Gosálvez, J, López-Fernández, C, and Keeley, T (2017). Cryopreservation of saltwater crocodile (Crocodylus porosus) spermatozoa. Reproduction, Fertility and Development 29, 2235–2244.
| Cryopreservation of saltwater crocodile (Crocodylus porosus) spermatozoa.Crossref | GoogleScholarGoogle Scholar |
Johnston, SD, Lever, J, McLeod, R, Qualischefski, E, Madrigal-Valverde, M, and Nixon, B (2021). Assisted breeding technology in the saltwater crocodile Crocodylus porosus: a review and look to the future. Reproduction, Fertility and Development 33, 503–518.
| Assisted breeding technology in the saltwater crocodile Crocodylus porosus: a review and look to the future.Crossref | GoogleScholarGoogle Scholar |
Jørgensen, D (2013). Reintroduction and de-extinction. BioScience 63, 719–720.
| Reintroduction and de-extinction.Crossref | GoogleScholarGoogle Scholar |
Kaurova, SA, Uteshev, VK, Gapeyev, AB, Shishova, NV, Gakhova, EN, Browne, RK, and Kramarova, LI (2021). Cryopreservation of spermatozoa obtained postmortem from the European common frog Rana temporaria. Reproduction, Fertility and Development 33, 588–595.
| Cryopreservation of spermatozoa obtained postmortem from the European common frog Rana temporaria.Crossref | GoogleScholarGoogle Scholar |
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 |
Khosla, K, Zhan, L, Bhati, A, Carley-Clopton, A, Hagedorn, M, and Bischof, J (2019). Characterization of laser gold nanowarming: a platform for millimeter-scale cryopreservation. Langmuir 35, 7364–7375.
| Characterization of laser gold nanowarming: a platform for millimeter-scale cryopreservation.Crossref | GoogleScholarGoogle Scholar |
Khosla, K, Kangas, J, Liu, Y, Zhan, L, Daly, J, Hagedorn, M, and Bischof, J (2020). Cryopreservation and laser nanowarming of zebrafish embryos followed by hatching and spawning. Advanced Biosystems 4, 2000138.
| Cryopreservation and laser nanowarming of zebrafish embryos followed by hatching and spawning.Crossref | GoogleScholarGoogle Scholar |
Kouba AJ (2022) Genome Resource Banks as a tool for amphibian conservation. In ‘Reproductive technologies and biobanking as tools for the conservation of amphibians’. (Eds AJ Silla, AJ Kouba, H Heatwole). (CSIRO Publishing: Melbourne)
Kouba, AJ, Langhorne, CJ, Willard, ST, Smith, T, and Kouba, CK (2022). Spermiation response to exogenous hormone therapy in hibernated and non-hibernated boreal toads (Anaxyrus boreas boreas). Reproduction, Fertility and Development 34, 453–460.
| Spermiation response to exogenous hormone therapy in hibernated and non-hibernated boreal toads (Anaxyrus boreas boreas).Crossref | GoogleScholarGoogle Scholar |
Lamar, SK, Nelson, NJ, Moore, JA, Taylor, HR, Keall, SN, and Ormsby, DK (2021). Initial collection, characterization, and storage of tuatara (Sphenodon punctatus) sperm offers insight into their unique reproductive system. PLoS ONE 16, e0253628.
| Initial collection, characterization, and storage of tuatara (Sphenodon punctatus) sperm offers insight into their unique reproductive system.Crossref | GoogleScholarGoogle Scholar |
Larsen, RE, Cardeilhac, PT, and Lane, T (1984). Semen extenders for artificial insemination in the American alligator. Aquaculture 42, 141–149.
| Semen extenders for artificial insemination in the American alligator.Crossref | GoogleScholarGoogle Scholar |
Lawson, B, Clulow, S, Mahony, MJ, and Clulow, J (2013). Towards gene banking amphibian maternal germ lines: short-term incubation, cryoprotectant tolerance and cryopreservation of embryonic cells of the frog, Limnodynastes peronii. PLoS ONE 8, e60760.
| Towards gene banking amphibian maternal germ lines: short-term incubation, cryoprotectant tolerance and cryopreservation of embryonic cells of the frog, Limnodynastes peronii.Crossref | GoogleScholarGoogle Scholar |
Lin, S, Long, W, Chen, J, and Hopkins, N (1992). Production of germ-line chimeras in zebrafish by cell transplants from genetically pigmented to albino embryos. Proceedings of the National Academy of Sciences of the United States of America 89, 4519–4523.
| Production of germ-line chimeras in zebrafish by cell transplants from genetically pigmented to albino embryos.Crossref | GoogleScholarGoogle Scholar |
Madsen, T, Loman, J, Anderberg, L, Anderberg, H, Georges, A, and Ujvari, B (2020). Genetic rescue restores long-term viability of an isolated population of adders (Vipera berus). Current Biology 30, R1297–R1299.
| Genetic rescue restores long-term viability of an isolated population of adders (Vipera berus).Crossref | GoogleScholarGoogle Scholar |
Marinović, Z, Li, Q, Lujić, J, Iwasaki, Y, Csenki, Z, Urbányi, B, Horváth, Á, and Yoshizaki, G (2018). Testis cryopreservation and spermatogonia transplantation as a tool for zebrafish line reconstitution. Cryobiology 85, 145–146.
| Testis cryopreservation and spermatogonia transplantation as a tool for zebrafish line reconstitution.Crossref | GoogleScholarGoogle Scholar |
Marinović, Z, Li, Q, Lujić, J, Iwasaki, Y, Csenki, Z, Urbányi, B, Yoshizaki, G, and Horváth, Á (2019). Preservation of zebrafish genetic resources through testis cryopreservation and spermatogonia transplantation. Scientific Reports 9, 13861.
| Preservation of zebrafish genetic resources through testis cryopreservation and spermatogonia transplantation.Crossref | GoogleScholarGoogle Scholar |
McGinnity, D, Reinsch, SD, Schwartz, H, Trudeau, V, and Browne, RK (2022). Semen and oocyte collection, sperm cryopreservation and IVF with the threatened North American giant salamander Cryptobranchus alleganiensis. Reproduction, Fertility and Development 34, 470–477.
| Semen and oocyte collection, sperm cryopreservation and IVF with the threatened North American giant salamander Cryptobranchus alleganiensis.Crossref | GoogleScholarGoogle Scholar |
Mengden G, Platz C, Hubbard R, Quinn H (1980) Semen collection freezing and artificial insemination in snake. In ‘Contributions to herpetology. No. 1. Reproductive biology and diseases of captive reptiles’. (Eds JB Murphy, JT Collins) pp. 71–78. (Society for the Study of Reptiles: St Louis)
Miller, RR, Beranek, F, Anderson, AL, Johnston, SD, and Nixon, B (2021). Plasma and acrosomal membrane lipid content of saltwater crocodile spermatozoa. Reproduction, Fertility and Development 33, 596–604.
| Plasma and acrosomal membrane lipid content of saltwater crocodile spermatozoa.Crossref | GoogleScholarGoogle Scholar |
Nixon, B, Anderson, AL, Bromfield, EG, Martin, JH, Cafe, SL, Skerrett-Byrne, DA, Dun, MD, Eamens, AL, De Iuliis, GN, and Johnston, SD (2021a). Post-testicular sperm maturation in the saltwater crocodile Crocodylus porosus: assessing the temporal acquisition of sperm motility. Reproduction, Fertility and Development 33, 530–539.
| Post-testicular sperm maturation in the saltwater crocodile Crocodylus porosus: assessing the temporal acquisition of sperm motility.Crossref | GoogleScholarGoogle Scholar |
Nixon, B, Anderson, AL, Bromfield, EG, Martin, JH, Lord, T, Cafe, SL, Roman, SD, Skerrett-Byrne, DA, Eamens, AL, De Iuliis, GN, and Johnston, SD (2021b). Gross and microanatomy of the male reproductive duct system of the saltwater crocodile Crocodylus porosus. Reproduction, Fertility and Development 33, 540–554.
| Gross and microanatomy of the male reproductive duct system of the saltwater crocodile Crocodylus porosus.Crossref | GoogleScholarGoogle Scholar |
Oliveri, M, Bartoskova, A, Spadola, F, Morici, M, di Giuseppe, M, and Knotek, Z (2018). Method of semen collection and artificial insemination in snakes. Journal of Exotic Pet Medicine 27, 75–80.
| Method of semen collection and artificial insemination in snakes.Crossref | GoogleScholarGoogle Scholar |
Perry, SM, and Mitchell, MA (2022). Reptile assisted reproductive technologies: can ART help conserve 300 million years of evolution by preserving extant reptile biodiversity? Reproduction, Fertility and Development 34, 385–400.
| Reptile assisted reproductive technologies: can ART help conserve 300 million years of evolution by preserving extant reptile biodiversity?Crossref | GoogleScholarGoogle Scholar |
Perry, SM, Park, T, and Mitchell, MA (2022). Sex, drugs and rock iguanas: testicular dynamics and plasma testosterone concentrations could predict optimal semen collection times in Cyclura. Reproduction, Fertility and Development 34, 417–427.
| Sex, drugs and rock iguanas: testicular dynamics and plasma testosterone concentrations could predict optimal semen collection times in Cyclura.Crossref | GoogleScholarGoogle Scholar |
Platz C, Mengden G, Quinn H, Wood F, Wood J (1980) Semen collection, evaluation and freezing in the green sea turtle, Galapagos tortoise, and red-eared pond turtle. In ‘Proceedings of the American Association of Zoo Veterinarians, Arlington’. pp. 47–48. (American Association of Zoo Veterinarians)
Pukazhenthi, BS, and Wildt, DE (2004). Which reproductive technologies are most relevant to studying, managing and conserving wildlife? Reproduction, Fertility and Development 16, 33–46.
| Which reproductive technologies are most relevant to studying, managing and conserving wildlife?Crossref | GoogleScholarGoogle Scholar |
Pukazhenthi, B, Comizzoli, P, Travis, AJ, and Wildt, DE (2006). Applications of emerging technologies to the study and conservation of threatened and endangered species. Reproduction, Fertility and Development 18, 77–90.
| Applications of emerging technologies to the study and conservation of threatened and endangered species.Crossref | GoogleScholarGoogle Scholar |
Rhodin, AGJ, Stanford, CB, Van Dijk, PP, et al. (2018). Global conservation status of turtles and tortoises (order Testudines). Chelonian Conservation and Biology 17, 135–161.
| Global conservation status of turtles and tortoises (order Testudines).Crossref | GoogleScholarGoogle Scholar |
Rodger, JC, and Clulow, J (2021). Resetting the paradigm of reproductive science and conservation. Animal Reproduction Science , .
| Resetting the paradigm of reproductive science and conservation.Crossref | GoogleScholarGoogle Scholar |
Ryder, OA, and Onuma, M (2018). Viable cell culture banking for biodiversity characterization and conservation. Annual Review of Animal Biosciences 6, 83–98.
| Viable cell culture banking for biodiversity characterization and conservation.Crossref | GoogleScholarGoogle Scholar |
Sandfoss, MR, Whittington, OM, Reichling, S, and Roberts, BM (2021). Toxicity of cryoprotective agents to semen from two closely related snake species: the endangered Louisiana pinesnake (Pituophis ruthveni) and bullsnake (Pituophis cantenifer). Cryobiology 101, 20–27.
| Toxicity of cryoprotective agents to semen from two closely related snake species: the endangered Louisiana pinesnake (Pituophis ruthveni) and bullsnake (Pituophis cantenifer).Crossref | GoogleScholarGoogle Scholar |
Sandler, RL, Moses, L, and Wisely, SM (2021). An ethical analysis of cloning for genetic rescue: case study of the black-footed ferret. Biological Conservation 257, 109118.
| An ethical analysis of cloning for genetic rescue: case study of the black-footed ferret.Crossref | GoogleScholarGoogle Scholar |
Sandmaier, SES, Shepard, T, Reeves, A, Bohr, K, Krebs, J, and Herrick, JR (2022). Characterisation of sperm production and morphology in the male Philippine crocodile Crocodylus mindorensis via voluntary behavioural training. Reproduction, Fertility and Development 34, 410–416.
| Characterisation of sperm production and morphology in the male Philippine crocodile Crocodylus mindorensis via voluntary behavioural training.Crossref | GoogleScholarGoogle Scholar |
Scheele, BC, Pasmans, F, Skerratt, LF, et al. (2019). Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity. Science 363, 1459–1463.
| Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity.Crossref | GoogleScholarGoogle Scholar |
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 |
Silla, AJ, and Byrne, PG (2021). Hormone-induced ovulation and artificial fertilisation in four terrestrial-breeding anurans. Reproduction, Fertility and Development 33, 615–618.
| Hormone-induced ovulation and artificial fertilisation in four terrestrial-breeding anurans.Crossref | GoogleScholarGoogle Scholar |
Silla AJ, Kouba AJ (2022) Integrating reproductive technologies into the conservation toolbox for the recovery of amphibian species. In ‘Reproductive technologies and biobanking as tools for the conservation of amphibians’. (Eds AJ Silla, AJ Kouba, H Heatwole). (CSIRO Publishing: Melbourne)
Silla AJ, Kouba AJ, Heatwole H (2022) ‘Reproductive technologies and biobanking as tools for the conservation of amphibians’. (CSIRO Publishing: Melbourne)
Stuart, SN, Chanson, JS, Cox, NA, Young, BE, Rodrigues, ASL, Fischman, DL, and Waller, RW (2004). Status and trends of amphibian declines and extinctions worldwide. Science 306, 1783–1786.
| Status and trends of amphibian declines and extinctions worldwide.Crossref | GoogleScholarGoogle Scholar |
Upton, R, Clulow, S, Mahony, MJ, and Clulow, J (2018). Generation of a sexually mature individual of the Eastern dwarf tree frog, Litoria fallax, from cryopreserved testicular macerates: proof of capacity of cryopreserved sperm derived offspring to complete development. Conservation Physiology 6, coy043.
| Generation of a sexually mature individual of the Eastern dwarf tree frog, Litoria fallax, from cryopreserved testicular macerates: proof of capacity of cryopreserved sperm derived offspring to complete development.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 |
Van Dyke, JU, Thompson, MB, Burridge, CP, et al. (2021). Australian lizards are outstanding models for reproductive biology research. Australian Journal of Zoology 68, 168–199.
| Australian lizards are outstanding models for reproductive biology research.Crossref | GoogleScholarGoogle Scholar |
Walker, AD (1972). New light on the origin of birds and crocodiles. Nature 237, 257–263.
| New light on the origin of birds and crocodiles.Crossref | GoogleScholarGoogle Scholar |
Whetstone, KN, and Martin, LD (1979). New look at the origin of birds and crocodiles. Nature 279, 234–236.
| New look at the origin of birds and crocodiles.Crossref | GoogleScholarGoogle Scholar |
Whitfield Gibbons, JW, Scott, DE, Ryan, TJ, Buhlmann, TD, Metts, BS, Greene, JL, Mills, T, Leiden, Y, Poppy, S, and Winne, CT (2000). The global decline of reptiles, déjà vu amphibians. BioScience 50, 653–666.
Wildt, DE, Schiewe, MC, Schmidt, PM, Goodrowe, KL, Howard, JG, Phillips, LG, O’brien, SJ, and Bush, M (1986). Developing animal model systems for embryo technologies in rare and endangered wildlife. Theriogenology 25, 33–51.
| Developing animal model systems for embryo technologies in rare and endangered wildlife.Crossref | GoogleScholarGoogle Scholar |
Young, C, Ravida, N, Curtis, M, Mazzotti, F, and Durrant, B (2017). Development of a sperm cryopreservation protocol for the Argentine black and white tegu (Tupinambis merianae). Theriogenology 87, 55–63.
| Development of a sperm cryopreservation protocol for the Argentine black and white tegu (Tupinambis merianae).Crossref | GoogleScholarGoogle Scholar |
Young, C, Ravida, N, and Durrant, B (2021). Challenges in the development of sperm cryopreservation protocols for snakes. Reproduction, Fertility and Development 33, 605–609.
| Challenges in the development of sperm cryopreservation protocols for snakes.Crossref | GoogleScholarGoogle Scholar |
Young, C, Ravida, N, Rochford, M, Mazzotti, F, Curtis, M, and Durrant, B (2022). Sperm cryopreservation in the Burmese python Python bivittatus as a model for endangered snakes. Reproduction, Fertility and Development 34, 401–409.
| Sperm cryopreservation in the Burmese python Python bivittatus as a model for endangered snakes.Crossref | GoogleScholarGoogle Scholar |
