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

Integrating biobanking could produce significant cost benefits and minimise inbreeding for Australian amphibian captive breeding programs

Lachlan G. Howell https://orcid.org/0000-0003-1471-1674 A B I , Peter R. Mawson C , Richard Frankham D E , John C. Rodger A B , Rose M. O. Upton https://orcid.org/0000-0002-1324-6873 A B , Ryan R. Witt A B , Natalie E. Calatayud F G , Simon Clulow https://orcid.org/0000-0002-5700-6345 H and John Clulow A B
+ Author Affiliations
- Author Affiliations

A School of Environmental and Life Sciences, University of Newcastle, Callaghan, NSW 2308, Australia.

B FAUNA Research Alliance, Kahibah, NSW 2290, Australia.

C Perth Zoo, Department of Biodiversity, Conservation and Attractions, PO Box 489, South Perth, WA 6951, Australia.

D Department of Biological Sciences, Macquarie University, Sydney, NSW 2019, Australia.

E Australian Museum, Sydney, NSW 2010, Australia.

F San Diego Zoo Institute for Conservation Research, San Pasqual Valley Road, Escondido, CA 92027, USA.

G Conservation Science Network, 24 Thomas Street, Mayfield, NSW 2304, Australia.

H Centre for Conservation Ecology and Genomics, Institute for Applied Ecology, University of Canberra, Bruce, ACT 2617, Australia.

I Corresponding author. Email: lachlan.howell@newcastle.edu.au

Reproduction, Fertility and Development 33(9) 573-587 https://doi.org/10.1071/RD21058
Submitted: 12 February 2021  Accepted: 23 March 2021   Published: 18 May 2021

Journal Compilation © CSIRO 2021 Open Access CC BY-NC

Abstract

Captive breeding is an important tool for amphibian conservation despite high economic costs and deleterious genetic effects of sustained captivity and unavoidably small colony sizes. Integration of biobanking and assisted reproductive technologies (ARTs) could provide solutions to these challenges, but is rarely used due to lack of recognition of the potential benefits and clear policy direction. Here we present compelling genetic and economic arguments to integrate biobanking and ARTs into captive breeding programs using modelled captive populations of two Australian threatened frogs, namely the orange-bellied frog Geocrinia vitellina and the white bellied frog Geocrinia alba. Back-crossing with frozen founder spermatozoa using ARTs every generation minimises rates of inbreeding and provides considerable reductions in colony size and program costs compared with conventional captive management. Biobanking could allow captive institutions to meet or exceed longstanding genetic retention targets (90% of source population heterozygosity over 100 years). We provide a broad policy direction that could make biobanking technology a practical reality across Australia’s ex situ management of amphibians in current and future holdings. Incorporating biobanking technology widely across this network could deliver outcomes by maintaining high levels of source population genetic diversity and freeing economic resources to develop ex situ programs for a greater number of threatened amphibian species.

Graphical Abstract Image

Keywords: anuran, artificial reproductive technologies, captive survival-assurance colonies, cryopreservation, frog, genome resource banking, IVF.


References

Allentoft, M., and O’Brien, J. (2010). Global amphibian declines, loss of genetic diversity and fitness: a review. Diversity (Basel) 2, 47–71.
Global amphibian declines, loss of genetic diversity and fitness: a review.Crossref | GoogleScholarGoogle Scholar |

Ananjeva, N. B., Uteshev, V. K., Orlov, N. L., Ryabov, S. A., Gakhova, E. N., Kaurova, S. A., Kramarova, L. I., Shishova, N. V., and Browne, R. K. (2017). Comparison of the modern reproductive technologies for amphibians and reptiles. Russ. J. Herpetol. 24, 275–290.
Comparison of the modern reproductive technologies for amphibians and reptiles.Crossref | GoogleScholarGoogle Scholar |

Bishop, P. J., Angulo, A., Lewis, J. P., Moore, R. D., Rabb, G. B., and Moreno, J. G. (2012). The amphibian extinction crisis – what will it take to put the action into the Amphibian Conservation Action Plan? Sapiens 5, 1406.

Bloxam, Q. M. C., and Tonge, S. J. (1995). Amphibians: suitable candidates for breeding-release programmes. Biodivers. Conserv. 4, 636–644.
Amphibians: suitable candidates for breeding-release programmes.Crossref | GoogleScholarGoogle Scholar |

Bower, D. S., Lips, K. R., Schwarzkopf, L., Georges, A., and Clulow, S. (2017). Amphibians on the brink. Science 357, 454–455.
Amphibians on the brink.Crossref | GoogleScholarGoogle Scholar | 28774916PubMed |

Browne, R. K., Silla, A. J., Upton, R., Della Togna, G., Marcec-Greaves, R., Shishova, N. V., Uteshev, V. K., Proaño, B., Pérez, O. D., and Mansour, N. (2019). Sperm collection and storage for the sustainable management of amphibian biodiversity. Theriogenology 133, 187–200.
Sperm collection and storage for the sustainable management of amphibian biodiversity.Crossref | GoogleScholarGoogle Scholar | 31155034PubMed |

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. Reprod. Fertil. Dev. 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, S., and Clulow, J. (2018). The state of cryopreservation and assisted reproductive technologies for the conservation of amphibians and reptiles. Cryobiology 85, 142.
The state of cryopreservation and assisted reproductive technologies for the conservation of amphibians and reptiles.Crossref | GoogleScholarGoogle Scholar |

Clulow, S., and Swan, M. (2018). ‘A Complete Guide to Frogs of Australia.’ (Australian Geographic: Sydney.)

Clulow, J., Trudeau, V. L., and Kouba, A. J. (2014). Amphibian declines in the twenty-first century: why we need assisted reproductive technologies. In ‘Reproductive Sciences in Animal Conservation’. (Eds W. V. Holt, J. L. Brown and P. Comizzoli.) pp. 275–316. (Springer: New York.)

Clulow, S., Gould, J., James, H., Stockwell, M., Clulow, J., and Mahony, M. (2018a). Elevated salinity blocks pathogen transmission and improves host survival from the global amphibian chytrid pandemic: Implications for translocations. J. Appl. Ecol. 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., Pomering, M., Herbert, D., Upton, R., Calatayud, N., Clulow, S., Mahony, M. J., and Trudeau, V. L. (2018b). Differential success in obtaining gametes between male and female Australian temperate frogs by hormonal induction: a review. Gen. Comp. Endocrinol. 265, 141–148.
Differential success in obtaining gametes between male and female Australian temperate frogs by hormonal induction: a review.Crossref | GoogleScholarGoogle Scholar | 29859744PubMed |

Clulow, J., Upton, R., Trudeau, V. L., and Clulow, S. (2019). Amphibian assisted reproductive technologies: moving from technology to application. In ‘Reproductive Sciences in Animal Conservation’. (Eds P. Comizzoli, J. L. Brown and W. V. Holt.) pp. 413–463. (Springer: Cham, Switzerland.)

Conde, D. A., Colchero, F., Güneralp, B., Gusset, M., Skolnik, B., Parr, M., Byers, O., Johnson, K., Young, G., and Flesness, N. (2015). Opportunities and costs for preventing vertebrate extinctions. Curr. Biol. 25, R219–R221.
Opportunities and costs for preventing vertebrate extinctions.Crossref | GoogleScholarGoogle Scholar | 25784036PubMed |

Conroy, S. D. S. (2001). Population biology and reproductive ecology of Geocrinia alba and G. vitellina, two threatened frogs from southwestern Australia. Ph.D. Thesis, University of Western Australia, Perth.

Crow, J. F., and Kimura, M. (1970). ‘An Introduction to Population Genetics Theory.’ (Harper and Rowe: New York.)

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

Driscoll, D. A. (1997). Mobility and metapopulation structure of Geocrinia alba and Geocrinia vitellina, two endangered frog species from southwestern Australia. Aust. J. Ecol. 22, 185–195.
Mobility and metapopulation structure of Geocrinia alba and Geocrinia vitellina, two endangered frog species from southwestern Australia.Crossref | GoogleScholarGoogle Scholar |

Driscoll, D. A. (1998). Genetic structure, metapopulation processes and evolution influence the conservation strategies for two endangered frog species. Biol. Conserv. 83, 43–54.
Genetic structure, metapopulation processes and evolution influence the conservation strategies for two endangered frog species.Crossref | GoogleScholarGoogle Scholar |

Driscoll, D. A. (1999). Genetic neighbourhood and effective population size for two endangered frogs. Biol. Conserv. 88, 221–229.
Genetic neighbourhood and effective population size for two endangered frogs.Crossref | GoogleScholarGoogle Scholar |

Farquharson, K. A., Hogg, C. J., and Grueber, C. E. (2017). Pedigree analysis reveals a generational decline in reproductive success of captive Tasmanian devil (Sarcophilus harrisii): implications for captive management of threatened species. J. Hered. 108, 488–495.
Pedigree analysis reveals a generational decline in reproductive success of captive Tasmanian devil (Sarcophilus harrisii): implications for captive management of threatened species.Crossref | GoogleScholarGoogle Scholar | 28379457PubMed |

Farquharson, K. A., Hogg, C. J., and Grueber, C. E. (2018). A meta-analysis of birth-origin effects on reproduction in diverse captive environments. Nat. Commun. 9, 1055.
A meta-analysis of birth-origin effects on reproduction in diverse captive environments.Crossref | GoogleScholarGoogle Scholar | 29535319PubMed |

Frankham, R. (1995). Effective population size/adult population size ratios in wildlife: a review. Genet. Res. 66, 95–107.
Effective population size/adult population size ratios in wildlife: a review.Crossref | GoogleScholarGoogle Scholar |

Frankham, R. (2008). Genetic adaptation to captivity in species conservation programs. Mol. Ecol. 17, 325–333.
Genetic adaptation to captivity in species conservation programs.Crossref | GoogleScholarGoogle Scholar | 18173504PubMed |

Frankham, R., Ballou, J. D., and Briscoe, D. A. (2010). ‘Introduction to Conservation Genetics.’ 2nd edn. (Cambridge University Press: Cambridge, UK; New York)

Frankham, R., Ballou, J. D., Ralls, K., Eldridge, M., Dudash, M. R., Fenster, C. B., Lacy, R. C., and Sunnucks, P. (2019). ‘A Practical Guide for Genetic Management of Fragmented Animal and Plant Populations.’ (Oxford University Press: Oxford.)

Gagliardo, R., Crump, P., Griffith, E., Mendelson, J., Ross, H., and Zippel, K. (2008). The principles of rapid response for amphibian conservation, using the programmes in Panama as an example. Int. Zoo Yearb. 42, 125–135.
The principles of rapid response for amphibian conservation, using the programmes in Panama as an example.Crossref | GoogleScholarGoogle Scholar |

Gillespie, G. R., Roberts, J. D., Hunter, D., Hoskin, C. J., Alford, R. A., Heard, G. W., Hines, H., Lemckert, F., Newell, D., and Scheele, B. C. (2020). Status and priority conservation actions for Australian frog species. Biol. Conserv. 247, 108543.
Status and priority conservation actions for Australian frog species.Crossref | GoogleScholarGoogle Scholar |

González-del-Pliego, P., Freckleton, R. P., Edwards, D. P., Koo, M. S., Scheffers, B. R., Pyron, R. A., and Jetz, W. (2019). Phylogenetic and trait-based prediction of extinction risk for data-deficient amphibians. Curr. Biol. 29, 1557–1563.e3.
Phylogenetic and trait-based prediction of extinction risk for data-deficient amphibians.Crossref | GoogleScholarGoogle Scholar | 31063716PubMed |

Griffiths, R. A., and Pavajeau, L. (2008). Captive breeding, reintroduction, and the conservation of amphibians. Conserv. Biol. 22, 852–861.
Captive breeding, reintroduction, and the conservation of amphibians.Crossref | GoogleScholarGoogle Scholar | 18616746PubMed |

Grueber, C. E., Reid-Wainscoat, E. E., Fox, S., Belov, K., Shier, D. M., Hogg, C. J., and Pemberton, D. (2017). Increasing generations in captivity is associated with increased vulnerability of Tasmanian devils to vehicle strike following release to the wild. Sci. Rep. 7, 2161.
Increasing generations in captivity is associated with increased vulnerability of Tasmanian devils to vehicle strike following release to the wild.Crossref | GoogleScholarGoogle Scholar | 28526824PubMed |

Harley, D., Mawson, P. R., Olds, L., McFadden, M., and Hogg, C. J. (2018). The contribution of captive breeding in zoos to the conservation of Australia’s threatened fauna. In ‘Recovering Australian Threatened Species: A Book of Hope’. (Eds S. Garnett, P. Latch, D. Lindenmayer and J. Woinarski.) pp. 281–294. (CSIRO Publishing: Melbourne.)

Hero J.-M., and Roberts D. (2004). Geocrinia alba. The IUCN Red List of Threatened Species 2004: e.T9031A1295211210.2305/IUCN.UK.2004.RLTS.T9031A12952112.EN

Hodskins L. G. (1997). Annual report on conservation and science Volume 1: conservation program reports. Bethesda, MD: American Zoo Aquarium Association.

Hoffmann, E. P., Williams, K., Hipsey, M. R., and Mitchell, N. J. (2021). Drying microclimates threaten persistence of natural and translocated populations of threatened frogs. Biodivers. Conserv. 30, 15–34.
Drying microclimates threaten persistence of natural and translocated populations of threatened frogs.Crossref | GoogleScholarGoogle Scholar |

Hogg, C. J. (2013). Preserving Australian native fauna: zoo-based breeding programs as part of a more unified strategic approach1. Aust. J. Zool. 61, 101–108.
Preserving Australian native fauna: zoo-based breeding programs as part of a more unified strategic approach1.Crossref | GoogleScholarGoogle Scholar |

Holt, W. V., Bennett, P. M., Volobouev, V., and Watwon, P. F. (1996). Genetic resource banks in wildlife conservation. J. Zool. (Lond.) 238, 531–544.
Genetic resource banks in wildlife conservation.Crossref | GoogleScholarGoogle Scholar |

Howell, L. G., and Rodger, J. C. (2018). An examination of funding for terrestrial vertebrate fauna research from Australian federal government sources. Pacific Conserv. Biol. 24, 142–147.
An examination of funding for terrestrial vertebrate fauna research from Australian federal government sources.Crossref | GoogleScholarGoogle Scholar |

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

Kouba, A. J., and Vance, C. K. (2009). Applied reproductive technologies and genetic resource banking for amphibian conservation. Reprod. Fertil. Dev. 21, 719–737.
Applied reproductive technologies and genetic resource banking for amphibian conservation.Crossref | GoogleScholarGoogle Scholar | 19567216PubMed |

Kouba, A. J., Vance, C., Calatayud, N., Rowlison, T., Langhorne, C., and Willard, S. (2012). Assisted reproductive technologies (ART) for amphibians. In ‘Amphibian Husbandry Resource Guide’. 2nd edn. (Eds V. A. Poole.) pp. 60–118. (Amphibian Taxon Advisory Group, American Association of Zoos and Aquariums: Silver Spring, MD.)

Kouba, A. J., Lloyd, R. E., Houck, M. L., Silla, A. J., Calatayud, N., Trudeau, V. L., Clulow, J., Molinia, F., Langhorne, C., and Vance, C. (2013). Emerging trends for biobanking amphibian genetic resources: the hope, reality and challenges for the next decade. Biol. Conserv. 164, 10–21.
Emerging trends for biobanking amphibian genetic resources: the hope, reality and challenges for the next decade.Crossref | GoogleScholarGoogle Scholar |

Lees, C., Mcfadden, M., and Hunter, D. (2013). Genetic management of southern corroboree frogs: workshop report and plan. IUCN SSC Conservation Breeding Specialist Group, Apple Valley, MN, USA.

Mace, G. (1986). Genetic management of small populations. Int. Zoo Yearb. 24, 167–174.
Genetic management of small populations.Crossref | GoogleScholarGoogle Scholar |

Mawson, P. R., and Lambert, C. (2017). Challenges of operating a multi-species breeding-for-release facility at Perth Zoo, Australia. Int. Zoo Yearb. 51, 165–174.
Challenges of operating a multi-species breeding-for-release facility at Perth Zoo, Australia.Crossref | GoogleScholarGoogle Scholar |

Mintzer, J. L., Kronenthal, C. J., Kelly, V., Seneca, M., Butler, G., Fecenko-Tacka, K., Altamuro, D., and Madore, S. J. (2013). Preparedness for a natural disaster: How Coriell planned for Hurricane Sandy. Biopreserv. Biobank. 11, 216–220.
Preparedness for a natural disaster: How Coriell planned for Hurricane Sandy.Crossref | GoogleScholarGoogle Scholar | 24845588PubMed |

Monfort, S. L. (2014). ‘Mayday Mayday Mayday’, the millennium ark is sinking! In ‘Reproductive Sciences in Animal Conservation’. (Eds W. V. Holt, J. L. Brown and P. Comizzoli.) pp. 15–31. (Springer: New York)

Morrin, H. R., and Robinson, B. A. (2013). Sustaining a biobank through a series of earthquake swarms: lessons learned from our New Zealand experience. Biopreserv. Biobank. 11, 211–215.
Sustaining a biobank through a series of earthquake swarms: lessons learned from our New Zealand experience.Crossref | GoogleScholarGoogle Scholar | 24845587PubMed |

Morrison, C., and Hero, J. (2003). Geographic variation in life-history characteristics of amphibians: a review. J. Anim. Ecol. 72, 270–279.
Geographic variation in life-history characteristics of amphibians: a review.Crossref | GoogleScholarGoogle Scholar |

Morrison, C. E., Johnson, R. N., Grueber, C. E., and Hogg, C. J. (2020). Genetic impacts of conservation management actions in a critically endangered parrot species. Conserv. Genet. 21, 869–877.
Genetic impacts of conservation management actions in a critically endangered parrot species.Crossref | GoogleScholarGoogle Scholar |

Murphy, J. B., and Gratwicke, B. (2017). History of captive management and conservation amphibian programs mostly in zoos and aquariums. Part I – anurans. Herpetol. Rev. 48, 241–260.

Pearl, C. A., Adams, M. J., and Leuthold, N. (2009). Breeding habitat and local population size of the Oregon spotted frog (Rana pretiosa) in Oregon, USA. Northwest. Nat. (Olymp. Wash.) 90, 136–147.
Breeding habitat and local population size of the Oregon spotted frog (Rana pretiosa) in Oregon, USA.Crossref | GoogleScholarGoogle Scholar |

Phillipsen, I. C., Bowerman, J., and Blouin, M. (2010). Effective number of breeding adults in Oregon spotted frogs (Rana pretiosa): genetic estimates at two life stages. Conserv. Genet. 11, 737–745.
Effective number of breeding adults in Oregon spotted frogs (Rana pretiosa): genetic estimates at two life stages.Crossref | GoogleScholarGoogle Scholar |

Ralls, K., Ballou, J. D., and Templeton, A. (1988). Estimates of lethal equivalents and the cost of inbreeding in mammals. Conserv. Biol. 2, 185–193.
Estimates of lethal equivalents and the cost of inbreeding in mammals.Crossref | GoogleScholarGoogle Scholar |

Robert, A. (2009). Captive breeding genetics and reintroduction success. Biol. Conserv. 142, 2915–2922.
Captive breeding genetics and reintroduction success.Crossref | GoogleScholarGoogle Scholar |

Roberts D., and Hero J.-M. (2004). Geocrinia vitellina. The IUCN Red List of Threatened Species 2004: e.T9032A1295236510.2305/IUCN.UK.2004.RLTS.T9032A12952365.EN

Roberts, D., Conroy, S., and Williams, K. (1999). Conservation status of frogs in Western Australia. In ‘Declines and Disappearances of Australian Frogs’. (Eds A. Campbell.) pp. 177–184. (Environment Australia: Canberra.)

Scheele, B. C., Skerratt, L. F., Grogan, L. F., Hunter, D. A., Clemann, N., McFadden, M., Newell, D., Hoskin, C. J., Gillespie, G. R., and Heard, G. W. (2017). After the epidemic: ongoing declines, stabilizations and recoveries in amphibians afflicted by chytridiomycosis. Biol. Conserv. 206, 37–46.
After the epidemic: ongoing declines, stabilizations and recoveries in amphibians afflicted by chytridiomycosis.Crossref | GoogleScholarGoogle Scholar |

Scheele, B. C., Pasmans, F., Skerratt, L. F., Berger, L., Martel, A., Beukema, W., Acevedo, A. A., Burrowes, P. A., Carvalho, T., and Catenazzi, A. (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 | 30923224PubMed |

Silla, A. J. (2011). Effect of priming injections of luteinizing hormone-releasing hormone on spermiation and ovulation in Gϋnther’s toadlet, Pseudophryne guentheri. Reprod. Biol. Endocrinol. 9, 68.
Effect of priming injections of luteinizing hormone-releasing hormone on spermiation and ovulation in Gϋnther’s toadlet, Pseudophryne guentheri.Crossref | GoogleScholarGoogle Scholar | 21599916PubMed |

Silla, A. J. (2013). Artificial fertilisation in a terrestrial toadlet (Pseudophryne guentheri): effect of medium osmolality, sperm concentration and gamete storage. Reprod. Fertil. Dev. 25, 1134–1141.
Artificial fertilisation in a terrestrial toadlet (Pseudophryne guentheri): effect of medium osmolality, sperm concentration and gamete storage.Crossref | GoogleScholarGoogle Scholar | 23174151PubMed |

Silla, A. J., and Byrne, P. G. (2019). The role of reproductive technologies in amphibian conservation breeding programs. Annu. Rev. Anim. Biosci. 7, 499–519.
The role of reproductive technologies in amphibian conservation breeding programs.Crossref | GoogleScholarGoogle Scholar | 30359086PubMed |

Silla, A. J., and Roberts, J. D. (2012). Investigating patterns in the spermiation response of eight Australian frogs administered human chorionic gonadotropin (hCG) and luteinizing hormone-releasing hormone (LHRHa). Gen. Comp. Endocrinol. 179, 128–136.
Investigating patterns in the spermiation response of eight Australian frogs administered human chorionic gonadotropin (hCG) and luteinizing hormone-releasing hormone (LHRHa).Crossref | GoogleScholarGoogle Scholar | 22909973PubMed |

Skerratt, L. F., Berger, L., Clemann, N., Hunter, D. A., Marantelli, G., Newell, D. A., Philips, A., McFadden, M., Hines, H. B., and Scheele, B. C. (2016). Priorities for management of chytridiomycosis in Australia: saving frogs from extinction. Wildl. Res. 43, 105–120.
Priorities for management of chytridiomycosis in Australia: saving frogs from extinction.Crossref | GoogleScholarGoogle Scholar |

Snyder, N. F. R., Derrickson, S. R., Beissinger, S. R., Wiley, J. W., Smith, T. B., Toone, W. D., and Miller, B. (1996). Limitations of captive breeding in endangered species recovery. Conserv. Biol. 10, 338–348.
Limitations of captive breeding in endangered species recovery.Crossref | GoogleScholarGoogle Scholar |

Soulé, M., Gilpin, M., Conway, W., and Foose, T. (1986). The millenium ark: how long a voyage, how many staterooms, how many passengers? Zoo Biol. 5, 101–113.
The millenium ark: how long a voyage, how many staterooms, how many passengers?Crossref | GoogleScholarGoogle Scholar |

Wardell-Johnson, G., Roberts, J. D., Driscoll, D., and Williams, K. (1995). Orange-bellied and white-bellied frogs recovery plan, 2nd edition. Department of Conservation and Land Management, Perth, WA, Australia.

Wintle, B. A., Cadenhead, N. C. R., Morgain, R. A., Legge, S. M., Bekessy, S. A., Cantele, M., Possingham, H. P., Watson, J. E. M., Maron, M., and Keith, D. A. (2019). Spending to save: what will it cost to halt Australia’s extinction crisis? Conserv. Lett. 12, e12682.
Spending to save: what will it cost to halt Australia’s extinction crisis?Crossref | GoogleScholarGoogle Scholar |

Woinarski, J. C. Z., Garnett, S. T., Legge, S. M., and Lindenmayer, D. B. (2017). The contribution of policy, law, management, research, and advocacy failings to the recent extinctions of three Australian vertebrate species. Conserv. Biol. 31, 13–23.
The contribution of policy, law, management, research, and advocacy failings to the recent extinctions of three Australian vertebrate species.Crossref | GoogleScholarGoogle Scholar |

WWF (2020). Australia’s 2019–2020 bushfires: the wildlife toll. Interim report. Available at: https://www.wwf.org.au/what-we-do/bushfire-recovery/in-depth/resources/australia-s-2019-2020-bushfires-the-wildlife-toll#gs.wfuly6

Zippel, K., Johnson, K., Gagliardo, R., Gibson, R., McFadden, M., Browne, R., Martinez, C., and Townsend, E. (2011). The Amphibian Ark: a global community for ex situ conservation of amphibians. Herpetol. Conserv. Biol. 6, 340–352.