Register      Login
Wildlife Research Wildlife Research Society
Ecology, management and conservation in natural and modified habitats
RESEARCH ARTICLE

Monitoring post-release survival of the northern corroboree frog, Pseudophryne pengilleyi, using environmental DNA

Jack Rojahn https://orcid.org/0000-0001-9878-5878 A B , Dianne Gleeson A and Elise M. Furlan A
+ Author Affiliations
- Author Affiliations

A Institute for Applied Ecology, The University of Canberra, Bruce, ACT 2617, Australia.

B Corresponding author. Email: Jack.rojahn@canberra.edu.au

Wildlife Research 45(7) 620-626 https://doi.org/10.1071/WR17179
Submitted: 8 December 2017  Accepted: 20 September 2018   Published: 19 November 2018

Abstract

Context: Translocations are becoming an increasingly important conservation tool to combat rising levels of species extinction. Unfortunately, many translocation efforts fail; yet, the timing and cause of failure often remain unknown. Monitoring individuals in the days and weeks following release can provide valuable information on their capacity to survive this initial hurdle. In Australia, breeding programs have been established for the endangered northern corroboree frog, Pseudophryne pengilleyi, to enable reintroduction to the wild via captive-reared individuals, typically, early life stages such as eggs or juvenile frogs that cannot be monitored via traditional survey methods that target adult frogs (e.g. shout–response). Environmental DNA (eDNA) detects trace amounts of DNA that organisms release into their environment and could provide a means to infer population persistence for wildlife releases and translocations.

Aims: In the present study, we aim to develop an eDNA assay capable of detecting both sexes of P. pengilleyi across multiple life stages, and use it to monitor their survival.

Methods: An eDNA assay was developed to target the two corroboree frog species (P. pengilleyi and P. corroboree, the southern corroboree frog) and was tested for its sensitivity and specificity in silico and in vitro. Pseudophryne pengilleyi eggs were released into three naturally occurring ponds and water samples were, subsequently, collected from each pond on several occasions over a period of 78 days. Quantitative polymerase chain reaction was used to detect P. pengilleyi eDNA from water samples.

Key Results: The developed assay was shown to be sensitive and specific to corroboree frogs. eDNA monitoring of reintroduced P. pengilleyi detected the species’ DNA at three of three release ponds and DNA remained detectable until at least 78 days post-release at two of three ponds.

Conclusions: We show how the development of a corroboree frog-specific assay allowed us to monitor the post-release survival of P. pengilleyi in naturally occurring pools.

Implications: eDNA surveys may provide a useful tool to monitor post-release survival of translocated populations in a non-invasive manner, with the potential to identify the timing and causes of failure. Such knowledge can be used to inform the management of translocated populations and future release strategies.

Additional keywords: detection, eDNA, Australian Capital Territory, Pseudophryne corroboree, translocation.


References

Alberts, A. C. (2007). Behavioral considerations of headstarting as a conservation strategy for endangered rock iguanas. Applied Animal Behaviour Science 102, 380–391.
Behavioral considerations of headstarting as a conservation strategy for endangered rock iguanas.Crossref | GoogleScholarGoogle Scholar |

Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology 215, 403–410.
Basic local alignment search tool.Crossref | GoogleScholarGoogle Scholar |

Australian Government (2010). Survey Guidelines for Australia’s Threatened Frogs. (Department of the Environment, Water, Heritage and the Arts: Canberra, ACT.) Available at http://www.environment.gov.au/system/files/resources/ff3eb752-482d-417f-8971-f93a84211518/ files/survey-guidelines-frogs.pdf [accessed 30 October 2018]

Barnes, M. A., Turner, C. R., Jerde, C. L., Renshaw, M. A., Chadderton, W. L., and Lodge, D. M. (2014). Environmental conditions influence eDNA persistence in aquatic systems. Environmental Science & Technology 48, 1819–1827.
Environmental conditions influence eDNA persistence in aquatic systems.Crossref | GoogleScholarGoogle Scholar |

Beck, B. B., Rapaport, L. G., Stanley Price, M. R., and Wilson, A. C. (1994). Reintroduction of captive-born animals. In ‘Creative Conservation: Interactive Management of Wild and Captive Animals’. (Eds P. J. S. Olney, G. M. Mace, and A. T. C. Feistner.) pp. 265–286. (Chapman & Hall: London.)

Benson, D. A., Karsch-Mizrachi, I., Lipman, D. J., Ostell, J., and Sayers, E. W. (2009). GenBank. Nucleic Acids Research 37, D26–D31.
GenBank.Crossref | GoogleScholarGoogle Scholar |

Biggs, J., Ewald, N., Valentini, A., Gaboriaud, C., Dejean, T., Griffiths, R. A., Foster, J., Wilkinson, J. W., Arnell, A., Brotherton, P., Williams, P., and Dunn, F. (2015). Using eDNA to develop a national citizen science-based monitoring programme for the great crested newt (Triturus cristatus). Biological Conservation 183, 19–28.
Using eDNA to develop a national citizen science-based monitoring programme for the great crested newt (Triturus cristatus).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 |

Cawthorn, D.-M., Steinman, H. A., and Witthuhn, R. C. (2011). Comparative study of different methods for the extraction of DNA from fish species commercially available in South Africa. Food Control 22, 231–244.
Comparative study of different methods for the extraction of DNA from fish species commercially available in South Africa.Crossref | GoogleScholarGoogle Scholar |

Deiner, K., Fronhofer, E. A., Mächler, E., Walser, J.-C., and Altermatt, F. (2016). Environmental DNA reveals that rivers are conveyer belts of biodiversity information. Nature Communications 7, 12544.
Environmental DNA reveals that rivers are conveyer belts of biodiversity information.Crossref | GoogleScholarGoogle Scholar |

Dejean, T., Valentini, A., Duparc, A., Pellier-Cuit, S., Pompanon, F., Taberlet, P., and Miaud, C. (2011). Persistence of environmental DNA in freshwater ecosystems. PLoS One 6, e23398.
Persistence of environmental DNA in freshwater ecosystems.Crossref | GoogleScholarGoogle Scholar |

Dejean, T., Valentini, A., Miquel, C., Taberlet, P., Bellemain, E., and Miaud, C. (2012). Improved detection of an alien invasive species through environmental DNA barcoding: the example of the American bullfrog Lithobates catesbeianus. Journal of Applied Ecology 49, 953–959.
Improved detection of an alien invasive species through environmental DNA barcoding: the example of the American bullfrog Lithobates catesbeianus.Crossref | GoogleScholarGoogle Scholar |

Dickens, M. J., Delehanty, D. J., and Michael Romero, L. (2010). Stress: an inevitable component of animal translocation. Biological Conservation 143, 1329–1341.
Stress: an inevitable component of animal translocation.Crossref | GoogleScholarGoogle Scholar |

Donnellan, S., Mahony, M., and Bertozzi, T. (2012). A new species of Pseudophryne (Anura: Myobatrachidae) from the central Australian ranges. Zootaxa 2012, 69–85.

Ficetola, G. F., Miaud, C., Pompanon, F., and Taberlet, P. (2008). Species detection using environmental DNA from water samples. Biology Letters 4, 423–425.
Species detection using environmental DNA from water samples.Crossref | GoogleScholarGoogle Scholar |

Fischer, J., and Lindenmayer, D. B. (2000). An assessment of the published results of animal relocations. Biological Conservation 96, 1–11.
An assessment of the published results of animal relocations.Crossref | GoogleScholarGoogle Scholar |

Furlan, E. M., and Gleeson, D. M. (2016). Environmental DNA detection of redfin perch, Perca fluviatilis. Conservation Genetics Resources 8, 115–118.
Environmental DNA detection of redfin perch, Perca fluviatilis.Crossref | GoogleScholarGoogle Scholar |

Furlan, E. M., Gleeson, D. M., Hardy, C. M., and Duncan, R. P. (2016). A framework for estimating the sensitivity of eDNA surveys. Molecular Ecology Resources 16, 641–654.
A framework for estimating the sensitivity of eDNA surveys.Crossref | GoogleScholarGoogle Scholar |

Genet, K. S., and Sargent, L. G. (2003). Evaluation of methods and data quality from a volunteer-based amphibian call survey. Wildlife Society Bulletin 31, 703–714.

Germano, J. M., and Bishop, P. J. (2009). Suitability of amphibians and reptiles for translocation. Conservation Biology 23, 7–15.
Suitability of amphibians and reptiles for translocation.Crossref | GoogleScholarGoogle Scholar |

Gillespie, G., Hunter, D., Berger, L., and Marantelli, G. (2015). Rapid decline and extinction of a montane frog population in southern Australia follows detection of the amphibian pathogen Batrachochytrium dendrobatidis. Animal Conservation 18, 295–302.
Rapid decline and extinction of a montane frog population in southern Australia follows detection of the amphibian pathogen Batrachochytrium dendrobatidis.Crossref | GoogleScholarGoogle Scholar |

Gitzen, R. A., Keller, B. J., Miller, M. A., Goetz, S. M., Steen, D. A., Jachowski, D. S., Godwin, J. C., and Millspaugh, J. J. (2016). Effective and purposeful monitoring of species reintroductions. In ‘Reintroduction of Fish and Wildlife Populations’. (Eds D. S. Jachowski, J. J. Millspaugh, P. L. Angermeier, and R. Slotow.) pp. 283–304. (University of California Press: Oakland, CA.)

Goldberg, C. S., Pilliod, D. S., Arkle, R. S., and Waits, L. P. (2011). Molecular detection of vertebrates in stream water: a demonstration using Rocky Mountain tailed frogs and Idaho giant salamanders. PLoS One 6, e22746.
Molecular detection of vertebrates in stream water: a demonstration using Rocky Mountain tailed frogs and Idaho giant salamanders.Crossref | GoogleScholarGoogle Scholar |

Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis. Nucleic Acids Symposium Series 41, 95–98.
BioEdit: a user-friendly biological sequence alignment editor and analysis.Crossref | GoogleScholarGoogle Scholar |

Haskell, A., Graham, T. E., Griffin, C. R., and Hestbeck, J. B. (1996). Size related survival of headstarted redbelly turtles (Pseudemys rubriventris) in Massachusetts. Journal of Herpetology 30, 524–527.
Size related survival of headstarted redbelly turtles (Pseudemys rubriventris) in Massachusetts.Crossref | GoogleScholarGoogle Scholar |

Hinlo, M. R., Furlan, E. M., Suitor, L., and Gleeson, D. M. (2017). Environmental DNA monitoring and management of invasive fish: comparison of eDNA and fyke netting. Management of Biological Invasions 8, 89–100.
Environmental DNA monitoring and management of invasive fish: comparison of eDNA and fyke netting.Crossref | GoogleScholarGoogle Scholar |

Hunter, D. (2000). Population demography and conservation of the southern corroboree frog. Master of Applied Science Thesis, University of Canberra, ACT.

Hunter, D. (2001). Surveys and Monitoring of Threatened Frog Species in South-eastern New South Wales between October 2000 and March 2001. Unpublished report to the NSW National Parks and Wildlife Service (University of Canberra: ACT.)

Hunter, D., Osborne, W., Smith, M., and Mcdougall, K. (2009). Breeding habitat use and the future management of the critically endangered southern corroboree frog. Ecological Management & Restoration 10, S103–S109.
Breeding habitat use and the future management of the critically endangered southern corroboree frog.Crossref | GoogleScholarGoogle Scholar |

Hunter, D. A., Speare, R., Marantelli, G., Mendez, D., Pietsch, R., and Osborne, W. (2010). Presence of the amphibian chytrid fungus Batrachochytrium dendrobatidis in threatened corroboree frog populations in the Australian Alps. Diseases of Aquatic Organisms 92, 209–216.
Presence of the amphibian chytrid fungus Batrachochytrium dendrobatidis in threatened corroboree frog populations in the Australian Alps.Crossref | GoogleScholarGoogle Scholar |

IUCN (2013). Guidelines for Reintroductions and Other Conservation Translocations. (IUCN Species Survival Commission: Gland, Switzerland.) Available at https://portals.iucn.org/library/sites/library/files/documents/2013-009.pdf [accessed 26 June 2017]

IUCN (2017). The IUCN red list of threatened species. (IUCN Species Survival Commission: Gland, Switzerland.) Available at http://cmsdocs.s3.amazonaws.com/summarystats/2017-1_Summary_Stats_Page_Documents/2017_1_RL_Stats_Table_3a.pdf [accessed 28 June 2017]

Jule, K. R., Leaver, L. A., and Lea, S. E. G. (2008). The effects of captive experience on reintroduction survival in carnivores: a review and analysis. Biological Conservation 141, 355–363.
The effects of captive experience on reintroduction survival in carnivores: a review and analysis.Crossref | GoogleScholarGoogle Scholar |

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

Minamoto, T., Fukuda, M., Katsuhara, K. R., Fujiwara, A., Hidaka, S., Yamamoto, S., Takahashi, K., and Masuda, R. (2017). Environmental DNA reflects spatial and temporal jellyfish distribution. PLoS One 12, e0173073.
Environmental DNA reflects spatial and temporal jellyfish distribution.Crossref | GoogleScholarGoogle Scholar |

Moseby, K. E., Read, J. L., Paton, D. C., Copley, P., Hill, B. M., and Crisp, H. A. (2011). Predation determines the outcome of 10 reintroduction attempts in arid South Australia. Biological Conservation 144, 2863–2872.
Predation determines the outcome of 10 reintroduction attempts in arid South Australia.Crossref | GoogleScholarGoogle Scholar |

OEH NSW (2012). ‘National Recovery Plan for the Southern Corroboree Frog, Pseudophryne corroboree, and the Northern Corroboree Frog, Pseudophryne pengilleyi.’ (Office of Environment and Heritage (NSW): Hurstville, NSW.)

Osborne, W. (1989). Distribution, relative abundance and conservation status of corroboree frogs, Pseudophryne corroboree Moore (Anura, Myobatrachidae). Wildlife Research 16, 537–547.
Distribution, relative abundance and conservation status of corroboree frogs, Pseudophryne corroboree Moore (Anura, Myobatrachidae).Crossref | GoogleScholarGoogle Scholar |

Osborne, W. S., and Norman, J. A. (1991). Conservation genetics of corroboree frogs, PseudophryneCorroboree Moore (Anura, Myobatrachidae): population subdivision and genetic-divergence. Australian Journal of Zoology 39, 285–297.
Conservation genetics of corroboree frogs, PseudophryneCorroboree Moore (Anura, Myobatrachidae): population subdivision and genetic-divergence.Crossref | GoogleScholarGoogle Scholar |

Parker, K. A., Ewen, J. G., Seddon, P. J., and Armstrong, D. P. (2013). Post-release monitoring of bird translocations: why is it important and how do we do it? Notornis 60, 85–92.

Pengilley, R. (1971). Calling and associated behaviour of some species of Pseudophryne (Anura: Leptodactylidae). Journal of Zoology 163, 73–92.
Calling and associated behaviour of some species of Pseudophryne (Anura: Leptodactylidae).Crossref | GoogleScholarGoogle Scholar |

Pilliod, D. S., Goldberg, C. S., Arkle, R. S., and Waits, L. P. (2013). Estimating occupancy and abundance of stream amphibians using environmental DNA from filtered water samples. Canadian Journal of Fisheries and Aquatic Sciences 70, 1123–1130.

Pilliod, D. S., Goldberg, C. S., Arkle, R. S., and Waits, L. P. (2014). Factors influencing detection of eDNA from a stream‐dwelling amphibian. Molecular Ecology Resources 14, 109–116.
Factors influencing detection of eDNA from a stream‐dwelling amphibian.Crossref | GoogleScholarGoogle Scholar |

Rodgers, T. W., and Mock, K. E. (2015). Drinking water as a source of environmental DNA for the detection of terrestrial wildlife species. Conservation Genetics Resources 7, 693–696.
Drinking water as a source of environmental DNA for the detection of terrestrial wildlife species.Crossref | GoogleScholarGoogle Scholar |

Scheele, B., Driscoll, D., Fischer, J., and Hunter, D. (2012). Decline of an endangered amphibian during an extreme climatic event. Ecosphere 3, 1–15.
Decline of an endangered amphibian during an extreme climatic event.Crossref | GoogleScholarGoogle Scholar |

Secondi, J., Dejean, T., Valentini, A., Audebaud, B., and Miaud, C. (2016). Detection of a global aquatic invasive amphibian, Xenopus laevis, using environmental DNA. Amphibia-Reptilia 37, 131–136.
Detection of a global aquatic invasive amphibian, Xenopus laevis, using environmental DNA.Crossref | GoogleScholarGoogle Scholar |

Seddon, P. J., Armstrong, D. P., and Maloney, R. F. (2007). Developing the science of reintroduction biology. Conservation Biology 21, 303–312.
Developing the science of reintroduction biology.Crossref | GoogleScholarGoogle Scholar |

Seddon, P. J., Strauss, W. M., and Innes, J. (2012). Animal translocations: what are they and why do we do them? In ‘Reintroduction Biology: Integrating Science and Management’. (Eds J. G. Ewen, D. P. Armstrong, K. A. Parker, and P. J. Seddon.) pp. 1–31. (Blackwell Publishing, Hoboken, New Jersey, USA)

Seddon, P. J., Griffiths, C. J., Soorae, P. S., and Armstrong, D. P. (2014). Reversing defaunation: restoring species in a changing world. Science 345, 406–412.
Reversing defaunation: restoring species in a changing world.Crossref | GoogleScholarGoogle Scholar |

Skerratt, L. F., Berger, L., Speare, R., Cashins, S., McDonald, K. R., Phillott, A. D., Hines, H. B., and Kenyon, N. (2007). Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth 4, 125–134.
Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs.Crossref | GoogleScholarGoogle Scholar |

Tarszisz, E., Dickman, C. R., and Munn, A. J. (2014). Physiology in conservation translocations. Conservation Physiology 2, cou054.
Physiology in conservation translocations.Crossref | GoogleScholarGoogle Scholar |

Turner, C. R., Barnes, M. A., Xu, C. C. Y., Jones, S. E., Jerde, C. L., and Lodge, D. M. (2014). Particle size distribution and optimal capture of aqueous macrobial eDNA. Methods in Ecology and Evolution 5, 676–684.
Particle size distribution and optimal capture of aqueous macrobial eDNA.Crossref | GoogleScholarGoogle Scholar |