Novel microsatellites and investigation of faecal DNA as a non-invasive population monitoring tool for the banded hare-wallaby (Lagostrophus fasciatus)
Saul Cowen A B * , Michael Smith B C , Shelley McArthur A , Kelly Rayner A , Chantelle Jackson C , Georgina Anderson C and Kym Ottewell A DA Department of Biodiversity, Conservation and Attractions, Biodiversity and Conservation Science, Locked Bag 104, Bentley, WA 6983, Australia.
B School of Biological Sciences, University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.
C Australian Wildlife Conservancy, PO Box 8070, Subiaco East, Perth, WA 6008, Australia.
D Environmental and Conservation Sciences, Murdoch University, 90 South Street, Murdoch, WA 6150, Australia.
Australian Journal of Zoology 69(2) 55-66 https://doi.org/10.1071/ZO21015
Submitted: 7 May 2021 Accepted: 16 December 2021 Published: 8 February 2022
© 2021 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)
Abstract
Monitoring programs for populations of small or medium-sized animals often use live-capture or photo-monitoring trapping methods to estimate population size. The banded hare-wallaby (Lagostrophus fasciatus), a small macropodiform marsupial, does not readily enter traps or have individually unique distinguishing physical features and is consequently difficult to monitor using these methods. Isolating DNA from faecal material to obtain individual genotypes is a promising monitoring technique and may present an alternative approach for this species. We developed novel species-specific microsatellite markers and undertook trials to assess faecal DNA degradation in ambient environmental conditions at two locations where this species has been translocated. The quality of DNA yielded from faecal pellets was evaluated through amplification failure and genotyping error rates of microsatellite markers. Error rates were compared for different treatments and exposure duration across multiple individuals. DNA was successfully obtained from all samples and error rates increased with exposure duration, peaking after 14–30 days depending on the site and treatment. The level of solar exposure was the most significant factor affecting degradation rate but both this and exposure duration had significant effects on amplification failure. Analysing DNA obtained from faecal pellets may represent a practical non-invasive method of deriving population estimates for this species and warrants further development.
Keywords: conservation, faeces, hare-wallaby, Lagostrophus, minimally invasive, molecular genetics, monitoring, threatened species, wildlife management.
References
Australian Wildlife Conservancy (2018a) ‘Movement and Habitat use of Banded Hare-wallabies Posttranslocation: Faure Island (2013) and Mt Gibson (2017).’ (Australian Wildlife Conservancy: Perth, Australia)Australian Wildlife Conservancy (2018b) ‘Mt Gibson Mammal Translocation Summary May 2018.’ (Australian Wildlife Conservancy: Perth, Australia)
Ballard G, Meek PD, Doak S, Fleming PJS, Sparkes J (2014) Camera traps, sand plots and known events: what do camera traps miss? In ‘Camera Trapping: Wildlife Management and Research’. (Eds PM P Fleming, P Banks, G Ballard, A Claridge, J Sanderson, D Swann) pp. 189–202. (CSIRO Publishing: Melbourne, Vic., Australia)
Banks, SC, Hoyle, SD, Horsup, A, Sunnucks, P, and Taylor, AC (2003). Demographic monitoring of an entire species (the northern hairy-nosed wombat, Lasiorhinus krefftii) by genetic analysis of non-invasively collected material. Animal Conservation 6, 101–107.
| Demographic monitoring of an entire species (the northern hairy-nosed wombat, Lasiorhinus krefftii) by genetic analysis of non-invasively collected material.Crossref | GoogleScholarGoogle Scholar |
Blåhed, I-M, Ericsson, G, and Spong, G (2019). Noninvasive population assessment of moose (Alces alces) by SNP genotyping of fecal pellets. European Journal of Wildlife Research 65, 96.
| Noninvasive population assessment of moose (Alces alces) by SNP genotyping of fecal pellets.Crossref | GoogleScholarGoogle Scholar |
Bourgeois, S, Kaden, J, Senn, H, Bunnefeld, N, Jeffery, KJ, Akomo-Okoue, EF, Ogden, R, and McEwing, R (2019). Improving cost-efficiency of faecal genotyping: new tools for elephant species. PLoS ONE 14, e0210811.
| Improving cost-efficiency of faecal genotyping: new tools for elephant species.Crossref | GoogleScholarGoogle Scholar | 30699177PubMed |
Brinkman, TJ, Schwartz, MK, Person, DK, Pilgrim, KL, and Hundertmark, KJ (2010). Effects of time and rainfall on PCR success using DNA extracted from deer fecal pellets. Conservation Genetics 11, 1547–1552.
| Effects of time and rainfall on PCR success using DNA extracted from deer fecal pellets.Crossref | GoogleScholarGoogle Scholar |
Burbidge, AA, and Woinarski, J (2016). Lagostrophus fasciatus. The IUCN Red List of Threatened Species 2016 , e.T11171A21955969.
| Lagostrophus fasciatus.Crossref | GoogleScholarGoogle Scholar |
Bureau of Meteorology (2021) Climate classification maps. Available at http://www.bom.gov.au/jsp/ncc/climate_averages/climate-classifications. [Accessed 26 February 2021]
Carpenter, FM, and Dziminski, MA (2017). Breaking down scats: degradation of DNA from greater bilby (Macrotis lagotis) faecal pellets. Australian Mammalogy 39, 197–204.
| Breaking down scats: degradation of DNA from greater bilby (Macrotis lagotis) faecal pellets.Crossref | GoogleScholarGoogle Scholar |
Carroll, EL, Bruford, MW, DeWoody, JA, Leroy, G, Strand, A, Waits, L, and Wang, J (2018). Genetic and genomic monitoring with minimally invasive sampling methods. Evolutionary Applications 11, 1094–1119.
| Genetic and genomic monitoring with minimally invasive sampling methods.Crossref | GoogleScholarGoogle Scholar | 30026800PubMed |
Chao, A (2001). An overview of closed capture–recapture models. Journal of Agricultural, Biological, and Environmental Statistics 6, 158–175.
| An overview of closed capture–recapture models.Crossref | GoogleScholarGoogle Scholar |
Chapman TF, Sims C, Thomas ND, Reinhold L (2015) Assessment of mammal populations on Bernier and Dorre Island 2006–2013. Department of Parks and Wildlife, Perth, Australia.
Chiron, F, Hein, S, Chargé, R, Julliard, R, Martin, L, Roguet, A, and Jacob, J (2018). Validation of hair tubes for small mammal population studies. Journal of Mammalogy 99, 478–485.
| Validation of hair tubes for small mammal population studies.Crossref | GoogleScholarGoogle Scholar |
Cole, JR, Langford, DG, and Gibson, DF (1994). Capture myopathy in Lagorchestes hirsutus (Marsupialia: Macropodidae). Australian Mammalogy 17, 137–138.
| Capture myopathy in Lagorchestes hirsutus (Marsupialia: Macropodidae).Crossref | GoogleScholarGoogle Scholar |
Cowen S, Rayner K, Sims C, Morris K (2018) Dirk Hartog Island National Park Ecological Restoration Project: stage one – trial hare-wallaby translocations and monitoring. Department of Biodiversity, Conservation and Attractions, Perth, Australia.
De Bondi, ND, White, JG, Stevens, M, and Cooke, R (2010). A comparison of the effectiveness of camera trapping and live trapping for sampling terrestrial small-mammal communities. Wildlife Research 37, 456–465.
| A comparison of the effectiveness of camera trapping and live trapping for sampling terrestrial small-mammal communities.Crossref | GoogleScholarGoogle Scholar |
DeMay, SM, Becker, PA, Eidson, CA, Rachlow, JL, Johnson, TR, and Waits, LP (2013). Evaluating DNA degradation rates in faecal pellets of the endangered pygmy rabbit. Molecular Ecology Resources 13, 654–662.
| Evaluating DNA degradation rates in faecal pellets of the endangered pygmy rabbit.Crossref | GoogleScholarGoogle Scholar | 23590236PubMed |
Department of the Environment (2019) Lagostrophus fasciatus fasciatus in species profile and threats database. Commonwealth Department of the Environment, Canberra, Australia.
DEWHA (2010) Survey guidelines for Australia’s threatened frogs: guidelines for detecting frogs listed as threatened under the Environment Protection and Biodiversity Conservation Act 1999. Department of the Environment, Water, Heritage and the Arts, Canberra, Australia.
DSEWPaC (2011a) Survey guidelines for Australia’s threatened mammals: guidelines for detecting mammals listed as threatened under the Environment Protection and Biodiversity Conservation Act 1999. Department of Sustainability, Environment, Water, Population and Communities, Canberra, Australia.
DSEWPaC (2011b) Survey guidelines for Australia’s threatened reptiles: guidelines for detecting reptiles listed as threatened under the Environment Protection and Biodiversity Conservation Act 1999. Department of Sustainability, Environment, Water, Population and Communities, Canberra, Australia.
Dziminski MA, Carpenter F (2018) The conservation and management of the bilby (Macrotis lagotis) in the Pilbara, Annual Report 2017-18. Department of Biodiversity, Conservation and Attractions, Perth, Australia.
Dziminski, MA, Carpenter, FM, and Morris, F (2021). Monitoring the abundance of wild and reintroduced bilby populations. The Journal of Wildlife Management 85, 240–253.
| Monitoring the abundance of wild and reintroduced bilby populations.Crossref | GoogleScholarGoogle Scholar |
Efford, MG, and Fewster, RM (2013). Estimating population size by spatially explicit capture–recapture. Oikos 122, 918–928.
| Estimating population size by spatially explicit capture–recapture.Crossref | GoogleScholarGoogle Scholar |
Fabbri, E, Caniglia, R, Mucci, N, Thomsen, HP, Krag, K, Pertoldi, C, Loeschcke, V, and Randi, E (2012). Comparison of single nucleotide polymorphisms and microsatellites in non-invasive genetic monitoring of a wolf population. Archives of Biological Sciences 64, 321–335.
| Comparison of single nucleotide polymorphisms and microsatellites in non-invasive genetic monitoring of a wolf population.Crossref | GoogleScholarGoogle Scholar |
Fuller, AK, Sutherland, CS, Royle, JA, and Hare, MP (2016). Estimating population density and connectivity of American mink using spatial capture–recapture. Ecological Applications 26, 1125–1135.
| Estimating population density and connectivity of American mink using spatial capture–recapture.Crossref | GoogleScholarGoogle Scholar | 27509753PubMed |
Garden, JG, McAlpine, CA, Possingham, HP, and Jones, DN (2007). Using multiple survey methods to detect terrestrial reptiles and mammals: what are the most successful and cost-efficient combinations? Wildlife Research 34, 218–227.
| Using multiple survey methods to detect terrestrial reptiles and mammals: what are the most successful and cost-efficient combinations?Crossref | GoogleScholarGoogle Scholar |
Goode, MJ, Beaver, JT, Muller, LI, Clark, JD, van Manen, FT, Harper, CA, and Basinger, PS (2014). Capture–recapture of white-tailed deer using DNA from fecal pellet groups. Wildlife Biology 20, 270–278.
| Capture–recapture of white-tailed deer using DNA from fecal pellet groups.Crossref | GoogleScholarGoogle Scholar |
Harestad, AS, and Bunnell, FL (1987). Persistence of black-tailed deer fecal pellets in coastal habitats. The Journal of Wildlife Management 51, 33–37.
| Persistence of black-tailed deer fecal pellets in coastal habitats.Crossref | GoogleScholarGoogle Scholar |
Jones C, McShea WJ, Conroy MJ, Kunz TH (1996) Capturing mammals. In ‘Measuring and Monitoring Biological Diversity: Standard Methods for Mammals’. (Eds DE Wilson, FR Cole, JD Nichols, R Rudran, MS Foster) pp. 115–156. (Smithsonian Institution Press: Washington, DC, USA)
King, SRB, Schoenecker, KA, Fike, JA, and Oyler-McCance, SJ (2018). Long-term persistence of horse fecal DNA in the environment makes equids particularly good candidates for noninvasive sampling. Ecology and Evolution 8, 4053–4064.
| Long-term persistence of horse fecal DNA in the environment makes equids particularly good candidates for noninvasive sampling.Crossref | GoogleScholarGoogle Scholar | 29721279PubMed |
Lindenmayer, DB, Gibbons, P, Bourke, M, Burgman, M, Dickman, CR, Ferrier, S, Fitzsimons, J, Freudenberger, D, Garnett, ST, Groves, C, Hobbs, RJ, Kingsford, RT, Krebs, C, Legge, S, Lowe, AJ, McLean, R, Montambault, J, Possingham, H, Radford, J, Robinson, D, Smallbone, L, Thomas, D, Varcoe, T, Vardon, M, Wardle, G, Woinarski, J, and Zerger, A (2012). Improving biodiversity monitoring. Austral Ecology 37, 285–294.
| Improving biodiversity monitoring.Crossref | GoogleScholarGoogle Scholar |
Luikart, G, Ryman, N, Tallmon, DA, Schwartz, MK, and Allendorf, FW (2010). Estimation of census and effective population sizes: the increasing usefulness of DNA-based approaches. Conservation Genetics 11, 355–373.
| Estimation of census and effective population sizes: the increasing usefulness of DNA-based approaches.Crossref | GoogleScholarGoogle Scholar |
Lukacs, PM, and Burnham, KP (2005). Review of capture–recapture methods applicable to noninvasive genetic sampling. Molecular Ecology 14, 3909–3919.
| Review of capture–recapture methods applicable to noninvasive genetic sampling.Crossref | GoogleScholarGoogle Scholar | 16262847PubMed |
Meek, PD, Ballard, G-A, and Fleming, PJS (2015). The pitfalls of wildlife camera trapping as a survey tool in Australia. Australian Mammalogy 37, 13–22.
| The pitfalls of wildlife camera trapping as a survey tool in Australia.Crossref | GoogleScholarGoogle Scholar |
Meglécz, E, Costedoat, C, Dubut, V, Gilles, A, Malausa, T, Pech, N, and Martin, J-F (2010). QDD: a user-friendly program to select microsatellite markers and design primers from large sequencing projects. Bioinformatics 26, 403–404.
| QDD: a user-friendly program to select microsatellite markers and design primers from large sequencing projects.Crossref | GoogleScholarGoogle Scholar | 20007741PubMed |
Mills, LS, Citta, JJ, Lair, KP, Schwartz, MK, and Tallmon, DA (2000). Estimating animal abundance using noninvasive DNA sampling: promise and pitfalls. Ecological Applications 10, 283–294.
| Estimating animal abundance using noninvasive DNA sampling: promise and pitfalls.Crossref | GoogleScholarGoogle Scholar |
Morin, DJ, Kelly, MJ, and Waits, LP (2016). Monitoring coyote population dynamics with fecal DNA and spatial capture–recapture. The Journal of Wildlife Management 80, 824–836.
| Monitoring coyote population dynamics with fecal DNA and spatial capture–recapture.Crossref | GoogleScholarGoogle Scholar |
Mortelliti, A, and Boitani, L (2008). Inferring red squirrel (Sciurus vulgaris) absence with hair tubes surveys: a sampling protocol. European Journal of Wildlife Research 54, 353–356.
| Inferring red squirrel (Sciurus vulgaris) absence with hair tubes surveys: a sampling protocol.Crossref | GoogleScholarGoogle Scholar |
Mowat, G, and Strobeck, C (2000). Estimating population size of grizzly bears using hair capture, DNA profiling, and mark–recapture analysis. The Journal of Wildlife Management 64, 183–193.
| Estimating population size of grizzly bears using hair capture, DNA profiling, and mark–recapture analysis.Crossref | GoogleScholarGoogle Scholar |
Murphy, MA, Kendall, KC, Robinson, A, and Waits, LP (2007). The impact of time and field conditions on brown bear (Ursus arctos) faecal DNA amplification. Conservation Genetics 8, 1219–1224.
| The impact of time and field conditions on brown bear (Ursus arctos) faecal DNA amplification.Crossref | GoogleScholarGoogle Scholar |
Nichols, JD (1992). Capture–recapture models. BioScience 42, 94–102.
| Capture–recapture models.Crossref | GoogleScholarGoogle Scholar |
Panasci, M, Ballard, WB, Breck, S, Rodriguez, D, Densmore, LD, Wester, DB, and Baker, RJ (2011). Evaluation of fecal DNA preservation techniques and effects of sample age and diet on genotyping success. The Journal of Wildlife Management 75, 1616–1624.
| Evaluation of fecal DNA preservation techniques and effects of sample age and diet on genotyping success.Crossref | GoogleScholarGoogle Scholar |
Peakall, R, and Smouse, PE (2006). GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Resources 6, 288–295.
| GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research.Crossref | GoogleScholarGoogle Scholar |
Peakall, R, and Smouse, PE (2012). GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research – an update. Bioinformatics 28, 2537–2539.
| GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research – an update.Crossref | GoogleScholarGoogle Scholar | 22820204PubMed |
Piggott, MP (2004). Effect of sample age and season of collection on the reliability of microsatellite genotyping of faecal DNA. Wildlife Research 31, 485–493.
| Effect of sample age and season of collection on the reliability of microsatellite genotyping of faecal DNA.Crossref | GoogleScholarGoogle Scholar |
Piggott, MP, Banks, SC, Stone, N, Banffy, C, and Taylor, AC (2006). Estimating population size of endangered brush-tailed rock-wallaby (Petrogale penicillata) colonies using faecal DNA. Molecular Ecology 15, 81–91.
| Estimating population size of endangered brush-tailed rock-wallaby (Petrogale penicillata) colonies using faecal DNA.Crossref | GoogleScholarGoogle Scholar | 16367832PubMed |
Pinheiro J, Bates D, DebRoy S, Sarkar D, Team RC (2020) nlme: linear and nonlinear mixed effects models. R package version 3.1-148. Available at https://CRAN.R-project.org/package=nlme
Pocock, MJO, and Bell, SC (2011). Hair tubes for estimating site occupancy and activity-density of Sorex minutus. Mammalian Biology 76, 445–450.
| Hair tubes for estimating site occupancy and activity-density of Sorex minutus.Crossref | GoogleScholarGoogle Scholar |
Pompanon, F, Bonin, A, Bellemain, E, and Taberlet, P (2005). Genotyping errors: causes, consequences and solutions. Nature Reviews Genetics 6, 847–859.
| Genotyping errors: causes, consequences and solutions.Crossref | GoogleScholarGoogle Scholar | 16304600PubMed |
Ravanat, J-L, Douki, T, and Cadet, J (2001). Direct and indirect effects of UV radiation on DNA and its components. Journal of Photochemistry and Photobiology B: Biology 63, 88–102.
| Direct and indirect effects of UV radiation on DNA and its components.Crossref | GoogleScholarGoogle Scholar |
R Development Core Team (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at https://www.R-project.org/.
Richards, JD, Short, J, Prince, RIT, Friend, JA, and Courtenay, JM (2001). The biology of banded (Lagostrophus fasciatus) and rufous (Lagorchestes hirsutus) hare-wallabies (Diprotodontia: Macropodidae) on Dorre and Bernier Islands, Western Australia. Wildlife Research 28, 311–322.
| The biology of banded (Lagostrophus fasciatus) and rufous (Lagorchestes hirsutus) hare-wallabies (Diprotodontia: Macropodidae) on Dorre and Bernier Islands, Western Australia.Crossref | GoogleScholarGoogle Scholar |
Rodgers, TW, and Janečka, JE (2013). Applications and techniques for non-invasive faecal genetics research in felid conservation. European Journal of Wildlife Research 59, 1–16.
| Applications and techniques for non-invasive faecal genetics research in felid conservation.Crossref | GoogleScholarGoogle Scholar |
Ruibal, M, Peakall, R, Claridge, A, Murray, A, and Firestone, K (2010). Advancement to hair-sampling surveys of a medium-sized mammal: DNA-based individual identification and population estimation of a rare Australian marsupial, the spotted-tailed quoll (Dasyurus maculatus). Wildlife Research 37, 27–38.
| Advancement to hair-sampling surveys of a medium-sized mammal: DNA-based individual identification and population estimation of a rare Australian marsupial, the spotted-tailed quoll (Dasyurus maculatus).Crossref | GoogleScholarGoogle Scholar |
Sabino-Marques, H, Ferreira, CM, Paupério, J, Costa, P, Barbosa, S, Encarnação, C, Alpizar-Jara, R, Alves, PC, Searle, JB, Mira, A, Beja, P, and Pita, R (2018). Combining genetic non-invasive sampling with spatially explicit capture–recapture models for density estimation of a patchily distributed small mammal. European Journal of Wildlife Research 64, 44.
| Combining genetic non-invasive sampling with spatially explicit capture–recapture models for density estimation of a patchily distributed small mammal.Crossref | GoogleScholarGoogle Scholar |
Short, J, Bradshaw, SD, Giles, J, Prince, RIT, and Wilson, GR (1992). Reintroduction of macropods (Marsupialia: Macropodoidea) in Australia – a review. Biological Conservation 62, 189–204.
| Reintroduction of macropods (Marsupialia: Macropodoidea) in Australia – a review.Crossref | GoogleScholarGoogle Scholar |
Short, J, Turner, B, Majors, C, and Leone, J (1998). The fluctuating abundance of endangered mammals on Bernier and Dorre Islands, Western Australia – conservation implications. Australian Mammalogy 20, 53–61.
| The fluctuating abundance of endangered mammals on Bernier and Dorre Islands, Western Australia – conservation implications.Crossref | GoogleScholarGoogle Scholar |
Sloane, MA, Sunnucks, P, Alpers, D, Beheregaray, LB, and Taylor, AC (2000). Highly reliable genetic identification of individual northern hairy-nosed wombats from single remotely collected hairs: a feasible censusing method. Molecular Ecology 9, 1233–1240.
| Highly reliable genetic identification of individual northern hairy-nosed wombats from single remotely collected hairs: a feasible censusing method.Crossref | GoogleScholarGoogle Scholar | 10972763PubMed |
Smith, M, Volck, G, Palmer, N, Jackson, C, Moir, C, Parker, R, Palmer, B, and Thomasz, A (2020). Conserving the endangered woylie (Bettongia penicillata ogilbyi): establishing a semi-arid population within a fenced safe haven. Ecological Management & Restoration 21, 108–114.
| Conserving the endangered woylie (Bettongia penicillata ogilbyi): establishing a semi-arid population within a fenced safe haven.Crossref | GoogleScholarGoogle Scholar |
Soulsbury, CD, Gray, HE, Smith, LM, Braithwaite, V, Cotter, SC, Elwood, RW, Wilkinson, A, Collins, LM, and Fisher, D (2020). The welfare and ethics of research involving wild animals: a primer. Methods in Ecology and Evolution 11, 1164–1181.
| The welfare and ethics of research involving wild animals: a primer.Crossref | GoogleScholarGoogle Scholar |
Sunnucks, P, and Hales, DF (1996). Numerous transposed sequences of mitochondrial cytochrome oxidase I–II in aphids of the genus Sitobion (Hemiptera: Aphididae). Molecular Biology and Evolution 13, 510–524.
| Numerous transposed sequences of mitochondrial cytochrome oxidase I–II in aphids of the genus Sitobion (Hemiptera: Aphididae).Crossref | GoogleScholarGoogle Scholar | 8742640PubMed |
Taberlet, P, Waits, LP, and Luikart, G (1999). Noninvasive genetic sampling: look before you leap. Trends in Ecology & Evolution 14, 323–327.
| Noninvasive genetic sampling: look before you leap.Crossref | GoogleScholarGoogle Scholar |
Valière, N, Bonenfant, C, Toïgo, C, Luikart, G, Gaillard, J-M, and Klein, F (2006). Importance of a pilot study for non-invasive genetic sampling: genotyping errors and population size estimation in red deer. Conservation Genetics 8, 69–78.
| Importance of a pilot study for non-invasive genetic sampling: genotyping errors and population size estimation in red deer.Crossref | GoogleScholarGoogle Scholar |
Waits, LP, and Paetkau, D (2005). Noninvasive genetic sampling tools for wildlife biologists: a review of applications and recommendations for accurate data collection. Journal of Wildlife Management 69, 1419–1433.
| Noninvasive genetic sampling tools for wildlife biologists: a review of applications and recommendations for accurate data collection.Crossref | GoogleScholarGoogle Scholar |
White, DJ, Ottewell, K, Spencer, PBS, Smith, M, Short, J, Sims, C, and Mitchell, NJ (2020). Genetic consequences of multiple translocations of the banded hare-wallaby in Western Australia. Diversity 12, .
| Genetic consequences of multiple translocations of the banded hare-wallaby in Western Australia.Crossref | GoogleScholarGoogle Scholar |
Williams BK, Nichols JD, Conroy MJ (2002) ‘Analysis and Management of Animal Populations.’ (Academic Press: San Diego, CA, USA)
Woinarski JCZ, Burbidge AA, Harrison PL (2014) ‘The Action Plan for Australian Mammals 2012.’ (CSIRO Publishing: Melbourne, Vic., Australia)
Woodruff, SP, Johnson, TR, and Waits, LP (2015). Evaluating the interaction of faecal pellet deposition rates and DNA degradation rates to optimize sampling design for DNA-based mark–recapture analysis of Sonoran pronghorn. Molecular Ecology Resources 15, 843–854.
| Evaluating the interaction of faecal pellet deposition rates and DNA degradation rates to optimize sampling design for DNA-based mark–recapture analysis of Sonoran pronghorn.Crossref | GoogleScholarGoogle Scholar | 25522240PubMed |
Woodruff, SP, Lukacs, PM, Christianson, D, and Waits, LP (2016). Estimating Sonoran pronghorn abundance and survival with fecal DNA and capture–recapture methods. Conservation Biology 30, 1102–1111.
| Estimating Sonoran pronghorn abundance and survival with fecal DNA and capture–recapture methods.Crossref | GoogleScholarGoogle Scholar | 26918820PubMed |
Wright, JA, Barker, RJ, Schofield, MR, Frantz, AC, Byrom, AE, and Gleeson, DM (2009). Incorporating genotype uncertainty into mark–recapture-type models for estimating abundance using DNA samples. Biometrics 65, 833–840.
| Incorporating genotype uncertainty into mark–recapture-type models for estimating abundance using DNA samples.Crossref | GoogleScholarGoogle Scholar | 19173702PubMed |