Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Australian Journal of Zoology Australian Journal of Zoology Society
Evolutionary, molecular and comparative zoology
RESEARCH ARTICLE

The burrowing bettongs of Barrow Island: demographic and genetic insights into a threatened macropod

Felicity Donaldson A B , Roberta Bencini A , Keith Morris C , Roy Teale D , Celeste H. Wale E , Richard A. How E and Lincoln H. Schmitt E F
+ Author Affiliations
- Author Affiliations

A School of Agriculture and Environment, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.

B 360 Environmental Pty Ltd, 10 Bermondsey Street, West Leederville, WA 6007, Australia.

C Department of Biodiversity, Conservation and Attractions, Locked Bag 104, Bentley Delivery Centre, WA 6983, Australia.

D Biota Environmental Sciences Pty Ltd, 228 Carr Place, Leederville, WA 6007, Australia.

E School of Human Sciences, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.

F Corresponding author. Email: linc.schmitt@uwa.edu.au

Australian Journal of Zoology 65(4) 257-272 https://doi.org/10.1071/ZO17049
Submitted: 14 August 2017  Accepted: 31 January 2018   Published: 26 February 2018

Abstract

Islands provide the last refuge for many Australian species that have succumbed to range contractions since European settlement. These species have heightened vulnerability when developments are planned for the islands. The burrowing bettong (Bettongia lesueur), a threatened macropod, was once widespread across Australia but now occurs naturally only on Barrow Island and two other Western Australian offshore islands. Here, we document the demographic, social and genetic characteristics of the Barrow Island population, using nuclear microsatellites, mtDNA and demographic parameters from 286 individuals trapped around 29 warrens. The Barrow Island population utilises complex warren systems scattered across the landscape and exhibits continuous breeding, even during extensive dry conditions. Males (759 g) were significantly heavier than females (735 g), with the latter reaching sexual maturity at ~600 g. Warrens varied markedly in size and number of individuals, with 20% of females and 25% of males moving between nearby warrens. There were two deep mtDNA haplotype clades that coalesce around 298 000 years ago, indicating that this island population has maintained an effective population size that has permitted the retention of one marked feature of its preisolation genetic diversity. Dispersal and gene flow between warrens was severely constrained. Both mtDNA and 11 nuclear microsatellites showed a strong isolation by distance effect, with genetic differences between warrens increasing linearly with geographic separation. While this was marked in both sexes, it was stronger in females and consistent with shorter dispersal distances for females than for males. The trapping and genetic data are concordant, with between-warren sociality correlated with genetic similarity. Long-term conservation, management and translocation programs will benefit from cognisance of the strong fidelity to natal areas, as evidenced by both recapture data and genetic analyses.


References

Abbott, I., and Burbidge, A. A. (1995). The occurrence of mammal species on the islands of Australia: a summary of existing knowledge. CALMscience 1, 259–324.

Beaumont, M. A. (2003). Conservation genetics. In ‘Handbook of Statistical Genetics’. 2nd edn. (Eds D. J. Balding, M. Bishop, and C. Cannings.) pp. 751–792. (Wiley: Chichester, UK.)

Bird, C. E., Karl, S. A., Smouse, P. E., and Toonen, R. J. (2011). Detecting and measuring genetic differentiation. In ‘Crustacean Issues. 19: Phylogeography and Population Genetics Issues in Crustacea’. (Eds C. Held, S. Koenemann, and C. D. Schubart). pp. 31–55. (CRC Press: Boca Raton, FL.)

Burbidge, A. A., and Manly, B. F. J. (2002). Mammal extinctions on Australian islands: causes and conservation implications. Journal of Biogeography 29, 465–473.
Mammal extinctions on Australian islands: causes and conservation implications.Crossref | GoogleScholarGoogle Scholar |

Burbidge, A. A., and McKenzie, N. L. (1989). Patterns in the modern decline of Western Australia’s vertebrate fauna: causes and conservation implications. Biological Conservation 50, 143–198.
Patterns in the modern decline of Western Australia’s vertebrate fauna: causes and conservation implications.Crossref | GoogleScholarGoogle Scholar |

Burbidge, A. A., and Short, J. C. (2008). Burrowing bettong: Bettongia lesueur. In ‘The Mammals of Australia’. 3rd edn. (Ed. S. Van Dyck and R. Strahan.) pp. 288–291. (Reed New Holland: Sydney.)

Chevron Australia (2003). Environmental, social and economic review of the Gorgon Gas Development on Barrow Island. Chevron Australia, Perth. Available at: http://www.epa.wa.gov.au/sites/default/files/PER_documentation/1496-ESE-Technical%20Appendices.pdf

Chevron Australia (2006). Final environmental impact statement/environmental review and management programme for the Gorgon Gas Development. Technical appendices C1–C5. Chevron Australia, Perth. Appendix C2: Mammals and Reptiles Technical Report. pp. 18–19.

Clarke, K. R., and Gorley, R. N. (2006). ‘PRIMER v6: User Manual/Tutorial.’ (PRIMER-E Ltd: Plymouth, UK.)

Darriba, D., Taboada, G. L., Doallo, R., and Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.
jModelTest 2: more models, new heuristics and parallel computing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFWmsbfP&md5=a472f35231edaa5c03b1c0a4a1f4b30cCAS |

Dietz, E. J. (1983). Permutation tests for association between two distance matrices. Systematic Biology 32, 21–26.
Permutation tests for association between two distance matrices.Crossref | GoogleScholarGoogle Scholar |

Drummond, A. J., Suchard, M. A., Xie, D., and Rambaut, A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29, 1969–1973.
Bayesian phylogenetics with BEAUti and the BEAST 1.7.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFagu7fO&md5=039e0ad1aee38a78e594be3663f04bb1CAS |

Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.
MUSCLE: multiple sequence alignment with high accuracy and high throughput.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXisF2ks7w%3D&md5=63332555f294af07356c7eeffd30c183CAS |

Excoffier, L., and Lischer, H. E. L. (2010). Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564–567.
Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows.Crossref | GoogleScholarGoogle Scholar |

Excoffier, L., Smouse, P. E., and Quattro, J. M. (1992). Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131, 479–491.
| 1:CAS:528:DyaK38XlsVCntro%3D&md5=da3e2c1142323f42c1cdfb7a974fbbc3CAS |

Finlayson, G. R., and Moseby, K. E. (2004). Managing confined populations: the influence of density on the home range and habitat use of the reintroduced burrowing bettongs (Bettongia lesueur). Wildlife Research 31, 457–463.
Managing confined populations: the influence of density on the home range and habitat use of the reintroduced burrowing bettongs (Bettongia lesueur).Crossref | GoogleScholarGoogle Scholar |

Frankham, R. (2005). Genetics and extinction. Biological Conservation 126, 131–140.
Genetics and extinction.Crossref | GoogleScholarGoogle Scholar |

Fumagalli, L., Pope, L. C., Taberlet, P., and Moritz, C. (1997). Versatile primers for the amplification of the mitochondrial DNA control region in marsupials. Molecular Ecology 6, 1199–1201.
Versatile primers for the amplification of the mitochondrial DNA control region in marsupials.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXisVWntA%3D%3D&md5=01c669feb281feae0028caefdbc62d4dCAS |

Government of Western Australia (2009). Statement that a proposal may be implemented. Gorgon Gas Development revised and expanded proposal: Barrow Island Nature Reserve (Ministerial Statement No. 800), 10 August 2009. Perth, Western Australia. Available at: http://www.epa.wa.gov.au/sites/default/files/Ministerial_Statement/00800.pdf

Hampton, J. O., Spencer, P. B. S., Alpers, D. L., Twigg, L. E., Woolnough, A. P., Doust, J., Higgs, T., and Pluske, J. (2004). Molecular techniques, wildlife management and the importance of genetic population structure and dispersal: a case study with feral pigs. Journal of Applied Ecology 41, 735–743.
Molecular techniques, wildlife management and the importance of genetic population structure and dispersal: a case study with feral pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnt1Klt7c%3D&md5=4c5ee3a4f1f4a42787f587a8c585bec9CAS |

Hazlitt, S. L., Goldizen, A. W., Nicholls, J. A., and Eldridge, M. D. B. (2014). Three divergent lineages within an Australian marsupial (Petrogale penicillata) suggest multiple major refugia for mesic taxa in southeast Australia. Ecology and Evolution 4, 1102–1116.
Three divergent lineages within an Australian marsupial (Petrogale penicillata) suggest multiple major refugia for mesic taxa in southeast Australia.Crossref | GoogleScholarGoogle Scholar |

Holm, S. (1979). A simple sequentially rejective multiple test procedure. Scandinavian Journal of Statistics 6, 65–70.

Kumar, S., Stecher, G., and Tamura, K. (2016). MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.
MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhsF2ltrzN&md5=8f72aeaa108036ed6e6e5de47b3faee2CAS |

Lagdon, R., and Moro, D. (2013). The Gorgon Gas Development and its environmental conditions. Records of the Western Australian Museum , 9–11.
The Gorgon Gas Development and its environmental conditions.Crossref | GoogleScholarGoogle Scholar |

Lewis, S. E., Sloss, C. R., Murray-Wallace, C. V., Woodroffe, C. D., and Smithers, S. G. (2013). Post-glacial sea-level changes around the Australian margin: a review. Quaternary Science Reviews 74, 115–138.
Post-glacial sea-level changes around the Australian margin: a review.Crossref | GoogleScholarGoogle Scholar |

Mantel, N. (1967). The detection of disease clustering and a generalised regression approach. Cancer Research 27, 209–220.
| 1:STN:280:DyaF2s%2FptlSnsA%3D%3D&md5=d3291e765b230b833c69fcb3b912c2e7CAS |

Maxwell, S., Burbidge, A. A., and Morris, K. D. (1996). ‘Action Plan for Australian Marsupials and Monotremes.’ (Environment Australia: Canberra.)

Mills, H. R., Moro, D., and Spencer, P. B. S. (2004). Conservation significance of island versus mainland populations: a case study of dibblers (Parantechinus apicalis) in Western Australia. Animal Conservation 7, 387–395.
Conservation significance of island versus mainland populations: a case study of dibblers (Parantechinus apicalis) in Western Australia.Crossref | GoogleScholarGoogle Scholar |

Parsons, B. C., Short, J. C., and Calver, M. C. (2002). Evidence of male-biased dispersal in a reintroduced population of burrowing bettongs Bettongia lesueur at Heirisson Prong, Western Australia. Australian Mammalogy 24, 219–224.

Peakall, R., and Smouse, P. E. (2006). GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6, 288–295.
GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research.Crossref | GoogleScholarGoogle Scholar |

Peakall, R., and Smouse, P. E. (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 | 1:CAS:528:DC%2BC38XhsVehtbjI&md5=8a45fddcd34cb7f5ae63c2130a82fb99CAS |

Peakall, R., Ruibal, M., and Lindenmayer, D. B. (2003). Spatial autocorrelation analysis offers new insights into gene flow in the Australian bush rat, Rattus fuscipes. Evolution 57, 1182–1195.
Spatial autocorrelation analysis offers new insights into gene flow in the Australian bush rat, Rattus fuscipes.Crossref | GoogleScholarGoogle Scholar |

Rambaut, A., Suchard, M. A., Xie, D., and Drummond, A. J. (2014). Tracer v1.6. Available at: http://beast.bio.ed.ac.uk/Tracer

Richards, J., Morris, K., and Burbidge, A. (2008). Bettongia lesueur. The IUCN Red List of Threatened Species 2008: e.T2784A9480530. Available at: http://dx.doi.org/10.2305/IUCN.UK.2008.RLTS.T2784A9480530.en [accessed 6 February 2017].

Robertson, B. C., and Gemmell, N. J. (2004). Defining eradication units to control invasive pests. Journal of Applied Ecology 41, 1042–1048.
Defining eradication units to control invasive pests.Crossref | GoogleScholarGoogle Scholar |

Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A., and Huelsenbeck, J. P. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.
MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space.Crossref | GoogleScholarGoogle Scholar |

Rousset, F. (2008). GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Molecular Ecology Resources 8, 103–106.
GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux.Crossref | GoogleScholarGoogle Scholar |

Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989). ‘Molecular Cloning: a Laboratory Manual.’ (Cold Spring Harbor Laboratory Press: New York.)

Sander, U., Short, J., and Turner, B. (1997). Social organisation and warren use of the burrowing bettong, Bettongia lesueur (Macropodoidea: Potoroidae). Wildlife Research 24, 143–157.
Social organisation and warren use of the burrowing bettong, Bettongia lesueur (Macropodoidea: Potoroidae).Crossref | GoogleScholarGoogle Scholar |

Short, J., and Turner, B. (1993). The distribution and abundance of the burrowing bettong (Marsupialia: Macropodoidea). Wildlife Research 20, 525–534.
The distribution and abundance of the burrowing bettong (Marsupialia: Macropodoidea).Crossref | GoogleScholarGoogle Scholar |

Short, J., and Turner, B. (1999). Ecology of burrowing bettongs, Bettongia lesueur (Marsupialia: Potoroidae), on Dorre and Bernier Islands, Western Australia. Wildlife Research 26, 651–669.
Ecology of burrowing bettongs, Bettongia lesueur (Marsupialia: Potoroidae), on Dorre and Bernier Islands, Western Australia.Crossref | GoogleScholarGoogle Scholar |

Short, J., and Turner, B. (2000). Reintroduction of burrowing bettong Bettongia lesueur (Marsupialia: Potoroidae) to mainland Australia. Biological Conservation 96, 185–196.
Reintroduction of burrowing bettong Bettongia lesueur (Marsupialia: Potoroidae) to mainland Australia.Crossref | GoogleScholarGoogle Scholar |

Short, J., Turner, B., and Majors, C. (1989). The distribution, relative abundance, and habitat preferences of rare macropods and bandicoots on Barrow, Boodie, Bernier and Dorre Islands. Report, CSIRO Division of Wildlife and Ecology, Canberra.

Stodart, E. (1966). Observations on the behaviour of the marsupial Bettongia lesueuri (Quoy & Gaimard) in an enclosure. CSIRO Wildlife Research 11, 91–99.
Observations on the behaviour of the marsupial Bettongia lesueuri (Quoy & Gaimard) in an enclosure.Crossref | GoogleScholarGoogle Scholar |

Van Oosterhout, C., Hutchinson, W. F., Wills, D. P. M., and Shipley, P. (2004). MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4, 535–538.
MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvFOktb8%3D&md5=b7e08c630efc36d1d8b1fa8b19fb3ae6CAS |

VSN International (2015). ‘Genstat for Windows.’ 18th edn. (VSN International: Hemel Hempstead, UK.)

Walker, F. M., Taylor, A. C., and Sunnucks, P. (2008). Female dispersal and male kinship-based association in the southern hairy-nosed wombats (Lasiorhinus latifrons). Molecular Ecology 17, 1361–1374.
Female dispersal and male kinship-based association in the southern hairy-nosed wombats (Lasiorhinus latifrons).Crossref | GoogleScholarGoogle Scholar |

Weir, B. S., and Cockerham, C. C. (1984). Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370.
| 1:STN:280:DC%2BC1cnjt1SlsA%3D%3D&md5=300f3694f64a87bf8b615ee0f5820a72CAS |

Woinarski, J. C. Z., Milne, D. J., and Wanganeen, G. (2001). Changes in mammal populations in relatively intact landscapes of Kakadu National Park, Northern Territory, Australia. Austral Ecology 26, 360–370.
Changes in mammal populations in relatively intact landscapes of Kakadu National Park, Northern Territory, Australia.Crossref | GoogleScholarGoogle Scholar |

Woinarski, J. C. Z., Burbidge, A. A., and Harrison, P. L. (2015). Ongoing unraveling of a continental fauna: decline and extinction of Australian mammals since European settlement. Proceedings of the National Academy of Sciences of the United States of America 112, 4531–4540.
Ongoing unraveling of a continental fauna: decline and extinction of Australian mammals since European settlement.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXitlagsbg%3D&md5=0930c99aa749c38efc3262e2691a902cCAS |