Cryptic grey-bellied dunnart (Sminthopsis griseoventer) discovered in South Australia: genetic, morphological and subfossil analyses show the value of collecting voucher material
Catherine M. Kemper A F , Steven J. B. Cooper B C , Graham C. Medlin A , Mark Adams B C , David Stemmer A , Kathleen M. Saint B , Matthew C. McDowell A D and Jeremy J. Austin E
+ Author Affiliations
- Author Affiliations
A Mammal Section, South Australian Museum, North Terrace, Adelaide, SA 5000, Australia.
B Evolutionary Biology Unit, South Australian Museum, North Terrace, Adelaide, SA 5000, Australia.
C Australian Centre for Evolutionary Biology and Biodiversity and School of Earth and Environmental Science, The University of Adelaide, SA 5005, Australia.
D School of Biological Science, Flinders University of South Australia, PO Box 2100, Adelaide, SA 5001, Australia.
E Australian Centre for Ancient DNA and School of Earth and Environmental Science, The University of Adelaide, SA 5005, Australia.
F Corresponding author. Email: Catherine.Kemper@samuseum.sa.gov.au
Australian Journal of Zoology 59(3) 127-144 https://doi.org/10.1071/ZO11037
Submitted: 26 May 2011 Accepted: 23 September 2011 Published: 23 November 2011
Abstract
The assumption that almost all mammal species are known to science has led to a recent trend away from collecting voucher specimens/tissues during field studies. Here we present a case study of a recently discovered cryptic marsupial (Sminthopsis griseoventer) in South Australia (SA) and show how such collections can contribute to rigorous biodiversity and biogeographic assessments. Morphological and genetic (allozyme and mitochondrial control region (CR) sequence data) analyses, including ancient DNA analyses of type material, were applied to 188 voucher specimens and 94 non-vouchered tissues of Sminthopsis held at the SA Museum. These data were used to confirm the presence of S. griseoventer in SA, validate means of identifying it morphologically and describe recent and pre-European distributions. Pelage differences between S. griseoventer and S. dolichura enabled their identification, but external measurements overlapped considerably. Subfossil S. griseoventer were identified from seven deposits and confirmed that in the past the species was more widespread in SA. CR divergences (>1.8%) among Western Australian and SA S. griseoventer suggested its long-term presence in SA. Discrepancies between the mitochondrial and allozyme affinities of S. aitkeni and S. griseoventer, coupled with the lack of obvious morphological differences, indicate that a taxonomic reappraisal of these species is warranted. The study strongly demonstrates an ongoing need for the routine collection of mammal voucher material in biological and environmental impact surveys.
Additional keywords: allozyme electrophoresis, dasyurid, distribution, mitochondrial control region, paratype, Sminthopsis aitkeni, Sminthopsis dolichura, taxonomy.
References
Aitken, P. A. (1972). Sminthopsis murina (Waterhouse) 1838, a new record from Kangaroo Island, South Australia. South Australian Naturalist 46, 36–37.Archer, M. (1976). The dasyurid dentition and its relationships to that of didelphids, thylacinids, borhyaenids (Marsupicarnivora) and peramelids (Peramelina: Marsupialia). Australian Journal of Zoology Supplementary Series No. 39, 1–34.
Archer, M. (1981). Results of the Archbold Expeditions. No. 104. Systematic revision of the marsupial dasyurid genus Sminthopsis Thomas. Bulletin of the American Museum of Natural History 168, 63–223.
Avenant, N. L. (2005). Barn owl pellets: a useful tool for monitoring small mammal communities? Belgian Journal of Zoology 135, 39–43.
Baverstock, P. R., Archer, M., Adams, M., and Richardson, B. J. (1981). Genetic relationships among 32 species of Australian dasyurid marsupials. In ‘Carnivorous Marsupials’. (Ed. M. Archer.) pp. 641–650. (Royal Zoological Society of New South Wales: Sydney.)
Baverstock, P. R., Adams, M., and Archer, M. (1984). Electrophoretic resolution of species boundaries in the Sminthopsis murina complex (Dasyuridae). Australian Journal of Zoology 32, 823–832.
| Electrophoretic resolution of species boundaries in the Sminthopsis murina complex (Dasyuridae).Crossref | GoogleScholarGoogle Scholar |
Baynes, A. (1994). A concise report on the analysis of the mammal material from the E4 excavation in Allen’s Cave. In ‘A Taphonomic Analysis of the Vertebrate Material from Allen’s Cave: Implications for Australian Arid Zone Archaeology’. K. A. Walshe, Ph.D. Thesis, Australian National University, Canberra. Appendix 1, pp. A1.1–A1.8.
Beheregaray, L. B., and Caccone, A. (2007). Cryptic biodiversity in a changing world. Journal of Biology 6, 9.
| Cryptic biodiversity in a changing world.Crossref | GoogleScholarGoogle Scholar |
Blacket, M. J., Krajewski, C., Labrinidis, A., Cambron, B., Cooper, S., and Westerman, M. (1999). Systematic relationships within the dasyurid marsupial tribe Sminthopsini – a multigene approach. Molecular Phylogenetics and Evolution 12, 140–155.
| Systematic relationships within the dasyurid marsupial tribe Sminthopsini – a multigene approach.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjvFWrsLc%3D&md5=bf1320e2e93bf408e0b240fbe9282824CAS |
Blacket, M. J., Adams, M., Cooper, S. J. B., Krajewski, C., and Westerman, M. (2001). Systematics and evolution of the dasyurid marsupial genus Sminthopsis: I. The macroura species group. Journal of Mammalian Evolution 8, 149–170.
| Systematics and evolution of the dasyurid marsupial genus Sminthopsis: I. The macroura species group.Crossref | GoogleScholarGoogle Scholar |
Blacket, M. J., Cooper, S. J. B., Krajewski, C., and Westerman, M. (2006). Systematics and evolution of the dasyurid marsupial genus Sminthopsis: II. The murina species group. Journal of Mammalian Evolution 13, 125–138.
| Systematics and evolution of the dasyurid marsupial genus Sminthopsis: II. The murina species group.Crossref | GoogleScholarGoogle Scholar |
Brandle, R. (2001). A biological survey of the Flinders Ranges, South Australia 1997–1999. Department for Environment and Heritage, Adelaide.
Brandle, R. (2010). A biological survey of the Eyre Peninsula, South Australia. Department for Environment and Heritage, Adelaide.
Burbidge, A., Abbott, I., Comer, S., Adams, E., Berry, O., and Penwarden, K. (). Unforeseen consequences of a misidentified rodent: case study from the Archipelago of the Recherche, Western Australia. Australian Mammalogy , .
Burbidge, N. T. (1960). The phytogeography of the Australian region. Australian Journal of Botany 8, 75–212.
| The phytogeography of the Australian region.Crossref | GoogleScholarGoogle Scholar |
Byrne, M., Yeates, D. K., Joseph, L., Kearney, M., Bowler, J., Williams, M. A., Cooper, S. J. B., Donnellan, S. C., Keogh, S., Leijs, R., Melville, J., Murphy, D., Porch, N., and Wyrwoll, K.-H. (2008). Birth of a biome: synthesizing environmental and molecular studies of the assembly and maintenance of the Australian arid zone biota. Molecular Ecology 17, 4398–4417.
| Birth of a biome: synthesizing environmental and molecular studies of the assembly and maintenance of the Australian arid zone biota.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cjhvFGruw%3D%3D&md5=383a6dbca041980a7dc45069fb7940cdCAS |
Ceballos, G., and Ehrlich, P. R. (2009). Discoveries of new mammal species and their implications for conservation and ecosystem services. Proceedings of the National Academy of Sciences of the United States of America 106, 3841–3846.
| Discoveries of new mammal species and their implications for conservation and ecosystem services.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjt1Gksb4%3D&md5=ee4ba18fe3e9643d65db4558c91516bcCAS |
Cooper, A., and Poinar, H. N. (2000). Ancient DNA: do it right or not at all. Science 289, 1139.
| Ancient DNA: do it right or not at all.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmt1Sqtbo%3D&md5=3eb291d5c6556349a75c46949c4e1b3bCAS |
Cooper, N. K., Bertozzi, T., Baynes, A., and Teale, R. J. (2003). The relationship between eastern and western populations of the heath rat, Pseudomys shortridgei (Rodentia: Muridae). Records of the Western Australian Museum 21, 367–370.
Cooper, S. J. B., Adams, M., and Labrinidis, A. (2000). Phylogeography of the Australian dunnart Sminthopsis crassicaudata (Marsupialia: Dasyuridae). Australian Journal of Zoology 48, 461–473.
| Phylogeography of the Australian dunnart Sminthopsis crassicaudata (Marsupialia: Dasyuridae).Crossref | GoogleScholarGoogle Scholar |
Crowther, M. S., Dickman, C. R., and Lynham, A. J. (1999). Sminthopsis griseoventer boullangerensis (Marsupialia: Dasyuridae), a new subspecies in the S. murina complex from Boullanger Island, Western Australia. Australian Journal of Zoology 47, 215–243.
| Sminthopsis griseoventer boullangerensis (Marsupialia: Dasyuridae), a new subspecies in the S. murina complex from Boullanger Island, Western Australia.Crossref | GoogleScholarGoogle Scholar |
Draper, N. (1999). The history of Aboriginal land use on Kangaroo Island. In ‘A Biological Survey of Kangaroo Island South Australia, 1989 and 1990’. (Eds A. C. Robinson and D. M. Armstrong.) pp. 33–48. (Heritage and Biodiversity Division, Department for Environment, Heritage and Aboriginal Affairs: South Australia.)
Driscoll, D. A., and Henderson, M. K. (2008). How many common reptile species are fire specialists? A replicated natural experiment highlights the predictive weakness of a fire succession model. Biological Conservation 141, 460–471.
| How many common reptile species are fire specialists? A replicated natural experiment highlights the predictive weakness of a fire succession model.Crossref | GoogleScholarGoogle Scholar |
Edwards, S. V. (2009). Is a new and general theory of molecular systematics emerging? Evolution 63, 1–19.
| Is a new and general theory of molecular systematics emerging?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXisVKgtbs%3D&md5=50b9e5b27851eab5dc276b8ce69b8005CAS |
Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.
| Confidence limits on phylogenies: an approach using the bootstrap.Crossref | GoogleScholarGoogle Scholar |
Galloway, R. W., and Kemp, E. M. (1981). Late Cainozoic environments in Australia. In ‘Ecological Biogeography of Australia’. (Ed. A. Keast.) pp. 50−80. (Dr W. Junk: The Hague.)
Gates, J. A. (2001). The distribution and ecology of the Kangaroo Island dunnart Sminthopsis aitkeni. Endangered Species Project No. 006499. Final report to Department for Environment and Heritage, Adelaide.
Hammer, M., Adams, M., Unmack, P. J., and Walker, K. F. (2007). A rethink on Retropinna: conservation implications of new taxa and significant genetic sub-structure in Australian smelts (Pisces: Retropinnidae). Marine and Freshwater Research 58, 327–341.
| A rethink on Retropinna: conservation implications of new taxa and significant genetic sub-structure in Australian smelts (Pisces: Retropinnidae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkt1entbY%3D&md5=e6b380fd4333396d4998f3e09e9db147CAS |
Hasegawa, M., Kishino, H., and Yano, T. (1985). Dating of the human–ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22, 160–174.
| Dating of the human–ape splitting by a molecular clock of mitochondrial DNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXmtFSns7g%3D&md5=1048a49ee65f1560b73cafc0ff9623e8CAS |
Hesse, P. P., Magee, J. W., and van der Kaars, S. (2004). Late Quaternary climates of the Australian arid zone: a review. Quaternary International 118–119, 87–102.
| Late Quaternary climates of the Australian arid zone: a review.Crossref | GoogleScholarGoogle Scholar |
Heywood, M. R., and Pavey, C. R. (2002). Relative importance of plague rodents and dasyurids as prey of barn owls in central Australia. Wildlife Research 29, 203–207.
| Relative importance of plague rodents and dasyurids as prey of barn owls in central Australia.Crossref | GoogleScholarGoogle Scholar |
Hope, J. H., Lampert, R. J., Edmondson, E., Smith, M. J., and Tets, G. F. (1977). Late Pleistocene faunal remains from Seton Rock-shelter, Kangaroo Island, South Australia. Journal of Biogeography 4, 363–385.
| Late Pleistocene faunal remains from Seton Rock-shelter, Kangaroo Island, South Australia.Crossref | GoogleScholarGoogle Scholar |
Hutchinson, M. N. (1990). Leiolopisma trilineatum (Gray, 1838), an addition to the herpetofauna of South Australia. Transactions of the Royal Society of South Australia 114, 99–101.
Kemper, C., Medlin, G., and Bachmann, M. (2010). The discovery and history of the heath mouse Pseudomys shortridgei (Thomas, 1907) in South Australia. Transactions of the Royal Society of South Australia 134, 125–138.
Kitchener, D. J., Stoddart, J., and Henry, J. (1984). A taxonomic revision of the Sminthopsis murina complex (Marsupialia, Dasyuridae) in Australia, including descriptions of four new species. Records of the Western Australian Museum 11, 201–248.
Krajewski, C., Wroe, S., and Westerman, M. (2000). Molecular evidence for the pattern and timing of cladogenesis in dasyurid marsupials. Zoological Journal of the Linnean Society 130, 375–404.
| Molecular evidence for the pattern and timing of cladogenesis in dasyurid marsupials.Crossref | GoogleScholarGoogle Scholar |
Labrinidis, A., Cooper, S. J. B., Adams, M., and Baczocha, N. (1998). Systematic affinities of island and mainland populations of the dunnart Sminthopsis griseoventer in Western Australia: data from allozymes and mitochondrial DNA. Pacific Conservation Biology 4, 289–295.
Langeluddecke, C. J. (2000). Undervalued animals. The small faunal taphonomy and zooarchaeology of Cape du Couedic Rockshelter, Kangaroo Island, South Australia. B.Sc.(Honours) Thesis, Flinders University of South Australia, Adelaide.
Lomolino, M. V. (1985). Body size of mammals on islands: the island rule re-examined. American Naturalist 125, 310–316.
| Body size of mammals on islands: the island rule re-examined.Crossref | GoogleScholarGoogle Scholar |
Luckett, W. P. (1993). An ontogenetic assessment of dental homologies in therian mammals. In ‘Mammal Phylogeny: Mesozoic Differentiation, Multituberculates, Monotremes, Early Therians, and Marsupials’. (Eds F. S. Szalay, M. J. Novacek and M. C. McKenna.) pp. 192–204. (Springer-Verlag: New York.)
McDowell, M. C. (1997). Taphonomy and palaeoenvironmental interpretation of a late Holocene deposit from Black’s Point Sinkhole, Venus Bay, S.A. Proceedings of the Linnean Society of New South Wales 117, 79–96.
McDowell, M. C., and Medlin, G. C. (2009). The effects of drought on prey selection of the barn owl (Tyto alba) in the Strzelecki Regional Reserve, north-eastern South Australia. Australian Mammalogy 31, 47–55.
| The effects of drought on prey selection of the barn owl (Tyto alba) in the Strzelecki Regional Reserve, north-eastern South Australia.Crossref | GoogleScholarGoogle Scholar |
McDowell, M. C., and Medlin, G. C. (2010). Natural Resource Management implications of the pre-European non-volant mammal fauna of the southern tip of Eyre Peninsula, South Australia. Australian Mammalogy 32, 87–93.
| Natural Resource Management implications of the pre-European non-volant mammal fauna of the southern tip of Eyre Peninsula, South Australia.Crossref | GoogleScholarGoogle Scholar |
Medlin, G. C. (1996). Report on vertebrate remains from a sinkhole in the Venus Bay Conservation Park. Wildlife Conservation Fund, Department for Environment and Heritage, Adelaide.
Miller, E. H. (1993). Biodiversity research in museums: a return to the basics. In ‘Our Living Legacy: Proceedings of a Symposium on Biological Diversity’. (Eds E. H. Miller, J. A. Johnson and E. J. R. Williams.) pp. 141–173. (Royal British Columbia Museum: Victoria, Canada.)
Miller, E. H., and Scudder, G. G. E. (1994). A rose by any other name. In ‘Biodiversity in British Columbia: Our Changing Environment’. (Eds L. E. Harding and E. McCullum.) pp. 29–43. (Canadian Wildlife Service, Environment Canada: Ottawa.)
Murray, A. S., and Roberts, R. G. (1997). Determining the burial time of single grains of quartz using optically stimulated luminescence. Earth and Planetary Science Letters 152, 163–180.
| Determining the burial time of single grains of quartz using optically stimulated luminescence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXnvFOktrY%3D&md5=693212cb402e2d1583d53432fd867f52CAS |
Nicholls, J. A., Double, M. C., Rowell, D. M., and Magrath, R. D. (2000). The evolution of cooperative and pair breeding in thornbills Acanthiza (Pardalotidae). Journal of Avian Biology 31, 165–176.
| The evolution of cooperative and pair breeding in thornbills Acanthiza (Pardalotidae).Crossref | GoogleScholarGoogle Scholar |
Parsons, R. F. (1969). Distribution and palaeogeography of two mallee species of Eucalyptus in southern Australia. Australian Journal of Botany 17, 323–330.
| Distribution and palaeogeography of two mallee species of Eucalyptus in southern Australia.Crossref | GoogleScholarGoogle Scholar |
Pate, F. D., McDowell, M. C., Wells, R. T., and Smith, A. M. (2002). Last recorded evidence for megafauna at Wet Cave, Naracoorte, South Australia 45,000 years ago. Australian Archaeology 54, 53–55.
Prideaux G. J. Gully G. A. Couzens A. M. C. Ayliffe L. K. Jankowski N. R. Jacobs Z. Roberts R. G. Hellstrom J. C. Gagan M. C. Hatcher L. M. 2010
Richardson, B. J., Baverstock, P. R., and Adams, M. A. (1986). ‘Allozyme Electrophoresis: a Handbook for Animal Systematics and Population Studies.’ (Academic Press: Sydney.)
Ridgway, R. (1912). ‘Color Standards and Color Nomenclature.’ (Published by the author: Washington, DC.)
Roberts, R. G., Spooner, N. A., Jones, R., Cane, S., Olley, J. M., Murray, A. S., and Head, M. J. (1996). Preliminary luminescence dates for archaeological sediments on the Nullarbor Plain, South Australia. Australian Archaeology 42, 7–16.
Roberts, R. G., Flannery, T. F., Ayliffe, L. K., Yoshida, H., Olley, J. M., Prideaux, G. J., Laslett, G. M., Baynes, A., Smith, M. A., Jones, R., and Smith, B. L. (2001). New ages for the last Australian megafauna: continent-wide extinction about 46,000 years ago. Science 292, 1888–1892.
| New ages for the last Australian megafauna: continent-wide extinction about 46,000 years ago.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXksVaqsLs%3D&md5=747cf07b323bc17106418ecbe2c835f4CAS |
Robinson, A. C., Casperson, K. D., and Hutchinson, M. N. (2000). ‘A List of the Vertebrates of South Australia.’ (Department for Environment and Heritage: Adelaide.)
Rodríguez, F., Oliver, J. F., Marín, A., and Medina, J. R. (1990). The general stochastic model of nucleotide substitutions. Journal of Theoretical Biology 142, 485–501.
| The general stochastic model of nucleotide substitutions.Crossref | GoogleScholarGoogle Scholar |
Salinas, M., Bunce, M., Cancilla, D., Alpers, D. L., and Spencer, P. (2009). Divergent lineages in the heath mouse (Pseudomys shortridgei) are indicative of major contraction to geographically isolated refugia on the eastern and western sides of Australia during the early Pleistocene. Australian Journal of Zoology 57, 41–47.
| Divergent lineages in the heath mouse (Pseudomys shortridgei) are indicative of major contraction to geographically isolated refugia on the eastern and western sides of Australia during the early Pleistocene.Crossref | GoogleScholarGoogle Scholar |
Schmitt, L. H., and White, R. J. (1979). A comparison of metric and protein variation in the Australian bush-rat, Rattus fuscipes greyi. Australian Journal of Zoology 27, 547–559.
| A comparison of metric and protein variation in the Australian bush-rat, Rattus fuscipes greyi.Crossref | GoogleScholarGoogle Scholar |
Schodde, R. (1990). The bird fauna of the mallee – its biogeography and future. In ‘The Mallee Lands: a Conservation Perspective’. (Eds J. C. Noble, P. J. Joss and G. K. Jones.) pp. 61−70. (CSIRO: Melbourne.)
Stamatakis, A., Hoover, P., and Rougemont, J. (2008). Rapid bootstrap algorithm for the RAxML web-servers. Systematic Biology 57, 758–771.
| Rapid bootstrap algorithm for the RAxML web-servers.Crossref | GoogleScholarGoogle Scholar |
Start, A. N., Moro, D., Adams, M., and Bencini, R. (2006). Dunnarts from Boullanger Island: new evidence and reassessment of a taxonomic issue with resource implications. Australian Mammalogy 28, 51–58.
| Dunnarts from Boullanger Island: new evidence and reassessment of a taxonomic issue with resource implications.Crossref | GoogleScholarGoogle Scholar |
Swofford, D. L. (2002). PAUP*. ‘Phylogenetic Analysis Using Parsimony (* and Other Methods)’. Version 4.0b10. (Sinauer Associates: Sunderland, MA.)
Thackway, R., and Cresswell, I. D. (Eds) (1995). ‘An Interim Biogeographic Regionalization for Australia: a Framework for Establishing the National System of Reserves. Ver. 4.0’. (Australian Nature Conservation Agency: Canberra.) Version 6.1 available online at: http://www.environment.gov.au/parks/nrs/science/bioregion-framework/ibra/index.html
Thom, B. G., and Chappell, J. (1975). Holocene sea levels relative to Australia. Search 6, 90–93.
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., and Higgins, D. G. (1997). The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.
| The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXntFyntQ%3D%3D&md5=ebd43b5762d07b763aeebb1eaaa360f3CAS |
Turney, C. S. M., Bird, M. I., and Roberts, R. G. (2001). Elemental δ13C at Allen’s Cave, Nullarbor Plain, Australia: assessing post-depositional disturbance and reconstructing past environments. Journal of Quaternary Science 16, 779–784.
| Elemental δ13C at Allen’s Cave, Nullarbor Plain, Australia: assessing post-depositional disturbance and reconstructing past environments.Crossref | GoogleScholarGoogle Scholar |
Van Dyck, S., and Strahan, R. (2008). ‘The Mammals of Australia.’ 3rd edn. (Reed New Holland: Australia.)
Walshe, K. A. (1994). A taphonomic analysis of the vertebrate remains from Allen’s Cave: implications for Australian arid zone archaeology. Ph.D. Thesis, Australian National University, Canberra.
Watts, C. H. S., and Ling, J. K. (1985). Marine and terrestrial mammals. In ‘Natural History of Eyre Peninsula.’ (Eds C. R. Twidale, M. J. Tyler, and M. Davies.) pp. 139–147. (Royal Society of South Australia Inc.: Adelaide.)
Yang, Z. (1996). Among-site rate variation and its impact on phylogenetic analyses. Trends in Ecology & Evolution 11, 367–372.
| Among-site rate variation and its impact on phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itFGjtw%3D%3D&md5=93c599d43501d6a1ec221a87fb743a52CAS |
