Abstract
Many of Australia’s smaller marsupial species have been taxonomically described in just the past 50 years, and the Dasyuridae, a speciose family of carnivores, is known to harbour many cryptic taxa. Evidence from molecular studies is being increasingly utilised to help revise species boundaries and focus taxonomic efforts, and research over the past two decades has identified several undescribed genetic lineages within the dasyurid genus Planigale. Here, we describe two new species, Planigale kendricki sp. nov. (formerly known as ‘Planigale 1’) and P. tealei sp. nov. (formerly known as ‘Planigale sp. Mt Tom Price’). The two new species have broadly overlapping distributions in the Pilbara region of Western Australia. The new species are genetically distinct from each other and from all other members of the genus, at both mitochondrial and nuclear loci, and morphologically, in both external and craniodental characters. The new species are found in regional sympatry within the Pilbara but occupy different habitat types at local scales. This work makes a start at resolving the cryptic diversity within Planigale at a time when small mammals are continuing to decline throughout Australia.
References
- Adams, M., Raadik, T.A., Burridge, C.P. & Georges, A. (2014) Global biodiversity assessment and hyper-cryptic species complexes: more than one species of Elephant in the room? Systematic Biology, 63, 518–533. https://doi.org/10.1093/sysbio/syu017
- Aitken, P.F. (1972) Planigale gilesi (Marupialia, Dasyuridae); a new species from the interior of south eastern Australia. Records of the South Australian Museum, 16, 1–14.
- Australian Mammal Taxonomy Consortium. (2021) The AMTC Australian Mammal Species List. Version 1.0. Available from: https://australianmammals.org.au/publications/amtc-species-list (accessed 15 July 2022)
- Aplin, K.P., Rhind, S.G., Have, J.T. & Chesser, R.T. (2015) Taxonomic revision of Phascogale tapoatafa (Meyer, 1793) (Dasyuridae; Marsupialia), including descriptions of two new subspecies and confirmation of P. pirata Thomas, 1904 as a “Top End” endemic. Zootaxa, 4055 (1), 1–73. https://doi.org/10.11646/zootaxa.4055.1.1
- Archer, M. (1975) Ningaui, a new genus of tiny dasyurids (Marsupialia) and two new species, N. timealeyi and N. ridei, from arid Western Australia. Memoirs of the Queensland Museum, 17, 237–249.
- Archer, M. (1976a) Revision of the marsupial genus Planigale Troughton (Dasyuridae). Memoirs of the Queensland Museum, 17, 341–365.
- Archer, M. (1976b) The basicranial region of marsupicarnivores (Marsupialia), interrelationships of carnivorous marsupials, and affinities of the insectivorous marsupial peramelids. Zoological Journal of the Linnean Society, 59 (3), 217–322. https://doi.org/10.1111/j.1096-3642.1976.tb01016.x
- Archer, M. (1982) Review of the dasyurid (Marsupialia) fossil record, integration of data bearing on phylogenetic interpretation, and suprageneric classification. In: Archer, M. (Ed.), Carnivorous marsupials. Vol. 1. Royal Zoological Society of New South Wales, Sydney, pp. 397–443.
- Baker, A. & Dickman, C. (2018) Secret Lives of Carnivorous Marsupials. CSIRO Publishing, Clayton, 328 pp. https://doi.org/10.1071/9781486305155
- Baker, A., Mutton, T., Mason, E. & Gray, E. (2015) A taxonomic assessment of the Australian Dusky Antechinus complex: a new species, the Tasman Peninsula Dusky Antechinus (Antechinus vandycki sp. nov.) and an elevation to species of the Mainland Dusky Antechinus (Antechinus swainsonii mimetes (Thomas)). Memoirs of the Queensland Museum - Nature, 59, 75–126. https://doi.org/10.17082/j.2204-1478.59.2015.2014-10
- Beck, R.M.D., Voss, R.S. & Jansa, S.A. (2022) Craniodental morphology and phylogeny of marsupials. Bulletin of the American Museum of Natural History, 457, 1–350. https://doi.org/10.1206/0003-0090.457.1.1
- Benjamini, Y. & Hochberg, Y. (1995) Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society, Series B (Methodological), 57, 289–300. https://doi.org/10.1111/j.2517-6161.1995.tb02031.x
- Berner, D. (2011) Size correction in biology: how reliable are approaches based on (common) principal component analysis? Oecologia, 166, 961–971. https://doi.org/10.1007/s00442-011-1934-z
- Blacket, M.J., Adams, M., Krajewski, C. & Westerman, M. (2000) Genetic variation within the dasyurid marsupial genus Planigale. Australian Journal of Zoology, 48 (5), 443–449. https://doi.org/10.1071/ZO00020
- Blacket, M.J., Krajewski, C., Labrinidis, A., Cambron, B., Cooper, S. & Westerman, M. (1999) Systematic relationships within the dasyurid marsupial tribe Sminthopsini - a multigene approach. Molecular Phylogenetics and Evolution, 12 (2), 140–155. https://doi.org/10.1006/mpev.1998.0604
- Burgin, C.J., Colella, J.P., Kahn, P.L. & Upham, N.S. (2018) How many species of mammals are there? Journal of Mammalogy, 99 (1), 1–14. https://doi.org/10.1093/jmammal/gyx147
- Buuren, S. van & Groothuis-Oudshoorn, K. (2011) mice: Multivariate imputation by chained equations in R. Journal of Statistical Software, 45 (3), 1–67. https://doi.org/10.18637/jss.v045.i03
- Büyüköztürk, Þ. & Çokluk-Bökeoðlu, Ö. (2008) Discriminant function analysis: Concept and application. Egitim Arastirmalari - Eurasian Journal of Educational Research, 33, 73–92.
- Cooper, N.K., Withers, P.C. & Stewart, T. (2005) Description of sternal glands in Western Australian Sminthopsis and Ningaui (marsupialia: Dasyuridae). Journal of the Royal Society of Western Australia, 88, 45–49.
- Cremona, T., Banks, S.C., Davies, H.F., Geyle, H.M., Penton, C.E., Stobo-Wilson, A.M., von Takach, B., Trewella, G.J. & Murphy, B.P. (2022) On the brink of extinction: the small mammal decline in northern Australia. In: DellaSala, D.A. & Goldstein, M.I. (Eds.), Imperiled: The Encyclopedia of Conservation. Elsevier, Oxford, pp. 245–252. https://doi.org/10.1016/B978-0-12-821139-7.00143-4
- De Queiroz, K. (2007) Species concepts and species delimitation. Systematic Biology, 56 (6), 879–886. https://doi.org/10.1080/10635150701701083
- Department of Climate Change, Energy, Environment and Water (2022) Threatened Species List. EPBC Act List of Threatened Fauna. Available from: https://www.environment.gov.au/cgi-bin/sprat/public/publicthreatenedlist.pl (accessed 5 February 2023)
- Doughty, P., Rolfe, J.K., Burbidge, A.H., Pearson, D.J. & Kendrick, P.G. (2011) Herpetological assemblages of the Pilbara biogeographic region, Western Australia: ecological associations, biogeographic patterns and conservation. Records of the Western Australian Museum Supplement, 78, 315–341. https://doi.org/10.18195/issn.0313-122x.78(2).2011.315-341
- Gibson, L.A. & McKenzie, N.L. (2009) Environmental associations of small ground-dwelling mammals in the Pilbara region, Western Australia. Records of the Western Australian Museum Supplement, 78, 91–122. https://doi.org/10.18195/issn.0313-122x.78(1).2009.091-122
- Gill, T. (1872) Arrangement of the families of mammals with analytical tables. Smithsonian Miscellaneous Collections, 11, 1–98. https://doi.org/10.5962/bhl.title.14607
- Goldfuss, G.A. (1820) Handbuch der zoologie. J. L. Schrag, Nürnberg, 748 pp.
- Gould, J. (1851) s.n. In: The Mammals of Australia. Pt. 3. J. Gould, London, pl. 13 and txt.
- Hohnen, R., Tuft, K.D., Legge, S., Hillyer, M., Spencer, P.B.S., Radford, I.J., Johnson, C.N. & Burridge, C.P. (2016) Rainfall and topography predict gene flow among populations of the declining northern quoll (Dasyurus hallucatus). Conservation Genetics, 17, 1213–1228. https://doi.org/10.1007/s10592-016-0856-z
- Johnstone, R.E., Burbidge, A. & Darnell, J. (2013) Birds of the Pilbara region, including seas and offshore islands, Western Australia: distribution, status and historical changes. Records of the Western Australian Museum Supplement, 78, 343–441. https://doi.org/10.18195/issn.0313-122x.78(2).2013.343-441
- Jolicoeur, P. (1963) 193. Note: The multivariate generalization of the allometry equation. Biometrics, 19 (3), 497–499. https://doi.org/10.2307/2527939
- Jolliffe, I.T. (2002) Principal Component Analysis, Second Edition. Springer-Verlag, New York, New York, 487 pp.
- Katoh, K., Misawa, K., Kuma, K. & Miyata, T. (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic acids research, 30, 3059–3066. https://doi.org/10.1093/nar/gkf436
- Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P. & Drummond, A. (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28 (12), 1647–1649. https://doi.org/10.1093/bioinformatics/bts199
- Krajewski, C., Driskell, A.C., Baverstock, P.R. & Braun, M.J. (1997a) Phylogenetic relationships of the thylacine (Mammalia: Thylacinidae) among dasyuroid marsupials: evidence from cytochrome b DNA sequences. Proceedings of the Royal Society of London. Series B: Biological Sciences, 250 (1327), 19–27. https://doi.org/10.1098/rspb.1992.0125
- Krajewski, C. & Westerman, M. (2003) Molecular systematics of Dasyuromorphia. In: Jones, M., Dickman, C. & Archer, M. (Eds.), Predators with Pouches. CSIRO Publishing, Collingwood, Victoria, pp. 3–20.
- Krajewski, C., Woolley, P.A. & Westerman, M. (2000) The evolution of reproductive strategies in dasyurid marsupials: implications of molecular phylogeny. Biological Journal of the Linnean Society, 71 (3), 417–435. https://doi.org/10.1111/j.1095-8312.2000.tb01267.x
- Krajewski, C., Young, J., Buckley, L., Woolley, P.A. & Westerman, M. (1997b) Reconstructing the evolutionary radiation of dasyurine marsupials with cytochrome b, 12S rRNA, and protamine P1 gene trees. Journal of Mammalian Evolution, 4, 217–236. https://doi.org/10.1023/A:1027349725642
- Lavery, T.H., Collett, R., Fisher, D.O., Hoskin, C.J. & Rowland, J. (2022) White-footed dunnarts (Sminthopsis leucopus) in Queensland’s Wet Tropics, with the description of a new subspecies. Australian Mammalogy, 45 (1), 77–90. https://doi.org/10.1071/AM22002
- Luckett, W.P. (1993) An ontogenetic assessment of dental homologies in therian mammals. In: Szalay, F.S., Novacek, M.J. & McKenna, M.C. (Eds.), Mammal Phylogeny: Mesozoic Differentiation, Multituberculates, Monotremes, Early Therians, and Marsupials. Springer-Verlag, New York, New York, pp. 192–204. https://doi.org/10.1007/978-1-4613-9249-1_13
- Menkhorst, P. & Knight, F. (2004) A Field Guide to the Mammals of Australia. Oxford University Press, Melbourne, 296 pp.
- Mitchell, K.J., Pratt, R.C., Watson, L.N., Gibb, G.C., Llamas, B., Kasper, M., Edson, J., Hopwood, B., Male, D., Armstrong, K.N., Meyer, M., Hofreiter, M., Austin, J., Donnellan, S.C., Lee, M.S.Y., Phillips, M.J. & Cooper, A. (2014) Molecular phylogeny, biogeography, and habitat preference evolution of marsupials. Molecular Biology and Evolution, 31 (9), 2322–2330. https://doi.org/10.1093/molbev/msu176
- Mosimann, J.E. (1970) Size allometry: size and shape variables with characterizations of the lognormal and generalized gamma distributions. Journal of the American Statistical Association, 65, 930–945. https://doi.org/10.2307/2284599
- Oksanen, J., Simpson, G., Blanchet, F., Kindt, R., Legendre, P., Minchin, P., O'Hara, R., Solymos, P., Stevens, M., Szoecs, E., Wagner, H., Barbour, M., Bedward, M., Bolker, B., Borcard, D., Carvalho, G., Chirico, M., De Caceres, M., Durand, S., Evangelista, H., FitzJohn, R., Friendly, M., Furneaux, B., Hannigan, G., Hill, M., Lahti, L., McGlinn, D., Ouellette, M., Ribeiro Cunha, E., Smith, T., Stier, A., Ter Braak, C. & Weedon, J. (2022) Vegan: Community Ecology Package. R Package Version 2.6-2. Available from: https://CRAN.R-project.org/package=vegan (accessed 18 July 2023)
- Onley, I.R., Moseby, K.E., Austin, J.J. & Sherratt, E. (2022) Morphological variation in skull shape and size across extinct and extant populations of the greater stick-nest rat (Leporillus conditor): implications for translocation. Australian Mammalogy, 44 (3), 352–363. https://doi.org/10.1071/AM21047
- Painter, J., Krajewski, C. & Westerman, M. (1995) Molecular phylogeny of the marsupial genus Planigale (Dasyuridae). Journal of Mammalogy, 76 (2), 406–413. https://doi.org/10.2307/1382351
- Pavón-Vázquez, C.J., Brennan, I.G., Skeels, A. & Keogh, J.S. (2022) Competition and geography underlie speciation and morphological evolution in Indo-Australasian monitor lizards. Evolution, 76, 476–495. https://doi.org/10.1111/evo.14403
- Pepper, M., Doughty, P. & Keogh, J.S. (2013) Geodiversity and endemism in the iconic Australian Pilbara region: a review of landscape evolution and biotic response in an ancient refugium. Journal of Biogeography, 40, 1225–1239. https://doi.org/10.1111/jbi.12080
- R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available from: http://www.R-project.org/ (accessed 18 July 2023)
- Read, D.G. (1984) Reproduction and breeding season of Planigale gilesi and P. tenuirostris (Marsupialia: Dasyuridae). Australian Mammalogy, 7 (3), 161–173. https://doi.org/10.1071/AM84017
- Read, D.G. (1987) Habitat use by Sminthopsis crassicaudata, Planigale gilesi and Planigale tenuirostris (Marsupialia, Dasyuridae) in semiarid New South Wales. Wildlife Research, 14 (4), 385–395. https://doi.org/10.1071/wr9870385
- Richardson, B.J., Baverstock, P.R. & Adams, M. (1986) Allozyme electrophoresis: a handbook for animal systematics and population studies. Academic Press, Sydney, 410 pp. https://doi.org/10.1016/B978-0-12-587840-1.50009-5
- Ride, W.D.L. (1970) A guide to the native mammals of Australia. Oxford University Press, Melbourne, 249 pp.
- Šlenker, M., Koutecký, P. & Marhold, K. (2022) MorphoTools2: an R package for multivariate morphometric analysis. Bioinformatics, 38 (10), 2954–2955. https://doi.org/10.1093/bioinformatics/btac173
- Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22 (21), 2688–2690. https://doi.org/10.1093/bioinformatics/btl446
- Strahan, R. (Ed.) (1995) Mammals of Australia. Smithsonian Institution Press, Washington, D.C., 756 pp.
- von Takach, B., Ranjard, L., Burridge, C.P., Cameron, S.F., Cremona, T., Eldridge, M.D.B., Fisher, D.O., Frankenberg, S., Hill, B.M., Hohnen, R., Jolly, C.J., Kelly, E., MacDonald, A.J., Moussalli, A., Ottewell, K., Phillips, B.L., Radford, I.J., Spencer, P.B.S., Trewella, G.J., Umbrello, L.S. & Banks, S.C. (2022) Population genomics of a predatory mammal reveals patterns of decline and impacts of exposure to toxic toads. Molecular Ecology, 31, 5468–5486. https://doi.org/10.1111/mec.16680
- Tate, G.H.H. & Archbold, R. (1941) New rodents and marsupials from New Guinea. American Museum novitates, 1101, 1–9.
- Thomas, O. (1906) On a collection of mammals made by Mr. W. Stalker in the Northern Territory of South Australia, and presented to the National Museum by Sir William Ingram, Bart., and the Hon. John Forrest. Abstract of the Proceedings of the Zoological Society of London, 32, 6.
- Troughton, E.L.G. (1928) A new genus, species, and subspecies of marsupial mice (family Dasyuridae). Records of the Australian Museum, 16 (6), 281–288. https://doi.org/10.3853/J.0067-1975.16.1928.789
- Umbrello, L. (2018) Evolution and diversification of dasyurid marsupials of the Australian arid zone. Doctoral Thesis, The University of Western Australia, Perth, xvi + 187 pp. https://doi.org/10.26182/5ca6cffb21fc6
- Umbrello, L.S., Didham, R.K., How, R.A. & Huey, J.A. (2020) Multi-Species phylogeography of arid-zone Sminthopsinae (Marsupialia: Dasyuridae) reveals evidence of refugia and population expansion in response to Quaternary change. Genes, 11 (9), 963. https://doi.org/10.3390/genes11090963
- Unmack, P.J., Adams, M., Hammer, M.P., Johnson, J.B., Gruber, B., Gilles, A., Young, M. & Georges, A. (2022) Plotting for change: an analytical framework to aid decisions on which lineages are candidate species in phylogenomic species discovery. Biological Journal of the Linnean Society, 135 (1), 117–137. https://doi.org/10.1093/biolinnean/blab095
- Van Dyck, S. & Strahan, R. (Eds.) (2008) The Mammals of Australia. Reed New Holland, Sydney, 887 pp.
- Van Dyck, S., Woinarski, J.C.Z. & Press, A.J. (1994) The Kakadu dunnart Sminthopsis bindi (Marsupialia: Dasyuridae), a new species from the stony woodlands of the Northern Territory. Memoirs of the Queensland Museum, 37, 311–323.
- Viacava, P., Baker, A.M., Blomberg, S.P., Phillips, M.J. & Weisbecker, V. (2022) Using 3D geometric morphometrics to aid taxonomic and ecological understanding of a recent speciation event within a small Australian marsupial (Antechinus: Dasyuridae). Zoological Journal of the Linnean Society, 196 (3), 963–978. https://doi.org/10.1093/zoolinnean/zlab048
- Viacava, P., Blomberg, S.P. & Weisbecker, V. (2023) The relative performance of geometric morphometrics and linear-based methods in the taxonomic resolution of a mammalian species complex. Ecology and Evolution, 13, e9698. https://doi.org/10.1002/ece3.9698
- Westerman, M., Blacket, M.J., Hintz, A., Armstrong, K., Woolley, P.A. & Krajewski, C. (2016) A plethora of planigales: genetic variability and cryptic species in a genus of dasyurid marsupials from northern Australia. Australian Journal of Zoology, 64 (5), 303–311. https://doi.org/10.1071/ZO16052
- Westerman, M., Umbrello, L. & Woolley, P.A. (2023) On the composition of Antechinomys (Marsupialia: Dasyuridae): how many species? Australian Journal of Zoology, 70 (3), 95–103. https://doi.org/10.1071/ZO22041
- Williams, B.K. & Titus, K. (1988) Assessment of sampling stability in ecological applications of discriminant analysis. Ecology, 69, 1275–1285. https://doi.org/10.2307/1941283
- Woinarski, J.C.Z., Burbidge, A.A. & Harrison, P.L. (2015) Ongoing unravelling 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 (15), 4531–40. https://doi.org/10.1073/pnas.1417301112
- Woinarski, J.C.Z., Legge, S., Fitzsimons, J.A., Traill, B.J., Burbidge, A.A., Fisher, A., Firth, R.S.C., Gordon, I.J., Griffiths, A.D., Johnson, C.N., McKenzie, N.L., Palmer, C., Radford, I., Rankmore, B., Ritchie, E.G., Ward, S. & Ziembicki, M. (2011) The disappearing mammal fauna of northern Australia: context, cause, and response. Conservation Letters, 4, 192–201. https://doi.org/10.1111/j.1755-263X.2011.00164.x
- Woolley, P. (1974) The pouch of Planigale subtilissima and other dasyurid marsupials. Journal of the Royal Society of Western Australia, 57, 11–15.