Bivalves in a bottleneck: taxonomy, phylogeography and conservation of freshwater mussels (Bivalvia: Unionoida) in Australasia
- 911 Downloads
The conservation biology of Australasian freshwater mussels is hindered by lack of a taxonomic framework that employs molecular data as a complement to shell characters, larval forms and internal anatomy. The fauna includes more than 32 known species (30+ Hyriidae, 2 Unionidae), but has not been revised for 55 years, despite minor amendments. The hyriids are relics of Gondwana, represented in Australia and New Guinea by the ancestral Velesunioninae and in Australia and New Zealand by the Hyriinae (Tribe Hyridellini). Many taxonomic and phylogeographic issues await resolution, including the relationships between Australasian and South American species, and between Australian and New Zealand species, and the status of species in New Guinea (including uncertain reports of Unionidae) and the Solomon Islands. Once these are clarified, it will be easier to identify threatened species and evaluate the conservation status of the fauna. At present, only seven taxa are named in the IUCN Red List or under national/state legislation, and these are not representative. Threatening processes include altered flow regimes, catchment disturbances, salinisation, pollution and invasive species. While the need for a taxonomic revision is paramount, progress in conservation may depend also upon involving the wider community.
KeywordsUnionoida Hyriidae Unionidae Australia Papua New Guinea West Papua New Zealand Solomon Islands Sahul Taxonomy Biogeography Phylogeny Conservation Threatened species IUCN Red List EPBC Act Citizen science
We are grateful for support from Professor Maria Byrne, University of Sydney, postgraduate supervisor to HAJ, and Associate Professor Alan Lymbery, Dr. Stephen Beatty and Dr. David Morgan, Murdoch University, supervisors to MWK. Our thanks also to Dr. Bruce Marshall, Museum of New Zealand Te Papa Tongarewa, and Mr. Mark Fenwick, National Institute of Water and Atmospheric Research, Wellington, New Zealand, for advice about Echyridella, to Dr. Manuel Lopes Lima, Universidade do Porto, Portugal, for inviting us to contribute to the symposium in absentia, and to two reviewers for helpful advice.
- Abell, R., M. L. Thieme, C. Revenga, M. Bryer, M. Kottelat, N. Bogutskaya, B. Coad, N. Mandrak, S. Contreras Balderas, W. Bussing, M. L. J. Stiassny, P. Skelton, G. R. Allen, P. Unmack, A. Naseka, R. Ng, N. Sindorf, J. Robertson, E. Armijo, J. V. Higgins, T. J. Heibel, E. Wikramanayake, D. Olson, H. L. López, R. E. Reis, J. G. Lundberg, M. H. Sabaj Pérez & P. Petry, 2008. Freshwater ecoregions of the world: a new map of biogeographic units for freshwater biodiversity conservation. BioScience 58: 403–414.CrossRefGoogle Scholar
- Baker, A. M., F. Sheldon, J. Somerville, K. F. Walker & J. M. Hughes, 2004. Mitochondrial DNA phylogenetic structuring suggests similarity between two morphologically plastic genera of Australian freshwater mussels (Unionoida: Hyriidae). Molecular Phylogenetics and Evolution 32: 902–912.PubMedCrossRefGoogle Scholar
- Bauer, G. & K. Wächtler, 2001. Ecology and Evolution of the Freshwater Mussels Unionoida. Springer, Berlin: 394 pp.Google Scholar
- Bell, S., M. Marzano, J. Cent, H. Kobierska, D. Podjed, D. Vandzinskaite, H. Reinert, A. Armaitiene, M. Grodińska-Jurczak & R. Muršič, 2008. What counts? Volunteers and their organisations in the recording and monitoring of biodiversity. Biodiversity Conservation 17: 3443–3454.CrossRefGoogle Scholar
- Bieler, R., J. G. Carter & E. V. Coan, 2010. Nomenclator of bivalve families with a classification of bivalve families, Part 2: Classification of bivalve families. Malacologia 52: 113–153.Google Scholar
- Bogan, A. E. & W. R. Hoeh, 2000. On becoming cemented: evolutionary relationships among the genera in the freshwater bivalve family Etheriidae (Bivalvia: Unionoida). In Harper, E. M., J. D. Taylor & J. A. Crame (eds), The Evolutionary Biology of the Bivalvia. Geological Society: Special Publications, London: 159–168.Google Scholar
- Butterworth, J., 2008. Lake Rotokakahi: the kakahi (Hyridella menziesi) in a general framework of lake health. MSc (Biological Science) thesis, The University of Waikato, New Zealand.Google Scholar
- Byrne, M., 2000. Calcium concretions in the interstitial tissues of the Australian freshwater mussel Hyridella depressa (Hyriidae). In Harper, E. M., J. D. Taylor & J. A. Crame (eds), The Evolutionary Biology of the Bivalvia. Geological Society: Special Publications, London: 29–43.Google Scholar
- Carter, J. G., C. R. Altaba, L. C. Anderson, R. Araujo, A. S. Biakov, A. E. Bogan, D. C. Campbell, M. Campbell, J.-h. Chen, J. C. W. Cope, G. Delvene, H. H. Dijkstra, Z.-j. Fang, R. N. Gardner, V. A. Gavrilova, I. A. Goncharova, P. J. Harries, J. H. Hartman, M. Hautmann, W. R. Hoeh, J. Hylleberg, B.-y. Jiang, P. Johnston, L. Kirkendale, K. Kleemann, J. Koppka, J. Kříž, D. Machado, N. Malchus, A. Márquez-Aliaga, J.-P. Masse, C. A. McRoberts, P. U. Middelfart, S. Mitchell, L. A. Nevesskaja, S. Özer, J. Pojeta Jr., I. V. Polubotko, J. Maria Pons, S. Popov, T. Sánchez, A. F. Sartori, R. W. Scott, I. I. Sey, J. H. Signorelli, V. V. Silantiev, P. W. Skelton, T. Steuber, J. B. Waterhouse, G. L. Wingard & T. Yancey, 2011. A synoptical classification of the Bivalvia (Mollusca). Kansas University Paleontological Institute, Paleontological Contributions 4: 47 pp.Google Scholar
- Clearwater, S. J., S. A. Wood, N. R. Phillips, S. M. Parkyn, R. Van Ginkel & K. J. Thompson, 2012. Toxicity thresholds for juvenile freshwater mussels Echyridella menziesii and crayfish Paranephrops planifrons, after acute or chronic exposure to Microcystis sp. Environmental Toxicology. doi: 10.1002/tox.21774.
- Cummings, K. & D. Van Damme, 2011. Cucumerunio novaehollandiae. In IUCN Red List of Threatened Species, v. 2012.1 [available on internet at http://www.iucnredlist.org/details/189415/0] (March 2013).
- DEC, 2012. Current list of threatened and priority fauna rankings, Department of Environment and Conservation, Western Australia [available on internet at http://www.dec.wa.gov.au] (March 2013).
- Dell, R. K., 1953. The freshwater Mollusca of New Zealand, Part I: the genus Hyridella. Transactions of the Royal Society of New Zealand 81: 221–237.Google Scholar
- Downing, J. A., P. van Meter & D. A. Woolnough, 2010. Suspects and evidence: a review of the causes of extirpation and decline in freshwater mussels. Animal Biodiversity and Conservation 33: 151–185.Google Scholar
- DPIPWE, 2009. Status of fish communities and observations on South Esk freshwater mussel (Velesunio moretonicus) populations in the Macquarie River catchment upstream of Lake River. Water Assessment Aquatic Ecology Report Series, Report WA 09/02. Department of Primary Industries, Parks, Water and Environment, Tasmania: 78 pp.Google Scholar
- DSE, 2009. Advisory list of threatened invertebrate fauna in Victoria. Department of Sustainability and Environment, Victoria [available on internet at http://www.dse.vic.gov.au] (March 2013).
- DSEWPaC, 2012. Hyridella glenelgensis. In Species profile and threats database, Department of Sustainability, Environment, Water, Population and Communities, Canberra [available on internet at http://www.environment.gov.au/sprat] (March 2013).
- Fenwick, M. C., 2006. The molecular phylogenetics of the New Zealand freshwater mussels. MSc thesis, Victoria University of Wellington, New Zealand: 113 pp.Google Scholar
- Fenwick, M. C. & B. A. Marshall, 2006. A new species of Echyridella from New Zealand, and recognition of Echyridella lucasi (Suter, 1905) (Mollusca: Bivalvia: Hyriidae). Molluscan Research 26: 69–76.Google Scholar
- Flannery, T., 1998. Throwim Way Leg: An Adventure. Text Publishing, Melbourne: 326 pp.Google Scholar
- Graf, D. L., 2000. The Etherioidea revisited: a phylogenetic analysis of hyriid relationships (Mollusca: Bivalvia: Paleoheterodonta: Unionoida). Occasional Papers of the University of Michigan Museum of Zoology 729: 1–21.Google Scholar
- Graf, D. L. & D. Ó Foighil, 2000. Molecular phylogenetic analysis of 28S rDNA supports a Gondwanan origin for Australasian Hyriidae (Mollusca: Bivalvia: Unionoida). Vie et Milieu 50: 245–254.Google Scholar
- Haag, W., 2010. Past and future patterns of freshwater mussel extinctions in North America during the Holocene. In Turvey, S. T. (ed.), Holocene Extinctions. Oxford University Press, Oxford: 107–128.Google Scholar
- Heard, W. H. & R. H. Guckert, 1970. A re-evaluation of the recent Unionacea (Pelecypoda) of North America. Malacologia 10: 333–355.Google Scholar
- Hickey, C. W., S. J. Buckland, D. J. Hannah, D. S. Roper & K. Stuben, 1997. Polychlorinated biphenyls and organochlorine pesticides in the freshwater mussel Hyridella menziesi from the Waikato River, New Zealand. Bulletin of Environmental Contamination and Toxicology 59: 106–112.PubMedCrossRefGoogle Scholar
- Hitchmough, R., L. Bull & P. Cromarty, 2007. New Zealand threat classification system lists, 2005. Department of Conservation, Wellington: 194 pp.Google Scholar
- Hocknull, S. A., 2000. Mesozoic freshwater and estuarine bivalves from Australia. Memoirs of the Queensland Museum 45: 405–426.Google Scholar
- Hoeh, W. R., A. E. Bogan, K. S. Cummings & S. I. Guttman, 2002. Evolutionary relationships among the higher taxa of freshwater mussels (Bivalvia: Unionoida): inferences on phylogeny and character evolution from analyses of DNA sequence data. Malacological Review 31(32): 123–141.Google Scholar
- Humphrey, C. L., 1995. Reproduction in the freshwater mussel Velesunio angasi in response to the release of water from Ranger Uranium Mine to Magela Creek. Technical Memorandum 49, Supervising Scientist for the Alligator Rivers Region, Canberra.Google Scholar
- Iredale, T., 1934. The freshwater mussels of Australia. Australian Zoologist 8: 57–78.Google Scholar
- Iredale, T. & G. Whitley, 1938. The fluvifaunulae of Australia. South Australian Naturalist 18: 64–68.Google Scholar
- IUCN Standards & Petitions Subcommittee, 2011. Guidelines for using the IUCN red list categories and criteria, v. 9.0 [available on internet at http://www.iucnredlist.org/documents/RedListGuidelines.pdf] (March 2013).
- Jones, H. A., 2007. The influence of hydrology on freshwater mussel (Bivalvia: Hyriidae) distributions in a semi-arid river system, the Barwon-Darling River and intersecting streams. In Dickman, C. R., S. Burgin & D. Lunney (eds), Animals of Arid Australia: Out on their Own. Royal Zoological Society, Sydney: 132–142.CrossRefGoogle Scholar
- Jones, H. A., 2013. Landscape scale impacts on freshwater mussel (Unionoida: Hyriidae) distribution and status in southeastern Australia. PhD thesis, University of Sydney, New South Wales (in preparation).Google Scholar
- Jones, H. A. & M. Byrne, 2010. The impact of catastrophic channel change on freshwater mussels in the Hunter River system, Australia: a conservation assessment. Aquatic Conservation: Marine and Freshwater Ecosystems 20: 18–30.Google Scholar
- Jones, H. A. & M. Byrne, 2013. Changes in the distributions of freshwater mussels (Unionoida: Hyriidae) in coastal southeastern Australia and implications for their conservation status. Aquatic Conservation: Marine and Freshwater Ecosystems (in press).Google Scholar
- Jones, H. A., R. D. Simpson & C. L. Humphrey, 1986. The reproductive cycles and glochidia of freshwater mussels (Bivalvia: Hyriidae) of the Macleay River, northern New South Wales, Australia. Malacologia 27: 185–202.Google Scholar
- Kendrick, G. W., 1976. The Avon: faunal and other notes on a dying river in south-western Australia. The Western Australian Naturalist 13: 97–114.Google Scholar
- Klunzinger, M. W., 2012. Ecology, life history and conservation status of Westralunio carteri Iredale, 1934, an endemic freshwater mussel of south-western Australia. PhD thesis, Murdoch University, Western Australia.Google Scholar
- Klunzinger, M. W., S. J. Beatty, D. L. Morgan, G. J. Thompson & A. J. Lymbery, 2012a. Glochidia ecology in wild fish populations and laboratory determination of competent host fishes for an endemic freshwater mussel of south-western Australia. Australian Journal of Zoology 60: 26–36.CrossRefGoogle Scholar
- Klunzinger, M. W., S. J. Beatty, D. L. Morgan, A. J. Lymbery, A. M. Pinder & D. J. Cale, 2012b. Distribution of Westralunio carteri Iredale, 1934 (Bivalvia: Unionoida: Hyriidae) on the south coast of south-western Australia, including new records of the species. Journal of the Royal Society of Western Australia 95: 77–81.Google Scholar
- Klunzinger, M. W., S. J. Beatty, D. L. Morgan, G. J. Thomson & A. J. Lymbery, 2013a. Morphological and morphometrical description of the glochidia of Westralunio carteri Iredale, 1934 (Bivalvia: Unionoida: Hyriidae). Molluscan Research (in press). doi: 10.1080/13235818.2013.782791.
- Klunzinger, M. W., H. A. Jones, J. Keleher & D. L. Morgan, 2013b. A new record of Lortiella froggatti Iredale, 1934 (Bivalvia: Unionoida: Hyriidae) from the Pilbara region, Western Australia, with notes on anatomy and geographic range. Records of the Western Australian Museum (in press).Google Scholar
- Köhler, F., 2011. Westralunio carteri. In IUCN red list of threatened species, v. 2012.1 [available on internet at http://www.iucnredlist.org/details/23073/0] (March 2013).
- McMichael, D. F., 1956. Notes on the freshwater mussels of New Guinea. Nautilus 70: 38–48.Google Scholar
- McMichael, D. F., 1957. A review of the fossil freshwater mussels (Mollusca, Pelecypoda) of Australasia. Proceedings of the Linnean Society of New South Wales 81: 222–244.Google Scholar
- McMichael, D. F., 1958. The nature and origin of the New Zealand freshwater mussel fauna. Transactions of the Royal Society of New Zealand 85: 427–432.Google Scholar
- McMichael, D. F., 1967. Australian freshwater Mollusca and their probable evolutionary relationships: a summary of present knowledge. In Weatherley, A. H. (ed.), Australian Inland Waters and their Fauna: Eleven Studies. ANU Press, Canberra: 123–149.Google Scholar
- Morrongiello, J. R., S. J. Beatty, J. C. Bennett, D. A. Crook, D. N. E. N. Ikedife, M. J. Kennard, A. Kerezsy, M. Lintermans, D. G. McNeil, B. J. Pusey & T. Rayner, 2011. Climate change and its implications for Australia’s freshwater fish. Marine & Freshwater Research 62: 1082–1098.CrossRefGoogle Scholar
- Nobles, T. & Y. Zhang, 2011. Biodiversity loss in freshwater mussels: importance, threats, and solutions. In Grillo, O. & G. Verona (eds), Biodiversity Loss in a Changing Planet. INTECH, Rijeka: 19–48.Google Scholar
- O’Connor, S., K. Aplin, J. Pasveer & G. Hope, 2006. Liang Nabulei Lisa: a late Pleistocene and Holocene sequence from the Aru Islands. In O’Connor, S., P. M. Veth & M. Spriggs (eds), The Archaeology of the Aru Islands, Eastern Indonesia. ANU E Press, Canberra: 125–161.Google Scholar
- Ogilvie, S. C. & S. F. Mitchell, 1995. A model of mussel filtration in a shallow New Zealand lake, with reference to eutrophication control. Archiv für Hydrobiologie 133: 471–482.Google Scholar
- Parodiz, J. J., 1969. The tertiary non-marine mollusca of South America. Annals of the Carnegie Museum 40: 1–242.Google Scholar
- Parodiz, J. J. & A. A. Bonetto, 1963. Taxonomy and zoogeographic relationships of the South American naiades (Pelecypoda: Unionacea and Mutelacea). Malacologia 1: 179–214.Google Scholar
- Percival, E., 1931. A note on the life history of Diplodon lutulentus Gould. Transactions and Proceedings of the New Zealand Institute 62: 86–91.Google Scholar
- Polhemus, D. A. & G. R. Allen, 2007. Inland water ecosystems in Papua: classification, biota and threats. In Marshall, A. J. & B. M. Beehler (eds), The Ecology of Papua, Part 2. The Ecology of Indonesia Series. Periplus Editions (HK), Singapore: 858–900.Google Scholar
- Rainforth, H. J., 2008. Tiakina Kia Ora—protecting our freshwater mussels. MSc thesis, Victoria University of Wellington, New Zealand.Google Scholar
- Smith, B. J., 2005. Significant range extension for the freshwater mussel Hyridella (Hyridella) narracanensis in Tasmania. The Tasmanian Naturalist 127: 49–53.Google Scholar
- State of the Environment Committee, 2011. Australia: State of the Environment 2011. Independent Report to the Minister for Sustainability, Environment, Water, Population and Communities. DSEWPaC, Canberra: 932.Google Scholar
- Van Damme, D., 2011. Hyridella narracanensis, In IUCN red list of threatened species, v. 2012.1 [available on internet at http://www.iucnredlist.org/details/189387/0] (March 2013).
- Walker, K. F., 1981a. Ecology of freshwater mussels in the River Murray. Australian Water Resources Council Technical Paper 63, Canberra: 119.Google Scholar
- Walker, K. F., 1981b. The distribution of freshwater mussels (Mollusca, Pelecypoda) in the Australian Zoogeographic Region. In Keast, A. (ed.), Ecological Biogeography of Australia. Dr W. Junk, The Hague: 1233–1249.Google Scholar
- Walker, K. F., 2006. Serial weirs, cumulative effects: the Lower River Murray, Australia. In Kingsford, R. (ed.), The Ecology of Desert Rivers. Cambridge University Press, Cambridge : 248–279.Google Scholar
- Walker, K. F., T. J. Hillman & W. D. Williams, 1978. The effects of impoundments on rivers: an Australian case study. Verhandlungen der Internationalen Vereinigung für Theoretische und Angewandte Limnologie 20: 1695–1701.Google Scholar
- Wesselingh, F. P., A. Ranzi & M. E. Räsänen, 2006. Miocene freshwater Mollusca from western Brazilian Amazonia. Scripta Geologica 133: 419–437.Google Scholar
- Whittaker, R. J. & J. M. Fernández-Palacios, 2007. Island Biogeography: Ecology, Evolution and Conservation. Oxford University Press, Oxford: 416.Google Scholar
- Zieritz, A., 2010. Variability, function and phylogenetic significance of unionoid shell characters. PhD thesis, University of Cambridge, United Kingdom: 173.Google Scholar
- Zieritz, A., A. E. Bogan & D. C. Aldridge, 2013a. Reconstructing the evolution of umbonal sculptures in the Unionoida. Journal of Zoological Systematics and Evolutionary Research (in press).Google Scholar
- Zieritz, A, A. F. Sartori & M. W. Klunzinger, 2013b. Morphological evidence shows that not all Velesunioninae have smooth umbos. Journal of Molluscan Studies (in press).Google Scholar