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RESEARCH ARTICLE

Population structure of sexually reproducing carp gudgeons: does a metapopulation offer refuge from sexual parasitism?

Daniel J. Schmidt A C , Joel A. Huey A , Nick R. Bond A B and Jane M. Hughes A
+ Author Affiliations
- Author Affiliations

A Australian Rivers Institute, Griffith University, Nathan, Qld 4111, Australia.

B School of Biological Sciences, Monash University, Vic. 3800, Australia.

C Corresponding author. Email: d.schmidt@griffith.edu.au

Marine and Freshwater Research 64(3) 223-232 https://doi.org/10.1071/MF12305
Submitted: 22 October 2012  Accepted: 13 December 2012   Published: 18 March 2013

Abstract

Australian carp gudgeons (Hypseleotris spp.) of the Murray–Darling basin are a species complex including sexually reproducing taxa and unisexual hybrid lineages that reproduce via hybridogenesis. Unisexual fish require gametes of a sexual species to propagate themselves and can be regarded as ‘sexual parasites’ capable of driving closed populations to extinction. Metapopulation dynamics have been proposed as a mechanism that could facilitate coexistence between a sexual parasite and its ‘host’. This study evaluates whether patterns of spatial genetic variation are compatible with metapopulation dynamics for a sexually reproducing member of the carp gudgeon complex (Hypseleotris sp. HA), in the Granite Creeks system of central Victoria. Genetic differentiation of fish among all study sites was accommodated by a model of migration-drift equilibrium using decomposed pairwise regression analysis. Given that the population was divided into discrete patches in the form of refugial waterholes during the time of this study, we infer that spatially constrained source–sink metapopulation dynamics may be responsible for producing this pattern. It is therefore possible that metapopulation dynamics contribute to coexistence in the Granite Creeks carp gudgeon hybridogenetic system, and further analysis is required to determine the relative importance of environmental versus demographic factors towards patch extinction.

Additional keywords: asexual, Eleotridae, freshwater fish, hemiclone, hybridogenesis, Hypseleotris, microsatellite.


References

Abbott, J. K., and Morrow, E. H. (2011). Obtaining snapshots of genetic variation using hemiclonal analysis. Trends in Ecology & Evolution 26, 359–368.
Obtaining snapshots of genetic variation using hemiclonal analysis.Crossref | GoogleScholarGoogle Scholar |

Adams, M., Wedderburn, S. D., Unmack, P. J., Hammer, M. P., and Johnson, J. B. (2011). Use of congeneric assessment to reveal the linked genetic histories of two threatened fishes in the Murray–Darling basin, Australia. Conservation Biology 25, 767–776.
Use of congeneric assessment to reveal the linked genetic histories of two threatened fishes in the Murray–Darling basin, Australia.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MfgsVWnsQ%3D%3D&md5=faf60d292944f78b1526d10999e14a6eCAS |

Allen, G. R., Midgley, S. H., and Allen, M. (2002) ‘Field Guide to the Freshwater Fishes of Australia.’ (Western Australian Museum: Perth.)

Balcombe, S. R., and Closs, G. P. (2004). Spatial relationships and temporal variability in a littoral macrophyte fish assemblage. Marine and Freshwater Research 55, 609–617.
Spatial relationships and temporal variability in a littoral macrophyte fish assemblage.Crossref | GoogleScholarGoogle Scholar |

Balcombe, S. R., and Humphries, P. (2006). Diet of the western carp gudgeon (Hypseleotris klunzingeri Ogilby) in an Australian floodplain lake: the role of water level stability. Journal of Fish Biology 68, 1484–1493.
Diet of the western carp gudgeon (Hypseleotris klunzingeri Ogilby) in an Australian floodplain lake: the role of water level stability.Crossref | GoogleScholarGoogle Scholar |

Balcombe, S. R., Sheldon, F., Capon, S. J., Bond, N. R., Hadwen, W. L., Marsh, N., and Bernays, S. J. (2011). Climate-change threats to native fish in degraded rivers and floodplains of the Murray–Darling Basin, Australia. Marine and Freshwater Research 62, 1099–1114.
Climate-change threats to native fish in degraded rivers and floodplains of the Murray–Darling Basin, Australia.Crossref | GoogleScholarGoogle Scholar |

Bertozzi, T., Adams, M., and Walker, K. F. (2000). Species boundaries in carp gudgeons (Eleotrididae: Hypseleotris) from the River Murray, South Australia: evidence for multiple species and extensive hybridization. Marine and Freshwater Research 51, 805–815.
Species boundaries in carp gudgeons (Eleotrididae: Hypseleotris) from the River Murray, South Australia: evidence for multiple species and extensive hybridization.Crossref | GoogleScholarGoogle Scholar |

Beukeboom, L. W., and Vrijenhoek, R. C. (1998). Evolutionary genetics and ecology of sperm-dependent parthenogenesis. Journal of Evolutionary Biology 11, 755–782.
Evolutionary genetics and ecology of sperm-dependent parthenogenesis.Crossref | GoogleScholarGoogle Scholar |

Conallin, A. J., Hillyard, K. A., Walker, K. F., Gillanders, B. M., and Smith, B. B. (2011). Offstream movements of fish during drought in a regulated lowland river. River Research and Applications 27, 1237–1252.
Offstream movements of fish during drought in a regulated lowland river.Crossref | GoogleScholarGoogle Scholar |

Cook, B. D., Bunn, S. E., and Hughes, J. M. (2007). A comparative analysis of population structuring and genetic diversity in sympatric lineages of freshwater shrimp (Atyidae: Paratya): concerted or independent responses to hydrographic factors? Freshwater Biology 52, 2156–2171.
A comparative analysis of population structuring and genetic diversity in sympatric lineages of freshwater shrimp (Atyidae: Paratya): concerted or independent responses to hydrographic factors?Crossref | GoogleScholarGoogle Scholar |

DeWoody, J. A., and Avise, J. C. (2000). Microsatellite variation in marine, freshwater and anadromous fishes compared with other animals. Journal of Fish Biology 56, 461–473.
Microsatellite variation in marine, freshwater and anadromous fishes compared with other animals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXht1Khu7s%3D&md5=a4ac1c40893ac9bfa465a7cf6b0eccfbCAS |

Earl, D. A., and Vonholdt, B. M. (2012). STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4, 359–361.
STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method.Crossref | GoogleScholarGoogle Scholar |

Evanno, G., Regnaut, S., and Goudet, J. (2005). Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14, 2611–2620.
Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmvF2qtrg%3D&md5=940504aeb995dd3cf6a845153ac85f2dCAS |

Excoffier, L., Laval, G., and Schneider, S. (2005). Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1, 47–50.
| 1:CAS:528:DC%2BD28XjsFSltg%3D%3D&md5=a34b11451ded86925196f3b5d358655bCAS |

Falke, J. A., and Fausch, K. D. (2010) From metapopulations to metacommunities: linking theory with empirical observations of the spatial dynamics of stream fishes. In ‘Community Ecology of Stream Fishes’. (Eds K. B. Gido and D. A. Jackson.) pp. 457–471. (American Fisheries Society Symposium, 73: Bethesda.)

Faulks, L. K., Gilligan, D. M., and Beheregaray, L. B. (2010). Islands of water in a sea of dry land: hydrological regime predicts genetic diversity and dispersal in a widespread fish from Australia’s arid zone, the golden perch (Macquaria ambigua). Molecular Ecology 19, 4723–4737.
Islands of water in a sea of dry land: hydrological regime predicts genetic diversity and dispersal in a widespread fish from Australia’s arid zone, the golden perch (Macquaria ambigua).Crossref | GoogleScholarGoogle Scholar |

Gabor, C. R., Ryan, M. J., and Morizot, D. C. (2005). Character displacement in sailfin mollies, Poecilia latipinna: allozymes and behavior. Environmental Biology of Fishes 73, 75–88.
Character displacement in sailfin mollies, Poecilia latipinna: allozymes and behavior.Crossref | GoogleScholarGoogle Scholar |

Hanfling, B., and Weetman, D. (2006). Concordant genetic estimators of migration reveal anthropogenically enhanced source-sink population structure in the River Sculpin, Cottus gobio. Genetics 173, 1487–1501.
Concordant genetic estimators of migration reveal anthropogenically enhanced source-sink population structure in the River Sculpin, Cottus gobio.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XptVeitLY%3D&md5=0c33c9fb138f826580f771455ab53fa0CAS |

Hardy, C. M., Adams, M., Jerry, D. R., Court, L. N., Morgan, M. J., and Hartley, D. M. (2011). DNA barcoding to support conservation: species identification, genetic structure and biogeography of fishes in the Murray–Darling River Basin, Australia. Marine and Freshwater Research 62, 887–901.
DNA barcoding to support conservation: species identification, genetic structure and biogeography of fishes in the Murray–Darling River Basin, Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVOgu7jF&md5=0a68f4eab7faa5c1d2d63be86b6d18a7CAS |

Heubel, K. U., Rankin, D. J., and Kokko, H. (2009). How to go extinct by mating too much: population consequences of male mate choice and efficiency in a sexual-asexual species complex. Oikos 118, 513–520.

Hood, G. M. (2011). PopTools version 3.2.5. Available on the internet. URL http://www.poptools.org

Huey, J. A., Schmidt, D. J., Balcombe, S. R., Marshall, J. C., and Hughes, J. M. (2011). High gene flow and metapopulation dynamics detected for three species in a dryland river system. Freshwater Biology 56, 2378–2390.
High gene flow and metapopulation dynamics detected for three species in a dryland river system.Crossref | GoogleScholarGoogle Scholar |

Hughes, J. M., Schmidt, D. J., and Finn, D. S. (2009). Genes in streams: using DNA to understand the movement of freshwater fauna and their riverine habitat. Bioscience 59, 573–583.
Genes in streams: using DNA to understand the movement of freshwater fauna and their riverine habitat.Crossref | GoogleScholarGoogle Scholar |

Hughes, J. M., Real, K. M., Marshall, J. C., and Schmidt, D. J. (2012). Extreme genetic structure in a small-bodied freshwater fish, the purple spotted gudgeon, Mogurnda adspersa (Eleotridae). PLoS ONE 7, e40546.
Extreme genetic structure in a small-bodied freshwater fish, the purple spotted gudgeon, Mogurnda adspersa (Eleotridae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVOnsL3M&md5=541d331e918694a2138ea39fd203163aCAS |

Kerezsy, A., Balcombe, S. R., Arthington, A. H., and Bunn, S. E. (2011). Continuous recruitment underpins fish persistence in the arid rivers of far-western Queensland, Australia. Marine and Freshwater Research 62, 1178–1190.
Continuous recruitment underpins fish persistence in the arid rivers of far-western Queensland, Australia.Crossref | GoogleScholarGoogle Scholar |

King, A. J., Humphries, P., and Lake, P. S. (2003). Fish recruitment on floodplains: the roles of patterns of flooding and life history characteristics. Canadian Journal of Fisheries and Aquatic Sciences 60, 773–786.
Fish recruitment on floodplains: the roles of patterns of flooding and life history characteristics.Crossref | GoogleScholarGoogle Scholar |

Koizumi, I. (2011). Integration of ecology, demography and genetics to reveal population structure and persistence: a mini review and case study of stream-dwelling Dolly Varden. Ecology Freshwater Fish 20, 352–363.
Integration of ecology, demography and genetics to reveal population structure and persistence: a mini review and case study of stream-dwelling Dolly Varden.Crossref | GoogleScholarGoogle Scholar |

Koizumi, I., Yamamoto, S., and Maekawa, K. (2006). Decomposed pairwise regression analysis of genetic and geographic distances reveals a metapopulation structure of stream-dwelling Dolly Varden charr. Molecular Ecology 15, 3175–3189.
Decomposed pairwise regression analysis of genetic and geographic distances reveals a metapopulation structure of stream-dwelling Dolly Varden charr.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1Shu7%2FP&md5=144f2e4ddf452d4bf6410cd4847366cfCAS |

Kokko, H., and Heubel, K. U. (2011). Prudent males, group adaptation, and the tragedy of the commons. Oikos 120, 641–656.
Prudent males, group adaptation, and the tragedy of the commons.Crossref | GoogleScholarGoogle Scholar |

Kokko, H., Heubel, K. U., and Rankin, D. J. (2008). How populations persist when asexuality requires sex: the spatial dynamics of coping with sperm parasites. Proceedings. Biological Sciences 275, 817–825.
How populations persist when asexuality requires sex: the spatial dynamics of coping with sperm parasites.Crossref | GoogleScholarGoogle Scholar |

Lamatsch, D. K., and Stöck, M. (2009). Sperm-dependent parthenogenesis and hybridogenesis in teleost fishes. In ‘Lost Sex – The Evolutionary Biology of Parthenogenesis’. (Eds I. Schoen, K. Martens and P. van Dijk.) pp. 399–432. (Springer: Heidelberg.)

Lamy, T., Pointier, J. P., Jarne, P., and David, P. (2012). Testing metapopulation dynamics using genetic, demographic and ecological data. Molecular Ecology 21, 1394–1410.
Testing metapopulation dynamics using genetic, demographic and ecological data.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC383ptVejtA%3D%3D&md5=54e024dc5bd53b3e4427409c00c0d344CAS |

Larson, H. K. (2007). A new species of carp gudgeon, ‘Hypseleotris’ (Pisces: Gobioidei: Eleotridae), from the Katherine River system, Northern Territory. Beagle: Records of the Museums and Art Galleries of the Northern Territory 23, 111–117.

Larson, H. K., and Hoese, D. F. (1996). Family Gobiidae, subfamilies Eleotridinae and Butinae. Gudgeons. In ‘Freshwater Fishes of South-eastern Australia’. (Ed. R. M. McDowall.) pp. 200–219. (Reed Books: Sydney.)

Lehtonen, J., Jennions, M. D., and Kokko, H. (2012). The many costs of sex. Trends in Ecology & Evolution 27, 172–178.
The many costs of sex.Crossref | GoogleScholarGoogle Scholar |

Lehtonen, J., Schmidt, D. J., Heubel, K. U., and Kokko, H. (2013). Ecological and evolutionary implications of sexual parasitism. Trends in Ecology & Evolution , .
Ecological and evolutionary implications of sexual parasitism.Crossref | GoogleScholarGoogle Scholar |

Lisle, T. E. (1987). Using “residual depths” to monitor pool depths independently of discharge. (Ed. Do Agriculture.) (Forest Service, Pacific Southwest Forest and Range Experiment Station: Berkeley, CA.)

Lyon, J., Stuart, I., Ramsey, D., and O’Mahony, J. (2010). The effect of water level on lateral movements of fish between river and off-channel habitats and implications for management. Marine and Freshwater Research 61, 271–278.
The effect of water level on lateral movements of fish between river and off-channel habitats and implications for management.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjvFSjsL4%3D&md5=3b4fae27a7791494eab2b1ef5698e85fCAS |

Maynard Smith, J. (1978). ‘The Evolution of Sex.’ (Cambridge University Press: Cambridge.)

McMaster, D., and Bond, N. (2008). A field and experimental study on the tolerances of fish to Eucalyptus camaldulensis leachate and low dissolved oxygen concentrations. Marine and Freshwater Research 59, 177–185.
A field and experimental study on the tolerances of fish to Eucalyptus camaldulensis leachate and low dissolved oxygen concentrations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXisVWitLo%3D&md5=4b773e9a224b3fe8957f792c27335bb0CAS |

McNeil, D. G., and Closs, G. P. (2007). Behavioural responses of a south-east Australian floodplain fish community to gradual hypoxia. Freshwater Biology 52, 412–420.
Behavioural responses of a south-east Australian floodplain fish community to gradual hypoxia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjvFSit74%3D&md5=7c2cf003399bd495b3456cf2f6da99e9CAS |

Mee, J. A., and Otto, S. P. (2010). Variation in the strength of male mate choice allows long-term coexistence of sperm-dependent asexuals and their sexual hosts. Evolution 64, 2808–2819.

Meffe, G. K., and Vrijenhoek, R. C. (1988). Conservation genetics in the management of desert fishes. Conservation Biology 2, 157–169.
Conservation genetics in the management of desert fishes.Crossref | GoogleScholarGoogle Scholar |

Meirmans, P. G. (2006). Using the AMOVA framework to estimate a standardized genetic differentiation measure. Evolution 60, 2399–2402.

Meirmans, P. G., and Hedrick, P. W. (2011). Assessing population structure: F-ST and related measures. Molecular Ecology Resources 11, 5–18.
Assessing population structure: F-ST and related measures.Crossref | GoogleScholarGoogle Scholar |

Meredith, S. N., Matveev, V. F., and Mayes, P. (2003). Spatial and temporal variability in the distribution and diet of the gudgeon (Eleotridae: Hypseleotris spp.) in a subtropical Australian reservoir. Marine and Freshwater Research 54, 1009–1017.
Spatial and temporal variability in the distribution and diet of the gudgeon (Eleotridae: Hypseleotris spp.) in a subtropical Australian reservoir.Crossref | GoogleScholarGoogle Scholar |

Ning, N. S. P., Nielsen, D. L., Hillman, T. J., and Suter, P. J. (2010). The influence of planktivorous fish on zooplankton communities in riverine slackwaters. Freshwater Biology 55, 360–374.
The influence of planktivorous fish on zooplankton communities in riverine slackwaters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitlKnsLw%3D&md5=77e9cdd46b86c7deac606dc50ff1398bCAS |

Ning, N. S. P., Hladyz, S., Gawne, B., Maffei, S., Price, A., and Nielsen, D. L. (2012). Morphological, physiological and behavioural response patterns of carp gudgeon Hypseleotris spp. to food deprivation: implications for assessing health. Journal of Fish Biology 80, 218–224.
Morphological, physiological and behavioural response patterns of carp gudgeon Hypseleotris spp. to food deprivation: implications for assessing health.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC387itlKnsA%3D%3D&md5=8f748d0c78c391b06f3d33596f06e1d3CAS |

Perry, G. L. W., and Bond, N. R. (2009). Spatially explicit modeling of habitat dynamics and fish population persistence in an intermittent lowland stream. Ecological Applications 19, 731–746.
Spatially explicit modeling of habitat dynamics and fish population persistence in an intermittent lowland stream.Crossref | GoogleScholarGoogle Scholar |

Pritchard, J. K., Stephens, M., and Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics 155, 945–959.
| 1:STN:280:DC%2BD3cvislKrtA%3D%3D&md5=a651e5b2cca1da751d9a8c5053900888CAS |

Pulliam, H. R., Dunning, J. B., and Liu, J. (1992). Population dynamics in complex landscapes: a case study. Ecological Applications 2, 165–177.
Population dynamics in complex landscapes: a case study.Crossref | GoogleScholarGoogle Scholar |

Real, K. M., Schmidt, D. J., and Hughes, J. M. (2009). Mogurnda adspersa microsatellite markers: multiplexing and multi-tailed primer tagging. Conservation Genetics Resources 1, 411–414.
Mogurnda adspersa microsatellite markers: multiplexing and multi-tailed primer tagging.Crossref | GoogleScholarGoogle Scholar |

Rourke, M. L., McPartlan, H. C., Ingram, B. A., and Taylor, A. C. (2011). Variable stocking effect and endemic population genetic structure in Murray cod Maccullochella peelii. Journal of Fish Biology 79, 155–177.
Variable stocking effect and endemic population genetic structure in Murray cod Maccullochella peelii.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3Mnlt1ehtA%3D%3D&md5=bc691b696c032af07af598476bc63816CAS |

Schlupp, I. (2005). The evolutionary ecology of gynogenesis. Annual Review of Ecology Evolution and Systematics 36, 399–417.
The evolutionary ecology of gynogenesis.Crossref | GoogleScholarGoogle Scholar |

Schlupp, I. (2010). Mate choice and the Amazon Molly: how sexuality and unisexuality can coexist. The Journal of Heredity 101, S55–S61.
Mate choice and the Amazon Molly: how sexuality and unisexuality can coexist.Crossref | GoogleScholarGoogle Scholar |

Schmidt, D. J., Bond, N. R., Adams, M., and Hughes, J. M. (2011). Cytonuclear evidence for hybridogenetic reproduction in natural populations of the Australian carp gudgeon (Hypseleotris: Eleotridae). Molecular Ecology 20, 3367–3380.
Cytonuclear evidence for hybridogenetic reproduction in natural populations of the Australian carp gudgeon (Hypseleotris: Eleotridae).Crossref | GoogleScholarGoogle Scholar |

Schultz, R. J. (1969). Hybridization, unisexuality, and polyploidy in the teleost Poeciliopsis (Poeciliidae) and other vertebrates. American Naturalist 103, 605–619.
Hybridization, unisexuality, and polyploidy in the teleost Poeciliopsis (Poeciliidae) and other vertebrates.Crossref | GoogleScholarGoogle Scholar |

Stuart, I. G., Zampatti, B. P., and Baumgartner, L. J. (2008). Can a low-gradient vertical-slot fishway provide passage for a lowland river fish community? Marine and Freshwater Research 59, 332–346.
Can a low-gradient vertical-slot fishway provide passage for a lowland river fish community?Crossref | GoogleScholarGoogle Scholar |

Suk, H. Y., and Neff, B. D. (2009). Microsatellite genetic differentiation among populations of the Trinidadian guppy. Heredity 102, 425–434.
Microsatellite genetic differentiation among populations of the Trinidadian guppy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXkvVWmu74%3D&md5=6ae2adcdf018e5422bbb80fa0ed7340cCAS |

Thacker, C., and Unmack, P. J. (2005). Phylogeny and biogeography of the eleotrid genus Hypseleotris (Teleostei: Gobioidei: Eleotridae), with redescription of H-cyprinoides. Records of the Australian Museum 57, 1–13.
Phylogeny and biogeography of the eleotrid genus Hypseleotris (Teleostei: Gobioidei: Eleotridae), with redescription of H-cyprinoides.Crossref | GoogleScholarGoogle Scholar |

Thacker, C. E., Unmack, P. J., Matsui, L., and Rifenbark, N. (2007). Comparative phylogeography of five sympatric Hypseleotris species (Teleostei: Eleotridae) in south-eastern Australia reveals a complex pattern of drainage basin exchanges with little congruence across species. Journal of Biogeography 34, 1518–1533.
Comparative phylogeography of five sympatric Hypseleotris species (Teleostei: Eleotridae) in south-eastern Australia reveals a complex pattern of drainage basin exchanges with little congruence across species.Crossref | GoogleScholarGoogle Scholar |

Unmack, P. J. (2000). The genus Hypseleotris of southeastern Australia: its identification and breeding biology. Fishes of Sahul 14, 647–657.

Vrijenhoek, R. C. (1994). Unisexual fish: model systems for studying ecology and evolution. Annual Review of Ecology Evolution and Systematics 25, 71–96.
Unisexual fish: model systems for studying ecology and evolution.Crossref | GoogleScholarGoogle Scholar |

Williams, M. D., and Williams, W. D. (1991). Salinity tolerances of four species of fish from the Murray-Darling river system. Hydrobiologia 210, 145–150.
Salinity tolerances of four species of fish from the Murray-Darling river system.Crossref | GoogleScholarGoogle Scholar |

Woods, R. J., Macdonald, J. I., Crook, D. A., Schmidt, D. J., and Hughes, J. M. (2010). Contemporary and historical patterns of connectivity among populations of an inland river fish species inferred from genetics and otolith chemistry. Canadian Journal of Fisheries and Aquatic Sciences 67, 1098–1115.
Contemporary and historical patterns of connectivity among populations of an inland river fish species inferred from genetics and otolith chemistry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnsleit7w%3D&md5=d168f1425d600efeb24e4b5d922cff7bCAS |