Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Connectivity of the seagrass Zostera muelleri within south-eastern Australia

R. E. Stafford-Bell A E , W. F. D. van Dongen B , R. W. Robinson C and A. A. Chariton D
+ Author Affiliations
- Author Affiliations

A Department of Jobs, Precincts and Regions, 475 Mickleham Road, Attwood, Vic. 3049, Australia.

B School of Life and Environmental Sciences, Deakin University, 221 Burwood Highway, Burwood, Vic. 3125, Australia.

C Institute for Sustainable Industries and Liveable Cities, Victoria University, PO Box 14428, Melbourne, Vic. 8001, Australia.

D Department of Biological Sciences, Macquarie University, Balaclava Road, Macquarie Park, NSW 2109, Australia.

E Corresponding author. Email: richard.stafford-bell@djpr.vic.gov.au

Marine and Freshwater Research 70(8) 1056-1064 https://doi.org/10.1071/MF18333
Submitted: 4 September 2018  Accepted: 7 January 2019   Published: 25 March 2019

Abstract

Contemporary oceanic conditions and local dispersal of propagules influence the genetic diversity and connectivity among seagrass populations. The degree of connectivity between populations of Zostera muelleri in south-eastern Australia is unknown. In this study we examined genetic connectivity among 25 sites containing Z. muelleri using nine polymorphic microsatellite DNA loci. We hypothesised minimal sharing of genetic material between distant populations and a degree of connectivity between local populations. Genotypic diversity was high, with 64% of populations having unique multilocus genotypes (MLGs), indicating the importance of sexual reproduction. Two sites shared MLGs, which may be due to the dispersal and recruitment of vegetative propagules. Genetic differentiation was observed between most sites. With the exception of two outlying sites, two genetic population clusters were identified across the studied populations. Regionally, the populations have high clonal diversity, are strongly differentiated and generally exist in isolation from one another. However, non-significant within-estuary differentiation was observed for three estuaries, indicating a degree of connectivity. The results of this research improve our understanding of the connectivity of Z. muelleri populations in the region, an important process for managing this ecosystem engineer.

Additional keywords: clonal diversity, microsatellite.


References

Ackerman, J. D. (1997). Submarine pollination in the marine angiosperm Zostera marina (Zosteraceae). II. Pollen transport in flow fields and capture by stigmas. American Journal of Botany 84, 1110–1119.
Submarine pollination in the marine angiosperm Zostera marina (Zosteraceae). II. Pollen transport in flow fields and capture by stigmas.Crossref | GoogleScholarGoogle Scholar |

Ackerman, J. D. (2006). Sexual reproduction of seagrasses: Pollination in the marine context. In ‘Seagrasses: Biology, Ecology and Conservation’. (Eds A. W. D. Larkhum, R. J. Orth, and C. M. Carlos.) pp. 89–109. (Springer: Dordrecht, Netherlands.)

Aguilar, R., Quesada, M., Ashworth, L., Herrerias-Diego, Y., and Lobo, J. (2008). Genetic consequences of habitat fragmentation in plant populations: susceptible signals in plant traits and methodological approaches. Molecular Ecology 17, 5177–5188.
Genetic consequences of habitat fragmentation in plant populations: susceptible signals in plant traits and methodological approaches.Crossref | GoogleScholarGoogle Scholar | 19120995PubMed |

Arnaud-Haond, S., Duarte, C. M., Alberto, F., and Serrão, E. A. (2007). Standardizing methods to address clonality in population studies. Molecular Ecology 16, 5115–5139.
Standardizing methods to address clonality in population studies.Crossref | GoogleScholarGoogle Scholar | 17944846PubMed |

Berković, B., Cabaco, S., Barrio, J. M., Santos, R., Serrão, E. A., and Alberto, F. (2014). Extending the life history of a clonal aquatic plant: dispersal potential of sexual and asexual propagules of Zostera noltii. Aquatic Botany 113, 123–129.
Extending the life history of a clonal aquatic plant: dispersal potential of sexual and asexual propagules of Zostera noltii.Crossref | GoogleScholarGoogle Scholar |

Bird, E. C. F. (Ed.) (2010). Victoria: the Port Campbell coast (Mepunga to Princetown). In ‘Encyclopedia of the World’s Coastal Landforms’. pp. 1319–1324. (Springer: Dordrecht, Netherlands.)

Bos, A. R., Bouma, T. J., de Kort, G. L. J., and van Katwijk, M. M. (2007). Ecosystem engineering by annual intertidal seagrass beds: sediment accretion and modification. Estuarine, Coastal and Shelf Science 74, 344–348.
Ecosystem engineering by annual intertidal seagrass beds: sediment accretion and modification.Crossref | GoogleScholarGoogle Scholar |

Boutin-Ganache, I., Raposo, M., Raymond, M., and Deschepper, C. F. (2001). M13-tailed primers improve the readability and usability of microsatellite analyses performed with two different allele-sizing methods. BioTechniques 31, 25–28.
M13-tailed primers improve the readability and usability of microsatellite analyses performed with two different allele-sizing methods.Crossref | GoogleScholarGoogle Scholar |

Bradshaw, W. E., and Holzapfel, C. M. (2006). Evolutionary response to rapid climate change. Science 312, 1477–1478.
Evolutionary response to rapid climate change.Crossref | GoogleScholarGoogle Scholar | 16763134PubMed |

Cowen, R. K., Paris, C. B., and Srinivasan, A. (2006). Scaling of connectivity in marine populations. Science 311, 522–527.
Scaling of connectivity in marine populations.Crossref | GoogleScholarGoogle Scholar | 16357224PubMed |

Dawson, M. N. (2005). Incipient speciation of Catostylus mosaicus (Scyphozoa, Rhizostomeae, Catostylidae), comparative phylogeography and biogeography in south‐east Australia. Journal of Biogeography 32, 515–533.
Incipient speciation of Catostylus mosaicus (Scyphozoa, Rhizostomeae, Catostylidae), comparative phylogeography and biogeography in south‐east Australia.Crossref | GoogleScholarGoogle Scholar |

Di Carlo, G., Badalamenti, F., Jensen, A., Koch, E., and Riggio, S. (2005). Colonisation process of vegetative fragments of Posidonia oceanica (L.) Delile on rubble mounds. Marine Biology 147, 1261–1270.
Colonisation process of vegetative fragments of Posidonia oceanica (L.) Delile on rubble mounds.Crossref | GoogleScholarGoogle Scholar |

Dorken, M. E., and Eckert, C. G. (2001). Severely reduced sexual reproduction in northern populations of a clonal plant, Decodon verticillatus (Lythraceae). Journal of Ecology 89, 339–350.
Severely reduced sexual reproduction in northern populations of a clonal plant, Decodon verticillatus (Lythraceae).Crossref | GoogleScholarGoogle Scholar |

Edgar, G. J., Mukai, H., and Orth, R. J. (2001). Fish, crabs, shrimp and other large mobile epibenthos: measurement and methods for their biomass and abundance in seagrass. In ‘Global Seagrass Research Methods’. (Eds F. T. Short and R. G. Coles.) pp. 255–270. (Springer: Dordrecht, Netherlands.)

Einfeldt, A., and Addison, J. (2013). Hydrology influences population genetic structure and connectivity of the intertidal amphipod Corophium volutator in the northwest Atlantic. Marine Biology 160, 1015–1027.
Hydrology influences population genetic structure and connectivity of the intertidal amphipod Corophium volutator in the northwest Atlantic.Crossref | GoogleScholarGoogle Scholar |

Erftemeijer, P. L., Lewis, R., and Roy, R. (2006). Environmental impacts of dredging on seagrasses: a review. Marine Pollution Bulletin 52, 1553–1572.
Environmental impacts of dredging on seagrasses: a review.Crossref | GoogleScholarGoogle Scholar | 17078974PubMed |

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 | 15969739PubMed |

Frankham, R., Briscoe, D. A., and Ballou, J. D. (2002). ‘Introduction to Conservation Genetics.’ (Cambridge University Press: Cambridge, UK.)

Hanski, I. A., and Simberloff, D. (1997). The metapopulation approach, its history, conceptual domain and application to conservation. In ‘Metapopulation Biology: Ecology, Genetics and Evolution’. (Eds I. A. Hanski and M. E. Gilpin.) pp. 5–26. (Academic Press: New York, NY, USA.)

Harrison, S., Black, K., and Greer, D. (2008). ‘Description of Bass Strait physical and Geological Marine Environment.’ (ASR Ltd: Raglan, New Zealand.)

Hartl, D. L., and Clark, A. G. (2007). ‘Principles of Population Genetics.’ (Sinauer Associates: Sunderland, MA, USA.)

Hedrick, P. W. (2005). Evolution 59, 1633–1638.
Crossref | GoogleScholarGoogle Scholar | 16329237PubMed |

Hemminga, M. A., and Duarte, C. M. (2000). ‘Seagrass Ecology.’ (Cambridge University Press: Cambridge, UK.)

Hernández‐Carmona, G., Hughes, B., and Graham, M. H. (2006). Reproductive longevity of drifting kelp Macrocystis pyrifera (Phaeophyceae) in Monterey Bay, USA. Journal of Phycology 42, 1199–1207.
Reproductive longevity of drifting kelp Macrocystis pyrifera (Phaeophyceae) in Monterey Bay, USA.Crossref | GoogleScholarGoogle Scholar |

Hughes, R., and Stachowicz, J. J. (2004). Genetic diversity enhances the resistance of a seagrass ecosystem to disturbance. Proceedings of the National Academy of Sciences of the United States of America 101, 8998–9002.
Genetic diversity enhances the resistance of a seagrass ecosystem to disturbance.Crossref | GoogleScholarGoogle Scholar |

Inglis, G. J., and Waycott, M. (2001). Methods for assessing seagrass seed ecology and population genetics. In ‘Global Seagrass Research Methods’. (Eds F. T. Short and R. G. Coles.) pp. 123–140. (Elsevier Science: Amsterdam, Netherlands.)

Jenkins, G. P., Black, K. P., and Hamer, P. A. (2000). Determination of spawning areas and larval advection pathways for King George whiting in southeastern Australia using otolith microstructure and hydrodynamic modelling. I. Victoria. Marine Ecology Progress Series 199, 231–242.
Determination of spawning areas and larval advection pathways for King George whiting in southeastern Australia using otolith microstructure and hydrodynamic modelling. I. Victoria.Crossref | GoogleScholarGoogle Scholar |

Jones, T. C., Gemmill, C. E. C., and Pilditch, C. A. (2008). Genetic variability of New Zealand seagrass (Zostera muelleri) assessed at multiple spatial scales. Aquatic Botany 88, 39–46.
Genetic variability of New Zealand seagrass (Zostera muelleri) assessed at multiple spatial scales.Crossref | GoogleScholarGoogle Scholar |

Jost, L. (2008). GST and its relatives do not measure differentiation. Molecular Ecology 17, 4015–4026.
GST and its relatives do not measure differentiation.Crossref | GoogleScholarGoogle Scholar | 19238703PubMed |

Kendrick, G. A., Waycott, M., Carruthers, T. J., Cambridge, M. L., Hovey, R., Krauss, S. L., Lavery, P. S., Les, D. H., Lowe, R. J., and Vidal, O. M. (2012). The central role of dispersal in the maintenance and persistence of seagrass populations. Bioscience 62, 56–65.
The central role of dispersal in the maintenance and persistence of seagrass populations.Crossref | GoogleScholarGoogle Scholar |

Keough, M. J., and Black, K. P. (1996). Predicting the scale of marine impacts: understanding planktonic links between populations. In ‘Detecting Ecological Impacts: Concepts and Applications in Coastal Habitats’. (Eds R. J. Schmitt and C. W. Osenberg.) pp. 199–234. (Academic Press: San Diego, CA, USA.)

Lanyon, J., and Sanson, G. (2006). Mechanical disruption of seagrass in the digestive tract of the dugong. Journal of Zoology 270, 277–289.
Mechanical disruption of seagrass in the digestive tract of the dugong.Crossref | GoogleScholarGoogle Scholar |

Macreadie, P. I., York, P. H., and Sherman, C. D. (2014). Resilience of Zostera muelleri seagrass to small‐scale disturbances: the relative importance of asexual versus sexual recovery. Ecology and Evolution 4, 450–461.
Resilience of Zostera muelleri seagrass to small‐scale disturbances: the relative importance of asexual versus sexual recovery.Crossref | GoogleScholarGoogle Scholar | 24634729PubMed |

McMahon, K., Sinclair, E. A., Sherman, C. D., van Dijk, K.-J., Hernawan, U. E., Verduin, J., and Waycott, M. (2018). Genetic connectivity in tropical and temperate Australian seagrass species. In ‘Seagrasses of Australia: Structure, Ecology and Conservation’. (Eds A. W. D. Larkum, G. A. Kendrick, and P. J. Ralph.) pp. 155–194. (Springer: Dordrecht, Netherlands.)

Molloy, R., Chidgey, S., Webster, I. T., Hancock, G., and Fox, D. (2005) Corner Inlet environmental audit: report to the Gippsland Coastal Board. CSIRO, Canberra, ACT, Australia.

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 | 22820204PubMed |

Pritchard, J. K., Stephens, M., and Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics 155, 945–959.
| 10835412PubMed |

Procaccini, G., Olsen, J. L., and Reusch, T. B. H. (2007). Contribution of genetics and genomics to seagrass biology and conservation. Journal of Experimental Marine Biology and Ecology 350, 234–259.
Contribution of genetics and genomics to seagrass biology and conservation.Crossref | GoogleScholarGoogle Scholar |

Reusch, T. B., Ehlers, A., Hämmerli, A., and Worm, B. (2005). Ecosystem recovery after climatic extremes enhanced by genotypic diversity. Proceedings of the National Academy of Sciences of the United States of America 102, 2826–2831.
Ecosystem recovery after climatic extremes enhanced by genotypic diversity.Crossref | GoogleScholarGoogle Scholar | 15710890PubMed |

Sherman, C. D. H., Stanley, A. M., Keough, M. J., Gardner, M. G., and Macreadie, P. I. (2012). Development of twenty-three novel microsatellite markers for the seagrass, Zostera muelleri from Australia. Conservation Genetics Resources 4, 689–693.
Development of twenty-three novel microsatellite markers for the seagrass, Zostera muelleri from Australia.Crossref | GoogleScholarGoogle Scholar |

Sherman, C. D., York, P. H., Smith, T. M., and Macreadie, P. I. (2016). Fine-scale patterns of genetic variation in a widespread clonal seagrass species. Marine Biology 163, 82.
Fine-scale patterns of genetic variation in a widespread clonal seagrass species.Crossref | GoogleScholarGoogle Scholar |

Sinclair, E. A., Krauss, S. L., Anthony, J., Hovey, R., and Kendrick, G. A. (2014). The interaction of environment and genetic diversity within meadows of the seagrass Posidonia australis (Posidoniaceae). Marine Ecology Progress Series 506, 87–98.
The interaction of environment and genetic diversity within meadows of the seagrass Posidonia australis (Posidoniaceae).Crossref | GoogleScholarGoogle Scholar |

Sinclair, E. A., Anthony, J. M., Greer, D., Ruiz‐Montoya, L., Evans, S. M., Krauss, S. L., and Kendrick, G. A. (2016). Genetic signatures of Bassian glacial refugia and contemporary connectivity in a marine foundation species. Journal of Biogeography 43, 2209–2222.
Genetic signatures of Bassian glacial refugia and contemporary connectivity in a marine foundation species.Crossref | GoogleScholarGoogle Scholar |

Smith, C. M., and Walters, L. J. (1999). Fragmentation as a strategy for Caulerpa species: fates of fragments and implications for management of an invasive weed. Marine Ecology 20, 307–319.
Fragmentation as a strategy for Caulerpa species: fates of fragments and implications for management of an invasive weed.Crossref | GoogleScholarGoogle Scholar |

Stafford-Bell, R. E., Chariton, A. A., and Robinson, R. W. (2015). Prolonged buoyancy and viability of Zostera muelleri Irmisch ex Asch. vegetative fragments indicate a strong dispersal potential. Journal of Experimental Marine Biology and Ecology 464, 52–57.
Prolonged buoyancy and viability of Zostera muelleri Irmisch ex Asch. vegetative fragments indicate a strong dispersal potential.Crossref | GoogleScholarGoogle Scholar |

Stafford-Bell, R. E., Chariton, A. A., and Robinson, R. W. (2016). Germination and early-stage development in the seagrass, Zostera muelleri Irmisch ex Asch. in response to multiple stressors. Aquatic Botany 128, 18–25.
Germination and early-stage development in the seagrass, Zostera muelleri Irmisch ex Asch. in response to multiple stressors.Crossref | GoogleScholarGoogle Scholar |

Thomson, A. C. G., York, P. H., Smith, T. M., Sherman, C. D., Booth, D. J., Keough, M. J., Ross, D. J., and Macreadie, P. I. (2015). Seagrass viviparous propagules as a potential long-distance dispersal mechanism. Estuaries and Coasts 38, 927–940.
Seagrass viviparous propagules as a potential long-distance dispersal mechanism.Crossref | GoogleScholarGoogle Scholar |

Walker, D., Dennison, W., and Edgar, G. (1999). Status of Australian seagrass research and knowledge. In ‘Seagrass in Australia: Strategic Review and Development of an R&D Plan’. (Eds A. J. Butler and P. Jernakoff.) pp. 1–24. (CSIRO Publishing: Melbourne, Vic., Australia.)

Walker, D., Olesen, B., and Phillips, R. (2001). Reproduction and phenology in seagrasses. In ‘Global Seagrass Research Methods’. (Eds F. T. Short and R. G. Coles.) pp. 59–78. (Elsevier: Amsterdam, Netherlands.)

Waters, J. M. (2008). Driven by the West Wind Drift? A synthesis of southern temperate marine biogeography, with new directions for dispersalism. Journal of Biogeography 35, 417–427.
Driven by the West Wind Drift? A synthesis of southern temperate marine biogeography, with new directions for dispersalism.Crossref | GoogleScholarGoogle Scholar |

Waters, J. M., Wernberg, T., Connell, S. D., Thomsen, M. S., Zuccarello, G. C., Kraft, G. T., Sanderson, J. C., West, J. A., and Gurgel, C. F. (2010). Australia’s marine biogeography revisited: back to the future? Austral Ecology 35, 988–992.
Australia’s marine biogeography revisited: back to the future?Crossref | GoogleScholarGoogle Scholar |

Waycott, M., Duarte, C. M., Carruthers, T. J., Orth, R. J., Dennison, W. C., Olyarnik, S., Calladine, A., Fourqurean, J. W., Heck, K. L., Hughes, A. R., Kendrick, G. A., Kenworthy, W. J., Short, F. T., and Williams, S. L. (2009). Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proceedings of the National Academy of Sciences of the United States of America 106, 12377–12381.
Accelerating loss of seagrasses across the globe threatens coastal ecosystems.Crossref | GoogleScholarGoogle Scholar | 19587236PubMed |

West Gippsland Catchment Management Authority (2013). Corner Inlet water quality improvement plan 2013. WGCMA, Traralgon, Vic., Australia.

Wilson, N. G., Stiller, J., and Rouse, G. W. (2017). Barriers to gene flow in common seadragons (Syngnathidae: Phyllopteryx taeniolatus). Conservation Genetics 18, 53–66.
Barriers to gene flow in common seadragons (Syngnathidae: Phyllopteryx taeniolatus).Crossref | GoogleScholarGoogle Scholar |

Wright, S. (1943). Isolation by distance. Genetics 28, 114–138.
| 17247074PubMed |