Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Modelling the distribution and density of the invasive seaweed Sargassum muticum (Fucales, Sargassaceae) in shallow subtidal areas

Giulia Cambiè A C , Diana Fernández-Márquez B and Ramón Muiño B
+ Author Affiliations
- Author Affiliations

A School of Ocean Sciences, Bangor University, Menai Bridge, Anglesey, LL59 5AB, UK.

B Universidade da Coruña, Facultad de Ciencias, Rua da Fraga 10, E-15008 A Coruña, Spain.

C Corresponding author. Email: g.cambie@bangor.ac.uk

Marine and Freshwater Research 68(2) 244-251 https://doi.org/10.1071/MF15347
Submitted: 8 September 2015  Accepted: 9 December 2015   Published: 21 March 2016

Abstract

The present study describes the distribution and density of Sargassum muticum in shallow subtidal areas of the Marine Fishery Reserve (MFR) ‘Os Miñarzos’ (Galicia, north-western Spain) by using a data-collection strategy and a statistical approach fairly unused in literature. Our surveys showed a rapid spread of the invasive alga in the study area, where the number of patches increased more than 50% between 2008 and 2009. A model-selection approach was used to test the goodness of fit of Sargassum density data and the zero-inflated Poisson (ZIP) appeared to be the best model. The ZIP model quantified a probability of 22% of finding at least one Sargassum plant in a randomly placed quadrat within 11-m depth, demonstrating that a large part of the MFR has been invaded. In particular, the ZIP model showed that season, richness of macroalgal community, and abiotic factors, such as wave exposure and depth, are essential drivers for the establishment of S. muticum thalli in subtidal areas. Our results showed that the invasion of subtidal areas often follows patterns similar to the intertidal areas. The present study also demonstrated the usefulness of zero-inflated models to assess early and mid-stages of a seaweed invasion.

Additional keywords: Atlantic coast, invasion, Spain, zero-inflated model.


References

Arenas, F., and Fernández, C. (2000). Size structure and dynamics in a population of Sargassum muticum (Phaeophyceae). Journal of Phycology 36, 1012–1020.
Size structure and dynamics in a population of Sargassum muticum (Phaeophyceae).Crossref | GoogleScholarGoogle Scholar |

Arenas, F., Sánchez, I., Hawkins, S. J., and Jenkins, S. R. (2006). The invasibility of marine algal assemblages: role of functional diversity and identity. Ecology 87, 2851–2861.
The invasibility of marine algal assemblages: role of functional diversity and identity.Crossref | GoogleScholarGoogle Scholar | 17168029PubMed |

Berman, J., Harris, L., and Buttrick, M. (1992). Recent invasions of the Gulf of Maine: three contrasting ecological histories. Conservation Biology 6, 435–441.
Recent invasions of the Gulf of Maine: three contrasting ecological histories.Crossref | GoogleScholarGoogle Scholar |

Britton-Simmons, K. H. (2004). Direct and indirect effects of the introduced alga Sargassum muticum on benthic, subtidal communities of Washington state, USA. Marine Ecology Progress Series 277, 61–78.
Direct and indirect effects of the introduced alga Sargassum muticum on benthic, subtidal communities of Washington state, USA.Crossref | GoogleScholarGoogle Scholar |

Britton-Simmons, K. H., and Abbott, K. C. (2008). Short- and long-term effects of disturbance and propagule pressure on a biological invasion. Journal of Ecology 96, 68–77.
Short- and long-term effects of disturbance and propagule pressure on a biological invasion.Crossref | GoogleScholarGoogle Scholar |

Byers, J. E. (2005). Marine reserves enhance abundance but not competitive impacts of a harvested nonindigenous species. Ecology 86, 487–500.
Marine reserves enhance abundance but not competitive impacts of a harvested nonindigenous species.Crossref | GoogleScholarGoogle Scholar |

Cacabelos, E., Olabarria, C., Viejo, R. M., Rubal, M., Veiga, P., Incera, M., Gestoso, I., Vaz-Pinto, F., Mejia, A., Engelen, A. H., and Arenas, F. (2013). Invasion of Sargassum muticum in intertidal rockpools: patterns along the Atlantic Iberian Peninsula. Marine Environmental Research 90, 18–26.
Invasion of Sargassum muticum in intertidal rockpools: patterns along the Atlantic Iberian Peninsula.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXptFKqtrg%3D&md5=38cdf0d75e754b62e7594c14aa9dcb8dCAS | 23764086PubMed |

Cambiè, G. (2011). Incidental capture of Caretta caretta in trammel nets off the western coast of Sardinia (Italy): statistical models of capture abundance and immediate survival. Aquatic Conservation: Marine and Freshwater Ecosystems 21, 28–36.
Incidental capture of Caretta caretta in trammel nets off the western coast of Sardinia (Italy): statistical models of capture abundance and immediate survival.Crossref | GoogleScholarGoogle Scholar |

Casares, C., Gómez Garreta, A., Ribera Siguan, M. A., and Seoane-Camba, J. A. (1987). Sargassum muticum (Yendo) Fensholt nueva cita para la Península Ibérica. Collectanea Botanica 17, 151.

Ceccherelli, G., Piazzi, L., and Cinelli, F. (2000). Response of nonindigenous Caulerpa racemosa (Forsskal) J.Agardh to the native seagrass Posidonia oceanica (L) Delile: effect of density of shoots and orientation of edges of meadows. Journal of Experimental Marine Biology and Ecology 243, 227–240.
Response of nonindigenous Caulerpa racemosa (Forsskal) J.Agardh to the native seagrass Posidonia oceanica (L) Delile: effect of density of shoots and orientation of edges of meadows.Crossref | GoogleScholarGoogle Scholar |

Crooks, J. A. (2002). Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers. Oikos 97, 153–166.
Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers.Crossref | GoogleScholarGoogle Scholar |

Elton, C. S. (1958). ‘The Ecology of Invasions by Animals and Plants.’ (Methuen and Company: London.)

Farnham, W. F., Fletcher, R. L., and Irvine, L. M. (1973). Attached Sargassum found in Britain. Nature 243, 231–232.
Attached Sargassum found in Britain.Crossref | GoogleScholarGoogle Scholar |

Gray, B. R. (2005). Selecting distributional assumption for modelling relative densities of benthic macroinvertebrates. Ecological Modelling 185, 1–12.
Selecting distributional assumption for modelling relative densities of benthic macroinvertebrates.Crossref | GoogleScholarGoogle Scholar |

Hall, D. B. (2000). Zero-inflated Poisson and binomial regression with random effects: a case study. Biometrics 56, 1030–1039.
Zero-inflated Poisson and binomial regression with random effects: a case study.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M7it1Cnsg%3D%3D&md5=03353aea4c28c0f676fa64efed2512afCAS | 11129458PubMed |

Harris, L. G., and Tyrrell, M. C. (2001). Changing community states in the Gulf of Maine: synergism between invaders, overfishing and climate change. Biological Invasions 3, 9–21.
Changing community states in the Gulf of Maine: synergism between invaders, overfishing and climate change.Crossref | GoogleScholarGoogle Scholar |

Hewitt, C. L., Campbell, M. L., McEnnulty, F., Moore, K. M., Murfet, N. B., Robertson, B., and Schaffelke, B. (2005). Efficacy of physical removal of a marine pest: the introduced kelp Undaria pinnatifida in a Tasmanian Marine Reserve. Biological Invasions 7, 251–263.
Efficacy of physical removal of a marine pest: the introduced kelp Undaria pinnatifida in a Tasmanian Marine Reserve.Crossref | GoogleScholarGoogle Scholar |

Iglesias, G., and Carballo, R. (2009). Wave energy potential along the Death Coast (Spain). Energy 34, 1963–1975.
Wave energy potential along the Death Coast (Spain).Crossref | GoogleScholarGoogle Scholar |

Incera, M., Olabarria, C., Cacabelos, E., César, J., and Troncoso, J. S. (2011). Distribution of Sargassum muticum on the north west coast of Spain: relationships with urbanization and community diversity. Continental Shelf Research 31, 488–495.
Distribution of Sargassum muticum on the north west coast of Spain: relationships with urbanization and community diversity.Crossref | GoogleScholarGoogle Scholar |

Katsanevakis, S., Issaris, Y., Poursanidis, D., and Thessalou-Legaki, M. (2010). Vulnerability of marine habitats to the invasive green alga Caulerpa racemosa var. cylindracea within a marine protected area. Marine Environmental Research 70, 210–218.
Vulnerability of marine habitats to the invasive green alga Caulerpa racemosa var. cylindracea within a marine protected area.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXotVagt7k%3D&md5=9036c7d7f170e223d23607b7c9de17f7CAS | 20621771PubMed |

Kersting, D. K., Ballesteros, E., De Caralt, S., and Linares, C. (2014). Invasive macrophytes in a marine reserve (Columbretes Islands, NW Mediterranean): spread dynamics and interactions with the endemic scleractinian coral Cladocora caespitosa. Biological Invasions 16, 1599–1610.

Klinger, T., Padilla, D. K., and Britton-Simmons, K. (2006). Two invaders achieve higher densities in reserves. Aquatic Conservation: Marine and Freshwater Ecosystems 16, 301–311.
Two invaders achieve higher densities in reserves.Crossref | GoogleScholarGoogle Scholar |

Knoepffler-Peguy, M., Belsher, T., Boudouresque, C. F., and Lauret, M. (1985). Sargassum muticum begins to invade the Mediterranean. Aquatic Botany 23, 291–295.

Kokko, H., Mackenzie, A., Reynolds, J. D., Lindström, J., and Sutherland, W. J. (1999). Measures of inequality are not equal. American Naturalist 154, 358–382.
Measures of inequality are not equal.Crossref | GoogleScholarGoogle Scholar | 10506550PubMed |

Lambert, D. (1992). Zero-inflated Poisson regression, with an application to defects in manufacturing. Technometrics 34, 1–14.
Zero-inflated Poisson regression, with an application to defects in manufacturing.Crossref | GoogleScholarGoogle Scholar |

Lawson, J., Davenport, J., and Whitaker, A. (2004). Barnacle distribution in Lough Hyne Marine Nature Reserve: a new baseline and an account of invasion by the introduced Australasian species Elminius modestus Darwin. Estuarine, Coastal and Shelf Science 60, 729–735.
Barnacle distribution in Lough Hyne Marine Nature Reserve: a new baseline and an account of invasion by the introduced Australasian species Elminius modestus Darwin.Crossref | GoogleScholarGoogle Scholar |

Levin, P. S., Coyer, Y. A., Petrik, R., and Good, T. P. (2002). Community-wide effects of nonindigenous species on temperate rocky reefs. Ecology 83, 3182–3193.
Community-wide effects of nonindigenous species on temperate rocky reefs.Crossref | GoogleScholarGoogle Scholar |

Mack, R. N., Simberloff, D., Lonsdale, W. M., Evans, H., Clout, M., and Bazzaz, F. A. (2000). Biotic invasions: causes, epidemiology, global consequences, and control. Ecological Applications 10, 689–710.
Biotic invasions: causes, epidemiology, global consequences, and control.Crossref | GoogleScholarGoogle Scholar |

Mooney, H. A., and Drake, J. A. (Eds) (1986). ‘Ecology of Biological Invasions of North America and Hawaii. Ecological Studies, Vol. 58.’ (Springer-Verlag: New York.)10.1007/978-1-4612-4988-7

Occhipinti-Ambrogi, A., and Savini, D. (2003). Biological invasions as a component of global change in stressed marine ecosystems. Marine Pollution Bulletin 46, 542–551.
Biological invasions as a component of global change in stressed marine ecosystems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjsVaqtL4%3D&md5=8895b55b84867baab487f6eddd94157eCAS | 12735951PubMed |

Olabarria, C., Rodil, I. F., Incera, M., and Troncoso, J. S. (2009a). Limited impact of Sargassum muticum on native algal assemblages from rocky intertidal shores. Marine Environmental Research 67, 153–158.
Limited impact of Sargassum muticum on native algal assemblages from rocky intertidal shores.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXit1Oksbc%3D&md5=e3f88013fd0d5a7860ecbe68154ed5efCAS | 19168211PubMed |

Olabarria, C., Rossi, F., Rodil, I. F., Quintas, P., and Troncoso, J. S. (2009b). Use of hierarchical designs to detect scales of heterogeneity in the invasive species Sargassum muticum. Scientia Marina 73, 507–514.
Use of hierarchical designs to detect scales of heterogeneity in the invasive species Sargassum muticum.Crossref | GoogleScholarGoogle Scholar |

Pérez-Cirera, J. L., Cremades, J., and Bárbara, I. (1989). Precisiones sistemáticas y sinecológicas sobre algunas algas nuevas para Galicia o para las costas atlánticas de la Península Ibérica. Anales del Jardin Botanico de Madrid 46, 35–45.

Plouguerné, E., Le Lann, K., Connan, S., Jechoux, G., Deslandes, E., and Stiger-Pouvreau, V. (2006). Spatial and seasonal variation in density, reproductive status, length and phenolic content of the invasive brown macroalga Sargassum muticum (Yendo) Fensholt along the coast of Western Brittany (France). Aquatic Botany 85, 337–344.
Spatial and seasonal variation in density, reproductive status, length and phenolic content of the invasive brown macroalga Sargassum muticum (Yendo) Fensholt along the coast of Western Brittany (France).Crossref | GoogleScholarGoogle Scholar |

Relini, G., Relini, M., and Torchia, G. (2000). The role of fishing gear in the spreading of allochthonous species: the case of Caulerpa taxifolia in the Ligurian sea. ICES Journal of Marine Science 57, 1421–1427.
The role of fishing gear in the spreading of allochthonous species: the case of Caulerpa taxifolia in the Ligurian sea.Crossref | GoogleScholarGoogle Scholar |

Sánchez, I., Fernández, C., and Arrontes, J. (2005). Long-term changes in the structure of intertidal assemblages after invasion by Sargassum muticum (Phaeophyta). Journal of Phycology 41, 942–949.
Long-term changes in the structure of intertidal assemblages after invasion by Sargassum muticum (Phaeophyta).Crossref | GoogleScholarGoogle Scholar |

Schaffelke, B., and Hewitt, C. L. (2007). Impacts of introduced seaweeds. Botanica Marina 50, 397–417.
Impacts of introduced seaweeds.Crossref | GoogleScholarGoogle Scholar |

Sileshi, G., Hailu, G., and Nyadzi, G. I. (2009). Traditional occupancy–abundance models are inadequate for zero-inflated ecological count data. Ecological Modelling 220, 1764–1775.
Traditional occupancy–abundance models are inadequate for zero-inflated ecological count data.Crossref | GoogleScholarGoogle Scholar |

Simberloff, D., and Von Holle, B. (1999). Positive interactions of nonindigenous species: invasional meltdown? Biological Invasions 1, 21–32.
Positive interactions of nonindigenous species: invasional meltdown?Crossref | GoogleScholarGoogle Scholar |

Stachowicz, J. J., Fried, H., Osman, R. W., and Whitlatch, R. B. (2002). Biodiversity, invasion resistance, and marine ecosystem function: reconciling pattern and process. Ecology 83, 2575–2590.
Biodiversity, invasion resistance, and marine ecosystem function: reconciling pattern and process.Crossref | GoogleScholarGoogle Scholar |

Streftaris, N., and Zenetos, A. (2006). Alien marine species in the Mediterranean: the 100 ‘worst invasives’ and their impacts. Mediterranean Marine Science 7, 87–118.
Alien marine species in the Mediterranean: the 100 ‘worst invasives’ and their impacts.Crossref | GoogleScholarGoogle Scholar |

Strong, J. A., Dring, M. J., and Maggs, C. A. (2006). Colonisation and modification on soft substratum habitats by the invasive macroalga Sargassum muticum. Marine Ecology Progress Series 321, 87–97.
Colonisation and modification on soft substratum habitats by the invasive macroalga Sargassum muticum.Crossref | GoogleScholarGoogle Scholar |

Van der Maarel, E. (1979). Transformation of cover-abundance values in phytosociology and its effects in community similarity. Vegetatio 39, 97–114.
Transformation of cover-abundance values in phytosociology and its effects in community similarity.Crossref | GoogleScholarGoogle Scholar |

Viejo, R. M., Arrontes, J., and Andrew, N. L. (1995). An experimental evaluation of the effect of wave action on the distribution of Sargassum muticum in northern Spain. Botanica Marina 38, 437–441.
An experimental evaluation of the effect of wave action on the distribution of Sargassum muticum in northern Spain.Crossref | GoogleScholarGoogle Scholar |

Weiner, J., and Thomas, S. C. (1986). Size variability and competition in plant monocultures. Oikos 47, 211–222.
Size variability and competition in plant monocultures.Crossref | GoogleScholarGoogle Scholar |

White, L. L. F. (2010). Mechanisms underlying marine macroalgal invasions: understanding invasion success of Sargassum muticum. Ph.D. Thesis, University of British Columbia, Vancouver, Canada.

Williams, S. L., and Smith, J. E. (2007). A global review of the distribution, taxonomy and impacts of introduced seaweeds. Annual Review of Ecology Evolution and Systematics 38, 327–359.
A global review of the distribution, taxonomy and impacts of introduced seaweeds.Crossref | GoogleScholarGoogle Scholar |