The role of nutrient enrichment in the invasion process in intertidal rock pools
Anthropogenic-mediated disturbances can induce major effects on the structure and functioning of natural systems. Understanding how stressors jointly interact to impact ecosystems has become a central interest to ecological researchers. In this study, we investigated the potential synergies between two recognised threats to the marine environment: eutrophication and biological invasions. Coastal eutrophication is usually regarded as a local stressor resulting from inland agricultural and industrial runoffs. Biological invasions are considered a global threat to coastal ecosystems, mainly derived from the increase of the spatial scale of human activities. We carried out an experimental study to investigate how nutrient supply affected the invasion success of two introduced seaweeds widely recognised as highly invasive species, Sargassum muticum and Grateloupia turuturu. In our study, we seeded experimental macroalgae assemblages with propagules from these two invaders, which were afterwards placed in rock pools under two different nutrient conditions. Results suggested that besides species-specific differences, nutrients promoted the establishment of these two introduced seaweeds. Also, the results from our structural and functional studies showed that functional impacts by invaders may occur even before structural effects are detected in the invaded communities. Even in the absence of large structural impacts associated with the invasion of S. muticum, functional effects were obvious for this species. The assemblages initially seeded with S. muticum presented higher rates of productivity and higher photosynthetic efficiency compared to the other treatments.
KeywordsSargassum muticum Grateloupia turuturu Eutrophication Invasive seaweeds Invasion impact Rocky shores
RV was supported by funds from the Fundação para a Ciência e Tecnologia (FCT) SFRH/BD/74266/2010. FA and ISP were funded by the European Regional Development Fund (ERDF) through the ‘Programa Operacional Factores de Competitividade’ (POFC-COMPETE) within the ‘Quadro de Referência Estratégico Nacional (QREN) and PEst-C/MAR/LA0015/2011 (by ERDF through the COMPETE Program and national FCT funds). Additional funding was obtained from FCT project CLEF (PTDC/AAC-AMB/102866/2008) and the Framework of the Structured Program of R&D&I INNOVMAR - Innovation and Sustainability in the Management and Exploitation of Marine Resources (Reference NORTE-01-0145-FEDER-000035), namely within the Research Line ECOSERVICES, supported by the Northern Regional Operational Programme (NORTE2020), through the European Regional Development Fund (ERDF).
- Arenas, F., C. Fernandez, J. M. Rico, E. Fernandez & D. Haya, 1995. Growth and reproductive strategies of Sargassum muticum (Yendo) Fensholt and Cystoseira nodicaulis (Whit) Roberts. Scientia Marina 59: 1–8.Google Scholar
- Bertocci, I., R. Araújo, M. Incera, F. Arenas, R. Pereira, H. Abreu, K. Larsen & I. Sousa-Pinto, 2012. Benthic assemblages of rock pools in northern Portugal: seasonal and between-pool variability. Scientia Marina 76: 781–789.Google Scholar
- Bertocci, I., Godino J. Dominguez, C. Freitas, M. Incera, R. Araújo, A. Bio, F. Arenas, I. Sousa-Pinto, P. A. Reis & R. Dominguez, 2015. The regime of climate-related disturbance and nutrient enrichment modulate macroalgal invasions in rockpools. Biological Invasions 17: 133–147.CrossRefGoogle Scholar
- Bokn, T. L., C. M. Duarte, M. F. Pedersen, N. Marba, F. E. Moy, C. Barron, B. Bjerkeng, J. Borum, H. Christie, S. Engelbert, F. L. Fotel, E. E. Hoell, R. Karez, K. Kersting, P. Kraufvelin, C. Lindblad, M. Olsen, K. A. Sanderud, U. Sommer & K. Sorensen, 2003. The response of experimental rocky shore communities to nutrient additions. Ecosystems 6: 577–594.CrossRefGoogle Scholar
- Cabioch, J., A. Castric-Fey, M. T. L’Hardy-Halos & A. Rio, 1997. Grateloupia doryphora et Grateloupia filicina var. luxurians (Rodophyta, Halymeniaceae) sur les côtes de Bretagne (France). Cryptogamie, Algologie 18: 117–137.Google Scholar
- Cacabelos, E., C. Olabarria, R. M. Viejo, M. Rubal, P. Veiga, M. Incera, I. Gestoso, F. Vaz-Pinto, A. Mejia, A. H. Engelen & F. Arenas, 2013. Invasion of Sargassum muticum in intertidal rockpools: patterns along the Atlantic Iberian Peninsula. Marine Environmental Research 90: 18–26.CrossRefPubMedGoogle Scholar
- Ceccherelli, G. & F. Cinelli, 1997. Short-term effects of nutrient enrichment of the sediment and interactions between the seagrass Cymodocea nodosa and the introduced green alga Caulerpa taxifolia in a Mediterranean bay. Journal of Experimental Marine Biology and Ecology 217: 165–177.CrossRefGoogle Scholar
- Critchley, A. T., 1983. The establishment and increase of Sargassum muticum (Yendo) Fensholt populations within the solent area of Southern Britain. An investigation of the increase in canopy cover of the alga at low water. Botanica Marina 26: 547–552.Google Scholar
- Davis, M. A. & K. Thompson, 2000. Eight ways to be a colonizer; two ways to be an invader: a proposed nomenclature for invasion ecology. Bulletin of the Ecological Society of America 81: 226–230.Google Scholar
- Deysher, L. E. & T. A. Norton, 1982. Dispersal and colonization in Sargassum muticum (Yendo) Fensholt. Journal of Experimental Marine Biology and Ecology 56(2–3): 179–195.Google Scholar
- Elser, J. J., M. E. Bracken, E. E. Cleland, D. S. Gruner, W. S. Harpole, H. Hillebrand, J. T. Ngai, E. W. Seabloom, J. B. Shurin & J. E. Smith, 2007. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecology Letters 10(12): 1135–1142.CrossRefPubMedGoogle Scholar
- Engelen, A. H., A. Serebryakova, P. Ang, K. Britton-Simmons, F. Mineur, M. Pedersen, F. Arenas, C. Fernández, H. Steen, R. Svenson, H. Pavia, G. Toth, F. Viard & R. Santos, 2015. Circumglobal invasion by the brown seaweed Sargassum muticum. Oceanography and Marine Biology: Annual Reviews 53: 81–126.Google Scholar
- Halpern, B. S., S. Walbridge, K. A. Selkoe, C. V. Kappel, F. Micheli, C. D’Agrosa, J. F. Bruno, K. S. Casey, C. Ebert, H. E. Fox, R. Fujita, D. Heinemann, H. S. Lenihan, E. M. P. Madin, M. T. Perry, E. R. Selig, M. Spalding, R. Steneck & R. Watson, 2008. A global map of human impact on marine ecosystems. Science 319: 948–952.CrossRefPubMedGoogle Scholar
- Lyons, D. A., C. Arvanitidis, A. J. Blight, E. Chatzinikolaou, T. Guy-Haim, J. Kotta, H. Orav-Kotta, A. M. Queiros, G. Rilov, P. J. Somerfield & T. P. Crowe, 2014. Macroalgal blooms alter community structure and primary productivity in marine ecosystems. Global Change Biology 20: 2712–2724.CrossRefPubMedGoogle Scholar
- Maggi, E., L. Benedetti-Cecchi, A. Castelli, E. Chatzinikolaou, T. P. Crowe, G. Ghedini, J. Kotta, D. A. Lyons, C. Ravaglioli, G. Rilov, L. Rindi, F. Bulleri & H. MacIsaac, 2015. Ecological impacts of invading seaweeds: a meta-analysis of their effects at different trophic levels. Diversity and Distributions 21: 1–12.CrossRefGoogle Scholar
- Pinheiro J., Bates D., DebRoy S., Sarkar D. & R Core Team (2017). nlme: linear and nonlinear mixed effects models. R package version 3.1-131.Google Scholar
- R Core Team, (2016). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/.
- Skaug H., Fournier D., Bolker B., Magnusson A. & A. Nielsen, 2016. Generalized linear mixed models using ‘AD model builder. R package version 0.8.3.3.Google Scholar
- Underwood, A. J., 1997. Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, Cambridge.Google Scholar