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The extent of grazing release from epiphytism for Sargassum muticum (Phaeophyceae) within the invaded range

Published online by Cambridge University Press:  02 April 2009

Christine A. Maggs
Affiliation:
School of Biological Sciences, Queen's University, Belfast BT9 7BL, UK
Mark P. Johnson
Affiliation:
School of Biological Sciences, Queen's University, Belfast BT9 7BL, UK

Abstract

The overall biotic pressure on a newly introduced species may be less than that experienced within its native range, facilitating invasion. The brown alga Sargassum muticum (Yendo) Fensholt is a conspicuous and successful invasive species originally from Japan and China. We compared S. muticum and native macroalgae with respect to the biotic pressures of mesoherbivore grazing and ectocarpoid fouling. In Strangford Lough, Northern Ireland, S. muticum thalli were as heavily overgrown with seasonal blooms of epiphytic algae as native macroalgal species were. The herbivorous amphipod Dexamine spinosa was much more abundant on S. muticum than on any native macroalga. When cultured with this amphipod, S. muticum lost more tissue than three native macroalgae, Saccharina latissima (Linnaeus) Lane et al., Halidrys siliquosa (Linnaeus) Lyngbye and Fucus serratus Linnaeus. Sargassum muticum cultured with both ectocarpoid fouling and amphipods showed a severe impact, consistent with our previous findings of large declines in the density of S. muticum observed in the field during the peak of fouling. Despite being a recent introduction into the macroalgal community in Strangford Lough, S. muticum appears to be under biotic pressure at least equal to that on native species, suggesting that release from grazing and epiphytism does not contribute to the invasiveness of this species in Strangford Lough.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2009

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References

REFERENCES

Bjæke, M.R. and Fredriksen, S. (2003) Epiphytic macroalgae on the introduced brown seaweed Sargassum muticum (Yendo) Fensholt (Phaeophyceae) Norway. Sarsia 88, 353364.CrossRefGoogle Scholar
Brawley, S.H. and Fei, X.G. (1987) Studies of mesoherbivory in aquaria and in an unbarricaded mariculture farm on the Chinese coast. Journal of Phycology 23, 614623.CrossRefGoogle Scholar
Bronmark, C. (1985) Interactions between macrophytes, epiphytes and herbivores: an experimental approach. Oikos 45, 2630.CrossRefGoogle Scholar
Bulthuis, D.A. and Woelkerling, W.J. (1983) Biomass accumulation and shading effects of epiphytes on leaves of the seagrass, Heterozostera tasmanica, in Victoria, Australia. Aquatic Botany 16, 137148.Google Scholar
Cattaneo, A. (1983) Grazing on epiphytes. Journal of Limnology and Oceanography 28, 124132.CrossRefGoogle Scholar
Clarke, K.R. and Gorley, R.N. (2001) PRIMER v5: user manual and tutorial. PRIMER-E: Plymouth, UK.Google Scholar
Colautti, R.I., Ricciardi, A., Grigorovich, L.A. and MacIsaac, H.J. (2004) Is invasion success explained by the enemy release hypothesis? Ecological Letters 7, 721733.Google Scholar
Conover, J.T. and Sieburth, J.McN. (1964) Effects of Sargassum distribution on its epibiota and antibacterial activity. Marine Biology 6, 147157.Google Scholar
Critchley, A.T. (1981) Ecological studies on Sargassum muticum (Yendo) Fensholt. PhD thesis. Portsmouth Polytechnic, UK.Google Scholar
Cruz-Rivera, E. and Hay, M.E. (2000) The effects of diet mixing on consumer fitness: macroalgae, epiphytes, and animal matter as food for marine amphipods. Oecologica 123, 252264.CrossRefGoogle ScholarPubMed
Cruz-Rivera, E. and Hay, M.E. (2001) Macroalgal traits and the feeding and fitness of an herbivorous amphipod: the roles of selectivity, mixing and compensation. Marine Ecology Progress Series 218, 249266.CrossRefGoogle Scholar
Davison, D.M. (1999) Sargassum muticum in Strangford Lough, 1995–1998; a review of the introduction and colonization of Strangford Lough MNR (Marine Nature Reserve) and cSAC (Special Area of Conservation) by the invasive brown algae Sargassum muticum. Environment and Heritage Service Research and Development Series No. 99/27, 184.Google Scholar
De Rivera, C.E., Ruiz, G.M., Hines, A.H. and Jivoff, P. (2005) Biotic resistance to invasion: native predator limits abundance and distribution of an introduced crab. Ecology 86, 33643376.Google Scholar
Dodds, W.K. (1991) Community interactions between the filamentous alga Cladophora glomerata (L.) Kuetzing, its epiphytes, and epiphyte grazers. Oecologica 85, 572580.CrossRefGoogle ScholarPubMed
Duffy, J.E. (1990) Amphipods on seaweeds: partners or pests? Oecologia 83, 267276.Google Scholar
Duffy, J.E. and Hay, M.E. (2000) Strong impacts of grazing amphipods on the organization of a benthic community. Ecological Monographs 70, 237263.CrossRefGoogle Scholar
Elton, C.S. (1958) The ecology of invasions by animals and plants. London: Methuen.CrossRefGoogle Scholar
Fensholt, D.E. (1955) An emendation of the genus Cystophyllum (Fucales). American Journal of Botany 42, 305322.Google Scholar
Finnoff, D. and Tschirhart, J. (2005) Identifying, preventing and controlling invasive plant species using their physiological traits. Ecology and Economics 52, 397416.CrossRefGoogle Scholar
Gee, J.M. and Warwick, R.M. (1994) Metazoan community structure in relation to the fractal dimensions of marine macroalgae. Marine Ecology Progress Series 103, 141150.Google Scholar
Glombitza, K.W., Eckhardt, G. and Farnham, W.F. (1982) Antibiotics from algae, part 25. Polyhydroxphenyl ethers from the brown alga Sargassum muticum (Yendo) Fensholt, Part II. Botanica Marina 25, 449453.CrossRefGoogle Scholar
Gray, P.W.G. (1978) An investigation of the fauna associated with Sargassum muticum. PhD thesis. Portsmouth Polytechnic, UK.Google Scholar
Hales, J.M. and Fletcher, R.L. (1989) Studies on the recently introduced brown alga Sargassum muticum (Yendo) Fensholt. IV. The effect of temperature, irradiance and salinity on germling growth. Botanica Marina 32, 167176.CrossRefGoogle Scholar
Hay, M.E. and Fenical, W. (1988) Marine plant–herbivore interactions: the ecology of chemical defense. Annual Review of Ecology and Systematics 19, 111145.Google Scholar
Heckscher, E., Hauxwell, J., Jimenez, E.G., Rietsma, C. and Valiela, I. (1996) Selectivity by the herbivorous amphipod Microdeutopus gryllotalpa among five species of macroalgae. Biological Bulletin. Marine Biological Laboratory, Woods Hole 191, 324326.Google Scholar
Hokkanen, H.M.T. and Pimentel, D. (1989) New associations in biological control—theory and practice. Canadian Entomologist 121, 829840.Google Scholar
Karez, R., Engelbert, S. and Sommer, U. (2000) ‘Co-consumption’ and ‘protective coating’: two new proposed effects of epiphytes on their macroalgal hosts in mesograzer–epiphyte–host interactions. Marine Ecology Progress Series 205, 8593.CrossRefGoogle Scholar
Lewey, S.A. and Farnham, W.F. (1981) Observations on Sargassum muticum in Britain. Proceedings of the International Seaweed Symposium 8, 388394.Google Scholar
McGlathery, K.J. (2001) Macroalgal bloom contribution to the decline of seagrass in nutrients-enriched coastal waters. Journal of Phycology 37, 453456.Google Scholar
Moore, K.A., Neckles, H.A. and Orth, R.J. (1996) Zostera marina (eelgrass) growth and survival a gradient of nutrients and turbidity in the lower Chesapeake Bay. Marine Ecology Progress Series 142, 247259.Google Scholar
Nicholson, N.L., Hosmer, H.M., Bird, K., Hart, L., Sandlin, W., Shoemaker, C. and Sloan, C. (1981) The biology of Sargassum muticum (wireweed) at Santa Catalina (California, USA). Proceedings of the International Seaweed Symposium 8, 416424.Google Scholar
Norton, T.A. (1976) Why is Sargassum muticum so invasive? British Journal of Phycology 11, 197198.Google Scholar
Norton, T.A. and Benson, M.R. (1983) Ecological interaction between the brown seaweed Sargassum muticum and its associated fauna. Marine Biology 75, 169177.CrossRefGoogle Scholar
Norton, T.A. and Deysher, L.E. (1989) The reproductive ecology of Sargassum muticum at different latitudes. In Ryland, J.S. and Tyler, P.A. (eds) Reproduction, genetics and distributions of marine organisms. Fredensborg, Denmark: Olsen and Olsen, pp. 147152.Google Scholar
Nyberg, C.D. and Wallentinus, I. (2005) Can species traits be used to predict marine macroalgal introductions? Biological Invasions 7, 265279.CrossRefGoogle Scholar
Parker, J.D. and Hay, M.E. (2005) Biotic resistance to plant invasions? Native herbivores prefer non-native plants. Ecological Letters 8, 959967.CrossRefGoogle ScholarPubMed
Parker, D.J., Burkepile, D.E. and Hay, M.E. (2006) Opposing effects of native and exotic herbivores on plant invasion. Science 311, 14591461.Google Scholar
Pavia, H., Carr, H. and Åberg, P. (1999) Habitat and feeding preferences of crustacean mesoherbivores inhabiting the brown seaweed Ascophyllum nodosum (L.) Le Jol. and its epiphytic macroalgae. Journal of Experimental Marine Biology and Ecology 236, 1532.Google Scholar
Pedersen, M.F., Staehr, P.A, Wernberg, T. and Thomsen, M.S. (2005) Biomass dynamics of exotic Sargassum muticum and native Halidrys siliquosa in Limfjorden, Denmark—implications of species replacements on turnover rates. Aquatic Botany 83, 3147.Google Scholar
Plouguerne, E., Le Lann, K., Connan, S., Jechoux, G., Deslandes, E. and Stiger, V. (2006) Spatial and seasonal variations in density, maturity, length and phenolic content of the invasive brown macroalga Sargassum muticum along the coast of Western Brittany (France). Aquatic Botany 8, 337344.CrossRefGoogle Scholar
Poore, A.G.B. (2004) Spatial associations among algae affect host use in a herbivorous marine amphipod. Oecologia 140, 104112.CrossRefGoogle Scholar
Rico, J.M. and Fernandez, C. (1997) Ecology of Sargassum muticum on the North Coast of Spain II. Physiological differences between Sargassum muticum and Cytoseira nodicaulis. Botanica Marina 40, 405410.Google Scholar
Sanchez, I. and Fernandez, C. (2005) Impact of the invasive seaweed Sargassum muticum (Phaeophyta) on an intertidal macroalgal assemblage. Journal of Phycology 41, 923930.Google Scholar
Schmidt, A.L and Scheibling, R.E. (2007) Effects of native and invasive macroalgal canopies on composition and abundance of mobile benthic macrofauna and turf-forming algae. Journal of Experimental Marine Biology and Ecology 341, 110130.CrossRefGoogle Scholar
Steinberg, P.D. and de Nys, R. (2002) Chemical mediation of colonization of seaweed surfaces. Journal of Phycology 38, 621629.CrossRefGoogle Scholar
Strong, J.A., Maggs, C. and Dring, M. (2005) Colonization and modification of soft substratum habitats by the invasive macroalga Sargassum muticum. Marine Ecology Progress Series 321, 8797.CrossRefGoogle Scholar
Thomsen, M.S., Wernberg, T., Stæhr, P.A. and Pedersen, M.F. (2006) Spatio-temporal distribution patterns of the invasive macroalga Sargassum muticum within a Danish Sargassum-bed. Helgoland Marine Research 60, 5058.Google Scholar
Torchin, M.E., Lafferty, K.D. and Kuris, A.M. (2001) Release from parasites as natural enemies: increased performance of a globally introduced marine crab. Biological Invasions 3, 333345.CrossRefGoogle Scholar
Viejo, R.M. (1999) Mobile epifauna inhibiting the invasive Sargassum muticum and two local seaweeds in northern Spain. Aquatic Botany 64, 131149.CrossRefGoogle Scholar
Vila-Gispert, A., Alcaraz, C. and a-Berthou, E.G. (2005) Life-history traits of invasive fish in small Mediterranean streams. Biolical Invasions 7, 107116.CrossRefGoogle Scholar
Wahl, M. (1989) Marine epibiosis. I. Fouling and antifouling: some basic aspects. Marine Ecology Progress Series 58, 175189.Google Scholar
Wahl, M. and Hay, M.E. (1995) Associational resistance and shared doom: effects of epibiosis on herbivory. Oecologia 102, 329340.CrossRefGoogle ScholarPubMed
Wallentinus, I. (1999) Case histories on introduced species: their general biology, distribution, range expansion and impact. Sargassum muticum. Department of Fishery Biology, University of Kiel, Germany, pp. 2129.Google Scholar
Wernberg, T., Thomsen, M.S., Staehr, P.A. and Morten, F.P. (2004) Epibiota communities of the introduced and indigenous macroalgal relatives Sargassum muticum and Halidrys siliquosa in Limfjorden (Demark). Helgoland Marine Research 58, 154161.CrossRefGoogle Scholar
Withers, R.G., Farnham, W.F., Lewey, S., Jephson, N.A., Haythorn, J.M. and Gray, P.W.G. (1975) The epibonts of Sargassum muticum in British waters. Marine Biology 35, 7986.Google Scholar
Wolfe, L.M. (2002) Why alien invaders succeed: support for the escape-from-enemy hypothesis. American Naturalist 160, 705711.Google Scholar
Wonham, M.J., Carlton, J.T., Ruiz, G.M. and Smith, L.D. (2000) Fish and ships: relating dispersal frequency to success in biological invasions. Marine Biology 136, 11111121.Google Scholar