Skip to main content

Time-since-invasion increases native mesoherbivore feeding rates on the invasive alga, Sargassum muticum (Yendo) Fensholt

  • Martyn Kurr (a1) and Andrew J. Davies (a1)

Invasive algae can have substantial negative impacts in their invaded ranges. One widely cited mechanism that attempts to explain how invasive plants and algae are often able to spread quickly, and even become dominant in their invaded ranges, is the Enemy Release Hypothesis. This study assessed the feeding behaviours of two species of gastropod herbivore from populations exposed to the invasive alga Sargassum muticum for different lengths of time. Feeding trials, consisting of both choice and no-choice, showed that the herbivores from older stands (35–40 years established) of S. muticum were more likely to feed upon it than those taken from younger (10–19 years established) stands. These findings provide evidence in support of the ERH, by showing that herbivores consumed less S. muticum if they were not experienced with it. These findings are in accordance with the results of other feeding-trials with S. muticum, but in contrast to research that utilizes observations of herbivore abundance and diversity to assess top-down pressure. The former tend to validate the ERH, and the latter typically reject it. The potential causes of this disparity are discussed, as are the importance of palatability, herbivore species and time-since-invasion when considering research into the ERH. This study takes an important, yet neglected, approach to the study of invasive ecology.

Corresponding author
Correspondence should be addressed to: M. Kurr, Marine Science, School of Natural and Environmental Sciences, Newcastle University, Newcastle NE1 7RU, UK email:
Hide All

Present address: Marine Science, School of Natural and Environmental Sciences, Newcastle University, Newcastle NE1 7RU, UK.

Hide All
Andrew, N.L. and Viejo, R.M. (1998) Effects of wave exposure and intraspecific density on the growth and survivorship of Sargassum muticum (Sargassaceae: Phaeophyta). European Journal of Phycology 33, 251258.
Arenas, F., Fernandez, C., Rico, J.M., Fernandez, E. and Haya, D. (1995) Growth and reproductive strategies of Sargassum muticum (Yendo) Fensholt and Cystoseira nodicaulis (Whit.) Roberts. Scientia Marina 59, 18.
Auerbach, M. and Simberloff, D. (1988) Rapid leaf-miner colonization of introduced trees and shifts in sources of herbivore mortality. Oikos 52, 4150.
Bell, T.M. and Sotka, E.E. (2012) Local adaptation in adult feeding preference and juvenile performance in the generalist herbivore Idotea balthica . Oecologia 170, 383393.
Bennett, J.R., Vellend, M., Lilley, P.L., Cornwell, W.K. and Arcese, P. (2013) Abundance, rarity and invasion debt among exotic species in a patchy ecosystem. Biological Invasions 15, 707716.
Blois, J.L., Williams, J.W., Fitzpatrick, M.C., Jackson, S.T. and Ferrier, S. (2013) Space can substitute for time in predicting climate-change effects on biodiversity. Proceedings of the National Academy of Sciences USA 110, 93749379.
Boaden, P.J.S., O'Connor, R.J. and Seed, R. (1975) The composition and zonation of a Fucus serratus community in Strangford Lough, Co. Down. Journal of Experimental Marine Biology and Ecology 17, 111136.
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, 6178.
Buschmann, A.H. (1990) Intertidal macroalgae as refuge and food for amphipoda in Central Chile. Aquatic Botany 36, 237245.
Byers, J.E., Smith, R.S., Pringle, J.M., Clark, G.F., Gribben, P.E., Hewitt, C.L., Inglis, G.J., Johnston, E.L., Ruiz, G.M., Stachowicz, J.J. and Bishop, M.J. (2015) Invasion expansion: time since introduction best predicts global ranges of marine invaders. Scientific Reports 5, 12436.
Cacabelos, E., Olabarria, C., Incera, M. and Troncoso, J.S. (2010a) Do grazers prefer invasive seaweeds? Journal of Experimental Marine Biology and Ecology 393, 182187.
Cacabelos, E., Olabarria, C., Incera, M. and Troncoso, J.S. (2010b) Effects of habitat structure and tidal height on epifaunal assemblages associated with macroalgae. Estuarine and Coastal Marine Science 89, 4352.
Caño, L., Escarré, J., Vrieling, K. and Sans, F.X. (2009) Palatability to a generalist herbivore, defence and growth of invasive and native Senecio species: testing the evolution of increased competitive ability hypothesis. Oecologia 159, 95106.
Claridge, K. and Franklin, S.B. (2002) Compensation and plasticity in an invasive plant species. Biological Invasions 4, 339347.
Critchley, A.T., Farnham, W.F. and Morrell, S.L. (1986) An account of the attempted control of an introduced marine alga, Sargassum muticum, in southern England. Biological Conservation 35, 313332.
Cronin, G. and Hay, M.E. (1996) Susceptibility to herbivores depends on recent history of both the plant and animal. Ecology 77, 15311543.
Davis, A.R., Benkendorff, K. and Ward, D.W. (2005) Responses of common SE Australian herbivores to three suspected invasive Caulerpa spp. Marine Biology 146, 859868.
Davis, T.A., Volesky, B. and Mucci, A. (2003) A review of the biochemistry of heavy metal biosorption by brown algae. Water Research 77, 43114330.
Davison, D.M. (2009) Sargassum muticum in Scotland 2008: a review of information, issues and implications. Scottish Natural Heritage Commissioned Report No. 324. ROAME Number R07AC707.
Dostál, P., Müllerová, J., Pyšek, P., Pergl, J. and Klinerová, T. (2013) The impact of an invasive plant changes over time. Ecology Letters 16, 12771284.
Dudgeon, S. and Petraitis, P.S. (2005) First year demography of the foundation species, Ascophyllum nodosum, and its community implications. Oikos 109, 405415.
Engelen, A.H., Henriques, N., Monteiro, C. and Santos, R. (2011) Mesograzers prefer mostly native seaweeds over the invasive brown seaweed Sargassum muticum . Hydrobiologia 669, 157165.
Engelen, A.H., Primo, A.L., Cruz, T. and Santos, R. (2013) Faunal differences between the invasive brown macroalga Sargassum muticum and competing native macroalgae. Biological Invasions 15, 171183.
Engelen, A.H. and Santos, R. (2009) Which demographic traits determine population growth in the invasive brown seaweed Sargassum muticum? Journal of Ecology 97, 675684.
Engelen, A.H., Serebryakova, A., Ang, P., Britton-Simmons, K., Mineur, F., Pedersen, M.F., Arenas, F., Fernández, C., Steen, H., Svenson, R., Pavia, H. and Toth, G.B. (2015) Circumglobal invasion by the brown seaweed Sargassum muticum . Oceanography and Marine Biology 53, 81126.
Escobedo, J.F., Gomes, E.N., Oliveira, A.P. and Soares, J. (2009) Modelling hourly and daily fractions of UV, PAR and NIR to global solar radiation under various sky conditions at Botucatu, Brazil. Applied Energy 86, 299309.
Forslund, H., Wikström, S.A. and Pavia, H. (2010) Higher resistance to herbivory in introduced compared to native populations of a seaweed. Oecologia 164, 833840.
Hallas, P. (2012) Genetics and ecology of the invasive marine alga, Sargassum muticum within Wales. PhD thesis. University of Glamorgan, Pontypridd, UK.
Harvey, K.J., Nipperess, D.A., Britton, D.R. and Hughes, L. (2013) Does time since introduction influence enemy release of an invasive weed? Oecologia 173, 493506.
Hayward, P.J. and Ryland, J.S. (2006) Handbook of the marine fauna of North-West Europe. New York, NY: Oxford University Press.
Heger, T. and Jeschke, J.M. (2014) The enemy release hypothesis as a hierarchy of hypotheses. Oikos 123, 741750.
Hull-Sanders, H.M., Clare, R., Johnson, R.H. and Meyer, G.A. (2007) Evaluation of the evolution of increased competitive ability (EICA) hypothesis: loss of defense against generalist but not specialist herbivores. Journal of Chemical Ecology 33, 781799.
Jogesh, T., Carpenter, D. and Cappuccino, N. (2008) Herbivory on invasive exotic plants and their non-invasive relatives. Biological Invasions 10, 797804.
Jormalainen, V., Honkanen, T., Mäkinen, A., Hemmi, A. and Vesakoski, O. (2001) Why does herbivore sex matter? Sexual differences in utilization of Fucus vesiculosus by the isopod Idotea baltica . Oikos 93, 7786.
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.
Keane, R.M. and Crawley, M.J. (2002) Exotic plant invasions and the enemy release hypothesis. Trends in Ecology and Evolution 17, 164170.
Le Cam, S., Thiebaut, C.D., Bouchemousse, S. and Viard, F. (2015) Elucidating unresolved invasion history with genome-wide sequencing approach: the case of the global invader Sargassum muticum . European Journal of Phycology Keynote and Oral Papers 50, 2425.
Machado, G.B.D.O., Neufeld, A.B., Dena, S.A., Siqueira, S.G.L. and Leite, F.P.P. (2015) Variation of amphipod assemblage along the Sargassum stenophyllum (Phaeophyta, Fucales) thallus. Nauplius 23, 7378.
Maron, J.L. and Vilá, M. (2001) When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses. Oikos 95, 361373.
Maron, J.L. and Vilá, M. (2007) Exotic plants in an altered enemy landscape: effects on enemy resistance. In Kelley, J. and Tilmon, J. (eds) Specialization, speciation and radiation – the evolutionary biology of herbivorous insects. Berkeley, CA: University of California Press, pp. 280295.
Mattila, J.M., Zimmer, M., Vesakoski, O. and Jormalainen, V. (2014) Habitat-specific gut microbiota of the marine herbivore Idotea balthica (Isopoda). Journal of Experimental Marine Biology and Ecology 455, 2228.
Monteiro, C.A., Engelen, A.H. and Santos, R.O. (2009) Macro- and mesoherbivores prefer native seaweeds over the invasive brown seaweed Sargassum muticum: a potential regulating role on invasions. Marine Biology 156, 25052515.
Morrison, W.E. and Hay, M.E. (2011) Herbivore preference for native vs exotic plants: generalist herbivores from multiple continents prefer exotic plants that are evolutionarily naïve. PLoS ONE 6, e17227.
Norton, T.A. (1977) The growth and development of Sargassum muticum (Yendo) Fensholt. Journal of Experimental Marine Biology and Ecology 26, 4153.
Norton, T.A. and Benson, M.R. (1983) Ecological interactions between the brown seaweed Sargassum muticum and its associated fauna. Marine Biology 75, 169177.
Parker, J.D., Burkepile, D.E. and Hay, M.E. (2006) Opposing effects of native and exotic herbivores on plant invasions. Science 311, 14591461.
Parker, J.D. and Hay, M.E. (2005) Biotic resistance to plant invasions? Native herbivores prefer non-native plants. Ecology Letters 8, 959967.
Pavia, H., Cervin, G., Lindgren, A. and Aberg, P. (1998) Effects of UV-B radiation and simulated herbivory on phlorotannins in the brown alga Ascophyllum nodosum . Marine Ecology Progress Series 157, 139146.
Pavia, H. and Toth, G.B. (2000) Inducible chemical resistance to herbivory in the brown seaweed Ascophyllum nodosum . Ecology 81, 32123225.
Pavia, H. and Toth, G.B. (2008) Macroalgal models in testing and extending defense theories. In Amsler, C.D. (ed.) Algal chemical ecology. Berlin: Springer-Verlag, pp. 147172.
Pavia, H., Toth, G.B. and Åberg, P. (2002) Optimal defence theory: elasticity analysis as a tool to predict intraplant variation in defences. Ecology 83, 891897.
Pearse, I.S., Harris, D.J., Karban, R., and Sih, A. (2013) Predicting novel herbivore–plant interactions. Oikos 122, 15541564.
Pedersen, M.F., Stæhr, 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.
Pickett, S.T. (1989) Space-for-time substitution as an alternative to long-term studies. In Lickens, G.E. (ed.) Long-term studies in ecology. New York, NY: Springer, pp. 110135.
Roa, R. (1992) Design and analysis of multiple-choice feeding-preference experiments. Oecologia 89, 509515.
Rossi, F., Olabarria, C., Incera, M. and Garrido, J. (2010) The trophic significance of the invasive seaweed Sargassum muticum in sandy beaches. Journal of Sea Research 63, 5261.
Schultheis, E.H., Berardi, A.E. and Lau, J.A. (2015) No release for the wicked: enemy release is dynamic and not associated with invasiveness. Ecology 96, 24462457.
Sotka, E.E. (2005) Local adaptation in host use among marine invertebrates. Ecology Letters 8, 448459.
Strayer, D.L., Eviner, V.T., Jeschke, J.M. and Pace, M.L. (2006) Understanding the long-term effects of species invasions. Trends in Ecology and Evolution 21, 645651.
Strong, D.R. Jr, McCoy, E.D. and Rey, J.R. (1977) Time and the number of herbivore species: the pests of sugarcane. Ecology 58, 167175.
Strong, J.A., Maggs, C.A. and Johnson, M.P. (2009) The extent of grazing release from epiphytism for Sargassum muticum (Phaeophyceae) within the invaded range. Journal of the Marine Biological Association of the United Kingdom 89, 303314.
Šúri, M., Huld, T.A. and Dunlop, E.D. (2007) Potential of solar electricity generation in the European Union member states and candidate countries. Solar Energy 81, 12951305.
Thomaz, S.M., Agostinho, A.A., Gomes, L.C., Silveira, M.J., Rejmanek, M., Aslan, C.E. and Chow, E. (2012) Using space-for-time substitution and time sequence approaches in invasion ecology. Freshwater Biology 57, 24012410.
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 Maine Research 60, 5058.
Thomsen, M.S., Wernberg, T., Tuya, F. and Silliman, B.R. (2009) Evidence for impacts of non-indigenous macroalgae: a meta-analysis of experimental field studies. Journal of Phycology 45, 812819.
Toth, G.B., Karlsson, M. and Pavia, H. (2007) Mesoherbivores reduce net growth and induce chemical resistance in natural seaweed populations. Oecologia 152, 245255.
Trowbridge, C.D. (2004) Emerging associations on marine rocky shores: specialist herbivores on introduced macroalgae. Journal of Animal Ecology 73, 294308.
Van Alstyne, K.L. (1995) Comparison of three methods for quantifying brown algal polyphenolic compounds. Journal of Chemical Ecology 21, 4558.
Van Alstyne, K.L. and Paul, V.J. (1990) The biogeography of polyphenolic compounds in marine macroalgae: temperate brown algal defenses deter feeding by tropical herbivorous fishes. Oecologia 84, 158163.
Vesakoski, O., Rautanen, J., Jormalainen, V. and Ramsay, T. (2009) Divergence in host use ability of a marine herbivore from two habitat types. Journal of Evolutionary Biology 22, 15451555.
Vicente, J.R., Pereira, H.M., Randin, C.F., Goncalves, J., Lomba, A., Alves, P., Metzger, J., Cezar, M., Guisan, A. and Honrado, J. (2014) Environment and dispersal paths override life strategies and residence time in determining regional patterns of invasion by alien plants. Perspectives in Plant Ecology, Evolution and Systematics 16, 110.
Viejo, R.M. (1999) Mobile epifauna inhabiting the invasive Sargassum muticum and two local seaweeds in northern Spain. Aquatic Botany 64, 131149.
Watanabe, J.M. (1984) Food preference, food quality and diets of three herbivorous gastropods (Trochidae: Tegula) in a temperate kelp forest habitat. Oecologia 62, 4752.
Watson, D.C. and Norton, T.A. (1987) The habitat and feeding preferences of Littorina obtusata and L. mariae Sacchi et Rastelli. Journal of Experimental Marine Biology and Ecology 112, 6172.
Wernberg, T., Thomsen, M.S., Staehr, P.A. and Pedersen, M.F. (2004) Epibiota communities of the introduced and indigenous macroalgal relatives Sargassum muticum and Halidrys siliquosa in Limfjorden (Denmark). Helgoland Marine Research 58, 154161.
Whelan, R.J. (1982) Response of slugs to unacceptable food items. Journal of Applied Ecology 19, 7987.
Williams, G.A. and Brailsford, T.J. (1998) Temporal variation in parasite loading in relation to life history patterns of Littorina obtusata and L. fabalis . Hydrobiologia 378, 115127.
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, 327359.
Willis, A.J., Thomas, M.B. and Lawton, J.H. (1999) Is the increased vigour of invasive weeds explained by a trade-off between growth and herbivore resistance? Oecologia 120, 632640.
Withers, R.G., Farnham, W.F., Lewey, S., Jephson, N.A., Haythorn, J.M. and Gray, P.W.G. (1975) The epibionts of Sargassum muticum in British waters. Marine Biology 31, 7986.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Journal of the Marine Biological Association of the United Kingdom
  • ISSN: 0025-3154
  • EISSN: 1469-7769
  • URL: /core/journals/journal-of-the-marine-biological-association-of-the-united-kingdom
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Full text views

Total number of HTML views: 8
Total number of PDF views: 58 *
Loading metrics...

Abstract views

Total abstract views: 267 *
Loading metrics...

* Views captured on Cambridge Core between 22nd August 2017 - 19th August 2018. This data will be updated every 24 hours.