Advertisement

Hydrobiologia

, Volume 669, Issue 1, pp 157–165 | Cite as

Mesograzers prefer mostly native seaweeds over the invasive brown seaweed Sargassum muticum

  • Aschwin H. EngelenEmail author
  • Nuno Henriques
  • Carla Monteiro
  • Rui Santos
Primary Research Paper

Abstract

Introduced algae form globally an increasing problem. Grazing on invaders could provide communities with resistance to algal invasions. In this study, we experimentally tested the food choice of mesoherbivores for native macroalgae versus the invader Sargassum muticum. We performed food choice experiments with common grazers (Gammarus insensibilis, Hydrobia ulvae and Stenosoma nadejda) and both the brown algal invader Sargassum muticum and its native macroalgal competitors, from both the south (Cystoseira humilis, Stypocaulon scoparium, Cladostephus spongiosus, Dictyota dichotoma, Dictyopteris polypodioides, Sargassum vulgare) and southwest (Cystoseira humilis) coast of Portugal. We tested whether (i) the invader affects the growth rates of native macro algae, and (ii) the grazers have a food preference for S. muticum compared to native macroalgae. The presence of S. muticum did not affect the growth rates of any of the native species. Grazers affected the growth rate of all seaweeds, but S. muticum had the highest growth rates with and without grazers. For the south coast set of species, Stypocaulon scoparium was the most and S. muticum was the least or among the least preferred by grazers. The grazers from the southwest coast did not show a specific preference for C. humilis or S. muticum. Contrary to our expectations the food choice of mesoherbivores may provide S. muticum with some competitive advantage on the Portuguese south coast, but this may not be applicable to the Southwest communities.

Keywords

Food choice Invasion theory Sargassum muticum Seaweed–grazer interaction 

Notes

Acknowledgments

We are grateful to the Ramalhete staff for provision of laboratory facilities and their technical help. Comments and suggestions of two anonymous reviewers improved an early version of this paper. We would like to acknowledge funding by the Portuguese Science Foundation (FCT) through the project grant POCI/MAR/55377/2004 and through the scholarship SFRH/BPD/7153/2001 to AHE financed under the ‘Programa Operacional Ciência e Inovaçao 2010 (POCI 2010) do Quadro Comunitário de Apoio III e comparticipado pelo Fundo Comunitário Europeu FEDER.

References

  1. Abelho, M. & M. C. Molles Jr, 2009. Effect of introduced exotic tree litter on consumption patterns of the introduced exotic isopod Armadillidium vulgare. European Journal of Soil Biology 45: 306–311.CrossRefGoogle Scholar
  2. Amsler, C. D., 2001. Induced defenses in macroalgae: the herbivore makes a difference. Journal of Phycology 37: 353–356.CrossRefGoogle Scholar
  3. Arrontes, J., 1999. On the evolution of interactions between marine mesoherbivores and algae. Botanica Marina 42: 137–155.CrossRefGoogle Scholar
  4. Baker, H. G., 1974. The evolution of weeds. Annual Reviews of Ecology and Systematics 5: 1–24.CrossRefGoogle Scholar
  5. Bärlocher, F., 2005. A primer for statistical analysis. In Graça, M. A. S., F. Bärlocher & M. O. Gessner (eds), Methods to Study Litter Decomposition: A Practical Guide. Springer, The Netherlands: 313–329.CrossRefGoogle Scholar
  6. Brawley, S. H., 1992. Mesoherbivores. In John, D. M., S. J. Hawkins & J. H. Price (eds), Plant–Animal Interactions in the Marine Benthos. Systematics Association Special Volume 46. Clarendon Press, Oxford: 235–263.Google Scholar
  7. Britton-Simmons, K. H., 2004. Direct and indirect effects of the introduced alga, Sargassum muticum (Yendo), in subtidal kelp communities of Washington State, USA. Marine Ecology Progress Series 277: 61–78.CrossRefGoogle Scholar
  8. Castello, J. & J. L. Carballo, 2001. Isopod fauna, excluding Epicaridea, from the Strait of Gibraltar and nearby areas (Southern Iberian Peninsula). Sciencia Marina 65: 221–241.Google Scholar
  9. Ceh, J., M. Molis, T. M. Dzeha & M. Wahl, 2005. Induction and reduction of antihervibore defenses in brown and red macroalgae off the Kenyan Coast. Journal of Phycology 41: 726–731.CrossRefGoogle Scholar
  10. Colautti, R. I., A. Ricciardi, I. Ä. Grigorovich & H. J. MacIsaac, 2004. Is invasion success explained by the enemy release hypothesis? Ecological Letters 7: 721–733.CrossRefGoogle Scholar
  11. Critchley, A. T., 1983. The establishment and increase of Sargassum muticum (Yendo) Fensholt populations within the Solent area of southern Britain. II. An investigation of the increase in canopy cover of the alga at low water. Botanica Marina 26: 547–552.CrossRefGoogle Scholar
  12. Daehler, C. C., 2003. Performance comparisons of co-occurring native and alien invasive plants: implications for Conservation and Restoration. Annual Reviews of Ecology, Evolution and Systematics 34: 183–211.CrossRefGoogle Scholar
  13. Díaz, E., C. Güldenzoph, M. Molis, C. McQuaid & M. Wahl, 2006. Variability in grazer-mediated defensive responses of green and red macroalgae on the south coast of South Africa. Marine Biology 149: 1301–1311.CrossRefGoogle Scholar
  14. Diaz-Villa, T., M. Sansón & J. Afonso-Carrillo, 2005. Seasonal variations in growth and reproduction of Sargassum orotavicum (Fucales, Phaeophyceae) from the Canary Islands. Botanica Marina 48: 18–29.CrossRefGoogle Scholar
  15. Druehl, L., 1973. Marine transplantations. Science 170: 12.CrossRefGoogle Scholar
  16. Elton, C. S., 1958. The Ecology of Invasions by Animals and Plants. Methuen and Co. Ltd, London: 196.Google Scholar
  17. Engelen, A. & R. Santos, 2009. Which demographic traits determine population growth in the invasive brown seaweed Sargassum muticum? Journal of Ecology 97: 675–684.CrossRefGoogle Scholar
  18. Engelen, A. H., A. M. Breeman, J. L. Olsen, W. T. Stam & P. Åberg, 2005. Life history flexibility allows Sargassum polyceratium to persist in different environments subjected to stochastic disturbance events. Coral Reefs 24: 670–680.CrossRefGoogle Scholar
  19. Engelen, A. H., C. Espirito-Santo, T. Simões, C. Monteiro, R. O. P. Santos, E. A. Serrão & G. A. Pearson, 2008. Periodicity of egg expulsion and germling release in the competing native brown seaweed Cystoseira humilis and the invader Sargassum muticum, in Portugal. European Journal of Phycology 43: 275–282.CrossRefGoogle Scholar
  20. Fernández, C., 1999. Ecology of Sargassum muticum (Phaeophyta) on the North Coast of Spain: IV. Sequence of Colonization on a Shore. Botanica Marina 42: 553–562.CrossRefGoogle Scholar
  21. Gollan, J. R. & J. T. Wright, 2006. Limited grazing pressure by native herbivores on the invasive seaweed Caulerpa taxifolia in a temperate Australian estuary. Marine and Freshwater Research 57: 685–694.CrossRefGoogle Scholar
  22. Guerra-Garcia, J. M., M. Ros & J. A. Sánchez, 2009. Isopods, tanaids and cumaceans (Crustacea, Peracarida) associated to the seaweed Stypocaulon scoparium in the Iberian Peninsula. Zoologica Baetica 20: 35–48.Google Scholar
  23. Hay, M. E., J. E. Duffy, C. A. Pfister & W. Fenical, 1987. Chemical defense against different marine herbivores: are amphipods insect equivalents? Ecology 68: 1567–1580.CrossRefGoogle Scholar
  24. Hemmi, A., T. Honkanen & V. Jormalainen, 2004. Inducible resistance to herbivory in Fucus vesiculosus – duration, spreading and variation with nutrient availability. Marine Ecology Progress Series 273: 109–120.CrossRefGoogle Scholar
  25. Jernakoff, P., A. Brearley & J. Nielsen, 1996. Factors affecting grazer–epiphyte interactions in temperate seagrass meadows. Oceanography, Marine Biology Annual Reviews 34: 109–162.Google Scholar
  26. Jormalainen, V., T. Honkanen & N. Heikkila, 2001. Feeding preferences and performance of a marine isopod on seaweed hosts: cost of habitat specialization. Marine Ecology progress series 220: 219–230.CrossRefGoogle Scholar
  27. Keane, R. M. & M. J. Crawley, 2002. Exotic plant invasions and the enemy release hypothesis. Trends in Ecology and Evolution 17: 164–170.CrossRefGoogle Scholar
  28. Lubchenco, J., 1982. Effects of grazers and algal competitors on fucoid colonization in tide pools. Journal of Phycology 18: 544–550.CrossRefGoogle Scholar
  29. Lubchenco, J., 1983. Littorina and Fucus: effects of herbivores, substratum heterogeneity, and plant escapes during succession. Ecology 64: 1116–1123.CrossRefGoogle Scholar
  30. Lyons, D. A. & R. E. Scheibling, 2009. Range expansion by invasive marine algae: rates and patterns of spread at a regional scale. Diversity and Distributions 15: 762–775.CrossRefGoogle Scholar
  31. Mack, R. N., D. Simberloff, W. M. Lonsdale, H. Evans, M. Clout & F. A. Bazzaz, 2000. Biological invasions: causes, epidemiology, global consequences, and control. Ecological Applications 10: 689–710.CrossRefGoogle Scholar
  32. Maron, J. L. & M. Vilà, 2001. When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses. Oikos 95: 361–373.CrossRefGoogle Scholar
  33. Marques, J. C., 1989. Amphipoda (Crustaceae) bentónicos da costa portuguesa: estudo taxonómico, ecólogico e biogeográfico. PhD thesis, Universidade de Coimbra, Coimbra, Portugal.Google Scholar
  34. Mitchell, C. E. & A. G. Power, 2003. Release of invasive plant species from fungal and viral pathogens. Nature 421: 625–627.PubMedCrossRefGoogle Scholar
  35. Mitchell, C. E., A. A. Agrawal, J. D. Bever, G. S. Gilbert, R. A. Hufbauer, J. N. Klironomos, J. L. Maron, W. F. Morris, I. M. Parker, A. G. Power, E. W. Seabloom, M. E. Torchin & D. P. Vázquez, 2006. Biotic interactions and plant invasions. Ecology Letters 9: 726–740.PubMedCrossRefGoogle Scholar
  36. Monteiro, C. A., A. H. Engelen & R. O. P. Santos, 2009. Macro- and mesoherbivores prefer native seaweeds over the invasive brown seaweed Sargassum muticum: a potential regulating role on invasions. Marine Biology 156: 2505–2515.CrossRefGoogle Scholar
  37. Parker, J. D., D. E. Burkepile & M. E. Hay, 2006. Opposing effects of native and exotic herbivores on plant invasions. Science 311: 1459–1461.PubMedCrossRefGoogle Scholar
  38. Paul, N. A. & M. E. Hay, 1986. Seaweed susceptibility to herbivory: chemical and morphological correlates. Marine Ecology Progress Series 33: 255–264.CrossRefGoogle Scholar
  39. Paula, D. E. J. & D. E. C. Oliveira, 1982. Wave exposure and ecotypical differentiation in Sargassum cymosum (Phaeophyta-Fucales). Phycologia 21: 145–153.CrossRefGoogle Scholar
  40. Pavia, H. & G. B. Toth, 2000. Influence of light and nitrogen on the phlorotannin content of the brown seaweeds Ascophyllum nodosum and Fucus vesiculosus. Hydrobiologia 440: 299–305.CrossRefGoogle Scholar
  41. Petraitis, P. S., 1987. Factors organizing rocky intertidal communities of New England: herbivory and predation in sheltered bays. Journal of Experimental Marine Biology and Ecology 109: 117–136.CrossRefGoogle Scholar
  42. Pimentel, D., L. Lach, R. Zuniga & D. Morison, 2000. Environmental and economic costs of non-indigenous species in the United States. BioScience 50: 53–65.CrossRefGoogle Scholar
  43. Richardson, D. M., P. Pyšek, M. Rejmánek, M. G. Barbour & F. D. Panetta, 2000. Naturalization and invasion of alien plants: concepts and definitions. Diversity and Distribution 6: 93–107.CrossRefGoogle Scholar
  44. Roa, R., 1992. Design and analysis of multiple-choice feeding preference experiments. Oecologia 89: 509–515.Google Scholar
  45. Rohde, S., M. Molis & M. Wahl, 2004. Regulation of anti-herbivore defence by Fucus vesiculosus in response to various cues. Journal of Ecology 92: 1011–1018.CrossRefGoogle Scholar
  46. Roy, J., 1990. In search of the characteristics of plant invaders. In di Castri, F., A. J. Hansen & M. Debussche (eds), Biological Invasions in Europe and the Mediterranean Basin. Kluwer Academic, Dordrecht: 463.Google Scholar
  47. Sánchez, Í., C. Fernández & J. Arrontes, 2005. Long-term changes in the structure of intertidal assemblages after invasion by Sargassum muticum (Phaeophyta). Journal of Phycology 41: 942–949.CrossRefGoogle Scholar
  48. Schiffman, P. M., 1997. Animal-mediated dispersal and disturbance: driving forces behind alien plant naturalization. Chapter 7. In Luken, J. O. & J. W. Thieret (eds), Assessment and Management of Plant Invasions. Springer-Verlag, New York: 324.Google Scholar
  49. Schories, D., J. Anibal, A. S. Chapman, E. Herre, I. Isaksson, A. I. Lillebö, L. Pihl, K. Reise, M. Sprung & M. Thiel, 2000. Flagging greens: hydrobiid snails as substrata for the development of green algal mats (Enteromorpha spp.) on tidal mats of North Atlantic coasts. Marine Ecologu Progress Series 199: 127–136.CrossRefGoogle Scholar
  50. Siemann, E. & W. E. Rogers, 2003. Increased competitive ability of an invasive tree may be limited by an invasive beetle. Ecological Applications 13: 1503–1507.CrossRefGoogle Scholar
  51. Sotka, E. E., R. B. Taylor & M. E. Hay, 2002. Tissue-speciWc induction of resistance to herbivores in a brown seaweed: the importance of direct grazing versus waterborne signals from grazed neighbors. Journal of Experimental Marine Biology and Ecology 277: 1–12.CrossRefGoogle Scholar
  52. Southward, A. J. & E. C. Southward, 1978. Recolonization of rocky shores in Cornwall after use of toxic dispersants to clean up the Torrey Canyon spill. Journal of Fisheries Research Board Canada 35: 682–706.CrossRefGoogle Scholar
  53. Staehr, P. A., M. F. Pedersen, M. S. Thomsen, T. Wernberg & D. Krause-Jensen, 2000. Invasion of Sargassum muticum in Limfjorden (Denmark) and its possible impact on the indigenous macroalgal community. Marine Ecology Progress Series 207: 79–88.CrossRefGoogle Scholar
  54. Thomsen, M. S. & K. J. McGlathery, 2007. Stress tolerance of the invasive macroalgae Codium fragile and Gracilaria vermiculophylla in a soft-bottom turbid lagoon. Biological Invasions 9: 499–513.CrossRefGoogle Scholar
  55. Torchin, M. E. & C. E. Mitchell, 2004. Parasites, pathogens, and invasions by plants and animals. Frontiers in Ecology and Environment 2: 183–190.CrossRefGoogle Scholar
  56. Underwood, A. J., 1997. Experiments in Ecology: Their Logical Design and Interpretation Using Analysis of Variance. Cambridge University Press, Cambridge: 184–185. ISBN 0 521 55696 1.Google Scholar
  57. Vermeij, M. J. A., T. B. Smith, M. L. Dailer & C. M. Smith, 2009. Release from native herbivores facilitates the persistence of invasive marine algae: a biogeographical comparison of the relative contribution of nutrents and herbivory to invasion success. Biological Invasions 11: 1463–1474.CrossRefGoogle Scholar
  58. Weidner, K., B. G. Lages, B. A. P. da Gama, M. Molis, M. Wahl & R. C. Pereira, 2004. Effects of mesograzers and nutrient levels on the induction of defenses in several Brazilian macroalgae. Marine Ecology Progress Series 283: 113–125.CrossRefGoogle Scholar
  59. Wernberg, T., M. S. Thomsen, P. A. Staehr & M. F. Pedersen, 2000. Comparative phenology of Sargassum muticum and Halidrys siliquosa (Phaeophyceae: Fucales) in Limfjorden, Denmark. Botanica Marina 43: 31–39.Google Scholar
  60. Wikström, S. A., M. B. Steinarsdóttir, L. Kautsky & H. Pavia, 2006. Increased chemical resistance explains low herbivore colonization of introduced seaweed. Oecologia 148: 593–601.PubMedCrossRefGoogle Scholar
  61. Williams, G. A., 1990. Littorina mariae – a factor structuring low shore communities? Hydrobiologia 193: 139–146.CrossRefGoogle Scholar
  62. Worm, B. & A. R. O. Chapman, 1998. Relative effects of elevated grazing pressure and competition by a red algal turf on two post-settlement stages of Fucus evanescens C. Ag. Journal of Experimental Marine Biology and Ecology 220: 247–268.CrossRefGoogle Scholar
  63. Yun, H. Y., J. Cruz, M. Treitschke, M. Wahl & M. Molis, 2007. Testing for the induction of anti-herbivory defences in four Portuguese macroalgae by direct and water-borne cues of grazing amphipods. Helgolander Marine Research 61: 203–209.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Aschwin H. Engelen
    • 1
    Email author
  • Nuno Henriques
    • 1
  • Carla Monteiro
    • 1
  • Rui Santos
    • 1
  1. 1.ALGAE Research Group, CCMAR, CIMAR-Laboratório AssociadoUniversidade do Algarve, FCMAFaroPortugal

Personalised recommendations