Biological Invasions

, Volume 15, Issue 1, pp 171–183 | Cite as

Faunal differences between the invasive brown macroalga Sargassum muticum and competing native macroalgae

  • Aschwin H. EngelenEmail author
  • Ana L. Primo
  • Teresa Cruz
  • Rui Santos
Original Paper


Interactions between macroalgae and their associated fauna are of great interest for marine invasions, because fauna may increase the biotic resistance of a system and macroalgal invasions may cause shifts in faunal composition. We tested for differences in faunal community structure between a macroalgal invader, Sargassum muticum, and several native macroalgae in intertidal pools on both the west and south coast of Portugal. On each coast, we compared the faunal diversity and composition associated with the invader with that of the competing native macroalga(e). On the west coast, the diversity of the fauna associated with S. muticum was equal to or lower than with the native competitor, Cystoseira humilis. Fauna composition differed between S. muticum and C. humilis at both locations, but within each species, no differences between locations were detected. In contrast, the fauna diversity on S. muticum of the south coast varied among locations. S. muticum fauna differed from the fauna of all native macroalgae at one location, but only from three out of seven native macroalgae at the other location. Discriminating fauna species did not show a consistent pattern towards higher or lower abundances in S. muticum compared to most native macroalgae, and species-specific contributions were small. Differences in fauna community also depended on the identity of the native macroalga. In conclusion, the fauna associated with S. muticum differs from many native brown macroalgae, but these differences were not consistent as they depend both on the native macroalgal species and on location. This invader does not seem to have a severe negative impact on local macroalgae-associated fauna.


Invasion Sargassum muticum Associated fauna Biodiversity Community composition Native macroalgae 



We thank Allison Schmidt, Erik-Jan Malta, Mads Thomsen, Ladd Johnson as well as two anonymous referees for their valuable comments and suggestions on the manuscript. This study was funded by FCT project POCI/MAR/55377/2004, and A.H.E. was supported by FCT scholarship SFRH/BPD/7153/2001 and SFRH/BPD/63703/2009.


  1. Ambrose RF, Nelson BV (1982) Inhibition of giant kelp recruitment by an introduced brown alga. Bot Mar 25:265–267. doi: 10.1515/botm.1982.25.6.265,//1982 CrossRefGoogle Scholar
  2. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46. doi: 10.1046/J.1442-9993.2001.01070.X Google Scholar
  3. Anderson MJ (2004) PERMDISP: a FORTRAN computer program for permutational analysis of multivariate dispersions (for any two-factor ANOVA design) using permutation tests. University of Auckland, New ZealandGoogle Scholar
  4. Anderson MJ (2005) PERMANOVA permutational multivariate analysis of variance.
  5. Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA + for PRIMER: guide to software and statistical methods. PRIMER-E, PlymouthGoogle Scholar
  6. Ayres DR, Strong DR, Baye P (2003) Spartina foliosa (Poaceae)—a common species on the road to rarity. Madronõ 50:209–213Google Scholar
  7. Battershill C, Miller K, Cole R (1998) The understorey of marine invasions. Seaf N Z 6:31–33Google Scholar
  8. Bellan-Santini D, Arnaud PM, Bellan G, Verlaque M (1996) The influence of the introduced tropical alga Caulerpa taxifolia, on the biodiversity of the Mediterranean marine biota. J Mar Biol Assoc UK 76:235–237CrossRefGoogle Scholar
  9. Boudouresque CF, Bellan-Santini D, Belsher T, Duclerc J, Durand-Clement M, Francour P, Harmelin-Vivien M, Henocque Y, Meinesz A, Pesando D, Pietra F, Verlaque M (1992) The introduction of the green alga Caulerpa taxifolia into the Mediterranean: the repercussions for the indigenous communities. Mésogée 52:88–89Google Scholar
  10. Britton-Simmons KH (2004) Direct and indirect effects of the introduced alga, Sargassum muticum (Yendo), in subtidal kelp communities of Washington State, USA. Mar Ecol Prog Ser 277:61–78. doi: 10.3354/meps277061 CrossRefGoogle Scholar
  11. Buschbaum C, Chapman AS, Saier B (2006) How an introduced seaweed can affect epibiota diversity in different coastal systems. Mar Biol 148:743–754CrossRefGoogle Scholar
  12. Clark RP, Edwards MS, Foster MS (2004) Effects of shade from multiple kelp canopies on an understory algal assemblage. Mar Ecol Prog Ser 267:107–119CrossRefGoogle Scholar
  13. Clarke KR, Gorley RN (2006) PRIMER v6 users manual and tutorial. PRIMER-E, PlymouthGoogle Scholar
  14. Cosson J (1999) On the progressive disappearance of Laminaria digitata on the coasts of Calvados (France) (in French). Cryptogam Algologie 20:35–42CrossRefGoogle Scholar
  15. Critchley AT, Farnham WF, Morrell SL (1986) An account of the attempted control of an introduced marine alga, Sargassum muticum, in Southern England. Biol Conserv 35:313–332CrossRefGoogle Scholar
  16. Critchley AT, de Visscher RPM, Nienhuis PH (1990) Canopy characteristics of the brown alga Sargassum muticum in Lake Grevelingen, south west Netherlands. Hydrobiologia 204(205):211–217CrossRefGoogle Scholar
  17. Dean RL, Connell JH (1987) Marine invertebrates in an algal succession. I. Variations in abundance and diversity with succession. J Exp Mar Biol Ecol 109:195–215CrossRefGoogle Scholar
  18. Drouin A, McKindsey CW, Johnson LE (2011) Higher abundances and diversity in faunal assemblages with the invasion of Codium fragile ssp. fragile in eelgrass meadows. Mar Ecol Prog Ser 424:105–117CrossRefGoogle Scholar
  19. Duggins DO, Eckman JE, Sewell AT (1990) Ecology of understory kelp environments II. Effects of kelp on recruitment of benthic invertebrates. J Exp Mar Biol Ecol 143:27–45CrossRefGoogle Scholar
  20. Edgar GJ (1983) The ecology of South-Tasmanian phytal animal communities IV. Factors affecting the distribution and ampithoid amphipods among algae. J Exp Mar Biol 70:205–225CrossRefGoogle Scholar
  21. Engelen AH, Santos R (2009) Which demographic traits determine population growth in the invasive brown seaweed Sargassum muticum? J Ecol 97(4):675–684CrossRefGoogle Scholar
  22. Engelen AH, Espirito-Santo C, Simões T, Monteiro C, Santos R, Serrão E, Pearson G (2008) Periodicity of egg expulsion and germling release in the competing native brown seaweed Cystoseira humilis and the invader Sargassum muticum, in Portugal. Eur J Phycol 43:275–282CrossRefGoogle Scholar
  23. Farrell P, Fletcher RL (2006) An investigation of dispersal of the introduced brown alga Undaria pinnatifida (Harvey) Suringar and its competition with some species on the man-made structures of Torquay Marina (Devon. UK). J Exp Mar Biol Ecol 334:236–243CrossRefGoogle Scholar
  24. Gestoso I, Olabarria C, Troncoso JS (2010) Variability of epifaunal assemblages associated with native and invasive macroalgae. Mar Freshw Res 61:724–731CrossRefGoogle Scholar
  25. Giver K (1999) Effects of the invasive seaweed Sargassum muticum on native marine communities in northern Puget sound, Washington. MS thesis, Western Washington University, BellinghamGoogle Scholar
  26. Gribben PE, Byers JE, Clements M, McKenzie LA, Steinberg PD, Wright JT (2009) Behavioural interactions between ecosystem engineers control community species richness. Ecol Lett 12:1127–1136PubMedCrossRefGoogle Scholar
  27. Gunnill FC (1983) Seasonal variation in the invertebrate faunas of Pelvetia fastigata (Fucaceae): effects of plant size and distribution. Mar Biol 73:115–130CrossRefGoogle Scholar
  28. Hay ME, Steinberg PD (1992) The chemical ecology of plant-herbivore interactions in marine versus terrestrial communities. In: Rosenthal GA, Berenbaum MR (eds) Herbivores: their interaction with secondary metabolites, evolutionary and ecological processes, vol 2. Academic Press, San Diego, pp 371–413Google Scholar
  29. Hay ME, Duffy JE, Fenical W (1990) Host-plant specialization decreases predation on a marine amphipod: an herbivore in plant’s clothing. Ecology 71:733–743CrossRefGoogle Scholar
  30. Hobson ES, Chess JR (1976) Trophic interactions among fishes and zooplankters near shore at Santa Catalina Island, California. Fish Bull US 74:567–598Google Scholar
  31. Johnson CR, Mann KH (1986) The importance of plant defence abilities to the structure of subtidal seaweed communities: the kelp Laminaria longicruris de la Pylaie survives grazing by the snail Lacuna vincta (Montagu) at high population densities. J Exp Mar Biol Ecol 97:231–267CrossRefGoogle Scholar
  32. Lima FP, Ribeiro PA, Queiroz N, Hawkins SJ, Santos AM (2007) Do distributional shifts of northern and southern species of algae match the warming pattern? Global Change Biol 13:1–13CrossRefGoogle Scholar
  33. McEvoy PB, Coombs EM (1999) Biological control of plant invaders: regional patterns, field experiments, and structured population models. Ecol Appl 9:387–401CrossRefGoogle Scholar
  34. McKinnon JG, Gribben PE, Davis AR, Jolley DF, Wright JT (2009) Differences in soft-sediment macrobenthic assemblages invaded by Caulerpa taxifolia compared to uninvaded habitats. Mar Ecol Prog Ser 380:59–71CrossRefGoogle Scholar
  35. Neira C, Grosholz ED, Levin LA, Blake R (2006) Mechanisms generating modification of benthos following tidal flat invasion by a Spartina (alterniflora 3 foliosa) hybrid. Ecol Appl 16:1391–1404PubMedCrossRefGoogle Scholar
  36. Pacciardi L, De Biasi AM, Piazzi L (2011) Effects of Caulerpa racemosa invasion on soft bottom assemblages in the Western Mediterranean Sea. Biol Invasion 13:2677–2690CrossRefGoogle Scholar
  37. Parker IM (2000) Invasion dynamics of Cystisus scoparius: a matrix model approach. Ecol Appl 10:726–743CrossRefGoogle Scholar
  38. Parker IM, Simberloff D, Lonsdale WM, Goodell K, Wonham M, Kareiva PM, Williamson MH, Von Holle B, Moyle PB, Byers BE, Goldwasser L (1999) Impact: towards a framework for understanding the ecological effect of invaders. Biol Invasion 1:3–9CrossRefGoogle Scholar
  39. Pedersen MF, Staehr PA, Wernberg T, Thomsen MS (2005) Biomass dynamics of exotic Sargassum muticum and native Halidrys in Limfjorden, Denmark—Implications of species replacements on turnover rate. Aquat Bot 83:31–47CrossRefGoogle Scholar
  40. Pimentel D, Lach L, Zuniga R, Morison D (2000) Environmental and economic costs of non-indigenous species in the United States. Bioscience 50:53–65CrossRefGoogle Scholar
  41. Relini G, Molinari A, Relini M, Torchia G (1998a) Confronto tra la fauna epifitica di Caulerpa taxifolia e Cymodocea nodosa. Biol Mar Mediterr 5:185–195Google Scholar
  42. Relini G, Relini M, Torchia G (1998b) Fish and epiphytic fauna on Caulerpa taxifolia and Cymodocea nodosa at Imperia (Ligurian Sea). In: Boudouresque CF, Gravez V, Meinesz A, Palluy F (eds) Third international workshop on Caulerpa taxifolia. GIS Posidonie Publications, France, pp 185–195Google Scholar
  43. Russo AR (1990) The role of seaweed complexity in structuring Hawaiian epiphytal amphipod communities. Hydrobiologia 194:1–12CrossRefGoogle Scholar
  44. Sánchez-Moyano JE, García-Adiego EM, Estacio FJ, García-Gómez JC (2000) Effect of environmental factors on the spatial distribution of the epifauna of the alga Stypocaulon scoparia in Algeciras Bay, Southern Spain. Aquat Ecol 34:355–367CrossRefGoogle Scholar
  45. Schmidt AL, Scheibling RE (2006) A comparison of epifauna and epiphytes on native kelps (Laminaria species) and an invasive alga (Codium fragile ssp. tomentosoides) in Nova Scotia, Canada. Bot Mar 49:315–330CrossRefGoogle Scholar
  46. Stæhr P, Pedersen MF, Thomsen MS, Wernberg T, Krause-Jensen D (2000) The invasion of Sargassum muticum in Limfjorden (Denmark) and its possible impact on the indigenous macroalgal community. Mar Ecol Prog Ser 207:79–88CrossRefGoogle Scholar
  47. Steinberg PD, de Nys R (2002) Chemical mediation of colonization of seaweed surfaces. J Phycol 38:621–629CrossRefGoogle Scholar
  48. Strong JA, Dring MJ, Maggs CA (2006) Colonisation and modification of soft substratum habitats by the invasive macroalga Sargassum muticum. Mar Ecol Prog Ser 321:87–97CrossRefGoogle Scholar
  49. Tanner J (2008) Utilisation of Caulerpa taxifolia as habitat by faunal assemblages in the Port River-Barker Inlet estuary. In: Deveney MR, Rowling KP, Wiltshire KH, Manning CE, Fernandes MB, Collings GK, Tanner JE (eds) Caulerpa taxifolia (M Vahl) C. Environmental risk assessment, Agardh, pp 68–81Google Scholar
  50. Taylor RB, Cole RG (1994) Mobile epifauna on subtidal brown seaweeds in northeastern New Zealand. Mar Ecol Prog Ser 115:271–282CrossRefGoogle Scholar
  51. Thomsen MS, Wernberg T, Tuya F, Silliman BR (2009) Evidence for impacts of nonindigenous macroalgae: a meta-analysis of experimental field studies. J Phycol 45:812–819CrossRefGoogle Scholar
  52. Tippets K (2002) The effects of Caulerpa taxifolia on invertebrate abundance in Agua Hedionda Lagoon, California. Report for University of California at Berkeley Environmental Sciences Senior Seminar, Berkeley, CA, pp 8Google Scholar
  53. Verlaque M, Fritayre P (1994) Modifications des communautés algales méditerranéennes en présence de l’algue envahissante Caulerpa taxifolia (Vahl) C. Agardh. Oceanol Acta 17:659–672Google Scholar
  54. Viejo RM (1999) Mobile epifauna inhabiting the invasive Sargassum muticum and two local seaweeds in northern Spain. Aquat Bot 64:131–149CrossRefGoogle Scholar
  55. Vitousek PM, Walker LR (1989) Biological invasion by Myrica faya in Hawaii: plant demography, nitrogen-fixation, ecosystem effects. Ecol Monogr 59:247–265CrossRefGoogle Scholar
  56. Vitousek PM, Mooney JA, Lubchenco JA, Melillo JM (1997) Human domination of Earth’s ecosystems. Science 277:494–499CrossRefGoogle Scholar
  57. Wernberg T, Thomsen MS, Staehr PA, Pedersen MF (2004) Epibiota communities of the introduced and indigenous macroalgal relatives Sargassum muticum and Halidrys siliquosa in Limfjorden (Denmark). Helgol Mar Res 58:154–161CrossRefGoogle Scholar
  58. Wikström SA, Kautsky L (2004) Invasion of a habitat-forming seaweed: effects on associated biota. Biol Invasions 6:141–150CrossRefGoogle Scholar
  59. Wikström SA, Steinarsdóttir MB, Kautsky L, Pavia H (2006) Increased chemical resistance explains low herbivore colonization of introduced seaweed. Oecologia 148:593–601PubMedCrossRefGoogle Scholar
  60. Wilson CM (2001) Is Sargassum muticum a benign invader of tidepools on the Pacific coast of North America?. California State University Monterey Bay, Seaside, MS thesisGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Aschwin H. Engelen
    • 1
    Email author
  • Ana L. Primo
    • 1
    • 4
  • Teresa Cruz
    • 2
    • 3
  • Rui Santos
    • 1
  1. 1.ALGAE, Marine Plant Ecology Research Group, CCMAR Centro de Ciências Do Mar, CIMAR-Laboratório Associado, FCMAUniversidade do AlgarveFaroPortugal
  2. 2.Laboratório de Ciências do Mar and Departamento de BiologiaUniversidade de ÉvoraSinesPortugal
  3. 3.Centro de OceanografiaFaculdade de Ciências da Universidade de LisboaLisbonPortugal
  4. 4.CFE - Centre for Functional Ecology, Department of Life SciencesUniversity of CoimbraCoimbraPortugal

Personalised recommendations