Hydrobiologia

, Volume 776, Issue 1, pp 35–49 | Cite as

Epiphytic macroalgae mediate the impact of a non-native alga on associated fauna

Primary Research Paper

Abstract

The introduction of a non-native, habitat-forming macroalga may have impacts on the seaweed-associated faunal community. Codium fragile subsp. fragile is a well-known and widespread algal invader that may compete with native habitat-forming macroalgae and affect ecosystem services. This alga can be abundant at semi-exposed/sheltered sites on the south-west coast of Norway, where its vertical distribution range overlaps with another canopy-forming alga, the native Fucus serratus. Whether these seaweeds support similar or dissimilar associated communities will influence the ecological impact of C. fragile subsp. fragile. Therefore, the richness and composition of fauna associated with these species was assessed by sampling at three localities. While the majority of taxa occurred on both F. serratus and C. fragile subsp. fragile, there were clear differences in community composition between them. Fauna taxa richness and community composition were also related to macroalgal epiphyte abundance, and there were a number of taxa associated to high epiphyte samples. The results suggest that shared macroalgal epiphytes lead to higher similarity between the invertebrate communities associated with C. fragile subsp. fragile and F. serratus, providing correlative evidence that epiphytic macroalgae play a role in shaping the impact of this macroalga on associated fauna.

Keywords

Codium fragile Fucus serratus Associated communities Non-native species impact Epiphyte 

Notes

Acknowledgments

C. Todt, T. Høisæter, G. Velle and H. Glenner are acknowledged for their assistance with identification of fauna, H. Glenner for valuable input into the design of this project and the anonymous referees for their comments which greatly improved this manuscript. This work was financially supported by the Research Council of Norway through the project “Towards integrated European marine research strategy and programmes—SEAS-ERA” (ERAC-CT2009-249552) within the framework of the EU ERA-Net initiative (7th Framework Program).

Supplementary material

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Supplementary material 1 (DOCX 22 kb)

References

  1. Amsler, C. D. & V. A. Fairhead, 2005. Defensive and sensory chemical ecology of brown algae. In Callow, J. A. (ed.), Advances in Botanical Research. Academic Press, Cambridge: 1–91.Google Scholar
  2. Armitage, C. S., K. Sjøtun & K. H. Jensen, 2014. Correlative evidence for competition between Fucus serratus and the introduced chlorophyte Codium fragile subsp. fragile on the southwest coast of Norway. Botanica Marina 57: 85–97.CrossRefGoogle Scholar
  3. Barange, M. & J. M. Gili, 1988. Feeding cycles and prey capture in Eudendrium racemosum (Cavolini, 1785). Journal of Experimental Marine Biology and Ecology 115: 281–293.CrossRefGoogle Scholar
  4. Barton, K., 2015. MuMIn: Multi-model inference (R package version 1.15.1). http://CRAN.R-project.org/package=MuMIn
  5. Bouck, G. B. & E. Morgan, 1957. The occurrence of Codium in Long Island waters. Bulletin of the Torrey Botanical Club 84: 384–387.CrossRefGoogle Scholar
  6. Bray, J. R. & J. T. Curtis, 1957. An ordination of the upland forest communities of southern Wisconsin. Ecological Monographs 27: 326–349.CrossRefGoogle Scholar
  7. Buschbaum, C., A. Chapman & B. Saier, 2006. How an introduced seaweed can affect epibiota diversity in different coastal systems. Marine Biology 148: 743–754.CrossRefGoogle Scholar
  8. Chadwick, S. R. & J. P. Thorpe, 1981. An investigation of some aspects of bryozoan predation by dorid nudibranchs (Mollusca: Opisthobranchia). Olsen & Olsen, Fredensborg: 51–58.Google Scholar
  9. Christie, H., N. M. Jørgensen & K. M. Norderhaug, 2007. Bushy or smooth, high or low; importance of habitat architecture and vertical position for distribution of fauna on kelp. Journal of Sea Research 58: 198–208.CrossRefGoogle Scholar
  10. Christie, H., K. M. Norderhaug & S. Fredriksen, 2009. Macrophytes as habitat for fauna. Marine Ecology Progress Series 396: 221–233.CrossRefGoogle Scholar
  11. Crisp, D. J. & G. B. Williams, 1960. Effect of extracts from fucoids in promoting settlement of epiphytic Polyzoa. Nature 188: 1206–1207.CrossRefGoogle Scholar
  12. De Burgh, M. E. & P. V. Fankboner, 1978. A nutritional association between the bull kelp Nereocystis luetkeana and its epizootic bryozoan Membranipora membranacea. Oikos 31: 69–72.CrossRefGoogle Scholar
  13. De Cáceres, M., P. Legendre & M. Moretti, 2010. Improving indicator species analysis by combining groups of sites. Oikos 119: 1674–1684.CrossRefGoogle Scholar
  14. Dromgoole, F. I., 1975. Occurrence of Codium fragile subspecies tomentosoides in New Zealand waters. New Zealand Journal of Marine and Freshwater Research 9: 257–264.CrossRefGoogle Scholar
  15. Drouin, A., C. W. McKindsey & L. E. Johnson, 2011. Higher abundance and diversity in faunal assemblages with the invasion of Codium fragile ssp. fragile in eelgrass meadows. Marine Ecology Progress Series 424: 105–117.CrossRefGoogle Scholar
  16. Edgar, G. J., 1991. Artificial algae as habitats for mobile epifauna: factors affecting colonization in a Japanese Sargassum bed. Hydrobiologia 226: 111–118.CrossRefGoogle Scholar
  17. Eilertsen, M., K. M. Norderhaug & K. Sjøtun, 2011. Does the amphipod fauna associated with epiphytes on kelp (Laminaria hyperborea) change with depth? Marine Biology Research 7: 224–234.CrossRefGoogle Scholar
  18. Engelen, A. H., A. L. Primo, T. Cruz & R. Santos, 2013. Faunal differences between the invasive brown macroalga Sargassum muticum and competing native macroalgae. Biological Invasions 15: 171–183.CrossRefGoogle Scholar
  19. Fosså, J. H. 1991. The ecology of the two-spot goby (Gobiusculus flavescens Fabricius): the potential for cod enhancement, pp. 147–155. In ICES Marine Science SymposiaGoogle Scholar
  20. Fox, J. & S. Weisberg (2011) An R Companion to Applied Regression, 2nd edn. Sage, Thousand Oaks CA http://socserv.socsci.mcmaster.ca/jfox/Books/Companion
  21. Fredriksen, S., H. Christie & B. A. Sæthre, 2005. Species richness in macroalgae and macrofauna assemblages on Fucus serratus L. (Phaeophyceae) and Zostera marina L. (Angiospermae) in Skagerrak, Norway. Marine Biology Research 1: 2–19.CrossRefGoogle Scholar
  22. Garbary, D. J., M. M. Jamieson, S. J. Fraser, C. A. Ferguson & P. S. Cranston, 2005. Ascophyllum (Phaeophyceae) and its symbionts. IX. A novel symbiosis between Halocladius variabilis (Chironomidae, Insecta) and Elachista fucicola (Elachistaceae, Phaeophyceae) from marine rocky shores of Nova Scotia. Symbiosis 40: 61–68.Google Scholar
  23. Gederaas, L., T. L. Moen, S. Skjelseth & L.-K. Larsen, 2012. Alien species in Norway—the Norwegian Black List 2012. The Norwegian Biodiversity Information Centre. http://www.artsdatabanken.no/Article/Article/133437. Accessed 15 Nov 2014
  24. Gestoso, I., C. Olabarria & J. Troncoso, 2012. Effects of macroalgal identity on epifaunal assemblages: native species versus the invasive species Sargassum muticum. Helgoland Marine Research 66: 159–166.CrossRefGoogle Scholar
  25. Gibbons, M. J., 1988. The impact of sediment accumulations, relative habitat complexity and elevation on rocky shore meiofauna. Journal of Experimental Marine Biology and Ecology 122: 225–241.CrossRefGoogle Scholar
  26. Gili, J.-M. & R. Coma, 1998. Benthic suspension feeders: their paramount role in littoral marine food webs. Trends in Ecology & Evolution 13: 316–321.CrossRefGoogle Scholar
  27. Gili, J. & R. Hughes, 1995. The ecology of marine benthic hydroids. Oceanography and Marine Biology: An Annual Review 33: 351–426.Google Scholar
  28. Gower, J., 1971. Statistical methods of comparing different multivariate analyses of the same data. Mathematics in the Archaeological and Historical Sciences 138–149Google Scholar
  29. Haavisto, F. & V. Jormalainen, 2014. Seasonality elicits herbivores’ escape from trophic control and favors induced resistance in a temperate macroalga. Ecology 95: 3035–3045.CrossRefGoogle Scholar
  30. Hacker, S. D. & R. S. Steneck, 1990. Habitat architecture and the abundance and body-size-dependent habitat selection of a phytal amphipod. Ecology 71: 2269–2285.CrossRefGoogle Scholar
  31. Hagerman, L., 1966. The macro- and microfauna associated with Fucus serratus L., with some ecological remarks. Ophelia 3: 1–43.CrossRefGoogle Scholar
  32. Hall, M. O. & S. S. Bell, 1988. Response of small motile epifauna to complexity of epiphytic algae on seagrass blades. Journal of Marine Research 46: 613–630.CrossRefGoogle Scholar
  33. Hall, M. O. & S. S. Bell, 1993. Meiofauna on the seagrass Thalassia testudinum: population characteristics of harpacticoid copepods and associations with algal epiphytes. Marine Biology 116: 137–146.CrossRefGoogle Scholar
  34. Harris, L. G. & A. C. Jones, 2005. Temperature, herbivory and epibiont acquisition as factors controlling the distribution and ecological role of an invasive seaweed. Biological Invasions 7: 913–924.CrossRefGoogle Scholar
  35. Harries, D. B., S. Harrow, J. R. Wilson, J. M. Mair & D. W. Donnan, 2007. The establishment of the invasive alga Sargassum muticum on the west coast of Scotland: a preliminary assessment of community effects. Journal of the Marine Biological Association of the United Kingdom 87: 1057–1067.CrossRefGoogle Scholar
  36. Hauser, A., M. J. Attrill & P. A. Cotton, 2006. Effects of habitat complexity on the diversity and abundance of macrofauna colonising artificial kelp holdfasts. Marine Ecology Progress Series 325: 100.CrossRefGoogle Scholar
  37. Hayward, P. J. & J. S. Ryland, 1995. Handbook of the marine fauna of North-West Europe. Oxford University Press, Oxford.Google Scholar
  38. Jackson, D. A., 1995. PROTEST: a PROcrustean randomization TEST of community environment concordance. Ecoscience 2: 297–303.Google Scholar
  39. Johnson, C. R., 2007. Seaweed invasions: conclusions and future directions. Botanica Marina 50: 451–457.Google Scholar
  40. Jones, E. & C. S. Thornber, 2010. Effects of habitat-modifying invasive macroalgae on epiphytic algal communities. Marine Ecology Progress Series 400: 87–100.CrossRefGoogle Scholar
  41. Jorde, I., 1966. Algal associations of a coastal area south of Bergen, Norway. Sarsia 23: 1–52.CrossRefGoogle Scholar
  42. Jueterbock, A., L. Tyberghein, H. Verbruggen, J. A. Coyer, J. L. Olsen, et al., 2013. Climate change impact on seaweed meadow distribution in the North Atlantic rocky intertidal. Ecology and Evolution 3: 1356–1373.CrossRefPubMedPubMedCentralGoogle Scholar
  43. Keats, D. W., D. H. Steele & G. R. South, 1987. The rôle of fleshy macroalgae in the ecology of juvenile cod (Gadus morhua L.) in inshore waters off eastern Newfoundland. Canadian Journal of Zoology 65: 49–53.CrossRefGoogle Scholar
  44. Kelaher, B. P., 2003. Changes in habitat complexity negatively affect diverse gastropod assemblages in coralline algal turf. Oecologia 135: 431–441.CrossRefPubMedGoogle Scholar
  45. Kerr, J. T. & L. Packer, 1997. Habitat heterogeneity as a determinant of mammal species richness in high-energy regions. Nature 385: 252–254.CrossRefGoogle Scholar
  46. Kruskal, J. B., 1964. Nonmetric multidimensional scaling: a numerical method. Psychometrika 29: 115–129.CrossRefGoogle Scholar
  47. Leidenberger, S., K. Harding & P. R. Jonsson, 2012. Ecology and distribution of the isopod genus Idotea in the Baltic Sea: key species in a changing environment. Journal of Crustacean Biology 32: 359–381.CrossRefGoogle Scholar
  48. Lomolino, M. V., 2000. Ecology’s most general, yet protean pattern: the species-area relationship. Journal of Biogeography 27: 17–26.CrossRefGoogle Scholar
  49. Lutz, M., A. Davis & T. Minchinton, 2010. Non-indigenous macroalga hosts different epiphytic assemblages to conspecific natives in southeast Australia. Marine Biology 157: 1095–1103.CrossRefGoogle Scholar
  50. Lüning, K., 1990. Seaweeds: Their environment, biogeography and ecophysiology. Wiley, New York.Google Scholar
  51. Lyons, D. A., K. L. Van Alstyne & R. E. Scheibling, 2007. Anti-grazing activity and seasonal variation of dimethylsulfoniopropionate-associated compounds in the invasive alga Codium fragile ssp. tomentosoides. Marine Biology 153: 179–188.CrossRefGoogle Scholar
  52. MacArthur, R. H. & J. W. MacArthur, 1961. On bird species diversity. Ecology 42: 594–598.CrossRefGoogle Scholar
  53. Martin-Smith, K. M., 1993. Abundance of mobile epifauna: the role of habitat complexity and predation by fishes. Journal of Experimental Marine Biology and Ecology 174: 243–260.CrossRefGoogle Scholar
  54. Matias, M. G., A. J. Underwood, D. F. Hochuli & R. A. Coleman, 2010. Independent effects of patch size and structural complexity on diversity of benthic macroinvertebrates. Ecology 91: 1908–1915.CrossRefPubMedGoogle Scholar
  55. Meyer, H. A. & S. S. Bell, 1989. Response of harpacticoid copepods to detrital accumulation on seagrass blades: a field experiment with Metis holothuriae (Edwards). Journal of Experimental Marine Biology and Ecology 132: 141–149.CrossRefGoogle Scholar
  56. Norderhaug, K. M., 2004. Use of red algae as hosts by kelp-associated amphipods. Marine Biology 144: 225–230.CrossRefGoogle Scholar
  57. Norderhaug, K. M., H. Christie & E. Rinde, 2002. Colonisation of kelp imitations by epiphyte and holdfast fauna; a study of mobility patterns. Marine Biology 141: 965–973.CrossRefGoogle Scholar
  58. Norderhaug, K. M., S. Fredriksen & K. Nygaard, 2003. Trophic importance of Laminaria hyperborea to kelp forest consumers and the importance of bacterial degradation to food quality. Marine Ecology Progress Series 255: 135–144.CrossRefGoogle Scholar
  59. Norderhaug, K. M., H. Christie, J. H. Fosså & S. Fredriksen, 2005. Fish–macrofauna interactions in a kelp (Laminaria hyperborea) forest. Journal of the Marine Biological Association of the United Kingdom 85: 1279–1286.CrossRefGoogle Scholar
  60. Norwegian Biodiversity Information Centre, 2012. Artsdatabanken; Codium fragile. http://databank.artsdatabanken.no/FremmedArt2012/N65924. Accessed 5 April 2013
  61. Nyberg, C. & I. Wallentinus, 2005. Can species traits be used to predict marine macroalgal introductions? Biological Invasions 7: 265–279.CrossRefGoogle Scholar
  62. Oksanen, J., F. G. Blanchet, R. Kindt, P. Legendre, P. R. Minchin, et al., 2013. vegan: Community Ecology package (R package version 2.0-10). http://CRAN.R-project.org/package=vegan
  63. Pinheiro, J., D. Bates, S. DebRoy, D. Sarkar & R Development Core Team, 2015. nlme: Linear and Nonlinear Mixed Effects Models (R package version 3.1-122)Google Scholar
  64. Potts, G. W., J. Edwards & M. J. Costello, 1990. The diet of the two-spot goby, Gobiusculus flavescens (Pisces). Journal of the Marine Biological Association of the United Kingdom 70: 329–342.CrossRefGoogle Scholar
  65. Provan, J., D. Booth, N. P. Todd, G. E. Beatty & C. A. Maggs, 2008. Tracking biological invasions in space and time: elucidating the invasive history of the green alga Codium fragile using old DNA. Diversity and Distributions 14: 343–354.CrossRefGoogle Scholar
  66. R Development Core Team, 2014. R: A language and environment for statistical computing R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
  67. Ryland, J. S., 1959. Experiments on the selection of algal substrates by polyzoan larvae. Journal of Experimental Biology 36: 613–631.Google Scholar
  68. Råberg, S. & L. Kautsky, 2008. Grazer identity is crucial for facilitating growth of the perennial brown alga Fucus vesiculosus. Marine Ecology Progress Series 361: 111–118.CrossRefGoogle Scholar
  69. Salvaterra, T., D. Green, T. Crowe & E. O’Gorman, 2013. Impacts of the invasive alga Sargassum muticum on ecosystem functioning and food web structure. Biological Invasions 15: 2563–2576.CrossRefGoogle Scholar
  70. Scheibling, R. E. & P. Gagnon, 2006. Competitive interactions between the invasive green alga Codium fragile ssp. tomentosoides and native canopy-forming seaweeds in Nova Scotia (Canada). Marine Ecology Progress Series 325: 1–14.CrossRefGoogle Scholar
  71. Schmidt, A. L. & R. E. Scheibling, 2006. A comparison of epifauna and epiphytes on native kelps (Laminaria species) and an invasive alga (Codium fragile ssp. tomentosoides) in Nova Scotia, Canada. Botanica Marina 49: 315–330.CrossRefGoogle Scholar
  72. Shepard, R. N., 1962. The analysis of proximities: multidimensional scaling with an unknown distance function. I. Psychometrika 27: 125–140.CrossRefGoogle Scholar
  73. Silva, P. C., 1955. The dichotomous species of Codium in Britain. Journal of the Marine Biological Association of the United Kingdom 34: 565–577.CrossRefGoogle Scholar
  74. Silva, P. C., 1957. Codium in Scandinavian Waters. Svensk Botanisk Tidskrift 51: 117–134.Google Scholar
  75. Skutch, A. F., 1926. On the habits and ecology of the tube-building amphipod Ampithoe rubricata Montagu. Ecology 7: 481–502.CrossRefGoogle Scholar
  76. Statens Kartverk, Vannstandsnivå. http://www.sehavniva.no/sted/Hordaland/Bergen/Bergen~9000002/vannstand.html. Accessed 17 Nov 2014
  77. Tews, J., U. Brose, V. Grimm, K. Tielbörger, M. C. Wichmann, et al., 2004. Animal species diversity driven by habitat heterogeneity/diversity: the importance of keystone structures. Journal of Biogeography 31: 79–92.CrossRefGoogle Scholar
  78. Thomsen, M. S., T. Wernberg, F. Tuya & B. R. Silliman, 2009. Evidence for impacts of nonindigenous macroalgae: a meta-analysis of experimental field studies. Journal of Phycology 45: 812–819.CrossRefPubMedGoogle Scholar
  79. Thomsen, M. S., T. Wernberg, P. M. South & D. R. Schiel, 2016. Non-native Seaweeds Drive Changes in Marine Coastal Communities Around the World. In Hu, Z.-M. & C. Fraser (eds), Seaweed Phylogeography: Adaptation and Evolution of Seaweeds under Environmental Change. Springer, Netherlands, Dordrecht: 147–185.CrossRefGoogle Scholar
  80. Trowbridge, C. D., 1998. Ecology of the green macroalga Codium fragile (Suringar) Hariot 1889: invasive and non-invasive subspecies. Oceanography and Marine Biology: An Annual Review 36: 1–64.Google Scholar
  81. Venables, W. N. & B. D. Ripley, 2002. Modern Applied Statistics with S, 4th ed. Springer, New York.CrossRefGoogle Scholar
  82. Viejo, R. M., 1999. Mobile epifauna inhabiting the invasive Sargassum muticum and two local seaweeds in northern Spain. Aquatic Botany 64: 131–149.CrossRefGoogle Scholar
  83. Vilà, M., C. Basnou, P. Pyšek, M. Josefsson, P. Genovesi, et al., 2010. How well do we understand the impacts of alien species on ecosystem services? A pan-European, cross-taxa assessment. Frontiers in Ecology and the Environment 8: 135–144.CrossRefGoogle Scholar
  84. Wahl, M. & M. E. Hay, 1995. Associational resistance and shared doom: effects of epibiosis on herbivory. Oecologia 102: 329–340.CrossRefGoogle Scholar
  85. Watson, D. C. & T. A. Norton, 1987. The habitat and feeding preferences of Littorina obtusata (L.) and L. mariae sacchi et rastelli. Journal of Experimental Marine Biology and Ecology 112: 61–72.CrossRefGoogle Scholar
  86. Wernberg, T., M. Thomsen, P. Staehr & M. Pedersen, 2004. Epibiota communities of the introduced and indigenous macroalgal relatives Sargassum muticum and Halidrys siliquosa in Limfjorden (Denmark). Helgoland Marine Research 58: 154–161.CrossRefGoogle Scholar
  87. Williams, G. B., 1964. The effect of extracts of Fucus serratus in promoting the settlement of larvae of Spirorbis borealis [Polychaeta]. Journal of the Marine Biological Association of the United Kingdom 44: 397–414.CrossRefGoogle Scholar
  88. Williams, G. A., 1996. Seasonal variation in a low shore Fucus serratus (Fucales, Phaeophyta) population and its epiphytic fauna. Hydrobiologia 326–327: 191–197.CrossRefGoogle Scholar
  89. Williams, S. L. & J. E. Smith, 2007. A global review of the distribution, taxonomy, and impacts of introduced seaweeds. Annual Review of Ecology, Evolution, and Systematics 38: 327–359.CrossRefGoogle Scholar

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© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Department of BiologyUniversity of BergenBergenNorway

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