Biological Invasions

, Volume 18, Issue 3, pp 661–676 | Cite as

The structure of biogenic habitat and epibiotic assemblages associated with the global invasive kelp Undaria pinnatifida in comparison to native macroalgae

  • Matthew Arnold
  • Harry Teagle
  • Matthew P. Brown
  • Dan A. SmaleEmail author
Original Paper


Kelp forests dominate temperate and polar rocky coastlines and represent critical marine habitats because they support elevated rates of primary and secondary production and high biodiversity. A major threat to the stability of these ecosystems is the proliferation of non-native species, such as the Japanese kelp Undaria pinnatifida (‘Wakame’), which has recently colonised natural habitats in the UK. We quantified the abundance and biomass of U. pinnatifida on a natural rocky reef habitat over 10 months to make comparisons with three native canopy-forming brown algae (Laminaria ochroleuca, Saccharina latissima, and Saccorhiza polyschides). We also examined the biogenic habitat structure provided by, and epibiotic assemblages associated with, U. pinnatifida in comparison to native macroalgae. Surveys conducted within the Plymouth Sound Special Area of Conservation indicated that U. pinnatifida is now a dominant and conspicuous member of kelp-dominated communities on natural substrata. Crucially, U. pinnatifida supported a structurally dissimilar and less diverse epibiotic assemblage than the native perennial kelp species. However, U. pinnatifida-associated assemblages were similar to those associated with Saccorhiza polyschides, which has a similar life history and growth strategy. Our results suggest that a shift towards U. pinnatifida dominated reefs could result in impoverished epibiotic assemblages and lower local biodiversity, although this could be offset, to some extent, by the climate-driven proliferation of L. ochroleuca at the poleward range edge, which provides complex biogenic habitat and harbours relatively high biodiversity. Clearly, greater understanding of the long-term dynamics and competitive interactions between these habitat-forming species is needed to accurately predict future biodiversity patterns.


Non-native species Epifauna Biodiversity Benthic ecology Temperate reefs Macroalgae 



The authors would like to thank the University of Plymouth Marine Station for diving support. DS is supported by an Independent Research Fellowship awarded by the Natural Environment Research Council of the UK (NE/K008439/1). We thank Anna Yunnie for taxonomic assistance.

Supplementary material

10530_2015_1037_MOESM1_ESM.pdf (84 kb)
Supplementary material 1 (PDF 83 kb)


  1. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46Google Scholar
  2. Anderson MJ, Diebel CE, Blom WM, Landers TJ (2005) Consistency and variation in kelp holdfast assemblages: spatial patterns of biodiversity for the major phyla at different taxonomic resolutions. J Exp Mar Biol Ecol 320:35–56CrossRefGoogle Scholar
  3. Anderson MJ, Gorley RN, Clarke KR (2008) Permanova + for primer: guide to software and statistical methods. PRIMER-E, PlymouthGoogle Scholar
  4. Angelini C, Altieri AH, Silliman BR, Bertness MD (2011) Interactions among foundation species and their consequences for community organization, biodiversity, and conservation. Bioscience 61:782–789CrossRefGoogle Scholar
  5. Birchenough S, Bremmer J (2010) Shallow and shelf subtidal habitats and ecology. MCCIP Annual Report Card 2010-11, MCCIP Science ReviewGoogle Scholar
  6. Blight AJ, Thompson RC (2008) Epibiont species richness varies between holdfasts of a northern and southerly distributed kelp species. J Mar Biol Assoc UK 88:469–475CrossRefGoogle Scholar
  7. Buschbaum C, Chapman A, Saier B (2006) How an introduced seaweed can affect epibiota diversity in different coastal systems. Mar Biol 148:743–754CrossRefGoogle Scholar
  8. Byrnes JE, Reed DC, Cardinale BJ, Cavanaugh KC, Holbrook SJ, Schmitt RJ (2011) Climate-driven increases in storm frequency simplify kelp forest food webs. Glob Change Biol 17:2513–2524CrossRefGoogle Scholar
  9. Casas GN, Piriz ML (1996) Surveys of Undaria pinnatifida (Laminariales, Phaeophyta) in Golfo Nuevo, Argentina. Hydrobiologia 326–327:213–215CrossRefGoogle Scholar
  10. Casas G, Scrosati R, Luz Piriz M (2004) The invasive kelp Undaria Pinnatifida (Phaeophyceae, Laminariales) reduces native seaweed diversity in Nuevo Gulf (Patagonia, Argentina). Biol Invasions 6:411–416CrossRefGoogle Scholar
  11. Castric-Fey A, Girard A, L’Hardy-Halos MT (1993) The distribution of Undaria pinnatifida (Phaeophyceae, Laminariales) on the coast of St. Malo (Brittany, France). Bot Mar 36:351–358CrossRefGoogle Scholar
  12. Castric-Fey A, Beaupoil C, Bouchain J, Pradier E, L’Hardy-Halos M (1999) The introduced alga Undaria pinnatifida (Laminariales, Alariaceae) in the rocky shore ecosystem of the St Malo Area: growth rate and longevity of the sporophyte. Bot Mar 42:83–96Google Scholar
  13. Cecere E, Petrocelli A, Daniela Saracino O (2000) Undaria pinnatifida (Fucophyceae, Laminariales) spread in the central Mediterranean: its occurrence in the Mar Piccolo of Taranto (Ionian Sea, southern Italy). Cryptogamie Algol 21:305–309CrossRefGoogle Scholar
  14. Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. PRIMER-E Ltd., PlymouthGoogle Scholar
  15. Connor DW, Allen JH, Golding N, Howell KL, Lieberknecht LM, Northen KO, Reker JB (2004) The marine habitat classification for Britain and Ireland version 04.05. JNCC, Peterborough, UKGoogle Scholar
  16. Curiel D, Bellemo G, Marzocchi M, Scattolin M, Parisi G (1998) Distribution of introduced Japanese macroalgae Undaria pinnatifida, Sargassum muticum (Phaeophyta) and Antithamnion Pectinatum (Rhodophyta) in the Lagoon of Venice. Hydrobiologia 385:17–22CrossRefGoogle Scholar
  17. Da Gama BAP, Pereira RC, Carvalho AGV, Coutinho R, Yoneshigue-Valentin Y (2002) The effects of seaweed secondary metabolites on biofouling. Biofouling 18:13–20CrossRefGoogle Scholar
  18. Dellatorre FG, Amoroso R, Saravia J, Orensanz JM (2014) Rapid expansion and potential range of the invasive kelp Undaria pinnatifida in the Southwest Atlantic. Aquat Invasions 9:467–478CrossRefGoogle Scholar
  19. 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
  20. Fitzpatrick F (1990) Remotely sensed sedimentology of Plymouth Sound. Proc Ussher Soc 7:289–294Google Scholar
  21. Fletcher RL, Manfredi C (1995) The Occurrence of Undaria pinnatifida (Phaeophyceae, Laminariales) on the south coast of England. Bot Mar 38:355CrossRefGoogle Scholar
  22. Floc’h J-Y, Pajot R, Mouret V (1996) Undaria pinnatifida (Laminariales, Phaeophyta) 12 years after its introduction into the Atlantic Ocean. Hydrobiologia 326–327:217–222CrossRefGoogle Scholar
  23. Gorgula S, Connell S (2004) Expansive covers of turf-forming algae on human-dominated coast: the relative effects of increasing nutrient and sediment loads. Mar Biol 145:613–619CrossRefGoogle Scholar
  24. Gurevitch J, Padilla DK (2004) Are invasive species a major cause of extinctions? Trends Ecol Evol 19:470–474CrossRefPubMedGoogle Scholar
  25. Hauser A, Attrill MJ, Cotton PA (2006) Effects of habitat complexity on the diversity and abundance of macrofauna colonising artificial kelp holdfasts. Mar Ecol Prog Ser 325:93–100CrossRefGoogle Scholar
  26. Hay CH, Luckens PA (1987) The Asian kelp Undaria pinnatifida (Phaeophyta: laminariales) found in a New Zealand harbour. New Zeal J Bot 25:329–332CrossRefGoogle Scholar
  27. Heiser S, Hall-Spencer JM, Hiscock K (2014) Assessing the extent of establishment of Undaria pinnatifida in Plymouth Sound Special Area of Conservation, UK. Mar Biodivers Rec 7:e93CrossRefGoogle Scholar
  28. Hellio C, Berge JP, Beaupoil C, Le Gal Y, Bourgougnon N (2002) Screening of marine algal extracts for anti-settlement activities against microalgae and macroalgae. Biofouling 18:205–215CrossRefGoogle Scholar
  29. Irigoyen A, Trobbiani G, Sgarlatta M, Raffo M (2011) Effects of the alien algae Undaria pinnatifida (Phaeophyceae, Laminariales) on the diversity and abundance of benthic macrofauna in Golfo Nuevo (Patagonia, Argentina): potential implications for local food webs. Biol Invasions 13:1521–1532CrossRefGoogle Scholar
  30. James K, Middleton I, Middleton C, Shears NT (2014) Discovery of Undaria pinnatifida (Harvey) Suringar, 1873 in northern New Zealand indicates increased invasion threat in subtropical regions. BioInvasion Rec 3:21–24CrossRefGoogle Scholar
  31. Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386CrossRefGoogle Scholar
  32. Krumhansl K, Scheibling RE (2012) Production and fate of kelp detritus. Mar Ecol Prog Ser 467:281–302CrossRefGoogle Scholar
  33. Leclerc J, Riera P, Leroux C, Lévêque L, Davoult D (2013) Temporal variation in organic matter supply in kelp forests: linking structure to trophic functioning. Mar Ecol Prog Ser 494:87–105CrossRefGoogle Scholar
  34. Ling SD (2008) Range expansion of a habitat-modifying species leads to loss of taxonomic diversity: a new and impoverished reef state. Oecologia 156:883–894CrossRefPubMedGoogle Scholar
  35. Ling SD, Johnson CR, Frusher SD, Ridgway KR (2009) Overfishing reduces resilience of kelp beds to climate-driven catastrophic phase shift. Proc Nat Acad Sci USA 106:22341–22345PubMedCentralCrossRefPubMedGoogle Scholar
  36. MacDougall AS, Turkington R (2005) Are invasive species the drivers or passengers of change in degraded ecosystems? Ecology 86:42–55CrossRefGoogle Scholar
  37. Mann KH (1973) Seaweeds: their productivity and strategy for growth. Science 182:975–981CrossRefPubMedGoogle Scholar
  38. McLaughlan C, Gallardo B, Aldridge DC (2014) How complete is our knowledge of the ecosystem services impacts of Europe’s top 10 invasive species? Acta Oecol 54:119–130CrossRefGoogle Scholar
  39. Messmer V, Jones GP, Munday PL, Holbrook SJ, Schmitt RJ, Brooks AJ (2011) Habitat biodiversity as a determinant of fish community structure on coral reefs. Ecology 92:2285–2298CrossRefPubMedGoogle Scholar
  40. Minchin D, Nunn J (2014) The invasive brown alga Undaria pinnatifida (Harvey) Suringar, 1873 (Laminariales: Alariaceae), spreads northwards in Europe. BioInvasions Rec 3:57–63CrossRefGoogle Scholar
  41. Molnar JL, Gamboa RL, Revenga C, Spalding MD (2008) Assessing the global threat of invasive species to marine biodiversity. Front Ecol Environ 6:485–492CrossRefGoogle Scholar
  42. Moy FE, Christie H (2012) Large-scale shift from sugar kelp (Saccharina latissima) to ephemeral algae along the south and west coast of Norway. Mar Biol Res 8:309–321CrossRefGoogle Scholar
  43. Peteiro C, Freire Ó (2013) Epiphytism on blades of the edible kelps Undaria pinnatifida and Saccharina latissima farmed under different abiotic conditions. J World Aquacult Soc 44:706–715CrossRefGoogle Scholar
  44. Raffo MP, Eyras MC, Iribarne OO (2009) The invasion of Undaria pinnatifida to a Macrocystis pyrifera kelp in Patagonia (Argentina, south-west Atlantic). J Mar Biol Assoc UK 89:1571–1580CrossRefGoogle Scholar
  45. Raybaud V, Beaugrand G, Goberville E, Delebecq G, Destombe C, Valero M, Davoult D, Morin P, Gevaert F (2013) Decline in kelp in west Europe and climate. PLoS ONE 8:e66044PubMedCentralCrossRefPubMedGoogle Scholar
  46. Saunders M, Metaxas A (2008) High recruitment of the introduced bryozoan Membranipora membranacea is associated with kelp bed defoliation in Nova Scotia, Canada. Mar Ecol Prog Ser 369:139–151CrossRefGoogle Scholar
  47. Schiel DR, Thompson GA (2012) Demography and population biology of the invasive kelp Undaria pinnatifida on shallow reefs in southern New Zealand. J Exp Mar Biol Ecol 434–435:25–33CrossRefGoogle Scholar
  48. Silva PC, Woodfield RA, Cohen AN, Harris LH, Goddard JHR (2002) First Report of the Asian kelp Undaria pinnatifida in the Northeastern Pacific Ocean. Biol Invasions 4:333–338CrossRefGoogle Scholar
  49. Simberloff D (2011) How common are invasion-induced ecosystem impacts? Biol Invasions 13:1255–1268CrossRefGoogle Scholar
  50. Smale DA (2010) Monitoring marine macroalgae: the influence of spatial scale on the usefulness of biodiversity surrogates. Divers Dist 16:985–995CrossRefGoogle Scholar
  51. Smale DA, Wernberg T (2013) Extreme climatic event drives range contraction of a habitat-forming species. Proc Roy Soc B: Biol Sci 280:20122829CrossRefGoogle Scholar
  52. Smale DA, Wernberg T, Vance T (2011) Community development on subtidal temperate reefs: the influences of wave energy and the stochastic recruitment of a dominant kelp. Mar Biol 158:1757–1766CrossRefGoogle Scholar
  53. Smale DA, Burrows MT, Moore PJ, O’Connor N, Hawkins SJ (2013) Threats and knowledge gaps for ecosystem services provided by kelp forests: a northeast Atlantic perspective. Ecol Evol 3:4016–4038PubMedCentralCrossRefPubMedGoogle Scholar
  54. Smale DA, Wernberg T, Yunnie ALE, Vance T (2015) The rise of Laminaria ochroleuca in the Western English Channel (UK) and preliminary comparisons with its competitor and assemblage dominant Laminaria hyperborea. Mar Ecol 36:1033–1044CrossRefGoogle Scholar
  55. South PM, Lilley SA, Tait LW, Alestra T, Hickford MJH, Thomsen MS, Schiel DR (2015) Transient effects of an invasive kelp on the community structure and primary productivity of an intertidal assemblage. Mar Freshwater Res. doi: 10.1071/MF14211 Google Scholar
  56. Steneck RS, Graham MH, Bourque BJ, Corbett D, Erlandson JM, Estes JA, Tegner MJ (2002) Kelp forest ecosystems: biodiversity, stability, resilience and future. Environ Conserv 29:436–459CrossRefGoogle Scholar
  57. Tegner MJ, Dayton PK (2000) Ecosystem effects of fishing in kelp forest communities. ICES J Mar Sci J du Conseil 57:579–589CrossRefGoogle Scholar
  58. 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
  59. Thomsen MS, Wernberg T, Altieri A, Tuya F, Gulbransen D, McGlathery KJ, Holmer M, Silliman BR (2010) Habitat cascades: the conceptual context and global relevance of facilitation cascades via habitat formation and modification. Integr Comp Biol 50:158–175CrossRefPubMedGoogle Scholar
  60. Thomsen MS, Wernberg T, Olden JD, Byers JE, Bruno JF, Silliman BR, Schiel DR (2014) Forty years of experiments on aquatic invasive species: are study biases limiting our understanding of impacts? Neobiota 22:1–22CrossRefGoogle Scholar
  61. Tuya F, Larsen K, Platt V (2011) Patterns of abundance and assemblage structure of epifauna inhabiting two morphologically different kelp holdfasts. Hydrobiologia 658:373–382CrossRefGoogle Scholar
  62. Valentine JP, Johnson CR (2003) Establishment of the introduced kelp Undaria pinnatifida in Tasmania depends on disturbance to native algal assemblages. J Exp Mar Biol Ecol 295:63–90CrossRefGoogle Scholar
  63. Valentine JP, Johnson CR (2005) Persistence of the exotic kelp Undaria pinnatifida does not depend on sea urchin grazing. Mar Ecol Prog Ser 285:43–55CrossRefGoogle Scholar
  64. Vergés A, Steinberg PD, Hay ME, Poore AGB, Campbell AH, Ballesteros E, Heck KL, Booth DJ, Coleman MA, Feary DA, Figueira W, Langlois T, Marzinelli EM, Mizerek T, Mumby PJ, Nakamura Y, Roughan M, van Sebille E, Gupta AS, Smale DA, Tomas F, Wernberg T, Wilson SK (2014) The tropicalization of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts. Proc Roy Soc B Biol Sci 281:20140846CrossRefGoogle Scholar
  65. Vilà M, Basnou C, Pyšek P, Josefsson M, Genovesi P, Gollasch S, Nentwig W, Olenin S, Roques A, Roy D, Hulme PE (2009) How well do we understand the impacts of alien species on ecosystem services? A pan-European, cross-taxa assessment. Front Ecol Environ 8:135–144CrossRefGoogle Scholar
  66. Wernberg T, Kendrick GA, Toohey BD (2005) Modification of the physical environment by an Ecklonia radiata (Laminariales) canopy and its implications to associated foliose algae. Aquat Ecol 39:419–430CrossRefGoogle Scholar
  67. Wernberg T, Russell BD, Moore PJ, Ling SD, Smale DA, Coleman M, Steinberg PD, Kendrick GA, Connell SD (2011) Impacts of climate change in a global hotspot for temperate marine biodiversity and ocean warming. J Exp Mar Biol Ecol 400:7–16CrossRefGoogle Scholar
  68. Wernberg T, Smale DA, Tuya F, Thomsen MS, Langlois TJ, de Bettignies T, Bennett S, Rousseaux CS (2013) An extreme climatic event alters marine ecosystem structure in a global biodiversity hotspot. Nat Clim Change 3:78–82CrossRefGoogle Scholar
  69. Williams FE, Eschen R, Harris A, Djeddour DH, Pratt CF, Shaw RS, Varia S, Lamontagne-Godwin JD, Thomas SE, Murphy ST (2010) The economic cost of invasive non-native species on Great Britain. CABI Project No. VM10066 Final Report, Wallingford, UKGoogle Scholar
  70. Wood C, Bishop J, Yunnie ALE (2015) Comprehensive reassessment of NNS in Welsh marinas. Welsh Government Resilient Ecosystems Fund (REF), Grant GU9430Google Scholar
  71. Zabin CJ, Ashton GV, Brown CW, Ruiz GM (2009) Northern range expansion of the Asian kelp Undaria pinnatifida (Harvey) Suringar (Laminariales, Phaeophyceae) in western North America. Aquat Invasions 4:429–434CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Matthew Arnold
    • 1
  • Harry Teagle
    • 1
  • Matthew P. Brown
    • 2
  • Dan A. Smale
    • 1
    Email author
  1. 1.The LaboratoryMarine Biological Association of the United KingdomCitadel Hill, PlymouthUK
  2. 2.School of Marine Science and EngineeringPlymouth UniversityDrake Circus, PlymouthUK

Personalised recommendations