Abstract
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.
Similar content being viewed by others
References
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46
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 320:35–56
Anderson MJ, Gorley RN, Clarke KR (2008) Permanova + for primer: guide to software and statistical methods. PRIMER-E, Plymouth
Angelini C, Altieri AH, Silliman BR, Bertness MD (2011) Interactions among foundation species and their consequences for community organization, biodiversity, and conservation. Bioscience 61:782–789
Birchenough S, Bremmer J (2010) Shallow and shelf subtidal habitats and ecology. MCCIP Annual Report Card 2010-11, MCCIP Science Review
Blight AJ, Thompson RC (2008) Epibiont species richness varies between holdfasts of a northern and southerly distributed kelp species. J Mar Biol Assoc UK 88:469–475
Buschbaum C, Chapman A, Saier B (2006) How an introduced seaweed can affect epibiota diversity in different coastal systems. Mar Biol 148:743–754
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 17:2513–2524
Casas GN, Piriz ML (1996) Surveys of Undaria pinnatifida (Laminariales, Phaeophyta) in Golfo Nuevo, Argentina. Hydrobiologia 326–327:213–215
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 6:411–416
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 36:351–358
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 42:83–96
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 21:305–309
Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. PRIMER-E Ltd., Plymouth
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, UK
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 385:17–22
Da Gama BAP, Pereira RC, Carvalho AGV, Coutinho R, Yoneshigue-Valentin Y (2002) The effects of seaweed secondary metabolites on biofouling. Biofouling 18:13–20
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 9:467–478
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 334:236–243
Fitzpatrick F (1990) Remotely sensed sedimentology of Plymouth Sound. Proc Ussher Soc 7:289–294
Fletcher RL, Manfredi C (1995) The Occurrence of Undaria pinnatifida (Phaeophyceae, Laminariales) on the south coast of England. Bot Mar 38:355
Floc’h J-Y, Pajot R, Mouret V (1996) Undaria pinnatifida (Laminariales, Phaeophyta) 12 years after its introduction into the Atlantic Ocean. Hydrobiologia 326–327:217–222
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 145:613–619
Gurevitch J, Padilla DK (2004) Are invasive species a major cause of extinctions? Trends Ecol Evol 19:470–474
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 325:93–100
Hay CH, Luckens PA (1987) The Asian kelp Undaria pinnatifida (Phaeophyta: laminariales) found in a New Zealand harbour. New Zeal J Bot 25:329–332
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:e93
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 18:205–215
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 13:1521–1532
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 3:21–24
Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386
Krumhansl K, Scheibling RE (2012) Production and fate of kelp detritus. Mar Ecol Prog Ser 467:281–302
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 494:87–105
Ling SD (2008) Range expansion of a habitat-modifying species leads to loss of taxonomic diversity: a new and impoverished reef state. Oecologia 156:883–894
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 106:22341–22345
MacDougall AS, Turkington R (2005) Are invasive species the drivers or passengers of change in degraded ecosystems? Ecology 86:42–55
Mann KH (1973) Seaweeds: their productivity and strategy for growth. Science 182:975–981
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 54:119–130
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 92:2285–2298
Minchin D, Nunn J (2014) The invasive brown alga Undaria pinnatifida (Harvey) Suringar, 1873 (Laminariales: Alariaceae), spreads northwards in Europe. BioInvasions Rec 3:57–63
Molnar JL, Gamboa RL, Revenga C, Spalding MD (2008) Assessing the global threat of invasive species to marine biodiversity. Front Ecol Environ 6:485–492
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 8:309–321
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 44:706–715
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 89:1571–1580
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:e66044
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 369:139–151
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 434–435:25–33
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 4:333–338
Simberloff D (2011) How common are invasion-induced ecosystem impacts? Biol Invasions 13:1255–1268
Smale DA (2010) Monitoring marine macroalgae: the influence of spatial scale on the usefulness of biodiversity surrogates. Divers Dist 16:985–995
Smale DA, Wernberg T (2013) Extreme climatic event drives range contraction of a habitat-forming species. Proc Roy Soc B: Biol Sci 280:20122829
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 158:1757–1766
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 3:4016–4038
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 36:1033–1044
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
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 29:436–459
Tegner MJ, Dayton PK (2000) Ecosystem effects of fishing in kelp forest communities. ICES J Mar Sci J du Conseil 57:579–589
Thomsen MS, Wernberg T, Tuya F, Silliman BR (2009) Evidence for impacts of nonindigenous macroalgae: a meta-analysis of experimental field studies. J Phycol 45:812–819
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 50:158–175
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 22:1–22
Tuya F, Larsen K, Platt V (2011) Patterns of abundance and assemblage structure of epifauna inhabiting two morphologically different kelp holdfasts. Hydrobiologia 658:373–382
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 295:63–90
Valentine JP, Johnson CR (2005) Persistence of the exotic kelp Undaria pinnatifida does not depend on sea urchin grazing. Mar Ecol Prog Ser 285:43–55
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 281:20140846
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 8:135–144
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 39:419–430
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 400:7–16
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 3:78–82
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, UK
Wood C, Bishop J, Yunnie ALE (2015) Comprehensive reassessment of NNS in Welsh marinas. Welsh Government Resilient Ecosystems Fund (REF), Grant GU9430
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 4:429–434
Acknowledgments
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.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Arnold, M., Teagle, H., Brown, M.P. et al. The structure of biogenic habitat and epibiotic assemblages associated with the global invasive kelp Undaria pinnatifida in comparison to native macroalgae. Biol Invasions 18, 661–676 (2016). https://doi.org/10.1007/s10530-015-1037-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-015-1037-6