Undaria pinnatifida: A case study to highlight challenges in marine invasion ecology and management

Abstract

Marine invasion ecology and management have progressed significantly over the last 30 years although many knowledge gaps and challenges remain. The kelp Undaria pinnatifida, or “Wakame,” has a global non-native range and is considered one of the world's “worst” invasive species. Since its first recorded introduction in 1971, numerous studies have been conducted on its ecology, invasive characteristics, and impacts, yet a general consensus on the best approach to its management has not yet been reached. Here, we synthesize current understanding of this highly invasive species and adopt Undaria as a case study to highlight challenges in wider marine invasion ecology and management. Invasive species such as Undaria are likely to continue to spread and become conspicuous, prominent components of coastal marine communities. While in many cases, marine invasive species have detectable deleterious impacts on recipient communities, in many others their influence is often limited and location specific. Although not yet conclusive, Undaria may cause some ecological impact, but it does not appear to drive ecosystem change in most invaded regions. Targeted management actions have also had minimal success. Further research is needed before well-considered, evidence-based management decisions can be made. However, if Undaria was to become officially unmanaged in parts of its non-native range, the presence of a highly productive, habitat former with commercial value and a broad ecological niche, could have significant economic and even environmental benefit. How science and policy reacts to the continued invasion of Undaria may influence how similar marine invasive species are handled in the future.

REFERENCES Agatsuma, Y., Matsuyama, K., Nakata, A., Kawai, T., & Nishikawa, N. (1997). Marine algal succession on coralline flats after removal of sea urchins in suttsu bay on the Japan sea coast of Hokkaido, Japan. Nippon Susian Gakkaishi, 63(5), 672–680. Aguilar-Rosas, R., Aguilar-Rosas, L. E., Avila-Serrano, G., & Marcos-Ramirez, R. (2004). First record of Undaria pinnatifida (Harvey) Suringar (laminariales, phaeophyta) on the pacific coast of Mexico. Botanica Marina, 47(3), 255–258. Anderson, L. W. J. (2005). California's reaction to Caulerpa taxifolia: A model for invasive species rapid response. Biological Invasions, 7(6), 1003–1016. Antoine, L., Lemoine, M., Boulben, S., Kaas, R., Laurans, M., Viard, F., & Potin, P. (2012). Emergence d'une filiere de culture de macro-algues en bretagne et probleme relatifa une espece non indigene, le wakame (Undaria pinnatifida). Report, IFREMER, 16 pp. Arakawa, H., & Morinaga, T. (1994). The rate of brown algal zoospores adhered in the seaweed substrate in relation to gradient of the substrate. Nippon Suisan Gakkaishi, 60(4), 461–466. Arnold, M., Teagle, H., Brown, M. P., & Smale, D. A. (2016). The structure and diversity of epibiotic assemblages associated with the invasive kelp Undaria pinnatifida in comparison to native habitat-forming macroalgae on a subtidal temperate reef. Biological Invasions, 18(3), 661–676. Baez, J. C., Olivero, J., Peteiro, C., Ferri-Yanez, F., Garcia-Soto, C., & Real, R. (2010). Macro environmental modelling of the current distribution of Undaria pinnatifida (Laminariales, Ochrophyta) in northern Iberia. Biological Invasions, 12(7), 2131–2139. Bauer, J. T. (2012). Invasive species: “back-seat drivers” of ecosystem change? Biological Invasions, 14(7), 1295–1304. Bax, N., Carlton, J. T., Mathews-Amos, A., Haedrich, R. L., Howarth, F. G., Purcell, J. E., … Gray, A. (2001). The control of biological invasions in the world's oceans. Conservation Biology, 15(5), 1234–1246. Bax, N., Williamson, A., Aguero, M., Gonzalez, E., & Geeves, W. (2003). Marine invasive alien species: A threat to global biodiversity. Marine Policy, 27(4), 313–323. Beric, B., & MacIsaac, H. J. (2015). Determinants of rapid response success for alien invasive species in aquatic ecosystems. Biological Invasions, 17(11), 3327–3335. BOE (2013). Real decreto 630/2013, de 2 de agosto, por el que se regula el catlogo espaol de especies exticas invasoras. Boletn Oficial del Estado No. 185, 56764–56786. Bollen, M., Pilditch, C. A., Battershill, C. N., & Bischof, K. (2016). Salinity and temperature tolerance of the invasive alga Undaria pinnatifida and native New Zealand kelps: Implications for competition. Marine Biology, 163, 194. Buestel, D., Ropert, M., Prou, J., & Goulletquer, P. (2009). History, status, and future of oyster culture in France. Journal of Shellfish Research, 28(4), 813–820. Bullard, S. G., Lambert, G., Carman, M. R., Byrnes, J., Whitlatch, R. B., Ruiz, G., … Heinonen, K. (2007). The colonial ascidian Didemnum sp. A: Current distribution, basic biology and potential threat to marine communities of the northeast and west coasts of North America. Journal of Experimental Marine Biology and Ecology, 342(1), 99–108. Campbell, S. J., Bite, J. S., & Burridge, T. R. (1999). Seasonal patterns in the photosynthetic capacity, tissue pigment and nutrient content of different developmental stages of Undaria pinnatifida (Phaeophyta: Laminariales) in Port Phillip Bay, South-Eastern Australia. Botanica Marina, 42(3), 231–241. Carnell, P. E., & Keough, M. J. (2014). Spatially variable synergistic effects of disturbance and additional nutrients on kelp recruitment and recovery. Oecologia, 175(1), 409–416. Casas, G. N., Piriz, M. L., & Parodi, E. R. (2008). Population features of the invasive kelp Undaria pinnatifida (Phaeophyceae: Laminariales) in Nuevo Gulf (Patagonia, Argentina). Journal of the Marine Biological Association of the United Kingdom, 88(1), 21–28. Casas, G., Scrosati, R., & Piriz, M. L. (2004). The invasive kelp Undaria pinnatifida (Phaeo-phyceae, Laminariales) reduces native seaweed diversity in Nuevo Gulf (Patagonia, Argentina). Biological Invasions, 6, 411–416. Castric-Fey, A., Beaupoil, C., Bouchain, J., Pradier, E., & L'Hardy-Halos, M. T. (1999). The introduced alga Undaria pinnatifida (Laminariales, Alariaceae) in the rocky shore ecosystem of the St Malo area: Morphology and growth of the sporophyte. Botanica Marina, 42(1), 71–82. Castric-Fey, A., Girard, A., & Lhardyhalos, M. T. (1993). The distribution of Undaria pinnatifida (Phaeophyceae, Laminariales) on the coast of St. Malo (Brittany, France). Botanica Marina, 36(4), 351–358. Cecere, E., Petrocelli, A., & Saracino, O. D. (2000). Undaria pinnatifida (Fucophyceae, Laminariales) spread in the central Mediterranean: its occurrence in the mar piccolo of Taranto (Ionian Sea, southern Italy). Cryptogamie Algologie, 21(3), 305–309. Choi, H. G., Kim, Y. S., Lee, S. J., & Nam, K. W. (2007). Growth and reproductive patterns of Undaria pinnatifida sporophytes in a cultivation farm in Busan, Korea. Journal of Applied Phycology, 19(2), 131–138. Choi, H. G., Young, S. K., Soon, J. L., Eun, J. P., & Ki, W. N. (2005). Effects of daylength, irradiance and settlement density on the growth and reproduction of Undaria pinnatifida gametophytes. Journal of Applied Phycology, 17(5), 423–430. Cognie, B., Haure, J., & Barill, L. (2006). Spatial distribution in a temperate coastal ecosystem of the wild stock of the farmed oyster Crassostrea gigas (Thunberg). Aquaculture, 259(1–4), 249–259. Cohen, A. N., & Carlton, J. T. (1998). Accelerating invasion rate in a highly invaded estuary. Science, 279(5350), 555–558. Copp, G. H., Bianco, P. G., Bogutskaya, N. G., Eros, T., Falka, I., Ferreira, M. T., … Wiesner, C. (2005). To be, or not to be, a non-native freshwater fish? Journal of Applied Ichthyology, 21(4), 242–262. Cranfield, H. J., Gordon, D. P., Willian, R. C., Marshall, B. A., Battershill, C. N., Francis, M. P., … Read, G. B. (1998). Adventive marine species in New Zealand. Technical report, NIWA Technical Report 34, 48 pp. Creese, R., Hooker, S., De Luca, S., & Wharton, Y. (1997). Ecology and environmental impact of Musculista senhousia (Mollusca: Bivalvia: Mytilidae) in Tamaki estuary, Auckland, New Zealand. New Zealand Journal of Marine and Freshwater Research, 31(2), 225–236. Cremades, J., Freire, O., & Peteiro, C. (2006). Biologia, distribucion e integracion del alga aloctona Undaria pinnatifida (laminariales, phaeophyta) en las comunidades bentonicas de las costas de galicia (nw de la peninsula iberica). Anales del Jardin Botanico de Madrid, 63(2), 169–187. Critchley, A. T., Farnham, W. F., & Morrell, S. L. (1986). An account of the attempted control of an introduced marine alga, Sargassum muticum, in Southern England. Biological Conservation, 35(4), 313–332. Crooks, J. A. (2002). Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers. Oikos, 97(2), 153–166. Crooks, J. A. (2005). Lag times and exotic species: The ecology and management of biological invasions in slow-motion. Ecoscience, 12(3), 316–329. Crooks, J. A., & Khim, H. S. (1999). Architectural vs. biological effects of a habitat-altering, exotic mussel, Musculista senhousia. Journal of Experimental Marine Biology and Ecology, 240(1), 53–75. Curiel, D., Guidetti, P., Bellemo, G., Scattolin, M., & Marzocchi, M. (2001). The introduced alga Undaria pinnatifida (Laminariales, Alariaceae) in the lagoon of Venice. Hydrobiologia, 477(1–3), 209–219. DAISIE (2009). Handbook of Alien species in Europe, volume 3 of invading nature – Springer series in invasion ecology. Netherlands: Springer, 399 pp. Davis, M. A., Chew, M. K., Hobbs, R. J., Lugo, A. E., Ewel, J. J., Vermeij, G. J., … Briggs, J. C. (2011). Don't judge species on their origins. Nature, 474(7350), 153–154. Dayton, P. K. (1985). Ecology of kelp communities. Annual Review of Ecology and Systematics, 16, 215–245. De Leij, R., Epstein, G., Brown, M., & Smale, D. A. (2017). The inuence of native macroalgal canopies on the distribution and abundance of the non-native kelp Undaria pinnatifida in natural reef habitats. Marine Biology, 164, 156–171. Dean, P. R., & Hurd, C. L. (2007). Seasonal growth, erosion rates, and nitrogen and photo-synthetic ecophysiology of Undaria pinnatifida (Heterokontophyta) in Southern New Zealand. Journal of Phycology, 43(6), 1138–1148. Dellatorre, F. G., Amoroso, R., Saravia, J., & Orensanz, J. M. (2014). Rapid expansion and potential range of the invasive kelp Undaria pinnatifida in the Southwest Atlantic. Aquatic Invasions, 9(4), 467–478. Didham, R. K., Tylianakis, J. M., Hutchison, M. A., Ewers, R. M., & Gemmell, N. J. (2005). Are invasive species the drivers of ecological change? TRENDS in Ecology and Evolution, 20(9), 470–474. Dijkstra, J. A., Harris, L. G., Mello, K., Litterer, A., Wells, C., & Ware, C. (2017). Invasive seaweeds transform habitat structure and increase biodiversity of associated species. Journal of Ecology, https://doi.org/10.1111/1365-2745.12775 Duyck, P. F., David, P., & Quilici, S. (2007). Can more K-selected species be better invaders? A case study of fruit flies in La Runion. Diversity and Distributions, 13(5), 535–543. Edgar, G. J., Barrett, N. S., Morton, A. J., & Samson, C. R. (2004). Effects of algal canopy clearance on plant, fish and macroinvertebrate communities on eastern Tasmanian reefs. Journal of Experimental Marine Biology and Ecology, 312(1), 67–87. Eno, N. C., Clark, R. A., & Sanderson, W. G. (1997). Non-native marine species in British waters: a review and directory (p. 136). Peterborough, UK: Joint Nature Conservation Committee. ES (2016). Proposal for a fiordland marine regional pathway management plan under the biosecurity act 1993. Report, Environment Southland, 71 pp. Escapa, M., Isacch, J. P., Daleo, P., Alberti, J., Iribarne, O., Borges, M., … Lasta, M. (2004). The distribution and ecological effects of the introduced pacific oyster Crassostrea gigas (Thunberg, 1793) in northern Patagonia. Journal of Shellfish Research, 23(3), 765–772. Eustice, G. (2014). Prohibition of keeping or release of live fish (specified species) (England) order 2014. Statutory Instrument No. 143, 4 pp. Ewel, J. J., O'Dowd, D. J., Bergelson, J., Daehler, C. C., D'Antonio, C. M., Gmez, L. D., … Vitousek, P. M. (1999). Deliberate introductions of species: Research needs. Benefits can be reaped, but risks are high. BioScience, 49(8), 619–630. Farrell, P., & Fletcher, R. L. (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). Journal of Experimental Marine Biology and Ecology, 334(2), 236–243. Feldman, K. L., Armstrong, D. A., Dumbauld, B. R., DeWitt, T. H., & Doty, D. C. (2000). Oysters, crabs and burrowing shrimp: Review of an environmental conflict over aquatic resources and pesticide use in Washington State's (USA) coastal estuaries. Estuaries, 23(2), 141–176. Fletcher, R. L., & Farrell, P. (1999). Introduced brown algae in the North East Atlantic, with particular respect to Undaria pinnatifida (Harvey) Suringar. Helgolander Meeresuntersuchungen, 52(3–4), 259–275. 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. Floc'h, J. Y., Pajot, R., & Wallentinus, I. (1991). The Japanese brown alga Undaria pinnatifida on the coast of France and its possible establishment in European waters. Journal du Conseil – Conseil International pour l'Exploration de la Mer, 47(3), 379–390. Forrest, B. M., Brown, S. N., Taylor, M. D., Hurd, C. L., & Hay, C. H. (2000). The role of natural dispersal mechanisms in the spread of Undaria pinnatifida (Laminariales, Phaeophyceae). Phycologia, 39(6), 547–553. Forrest, B. M., Gardner, J. P. A., & Taylor, M. D. (2009). Internal borders for managing invasive marine species. Journal of Applied Ecology, 46(1), 46–54. Forrest, B. M., & Taylor, M. D. (2002). Assessing invasion impact: survey design considerations and implications for management of an invasive marine plant. Biological Invasions, 4, 375–386. Gao, X., Endo, H., Taniguchi, K., & Agatsuma, Y. (2013). Combined effects of seawater temperature and nutrient condition on growth and survival of juvenile sporophytes of the kelp Undaria pinnatifida (Laminariales; Phaeophyta) cultivated in northern Honshu, Japan. Journal of Applied Phycology, 25(1), 269–275. Gao, X., Endo, H., Taniguchi, K., & Agatsuma, Y. (2014). Effects of experimental thinning on the growth and maturation of the brown alga Undaria pinnatifida (Laminariales; Phaeophyta) cultivated in Matsushima bay, northern Japan. Journal of Applied Phycology, 26(1), 529–535. Gerard, V. A. (1982). In situ water motion and nutrient uptake by the giant kelp Macrocystis pyrifera. Marine Biology, 69(1), 51–54. Gittenberger, A. (2007). Recent population expansions of non-native ascidians in the Netherlands. Journal of Experimental Marine Biology and Ecology, 342(1), 122–126. Gittenberger, A., & Stegenga, H. (2013). Risico analyse van uitheemse soorten in de export gebieden voor zuid - noord transporten van de oosterschelde naar de waddenzee. Report, Producentenorganisatie van de Nederlandse Mosselcultuur, 8 pp. Gozlan, R. E. (2008). Introduction of non-native freshwater fish: Is it all bad? Fish and Fisheries, 9(1), 106–115. Green, S. J., Akins, J. L., Maljkovi, A., & Ct, I. M. (2012). Invasive lionfish drive Atlantic coral reef fish declines. PLoS ONE, 7(3), e32596. Grosholz, E. (2002). Ecological and evolutionary consequences of coastal invasions. Trends in Ecology & Evolution, 17(1), 22–27. Gurevitch, J., & Padilla, D. K. (2004). Are invasive species a major cause of extinctions? Trends in Ecology & Evolution, 19(9), 470–474. Guy, C., & Roberts, D. (2010). Can the spread of non-native oysters (Crassostrea gigas) at the early stages of population expansion be managed? Marine Pollution Bulletin, 60(7), 1059–1064. Harries, D. B., Harrow, S., Wilson, J. R., Mair, J. M., & Donnan, D. W. (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 UK, 87, 1057–1067. Hay, C. H. (1990). The dispersal of sporophytes of Undaria pinnatifida by coastal shipping in New Zealand, and implications for further dispersal of Undaria in France. British Phycological Journal, 25(4), 301–313. Hay, C. H., & Luckens, P. A. (1987). The Asian kelp Undaria pinnatifida (Phaeophyta: Laminariales) found in a New Zealand Harbour. New Zealand Journal of Botany, 25(2), 329–332. Hay, C. H., & Villouta, E. (1993). Seasonality of the adventive Asian kelp Undaria pinnatifida in New Zealand. Botanica Marina, 36(5), 461–476. Heiser, S., Hall-Spencer, J. M., & Hiscock, K. (2014). Assessing the extent of establishment of Undaria pinnatifida in Plymouth sound special area of conservation, UK. Marine Biodiversity Records, 7, e93. Henkel, S. K., & Hofmann, G. E. (2008). Thermal ecophysiology of gametophytes cultured from invasive Undaria pinnatifida (Harvey) Suringar in coastal California harbors. Journal of Experimental Marine Biology and Ecology, 367(2), 164–173. Hewitt, C. L. (2003). Marine biosecurity issues in the world oceans: Global activities and Australian directions. Ocean Yearbook Online, 17(1), 193–212. Hewitt, C. L., Campbell, M. L., McEnnulty, F., Moore, K. M., Murfet, N. B., Robertson, B., & Schaffelke, B. (2005). Efficacy of physical removal of a marine pest: the introduced kelp Undaria pinnatifida in a Tasmanian marine reserve. Biological Invasions, 7(2), 251–263. Hobbs, R. J., & Humphries, S. E. (1995). An integrated approach to the ecology and management of plant invasions. Conservation Biology, 9(4), 761–770. Hulme, P. E. (2006). Beyond control: Wider implications for the management of biological invasions. Journal of Applied Ecology, 43(5), 835–847. Irigoyen, A. J., Eyras, C., & Parma, A. M. (2010). Alien algae Undaria pinnatifida causes habitat loss for rocky reef fishes in North Patagonia. Biological Invasions, 13(1), 17–24. Irigoyen, A. J., Trobbiani, G., Sgarlatta, M. P., & Raffo, M. P. (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. Biological Invasions, 13(7), 1521–1532. James, K., Kibele, J., & Shears, N. T. (2015). Using satellite-derived sea surface temperature to predict the potential global range and phenology of the invasive kelp Undaria pinnatifida. Biological Invasions, 17(12), 3393–3408. James, K., Middleton, I., Middleton, C., & Shears, N. (2014). Discovery of Undaria pinnatifida (Harvey) Suringar, 1873 in northern New Zealand indicates increased invasion threat in subtropical regions. BioInvasions Records, 3(1), 21–24. James, K., & Shears, N. T. (2016a). Population ecology of the invasive kelp Undaria pinnatifida towards the upper extreme of its temperature range. Marine Biology, 163, 34. James, K., & Shears, N. T. (2016b). Proliferation of the invasive kelp Undaria pinnatifida at aquaculture sites promotes spread to coastal reefs. Marine Biology, 163, 225. Jimenez, R. S., Hepburn, C. D., Hyndes, G. A., McLeod, R. J., Taylor, R. B., & Hurd, C. L. (2015). Do native subtidal grazers eat the invasive kelp Undaria pinnatifida? Marine Biology, 162, 2521–2526. Jormalainen, V., Gagnon, K., Sjroos, J., & Rothusler, E. (2016). The invasive mud crab enforces a major shift in a rocky littoral invertebrate community of the Baltic Sea. Biological Invasions, 18(5), 1409–1419. Jousson, O., Pawlowski, J., Zaninetti, L., Zechman, F. W., Dini, F., Di Giuseppe, G., … Meinesz, A. (2000). Invasive alga reaches California: The alga has been identified that threatens to smother Californian coastal ecosystems. Nature, 408(6809), 157–158. Kaplanis, N. J., Harris, J. L., & Smith, J. E. (2016). Distribution patterns of the non-native seaweeds Sargassum horneri (turner) C. Agardh and Undaria pinnatifida (Harvey) Suringar on the San Diego and Pacific coast of North America. Aquatic Invasions, 11(2), 111–124. Kim, Y. D., Ahn, J. K., Nam, M. M., Lee, C., Yoo, H. I., Yeon, S. Y., … Choi, J. S. (2016). Characteristics of algal succession following rock scraping at Imwon area in the east coast of Korea. Journal of Ocean University of China, 15(6), 1087–1093. Kim, Y. S., & Nam, K. W. (1997). Temperature and light responses on the growth and maturation of gametophytes of Undaria pinnatifida (Harvey) Suringar in Korea. Journal of the Korean Fisheries Society, 30, 505–510. Koh, C. H., & Shin, H. C. (1990). Growth and size distribution of some large brown algae in Ohori, east coast of Korea. Hydrobiologia, 204–205(1), 225–231. Kolar, C. S., & Lodge, D. M. (2001). Progress in invasion biology: Predicting invaders. TRENDS in Ecology and Evolution, 16(4), 199–204. Leliaert, F., Kerckhof, F., & Coppejans, E. (2000). Eerste waarnemingen van Undaria pinnatifida (Harvey) Suringar (Laminariales, Phaeophyta) en de epifyt pterothamnion plumula (Ellis) Nageli (Ceramiales, Rhodophyta) in Noord Frankrijk en belgie. Het Zeepard, 59, 71–73. Levine, J. M., & D'Antonio, C. M. (1999). Elton revisited: A review of evidence linking diversity and invasibility. Oikos, 87(1), 15–26. Lockwood, J. L., Cassey, P., & Blackburn, T. (2005). The role of propagule pressure in explaining species invasions. TRENDS in Ecology and Evolution, 20(5), 223–228. Lodge, D. M. (1993). Biological invasions: Lessons for ecology. Trends in Ecology & Evolution, 8(4), 133–137. Lowe, S., Browne, M., Boudjekas, S., & De Poorter, M. (2000). 100 of the World's Worst Invasive Alien Species. The Invasive Species Specialist Group (ISSG) a specialist group of the Species Survival Commission (SSC) of the World Conservation Union (IUCN), 11 pp. Lugo, A. E. (2004). The outcome of alien tree invasions in Puerto Rico. Frontiers in Ecology and the Environment, 2(5), 265–273. MacDougall, A. S., & Turkington, R. (2005). Are invasive species drivers or passengers of change in degraded ecosystems. Ecology, 86(1), 42–55. MAF (2010). The commercial use of Undaria pinnatifida an exotic Asian seaweed. Report Paper No: 2010/02, Ministry of Agriculture and Forestry, 11 pp. Martin, J. P., & Bastida, R. (2008). The invasive seaweed Undaria pinnatifida (Harvey) Suringar in Ria Deseado (southern Patagonia, Argentina): Sporophyte cycle and environmental factors determining its distribution. Revista De Biologia Marina Y Oceanografia, 43(2), 335–344. Matsuyama, K. (1983). Photosynthesis of Undaria pinnatifida Suringar f. Distans Miyabe et Okamura (Phaeophyceae) from Oshoro bay. 1. Seasonal changes of photosynthetic and respiratory rates. Scientific Reports of Hokkaido Fisheries Experimental Station, 25, 187–194. McKinney, M. L., & Lockwood, J. L. (1999). Biotic homogenization: A few winners replacing many losers in the next mass extinction. TRENDS in Ecology and Evolution, 14(11), 450–453. Minchin, D., Cook, E. J., & Clark, P. F. (2013). Alien species in British brackish and marine waters. Aquatic Invasions, 8(1), 3–19. Minchin, D., & Nunn, J. (2014). The invasive brown alga Undaria pinnatifida (Harvey) Suringar, 1873 (Laminariales: Alariaceae), spreads northwards in Europe. BioInvasions Records, 3(2), 57–63. Molnar, J. L., Gamboa, R. L., Revenga, C., & Spalding, M. D. (2008). Assessing the global threat of invasive species to marine biodiversity. Frontiers in Ecology and the Environment, 6(9), 485–492. Morelissen, B., Dudley, B. D., Geange, S. W., & Phillips, N. E. (2013). Gametophyte reproduction and development of Undaria pinnatifida under varied nutrient and irradiance conditions. Journal of Experimental Marine Biology and Ecology, 448, 197–206. Morelissen, B., Dudley, B. D., & Phillips, N. E. (2016). Recruitment of the invasive kelp Undaria pinnatifida does not always benefit from disturbance to native algal communities in low-intertidal habitats. Marine Biology, 163, 241. Morita, T., Kurashima, A., & Maegawa, M. (2003a). Temperature requirements for the growth and maturation of the gametophytes of Undaria pinnatifida and U. undarioides (Laminariales, Phaeophyceae). Phycological Research, 51(3), 154–160. Morita, T., Kurashima, A., & Maegawa, M. (2003b). Temperature requirements for the growth of young sporophytes of Undaria pinnatifida and Undaria undarioides (Laminariales, Phaeophyceae). Phycological Research, 51(4), 266–270. Morrison, K. D., Reekie, E. G., & Jensen, K. I. N. (1998). Biocontrol of common St. Johnswort (hypericum perforatum) with Chrysolina hyperici and a host-specific Colletotrichum gloeosporioides. Weed Technology, 12(3), 426–435. Nanba, N., Fujiwara, T., Kuwano, K., Ishikawa, Y., Ogawa, H., & Kado, R. (2011). Effect of water flow velocity on growth and morphology of cultured Undaria pinnatifida sporophytes (Laminariales, Phaeophyceae) in Okirai bay on the Sanriku coast, Northeast Japan. Journal of Applied Phycology, 23(6), 1023–1030. Newsome and Noble (1986) Ecological and physiological characters of invading species. In: Ecology of Biological Invasions. Eds R H Groves and J J Burdon. Cambridge University Press, Cambridge, UK. p1-20 NSPMMPI (2015). The national system for the prevention and management of marine pest in cursions – Australian Emergency marine pest plan (empplan) rapid response manual Undaria pinnatifida. Report, Australian Government – The National System for the Prevention and Management of Marine Pest Incursions, 52 pp. NSW (1994). Schedule 6C noxious fish and noxious marine vegetation. New South Wales Fisheries Management Act 1994 No. 38. Nyberg, C. D., & Wallentinus, I. (2005). Can species traits be used to predict marine macroalgal introductions? Biological Invasions, 7, 265–279. Occhipinti-Ambrogi, A. (2007). Global change and marine communities: Alien species and climate change. Marine Pollution Bulletin, 55(7–9), 342–352. Olabarria, C., Rodil, I. F., Incera, M., & Troncoso, J. S. (2009). Limited impact of Sargassum muticum on native algal assemblages from rocky intertidal shores. Marine Environmental Research, 67(3), 153–158. Paalvast, P., van Wesenbeeck, B. K., van der Velde, G., & de Vries, M. B. (2012). Pole and pontoon hulas: An effective way of ecological engineering to increase productivity and biodiversity in the hard-substrate environment of the port of Rotterdam. Ecological Engineering, 44, 199–209. Padilla, D. K. (2010). Context-dependent impacts of a non-native ecosystem engineer, the pacific oyster Crassostrea gigas. Integrative and Comparative Biology, 50(2), 213–225. Pang, S., & Luning, K. (2004). Photoperiodic long-day control of Sporophyll and hair formation in the brown alga Undaria pinnatifida. Journal of Applied Phycology, 16(2), 83–92. Pang, S., & Shan, T. (2008). Zoospores of Undaria pinnatifida: their efficiency to attach under different water velocities and conjugation behavior during attachment. Acta Oceanologica Sinica, 27(6), 94–101. Pang, S., & Wu, C. (1996). Study on gametophyte vegetative growth of Undaria pinnatifida and its applications. Chinese Journal of Oceanology and Limnology, 14(3), 205–210. Parker, I. M., Simberloff, D., Lonsdale, W. M., Goodell, K., Wonham, M., Kareiva, P. M., … Goldwasser, L. (1999). Impact: Toward a framework for understanding the ecological effects of invaders. Biological Invasions, 1(1), 3–19. Perez, R., Lee, J. Y., & Juge, C. (1981). Observations sur la biologie de l'algue japonaise Undaria pinnatifida (Harvey) suringar introduite accidentellement dans l'etang de thau. Science et Peche, 325, 1–12. Perez-Cirera, J., Salinas, J., Cremades, J., Barbara, I., Granja, A., Veiga, A., & Fuertes, C. (1997). Cultivo de Undaria pinnatifida (laminariales, phaeophyta) en galicia. Nova Acta Cientifica Compostelana (Bioloxia), 7, 3–28. Perrings, C., Burgiel, S., Lonsdale, M., Mooney, H., & Williamson, M. (2010). International cooperation in the solution to trade-related invasive species risks. Annals of the New York Academy of Sciences, 1195, 198–212. Peteiro, C., & Freire, O. (2011). Effect of water motion on the cultivation of the commercial seaweed Undaria pinnatifida in a coastal bay of Galicia, northwest Spain. Aquaculture, 314(1–4), 269–276. Peteiro, C., & Sanchez, N. (2012). Comparing salinity tolerance in early stages of the sporophytes of a non-indigenous kelp (Undaria pinnatifida) and a native kelp (Saccharina Latissima). Russian Journal of Marine Biology, 38(2), 197–200. Peteiro, C., Sanchez, N., & Martinez, B. (2016). Mariculture of the Asian kelp Undaria pinnatifida and the native kelp Saccharina Latissima along the Atlantic coast of Southern Europe: An overview. Algal Research, 15, 9–23. Pimentel, D., Zuniga, R., & Morrison, D. (2005). Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecological Economics 52 (3SPEC. ISS.), 273–288. Primo, C., Hewitt, C. L., & Campbell, M. L. (2010). Reproductive phenology of the introduced kelp Undaria pinnatifida (Phaeophyceae, Laminariales) in Port Phillip bay (Victoria, Australia). Biological Invasions, 12(9), 3081–3092. Raffo, P. M., Eyras, C. M., & Iribarne, O. O. (2009). The invasion of Undaria pinnatifida to a Macrocystis pyrifera kelp in Patagonia (Argentina, South-West Atlantic). Journal of the Marine Biological Association of the United Kingdom, 89(8), 1571–1580. Richardson, D. M., Pysek, P., & Carlton, J. T. (2011). A compendium of essential concepts and terminology in invasion ecology. In D. M. Richardson (Ed.), Fifty years of invasion ecology: the legacy of Charles Elton (pp. 409–420). Sussex, UK: Blackwell Publishing Ltd. Rodriguez, L. F. (2006). Can invasive species facilitate native species? Evidence of how, when, and why these impacts occur. Biological Invasions, 8(4), 927–939. Ross, D. J., Johnson, C. R., & Hewitt, C. L. (2003). Assessing the ecological impacts of an introduced seastar: The importance of multiple methods. Biological Invasions, 5(1–2), 3–21. Ruiz, G. M., Carlton, J. T., Grosholz, E. D., & Hines, A. H. (1997). Global invasions of marine and estuarine habitats by non-indigenous species: mechanisms, extent, and consequences. American Zoologist, 37(6), 621–632. Russell, L. K., Hepburn, C. D., Hurd, C. L., & Stuart, M. D. (2008). The expanding range of Undaria pinnatifida in southern New Zealand: distribution, dispersal mechanisms and the invasion of wave-exposed environments. Biological Invasions, 10(1), 103–115. Saito, Y. (1975). Advance of phycology in Japan, Book section Undaria (pp. 304–320). The Hague: VEB Gustav Fischer Verlag. Sala, O. E., Chapin Iii, F. S., Armesto, J. J., Berlow, E., Bloomfield, J., Dirzo, R., … Wall, D. H. (2000). Global biodiversity scenarios for the year. Science, 287(5459), 1770–1774. Sanchez, I., & Fernandez, C. (2005). Impact of the invasive seaweed Sargassum muticum (Phaeophyta) on an intertidal macroalgal assemblage. Journal of Phycology, 41(5), 923–930. Schaffelke, B., Campbell, M. L., & Hewitt, C. L. (2005). Reproductive phenology of the introduced kelp Undaria pinnatifida (Phaeophyceae, Laminariales) in Tasmania, Australia. Phycologia, 44(1), 84–94. Schaffelke, B., & Hewitt, C. L. (2007). Impacts of introduced seaweeds. Botanica Marina, 50(5–6), 397–417. Schiel, D. R., & Thompson, G. A. (2012). Demography and population biology of the invasive kelp Undaria pinnatifida on shallow reefs in southern New Zealand. Journal of Experimental Marine Biology and Ecology, 434, 25–33. Schlaepfer, M. A., Sax, D. F., & Olden, J. D. (2011). The potential conservation value of non-native species. Conservation Biology, 25(3), 428–437. Schlaepfer, M. A., Sax, D. F., & Olden, J. D. (2012). Toward a more balanced view of non-native species. Conservation Biology, 26(6), 1156–1158. Shpigel, M., & Blaylock, R. A. (1991). The pacific oyster, Crassostrea gigas, as a biological filter for a marine fish aquaculture pond. Aquaculture, 92(C), 187–197. Silva, P. C., Woodfield, R. A., Cohen, A. N., Harris, L. H., & Goddard, J. H. R. (2002). First report of the Asian kelp Undaria pinnatifida in the northeastern Pacific Ocean. Biological Invasions, 4(3), 333–338. Simberloff, D. (2011). How common are invasion-induced ecosystem impacts? Biological Invasions, 13(5), 1255–1268. Sinner, J., Forrest, B. M., & Taylor, M. D. (2000). A strategy for managing the Asian kelp Undaria: Final Report, Volume No. 578 of Cawthorn Report. Cawthorn Institute, Nelson: Ministry of Fisheries, New Zealand, pp 130. Skriptsova, A., Khomenko, V., & Isakov, V. (2004). Seasonal changes in growth rate, morphology and alginate content in Undaria pinnatifida at the northern limit in the Sea of Japan (Russia). Journal of Applied Phycology, 16, 17–21. Sliwa, C., Johnson, C. R., & Hewitt, C. L. (2006). Mesoscale dispersal of the introduced kelp Undaria pinnatifida attached to unstable substrata. Botanica Marina, 49(5–6), 396–405. South, P. M., Lilley, S. A., Tait, L. W., Alestra, T., Hickford, M. J. H., Thomsen, M. S., & Schiel, D. R. (2015). Transient effects of an invasive kelp on the community structure and primary productivity of an intertidal assemblage. Marine and Freshwater Research, 67(1), 103–112. South, P. M., & Thomsen, M. S. (2016). The ecological role of invading Undaria pinnatifida: an experimental test of the driver-passenger models. Marine Biology, 163, 175. Stachowicz, J. J., Fried, H., Osman, R. W., & Whitlatch, R. B. (2002). Biodiversity, invasion resistance, and marine ecosystem function: Reconciling pattern and process. Ecology, 83(9), 2575–2590. Staehr, P. A., Pedersen, M. F., Thomsen, M. S., Wernberg, T., & Krause-Jensen, D. (2000). Invasion of Sargassum muticum in Limfjorden (Denmark) and its possible impact on the indigenous macroalgal community. Marine Ecology Progress Series, 207, 79–88. Suarez-Jimenez, R., Hepburn, C. D., Hyndes, G. A., McLeod, R. J., Taylor, R. B., & Hurd, C. L. (2017). Importance of the invasive macroalga Undaria pinnatifida as trophic subsidy for a beach consumer. Marine Biology, 164(5), 113. Suto, S. (1952). On shedding of zoospores in some algae of Laminariaceae-II. Nippon Suisan Gakkaishi, 18(1), 1–5. Thompson, G. A., & Schiel, D. R. (2012). Resistance and facilitation by native algal communities in the invasion success of Undaria pinnatifida. Marine Ecology Progress Series, 468, 95–105. Thomsen, M. S., Olden, J. D., Wernberg, T., Griffin, J. N., & Silliman, B. R. (2011). A broad framework to organize and compare ecological invasion impacts. Environmental Research, 111(7), 899–908. Thomsen, M. S., Wernberg, T., South, P. M., & Schiel, D. R. (2016). Non-native seaweeds drive changes in marine coastal communities around the world (pp. 147–185). Dordrecht: Springer Netherlands. Thomsen, M. S., Wernberg, T., Tuya, F., & Silliman, B. R. (2009). Evidence for impacts of nonindigenous macroalgae: A meta-analysis of experimental field studies. Journal of Phycology, 45(4), 812–819. Thornber, C. S., Kinlnan, B. P., Graham, M. H., & Stachowicz, J. J. (2004). Population ecology of the invasive kelp Undaria pinnatifida in California: environmental and biological controls on demography. Marine Ecology Progress Series, 268, 69–80. Valentine, J. P., & Johnson, C. R. (2003). Establishment of the introduced kelp Undaria pinnatifida in Tasmania depends on disturbance to native algal assemblages. Journal of Experimental Marine Biology and Ecology, 295(1), 63–90. Valentine, J. P., & Johnson, C. R. (2004). Establishment of the introduced kelp Undaria pinnatifida following dieback of the native macroalga phyllospora comosa in Tasmania. Australia. Marine and Freshwater Research, 55(3), 223–230. Valentine, J. P., & Johnson, C. R. (2005). Persistence of sea urchin (Heliocidaris erythrogramma) barrens on the east coast of Tasmania: Inhibition of macroalgal recovery in the absence of high densities of sea urchins. Botanica Marina, 48(2), 106–115. Valentine, J. P., Magierowski, R. H., & Johnson, C. R. (2007). Mechanisms of invasion: Establishment, spread and persistence of introduced seaweed populations. Botanica Marina, 50(5–6), 351–360. Veiga, P., Torres, A. C., Rubal, M., Troncoso, J., & Sousa-Pinto, I. (2014). The invasive kelp Undaria pinnatifida (Laminariales, Ochrophyta) along the north coast of Portugal: Distribution model versus field observations. Marine Pollution Bulletin, 84(1–2), 363–365. Verbrugge, L., de Hoop, L., Leuven, R., Aukema, R., Beringen, R., Creemers, R., … deHullu, E. (2015). Expertpanelbeoordeling van (potentile) risicos en managementopties van invasieve exoten in nederland. Report Inhoudelijke input voor het Nederlandse standpunt over de plaatsing van soorten op EU-verordening 1143/2014., Bureau Risicobeoordeling & Onderzoeksprogrammering, Nederlandse Voedsel- enWarenautoriteit (NVWA), Ministerie van Economische Zaken, 54 pp. Viejo, R. M. (1997). The effects of colonization by Sargassum muticum on Tidepool Macroalgal assemblages. Journal of the Marine Biological Association of the United Kingdom, 77, 325–340. Vitule, J. R. S., Freire, C. A., Vazquez, D. P., Nuez, M. A., & Simberloff, D. (2012). Revisiting the potential conservation value of non-native species. Conservation Biology, 26(6), 1153–1155. VLIZ (2011). Japanese kelp - Undaria pinnatifida. Non-native species in the Belgian part of the north sea and adjacent estuaries, alien species consortium, Anders marine institute. Retrieved from http://www.marinespecies.org/introduced/wiki/Japanse_kelp. Watanabe, Y., Nishihara, G. N., Tokunaga, S., & Terada, R. (2014). The effect of irradiance and temperature responses and the phenology of a native alga, Undaria pinnatifida (Laminariales), at the southern limit of its natural distribution in Japan. Journal of Applied Phycology, 26, 2405–2415. Williams, F., Eschen, R., Harris, A., Djeddour, D., Pratt, C., Shaw, R. S., … Murphy, S. T (2010). The economic cost of invasive non-native species on Great Britain, Volume CABI Project No. VM10066 Final Report. Wallingford, UK, 199 pp. Williams, S. L., & Smith, J. E. (2007). A global review of the distribution, taxonomy, and impacts of introduced seaweeds. Annual Review of Ecology, Evolution, and Systematics, 38, 327–359. Williamson, M. H., & Fitter, A. (1996). The characters of successful invaders. Biological Conservation, 78(1–2), 163–170. Wood, C. A., Bishop, J. D. D., & Yunnie, A. L. E. (2015). Comprehensive Reassessment of NNS in Welsh marinas, Volume Grant GU9430. Welsh Government Resilient Ecosystems Fund (REF), 40 pp. Wotton, D. M., O'Brien, C., Stuart, M. D., & Fergus, D. J. (2004). Eradication success down under: heat treatment of a sunken trawler to kill the invasive seaweed Undaria pinnatifida. Marine Pollution Bulletin, 49(9–10), 844–849. Yamanaka, R., & Akiyama, K. (1993). Cultivation and utilization of Undaria pinnatifida (Wakame) as food. Journal of Applied Phycology, 5(2), 249–253. Zabin, C., Ashton, G., Brown, C., & Ruiz, G. (2009). Northern range expansion of the Asian kelp Undaria pinnatifida (Harvey) Suringar (Laminariales, Phaeophyceae) in western North America. Aquatic Invasions, 4(3), 429–434. Zenni, R. D., Lamy, J. B., Lamarque, L. J., & Port, A. J. (2014). Adaptive evolution and phenotypic plasticity during naturalization and spread of invasive species: Implications for tree invasion biology. Biological Invasions, 16(3), 635–644.