Abstract
It is likely that the introduction of the brown macroalga Undaria pinnatfida from the Pacific into the North Atlantic will impact competitively on the native species Saccorhiza polyschides; both are large kelps occupying the same subtidal zone with very similar life histories. The present study examines their tolerance to changes in salinity, under laboratory conditions, in order to provide a better understanding of their respective competitiveness in an estuarine environment. Experiments were carried out over a full range of salinity values, from 35 to 0, with respect to zoospore settlement and attachment, germination, post-germination progression to form gametophytes, gametophyte sex ratio, sporophyte production and blade length. Undaria zoospores settled and attached over the salinity range from 35 to 14 and germinated between 35 and 3.5. Post-germination progression occurred over the range from 35 to 14 whilst only small differences in the male/female ratio were recorded. Sporophyte blade production and development occurred over the range from 35 to 17.5 and peak production and longest blade length was recorded at 21. Saccorhiza zoospores settled and attached at and above 24.5 and germinated between 35 and 21. Sporophyte production and blade development occurred over the range from 35 to 24.5. In general, Undaria was shown to be much more tolerant of reductions in salinity compared to Saccorhiza and is more likely to penetrate further into estuarine environments.
About the authors
Marie-Fanny Racault is a biological oceanographer interested in the study of climate impact and risks on marine ecosystem resources and marine pathogens. She works as a senior Earth Observation scientist at the Plymouth Marine Laboratory, UK. Her main topics of expertise are (1) understanding the evolutionary history of pyrenoid-bearing taxa in brown algae using molecular phylogenies; (2) developing applications of Earth observations (in-situ, remote-sensing, modelling) for water-associated diseases surveillance and mapping; (3) analysing bio-physical interactions and climate processes to explain and predict changes in the phenology of oceanic primary producers.
Robert L. Fletcher is a reader in marine environmental sciences at the University of Portsmouth, UK. His main research interest is the taxonomy, systematics, life histories, molecular biology and floristics of the Phaeophyceae. Other interests include the marine algal flora of the south coast of England, introduced macroalgae, marine algae as fouling organisms and their control and marine pollution, particularly eutrophication and the use of macroalgae as bioassay test organisms.
Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
Research funding: None declared.
Conflict of interest statement: The authors declare no conflicts of interest regarding this article.
References
Aguilar-Rosas, R., Aguilar-Rosas, L.E., Avila-Serrano, G., and Marcos-Ramirez, R. (2004). First record of Undaria pinnatifida (Harvey) Suringar (Laminariales, Phaeophyta) on the Pacific coast of Mexico. Bot. Mar. 47: 255–258, https://doi.org/10.1515/bot.2004.028.Search in Google Scholar
Akiyama, K. and Kurogi, M. (1982). Cultivation of Undaria pinnatifida (Harvey) Suringar, the decrease in crops from natural plants following crop increase from cultivation. Bull. Tohoku Reg. Fish. Res. Lab. 44: 91–100.Search in Google Scholar
Anderson, E.K. and North, W.J. (1966). In situ studies of spore production and dispersal in the giant kelp Macrocystis pyrifera. Proc. Int. Seaweed Symp. 5: 73–86, https://doi.org/10.1016/b978-0-08-011841-3.50011-2.Search in Google Scholar
Báez, J.C., Olivero, J., Peteiro, C., Ferri-Yánez, F., García-Soto, C., and Real, R. (2010). Macro-environmental modelling of the current distribution of Undaria pinnatifida (Laminariales, Ochrophyta) in northern Iberia. Biol. Invasions 12: 21–31, https://doi.org/10.1007/s10530-009-9614-1.Search in Google Scholar
Battershill, C., Miller, K., and Cole, R. (1998). The understorey of marine invasions. Seaf. N. Z. 6: 3133.Search in Google Scholar
Bollen, M., Pilditch, C.A., Battershill, C.N., and Bischof, K. (2016). Salinity and temperature tolerance of the invasive alga Undaria pinnatifida and native New Zealand kelps: implications for competition. Mar. Biol. 163: 194, https://doi.org/10.1007/s00227-016-2954-3.Search in Google Scholar
Boudouresque, C.-F. and Verlaque, M. (2008). Biological pollution in the Mediterranean Sea: invasive versus introduced macrophytes. Mar. Pollut. Bull. 44: 32–38.10.1016/S0025-326X(01)00150-3Search in Google Scholar
Boudouresque, C.F., Gerbal, M., and Knoepffler-Peguy, M. (1985). L’algue japonnaise Undaria pinnatifida (Phaeophyceae, Laminariales) en Méditerranée. Phycologia 24: 364–366, https://doi.org/10.2216/i0031-8884-24-3-364.1.Search in Google Scholar
Brown, M.T. and Lamare, M.D. (1994). The distribution of Undaria pinnatifida (Harvey) Suringar within Timaru Harbour, New Zealand. Jpn. J. Phycol. 42: 63–70.Search in Google Scholar
Campbell, S.J. and Burridge, T.R. (1998). Occurrence of Undaria pinnatifida (Phaeophyta: Laminariales) in Port Phillip Bay, Victoria, Australia. Mar. Freshw. Res. 49: 379–381, https://doi.org/10.1071/mf97010.Search in Google Scholar
Casas, G., Scrosati, R., and Piriz, M.L. (2004). The invasive kelp Undaria pinnatifida (Phaeophyceae, Laminariales) reduces native seaweed diversity in Nuevo Gulf (Patagonia, Argentina). Biol. Invasions 6: 411–416, https://doi.org/10.1023/b:binv.0000041555.29305.41.10.1023/B:BINV.0000041555.29305.41Search in Google Scholar
Casas, G.N. and Piriz, M.L. (1996). Surveys of Undaria pinnatifida (Laminariales, Phaeophyta) in Golfo Nuevo, Argentina. Proc. Int. Seaweed Symp. 15: 213–215, https://doi.org/10.1007/978-94-009-1659-3_29.Search in Google Scholar
Casas, G.N., Piriz, M.L., and Parodi, E.R. (2008). Population features of the invasive kelp Undaria pinnatifida (Phaeophyceae: Laminariales) in Nuevo Gulf (Patagonia, Argentina). J. Mar. Biol. Assoc. U. K. 88: 21–28, https://doi.org/10.1017/s0025315408000246.Search in Google Scholar
Castric-Fey, A., Girard, A., and L’Hardy-Halos, M.T. (1993). The distribution of Undaria pinnatifida (Phaeophyceae, Laminariales) on the coast of St. Malo (Brittany, France). Bot. Mar. 36: 351–358, https://doi.org/10.1515/botm.1993.36.4.351.Search in Google Scholar
Cecere, E., Petrocelli, A., and 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). Cryptogam. Algol. 21: 305–309, https://doi.org/10.1016/s0181-1568(00)00113-6.Search in Google Scholar
Choi, H.G., Kim, Y.S., Lee, S.J., and Nam, K.W. (2007). Growth and Reproductive Patterns of Undaria pinnatifida Sporophytes in a Cultivation Farm in Busan, Korea. J. Appl. Phycol. 19: 131–138, https://doi.org/10.1007/s10811-006-9119-6.Search in Google Scholar PubMed PubMed Central
Cremades, J., Freire-Gago, Ó., and Peteiro, C. (2006). Biología, distribucióne integración del alga alóctona Undaria pinnatifida (Laminariales, Phaeophyta) en las comunidades bentónicas de las costas de Galicia (NW de la Península Ibérica). An. del Jardín Botánico Madr. 63: 169–187, https://doi.org/10.3989/ajbm.2006.v63.i2.6.Search in Google Scholar
Curiel, D., Bellemo, G., Marzocchi, M., Scattolin, M., and 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, https://doi.org/10.1023/a:1003437105147.10.1023/A:1003437105147Search in Google Scholar
Curiel, D., Guidetti, P., Bellemo, G., and Scattolin, M. (2002). The introduced alga Undaria pinnatifida (Laminariales, Alariaceae) in the lagoon of Venice. Hydrobiologia 477: 209–219, https://doi.org/10.1023/a:1021094008569.10.1023/A:1021094008569Search in Google Scholar
Dayton, P.K. (1973). Dispersion, dispersal and persistence of the annual intertidal alga Postelsia palmaeformis. Ecology 54: 433–438, https://doi.org/10.2307/1934353.Search in Google Scholar
Dayton, P.K. (1985). Ecology of kelp communities. Annu. Rev. Ecol. Systemat. 16: 215–245, https://doi.org/10.1146/annurev.es.16.110185.001243.Search in Google Scholar
Epstein, G. and Smale, D.A. (2017). Undaria pinnatifida: a case study to highlight challenges in marine invasion ecology and management. Ecol. Evol. 7: 8624–8642, https://doi.org/10.1002/ece3.3430.Search in Google Scholar PubMed PubMed Central
Farrell, P., and Fletcher, R.L. (2000). The biology and distribution of the kelp, Undaria pinnatiftda, (Harvey) Suringar in the Solent. In: Collins, M., and Ansell, K. (Eds.), Solent Science - a review. Elsevier, Oxford, pp. 311–314.Search in Google Scholar
Farrell, P. and 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). J. Exp. Mar. Biol. Ecol. 334: 236–243, https://doi.org/10.1016/j.jembe.2006.02.006.Search in Google Scholar
Fletcher, R.L. and Farrell, P. (1999). Introduced brown algae in the north east Atlantic, with particular respect to Undaria pinnatifida (Harvey) Suringar. Helgol. Meeresunters. 52: 259–275.10.1007/BF02908901Search in Google Scholar
Fletcher, R.L. and Manfredi, C. (1995). The occurrence of Undaria pinnatifida on the South Coast of England. Bot. Mar. 38: 355–358, https://doi.org/10.1515/botm.1995.38.1-6.355.Search in Google Scholar
Floc’h, J.Y., Pagot, R., and Wallentinus, I. (1991). The Japanese brown alga Undaria pinnatifida on the coast of France and its possible establishment in European waters. J. Conseil Int. pour Explor. Mer 47: 379–390, https://doi.org/10.1093/icesjms/47.3.379.Search in Google Scholar
Floc’h, J.-Y., Pajot, R., and Mouret, V. (1996). Undaria pinnatifida (Laminariales, Phaeophyta) 12 years after its introduction into the Atlantic Ocean. Proc. Int. Seaweed Symp. 15: 217–222, https://doi.org/10.1007/bf00047810.Search in Google Scholar
Forrest, B.M., Brown, S.N., Taylor, M.D., Hurd, C.L., and Hay, C.H. (2000). The role of natural dispersal mechanisms in the spread of Undaria pinnatifida Laminariales, Phaeophyceae. Phycologia 39: 547–553.10.2216/i0031-8884-39-6-547.1Search in Google Scholar
Grange, K.R., Singleton, R.J., Goldberg, W.M., and Hill, P.J. (1991). The underwater environment of Doubtful Sound: results from an instrument array moored from November 1987 to June 1989. Miscellaneous Publication No. 105. New Zealand Oceanographic Institute. 32 p. 32.Search in Google Scholar
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. Br. Phycol. J. 25: 301–313, https://doi.org/10.1080/00071619000650331.Search in Google Scholar
Hay, C.H. and Luckens, P.A. (1987). The Asian kelp Undaria pinnatifida (Phaeophyta: Laminariales) found in a New Zealand harbour. N. Z. J. Bot. 25: 329–332, https://doi.org/10.1080/0028825x.1987.10410079.Search in Google Scholar
Hay, C.H. and Villouta, E. (1993). Seasonality of the adventive Asian kelp Undaria pinnatifida in New Zealand. Bot. Mar. 36: 461–476, https://doi.org/10.1515/botm.1993.36.5.461.Search in Google Scholar
Hewitt, C.L., Campbell, M.L., Mcennulty, F., Moore, K.M., Murfet, N.B., Robertson, B., and Schaffelke, B. (2005). Efficacy of physical removal of a marine pest: the introduced kelp Undaria pinnatifida in a Tasmanian Marine. Reserve. Biol. Invasions 7: 251–263, https://doi.org/10.1007/s10530-004-0739-y.Search in Google Scholar
Hsiao, S.I.C. and Druehl, L.D. (1973). Environmental control of gametogenesis in Laminaria saccharina. IV. In situ development of gametophytes and young sporophytes. J. Phycol. 9: 160–164, https://doi.org/10.1111/j.0022-3646.1973.00160.x.Search in Google Scholar
Kain, J. (1979). A view of the genus Laminaria. Oceanogr. Mar. Biol. 17: 101–153.Search in Google Scholar
Kraan, S. (2017). Undaria marching on; late arrival in the Republic of Ireland. J. Appl. Phycol. 29: 1107–1114, https://doi.org/10.1007/s10811-016-0985-2.Search in Google Scholar PubMed PubMed Central
Kurogi, M., and Akiyama, K. (1957). Studies of ecology and culture of Undaria pinnatifida. Bull. Tohoku Reg. Fish. Res. Lab. 10: 95–117.Search in Google Scholar
Ladah, L.B. and Zertuche-González, J.M. (2007). Survival of microscopic stages of a perennial kelp (Macrocystis pyrifera) from the center and the southern extreme of its range in the Northern Hemisphere after exposure to simulated El Niño stress. Mar. Biol. 152: 677–686, https://doi.org/10.1007/s00227-007-0723-z.Search in Google Scholar
Ladah, L.B., Zertuche-González, J.A., and Hernández-Carmona, G. (1999). Giant kelp (Macrocystis pyrifera, Phaeophyceae) recruitment near its southern limit in Baja California after mass disappearance during ENSO 1997–1998. J. Phycol. 35: 1106–1112, https://doi.org/10.1046/j.1529-8817.1999.3561106.x.Search in Google Scholar
Martin, J.P. and Bastida, R. (2008). El Alga invasora Undaria pinnatifida (Harvey) Suringar en la Ría Deseado (Patagonia austral, Argentina): ciclo del esporofito y factores ambientales determinantes de su distribución. Rev. Biol. Mar. Oceanogr. 432: 335–344.10.4067/S0718-19572008000200011Search in Google Scholar
Minchin, D. and Nunn, J. (2014). The invasive brown alga Undaria pinnatifida (Harvey) Suringar, 1873 (Laminariales: Alariaceae), spreads northwards in Europe. BioInvasions Rec. 3: 57–63, https://doi.org/10.3391/bir.2014.3.2.01.Search in Google Scholar
Norton, T.A. (1970). Synopsis of biological data on Saccorhiza polyschides. Fao Fish. Synop. 83: 11–93.Search in Google Scholar
Norton, T.A. and Burrows, E.M. (1969). Studies on marine algae of the British Isles 7. Saccorhiza polyschides (Lightf.) Batt. Br. Phycol. J. 4: 19–53, https://doi.org/10.1080/00071616900650031.Search in Google Scholar
Norton, T.A. and South, G.R. (1969). Influence of reduced salinity on the distribution of two laminarian algae. Okois 20: 320–326, https://doi.org/10.2307/3543199.Search in Google Scholar
Paine, R.T. (1979). Disaster, catastrophe, and local persistence of the sea palm, Postelsia palmaeformis. Science 205: 685–687, https://doi.org/10.1126/science.205.4407.685.Search in Google Scholar PubMed
Perez, R., Lee, J.Y., and Juge, C. (1981). Observations sur la biologie de l’algue japonaise Undaria pinnatifida (Harvey) Suringar introduite accidentellement dans l’etang de Thau. Sci. Peche 315: 1–12.Search in Google Scholar
Peteiro, C. and Sánchez, N. (2012). Comparing salinity tolerance in early stages of the sporophytes of a non-indigenous kelp (Undaria pinnatifida) and a native kelp (Saccharina latissima). Russ. J. Mar. Biol. 38: 197–200, https://doi.org/10.1134/s1063074012020095.Search in Google Scholar
Piriz, M.L. and Casas, G. (1994). Occurrence of Undaria pinnatifida in Golfo Nuevo, Argentina. Appl. Phycol. Forum 10: 4.Search in Google Scholar
Primo, C., Hewitt, C.L., and Campbell, M.L. (2010). Reproductive phenology of the introduced kelp Undaria pinnatifida (Phaeophyceae, Laminariales) in Port Phillip Bay (Victoria, Australia). Biol. Invasions 12: 3081–3092, https://doi.org/10.1007/s10530-010-9700-4.Search in Google Scholar
Saito, Y. (1975). Undaria. In: Tokida, J., and Hirose, H. (Eds.), Advance of phycology in Japan. The Hague: Junk, pp. 304–320.Search in Google Scholar
Sanderson, J.C. (1990). A preliminary survey of the distribution of the introduced macroalga, Undaria pinnatifida (Harvey) Suringar on the East Coast of Tasmania, Australia. Bot. Mar. 33: 153–157, https://doi.org/10.1515/botm.1990.33.2.153.Search in Google Scholar
Sanderson, J.C. (1997). Survey of Undaria pinnatifida in Tasmanian coastal waters, January-February 1997. Hobart, Australia: Report to the Tasmanian Department of Marine Resources.Search in Google Scholar
Sanderson, J.C. and Barrett, N. (1989). A survey of the distribution of the introduced Japanese macroalga Undaria pinnatifida (Harvey) Suringer in Tasmania, December 1988. Tasmania, Australia: Department of Sea Fisheries, pp. 1–35, Technical Report 38.Search in Google Scholar
Schaffelke, B., Campbell, M.L., and Hewitt, C.L. (2005). Reproductive phenology of the introduced kelp Undaria pinnatifida (Phaeophyceae, Laminariales) in Tasmania, Australia. Phycologia 44: 84–94, https://doi.org/10.2216/0031-8884(2005)44[84:rpotik]2.0.co;2.10.2216/0031-8884(2005)44[84:RPOTIK]2.0.CO;2Search in Google Scholar
Schiel, D.R. and Thompson, G.A. (2012). Demography and population biology of the invasive kelp Undaria pinnatifida on shallow reefs in southern New Zealand. J. Exp. Mar. Biol. Ecol. 434: 25–33, https://doi.org/10.1016/j.jembe.2012.07.023.Search in Google Scholar
Schreiber, E. (1930). Untersuchungen über parthenogenesis, geschlechtsbestimmung und Bastardierungsvermögen bei Laminarien. Planta Archiv für wissenschaftliche Botanik 12: 333–353, https://doi.org/10.1007/bf01948810.Search in Google Scholar
Schiller, J., Lackschewitz, D., Buschbaum, C., Reise, K., Pang, S., and Bischof, K. (2018). Heading northward to Scandinavia: Undaria pinnatifida in the northern Wadden Sea. Bot. Mar. 6: 365–371, https://doi.org/10.1515/bot-2017-0128.Search in Google Scholar
Silva, P.C., Woodfield, R.A., Cohen, A.N., Harris, L.H., and Goddard, J.H.R. (2002). First report of the Asian kelp Undaria pinnatifida in the Northeastern Pacific Ocean. Biol. Invasions 4: 333–338, https://doi.org/10.1023/a:1020991726710.10.1023/A:1020991726710Search in Google Scholar
Sinner, J., Forrest, B., and Taylor, M. (2000). A strategy for managing the Asian kelp Undaria: final report. Cawthron Report no. 578, Available at: https://doi.org/10.13140/RG.2.1.5184.5608.Search in Google Scholar
Stuart, M.D. (2002). Translocation of Undaria pinnatifida by vessel fouling: analysis of the Department of Conservation vessel monitoring database, p. 55, May 1999–May 2001. MFish Project ZBS200104.Search in Google Scholar
Stuart, M.D. (2003). Review of research on Undaria pinnatifida in New Zealand and its potential impacts on the eastern coast of the South Island. DOC Sci. Intern. Ser. 166: 40.Search in Google Scholar
Stuart, M.D. and Brown, M.T. (1996). Phenology of Undaria pinnatifida (Harvey) Suringar in Otago Harbour, New Zealand, Available at: http://nzmss.rsnz.govt.nz/conf96/abstrs2s.html..Search in Google Scholar
Stuart, M.D., Hurd, C.L., and Brown, M.T. (1999). Effects of seasonal growth rate on morphological variation of Undaria pinnatifida (Alariaceae, Phaeophyceae). Proc. Int. Seaweed Symp. 16: 191–199, https://doi.org/10.1007/978-94-011-4449-0_22.Search in Google Scholar
Suto, S. (1950). Studies on shedding, swimming and fixing of the spores of seaweeds. Bull. Jpn. Soc. Sci. Fish. 16: 1–9, https://doi.org/10.2331/suisan.16.1.Search in Google Scholar
von Stosch, H.A. (1964). Wirkungen von Jod und Arsenit auf Meeresalgen in Kultur. Proc. Int. Seaweed Symp. 4: 142–150.Search in Google Scholar
Walker, D.I. and Kendrick, G.A. (1998). Threats to macroalgal diversity: marine habitat destruction and fragmentation, pollution and introduced species. Bot. Mar. 41: 105–112, https://doi.org/10.1515/botm.1998.41.1-6.105.Search in Google Scholar
Watanabe, Y., Nishihara, G.N., Tokunaga, S., and 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. J. Appl. Phycol. 26: 2405–2415, https://doi.org/10.1007/s10811-014-0264-z.Search in Google Scholar
White, N. (2003). Saccorhiza polyschides. Furbelows. Marine Life Information Network: Biology and Sensitivity Key Information Sub-programme [on-line]. Plymouth: Marine Biological Association of the UK.Search in Google Scholar
Yoshikawa, T., Takeuchi, I., and Furuya, K. (2001). Active erosion of Undaria pinnatifida Suringar (Laminariales, Phaeophyceae) mass-cultured in Otsuchi Bay in Northeastern Japan. J. Exp. Mar. Biol. Ecol. 266: 51–65, https://doi.org/10.1016/s0022-0981(01)00346-x.Search in Google Scholar
© 2021 Walter de Gruyter GmbH, Berlin/Boston
