Abstract
Invasions by non-indigenous species have the potential to alter the biodiversity of recipient systems. The magnitude of this effect often depends on the nature of the invaded communities and the ecology of the invader. We investigated the impacts of the Japanese seaweed Sargassum muticum (Phaeophyceae, Fucales) on biodiversity in a rocky and sedimentary environment on two islands in the North Sea. In each case, we compared the epibiota of non-indigenous S. muticum with epibiota communities on taxonomically related and structurally similar native seaweed hosts. Total and average species richness on S. muticum were similar on the rocky shore (60 species and 22±6 species, respectively) and the sandy shore (64 species and 20±3 species, respectively). However, community structure and species composition differed significantly between the environments. On the rocky shore, another native fucoid seaweed, Halidrys siliquosa, supported an epibiota community very similar to that of the invader. On the sandy shore, the only other abundant native habitat-providing algal species was Fucus vesiculosus. This species supported a different and less diverse assemblage of associated taxa. We conclude that S. muticum enhances epibiota diversity in the sedimentary environment, probably by increasing the substratum availability and habitat heterogeneity. In contrast, it has negligible impacts on epibiota diversity in the rocky shore environment, where it does not represent a fundamentally new habitat component. We conclude that even within the same region, the consequences of non-indigenous species on biodiversity cannot be generalised but depend on the composition and structural complexity of the species in the recipient community.
Similar content being viewed by others
References
Albrecht AS (1998) Soft bottom versus hard rock: community ecology of macroalgae on intertidal mussel beds in the Wadden Sea. J Exp Mar Biol Ecol 229:85–109
Albrecht A, Reise K (1994) Effects of Fucus vesiculosus covering intertidal mussel beds in the Wadden Sea. Helgol Meeresunters 48:243–256
Austen G (1994a) Hydrodynamics and particulate matter budget of Königshafen, southeastern North Sea. Helgol Meeresunters 48:183–200
Austen I (1994b) The surficial sediments of Königshafen; variations over the past 50 years. Helgol Meeresunters 48:163–171
Bayerl KA, Higelke B (1994) The development of northern Sylt during the last Holocene. Helgol Meeresunters 48:145–171
Bartsch I, Kuhlenkamp R (2000) The marine macroalgae of Helgoland (North Sea): an annotated list of records between 1845 and 1999. Helgol Mar Res 54:160–189
Bartsch I, Tittley I (2004) The rocky intertidal biotopes of Helgoland: present and past. Helgol Mar Res 58:289–302
Berman J, Harris L, Lambert W, Buttrick M, Dufresne M (1992) Recent invasions of the Gulf of Maine: three contrasting ecological histories. Cons Biol 6(3):435–441
Bertness MD (1984) Habitat and community modification by an introduced herbivorous snail. Ecology 65(5):370–381
Britton-Simmons KH (2004) Direct and indirect effects of the introduced alga Sargassum muticum on benthic, subtidal communities of Washington State, USA. Mar Ecol Prog Ser 277:61–78
Buschbaum C (2002) Siedlungsmuster und Wechselbeziehungen von Seepocken (Cirripedia) auf Muschelbänken (Mytilus edulis L.) im Wattenmeer. Ber Polarforsch Meeresforsch 408:1–143
Buschbaum C (2005) Pest oder Bereicherung? Der eingeschleppte japanische Beerentang Sargassum muticum an der deutschen Nordseeküste. Natur und Museum 135:216–221
Chapman AS (1999) From introduced species to invader: what determines variation in the success of Codium fragile ssp. tomentosoides (Chlorophyta) in the North Atlantic Ocean? Helgol Meeresunters 52:277–289
Chapman AS, Scheibling RE, Chapman ARO (2002) Species introductions and changes in marine vegetation of Atlantic Canada. In: Claudi R (eds) Alien invasive species: threat to Canadian biodiversity. Comissioned by Natural resources
Clarke KR, Warwick RH (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. PRIMER-E Ltd, Plymouth, UK
Critchley AT (1983) Sargassum muticum: a taxonomic history including world-wide and western pacific distributions. J Mar Biol Ass UK 63:617–625
Critchley AT, Nienhuis PH, Verschuure K (1987) Presence and development of populations of the introduced brown alga Sargassum muticum in the southwest Netherlands. Hydrobiologia 151/152:245–255
Crooks JA (1998) Habitat alteration and community-level effects of an exotic mussel, Musculista senhousia. Mar Ecol Prog Ser 162:137–152
Crooks JA (2002) Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers. Oikos 97:153–166
Crooks JA, Khim HS (1999) Architectural vs. biological effects of a habitat-altering, exotic mussel, Musculista senhousia. J Exp Mar Biol Ecol 240:53–75
Dame RF, Bushek D, Prins TC (2001) Benthic suspension feeders as determinants of ecosystem structure and function in shallow coastal waters. In: Reise K (ed) Ecological comparisons of sedimentary shores. Ecol Stud 151, Springer, Berlin Heidelberg New York, pp 11–38
Druehl L (1973) Marine transplantations. Science 170:12
Fletcher RL (1975) Studies on the recently introduced brown alga Sargassum muticum (Yendo) Fensholt I. Ecology and reproduction. Bot Mar 28:149–156
Fernández C (1999) Ecology of Sargassum muticum (Phaeophyta) on the North Coast of Spain: IV. Sequence of colonization on a shore. Bot Mar 42:553–562
Gätje C, Reise K (1998) Ökosystem Wattenmeer, Austausch-, Transport- und Stoffumwandlungsprozesse. Springer, Berlin Heidelberg, New York, p 584
Gee JM, Warwick RM (1993) Body-size distribution in a marine metazoan community and the fractal dimensions of macroalgae. J Exp Mar Biol Ecol 178:247–259
Gee JM, Warwick RM (1994) Metazoan community structure in relation to the fractal dimensions of marine macroalgae. Mar Ecol Prog Ser 103:141–150
Grosholz ED, Ruiz GM (1996) Predicting the impact of introduced marine species: lessons from the multiple invasions of the European green crab Carcinus maenas. Biol Conserv 78:59–66
Grosholz ED, Ruiz GM, Dean CA, Shirley KA, Maron JL, Connors PG (2000) The impacts of a non-indigenous marine predator in a Californian bay. Ecology 81(5):1206–1224
Hacker SD, Steneck RS (1990) Habitat architecture and the abundance and body-size dependent habitat selection of a phytal amphipod. Ecology 71:2269–2285
Hagmeier A (1930) Die Besiedlung des Felsstrandes und der Klippen von Helgoland. I. Der Lebensraum. Wiss. Meeresunters. (Abt Helgoland) 15(18a):1–35
Janke K (1986) Die Makrofauna und ihre Verteilung im Nordost-Felswatt von Helgoland. Helgol Meeresunters 40:1–55
Janke K (1990) Biological interactions and their role in community structure in the rocky intertidal of Helgoland (German Bight, North Sea). Helgol Meeresunters 44:219–263
Jephson NA, Gray WG (1977) Aspects of the ecology of Sargassum muticum (Yendo) Fensholt, in the Solent Region of the British Isles. I. The growth cycle and epiphytes. In: Biology of benthic organisms, proceedings of 11th European symposium on marine biology. Galway 1976, pp 367–375
Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386
Karlsson J, Loo LO (1999) On the distribution and the continuous expansion of the Japanese seaweed Sargassum muticum in Sweden. Bot Mar 42:285–294
Kraufvelin P, Salovius S (2004) Animal diversity in Baltic rocky shore macroalgae: can Cladophora glomerata compensate for lost Fucus vesiculosus? Estuar Coast Shelf Sci 61:369–378
Kornmann P, Sahling PH (1977) Meeresalgen von Helgoland. Helgol wiss Meeresunters 29:1–289
Kornmann P, Sahling PH (1994) Meeresalgen von Helgoland: Zweite Ergänzung. Helgol Meeresunters 48:365–406
Nienburg W (1925) Eine eigenartige Lebensgemeinschaft zwischen Fucus und Mytilus. Ber Dt Bot Ges 43:292–298
Nienburg W (1927) Zur Ökologie der Flora des Wattenmeeres. 1. Teil: Der Königshafen bei List auf Sylt. Wiss Meeresunters Kiel 20:146–196
Norton TA (1976) Why is Sargassum so invasive? Br Phycol J 11:197–198
Norton TA (1977a) The growth and development of Sargassum muticum (Yendo) Fensholt. J Exp Mar Biol Ecol 26:41–53
Norton TA (1977b) Ecological experiments with Sargassum muticum. J Mar Biol Ass UK 57:33–43
Norton TA, Benson MR (1983) Ecological interactions between the brown seaweed Sargassum muticum and its associated fauna. Mar Biol 75:169–177
Reichert K (2003) Die Makrofauna und ihre räumliche Verteilung und saisonale Veränderung im Felswatt von Helgoland. MSc Thesis, University of Hamburg, Germany
Reise K (1985) Tidal flat ecology. Springer Berlin Heidelberg New York, p 191
Reise K (1994) Changing life under the tides of the Wadden Sea during the 20th century. Ophelia Suppl 6:117–125
Rindi F, Guiry MD (2004) Composition and spatio temporal variability of the epiphytic macroalgal assemblage of Fucus vesiculosus Linnaeus at Clare Island, Mayo, western Ireland. J Exp Mar Biol Ecol 311:233–252
Ross DJ, Johnson CR, Hewitt CL, Ruiz GM (2004) Interaction and impacts of two introduced species on a soft-sediment marine assemblage in SE Tasmania. Mar Biol 144:747–756
Rueness J (1989) Sargassum muticum and other introduced Japanese macroalgae: biological pollution of European coasts. Mar Pollut Bull 20:173–176
Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O’Neil P, Parker IM, Thompson JN, Weller SG (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332
Schories D, Albrecht A, Lotze H (1997) Historical changes and inventory of macroalgae from Koenigshafen Bay in the northern Wadden Sea. Helgol Meeresunters 51(3):321–341
Schories D, Albrecht A (1996) Sargassum muticum—Der japanische Beerentang im deutschen Wattenmeer. Natur und Museum 125(3):92–98
Stæhr PA, Pedersen MF, Thomsen MS, Wernberg T, Krause-Jensen D (2000) Invasion of Sargassum muticum in Limfjorden (Denmark) and its possible impact on the indigenous macroalgal community. Mar Ecol Prog Ser 207:79–88
Steneck RS, Carlton JT (2001) Human alterations of marine communities. Students beware! In: Bertness MD, Gaines Sd, Hay ME (eds) Marine community ecology. Sinauer, Sunderland, pp 445–468
Taylor RB, Cole RG (1994) Mobile epifauna on subtidal brown seaweeds in northeastern New Zealand. Mar Ecol Prog Ser 115:271–282
Viejo RM (1999) Mobile epifauna inhabiting the invasive Sargassum muticum and two local seaweeds in northern Spain. Aquat Bot 64:131–149
Vitousek PM, D’Antonio CM, Loope LL, Westbrooks R (1996) Biological invasions as global environmental change. Am Sci 84:218–228
Wernberg T, Thomsen MS, Staehr PA, Pedersen (2000) Comparative phenology of Sargassum muticum and Halidrys siliquosa (Phaeophyceae: Fucales) in Limfjorden, Denmark. Bot Mar 43:31–39
Wernberg T, Thomsen MS, Staehr PA, Pedersen MF (2004) Epibiota communities of the introduced and indigenous macroalgal relatives Sargassum muticum and Halidrys siliquosa in Limfjorden (Denmark). Helgol Mar Res 58:154–161
Willan RC (1987) The mussel Musculista senhousia in Australasia; another aggressive alien highlights the need for quarantine at ports. Bull Mar Sci 41(2):475–489
Withers RG, Farnham WF, Lewey S, Jephson NA, Haythorn JM, Gray PWG (1975) The epibionts of Sargassum muticum in British Waters. Mar Biol 31:79–86
Wolff WJ, Reise K (2002) Oyster imports as a vector for the introduction of alien species into Northern and Western European Coastal Waters. In: Leppäkoski E, Gollasch S, Olenin S (eds) Invasive aquatic species of Europe. Distribution, impacts and management. Kluwer, Dordrecht, pp 193–205
Wurster P (1962) Geologisches Portrait Helgolands. Die Natur 70:135–150
Yendo K (1907) The fucaceae of Japan. J Coll Sci Imp Univ Tokyo 21(12):174
Acknowledgements
We thank Karsten Reise, Tony Chapman and three anonymous referees for their constructive criticism on earlier drafts of this manuscript. We also express our sincere appreciation to the research divers from Helgoland and Sylt for their logistical support.
This study was funded by a research grant from the Deutsche Forschungsgemeinschaft SA 931/1-2 (Bettina Saier).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by O. Kinne, Oldendorf/Luhe
This paper is dedicated to Udo Schilling, Chief Diving Officer, Alfred Wegener Institute who trained all of the authors in the waters off Helgoland to be scientific divers. The work reported here and in previous publications has been made possible through Udo’s training and support. We remain grateful for his enthusiasm, effort and patience.
Rights and permissions
About this article
Cite this article
Buschbaum, C., Chapman, A.S. & Saier, B. How an introduced seaweed can affect epibiota diversity in different coastal systems. Marine Biology 148, 743–754 (2006). https://doi.org/10.1007/s00227-005-0128-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-005-0128-9