Seaweed Invasions
Edited by Craig R. Johnson

Seaweed Invasions
A Synthesis of Ecological, Economic and Legal Imperatives
Reprinted from Botanica Marina Vol. 50 (2007) Double Issue 5/6

Edited by Craig R. Johnson

de Gruyter

Berlin · New York

Professor Craig R. Johnson School of Zoology and Tasmanian Aquaculture and Fisheries Institute University of Tasmania GPO Box 252-05 Hobart, Tasmania 7001 Australia E-mail: Cover images Front cover: Undaria pinnatifida on sea urchin barrens off the east coast of Tasmania, Australia. The photograph was taken in September 2000 at Lords Bluff within Mercury Passage. Courtesy of Dr. Hugh Pederson, Tasmanian Aquaculture and Fisheries Institute, University of Tasmania, Hobart, Australia. Back cover: Caulerpa taxifolia on a 3-m deep submarine cliff off the French Mediterranean coast. The photograph was taken in September 1991 at The Lavandou, Département Var. Courtesy of Professor Alexander Meinesz, Laboratoire Environnement Marin Littoral, Université de Nice-Sophia Antipolis, Nice, France. This work contains 18 figures and 13 tables. ISBN: 978-3-11-019534-7

Library of Congress Cataloging-in-Publication Data Seaweed invasions : a synthesis of ecological, economic, and legal imperatives / edited by Craig R. Johnson. p. cm. “Reprinted from Botanica marina, vol. 50 (2007), double issue 5/6.” Includes index. ISBN 978-3-11-019534-7 (pbk. : alk. paper) 1. Marine algae--Ecology. 2. Marine algae--Control. 3. Marine algae--Harvesting. 4. Invasive plants. I. Johnson, Craig R. (Craig Richard) QK570.2.S42 2007 363.7’8--dc22 2007044827 Bibliographic information published by the Deutsche Nationalbibliothek The Deutsche Nationalbibliothek lists this publication in the Deutsche Nationalbibliografie; detailed bibliographic data are available on the Internet at ∞ Printed on acid-free paper, which falls within the guidelines of the ANSI to ensure permanence and durability. © Copyright 2007 by Walter de Gruyter GmbH & Co. KG, 10785 Berlin All rights reserved, including those of translation into foreign languages. No part of this book may be reproduced or transmitted in any form or by any means, electronic or mechanic, including photocopy, recording, or any information storage retrieval system, without permission in writing from the publisher. Printed in Germany. Typesetting: Compuscript Ltd., Shannon, Ireland; Printing and binding: druckhaus köthen GmbH, Köthen, Germany; Cover design: Martin Zech, Bremen, Germany.


Seaweed invasions: introduction and scope Craig R. Johnson and Anthony R.O. Chapman

Methods for identifying and tracking seaweed invasions Alexandre Meinesz 1 Molecular approaches to the study of invasive seaweeds David Booth, Jim Provan and Christine A. Maggs Impacts of introduced seaweeds Britta Schaffelke and Chad L. Hewitt Control of invasive seaweeds Lars W.J. Anderson Invasive seaweeds: global and regional law and policy responses Meinhard Doelle, Moira L. McConnell and David L. VanderZwaag


65 77 98

Introductions of seaweeds: accidental transfer pathways and mechanisms Chad L. Hewitt, Marnie L. Campbell and Britta Schaffelke Intentional introductions of commercially harvested alien seaweeds Timothy D. Pickering, Posa Skelton and Reuben J. Sulu Mechanisms of invasion: establishment, spread and persistence of introduced seaweed populations Joseph P. Valentine, Regina H. Magierowski and Craig R. Johnson




Seaweed invasions: conclusions and future directions Craig R. Johnson Author information Subject index


131 139 141

Mechanisms of invasion: can the recipient community influence invasion rates? Piers K. Dunstan and Craig R. Johnson 41


including invasives. Bruno et al. and with ecological theory. appears to be increasing (e. there is good evidence to suggest that in some areas establishment of alien marine species originating from hull fouling exceeds that attributable to transport in ballast water (Hewitt et al. Didham et al. and have raised considerable angst about the ecological. Daskalov 2002. at any point in time. Levine and D’Antonio 1999.. Canada. Our intention here is to go beyond the case studies and the sui generis in search of patterns and commonalities.1515/BOT. Mack et al..5% of the total flora (Ribera and Boudouresque 1995) and . experiment and theory have contributed important advances in the understanding of invasions (e. Carlton 1999). Halifax.Johnson@utas. Fridley et al. B3H 4J1 1 * Corresponding author Background and motivation At no time in human history has the need to understand invasions of alien species – the process of invasion. by which seaweeds are introduced to new biogeographic domains.. MacDougall and Turkington 2005). Of course. Deep understanding also requires critical analysis of data and evidence.. Tasmania 7001. Because practical responses to seaweed invasions invariably take place within a regulatory framework. A deep understanding of the invasion process.* and Anthony R. and practical approaches to tracking and controlling seaweed invasions. DOI 10. A lack of integration of this kind and a focus on case studies and particular invasion events is arguably part of the reason for the historical disconnection between invasion ecology and mainstream ecological theory (Davis et al. and attempt to consider seaweed invasions in the context of a broader thinking about invasion ecology. and several species have been invasive (e. this special issue). large ecological or economic effects. as is the case in studying many other kinds of invasive marine species (Grosholz 2002). 2007).edu.g. investigation of the seaweed component has been dominated by case studies that are often strongly idiographic. 1999. Shiganova 1998. Nyberg and Wallentius 2005. This is particularly true for marine species. Carlton 1996. the rate of establishment of alien marine species. in some regions comprising . several thousand are being transported between biogeographic regions in ballast water alone (Carlton and Geller 1993. 2000). Dalhousie University.10–40% of the total alien species (Schaffelke et al. 2006).. Bax et al. Cohen and Carlton 1998. Chapman2 School of Zoology and Tasmanian Aquaculture and Fisheries Institute. Stachowicz and Tilman 2005. 2003). Ross et al. this review provides an opportunity to carefully examine available evidence of invasion processes and impacts for invasive seaweeds. The rate of anthropogenically-mediated translocation of species to regions outside native ranges has never been greater. Shea and Chesson 2002. However. This sounds self-evident. this work is also about identifying gaps. There has been little attempt to synthesise this body of work.g. or might have. 2004). 2005. Pimentel et al. Inevitably. Notwithstanding Davis’ (2006) harsh criticism that there has been little change in the questions and answers about invasion ecology in four decades. Seaweeds are a significant component of those marine organisms that have established as alien species in new bioregions. we suggest that recent syntheses working towards a confluence of survey. and. It is now both opportune and necessary to attempt to consider invasive seaweeds in this concourse. mechanisms of their invasion and impact. impacts and options to manage invasions can only come from integrating observation of natural systems across a variety of scales with results of controlled experiments. freshwater and terrestrial environments alike. We consider the means. Hobart. for they comprise the knowledge base on the species and communities invaded. Furthermore.037 Introduction Seaweed invasions: introduction and scope Craig R. and some marine bays realise a newly established species every 30–40 weeks (Hewitt 2003). 2003. a review of legal and policy responses is also included as a fundamental element of the interaction between society and invasive seaweeds. Not surprisingly. w1x . therefore. Nichols et al. 2001. the case studies must be included for reference. NS. Johnson1. While it is clear that some invasive marine species do have large impacts on the structure and dynamics of the systems in which they proliferate (e.g. 2005. 2000. Sala et al. 2000. putative claims of the impacts of alien invasive species are often unsupported by data or critical analysis (Gurevitch and Padilla 2004. Australia. but several authors have pointed out that. impacts of invasion and meaningful options to respond to invasion – been so urgent. GPO Box 252-05.O.2007.Botanica Marina 50 (2007): 321–325 2007 by Walter de Gruyter • Berlin • New York. either in the context of seaweed biology and ecology or more general invasion ecological theory. The overall aim of this collection is thus to synthesise current information about invasive seaweeds and human responses to them. see also Cadotte 2006).au 2 Department of Biology. focusing on high profile taxa that have. challenges and priorities for the future. Ruiz et al. University of Tasmania. for example. both accidental and intentional. and a recent review concludes there is little evidence that many alien invasive species cause the impacts and problems attributed to them (Bruno et al. among which it is estimated that. 2003). e-mail: Craig.g.g. These trends are evident in marine. 1990. Lodge 2001. 2005). economic and social consequences (e.

the first studies of invasive seaweeds concentrated on properties of the Modes of introduction In recognising that -3% of introductions of alien seaweed species are intentional. Valentine et al. may be evanescent. arguably. of the many taxa of the genus Codium off Japan.. were thought to explain patterns seen in nature (reviewed by Luning 1990). and perceptions that seaweed based industry offers an alternative and sustainable livelihood to coastal populations. cit. in particular. (op. Hewitt et al. 2006) but for only 17 have ecological impacts been considered at all and. there are several options for risk mitigation. (op. Notably. in line with suggestions two decades ago (e. Silva. Historically. it is useful to consider why some species become invasive while others do not. tomentosoides (van Goor) P. cit. Pickering et al. Indeed. Importantly however.) acknowledge. NGOs or intergovernmental organizations. (2007) corroborate this stance in concluding that there is no evidence of a common suite of traits of invasive seaweeds. facilitation) were recognised as major structuring agents of seaweed communities (Chapman 1986). driven by questions relevant to applied and theoretical ecology. Crawley 1987). transport mechanism for seaweeds. although the interface of some of these issues with ecological theory is considered where appropriate. seaweed ecologists sought explanations for species occurrences in physiological attributes. as Pickering et al.C.g. for example. species being considered for aquaculture should not be on watch lists of invasive species maintained by government agencies. ¨ although by the 1970s interactions among species (e. a problem that can only be dealt with by proper quarantine procedures. impacts realised in one area may not be good at predicting those in another (see also Grosholz 1996. establishment.O. Dunstan and Johnson (2007) in particular address the question of the properties of receiving communities in influencing invasion rates from a theoretical perspective. and these questions have framed the approach to this topic. Trowbridge 1998x. temperature and salinity. but also the most poorly managed. particularly in developing nations (Pickering et al. They include: • What are the major modes of introduction of invasive seaweeds? • Is there tangible pressure for ongoing intentional introductions? • What are sensible approaches to reducing risk of further introductions? • Is it possible to predict the ‘‘next pest’’ seaweed? • Are there common life-history or genetic traits of successful invaders? • Why do some species become invasive while others do not? • Are there common mechanisms underpinning seaweed invasions? • Why do some communities appear to be more susceptible to invasion than others? Do the traits of the recipient community influence invasion rates? • How have seaweed invasions been tracked. Moreover. Chapman: Seaweed invasions: introduction and scope Important questions that are not unique to seaweed invasions provide a structure for examining whether generalisations can be drawn from the case studies. For example. and rarely have these become particularly problematic wthe introduction of Undaria pinnatifida (Harvey) Suringar in Brittany may be a notable exceptionx. 260 or so alien seaweed species have been identified (Schaffelke et al. but we should be sanguine in establishing them as useful. For example. we recognise that this synthesis. Mechanisms of invasion and tracking invasions In addressing mechanisms of invasion (Dunstan and Johnson 2007. the extent of empirical knowledge of seaweed invasions is limited and highly skewed towards particular species. Clearly. Schaffelke and Hewitt 2007). This is driven by ongoing demand for seaweeds and their products. The approach to these questions by most of the authors is strongly empirical. and argue that this is best tackled based on assessment of risk at the three main stages of the invasion process (uptake and transport.) find that intentionally introduced seaweeds are no more or less risk prone than unintentionally introduced seaweeds. predation. spread) and not on particular properties of species. emerging techniques in genetics and genomics will provide a much deeper understanding of seaweed invasions? • How should humans respond to seaweed invasions? • Is the global regulatory framework in which responses to actual and potential seaweed invasions are determined adequate? We do not expect all of these questions to be answered with equal conviction.R. for only four is there a solid empirical and experimental basis (Schaffelke and Hewitt 2007). Valentine et al. competition. 2007). Species tolerances to light. Only a small number of seaweed species have been introduced intentionally. only one has become a worldwide pest wCodium fragile ssp. or figure prominently in scientific literature on invasive seaweeds. genetic and economic consequences of seaweed invasions? • Can we expect that existing and. there are only two published reports of quarantining seaweeds. Nonetheless it is overdue. Thus.g. (2007) focus w2x . Johnson and A.R. Another risk is that intentionally introduced specimens may harbour ‘‘hitchhikers’’.. But there is also pressure for further intentional introductions. They emphasise that while eliminating risk is rarely possible. they too consider a careful risk assessment essential when there are plans to introduce species for aquaculture purposes. Later in the issue.322 C. in part because of the dearth of meaningful empirical observations that contribute to the issue. 2007). Not surprisingly then. In the same way. if only to identify important areas of deficit in knowledge. They also address the challenge of identifying potential ‘‘next pests’’. on reviewing modes of accidental introductions and identify hull fouling as the most significant. and can existing approaches be improved? • Is it possible to predict the course of an invasion? • What are the ecological.

serratus L. In fact several species that are invasive elsewhere in the world are not pests in their native communities (Trowbridge 1998). In Tasmania. cit. interestingly. 2007). (op. disturbance patterns can account for observations that some patches are invaded by Undaria pinnatifida at high densities (Valentine and Johnson 2003. but they also emphasise the limited scope of extant work. Sophisticated genetic techniques can potentially be helpful in tracking invasions. with considerable success. which often manifest a dynamic mosaic of patches in space and time. including cryptic ones (Booth et al. However. whereas it forms meadows that can replace kelp forests in the western Atlantic Ocean (Chapman et al. Agardh was introduced to the Oslofjord but it migrated south into the Baltic Sea where it hybridised with F. in identifying the initial source(s) of invasions. (op. Indeed. for example.000 brochures across eight Mediterranean countries. and these positive results have underscored the importance of public education programs and community involvement in initial detection. for example.). so they escape early detection. sometimes with disastrous consequences as occurred with the introduction of Undaria pinnatifida in Brittany (Meinesz 2007). However. which Booth et al. Agardh in Tunisia was reported by a fisherman responding to a public awareness campaign that distributed 300. The work that has been done reveals the complexity of underlying colonisation patterns and genetic impacts.) work is largely theoretical. Means of tracking seaweed invasions have. in part because most of the other successful invasive seaweeds have experienced genetic bottlenecks and manifest greatly reduced genetic variation. Along with the rather limited information on ecological impacts. They catalogue a variety of impacts. Fucus evanescens C. Clearly. the highly invasive strain of Caulerpa taxifolia consists of male thalli that reproduce vegetatively. Indeed. Schaffelke et al. 2002). applied science studies have received government funding. Valentine et al. Australia. 2004) while others nearby are not. 2007). Although hybridisation involving invasive seaweeds is likely to be rare. This subspecies is quite rare in subtidal waters of the eastern North Atlantic Ocean. it seems that its vigour as an invader cannot be related to its genetic diversity. These observations suggest that properties of the invaded community also determine the success of the invader. With the exception of studies in Tasmania (on Undaria pinnatifida).R. as outlined earlier. eradication is not likely to be successful and management measures may need to be w3x . Cartographical data from an informed public. However. there is only a single unequivocal example of hybridisation involving an invasive seaweed. Nova Scotia (on Codium fragile ssp. and as few as four invasive species in any detail. has allowed tracking of the invasion pathways of two Caulerpa species. In one example. who suggest that this kind of variability can be explained by patterns of differential resource availability. but have largely been employed. been notable for the simplicity of the technologies employed. which covers remark- Human responses to seaweed invasions Unfortunately. with most genetic investigations focusing on identifying source populations (Booth et al. for example. in many cases. with the possible exception of some kinds of remote sensing (Meinesz 2007). (2007) and Dunstan and Johnson (2007). Dunstan and Johnson’s (op. there have been few comprehensive experimental works on seaweed invasion ecology. even the relatively limited amount of work to date shows that a given species might have very different impacts in different locales. have properties likely to show stronger responses to resource variability than to species richness or diversity of the recipient community per se. molecular analyses revealed considerable genetic diversity within invader populations of Undaria pinnatifida. Exotic species have been tracked along the coasts of several countries. op. cit. probably reflecting multiple introductions from different sources. (2007) show that life history characteristics are of little value in predicting invasion. This species is a vigorous invader. ably few of the total number of known alien seaweed species. New Zealand. Argentina and the northeastern Pacific Ocean. In these cases.R. about 97% of seaweed incursions are accidental (Hewitt et al. Chapman: Seaweed invasions: introduction and scope 323 invaders in predicting consequences of introduction at new sites. cit.C. Vahl) C. Consequences of invasions Schaffelke and Hewitt (2007) review the ecological impacts of seaweeds on recipient communities. This topic is explored by both Valentine et al. the hybrids occur in a restricted hybrid zone on the shore. tomentosoides) and Tuscany (on two invasive Caulerpa species co-existing with two introduced red turfing algae from Australia).. disturbances to native assemblages free resources and pave the way for alien species to establish at high densities. Codium fragile ssp. tomentosoides does not reach nuisance proportions in all of the communities in which it has been introduced. storms or other invasive species. on the whole. invasive virulence does not depend on genetic diversification. but with subsequent invasion of the northeastern Atlantic Ocean.) categorise broadly as changes in population genetic structure and changes in genomic structure. the first occurrence of Caulerpa taxifolia (M. There are even fewer studies of genetic consequences of invasive seaweeds. first found outside its native Japanese range in the Mediterranean Sea in 1971 (Meinesz 2007). Nevertheless. 2007). with the prospect of revealing adaptive traits and genotypephenotype-environment interactions (Booth et al. Johnson and A. through hybridisation. Invasion patterns are also highly variable at much larger spatial scales.O. At a genomic level. along with expert sampling. but they argue that seaweed communities. the future for genomic-level research is nonetheless a bright one. cit.) point out that there is surprisingly little known of economic impacts of seaweed invasions. resulting in considerable research effort. Rather they show that. These facilitative disturbances may be grazers. in the Mediterranean Sea. In most cases the mechanisms of observed ecological effects are unknown (Schaffelke et al. 2007) and usually occur in regions not subject to monitoring.

pp. Davis.P. the International Convention on Wetlands. Oceanography 9: 36–43. Reproduction. the Convention on Biodiversity. 15–33.W. K. Ultimately it is governments that determine responses to invasive species. Mar. Nonetheless. 2005. A. Elton and the dissociation of invasion ecology from the rest of ecology. as occurred in response to invasion of the California coast by Caulerpa taxifolia and Ascophyllum nodosum (L. J. Gonzalez and W. Cadotte. 1996. responses to invasive aliens. 2001. but it is necessary. the few eradication programs that aimed to completely extirpate an invader population have been highly successful. control of seaweed or any other invasions should be a component of an integrated multi-faceted approach dealing with all problems in the marine enviw4x ronment including. Accelerating invasion rate in a highly invaded estuary. Springer. M. J. 1986. pp.J. pp. Exp. eds) Colonization. K. J.J. Charles S.J. Bromberg and M. Control of invasive seaweeds.F. 1987. to stop things getting worse. Bax. Adv.J. 255: 259–270. M. Grime. Ecol. In: (R.M. Divers. Claudi.. Chapman 1984. Carlton. Overfishing drives a trophic cascade in the Black Sea. 1993. and because they are expensive. marine debris and habitat modification. immediate. op. Carlton. Geller. succession and stability. Dordrecht. Carlton. Springer. J. Mar. J.. 13–40. Doelle et al.O. 7: 97–102. ed. 1998. M. Blackwell Scientific. at least. Importantly. Mar.T.R. Long-term changes in fish abundance and environmental indices in the Black Sea. Daskalov. 2003. Geeves. References Anderson. 50: 385–396. Bot.D.E. coordinated and massive action using highly developed methodologies is usually necessary. In contrast. 2002. R. eds) Invasive species and biodiversity management. Cadotte. Booth. 2006. none of the international conventions is self-implementing. ˚ P. D. Ecological roulette: the global transport of nonindigenous marine organisms. This legislation has developed from both global and regional policies including the Law of Sea. use and handling of alien species and. J. 2002. Aguero. even those issued by a close-knit political alliance like the European Union.J. 35–64. Distrib. Daskalov. (op. Sunderland. in general.) Le Jolis (Anderson 2007).. eds) Conceptual ecology and invasion biology: reciprocal approaches to nature. pp. and the Convention on Migratory Species of Wild Animals (Doelle et al. Thompson and J. In: (O. Prog. 195–212. Switzerland and Germany have legislation controlling introductions for aquaculture. Ser. 2007). but there is yet a great deal to do. Science 279: 555–558. Carlton. and there are guidelines for handling waste water and sediment in ships. 1999. 2007. and J.W. Bertness. 78: 99–109.W. A. A. J. Mar. Marine bioinvasions: the alteration of marine ecosystems by nonindigenous species. In: (M. Bruno. Chapman. Insights into biotic interactions from studies of species invasions. Sax.R. eradication in concert with early detection emerges as a cost effective response (Anderson op. Johnson and A.R. Sinauer Associates.. M.D. Ser. A. the development of effective legal and policy responses to invasive seaweeds is fragmented at both regional and global levels. These policies have led to global initiatives such as the development of a Code of Conduct for Responsible Fisheries by the Food and Agriculture Organization. In: (D. M. Canada.W. Population and community ecology of seaweeds.D. The scale and ecological consequences of biological invasions in the world’s oceans.J. Dordrecht. not scientists or environmental agencies. In: (M. The International Maritime Organisation recognises ships’ ballast water as a major vector for invasives. cit. Species invasions and changes in marine vegetation of Atlantic Canada. McMahon and T. in part because of the massive reproductive potential of many seaweeds (e. A. Provan and C. 429–453.R.R. and so national legislation and enforcement are required. Biol.D. Scheibling and A. pp. 2006. Ottawa.O. Davis. overfishing. Darwin to Elton: early ecology and the problem of invasive species.T. L.F. only Australia.. Chapman: Seaweed invasions: introduction and scope invoked. Williamson. Success stories like this are rare because of long latency periods during which detection can be difficult. Cadotte. eds) Species invasions: insights into ecology. Gray. and B. Mar. McMahon and T. recruitment and mortality in two species of Laminaria in southwest Nova Scotia. Chapman. 50: 418–437. fouling of ship hulls is a much more important vector for seaweeds than ballast. but coordination among governments at a global scale is poor. Sandlund. Crawley and P. USA. for example. 133–148. and changes in the composition of anti-fouling substances on ships’ hulls (mandated by the International Convention on Control of Harmful Anti-Fouling systems on Ships) will promote increased fouling by seaweeds as the use of toxic compounds in antifoulants such as tributyltin (TBT) are phased out. Viken. However. G.T. Policy 27: 313–323. Stachowicz and S. Mar. S. What makes a community invasible? In: (A. Biol. Bot. efforts to manage invasive seaweed populations have not been very successful (Anderson 2007).O. Natural Resources Canada. Schaffelke et al. Mar. pp. Dordrecht. Ecol.) point out that there are a raft of powerful regulatory tools available to employ. 2005) and their capacity for relatively long distance dispersal (Reed et al.). evolution and biogeography. In the end. Molecular approaches to the study of invasive seaweeds.T. Oxford.A. cit. 1988.J. Ecol. Australia and New Zealand have taken this more seriously than other nation states but. Cohen. . S. N. Schei and A. cit. 225: 53–63. Kluwer Academic Publishers. Fukami. Fridley.O. New Zealand.) Alien invasive species: threats to Canadian biodiversity. Marine invasive alien species: a threat to global biodiversity. climate change.M. Gaines. and at an early stage of development (Doelle et al. Prog.M. Invasion biology 1958–2005: the pursuit of science and conservation. 2007. and even the sampling design to detect every single invading individual usually requires research development effort.M. It will not be possible to turn the clock back 500 years to the more pristine conditions that once existed. Chapman. 2003. G.g. M.J. E. Edwards.324 C. However. J. 23: 1–161. 1984. Chapman. Fukami.T. Maggs..). For example.N. Kinlan and Gaines 2003). Even when an invasion is discovered early. Science 261: 79–82. eds) Conceptual ecology and invasion biology: reciprocal approaches to nature. Crawley.S. in some cases.A. No consideration of human responses to invasive species would be complete without consideration of the regulatory environment that defines limits to movement.A.

Intentional introductions of commercially harvested alien seaweeds. J. A. Wonham and A. biogeography ¨ and ecophysiology. and C. 2006. Hewitt.E. Bot. M. Johnson and C. B. and C. R. 2003. 2007.F. Schaffelke. Laur and A. Luning.D. 1988. T. Biol. T. Remarkable invasion of San Francisco Bay (California. W. Nyberg. Schaffelke. Hines. Invasions 5: 3–21. R.D. Syst. Biol. Chapin. J. 2007.H. and C.W. Science 287: 1770–1774. 1995.L. In: (D. Invasion of the Black Sea by the ctenophore Mnemiopsis leidyi and recent changes in pelagic community structure. Ecology 88: 3–17. Trends Ecol. 2007. Johnson.H. Freshw.E.J. Simberloff. 2007. 50: 361–372. Rev. E. 11: 187–268. and control. Bioscience 50: 53–65. Can species traits be used to predict marine macroalgal introductions? Biol. Mechanisms of invasion: establishment. Ruiz. et al. R..J. Trends Ecol. Grosholz. B. Shiganova. 1996.J. 1998. Hewitt. Oceanogr. Monogr.O. Bot. Mar. P. Skelton and R. Mar. spread and persistence of introduced seaweed populations. 2002. R. Carlton. 50: 397–417. 50: 338–350.R. B. D. 2007. Hewitt. D. Lach. Ribera. Fish. 18: 529–541.. Victoria. 2000. Huber-Sannwald. D. New York. O.F. Appl. Valentine.J.S.D. Environmental and economic costs of nonindigenous species in the United States. Invasive seaweeds: global and regional law and policy responses.K.P.. Ross.A. 2005. Phycologia 44: 84–94. Bot. 1990.D. In: (F. F. Evol. 2007.E. Stachowicz and S.. M. Tilman.E. 31: 481–531. Chesson. Hutchinson. Hewitt. Laminariales) in Tasmania.. 1999. 2004. J. Gaines. Assessing the ecological impacts of an introduced seastar: the importance of multiple methods. 2003.E. Are invasive species the drivers of ecological change? Trends Ecol. Doelle. Wallentius. 2005. C. J. Boudouresque. Sala.H. 2004. McConnell and D. Von Holle. community saturation. Padilla. Morrison. Pickering. J. H. New York.R. Ecol. Mar. USA) by the Asian clam Potamocorbula amurensis. D’Antonio. and C. 2005. J.P.P. Hewitt. 2000.W. D.R.M. Stachowicz. L. with special reference to macroalgae: mechanisms and impact. Grosholz. 295: 63–90. J. 55: 223–230. 527. 41–64. Propagule dispersal in marine and terrestrial environments: a community perspective. Kinlan. Lodge. D.M. Appl. and C. Magierowski and C. Thompson and L. Evol. K. 1999. Res. C. Lakes. Mar. J. Invasions of coastal marine communities in North America: apparent patterns. eds) Species invasions: insights into ecology.L. Bot. Introduced and cryptogenic species in Port Phillip Bay. 1998. epidemiology. J. D. 50: 326–337. Seabloom. S. 144: 183–202. Mar.K. 50: 351– 360. Ocean Yearbook 17: 193–212. J. processes and biases. Ecology of the green macroalga Codium fragile (Suringar) Hariot 1889: invasive and non-invasive subspecies. J. Zuniga and D. S. Evans. Martin. Their enivironment.L.R. Gurevitch. Establishment of the introduced kelp Undaria pinnatifida in Tasmania depends on disturbance to native algal assemblages.A. Prog.. Invasions 7: 265–279. B. C. Mar. Johnson and A. Bot. Ecological and evolutionary consequences of coastal invasions. Mar. Campbell and B. VanderZwaag.J. R. Marine biosecurity issues in the world oceans: global activities and Australian directions. J. P. pp. Mar. Smith. 2001. Boyd. Meinesz. Phycol.J. and P. Reed. II.. Biotic invasions: causes. Establishment of the introduced kelp Undaria pinnatifida following dieback of the native macroalga Phyllospora comosa in Tasmania. Fridley. Armesto. Turkington. Reproductive phenology of the introduced kelp Undaria pinnatifida (Phaeophyceae. M.J. Johnson.-F. 19: 470–474. Mar.R. Are invasive species the drivers or passengers of change in degraded ecosystems? Ecology 86: 42–55. 277–312. 50: 438–450. Sala and E. Bloomfield.P. E. P. Schaffelke. Prog. Mack. Ecol. 7: 305–310. Pimentel. pp. Hewitt. Oceanogr. Ecol. Campbell and C.N. Species invasions and the relationships between species diversity. D.M. Oikos 87: 15–26. B. R. and C. Springer-Verlag. C.R. Berlow. MacDougall. Chapman: Seaweed invasions: introduction and scope 325 Didham. Lonsdale. Thresher. Tilman and B. Mechanisms of invasion: can the recipient community influence invasion rates? Bot. 58: 321–335.A. J.. Gemmel. Ecol.L. Johnson. 17: 170–176. Introductions of seaweeds: accidental transfer pathways and mechanisms. Ser. Campbell. Ecology 77: 1680–1686. M.. 10: 689–710. Sinauer Associates. Australia. Biol. Sax. Phycol. Nichols.L. 2002.S. eds) Future scenarios of global biodiversity. Ebeling. Mar. Clout and F.D. Evol.F. Stachowicz.D. 2005. Biol.K. J. Introduced macroalgae – a growing concern.L. Seaweeds. Ecol. Levine.M. T. E. D. Ann. Annu. Sulu.D.. M. Exp. Ecology 84: 2007–2020. Schemel. The invasion paradox: reconciling pattern and process in species invasions. 2005. Are invasive species a major cause of extinctions? Trends Ecol. 2007. and S.J.L. 2000. Trowbridge. and ecosystem functioning. E. Bot. Fofonoff. 36: 1–65.J. M. O. Australia. Chapin III. Ewers and N. Impacts of introduced seaweeds. Gaines.. M. Mar. Contrasting rates of spread for introduced species in terrestrial and marine systems. 20: 470–474. global consequences. Smith and C. Biodiversity scenarios for the year 2100. 17: 22–27. Sax.E. and R. Evol. Variation in algal dispersal and recruitment: the importance of episodic events. Displacement of a former community. M.D. Cohen. Elton revisited: a review of evidence linking diversity and invasibility.M.. Hewitt.M.R.S.L. Dunstan. F. Dirzo. Valentine. 2004.. R. A. Shea. w5x . Wiley. and D. M.A.L. Naeem. Valentine. G. Bazzaz. 2003.. 1990.C. Australia. Res. Introduced marine plants. pp. and D. Mar. M.. Rev. 2003. K. 66: 95–101. Johnson. Methods for identifying and tracking seaweed invasions.K.C.B. Schaffelke. evolution and biogeography. 2007. et al.T.L. C. Sunderland. J. J. C. Community ecology theory as a framework for biological invasions.R.L. J.. R. Tylianakis. Stohlgren. 50: 373–384.L. and I.

aquarium or live seafood trade) or accidental introductions (mainly as hull-fouling). We can now say with certainty that no region of the world’s oceans has remained free of alien (non-indigenous) marine species (e. 2000. 16 out of 19 orders in the Rhodophyta.g.a 1 National Centre for Marine and Coastal Conservation.g. Hewitt et al. Hewitt 2002. However. w6x . see Figure 1). QLD 4810. Williamson 1996. Ruiz et al. Our current ability to identify which species are likely to invade next is limited. the most significant and poorly managed transport mechanism for macroalgae. Townsville. While this issue was recognised by early workers (Ostenfeld 1908. Similarly.g. 1998. Smith. Castilla et al. 2001. 2007). a Carlton 1985. Schaffelke et al. Ribera and Boudouresque 1995. specifically for the prediction of the most likely ‘‘next pests’’ (but see Chapman 1999. an examination of the synergies between species’ functional traits. transported and released into a new environment..038 Review Introductions of seaweeds: accidental transfer pathways and mechanisms Chad L.L. transport constraints. either as regional assessments of marine invasions (e. and. Lewis et al. or as assessments of vectors associated with introduced macroalgae (e. and eight out of 12 orders in the Phaeophyceae (Schaffelke et al. PMB 10. Currently operating transport mechanisms for marine macroalgae are either associations with intentional introductions (translocations for aquaculture.2007. Rosebud. A number of potential management options exist. We will i) identify and discuss the constraints posed by individual transport vectors to the successful transport and inoculation of macroalgae. Lubchenco et al.. 2006). Current address: Australian Institute of Marine Science. McEnnulty et al. 2000.. but also represent significant economic and environmental risks for which we have limited post-incursion control and management options (e. Australia * Corresponding author Abstract Macroalgae are a significant component of historic and modern invasions. Schaffelke and C. 1996. Oresanz et al. with association to a wide variety of transport mechanisms. specifically on case histories that have provided indepth evaluations of the invasion process. Hewitt1. Victoria 3939.. Wyatt et al.*. vectors. Ruiz et al.g. 2002. Anderson 2007. Between 163 (Ribera Siguan 2002) and 260 (J. Keywords: aquaculture. packing material. Dunstan and Johnson 2007). hull fouling. 2005). with representatives from seven out of nine orders in the Chlorophyta. 1999. Ribera Siguan 2002.Botanica Marina 50 (2007): 326–337 2007 by Walter de Gruyter • Berlin • New York. Several authors have reviewed the current status of macroalgal introductions. 2006). Despite significant efforts. Introduction The global transfer of marine species by human-mediated means both within and between non-contiguous biotic provinces is of significant concern for biodiversity conservation and the sustainable development of coastal and oceanic resources (e.. 2006). Cranfield et al.hewitt@ncmcc. J. numerous intentional introductions have occurred for aquaculture purposes. DOI 10. Schaffelke and Hewitt 2007). unpublished data) macroalgal species are recognised introductions. 1991. 2004. ballast water. Campbell1 and Britta Schaffelke2. 2005).. Schaffelke et al. PO Box 772. 2002. This review paper draws heavily on previous work. Castilla et al. Australia. Leppakoski et al. QLD 4810. Leppakoski et al. The scope of this review paper is restricted to accidental introductions of macroalgae. Coles et al. Hewitt et al. significant progress on identifying patterns and processes has been made only in recent decades (e. 2002. PMB 3. These transport mechanisms pose specific constraints on the ways by which species can be taken up. Ribera and Boudouresque 1995. e-mail: c.g. risk management. Townsville. risk mitigation. ii) discuss the life history characteristics of successfully introduced macroalgae in relation to the current transport mechanisms. 2005. Cohen et al. Oresanz et al. and recipient community attributes will likely provide possible options in the 2 CRC Reef Research. Of these. 2002. Lewis 1999. Lewis 1999. including the development of international instruments and regional agreements. Hewitt et al. Coles and Eldredge 2002. Carlton 1979. 2004. Nyberg and Wallentinus 2005. Hayes and Sliwa 2003. 2004. alien marine species from all major animal. Ribera and Boudouresque 1995. Of these. 2003. Marnie L. is of urgent need. 1998. Australian Maritime College. Verlaque 2001. plant and algal phyla have been detected. ¨ 2003. 1999.g. Ribera Siguan 2002.. Hewitt. Elton 1958). iii) review relevant biosecurity (biological security) mitigation measures at both national and global scales.g. The development of treatment options for hull fouling. Australia. our understanding of the processes determining invasion success remains limited. -3% of macroalgal introductions have been intentional releases. introduced macroalgae. Wallentinus 1999.1515/BOT. ¨ 2002. Carlton 2001. Castilla et al. macroalgae not only represent a large component of the globally introduced biota (e. Ruiz and Carlton 2003). 2005. Thresher 1999. which are covered elsewhere in this issue (Pickering et al.

examining the range of potential transport mechanisms will prove useful in detecting common patterns.. nestling. di Castri 1989.g. influencing a species’ ability to successfully enter and survive the invasion process (Table 1). Campbell and Hewitt 1999.. fouling. but lacked light.. teredinid bivalves) creating deep ‘‘galleries’’ in the hulls of vessels (Carlton 1985). 1996.g. w7x . 2000. some linkages or transport corridors between donor and recipient regions have ceased to exist. while others have become more apparent (e. Miller et al. unpublished data). dry and semi-dry ballast. di Castri 1989). and motile species could have been found. Hewitt et al. and scientific research. Hull boring During the age of sail. 2004). While it is virtually impossible to establish with a high level of confidence the link between an introduction and the mechanism of transport. Elton 1958. Smith. Ribera and Boudouresque 1995. frozen and dried food products and the aquarium trade (e. These areas of the ship hull were completely subtidal and exposed to ambient seawater conditions of temperature and salinity. ballast water) (see Figure 2).g. Transport mechanisms in the marine environment are largely associated with commerce and exploration. Each of these transport mechanisms has a unique set of constraints that act as selection criteria. data from J. 1995). Hewitt et al. Carlton 1989. unpublished data).. were protected from wave action and the influence of vessel speed (Table 1). Crosby 1986. These galleries created protected habitats in which encrusting. organisms could bore into wood (e. The modern era of European expansion (post 1500 AD) has resulted in the massive transport and inoculation of species between non-contiguous biotic provinces (Crosby 1986. These vectors of transport typically result in the unidirectional movements of species over long periods..g. data from J.g.C. 2005).: Accidental introduction pathways of seaweeds 327 Figure 1 Number of recorded accidentally introduced taxa of macroalgae for each IUCN bioregion (see Figure 3. steel-hulled vessel fouling and the transport of planktonic organisms and fragments in ballast water. Similarly. Copper cladding or sheeting was frequently used to prevent the settlement Figure 2 Number of introduced macroalgal species attributed to specific vectors. Ribera Siguan 2002. Several transport mechanisms have ceased to exist as significant vectors (e. these movements are likely to have been spatially restricted and of relatively low frequency. the transfer of live. 1989. wooden hull boring.L. the intentional transfers of mariculture organisms (specifically oyster introductions) including the unintentional movement of associated organisms (e. Hewitt et al. inoculating new individuals or propagules for multiple generations (e. However.. Transport mechanisms Humans have undoubtedly transported species intentionally and accidentally for several thousand years (di Castri 1989). 1996. Many of these vectors have not been limited to single species movements but have often resulted in entire assemblages or communities of tens to hundreds of species being transported between disparate bioregions.g. Carlton and Geller 1993. with new linkages developing between bioregions as new trade routes became established (Carlton 1985. 2004). Ruiz et al.. accidental mariculture introductions). These include: woodenhulled vessel boring. Weigle et al.g. Kelleher et al. 2004). Ribera and Boudouresque 1995). the use of biological material for packing (e. dry and semi-dry ballast. Smith. Note – some species are represented in multiple vectors.

1995. 1991. plethysmothalli of Punctaria species (Phaeophyta). Lewis et al. copper. They are also exposed to wave action and shear forces as a result of vessel speed. organotins).: Accidental introduction pathways of seaweeds Table 1 Specific constraints associated with identified transport mechanisms. In one of the few modern studies of wooden hull fouling. Carlton 1996). Hull fouling can occur either through recruitment onto the hull from planktonic (albeit short-lived) life history stages. During a journey. exposure to changing temperature and salinity regimes depending on the voyage) control the successful transport of species by this vector (Table 1). We have little indication as to which organisms were transported by hull boring. Hay and Dodgshun 1997. and. no macroalgae were recorded. Carlton and Hodder (1995) observed the inadvertent collection and transport of crevicolous (species found in crevices or narrow spaces) species when the replica vessel Golden Hinde II settled into the mud of Humboldt Bay. dark nature of the galleries.. . particularly in artisanal fisheries and developing countries. water intakes such as sea-chests and internal piping etc.) of vessels. with the exception of shipworms (teredinid bivalves) and limnoriid isopods (Turner 1966). 2004 for successful hull-cleaning by heat treatment). Undaria pinnatifida (Harvey) Suringar (Phaeophyta) sporophytes )1 m have been observed attached to vessels. Carlton and Hodder 1995. Copper is toxic to marine invertebrates. Transport mechanism Uptake Transport Desiccation Darkness Crushing Exposure to and changing physical environment stress ● ● ● ● ● ● ● ● ● ● ● ● ● ● Exposure Planktonic Association Shear (settlement/ phase with target stress uptake) period species or habitat Hull boring ● Hull fouling ● Dry and semi-dry ballast Water ballast Ballast tank sediments Aquaculture/mariculture Aquarium and live seafood trade Bait and packing material Scientific research Maritime equipment ● ● ● ● ● ● ● ● ● ● ● ● of boring and fouling organisms. of these. Diannelidis and Delivopoulos 1997) and continues to be used as an active compound in many antifouling paints. Several macroalgae are common members of fouling communities (Fletcher 1980). with the development of anti-fouling paints and increased vessel speeds (Ribera and Boudouresque 1995. Gnassia-Barelli et al. subsequently. Coutts 1999.g. Coutts (1999) detected Phloiocaulon species (Phaeophyta) and microscopic life history stages of macroalgae. The constraints of the transport process (vessel speed. 2006). Virtually all macroalgae are capable of fouling hulls (Schaffelke et al. deep water or shaded pools in shallow coastal waters) of Australia and South Africa (Coutts 1999). Hull fouling Fouling organisms include both plants and animals that attach to the hulls (including the rudder. which are typically found in non-port habitats (i. Of significant interest was the detection of Phloiocaulon species. these species are exposed to variations in ambient sea temperature and salinity. timber hulls are still common in recreational vessels and regional trading and fishing vessels. Hewitt et al. While some potential for hull boring continues to exist.g. however. hull boring has virtually ceased to exist as a transport mechanism for merchant vessels. 31 were red algae. and its gametophytes have survived hull cleaning by scraping (Hay 1990. Larger macroalgae can also be transported during the microscopic phase of their life history (see Peters and Breeman 1992). this mechanism will not be considered further in this evaluation. indicate that this vector remains an active and significant mechanism of transport for a variety of species including w8x macroalgae (e. 2004. Ribera Siguan (2003) reported that of 189 taxa of alien marine algae and angiosperms reported worldwide. Womersley 1990. Lewis 1982. Recent studies.e.. However. However. but see Wotton et al. 2004). 1999. several large species have been collected from hulls. aluminium. having survived extensive sea voyages (Hay 1990). Australia). 2003. fish and algae (Anderson et al.. Hewitt et al. Since the advent of effective anti-fouling paints and the replacement of wooden hulls with steel. 39 were attributed to hull fouling as a likely vector of introduction and.L. Hewitt and Campbell 2001.328 C. 2004). the use of anti-fouling compounds has created hardselection pressures for species and ecotypes that demonstrate resistance to the active substances (e. While the majority of macroalgae associated with hull fouling are small or have crustose or filamentous growth forms. and fibreglass. attached to hulls of international commercial merchant vessels visiting the port of Launceston (Tasmania. propeller. Additionally. it is highly unlikely that this mechanism would have provided significant opportunities to macroalgae given the protected. However. this vector was believed to have been significantly reduced for merchant vessels by the use of copper cladding. Historically. direct attachment from adjacent surfaces or as attached drift (see Lewis et al.

The accidentally transported species growing attached to. However. Aquaculture associates Several authors have suggested that this transport mechanism. 2005) including Saccharina japonica (J. Mayes. However. the crushing shear stresses of the ballast pump. cobble. (1988) found over 69 taxa in five animal phyla wArthropoda. Lavoie et al. and Grateloupia.. is a significant commercial industry with well-prescribed quarantine practices. Wallentinus 2002) but see also the discussion of Lewis (1999) for Gymnogrongus crenulatus (Turner) J. Ribera and Boudouresque 1995) and include the availability of planktonic (including tychoplanktonic) material at the time of uptake. Only species present in these habitats were available to this transport mechanism.and tycho-planktonic organisms. Neushul et al. particularly their microscopic stages. This vector will not be considered further in this evaluation. Braun (Luther 1979. as well as demersal species (e. boring in. The ability to survive transport would be related to the similarity in physiological tolerances between the target species and the associated species (Table 1). and planktonic habitats. or associated with the transported substrata. 2003). These sediments can contain benthic organisms including the resting stages of toxic dinoflagellate species and benthic diatoms (e. these are likely to be ameliorated due to the strong commercial incentive to keep the target species alive during transport. 1990). Little is known about which species were transported by this vector. Mediterranean Sea) resulted in at least nine macroalgal introductions (Verlaque 2001. Areschoug) C. Discharge of species was accomplished during the discharge of the ballast itself by shovelling material out of the holds.E. 1996. This transport mechanism will not be considered further in this evaluation. Carlton and Geller 1993. may experience some transport constraints. providing a mechanism for holo-. Williams et al. and physical abrasion and/or crushing (Table 1). Gollasch et al. Carlton and Geller 1993. and Platyhelminthesx while Carlton and Geller (1993) reported 367 taxa. Hewitt et al.C. C. 2007). Undaria pinnatifida. ballast tanks and seachests can have an established and reproductive resident benthic fauna (Coutts et al. However. Critchley et al.g. This may well be the most generic vector of species transport. This transport vector imposed several constraints on macroalgal transport including desiccation. Verlaque et al. numerous studies have detected thousands of taxa within the ballast tank environment (see Carlton and Geller 1993. 2002). gigas into the Thau Lagoon (France. either for small-scale hobbyists or for large-scale commercial aquaria. Aquarium trade The aquarium trade.E. Lane.g. Cnidaria. the cosmopolitan nature of many beach and shore fauna may be attributable to the large quantities of shoreline transported around the world via this vector.L. no macroalgal species have been identified from ballast tank or sea-chest sediments. 1999). While this mechanism is active for microalgal species. Wallentinus 2002. Druehl et G. darkness. often with multiple releases through time to ensure establishment (see Pickering et al.: Accidental introduction pathways of seaweeds 329 Dry and semi-dry ballast Both dry and semi-dry ballast were used extensively prior to the twentieth century and can be considered to exist in the transport of dredged material as cargo for landfill or as ballast within hopper barges and dredges. Numerous unequivocal examples exist: the introduction of Pacific oysters wCrassostrea gigas (Thunberg 1793)x into the Northeast Pacific Ocean resulted in the establishment of Sargassum muticum (Yendo) Fensholt (Scagel 1956. Porphyra yezoensis Ueda. Agardh. this transport vector is unlikely to have a consistent suite of constraints. and rock from intertidal and supra-tidal environments. the transport of C. including taxa from three macrophytic phyla (including the angiosperms) – representing all of the major trophic groups from infaunal soft and hard bottom epifaunal. While many crustaceans and molluscs may have been introduced via this mechanism. Species which are intentionally released for stocking or aquaculture purposes are pre-selected for likely establishment in the new environment and are typically released at high inoculation densities. Ballast water Water ballast was first proposed as a vector for the transport of species nearly 100 years ago (Ostenfeld 1908). leads to the development of sediment layers in the base of ballast tanks and on horizontal surfaces. is responsible for the majority of global macroalgal introductions (Elton 1958. As a result. 1992. To be exempted.. Sargassum muticum. Chordata (ascidians and fish). In Australia and New Zealand. mero. particularly associated with oyster culture. Gollasch et al. The constraints limiting transport by ballast water have been reviewed extensively elsewhere (Carlton 1985. Additionally. or living inside the target organisms. This mechanism typically collected sand.W. Ribera Siguan 2003). and the ability to survive long periods in darkness as unattached material (Table 1). Mollusca. these measures have been developed to prevent the w9x . epibiotic. Ballast tank sediments (includes sea sediments) The uptake of sediment-laden (turbid) water coupled with the natural mortality of plankton in ballast tanks. propagules or vegetative fragments. non-approved species must undergo an individual risk assessment process. it also favours species that use vegetative fragments to establish. Saunders. Several macroalgae are capable of meeting these criteria. However. Uptake of associated species would be predicated on ecological association with the target species and the absence of management or quarantine measures to prevent transport and release of associated species (see risk mitigation below). Since then. only one brackish-water macroalga is suspected to have been introduced by this mechanism: Chara connivens Salzmann ex A. import is based on risk assessments that identify a suite of ‘‘approved’’ species that must comply with agreed quarantine standards (through Import Health Standards wIHSx. 2002). Australia) including specific quarantine periods and containment requirements.

Ascophyllum nodosum (L. Schaffelke. especially in domestic transport between biogeographic regions we. This mechanism of transport continues to exist. clams. 2004). lobsters. However. Kappaphycus alvarezii (Doty) Doty ex P. Ribera Siguan 2002). especially aquaculture research. 1998. However. the NE Pacific Ocean (Zostera japonica Aschers. 2007). Ceramium and Gigartina have been identified from live rock (Frisch and Murray 2002). Caulerpa taxifolia and Codium fragile ssp. Ribera and Boudouresque 1995. 1996. consequently. This ostensibly compassionate gesture will. C. packing material is not covered under IHS and therefore slips through biosecurity or quarantine detection. Constraints for this pathway are desiccation and. Rapid settlement of Undaria pinnatifida zoospores was shown on glass slides suspended from ropes in an infested Tasmanian bay (B.. Miller et al. numerous non-approved species bypass mandatory import requirements. this mechanism is intended to keep the target species (bait or live seafood) alive. many with subsequent escapes (e. Association with marine and maritime equipment Observations and anecdotal evidence indicate that introduced species often become entangled in fishing gear such as nets and ropes. possibly.L. This becomes an issue when aquarium species are discarded (‘‘released’’) into the local environment when no longer wanted. Silva.. Despite quarantine and IHS efforts. the species used for packing material is likely to survive the transport process (Table 1). this mechanism is likely to ensure high survivorship because effort is made so that the target species arrive in good condition. 2002. Schaffelke and Deane 2005). and in some countries. Risk mitigation and management Macroalgal introductions continue to occur through a variety of transport vectors and pathways in most regions . Trowbridge 1995. Packing material Marine macrophytes (both macroalgae and seagrasses) are commonly used as packing material for the transport of live bait and live seafood (e. in Australia between Pacific and Indian Oceans. Packing material for bait is the most likely to be discarded in the marine environment (Wallentinus 1999. especially from areas with high abundance of introduced macroalgae and during periods of high reproductive output.g. This import pathway is difficult to control. not controlled by regulations. tomentosoides survive emersion in high humidity for up to 10 and 90 days. Aquarium species can be also purchased via the Internet and enter many countries by post or courier mail. possibly leading to further spread of these species. at its worst. Agardh in the Mediterranean Sea (Meinesz et al. and. especially if these are imported as target species. Numerous packing material-associated invasions have been recognised in the Mediterranean Sea (Wallentinus 1999. as the commercial incentive is to ensure that the target species arrive in good condition. 2000). Sulu et al. Similarly. Most importations consist of species listed by common names (rather than scientific binomials. ˚ Several species of the genera Caulerpa. and the southern waters of Australia (Schaffelke et al. For example.330 C. Russell (1983) identified four macroalgae that were transported from Kaneohe Bay. 2002). Freshwater diatoms can be transported attached to equipment such as fishing gear.. Kiribati with a commercially cultivated species. many through accidental escapes. in France between the NE Atlantic Ocean and Mediterranean Sea. unpublished data).g. tomentosoides (Van Goor) Silva: Carlton and Scanlon 1985x.e. Ribera Siguan 2002. have been recognised (see Pickering et al. 2005) possibly allowing numerous species to be imported under a single common name. Consequently. Relini et al. have been associated with this transport mechanism. Scientific research Several intentional introductions of macroalgae for scientific research. Weigle et al.C. anchor ropes and chains (e. The most sensational has been the introduction and spread of Caulerpa taxifolia (Vahl) C. 2002. and the NW Atlantic Ocean wCodium fragile (Suringar) Hariot ssp..g.. Carlton and Scanlon 1985. e.) Le Jolie: Milw10x ler et al. 1995x. and spores or gametes of macroalgae could be also transported in a similar fashion. 2004) and documented impacts (Schaffelke and Hewitt 2007). USA to Fanning Island. the currently allowed import of ‘‘live rock’’ (i. Much like the transport of aquaculture species. by washing gear before re-immersion in salt water. 2004). Wallentinus 1999. Hawaii. Wallentinus 2002).g.: Accidental introduction pathways of seaweeds inadvertent introduction of fish pathogens and parasites and. see the species released into an unsuitable environment resulting in quick mortality. There are few uptake and transport constraints placed on the intentional transport of allowed macroalgae in the aquarium trade (Table 1). respectively (Sant et al. freshwater stress. Macroalgal species tolerant to emersion could be successfully transported by this vector. 1996. at its best.. hence. et Graebner: Harrison and Bigley 1982. once a species is sold to a private person it is under less stringent control. rock that has not been sterilised and contains numerous species) poses a significant risk (Fossa and Nilsen 1996. and oysters). do not deal effectively with macroalgae. in North America (USA and Canada) between the NW Atlantic and NE Pacific Oceans. Like aquaculture translocations. taxifolia has been intercepted entering New Zealand illegally in courier mail after being purchased via the Internet. 1995) and subsequent introductions in California (Williams and Grosholz 2002). Hewitt et al. a number of high profile macroalgal introductions. This vector includes translocation of target and associated species (Table 1). For example. this mechanism of transport must be considered as a high risk for the transport of macroalgae.g. The aquarium industry itself is generally regulated. it will result in release into a suitable environment where the species can thrive to become invasive. packing material used for transporting live seafood has also resulted in the establishment of species in the marine environment. abalone. Typically. consequently. For example. bioregions after Kelleher et al.

In contrast.. treatment of aquaculture stock). The ICES CoP recommends a risk assessment procedure. TBT) as active ingredients to prevent the settlement and growth of organisms has been effective at reducing the economic costs of fouling (i. Weigle et al. management of species translocations associated with commercial shipping (including slow-moving oil platforms. earthquakes. Risk mitigation addresses either the uptake of propagules at the source location (e. hull fouling is currently a largely unmanaged transport mechanism (Minchin 2004) that has been demonstrated to be a significant transport pathway of large numbers of invertebrates and macroalgae (e. prevention of hull fouling by anti-fouling paints). 2007). perhaps combined with cleaning methods (e. transport as D-stage larvae is less expensive. IMO 2004. Hewitt 2003). NW Atlantic Ocean. SE Pacific Ocean). Bax et al. 2000. risk mitigation is the only acceptable management option.g. These efforts are largely focused on a few transport mechanisms. ocean going barges and tugs) and recreational vessels is more problematic. Ruiz et al. a decision tree that includes feedback loops for seeking additional information. 1999. As has been noted. floods. Gonzalez personal communication). Such conditions should be included in IHSs but unfortunately this is often considered too prescriptive. 2003.L. 2002. control can be aimed at a variety of points in the invasion process.g. leading to a significant effort to establish concerted national.. 2001. Hewitt 2003. 2004.and macroalgae. tributyl tin. In situations where open ocean release is deemed acceptable. or are in the final stages of negotiation we. 2000.g. 2003). In the case of species associated with intentional movements of target species (aquaculture. the target species transported as adults should be maintained in a quarantine facility as brood stock. Intentional introductions. such as macroalgae. Similarly. Unintentional introductions In contrast to the intentional movements of target species. IMO 2004. with the establishment of agreed quarantine standards (through IHS) and treatment options. international opinion has identified ballast water as the transport pathway with the highest chance for successful management in the immediate future. cyclones. Lastly. the transport of adults has demonstrably introduced significant numbers of associated species. consequently. Hewitt et al. 1998.g. Gollasch 2002. however. Intentional transport and introduction of species for aquaculture. the main difficulty with the ICES CoP is that it is not a legally binding instrument. the selection of the life history stage for transport of the target species is a significant control point. Intentional introductions Achieving zero-risk is rarely possible.g. w11x . Cranfield et al. The probability of ‘‘uptake’’ of associated species can be controlled by maintaining specimens in a quarantine or containment facility. adequate filter systems are required for facilities that culture micro. and recommends decision criteria. regional and global management regimes including the adoption of a new International Convention for the Management and Control of Ships’ Ballast Water and Sediments (BWM. NE Atlantic Ocean. and significantly minimises the risk of transporting associated organisms. Similarly. 2004)... or in the accidental transport of non-target (associated) species. consideration should be given to the aquaculture (or mariculture) of non-indigenous target species in controlled.. aquarium trade or scientific research can result in the accidental release of target species through escapes from growing facilities... Schaffelke et al. which advises on how to evaluate the risk of introducing a marine organism. We discuss various management actions separately for intentional and unintentional introductions.. Doelle et al.g. 2007x. Ribera Siguan 2002. despite significant efforts to ‘‘clean’’ the valves prior to transport (Wallentinus 1999). this requires a significant investment in resources and remains fundamentally reliant on the availability of expertise and political ‘‘good will’’. Rainer 1995. 2007). Currently available treatment options are limited to preventative measures (anti-fouling paints) or reduction measures (in water hull cleaning or dry docking). more effective. Lewis 1999. pathogens or other associated species. The use of anti-fouling paints with copper and organotin (e. Sulu et al.: Accidental introduction pathways of seaweeds 331 of the world (e. also provide opportunities for maximum control through appropriate management either prior to introduction or in the establishment and operation of the growing facility. Several transport mechanisms are either under current management or regulation at national or global scales (e. Ribera and Boudouresque 1995. However. Hewitt et al. International Convention for the Management and Control of Ships’ Ballast Water and Sediments (BWM) Convention. Crassostrea gigas Thunberg.C. scientific research). see Doelle et al. land-based facilities with appropriate filtration and sterilisation measures prior to effluent discharge into the ocean. In contrast to ballast water.g. or the release of viable material into the recipient environment (management of ballast water discharge. Carlton 2001. At present. This would be equivalent to a stagegate approach whereby the target species could not be transported prior to demonstration that there are no associated macroscopic species (note that disease is controlled under other mechanisms).. Ribera and Boudouresque 1995. Carlton 1985. It has been applied successfully in a variety of circumstances and in several regions (Mediterranean Sea. see Doelle et al.. increased fuel costs associated with increased drag). including determining the likelihood and consequences of also introducing associated species. with the release of F1 generation material allowed only after demonstration of no infection by diseases. Minchin and Gollasch 2002. The International Council for the Exploration of the Seas (ICES) has developed a Code of Practice (ICES CoP) for Introductions and Transfers of Marine Organisms (ICES 2003). 2006). Ribera Siguan 2002.g. aquarium trade.g. For invertebrates such as the Pacific oyster. Ruiz et al. tsunamis) is reduced (E. Wallentinus 1999.e. This mechanism has been perceived by the international community as the greatest threat (e. Caution must be taken to ensure that quarantine facilities are sited where the impact of natural disasters that possibly breach containment (e. 2005.

Alternative paint technologies with appropriate application and renewal guidelines must be developed as a matter of urgency. diver-operated brush carts or physical abrasion using scrapers or brushes are common methods of reducing fouling between dry docking periods. packing material).L. Drake 1991.g. detached individuals without reproductive structures are generally unable to develop sporogenous tissue while drifting walthough the invasive Sargassum muticum is a notable exception (Norton 1977. Lodge 1993. with limited availability to benthic stages that have been ‘‘swept’’ off the substratum (tychoplankton). and often discharge removed materials into coastal waters. 2007). but not to determine the attributes for successful establishment and spread of populations.g. Baker 1965. (2007). Burns and Sauer 1992. because alternative paints with equivalent efficacy are likely to be more expensive or require more stringent application procedures (Minchin 2004). steam cleaning. aquaculture. Carlton 1979. with large effort being expended to date. Case 1990. a stenohaline species that is restricted to habitats of less than 15 psu would likely experience a ‘‘complete’’ filter in transiting the open ocean with salinity )30 psu. hull fouling and ballast water. water ballast.. Unfortunately. As Crawley (1987. Johnson and Chapman 2007). Prediction of new invaders The accurate prediction of likely invaders will continue to be a driving force in academic and applied invasion ecology (e. particularly when followed by the application of anti-fouling coatings. the International Convention on the Control of Harmful Anti-fouling Systems on Ships (AFS. In contrast. which aims to phase-out the use of organotin-based paints (specifically TBT). Beddington et al. However. traits believed to be essential for a species to become a successful invader are also found in non-invasive conspecifics and congenerics (Paula and Eston 1987 for Sargassum species. 1998 for Codium fragile subspecies). packing material) and exposure to varying environments such as changing temperature and salinity (hull fouling). Theoretical (e. the role the recipient environment and community plays in determining the success or failure of invasions must be critically examined in the marine environment (see Dunstan and Johnson 2007). Hayes and Sliwa 2003. In this evaluation.g. aquaculture. The factors that contribute to the successful introduction of a species include species’ functional traits. Australia and the USA. Hewitt et al. transport constraints consist of physical and physiological constraints (Table 1). gear transport. Robinson et al. In-water cleaning is a common mechanism for reducing fouling. Ricciardi and Rasmussen w12x 1998). of the myriad factors which ultimately influence success and failure of an invasion. Cleaning while in dry dock is the most effective procedure for removing organisms. however. Current research on the development of biologically safe in-water cleaning techniques is underway in numerous countries. and desiccation. ballast water is largely restricted to planktonic stages. 1996. spread) act as filters. but with little progress so far. Physiological constraints include desiccation (dry ballast. Dry dock cleaning is extremely effective. freshwater. where the physical removal of organisms can lead to vegetative fragments or gametes/spores being released in areas conducive to their establishment. high water hull fouling. We suggest that the three main stages of the invasion process (uptake/transport. many dry-docking facilities (particularly those suited to handling small vessels) do not have appropriate provisions to hold and treat removed materials. 1989) and Valentine et al. Several transport mechanisms are restricted to a limited set of the life history stages of a species. In addition. New Zealand. For example.. Most previous discussions concerning the identification of potential invaders have revolved around the development of species-specific invasion attributes (e. Trowbridge 1995. These filters may either completely prevent certain characteristics of species or ecotypes from passing through. individual species’ characteristics contribute only a small amount and are unlikely to be useful predictors alone. gear transport.: Accidental introduction pathways of seaweeds Unfortunately.g. aquaculture). e. and uses methods such as physical abrasion (scraping. Bazzaz 1986. establishment. For example. (2007) conclude. as discussed by Doelle et al. light limitation (dry ballast. Deysher and Norton 1982)x. In many macroalgae however. 1995) suggest that ‘‘ecological resistance’’ may indeed . Drake 1990) and empirical studies in terrestrial and freshwater environments (e. and/or partially prevent other characteristics from passing through.. The implications of understanding these critical points for developing cost-effective and appropriate management activities are great (Hayes and Hewitt 1998). For the primary modern transport vectors.g. and Australia has adopted a ban on inwater cleaning in several ports. 1991. with species’ attributes either being beneficial or detrimental to successfully pass the filter (Carlton 1985. may result in an increase in hull fouling associated introductions. 1978. this has not led to a concomitant elimination of biological risks. water pressure). Nyberg and Wallentinus 2005.. The removal of fouling organisms in-water often occurs in ports or in marinas. we undertook to delineate the constraints placed on uptake and transport of species. it is crucial that we begin to understand these constraints. 1996.. and exposure to the transport vector (Table 1). The need to develop standards for dry-docking facilities with guidelines on appropriate treatment is urgent (see the ANZECC Code of Practice). Lastly. The absence of knowledge about failed introductions hampers the accurate assessment of controlling factors (see Miller et al. 1996). Uptake constraints consist of presence of the species and availability of suitable life history stages in the donor location. Physical constraints include shear stress (hull fouling) and crushing (dry ballast. IMO 2001). Hayes and Hewitt 1998.332 C. This method is typically the only hull-cleaning treatment for small recreational vessels between anti-fouling applications. Arthington and Mitchell 1986. including viable hull fouling organisms. characteristics of transport vectors and attributes of the recipient community. It should be noted. that removal of species that originate in a port or marina prior to departure would act to reduce the transfer of species between regions.

Nyberg and Wallentinus 2005). Ribera and Boudouresque 1995. critical resources would include substratum. (15) NE Pacific Ocean. light and nutrients. (5) NE Atlantic Ocean. Britton-Simmons 2006) have identified resource use and subsequent preemption as an important process in restricting invasibility of systems. Smith. These are by no means the only species likely to be introduced in the future. E & G: Equipment and Gear. species’ traits. (1995)... In a simple analysis based on recognised introductions of marine macroalgae (e. occur. tomentosoides Striaria attenuata (C. Hayes and Sliwa 2003. (14a and 14b) S Pacific Ocean. Stachowicz et al. (9) S Atlantic Ocean. SR: Scientific Research. coupled with sufficient inoculation.) Grev. while fluctuations would be caused e. 2002. A number of authors (e. (13) E Asian Seas.L.. (18) Australia and New Zealand. Hooker et Harvey) Lyle Ceramiales Heterosiphonia japonica Yendo Ceramiales Polysiphonia brodiaei (Dillwyn) Sprengel Ceramiales Polysiphonia harveyi J. (2000) propose that invasibility of terrestrial plant communities is a function of fluctuations in resource availability. Schaffelke et al. (4) NW Atlantic Ocean. (12) E Africa. For macroalgae. (6) Baltic Sea. (1) Antarctica. J. A: Aquaculture.. Davis et al. as no evaluation of impact is incorporated into the analysis. see Figure 3)x and a continued association with active vectors deemed to pose a continuing global threat of invasion*. higher nutrient availability and changing herbivore pressure. (17) SE Pacific Ocean. (16) NW Pacific Ocean.g. 2003. This merely identifies those species with a demonstrated propensity to surmount the constraints of the invasion process. Taxa Species and authority Unintentional transport HF Chlorophyceae Caulerpales Codiales Phaeophyceae Dictyosiphonales Laminariales Caulerpa taxifolia Codium fragile ssp. 1999. attributes of the receiving environment). BW: Ballast Water. (19) Great Lakes.C. Ag. trophic structures. In the face of an overwhelming suite of successful invading marine species with disparate traits and life history patterns. (2) Arctic. PM: Packing Material.g.g. and their propensity for introduction (number of successful invasions into the IUCN large scale bioregions after Kelleher et al. (7) Wider Caribbean Sea. (8) W Africa. 2006. 2007. we must evaluate a species’ success or failure to invade in the light of Table 2 Identified macroalgae that have a high likelihood of invasion based on prior history wG3 invaded IUCN Bioregions (bioregions after Kelleher et al.g. Undaria pinnatifida ● ● BW ● ● E&G ● ● Intentional transport (associates) Number of invaded IUCN A LT PM SR bioregions ● ● ● ● ● ● 3 6 ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● ● 5 5 4 3 3 3 4 Rhodophyceae Bonnemaisoniales Bonnemaisonia hamifera Hariot Ceramiales Antithamnionella spirographidis (Schiffner) E.D.M. (11) Arabian Seas. competition strengths and niche occupancies. Evaluations of habitat invasibility need to incorporate information about native biodiversity. we identify twelve species that are likely to be of ongoing concern (Table 2). nor does this simple analysis take into account the likelihood of causing harm. Dunstan and Johnson 2004. Evaluation of intentional transport is limited to those species that are transported as associates of other intentionally transported species. Wallentinus 1999. 1995. Ribera Siguan 2002. w13x . Other analyses aimed at predicting future invaders list a similar suite of macroalgal species (e. by physical disturbance. unpublished data). coupled with indications of their associations with currently active transport mechanisms. Hewitt et al. An improved prediction of future invaders must take into account the synergy between the three aspects of invasions (vector strength.: Accidental introduction pathways of seaweeds 333 Figure 3 IUCN large scale bioregions after Kelleher et al. Transport mechanisms are abbreviated as: HF: Hull Fouling. see Figure 3). (10) Central Indian Ocean. 1995. LT: Live Trade (Aquarium and Live Seafood). Wollaston Ceramiales Antithamnionella ternifolia (J. Bailey Halymeniales Grateloupia subpectinata Holmes Halymeniales Grateloupia turuturu Yamada Rhodymeniales Lomentaria hakodatensis Yendo ● ● ● ● ● ● 3 3 3 3 *Note that this does not infer risk. (3) Mediterranean.

biogeography and ecology of the introduced marine and estuarine invertebrates of the Pacific Coast of North America. Biogeography and dispersal of coastal marine organisms: experimental studies on a replica of a 16th-century sailing vessel.A. D. Kruger. Carlton. H. 7: 213–232. embryos and larvae of Topsmelt Atherinops affinis. 1989. Soc. Invasion resistance arises in strongly interacting species-rich model competition communities. S. pp. T. Marshall. Science 261: 78–82. coastal waters: environmental impacts and management priorities. Mar. J. Lambert. A. 1998.G. Pew Oceans Commission. W. R. Australian Academy of Science. eds) Colonization.J.C. A. SCOPE 37. Pattern. Eldredge. F. Read. Sci. H. 121: 721–730.L. R. Crosby. H. T. species build-up and community collapse in metapopulation models with interspecies competition. W.H. New Zealand. Ships’ seachests: an overlooked transfer mechanism for non-indigenous marine species? Mar. Bahamonde. Norton. 50: 418–437. USA 87: 9610–9614. Glob. Transoceanic and interoceanic dispersal of coastal marine organisms: the biology of ballast water. In: (J. Coutts. L. Mooney. A.A. Willan.C.G. C.G. Cons. J. Linn. C. Carlton.J. Within this framework. 96–110. 1999.N. A. Carlton. In: (H. J. J. Stebbins. Groves.T. Geller.H. 1986. resource preemption and the genesis of invasion resistance in a community of marine algae. 904. Blackwell Scientific. and physiological features. 33: 551–562. pp.L. M. Moore and C.L. Hewitt. Resistance by natural vegetation in the San Gabriel Mountains of California to invasion by introduced conifers. USA.J. Burdon. Carlton. New York. Inv. F. Bot. Rejmanek and M. G.T.A. Sauer. Toft. Williamson. R. Campbell. 2001.P. Bax.T. 1998. Hewitt. J. di Castri. the field of potential invaders may be narrowed and ultimately predicted with increasing success.D. Biol. Edwards.J. 28.. pp.. Wellington. and J. Harris. Mooney. I. F. Coles. J. pp. Gonzales and W. Critchley. Nelson. eds) Ecology of biological invasions of North America and Hawaii. Unpublished Masters Thesis. NIWA Technical Report 34. Biol. Scanlon. eds). Moyano.A. Scope 37. S. Hewitt. Pac. Arthington.. di Castri. pp. Olympia. Man’s role in changing the face of the ocean: biological invasions and implications for conservation of nearshore environments. Chapman. Progression and dispersal of an introduced alga: Codium fragile ssp. Prepared for the Washington State Department of Natural Resources. Wonham. Bot. Mar. pp. J. and L.J. eds) The genetics of colonizing species.H. 1986. Drake. 1979. We would also like to thank John Lewis.J. tomentosoides (Chlorophyta) on the Atlantic coast of North America.T. Berry. 1985. M. Gray. Control of invasive seaweeds.A. Australia. 3: 265–273. Francis. Kong. Crawley. Biological invasions: a global perspective.T. A. F. Mar. Canberra. Rozbaczylo. Mar.H. A bibliography of invasive alga Sargassum muticum (Yendo) Fensholt (Fucales.P. Oikos 113: 395–401. L. A. A. In: (C. Drake. Case. Mooney and J. Introduced species in U. Drake. John Wiley & Sons. Life history of colonising plants: some demographic. 407–423. Biol. Baker and G. Eldredge and J. 52: 277–289. Baker.. 2: 46–51. Ecological imperialism: the biological expan- w14x . B. 2003. 1991. Britton-Simmons. Kohn. 1999. M. 37. Rev. 1985.. Clarke. Env. Beddington. Mar. Puget sound expedition: a rapid assessment survey of non-indigenous species in the shallow waters of puget sound.L. C. Lawton.: Accidental introduction pathways of seaweeds transport mechanisms acting as constraints and of other characteristics of the invasion process. Lett. In: (J. tomentosoides (Chlorophyta) in the North Atlantic Ocean? Helgol. 1993. Nonindigenous species introductions on coral reefs: a need for information. T. Cohen. Launceston. 23: 313–371.H. Stephan Gollasch and Inger Wallentinus for fruitful discussions in preparation of this manuscript. Thresher and R.W. Uribe.. M. Aquatic invading species. Hull fouling as a modern vector for marine biological invasions: investigation of merchant vessels visiting northern Tasmania. Functional group diversity. Res. 34–53. New York. Coutts. Battershill.M.L. such as recipient community attributes (see Dunstan and Johnson 2007). Campbell. Marine invasive alien species: a threat to global biodiversity. Carlton. Mills. Cons. New York. Carlton. J.T. C. Lambert. Groves and J. Free and J. Acad. Cranfield. 1992. National Institute of Water and Atmospheric Research. Adventive marine species in New Zealand. Academic Press. VA. 135: 147–158. Secord and J. 1987. 2002. Wiss.T.L. pp. K.R. shipping and trade.E. with notes on induced spawning. M.N. Biol. T. 147–172.M. 1990. M. K. Martin. Aguero.L. 42: 239–266. genetic. Oxford. and D. eds) Biological invasions: a global perspective. Mar. Wil´ liamson. A.S. What makes a community invisible? In: (A. pp.J. Hodder.S. Chance and timing in biological invasions. K. Biol. J. Carlton. New York. Copper toxicity to sperm. pp 45–60. Crawley.J.J. E. Springer-Verlag.J. Bull. F. et al. succession. Tasmania. 1990.. Vectors. Poll.L.T. Gordon. Case. Davis.T. B. J. D.. 1999. Li. 46: 1510–1512. Hawaiian Islands. Burns. and J. Klinger. Proc..A. N. History of biological invasions with special emphasis on the Old World. Biog.W. Biol. 2003. Mar. Sargassaceae). C. John Wiley & Sons.L. N. 2007. WA.A. 28: 155–165. Ecological roulette: the global transport of nonindigenous marine organisms.L. 1989. Chapman. Characteristics and modes of origin of weeds. In: (R. Ocean. Historical and recent introductions of non-indigenous marine species into Pearl Harbor. Castilla. J. Ecol. Bazzaz. Mitchell. History.J. K. 1999.J. J.B. Meeresunters. B. University of California.P. Carlton. 1996. USA. Hewitt et al. C.J.C. 1991. Anderson.S. Middaugh. Mar. M. Coles. and J. Acknowledgements We thank Drs Craig Johnson and Tony Chapman for inviting our participation in this special issue. Zavala. Oahu. F. and C. Glasby and G. and stability. Natl. 1965. 48. J. Hobart. 1995.W. B. DeFelice.S.334 C.A. Bot. Ann.T. H. 78: 97–106.G. 2005. B.A. 56: 191–209. pp. Victoria. Sci. pp. Farnham. 1978. R.B. di Castri. J. In: (H. Cordell.B. 31: 17–35. A. pp 1–30. Yoshida and T. 2006.A.M. C. eds) The introduced species of Port Phillip Bay. From introduced species to invader: what determines variation in the success of Codium fragile ssp. L. Geeves. H. Hunt and S. Desqueyroux-Faundez. CSIRO Marine Research. Invasion resistance. Nature 273: 513–519. M. 429–453.F.A.H. N. eds) Ecology of biological invasions: an Australian perspective. process. Kruger. Australian Maritime College. Policy 27: 313–323. Carlton. Down under the southeastern Pacific: marine non-indigenous species in Chile. and J. Valdovinos and P. J. and prediction in marine invasion ecology. Biol. R.. M. M. 1989. M. R. H. Carlton. Characters of successful natural enemies in models of biological control of insect pests. References Anderson. CA. Groves.D. 1986. Turpen. San´ telices.A. Bookheim. Bingham. 283. Crawley and P. PhD Dissertation.

1. Lockett.A. Poll. A global representative system of marine protected areas.A. Grime and K. Mechanisms of invasion: can the recipient community influence invasion rates? Bot. The distribution and diversity of tropical Australian marine bio-invasions.L. and ‘‘Live Rock’’ in retail aquarium outlets in southern California. Ecol. Effects of cadmium and copper contamination on calcium content of the bivalve Ruditapes decussates. Nilsen. Ecosystem transplant? The case of the Yefim Gorbenko.M. M. Kluwer. 2002. J.. McEnnulty. Gollasch and S. CSIRO Marine Research. P.E.L.H. Diannelidis. Lewis. Hayes. B. Centre for Research on Introduced Marine Pests Technical Report No. T. Norton. J. 1996. Ann.G. Paracerceis sculpta. Evol. The modern coral reef aquar˚ ium. Houvenaghel.E.R.D. 2001. pp. Martin. to the Pacific coast of North America.R. CRIMP Technical Report 14. Identifying potential marine pests — a deductive approach applied to Australia. Victoria. Romeo and S. 2007. 39: 1642–1648. 900-1900. H. H. Seaweed invasions: conclusions and future directions. Gomon. Davis. L. Bigley. and G. Env. 2004. M. 1995.N. MacDonald. Wallentinus..P. The Great Barrier Reef Marine Park Authority. Hobart. Centre for Research on Introduced Marine Pests Technical Report No. and M. Brit. 1991. Komatsu. 1982.. 147: 213–233. Volumes 1–4.L.L.L. Hewitt. 49: 999–1005. Hobart. Currie. 2001. Dodgshun. Dispersal and colonization in Sargassum muticum (Yendo) Fensholt. Biofouling 18: 105–121. Hamer. pp.. Hewitt. Sci. D. 2003. Marine biological invasions of Port Phillip Bay. D. and The World Conservation Union (IUCN). Community-assembly mechanics and the structure of an experimental species ensemble. pp. Env. Lucas. Murray. Gollasch and S. 144: 183–202. S. Methuen and Co. 1993. Lavoie. M. Division of Marine Research. R. Mar. ICES Code of Practice on the Introductions and Transfers of Marine Organisms 2002. The availability of Caulerpa spp. Nat. R. Campbell. 344.M.L.L.J. January 31–February 1. S. Mar.G. with emphasis on Port Phillip Bay. R. R. Ceramiales). 2007. pp. and C. L. Am.C. Gnassia-Barelli.P.M.M.L. 2004. Australia. 25: 301–313.R. J. Campbell. 2001. I.A. Storey. M. Mar. The introduced species of Port Phillip Bay. S. N. 39: 325–328.M. Centre for Research on Introduced Marine Pests Technical Report No. Meinesz.B. Bot.A. A. M. J. Hay.E.L. Olenin. 2004. Thresher and R. L. H. Coast. and C.A. 101. Berlin. Wetsteyn and T. 1979. 61–87. International Convention on the Management and Control of Ship’s Ballast Water and Sediments. 2003. Sliwa.R. Victoria.L. Bot. Olson. Fossa. Carpenter. Molenaar and X. Martin. Persson. Phycol. C. The ecology of invasions by plants and animals. The sustainable biosphere initiative: an ecological research agenda.J. McCollin. Christensen.L.P. Hay. eds.F.. C. Drake. and C. Schaffelke and M.. 20. 217–231. Lubchenco. P. Johnson. 23. eds) Invasive ¨ aquatic species of Europe distribution. C. Hewitt.J. 8: 133–137. T. Washington. D. 1980.R.L.R. Risser. 1997. E. International Council for the Exploration of the Seas. C. The importance of ship hull fouling as a vector of species introductions into the North Sea. Biol. P. 50: 361–372. 62. P. Mari.R.A. 367.A. Fletcher. Hewitt et al. Mar.R. Luther. Ross. Lewis. Drake. C. Johnson. 50: 451–457. J. 2002.H. S. London. International Convention on the Control of Harmful Anti-fouling Systems on Ships. L. Poore. Benichou. Peterson. Lewis. Wells. M.F. Mar. S. VanderZwaag. 1995. mor- w15x .org). A guide to the principal marine fouling organisms. and R. impact and management. 1997.J. Bot. The Australian distribution of the introduced sphaeromatid isopod. Poll. B. Mar. Matson.N.P. pp. 1995.. Johnson. Marine biosecurity issues in the world oceans: global activities and Australian directions. pp. M. Copenhagen. 56: 179–195. Hewitt. Campbell. C. International Caulerpa taxfolia Conference Proceedings.A. Fish. and T. Cohen. Leppakoski. I. C. M.A. J. Blachier. R. Australia. Doelle. Leppakoski. G. J. 2007.imo. Pulliam. with particular reference to Cockburn Sound. MacMahon.J. McConnell and D. M. J. and S. M. W. McArthur. D. 1999.K. C. Bax..M. 1998. eds. Mar. 2000.. J. S. 20. S. Gollasch. Holland. International Maritime Organization. Res. J. CSIRO.L.A. The effects of zinc.B. P. Jelmert. Variations in the structure. and C.. Olenin. The potential for intracoastal transfer of non-indigenous species in the ballast water of ships. copper and cadmium on the fine structure of Ceramium ciliatum (Rhodophyceae. Kluwer Academic Publishers. Boyd. Gollasch. Biol. Riddle and A. Bull. Cambridge University Press. 1982. Masson. S. Hewitt. K. Riddle and C.. C. S. Mar. 88: 528–534. California Sea Grant College Program. Biological invasions: lessons for ecology. -http://www.C. 1990. N.A. J. 46: 213–223. In: (E. Biol. Res. 1990. M. Wittling. et Graebn.J. Campbell. pp.A. C. 75. eds). P. Botnen. and T. S. Regal and P.. 2002. E. J. 1982. A rapid response toolbox: strategies for the control of ABWMAC listed species and related taxa in Australia.-E. May 1997 issue. Dordrecht. Bull. A. Ocean Yearbook 17: 193–212. Hewitt. Australia. Deysher. CSIRO Marine Research.: Accidental introduction pathways of seaweeds 335 sion of Europe.imo. Hobart.J. pp. Keogh. 25.K. Lemee. 2002. M. Publication No.A. J. Invasion rates increase with species richness in a marine epibenthic community by two mechanisms. 2002. 2004. Mar.A. M. Fennici 16: 141–150. Thresher and R. A risk assessment framework for ballast water introductions. The recent introduction of the seagrass Zostera japonica Aschers. Mooney.B. -http://www. Campbell. Watson and R. 2003. M. Department of Defence Support. J. Invasive ¨ aquatic species of Europe distribution. Mar.R. F. Invasive seaweeds: global and regional law and policy responses. 137: 1–26. 56: 213–222. Volume 6.A. IMO. Harrison. Dunstan. 368. Hewitt. Brubaker. 2002. pp. pp. London. Brussels: ODEMA.L. 1991. Levin.A. Can. International Maritime Organization. Management of exogenous threats to Antarctica and the sub-Antarctic Islands: balancing risks from TBT and non-indigenous marine organisms. pp.T.B. Bleakeley and S. Shelf Sci.B. 2003. R. M. impact and management. S. La Jolla. McMinn. Hewitt. Victoria. and implications for further dispersal of Undaria in France. P. The mechanics of community assembly and succession.. Victoria. Olenin. Seafood New Zealand magazine. Oecologia 138: 285–292. The dispersal of sporophytes of Undaria pinnatifida by shipping in New Zealand. Hubbell. Thompson. Theor. Frisch. 1958. Belson. 44: 127– 134. Delivopoulos. T-047 (CD-ROM). Hayes. Fluctuating resources in plant communities: a general theory of invasibility. Ecol. Lewis.L. Dunstan. K. D. C. 181. Est. Birgit Schmettkamp Verlag. Hobart. pp. 13–15. A. 1999. M. Aq.S. Ruiz. Ecology 72: 371–412. Bull.M. DC. Real. 583. Catalogue of main marine fouling organisms. Hewitt. Pac. Wilson. Poll. S.. Introduced and cryptogenic species in Port Phillip Bay. IMO. Lewis. Materials Research Laboratory Report MRL-R-858. J. L. 48: 551–564. 1999. The World Bank. M. B. Smith and G.D. J. Cambridge. L. algae. Crustaceana 74: 925–936. H. ICES. Chara connivens in the Baltic Sea area.E.E. T. London. Melillo. C. 46: 91–98. pp. J. CSIRO Marine Research. In: (C. Sci. Kelleher G. Lodge. Life in ballast tanks. Mays. Martin. A review of the occurrence of exotic macroalgae in southern Australia. Elton.L. Dordrecht. H. Marine introductions in the Southern Ocean: an unrecognised hazard to biodiversity. 50: 438–450. Puiseux-Dao. O’Hara. 30.. G. Trends Ecol. Thresher.L. and A. Exp.

D. Hay and T.W. 26: 41–53. D. Johnson. USA. A. G. Spivak and E. O. Introduced marine plants with special reference to macroalgae: mechanisms and impact. C. Olenin. B. G. 2005. Fish. Pickering.A. Bot. Mar. Checklist of the macroalgae of Thau Lagoon (Herault. Pac.. G. Rodriguez-Prieto and E. 1. Mechanisms of invasion: establishment. 1992.J.C. Leppakoski. 55: 1759– 1765. J. Fofonoff. R. 2006. Ribera Siguan. Penchaszadeh. Carlton. Phycol. Res. Paper 1: 49–59. Prog. boats and trains. P. J.E. Ecology of the green macroalga Codium fragile (Suringar) Hariot 1889: invasive and non-invasive subspecies. tomentosoides on New Zealand rocky shores: current distribution and invertebrate grazers. Aquatic transport and the spread of aquatic species: challenges for management. G. Syst. Scagel. Cosentino-Manning.W.J. Are there other Sargassum species potentially as invasive as S. and S. a hot spot of marine species introduction ´ in Europe. Ricciardi A. C. Mann. Sant. Bortolus.B. 2000. eds) Dispersal of living organisms into aquatic ecosystems.F. J. 18: 529– 541. Bot. In: (E.L.M. Biol. Elıas.A. J. In: (J. No longer the pristine confines of the world ocean: a survey of exotic marine species in the southwestern Atlantic. 183–192. Ecol. 332: 41–51. Ruiz. 1983. and D. Pas´ ´ cual..D. 50: 338–350. eds). Delgado. T. A. Gollasch and ¨ S. Ann. Davenport and J.. Australia. Ecol. USA. Fish. In: (E. M. Museum of Comparative Zoology. Pastorino.T. 2002. S. In: (G. Turner. Pathways of biological invasions of marine plants. Quinn and M.W. 50: 351–360. Trowbridge. 39: 427–430. Biol. Relini. Minchin. Wonham and A. Phycol. Thresher. Phycol. 2004. 2007.M. M. 18. P. Chang. Robinson. pp. Centre for Research on Introduced Marine Pests Technical Report No. N. M. Exp. 2005. Miller. 7: 265–279. E. 2003. R. Washington..B.J. Eston. R..L. Miller. Relini and G. 7: 577– 587. C. The growth and development of Sargassum muticum (Yendo) Fensholt. Phycologia 44: 477–496. Boston. Key threats from marine bioinvasions: a review of current and future issues. in the northeast Pacific.H. Ecology 76: 786–794. Ecol. Neushul. Uthicke. and A. Verlaque. 244–265. 36: 1–64. Ann. Can. R. M. Ruiz. 2007. 1999. Vectors – how exotics get around. Lewis. Rosenfield and R. Sargassum muticum. D. Verlaque. pp. w16x . A.T. Darrigran. R. 2004. Dordrecht. Res. Boudouresque. 28: 428–438. 1977. 265. Bull. Inv. E. G. The spreading of the introduced seaweed Caulerpa taxifolia (Vahl) C. processes. J. Science 286: 1577–1579. Ecology of the imported red seaweed Eucheuma striatum Schmitz on Coconut Island. Rev. ed. P. N. Pederson. Wallentinus. Sea Grant College Program. Ocean. T. Ruiz. M. 2002.L. 83: 949–965. Komm. Mar. Gollasch. 1999. 2002. Massachussetts Institute of Technology. Kappaphycus seaweed in the Pacific: review of introductions and field testing proposed quarantine protocols.: Accidental introduction pathways of seaweeds phology and biomass of Caulerpa taxifolia in the Mediterranean Sea. 37: 87–107. Pickering. Oresanz. Rhodophyta) in the Thau Lagoon (France. 1992. Vallarino. C.D. Harvard University. Mar. Aquatic Sci. ICES J. 1995.M.D. France). Peters. Kluwer Academic Publishers. pp. Minchin.D. Olenin.) Marine bioinvasions: proceedings of the first national conference. 1987.T. Mar. 2004. G. Inv. R. Hawaii. 40: 1028–1031. Appl. F. S. Whitlatch and R. Magierowski and C.W. 103–135. Oceanologica Acta 24: 29–49.M. 1995. MA. Mar. and J. In: (A. Hewitt..J. M. Establishment of the green alga Codium fragile ssp. Rainer. Noumea: Secretariat of the Pacific Community. Mar. 1908. Schaffelke. Dordrecht. Review of non-native marine plants in the Mediterranean Sea. Ballesteros. Hines. Medd. Maryland. Osman. D. Schaffelke. R. D. 2005. Washington.L. C. Sci. 2000. Sulu. P. Sci.. Temperature responses of disjunct temperate brown algae indicate long-distance dispersal of microthalli across the tropics. Carlton. Sulu. Schwindt. Obenat. pp. 518. Scarabino. 1998.L.F. and C. 183–226. Invasive species: vectors and management strategies. Biol. 2002. Ribera. A. Invasion of coastal marine communities in North America: apparent patterns. Trowbridge. and V. J. 1998. Ambrose. MA.C. Poll. eds) The effects of human transport on ecosystems: cars and planes... N. Bot. Ruiz and J. Invasability of experimental habitat islands in a California winter annual grassland. Maryland Sea Grant.J. A new record and eradication of the northern Atlantic alga Ascophyllum nodosum (Phaeophyceae) from San Francisco Bay. Dublin. and biases. impact and management. Kumar. Russell.C. L.R. Mar. Bot. Schaffelke. muticum? Bot. USA. and J. Island Press.A. Agardh in the Mediterranean Sea: testing the boat transportation hypothesis. tomentosoides-clues for likely transport vectors? Biol. A.D. B. 1995.. 44: 204–210. Lopez Gappa. Havunders. Predicting the identity and impact of future biological invaders: a priority for aquatic resource management. Carlton. C. S. Schaffelke. Gollasch and S.. 1996.. Ruiz G. pp. pp. Inv. and C. Villalard-Bohnsack and M. Mediterranean): a case study of marine plurispecific introductions. Davenport. Nyberg.M. CSIRO Division of Fisheries. 30: 405–410. G. B. Murphy and S. 38: 499–508. 1966. pp. Plankton 1(6): 1–44. 2003. D.A. Deane. J. The role of fishing gear in the spreading of allochthonous species: the case of Caulerpa taxifolia in the Ligurian Sea. Amsler. A survey and illustrated catalogue of the Teredinidae (Mollusca: Bivalvia). pp. T.F. 1999. Paula E. impact and management. Rev. Ostenfeld. Intentional introductions of commercially harvested alien seaweeds. J.D.. 291–310. Mar. M. Brannock. Leppakoski.R. Ribera Siguan. and its occurrence in the North Sea during 1903– 1907. 2007. 1956.E. 50: 397–417. eds. Trowbridge. Stachowicz. 31: 481–531.J. Minton. Ser. Casas. Rasmussen. G.L. J. Biol. 1996. pp. 2001. spread and persistence of introduced seaweed populations. eds) ¨ Invasive aquatic species of Europe distribution. Potential for the introduction and translocation of exotic marine species by hull fouling: a preliminary assessment. J. 1995. The genus Grateloupia C. Torchia. D. 11: 187–268. Marston. S. pp. M.J. Cambridge. Prog. M. Ser. B. Introduced versus native subspecies of Codium fragile: How distinctive is the invasive subspecies tomentosoides? Mar. 4: 115–143. Bot. M. Mar. California. and I. Norton. M. Using genetic techniques to investigate the sources of the invasive alga Caulerpa taxifolia in three new locations in Australia. Hewitt. Skelton and R.336 C. J. Breeman.F. 126: 193–204. Valentine.L. Introduced macroalgae – a growing concern. Piriz. R.H. J.P. January 24–27.F. 2007. Can species traits be used to predict marine macroalgal introductions? Biol.. Hobart. Royal Irish Academy. College Park.M. C. Oahu. Kluwer Academic Publishers. C. Smith and C. Invasive aquatic species of Europe distribution. Agardh (Halymeniaceae.S.R.H. Mar. Differentiating successful and failed molluscan invaders in estuarine ecosystems. Ecol. Stanton. Island Press. On the immigration of Biddulphia sinensis Grev. 24–36. eds) Invasive species: vectors and management strategies. J. 57: 1421–1427. M.. Mar. Reed and R. Introduction of marine plants for aquacultural purposes.M. In: (J. 84. Impacts of introduced seaweeds. S.A. Konmatsu. Introduction of a Japanese alga.. Hewitt et al. Phycol. Desiccation tolerance of the introduced marine green alga Codium fragile ssp.M. Species diversity and invasion resistance in a marine ecosystem.

Wyatt. Walker and T..N. pp. 233: 307–310.L. S.J. 244. Div. Prog.M. M. 19: 213–223. H. 11: 33–44. accepted 6 December. Kluwer Academic Publishers. Stuart and D.J. 1–43. 2002. Cargo vessel ballast water as a vector for the transport of non-indigenous marine species. Eradication success down under: heat treatment of a sunken trawler to kill the invasive seaweed Undaria pinnatifida. O’Brien.. 2002.I. I.D.H. L. Wallentinus. eds) Biology of marine plants. King. Biol. Carlton and J.B. Dist. eds) Invasive aquatic species of Europe: distribution.J. J. Williams. 27–52. In: (M.J. 2005. Introduction and transfer of plants.L. Denmark. 49: 844–849. 367–381. 1981–1990. Gollasch and S.S. Van der Wal and J. Marine introductions in the Shark Bay World Heritage Property. Received 22 December. Poll. Mar. Olenin. Cons.C. Biological invasions. Fergus. A. Hewitt et al. Womersley. Ward. 1999.J. pp. Uting and I. 1990.S. S. Williams. London. Longman. 2006 w17x . D. pp. D. 1988. Williamson. Griffiths.T. ¨ S. Smith. 1996. 2004. I. E. Leppakoski.L. In: (E. ICES Cooperative Research Report 231. pp. C.B. eds) Status of introductions of non-indigenous marine species to North Atlantic waters. Hewitt.J. M.D. F.L. Shelf Sci. UK. Kelly. Western Australia: a preliminary assessment. Munro.D.. Biogeography of Australasian marine macroalgae. Wotton.. 2005. Clayton and R. 26: 409–420.: Accidental introduction pathways of seaweeds 337 Wallentinus. Introduced marine algae and vascular plants in European aquatic environments. C. Chapman and Hall. Wallentinus. Mar. Bull. Pederson. and E. R.S.D. Assessing the risk of introducing exotic species via the live marine species trade. ICES. Sydney. Ecol. 2005. Grosholz. Dordrecht. Coast. S.M. Preliminary reports from the Caulerpa taxifolia invasion in southern California. Ser. Weigle. In: (A. Est. impact and management.

The macroalgal species that form the basis for commercial aquaculture (mainly Saccharina japonica (J. Undaria pinnatifida. e-mail: pickering_t@usp. Saunders. Areschoug) C. The University of the South Pacific. for which relevant communities perceive their advantages as outweighing any disadvantages. Unintentional introductions attributable to aquaculture may result from escape of target species from ‘‘secure’’ culture facilities. Lane. Suva. new proposals should follow formal risk assessment and w18x Economic and social imperatives for commercial-macroalgal introductions Two main drivers can be identified for intentional introductions of macroalgae. although the global spread of U. P. viz. Townsville. DOI 10. Trowbridge 2006). Reise et al. how- . In practice. however. provided that environmental threats can be avoided.O. Introduction We review intentional introductions of commercially harvested macroalgae for stock enhancement or cultivation in a geographical location that is outside the native range. Solomon Islands 1 monitoring processes that are science-based.E. Australia 3 Solomon Islands Center. alvarezii. Posa Skelton2 and Reuben J. C. This includes both introductions from one country to another (sometimes called ‘‘exotic introductions’’) and introductions to a location outside the native range but within the same country (sometimes called ‘‘translocation’’. it does not appear that commercial species are. Porphyra species. Private Mail Bag. 2006. Druehl et G. In principle. The highest-profile cases of ‘‘invasive’’ macroalgae have mainly resulted from unintentional introductions. Fiji Islands. Mayes. Almost half of the unintentional macroalgal introductions documented in Europe are thought to be a result of transfer of shellfish for aquaculture (Wallentinus 2002).O. pinnatifida and K. These introductions took place. Sulu3 School of Marine Studies. more recently it has emerged that Eucheuma denticulatum is in fact the main culprit at this locality. Two cases are species important commercially for aquaculture. U. * Corresponding author Abstract The two main drivers for intentional introductions of commercial macroalgae are (1) increasing global demand for macroalgae and macroalgal 2 International Ocean Institute Regional Center for Australia and the Western Pacific. Large industries generating thousands of jobs and millions of dollars in income are now based upon aquaculture of alien species. States cannot take it for granted that alien species may be introduced. Honiara. increasing global demand for commercially important macroalgae and macroalgal products. as a group. and this also applies to macroalgal introductions (Schaffelke et al. 1999). Keywords: commercial macroalgae. pinnatifida beyond Asia has been caused mainly by shipping. While environmental problems from intentional introductions have been few compared with those from unintentional introductions. Kappaphycus alvarezii. and should be strongly justifiable in terms of ability to provide expected economic benefits. but it is difficult to predict which will become pests. and (2) increasing need for alternative and sustainable livelihoods among coastal communities in less-developed countries (particularly to reduce degradation of coral reefs) and in the less-developed rural areas of more-developed countries. invasive.E. translocations. The University of the South Pacific. and increasing need for alternative and sustainable livelihoods among coastal communities in rural and less-developed areas. the burden of proof and duty of care about environmental threats and protection of biodiversity is nowadays much higher than before.039 Review Intentional introductions of commercially harvested alien seaweeds Timothy D. inherently any more or less risk-prone than most unintentionally introduced species. alvarezii has been intentionally introduced to many countries for aquaculture and has been reported as invasive in one locality in Hawaii. particularly via shipping.Botanica Marina 50 (2007): 338–350 2007 by Walter de Gruyter • Berlin • New York.*. introductions.2007. international norms allow states to intentionally introduce exotic species for commercial purposes. or from introduction of non-target species (‘‘hitchhikers’’ or ‘‘stowaways’’) associated with the target species or with gear and equipment used for culture or transportation of the target species (Maggs and Stegenga 1999. and Gracilaria species) are thus the ones most likely to be intentionally introduced to other places.1515/BOT. Box 1539. Introductions of macroalgae via shipping can usually be regarded as unintentional. Stickney 2002). Aquaculture and shipping are the two main vectors for introduction of alien marine species generally. Pickering1. P. In the case of aquaculture. Box 460. Only a minority of alien species may ever become invasive. introductions of macroalgae can be either intentional or unintentional. introductions have been regarded historically as a valid means to improve production and economic benefits from fisheries and aquaculture. While attention nowadays is often focused more upon the adverse impacts of alien species. Queensland 4810.

The great majority of seaweed production is for food (as a sea vegetable) or for food additives like carrageenan. and these are the main traditional uses of macroalgae. socio-economic conditions appear right for K. or when there is insufficient information about the culture requirements of native species to enable commercialization (Stickney 2002). This occurs either when appropriate native species do not occur in a country. particularly of the eucheumoids ‘‘cottonii’’ (Kappaphycus w19x . and as pharmaceuticals or nutraceuticals. or their agronomic traits lend them to large-scale aquaculture. Macroalgal species which are now known to contain either pharmaceutical or nutraceutical agents are very widely represented among the Chlorophyta. nevertheless there is unsatisfied demand globally for macroalgae and macroalgal products.5–6 billion. harvested either from naturally growing (wild) seaweed or from cultivated (farmed) crops. A second major driver for intentional introductions. aquaculture of macroalgae for alginates does not appear economical compared with mechanical harvesting of natural resources (Jensen 1993). nutraceuticals represent a middle ground between pharmaceuticals (‘‘drugs’’) and so-called ‘‘functional foods’’. Also known as ‘‘dietary supplements’’ or ‘‘nutritional supplements’’. and the unpredictability of risk. Food products for human consumption contribute about US$ 5 billion to this figure. The demand for macroalgae and their products stems from their uses as food or food constituents. Caulerpa species. therefore. The most likely target species for intentional introductions of macroalgae will. compared with the host of candidate species that would need to be anticipated in the case of unintentional introductions. Gracilaria species. was much lower. make up the rest. Undaria pinnatifida (Harvey) Suringar. It might then be expected that the economic imperatives behind efforts to introduce macroalgae beyond their native range will also be lower than for other aquaculture species. Silva. to tropical. Kappaphycus alvarezii. and many of wide geographical range) plus the still-emerging state of research and actual products. Critchley and Ohno (1998). such as Bird and Benson (1987). Commercial demand is met by the handful of macroalgal species for which large markets already exist. and Gracilaria species. Gelidium species. The farming of seaweed has expanded rapidly as demand has outstripped the supply available from natural resources. and Codium fragile (Suringar) Hariot. and Critchley et al. Meanwhile. (2006). Undaria pinnatifida. in waters ranging from cold. The industry uses 7. These are lower-volume but potentially high-value uses of macroalgae. Substances that are extracted from seaweeds – hydrocolloids – account for a large part of the remaining billion dollars. Schmitz. miscellaneous uses. spread between the northern and southern hemispheres. Commercial harvesting occurs in about 35 countries. aquacultured food species like Porphyra or Undaria pinnatifida.5–8 million t of wet seaweed annually. Phaeophyta and Rhodophyta.’’ Only in the cases of species like Kappaphycus alvarezii or Gracilaria where large-scale propagation can be vegetative (so life cycles do not need to be manipulated in shore-based facilities) does aquaculture of macroalgae as sources of industrial raw materials seem justified (McHugh 2002). An overview of the history and recent status of global seaweed utilization is provided by a range of books and reviews. and for which either natural stocks are abundant and accessible. 2003).D. This is one basis for continued interest to introduce or expand macroalgal cultivation in a number of places around the world. while smaller. Such a small group of likely targets should greatly ease the research and risk-assessment demands posed by intentional introductions of macroalgae for aquaculture. A pharmaceutical is a substance used in the treatment of disease. Agardh) F.G. Hizikia fusiformis (Harvey) Okamura. Kappaphycus alvarezii (Doty) Doty ex P. Porphyra species. Pickering et al. very low-wage economies need to be chosen. In FAO (2004) the situation is summarized thus: ‘‘The seaweed industry provides a wide variety of products that have an estimated total annual production value of US$ 5. Of all the macroalgal biodiversity potentially available however. or easily propagated food-constituent species like Kappaphycus alvarezii. alvarezii aquaculture in remote outer islands of the Fiji Group or Kiribati. a disproportionately smaller component of value. Even then. very few species are used commercially for these purposes.C. but not in the main centers of these countries where there are a range of other competing livelihoods (Namudu and Pickering 2006). whereas a nutraceutical is a product isolated or purified from plants or other foods that is taken in a dosage (non-food) form in order to provide a physiological benefit and/or protection against disease. For example. be either one of the select few high-value. Just a few of the species listed in reviews by Baker (1984) or Smit (2004) include Saccharina japonica. This wide range of species (far wider than the range of popular edible species. Even in China. It is a general rule that aquaculture (compared with wild fisheries) is based upon relatively few species.T. Gigartina skottsbergii Setchell et N. Agardhiella tenera (J.: Intentional introductions of commercially harvested alien seaweeds 339 ever. This scarcity of suitable species for aquaculture then results in trade and translocation. Emerging new uses for macroalgae are as pharmaceuticals and nutraceuticals. Macroalgae form a large component of global aquaculture production in terms of tonnage but. Areschoug.L. demand for the main food and food-constituent macroalgal species is large and continuing to increase. through temperate. such as fertilizers and animal feed additives. McHugh (2002. since they are of lower value than other aquaculture products such as crustaceans or molluscs. and even fewer are cultivated. makes it very difficult to discern the extent to which pharmaceutical or nutraceutical uses of macroalgae may become a driver toward further intentional introductions of macroalgae. FAO (2004). Sargassum species. agar or alginates (phycocolloids). The main macroalgal species now being commercially cultivated (and hence likely to be intentionally introduced to other places) are Saccharina japonica J. Hypnea species. Gardner. in an era when awareness about possible environmental risks.

The Swedish-funded CORDIO programme (Coral Reef Degradation in the Indian Ocean) has identified Kappaphycus aquaculture as one alternative livelihood suitable for some parts of the Indian Ocean region (Souter 2000. It is a potential source of income and employment in rural areas with few other incomegenerating opportunities. two objectives were set for recent seaweed aquaculture development initiatives. even small increases in the income of marginalized or peripheral communities can make a big difference to peoples’ lives. Australia. Though strongest in tropical least-developed countries. Mexico and Argentina (Hay 1990) are well known examples. There have been multiple introductions to some countries like Fiji. In many countries of Asia. as have Malaysian academics seeking to protect the coral reefs of Pulau Bangii in Sabah (Koh et al. Providing alternative livelihoods as a means to alleviate poverty and reduce pressure on wild marine resources is now a major strategy in global initiatives to protect coral reefs (e. seaweed aquaculture projects in Asia. In Ireland. Burman) F. or as part of efforts to revive defunct Kappaphycus aquaculture projects in countries where self-sustaining populations did not establish. the environmental non-government organization (NGO) ‘‘The Nature Conservancy (TNC)’’ has worked with park authorities to establish a Kappaphycus seaweed farming industry in Komodo National Park in Indonesia (Howard 2003). Agardh. For example. 2004) lists eleven countries in the region where this species has been introduced at one time or another. the International Coral Reef Initiative).g. while the other is to create jobs in ‘‘peripheral communities in coastal areas’’ (Werner et al.: Intentional introductions of commercially harvested alien seaweeds species) and ‘‘spinosum’’ (Eucheuma denticulatum (N. both within and outside their native range. Pickering et al. but notes marked regional asymmetries including the fact that some regions are much better studied in this regard than others. however. Arguments for or against such development based upon ‘‘utility’’ in terms of contribution to national GDP by the new seaweed industry tend to under-value their potential economic impact. but none of them are of interest for aquaculture or commercial harvesting: Asian Sargassum muticum (Yendo) Fensholt introduced to the Pacific seaboard of North America and to northern Europe.340 T. either to introduce new cultivars like sacol. At least three macroalgal species are now regarded internationally as serious pests. for example by Zemke-White (2004) and Zemke-White and Smith (2006). although benefits in dollar terms will certainly be small relative to GDP. Ask 1999).S. ‘‘Cottonii’’ and ‘‘spinosum’’ cultivars have now been intentionally introduced to over 20 other countries both within and outside the native range of eucheumoids (Ask 2003. A species of the red seaweed Asparagopsis introduced to the North Sea. as alternatives to unsustainable practices that cause degradation of tropical nearshore environments. relatively few have become serious ecological pests. Alternative views about the claimed benefits and environmental impacts from Kappaphycus alvarezii introductions for aquaculture have been expressed. 2002). Africa. cultivation of macroalgae is widely perceived as one of the most benign types of aquaculture activity in terms of environmental impacts. although several have become very widely distributed and abundant in their new habitats. 2003a). and the introduction of Codium fragile ssp. and in particular is an activity that can provide income for women (South and Pickering 2006). Vahl) C. the introduction of a variety of Caulerpa taxifolia (M. and is normally compatible with traditional fishing and other subsistence uses of the inshore environment. Nevertheless the prevailing general perception that eucheumoid aquaculture is a good alternative to other much-less sustainable coastal livelihoods in coral reef areas is likely to continue to be a driver for intentional w20x introductions of the economically-important cultivars of eucheumoids. Of these species.D. has relatively little environmental impact. does not require refrigeration or high-tech post-harvest processing within the country. New Zealand. Trowbridge’s (2006) review of non-native macroalgae lists approximately 250 species reported to have been introduced to new geographic regions worldwide. Africa and Pacific islands often enjoy political and community support out of proportion to the potential contribution to GDP. despite the recent proliferation of studies using these terms synonymously. one is to meet growing market demands for macroalgae. the Caribbean Sea and the Pacific Ocean..L. probably from Australia (Elton 1958). Ask et al. The nature of commercial seaweed species: are they more or less risk-prone with respect to establishment and impact of feral populations in exotic locations? Species that readily establish and which threaten other species or habitats or ecosystems in exotic locations are termed ‘‘alien invasive species’’. 2004). can be operated at the household level. This is because. and the introduction of Asian Undaria pinnatifida to France. Howard 2003). possibly from northern Australia. Invasive species form high-density populations in which the species are structurally and/or functionally major components of the invaded communities (Trowbridge 2006). A recent review of the history of Kappaphycus introductions in Pacific island countries (Sulu et al. For this reason. the term can be subjective because it depends upon the investigator’s perspective of what constitutes ecological and/or economic harm. tomentosoides from . similar interest in macroalgal aquaculture livelihoods also exists in the less-developed rural provinces of more-developed countries. Collins et Hervey). has been demand for new sustainable livelihoods for coastal communities in less-developed countries. Not all alien species are ‘‘invasive’’. and one worth promoting to lessen exploitive pressure on fisheries/reefs and to lessen destructive practices like dynamite fishing (Zertuche-Gonzalez 1998. to the Mediterranean Sea (Meinesz and Boudouresque 1996) and most recently to southern California. Kappaphycus farming has been promoted by governments and NGOs because it requires a low level of technology and investment. Kiribati and the Solomon Islands.

In making such comparisons. so that cultivation in coastal waters of laboratory-produced propagules would be ‘‘controllable’’. pinnatifida and K. Valentine and Johnson 2004). has been publicized as ‘‘invasive’’ in one of those places. Agardh) E. In recent reviews. New wide seasonal windows for propagule dispersal owing to the potential for multiple sporophyte generations within a population. Lamouroux. pinnatifida is easily spread over long distances as biofouling on vessels or marine equipment. unlike the other non-indigenous macroalgae they surveyed. and that of 19 species introduced to Hawaii. and Hypnea musciformis (Wulfen) J. K. 2003a. USA. from the original w21x .D. 2002). Caulerpa taxifolia (in the Mediterranean Sea. is virtually impossible to eradicate. The main vector for spread of U. Note. the potential for differences of interpretation about ‘‘invasive’’ must be borne in mind. Acanthophora spicifera (M. So should the fact that a species can be ‘‘invasive’’ in some places but not in others (Trowbridge 2006). muticum (in Europe). and has had its range extended by intentional introductions and translocations for aquaculture in China (Wu and Pang 2006) and to Atlantic France from Mediterranean France (Floc’h et al.T. pinnatifida has microscopic gametophyte stages. and Caulerpa taxifolia appear on the ICUN Global Invasive Species Database’s ‘‘100of-the-Worst’’ list (ICUN Invasive Species Specialist Group. viz. California). U. Characteristics and impacts of these species that render them ‘‘invasive pests’’ are reviewed by Zemke-White and Smith (2006).issg. April 1999). that in Tasmania U.vic. and Smith et al. 2004).Y. This is a relatively small yet significant proportion of the macroalgal species introduced. Environmental risks in culturing Undaria pinnatifida Undaria pinnatifida is one of the main commercially harvested and cultivated species in Asia. It has a microscopic gametophyte stage which. tomentosoides make up the four high-profile macroalgal ‘‘invaders’’ prominent in the scientific literature. One possible explanation is that the species here has commercial value that places it in high demand. 1991). Undaria pinnatifida. Environmental risks in culturing Kappaphycus The eucheumoid Kappaphycus alvarezii. Mexico). Zemke-White 2004). that of 113 species introduced to Europe as a whole. Eucheuma denticulatum. alvarezii that are important commercially for aquaculture. however. Schaffelke et al. Valentine and Johnson 2003. It does mean that the issue of macroalgal ‘‘invasiveness’’ must be taken seriously. As described by Floc’h et al. pinnatifida is unable to displace native algae in the absence of disturbance and that formation of high density stands depends on disturbance to limit native canopy-forming algae (Valentine and Johnson 2003. 2004. http://www. it is considered invasive on the Atlantic coast of Europe and has been linked with reduction of native seaweed diversity in places like Argentina and New Zealand. 2004).org). nor is it always associated with declines in native species richness and abundance. water temperatures of the North Atlantic Ocean would be too cold for the life cycle to be completed in nature. alvarezii is still restricted to this one locality. once established in the wild. and is not known to propagate vegetatively. The decision was based upon the hypothesis that. and (in Hawaii) exotic Rhodophyta like Kappaphycus alvarezii. (2006) and ZemkeWhite and Smith (2006) point out that Undaria pinnatifida is not considered invasive in some places (such as the Mediterranean Sea). However. K. Vahl) Børgesen. How many alien seaweed species proliferate and become aquatic nuisances? Trowbridge (2006) cites Boudouresque and Verlaque’s (2002) report that 8 of 84 macroalgal species introduced to the Mediterranean Sea are now ‘‘invasive’’. but particularly by unintentional introductions to Europe. Characteristics of U. According to Trowbridge (2006). USA. Dawson. U. alvarezii was intentionally introduced to the Kaneohe Bay area of Oahu in Hawaii for aquaculture experiments in the 1970s. 1991). introduced intentionally to over 20 countries and territories including 11 in the oceanic Pacific (Eldredge 1994. pinnatifida is regarded as invasive within Asia in locations outside its natural range. Pickering et al. pinnatifida at high densities on natural substrata requires persistent mechanisms to limit native canopy forming algae (Valentine and Johnson 2005a. New Zealand. Currently. pinnatifida that contribute to invasiveness are its rapid colonization of new or recentlydisturbed hard substrata. Sulu et al. 5 have become ‘‘successful’’ (Smith et al. These characteristics mean that U. while suitable for sporophyte growth. and a propensity for colonizing floating objects (Hay 1990. S. with one environmental NGOs. Furthermore. (1991). There are no reports to suggest that U. pinnatifida (in Europe. whenever intentional macroalgal introductions are contemplated.V. the controversial case of an intentional translocation to establish a new seaweed aquaculture industry in Brittany (Floc’h et al. These species and Sargassum muticum and Codium fragile ssp. (2002) report that. Gracilaria salicornia (C. or in any of the ‘‘watch lists’’ of invasive species maintained by government agencies. or inter-governmental organizations. Publication 67. along with other risks (including the unpredictability of risk). Australia.: Intentional introductions of commercially harvested alien seaweeds 341 Europe to the Atlantic seaboard of North America (Carlton and Scanlon 1985) and to Australia (http:// www. Two indicators of risk for commercially-cultivated macroalgae is whether or not any species important for aquaculture is prominent either in the literature on invasive macroalgae. Of the above ten species there are two.b). This hypothesis subsequently proved to be incorrect. translocation to Brittany first occurred in 1983 prior to consideration of risks by the ICES Working Group on Introductions and Transfers of Marine Organisms during 1984–1989. public-awareness ‘‘watch lists’’ or publicity materials about marine invasives currently feature U. ongoing persistence of U. 27 are ‘‘invasive’’ and 9 are ‘‘very invasive’’ (Wallentinus 2002). pinnatifida to all of the new locations outside of Asia has been via shipping (as biofouling on hulls). Its sporophytes can form large thalli (1–3 m) of a type that can be considered ‘‘invasive’’ in the sense of forming high-density populations that are structurally and/or functionally major components of invaded communities.epa. Australia. Mexico and Argentina (see literature reviewed by Casas et al. Ask et al.

Fiji has two emerging problems with nuisance algae (May 2005. (2002) states that the ability to fragment readily. Thirdly. 2004). this enterprise is destroyed occasionally by severe storm events. . In these oligotrophic reef environments. There are additional factors in the Kaneohe Bay case that must be taken into account in any discussion of the risk of Kappaphycus alvarezii introductions for aquaculture. when compared with other high-profile invasive macroalgae like Sargassum muticum. alvarezii. the farmer does not know of any residual K. According to Zemke-White and Smith (2006). However. rather than an international or even national scale. 2006) and chemical evidence (the plants yielded iota. Ask 1999. First. (2006) have found that K. so the species propagates almost entirely by vegetative fragments. it was a large (3 kg). Codium fragile or Undaria pinnatifida. ˚ 2002). these took almost three decades to develop and are still at a local.asp?ids38688&navs21). though the fate of many plants is to become washed away into unfavorable habitats and perish. alvarezii at Kaneohe Bay has led to bans or restrictions upon introduction of this species for aquaculture in countries of the Caribbean Sea and Central America (Oliveira and Paula 2003. K. alvarezii are certainly not trivial. unattached callus-like mass with few apical growing points and exhibiting damage consistent with grazing by siganid-fish and sea-urchins (e. http://www. alvarezii plants rely on either entanglement or their sheer weight to stay in place. for example.G. most recently. Currently. alvarezii thallus was found (Pickering and Mario 1999). Luxton 2001). (2002) indicates that. Beach-cast material is creating stench and requires removal and burial at the rate of 4 t (wet wt) per day at the two latter resorts alone. 2002). and K. Silva has also become abundant among sub-tidal seagrass beds adjacent to hotels like the Fijian Resort on the Coral Coast. Tripneustes gratilla Linnaeus). Kaneohe Bay is an urbanized and nutrientenriched environment. so must move quickly to recover any drifting farmed plants for re-planting before they are washed away completely. 2004).D. and resorts like Beachcomber and Treasure Island in the Mamanuca Group (Timothy D. and fragments do not have the capability of re-attaching to the substratum. while in other places there are small residual populations such as in some parts of Tonga (Luxton 2001). tourism and piggeries (Lovell et al.etravelblackboard. In recent years Sargassum species have greatly increased in abundance on many coral reefs. Further.342 T. Smith et al. Many Pacific island countries attempted to cultivate Kappaphycus aquaculture during the 1980s and 1990s but did not move on to commercialization of this species (Luxton 2001) except in Kiribati. Pickering et al. alvarezii aquaculture trials resulted in the thalli dying out. K. alvarezii currently cultivated around the world. 2003b. for example along the tourismdeveloped Coral Coast of Viti Levu.C. on the other hand. While K. negatively buoyant and so unable to disperse long distances.. 2004). in response to which several macroalgal species including natives. Gmelin) P. alvarezii population in the area. A farm still operates at Kiuva. in the Solomon Islands (Pickering 2006). alvarezii plants are rare in nature. This suite of characteristics can account for its apparent inability to spread over long distances or between islands (Smith et al. owing to low numbers of sea urchins like Tripneustes gratilla (Zemke-White and Smith 2006) as a result of heavy fishing pressure. Caulerpa taxifolia. The information presented by Smith et al. alvarezii is considered ‘‘invasive’’ in Kaneohe Bay given its high abundance (up to 80% cover) on some patch reefs in this nutrient-enriched bay where it overgrows corals. recent molecular (Zuccarello et al. and to siganid fishes being completely absent from the Hawaiian islands (Woodland 1990). Alan T. unlike Undaria pinnatifida it has a very low probability of spreading as a component of biofouling communities on vessels. The publicity generated about K. Pickering. The situation at Kaneohe Bay in Hawaii contrasts with the mainly anecdotal evidence (some of which is reviewed by Ask et al. K. Ask. for example Dictyosphaeria cavernosa (Forsskal) Børgesen (Smith et al. In some of these places. disperse widely before recruitment. Sulu et al. the species implicated are native to Fiji and the problems are most likely linked to anthropogenically driven nutrient loading of near-shore waters by sugar cane agriculture. personal observations). in terms of environmental risk. alvarezii is a palatable macroalga and siganid fishes are known to exert considerable grazing pressure on both farmed and free-living plants elsewhere (see. K. Pickering personal observations). alvarezii epithet has been misapplied in much of the literature about the Kaneohe Bay problem. 2004) from other places where Kappaphycus alvarezii has been introduced for aquaculture. the entity they refer to as Kappaphycus alvarezii has the least invasive characteristics. alvarezii had been farmed continuously from 1986 to 1993) only a single K. Fiji and. the dominant invader in Kaneohe Bay is in fact E. However. Fiji Islands (Ask et al. and re-attach successfully. w22x K.g. are all hallmarks of a highly invasive vegetatively propagating species.: Intentional introductions of commercially harvested alien seaweeds point of introduction it has spread at the rate of approximately 260 m year-1 (Rodgers and Cox 1999). Zuccarello et al. alvarezii can slowly spread laterally from a point of introduction by fragmentation. alvarezii is not nearly as abundant as previously thought. For example. Second. Reproductive K. the abandonment of K. personal communication) now indicates that the K. alvarezii from Kaneohe Bay is a lineage genetically distinct from the K. denticulatum. have become ecologically dominant. 2003b) and Solomon Islands (Sulu et al. com/index. Gracilaria edulis (S. alvarezii may be said to ‘‘persist’’ but it is not ‘‘proliferating’’ (Ask et al. While the problems caused at Kaneohe Bay by proliferations of algae such as K. or else must bring in new cuttings from farms in other parts of Fiji (Timothy D. K. of the five non-indigenous invasive species surveyed in their Hawaiian study. the level of herbivory that might otherwise act as a biological control is low in Kaneohe Bay. is a robust species. because of the misidentification of Eucheuma denticulatum (another eucheumoid also introduced in the 1970s). alvarezii has not been implicated in any of these problems with seaweeds in Fiji. not kappa carrageenan. 2003a and Sulu et al. For this reason it became the subject of a research program and public-awareness campaign to eradicate it and prevent further spread. Critchley personal communication). E. during a survey of commercial seaweeds in the Kaba and Kiuva area of Fiji in 1995 (where K.

Decisions about introduction of species rest with the governments of sovereign states and not with scientists. for aquaculture projects that were under-financed.T. its dispersal and rapid establishment globally has been mainly unintentional due to shipping or to aquaculture of other organisms. propagule pressure (for example. (2007) review various factors that might assist to better predict which macroalgal species may become invasive and under what circumstances. it must have clear socio-economic benefits. Points raised both for and against are based on arguments ranging from established empirical observation to hypothetical scenarios. whether for aquaculture. owing to its propensity for spore settlement onto floating objects. The bulk of problems caused by invasive macroalgae have arisen from unintentional intro- ductions. regulatory and moral imperatives Intentional introduction of species. nutrient status of receiving waters. These three factors appear useful to predict whether a macroalga introduced unintentionally will establish and survive. While Undaria pinnatifida is certainly used for aquaculture in Asia and in France. This will continue to be controversial. From the information currently available. Pickering et al. and must have regard to international norms and to possible responses from the international community or neighboring states.issg. Zertuche-Gonzalez 1998. No useful generalizations have emerged from consideration of these factors. or commercially. alvarezii for aquaculture. However. scientific research or other purposes. degree of anthropogenic modification of environments. and is destined to become a classic example of the differential application of the Precautionary Principle available to states under international law when competent authorities weigh up the benefits and risks of intentional exotic-species introductions. either by shipping. economic and political considerations in assessing whether to accept or reject proposals for introduction. Laminaria and Porphyra species have similar reproductive (and hence potentially bio-fouling) characteristics. but this species is not completely without risk as is shown by the Kaneohe Bay experience. Competent authorities will take into account not only scientific advice but also social. Oliveira and Paula 2003) or against (for example. But what of the future? What new species may be targeted for intentional introductions. The record so far shows that intentional introductions of commercial macroalgae for aquaculture have caused few serious effects (Eucheuma denticulatum. alvarezii introductions for aquaculture will be fertile ground for further research. always uncertain. however. as for any exotic-species introduction. without capturing any of the anticipated socio-economic benefits against which they had balanced this risk. the aquarium trade. and have been unintentionally introduced to places by the same vectors. and the invading species’ environmental tolerances. these factors are all ‘‘givens’’ in the case of an intentional introduction for aquaculture (after all. These include possible connections between invasiveness and the latitude of introduction. Zemke-White and Smith 2006) regarding K. suitability of the habitat. Policies and norms concerning introduction of species are found in a number of the international conventions. Trowbridge (2006) and Valentine et al. one well-justified and one less-justified. political. States are not unfettered in the exercise of their sovereign right to introduce species however.: Intentional introductions of commercially harvested alien seaweeds 343 Do commercial species of macroalgae pose enhanced environmental risks? Regarding the question ‘‘are commercial species more or less risk-prone’’ than other it is possible to construct cases either in favor (for example. will always have an element of associated risk. and so these ventures were set up to fail from the outset (Ask 2003). and two important unknowns are the impact of the alien species on the recipient community. and what species already introduced may result in unforeseen problems emerging over longer time-frames? Environmental risk associated with the introduction of any commercial macroalgae is. not Kappaphycus alvarezii. (2006). Ask 1999) or environmental risks (for example. growth and reproductive characteristics. species diversity of the receiving community (but see also Dunstan and Johnson 2007). Risk management and risk mitigation of intentional introductions of commercially harvested exotic macroalgae Environmental. There are now many cases of K. grazing pressure by herbivores. w23x . no one will want to introduce a species for aquaculture that is not going to survive) so they are not necessarily predictors of whether a commercial macroalga will become an ‘‘invasive pest’’ in the sense of causing negative environmental or socioeconomic impacts. that anytime a species is introduced intentionally. often without quarantine protocols in place. Schaffelke et al. By so doing. at Kaneohe Bay has recently emerged as the main example). at nodes for inter-regional vectors such as ports). The guidelines and advice provided by McHugh (2002) and Ask (2003) for anyone contemplating establishment of new eucheumoid cultivation projects are worthy of careful consideration. The characteristics of Kappaphycus alvarezii render it much less likely to become invasive. Verification of the various claims made about socio-economic benefits (for example. and its performance in the new ecosystem. but are not reported to be ‘‘invasive pests’’ in the sense of Trowbridge (2006). alvarezii having been introduced. these states expose themselves to the full extent of potential environmental risk.D. Advocates for and opponents against intentional Kappaphycus alvarezii introductions will agree. or without guaranteed markets. Zemke-White and Smith 2006) introduction of K. and previous success in other invasions (www. apart from propagule pressure. or by ‘‘hitchhiking’’ with other organisms introduced for aquaculture (Oliveira and Paula 2003). socio-economically or institutionally unsound. the answer is that two of the main commercially-cultivated species have gained a high profile for invasiveness. Any introduction poses a potential threat to the ecosystem.

This leaves states to grapple with application of a precautionary approach. here we highlight the FAO Technical Guidelines for Responsible Fisheries 5: Aquaculture Development (FAO 1997) because these explicitly contemplate intentional introductions of commercial species. revision. persuaded. It is implicit in these guidelines that states do not regard intentional introductions of species as completely prohibited.3. . These countries need assistance from their more developed counterparts or regional/international organizations to increase their capacity for compliance with international norms. non-target species). however. A country’s ability to carry out the elements of the code will depend upon the state of knowledge on its human and aquatic communities and on the financial and human resources available. • Notify international organizations and neighboring States.2 in FAO (1997) encapsulate the international norms on introduction of species as follows: ‘‘Basic elements of codes of practice such as ICES include: • A proposal to introduce a particular species in a particular area for a particular purpose. • An independent review of the proposal by competent authority. First. pressured and cajoled into adopting and implementing these guidelines. governments should request aquaculturists to: • Create a fish health management program including quarantine and disease diagnosis. and many states should. given that any introduction will have risks against which prevention is the best defense. before introducing nonindigenous species into transboundary aquatic ecosystems’’. w24x The annotations to Article 9.2. and (3) the genetic impact of alien species (ICES 1995). It is expected. risk mitigation and management of intentional introductions has often been poorly implemented (Zemke-White and Smith 2006). Second. This Code of Practice seeks to address (1) inadvertent coincident movement of harmful organisms (that is. While these are described more fully by Doelle et al. financial and human resources in many countries (particularly less-developed countries) are insufficient to fully implement all the measures now deemed appropriate. as appropriate. and this increases scientific and public uncertainty about the outcomes of control actions (Thresher and Kuris 2004). there is a dearth of floristic surveys for some regions. The FAO Technical Guidelines principles on species introductions include: • Article 9. the FAO guidelines are not legally binding but do carry moral force as an embodiment of international norms.3 ‘‘States should consult with their neighboring states.: Intentional introductions of commercially harvested alien seaweeds guidelines and codes of practice that have stemmed from the Law of the Sea Convention and Chapter 17 of Agenda 21. Pickering et al.D. adoption and implementation of international codes of practice and procedures for introductions and transfers of aquatic organisms’’. and so it can be problematic to ascertain the status of a species as alien or otherwise and to assess the impact of an intentional introduction once it establishes as a feral population. and the main issue for resource managers is to have in place mechanisms to assess risks and benefits and. they are likely to also take into account the opportunity costs of not allowing the activity.3. and this can be attributed to a variety of reasons. as a first step. Doelle et al. A significant problem is that information on the biology of most marine taxa is relatively limited. In so doing. the review should include ecological and socio-economic risk assessments. States should be urged.’’ Managing intentional introductions in practice These guidelines provide a useful framework for states to adopt when contemplating intentional introductions for aquaculture. While conventions are binding upon those states that are signatories. The FAO Guidelines hold up the ICES Code of Practice as a model for those states or regions that have not yet adopted any guidelines for species introductions (FAO 1997). strategies to manage the introduction in a way that maximizes the benefits and avoids. marketing surveys can help determine the cost-effectiveness and target consumer for a proposed introduction. Demand to introduce species for aquaculture can therefore be expected to continue. decision makers would have to engage in the difficult task of weighing the risk against the utility of the proposed activity. While international instruments like the FAO Guidelines can be criticized for being non-binding and for pitting ‘‘utility’’ against ‘‘prevention’’.344 T. For the same reason. Faunistic and floristic surveys of local aquatic ecosystems can help determine what local species may be affected by aquaculture development and what local species may be utilized instead of importing an alien species. base their policies upon them. the fact remains that the burden of proof and duty of care regarding environmental threats is now much higher than it was until a decade or so ago. (2007).2 ‘‘States should cooperate in the elaboration. that decisions whether or not to introduce should be made in accordance with codes of practice regarding risk assessments. (2) ecological and environmental impacts of the target species. and • Article 9. or acceptance of the proposal. (2007) note that prevention of unintentional introductions by placing a prohibition on some activities like shipping is simply not possible owing to its utility to society. most of the intentional introductions of macroalgae predated the development of current norms on exotic species introductions. For marine macroalgae. and • Rejection. Socio-economic information on the fishing sector and on the fish-consumers will also help identify those people benefiting or at risk from aquaculture development. Once an introduction has been approved. however. remedies or mitigates the risks. if the decision is affirmative. safeguards and procedures to avoid environmental threats. • Monitor and evaluate ecosystem and socio-economic effects. In addition. while for other less-compelling activities like intentional introductions for aquaculture.

Porphyra. so was not given high ranking among research priorities (Zemke-White and Smith 2006). Fourth. and if necessary should be provided with assistance to develop capacity for their implementation. the reasons given for this were usually either that funds were not available for the research. Great Britain and Switzerland) have adopted implementing legislation relating to deliberate introductions of alien species. There are few well documented examples of risk assessment for intentionally introduced marine macroalgae: well documented case histories. or funds were not allocated because K. and there is little literature on effects that these introductions may have had on the recipient community’s structure or function. 2004). and no authority is designated to assess risks ‘‘w«x which leaves the door wide open to whatever interpretation the country concerned considers (rightly or wrongly) to best suit its interests. For those regions that are relatively well-known. USA. New Zealand. mainly because current species inventories are incomplete or recent. as pointed out by Ribera and Boudouresque (1995). eradications of macroalgae once established are very difficult and expensive. such as those for Kappaphycus alvarezii.D. but there is scope to improve recommended protocols further. Pickering et al. Proposers of introductions relying upon containment measures must do so on the assumption that there will be escape and establishment in the wild (Stickney 2002).’’ While states are now clearly expected to move in the direction of giving teeth to recommended practices and protocols. or for follow-up monitoring (Schaffelke et al. however. the introductions. suitable native species will either be unavailable or have agronomic or marketing constraints. Canada. most cases of post-introduction monitoring have been done over relatively short time-scales following an unintentional or intentional introduction (Trowbridge 2006). there will be some species appropriate for introduction. Germany. because of site. Schaffelke et al. a further problem. The Convention on Biological Diversity recommends a hierarchical approach. EU directives legislate for the protection of ecosystems against the adverse effects of aquaculture-related introduced organisms (for detail see Zenetos and Strefaris 2004). While environmental threats from intentional introductions of commercial macroalgae have been few compared with those arising from unintentional introduction by other vectors such as w25x . In Europe alone. and have been successful in only very few cases where the response was rapid and the timeframe since introduction very short (for example. 2006). alvarezii was not seen as a major environmental threat. based primarily on the prevention of unwanted introductions. rather than before. While introductions are governed by international norms. in some place. States in other regions need to be encouraged to adopt similar measures.or time-specific factors and lack of ecological principles with general application (Schaffelke et al. is that texts in various conventions and agreements are generally couched as recommendations.) C. Third. and instead develop suitable native species for aquaculture. Progress is being made. cit. a total of 124 alien species (some of which are macroalgae) have been introduced in association with aquaculture activities (Zenetos and Strefaris 2004). This whole issue is difficult because. states in several regions lack the capacity for baseline ecological studies prior to introductions.T. New Zealand. 2004). and extend them to other target species. the fact remains that only a few countries (Australia. of Undaria pinnatifida from the hull of a sunken vessel at Chatham Is. These authors (op. while impacts of the high-profile invasive species have engaged many researchers’ interest after they have become established.) note that the rate of introductions has been declining recently. and numerous studies on these species are now completed. and Trowbridge (2006) have reviewed the risks associated with invasive macroalgal introductions. (2006). Saccharina japonica and Macrocystis pyrifera (L. Understanding one introduction does not necessarily enable prediction of other introductions of the same species. States balance ecological risk against socio-economic benefits. in many cases.. 2006). 2006). According to Zemke-White and Smith (2006) there are no published reports that any baseline floristic studies have been taken prior to the introduction of macroalgae for aquaculture purposes. Sulu et al.: Intentional introductions of commercially harvested alien seaweeds 345 Ribera and Boudouresque (1995) noted that it is relatively difficult for many regions of the world to recognize which species have been introduced. 2006). 2003a. The only certain way to ensure there is absolutely no risk from a macroalgal introduction is not to introduce it. suggesting that European Union measures are becoming more effective. It is no coincidence that 51% of marine macrophytes introduced into Europe were first introduced in France where legislation controlling introductions of alien species is relatively lax. Further. the capacity to predict environmental effects is poor. and noted that there is no correlation between particular groups (Orders) and the levels of associated risk. and no state has ruled out the possibility that at some time. reflecting the fact that invasion biology is a complex and relatively new area of study (Trowbridge 2006). Agardh illustrate the fact that the issue of risk came after. Identifying low. Fifth. In the case of Kappaphycus alvarezii.and high-risk species Schaffelke et al. whereas surveys decades after introduction may yield different outcomes because the impact of an alien species may change over time (Schaffelke et al. The Berne Convention in 1979 provides that ‘‘w«x each contracting party undertakes w«x to strictly control the introduction of nonnative species’’. there has been very little research to support development of appropriate quarantine protocols for intentional or unintentional macroalgal introductions associated with aquaculture (Ask et al. and because many authors are reluctant to specify whether certain species are introductions. This is an issue that the Aquaculture Programme of the Secretariat for the Pacific Community has begun to address on behalf of its member states (Sulu et al. introductions comprise 4–5% (Mediterranean Sea) to 2–3% of the known flora (Ribera and Boudouresque 1995). however. Thresher and Kuris (2004) have noted that eradication of marine invasive species in gen- eral has a low probability of success once the invaders are well established. For many countries.

with unpredictable consequences. however.g. 2003a. possessing intermediate characteristics of both low. physical surface cleaning. a microscopic epibiota possibly including harmful dinoflagellates. very little research has been directed at development of quarantine protocols for macroalgae. quarantine procedures such as washing.346 T. high-risk species remains largely arbitrary for marine macroalgae.D. those other vectors. They also showed. demonstrates the complexity of this issue (summarized in Sulu et al. A detailed case-history of quarantine for Kappaphycus alvarezii aquaculture and transportation to various countries in the Pacific Islands region is provided by Sulu et al. In Table 1 we suggest some of the criteria potentially useful in the determination of low. States are urged to develop quarantine protocols for the species of macroalgae most likely to be proposed for introduction. for example by utilizing criteria like those in Table 1 or like those reviewed by Schaffelke et al. Low-risk • • • • Does not cause serious impacts to the environment Reproduction and life-cycle non aggressive Life-cycle stages can be controlled or manipulated Not known to out-compete local species when released High-risk • • • • • • • • Causes serious impacts to the environment Aggressive reproduction and life-cycle Complex life-cycle that is difficult to control or manipulate Grows rapidly in a new environment and displaces local species in the wild Out-competes local species for space and habitat Possesses mechanisms aiding dispersal such as vegetative propagation Potential high cost of eradication Lack of natural predators in its new environment • Relatively easy to remove/discard if no longer desired • Lacks mechanisms or strategies (e. no introduction of commercial macroalgae will be completely without risk and it may be difficult to predict what the actual consequences will be. placement in holding tanks using closed water systems for an observation period can allow detection of ‘‘hitch- Table 1 Criteria to determine the potential risk factors of deliberately introduced macroalgae.vs. Pickering et al. a modicum of forethought to the application of simple and low-technology protocols can go a long way toward reducing ecological risk. Quarantine can thus play a vital role in reducing the risk of introductions of unwanted species and pathogens associated with host aquaculture species. this should be attributed more to the much greater propagule pressure posed by. Risk assessment procedures have resulted in some proposals for introduction of commercially valuable species to be declined. alvarezii (but now known to be Eucheuma) is regarded as a serious pest at one location in Hawaii (Zemke-White and Smith 2006). although the complete removal of micro-organisms or endophytes is virtually impossible (Sulu et al. Those states that have paid attention to quarantine matters have usually resorted to ad hoc approaches. unintentional introduction of non-target species (sometimes termed ‘‘hitchhikers’’). The determination of low. Thus. A number of intentionally introduced algae. washing with seawater) and quarantine procedures can greatly reduce this risk. 2004). do not match all criteria in either category. It is possible that this species could otherwise have colonized the European Atlantic coast from Spain to Norway.: Intentional introductions of commercially harvested alien seaweeds shipping. The historically lower threat posed by intentionally introduced species is not a result of their being intrinsically any more or less risky than unintentionally introduced species. Sulu et al. While K. For example. mild chemical treatment or washing in freshwater may be effective in the removal of larger fauna and flora. (2004). While there are a small number of examples where quarantine measures have been applied to K.g. For example. vegetative propagation) aiding its dispersal • Causes minimal economic and health costs • Has natural predators to help keep it in check w26x .and high-risk species. and later into the Pacific Islands. then grew a second generation of cultures from those plants before releasing K. grew plants. For seaweeds like Kappaphycs alvarezii with a relatively simple growth habit. Quarantine and farm procedures to minimize risk Quarantine procedures address the issue of inadvertent coincident movement of harmful organisms. (2006) and Trowbridge (2006). that relatively simple propagule selection. high-risk species. smaller seaweeds attached as epiphytes. Sulu et al. This was the procedure followed by Brazilian authorities when they introduced K. alvarezii has failed to establish in many localities in the Pacific Ocean where it was introduced (Eldredge 1994. treatment (e.vs. and potentially any disease organisms within the seaweed tissues. The introduction of Eucheuma/Kappaphycus from the Philippines into Hawaii. plans to introduce the giant kelp Macrocystis pyrifera into Europe in the 1950s and 1970s were dropped because of public protests and a recommendation from ICES (Boalch 1981). that is. 2003a.. They imported axenic cultures. alvarezii into the sea. 2004). and hardly any protocols or guides to best practice are available for macroalgae. Unfortunately. (2004) showed that Kappaphycus alvarezii shipped to new loca- tions may contain fauna such as copepods. K. While it is possible to identify macroalgal species that pose higher or lower levels of risk in terms of undesirable environmental or socio-economic impacts. 2004). it is clear that in the majority of cases no quarantine protocols have been applied. amphipods. For quarantine of whole plants of Kappaphycs alvarezii. alvarezii (Ask et al. cultured apical tips in agar. site-specific information is needed since the same species may behave quite differently in different environments. Ask et al. alvarezii. and much greater difficulty in regulating. however.. Sulu et al. However. The process took about four years and required fairly sophisticated laboratory facilities (Oliveira and Paula 2003). An alternative is to translocate just apical tips of the plant and then grow these at the new location using tissue culture methods. isopods or polychaete worms. 2004).

The majority of these countries lack legislation regarding introductions or it is sketchy. Once a species has been introduced and the quarantine period has ended.. to confine it to the aquaculture site and prevent it from becoming established in the wild as self-sustaining populations or spreading to other areas. Depletion of natural stocks of seaweeds is a much less significant issue because many stocks are inaccessible to fishing (e. risk). personal communication). and the massive public awareness campaigns carried out in Spain. which brings the twin benefits of avoiding damage to corals. Kappaphycus alvarezii plants in off-bottom culture can abrade and damage living corals that they contact (Zemke-White and Smith 2006). and ought to address all issues of environmental risk at the pre-introduction risk assessment stage of any proposal. As mentioned earlier. and maximizing economic gain (Watson et al. Proposers and resource managers would be prudent to assume that any marine species. Ribera and Boudouresque (1995) stress the importance of raising public awareness of the risks involved in species introductions. Usually these can be avoided.) or vessels do not harbor the macroalga through entanglement or biofouling before they are taken to other places. this very inaccessibility can be one driver for increased production through aquaculture in order to meet demand.. For most of these developing countries. New Zealand. as was done in Fiji in 1984 (Sam Mario. expectations are increasing that states should exercise a much greater w27x . and reducing herbivory of the cultivated macroalga by fishes which are often much more abundant around corals and in seagrass beds.spc. Pickering et al. once introduced. Australia. However. or they perceive aquaculture of an alien macroalga as preferable to alternatives such as continued unsustainable livelihoods or destructive practices associated with coral reefs. In other countries with greater capacity for coastal-management and weaker economic imperatives (for example. remedied or mitigated by appropriate farm management practices. with the majority of the recipients being developing countries. The Aquaculture Programme of the Secretariat for the Pacific Community is now raising awareness among member countries about the need for quarantine protocols in aquaculture (www. published in 49 languages. particular farm procedures may sometimes be applied to further minimize environmental risk. the ‘‘utility’’ of commercial production often takes precedence. There is a growing literature on ways to reduce the risk of unintentional translocation of Undaria pinnatifida. 2000). USA). further intentional introductions of non-indigenous macroalgae are now almost impossible. and as a consequence aquaculture is increasing (FAO 2004). and the resultant guidelines are being built in to publicity materials and awareness campaigns.T. Gunthorpe et al. These are usually directed at containment of the introduced in the example of the proposed introduction of Macrocystis pyrifera to Europe. alvarezii plants can greatly deteriorate in enclosed systems over two weeks. The health of K. In these countries. and this can be done in relatively simple land-based tank systems with daily water exchange provided by pumping seawater from an adjacent shore. and potentially serious ecological impacts can be averted. One component of environmental risk from introduction of a macroalgal species for aquaculture is the risk of adverse effects from the farm activity itself. because estimates of the temperature limits for reproduction of this species were incorrect. they lack the capacity to conduct meaningful baseline surveys or monitoring. One practice has been to propagate the target macroalga under controlled conditions onshore. This observation time could be safely shortened to 7–10 days if washing and/or chemical-dip treatments precede the observation period (Sulu et al. and that during that time they should be checked for the growth of microalgae and animals on the thalli. The rapid depletion of natural fish stocks through over-fishing in most parts of the world is placing increasing pressure on governments to seek alternative means of production. pinnatifida via mussel-farming equipment in Australia. For example. Zemke-White (2004) recommends that plants should be maintained for at least two weeks in a contained system. The majority of marine plant aquaculture (and thus the movement of organisms from country to country) is centered in SE Asia. and is taking steps to develop guidelines for best practice. Seed stock from this region has been used to establish aquaculture operations elsewhere.g. floats etc. These will always be political rather than purely scientific decisions. For example. where there are real or potential conflicts between risk mitigation and commercial production. (2001) report on tests of protocols to avoid spreading U. 2004).: Intentional introductions of commercially harvested alien seaweeds 347 hikers’’ or disease on the imported plants. however. economic potential has almost always taken precedence over ecological concerns. Risk of spreading the introduced macroalga to other areas away from the farm can be reduced by taking care that seaweed farm equipment (ropes. Water exchanged from this kind of quarantine system should be chlorinated and discarded at least 500 m from the coastline to ensure that no aquatic organisms escape into the local ecosystem. Italy and France on the invasion of Caulerpa taxifolia (see Meinesz 2007). will not be successfully contained. Caulerpa taxifolia and Sargassum muticum. then carefully select grow-out sites where environmental conditions are suitable for growth but not for reproduction (usually by virtue of unsuitable temperature and/or daylength regimes). deliberate introductions can be prevented in the face of public pressure and scientific advice.D. This approach was not successful in containing Undaria pinnatifida on the French Atlantic coast. This can be avoided through selection of farm sites on clean-bottomed sandy areas away from either corals or seagrasses (Ask 1999). Good examples of public awareness initiatives are the brochures distributed to people arriving in Australia explaining the main Australian quarantine regulations.e. Conflicts between risk mitigation and commercial production The intentional introduction of organisms for the purpose of aquaculture requires a balance between minimizing ecological impact (i. because they are located on exposed rocky coasts with high wave action). However.

A risk management framework should result from a risk analysis process. where they exist.. Invasions 6: 411–416. 2004) that might perhaps reduce the risk by 99%. 382. Boudouresque.. A risk management framework is a useful tool to identify gaps in knowledge or shortcomings in capacity. Piriz. members of the World Trade Organization (WTO) are required to use formal risk analysis to justify any restrictions on international trade based on risks to human. Poll. animal or plant health (WTO 1994). in order to completely eliminate the risk of introducing associated microbiota. 10: 657–667. or where permission for the introduction is granted but with onerous conditions attached. 2006. Casas. Amsterdam. Three decades of Kappaphycus alvarezii (Rhodophyta) introduction to non-endemic locations. and to highlight the most pressing issues. Bot. Biol. Yokosuka. Int. C. Developing the cottonii (Kappaphycus alvarezii) cultivation industry in the Fiji Islands. Benson. International Cooperation Agency.L. For the majority of deliberate seaweed introductions. Creating a sustainable commercial Eucheuma cultivation industry: the importance and necessity of the human factor. Orr (2003) provides a copy of the Organism Risk Assessment Form (including uncertainty reference w28x codes) which is the main decision support tool of that assessment. Erik I. Acknowledgements The authors are indebted to Alan T.T. and to Shital Swarup for assistance with literature searches and interloans. 2004. However. Seaweed Symp. de San. Bot. Doelle. Proc. E. the risks have proved to be relatively small and conflicts between risk mitigation and commercial production have not been an issue.I. developed by the US Aquatic Nuisance Species Task Force in 1996.T. eds. Verlaque. Proc.T. 1985. Ask. 2003a. and J. and prioritization in the delivery of control mechanisms and in contracting of scientific research (Hewitt et al. Batibasaga. The invasive kelp Undaria pinnatifida (Phaeophyceae. Bull. Boalch.I. Monitoring should be an important part of risk mitigation however. Seaweed resources of the world. Seaweed Symp. E. Int.R. such as that being carried out with introductions of Porphyra yezoensis Ueda from Japan to the Atlantic coast of the USA (Watson et al. The US system provides the necessary guidelines and tools for the development of a risk management framework for marine macroalgae.348 T. Invasive seaweeds: global and regional law and policy responses. Even (or perhaps. 2007.D. Pickering et al.: Intentional introductions of commercially harvested alien seaweeds duty of care and impose a greater burden of proof upon proposers of introductions than was the case twenty or even ten years ago. 2003b. Int. Ledua. Ohno and D.L. Biological pollution in the Mediterranean Sea: invasive versus introduced macrophytes.T. 2000).. and M. Decision support tools and other formal risk management frameworks Governments are cautious with aquaculture enterprises involving the introduction of exotic species into a new environment. especially) under circumstances where there is lack of knowledge.A. A. Ohno. eds. McConnell and D. Mar. Batibasaga and S. the process has some uncertainties about methodology. Orr (2003) describes a detailed risk analysis review process for non-indigenous aquatic organisms. University of Amsterdam (CD-ROM series). and P. tomentosoides (Chlorophyta) on the Atlantic coast of North America. Bird. although the complex infrastructure and taxonomic expertise required for the task is lacking in most countries where seaweeds are brought in for aquaculture purposes. as occurred in Brazil (Oliveira and Paula 2003). pp. J. M.. Zertuche-Gonzalez and M. Expert Centre for Taxonomic Identification (ETI). K. M. In cases where commercial production does not take precedence.O. 1981.. 1998. Critchley. eds. 52. The risk analysis process takes into account risk management and appropriate actions necessary to mitigate the risks’ impacts. E. . VanderZwaag. Chapman and Craig Johnson for providing comments on this manuscript. A. Japan. 429. 2004) which continues to be the main vector for macroalgal introductions owing to technical constraints and powerful lobbyists. M. Proc. limited capacity and low funding. Ask. Argentina).T. 17: 13–18. A. A hypothetical example might be if a jurisdiction were to require four years of high-technology tissue culture before Kappaphycus alvarezii propagules can be released from quarantine. can best be solved through transparent and accountable decision-making processes by competent authorities in which there is wide and meaningful consultation and participation by relevant stakeholders. Baker. 1984. Robin South. Seaweed Symp. G. if necessary. Ask. Elsevier. J. The aquaculture sector is a relatively easy target for regulators compared with the shipping sector (Hewitt et al. A. Critchley. R. Largo. human error or the biology and environmental requirements of the organisms.H. 1987. Seaweed cultivation for renewable resources.A. Seaweeds in pharmaceutical studies and applications. FMC Corporation. Cameron Hay. pp. Scrosati and M. the benefits in developing a risk management framework include identification of the core values that need to be protected. Progression and dispersal of an introduced alga: Codium fragile ssp. Cottoni and spinosum cultivation handbook. Conflicts about macroalgal introductions. and M. G. Do we really need to grow Macrocystis in Europe? Proc. Critchley A. 1999. In addition. 2004). Laminariales) reduces native seaweed diversity in Nuevo Gulf (Patagonia. E. compared with a two-week low-technology quarantine protocol (Sulu et al. Int. Seaweed Symp.I. 28: 155–165. 2007). The review process provides a standardized means for evaluating the risk of introducing non-indigenous organisms into a new environment and. due to potential adverse impacts on native flora and fauna (see Doelle et al.I. 17: 49–58. and it should be seen as a constantly evolving system that takes into account new information derived from research. Carlton.F. Ask. References Ask. Mar. Scanlon. Hydrobiologia 116/117: 29–40. Seaweed resources. G. 2002. 50: 438–450. Mar. Philadelphia. J. determining the correct risk management steps needed to mitigate that risk. the conflict becomes one where communities may have an opportunity cost imposed upon them either by an appropriate introduction being declined. E. pp. Mario.T. 44: 32–38. 17: 81–86. 2003.

205–220. 2000. December 2003. Rome. L. Introduced macroalgae – a growing concern.D. A guide to the seaweed industry.S. C. Ecol. 1999. Gollasch and W. Ser.-F.A. Marine and Freshwater Institute. pp. 153. Expert Centre for Taxonomic Identification (ETI). Boudouresque. Lovell. Fiji. and C. Biol. Koh.P. J. The dispersal of sporophytes of Undaria pinnatifida by coastal shipping in New Zealand. The state of world fisheries and aquaculture (SOFIA). A. Wolff. Mario. Science et Vie 319: 603–613. 18: 241–249.R. 1996. CABI Press. 2007. eds) Responsible marine aquaculture. In: (J. C. Jones and archive/newsoct2000. In: (C.J. Nauru. FAO. In: (R. 2006. ed. Pakoa. J. International Council for the Exploration of the Sea. 48. J. Proc. 48: 106–115. 285: 43–55. and Gracilaria salicornia and their current distributions in Kane’ohe Bay. Exotic seaweeds: friends or foes? Proc. pp. 84. 1995. Theodoropoulos. Explor. C. Establishment of the introduced kelp Undaria pinnatifida following dieback of the native macroalga Phyllospora comosa in Tasmania.D. The Japanese brown alga Undaria pinnatifida on the coast of France and its possible establishment in European waters. and implications for further dispersal of Undaria in France. Australian Institute of Marine Science. pp. Australia. pp. Res. Helgol. Stickney and J. Copenhagen. Smith. New Caledonia. 2006. Johnson. A. Survey of commercial seaweeds in south-east Viti Levu (Fiji Islands): a preliminary study on farming potential of seaweed species present in Fiji. Hawaii. FAO. 56: 299–315.T. University of Amsterdam (CDROM series). 2003.D. The ecology of invasions by animals and plants. Pickering. Br. A. 2007. 1994. Denmark. Options for managing invasive marine species. Jensen. 16: 245–262. 1997.. and C. Samuelu. C. pp. J. 181.R. and C. Wallingford. Johnson. C. 1. Appl. Exp. Suva. Hydrobiologia 260/261: 15–23. J.17: 41–47.E.P. Wantiez.D. Biol. Trowbridge. Washington. Mar. J. Ruiz and J. Appl.reefbase. 557. 2006. pp. pp. 50: 361–372. 25: 301–313. Pajot and I. Critchley. Orr. A. Pac. and E. Meinesz. On the origin of Caulerpa taxifolia in the Mediterranean Sea. Hunter and C. J. Int. Wallentinus. based on surveys in June 2002. Boudouresque. 11: 187–268. Noumea. Ohno and D. D. Stegenga. Deiye. 40. Appl. B. R. Res.L.: Intentional introductions of commercially harvested alien seaweeds 349 Dunstan. Poulasi. R. 2006. Cons. Gunthorpe.) Status of the coral reefs of the world: 2004. J. Hewitt. Smith. 105. Mar. J. Pickering. L. Status of coral reefs in the South West Pacific: Fiji. J. M. 2004. Int. E.M. Helgol. 1999. FAO. 18: 529– 541. D. pp. G. Kuris. M. Phycol. D.M. Sulu. S. pp. M. Island Press. 46. 2006.. pp. Townsville. Solofa. K. Maggs. Persistence of the exotic kelp Undaria pinnatifida does not depend on sea urchin grazing. Mer. South Pacific Regional Environment Programme Report Studies 78: 1–127. Introduced marine plants. w29x . Red algal exotics on the North Sea coasts. Rate of spread of introduced rhodophytes Kappaphycus alvarezii. N. J. 13 March. 1958. Hay and T. 52: 243–258. Phycol.. October 2000. Elton. Coral reef degradation in the Indian Ocean. Smit. Thresher. Rome. C. Cox. pp. T.. 38: 429–438. Namudu. Bot.M. and C. New Caledonia. 2004. Hay. J. Methods for identifying and tracking seaweed invasions. Cox. The Food and Agricultural Organisation of the United Nations.R. Generic nonindigenous aquatic organisms risk analysis review process. L. 2005b. 2004. R. A. McVey. Virly. London. 2004. Secretariat for the Pacific Community. In: (A. The status of coral reefs of Pulau Banggi and its vicinity. Ohno and D. FAO Fisheries Circular No.T. M. Food and Agricultural Organization of the United Nations. Phycol. L. K. FAO South Pacific Aquaculture Development Project (Phase II) Field Document No. Int. Wotton. Res. Issues associated with nonindigenous species in marine aquaculture.C. Kumar. Secretariat for the Pacific Community Women in Fisheries Information Bulletin 13. M. Valentine. and A.J. A.T... and C. 415–538. The seaweed resources of the Pacific Islands. T. 2003. with special reference to macroalgae: mechanisms and impact.17: 87–93. L. Appl.F. Ecol. New Caledonia. Introduced marine species of the North Sea coasts. Meeresunters. http://www. Rodgers. Marine and Freshwater Resources Institute Report No. Bauckham.A. 2003. Freshw. Wilkinson. 2005a. Phycol. J. R. pp. 53: 232–241. J. eds) Invasive species: vectors and management strategies. 18: 227–234. Meeresunters. 1993. When fishing grounds are closed: developing alternative livelihoods for fishing communities. Mar. M. Howard. S.K. Mechanisms of invasions: can the recipient community influence invasion rates? Bot. Kappaphycus agronomy in the Pacific Islands. Kappaphycus striatum. H. Sulu. 1. New Zealand marine biosecurity: delivering outcomes in a fluid environment. Noordeloos. Seaweed Symp. C. Tuvalu and Vanuatu. Pickering et al. Reise. Invasions 6: 295–300. Cassidy. 1995.M. Freshw. Medicinal and pharmaceutical uses of seaweed natural products: a review. In: (A. Smith and C. J. Pickering. FAO Fisheries Technical Paper No. J. Perspectives in aquatic exotic species management in the Pacific Islands. Methuen & Co. 2003. Samoa. Rome. eds) Seaweed resources. and E. 2003. Chou and K. Rapid survey technique using socio-economic indicators to assess the suitability of Pacific island rural communities for Kappaphycus seaweed farming development. Prospects for seaweed production in developing countries.P. O’ahu. Largo. Phyc. Johnson. eds) ReefBase: a global information system on coral reefs. Hughes and R.R. Prog. Newsletter No.T. eds) Seaweed resources. Seaweed Symp. Oliveira.P.R.. Ribera. and C. Schaffelke.T..M.R. 2001. Noumea.J. A global proliferation of non-native marine and brackish macroalgae. Carlton. Largo. E. 2002. 2004. Johnson. Sci. pp. http://www.. Eldredge. University of Amsterdam (CD-ROM series). Rome. Pickering. Advances in seaweed aquaculture among Pacific island countries. 2003. 28.G. Best practices for the sterilisation of aquaculture farming equipment: a case study for mussel ropes. 41. Distribution and reproductive characteristics of non-indigenous and invasive marine algae in the Hawaiian Islands. C. In: (G. Valentine.P. ICES Code of Practice on the Introductions and Transfers of Marine Organisms 1994. Z. McHugh. A. Sci. Oliver and M. and T. Solomon Islands.D. Bot. 1990. 2001. R. 50: 373–384.R. 52: 219–234. 1999. Afzal.P. J. 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. and S. 2002. 12.F. S. Rees and T.E.E.htm.R. FAO. 19–22. Souter. Prog.cordio. Paula.Y.D. and C. Mar. Pac. Stickney.J.D. A. 55: 223–230. Phycol.L. Valentine. 968. 1999. South. 47: 379–390. Mercer. 2004. C. Present and future needs for algae and algal products. Garrigue. 441. Meinesz. A. Hewitt C. McHugh.L. T. Willing. Floc’h. Queenscliff. Sykes. 2002. 1991. Mar. Valentine. D. Mar. 2004. Sabah.H..P. Luxton. Expert Centre for Taxonomic Identification (ETI). Pickering. Tun. Critchley. ICES. L. Introductions of commercially significant aquatic organisms to the Pacific Islands. D. and H. 2002. 295: 63–90. P. Johnson.J. Establishment of the introduced kelp Undaria pinnatifida in Tasmania depends on disturbance to native algal assemblages. Mar.K. Kappaphycus seaweed in the Pacific: review of introductions and field testing proposed quarantine protocols. FAO Technical guidelines for responsible fisheries 5: Aquaculture L. and T. Sabetian.

M. Porphyra yezoensis (Rhodophyta. Ohno and D. pp. eds.J.J. WTO. 1998. C. Critchley. 27–52. World Trade Organization. Smith.. The World Bank. Watson. Strategic review of the feasibility of seaweed aquaculture in Ireland.T. Bot. 12–16 May 2002. Aquaculture as a mode of introduction. V. Mechanisms of invasion: establishment. Macroalgal cultures as a sustainable coastal livelihood in coral reef areas. Largo. Pederson) Marine bioinvasions. Introduced species in marine and coastal waters.. MA.350 T. National Development Plan Marine RTDI Desk Study Series DK/01/ 008. eds) Coral reefs: challenges and opportunities for sustainable management. Largo. Olenin. K. pp. impacts. Distribution. Leppakoski. Magierowski and C. Expert Centre for Taxonomic Identification (ETI). and J. 2007.europa.E. Proceedings of a Conference.136. Bangiophycidae) in Cobscook Bay. Malaysia: 465–476. January 24–27. Zemke-White.. 1994.C. Werner. Amsterdam.H. Agreement on the Application of Sanitary and Phytosanitary Measures.P.T. pp. In: (E. Assessment of the current knowledge on the environmental impacts of seaweed farming in the tropics. 1–9. Biomonitoring of an aquacultured introduced seaweed. Washington DC. 120. 53–54.E. and S. General Agreement on Tariffs and Trade (GATT). Pang. Hatziolos. spread and persistence of introduced seaweed populations.. Marine Institute.D. Mar. A. Maine. The seaweed resources of China. Systematics and genetic variation in commercial Kappaphycus and Eucheuma (Solieriaceae. 2006.T. Received 31 January. 69–84. Specific_media/water/indicators/WEC07b. (2004). pp.: Intentional introductions of commercially harvested alien seaweeds Valentine.E.L. G. Revision of the fish family Siganidae with descriptions of two new species and comments on distribution and biology. eds) Seaweed resources. Cambridge. Wallentinus.A. 1990. D. Lhonneur and J.Y. 2004. Zemke-White. 2004. Appl. eds) Invasive aquatic species of Europe.R. Galway. Jooten and M. J.J. and management. pp. Feodar. 1999. 1997. S. Geneva. Bishop Museum. Cheney and I. October 9–11. http://themes. Wu. Kuala Lumpur. M. 50: 351–360. Critchley. 2002. eds) Seaweed resources. Smith. pp. 2007 w30x . pp. Kraan. Zenetos. Pickering et al. Johnson. Proceedings of the Asia-Pacific Marine Science and Technology Conference. Zuccarello. Critchley. A. Ohno and D. In: (A. University of Amsterdam (CD-ROM series). A. 260–264. Indo-Pacific Fishes series No. West. Gollasch and S. Strefaris. Levine. Woodland. 2006. and N. Marine science into the new millenium: new perspectives and challenges. J. In: (M. In: (J. Univ. In: (A. Introduced marine algae and vascular plants in European aquatic environments. D. 2006. G. 18: 643–651. Zertuche-Gonzalez. Amsterdam (CD-ROM series).L. A. 2000. R. Rhodophyta).eea. D. USA.B. Clarke and S.A. Environmental impacts of seaweed farming in the tropics.05/ WEC7b_IntroducedSpecies_140504. W. I. 19. W. Proceedings of an associated event of the fifth annual World Bank Conference on Environmentally and Socially Sustainable Development. Expert Centre for Taxonomic Identification (ETI).2004. 2006. J. Indicator Fact Sheet. Phyc. MIT.pdf. In: The results of the Uruguay Round of multilateral trade negotiations: the legal texts. Honolulu. accepted 17 April. Kluwer Academic Publishers. Sieber.

In several cases there is substantial evidence for positive feedback mechanisms that enable introduced species to persist in the absence of the disturbance factor that facilitated establishment in the first place. University of Tasmania. We define establishment w31x * Corresponding author Abstract Understanding the mechanisms that facilitate or inhibit invasion of exotic seaweeds is crucial in assessing the threat posed by their incursion and to define control options. Dunstan and Johnson 2007). Hobart. Piazzi and Cinelli 2000). Informed and responsible management should attempt to identify potential ‘‘next pests’’ and mitigate against their arrival and establishment at new locations (Hayes and Sliwa 2003. if a species ‘‘tracks’’ community dynamics and requires disturbance or another facilitating mechanism to establish and persist. Tasmania 7001. . For these species that are able to ‘‘drive’’ the community dynamic de novo. Once incursions do manifest. we consider how life history characteristics of the invading species and properties of the recipient environment influence the likelihood of invasion. it is clear that disturbance is an important process in the establishment of these invasive species. Sargassum muticum and Undaria pinnatifida). once they are established.g. predictions of invasibility based on life history characters alone are unlikely to be useful. persistence. knowledge of the threat posed by an introduced species is essential to effectively prioritise species for management purposes (Byers et spread and persistence of introduced seaweed populations. giving particular emphasis to how disturbance influences the establishment. These circumstances define examples of ecological hystereses that pose particular challenges for management and control. Regina H. tomentosoides. Consequently. disturbance appears to be a critical factor that is either a key requirement (e.. Understanding the mechanisms of invasion is an important element defining both threat and control options for introduced seaweeds. which to attempt to control if time and finances are available. Most studies of seaweed invasions have been ‘‘case studies’’ that simply document the occurrence and spread of the introduced species. The role of disturbance in the persistence of the invaders is more complex and depends on the species concerned. Relatively few studies have examined the mechanisms that underpin successful seaweed 2 School of Zoology and Tasmanian Aquaculture and Fisheries Institute. In this context. then it represents a major threat to the integrity of native algal communities. Introduction Seaweed invasions are increasingly recognised as a major problem worldwide with often dramatic effects on ecosystem structure and function (Walker and Kendrick 1998. 7001 Australia 1 Keywords: establishment. if presented with a number of introduced seaweeds. for these kinds of introduced species. DOI 10. or which accelerates (e. e-mail: Joseph. Magierowski2 and Craig R. University of Tasmania.1515/BOT. If a species is capable of displacing native algae in the absence of any primary mechanism of facilitation such as disturbance.Botanica Marina 50 (2007): 351–360 2007 by Walter de Gruyter • Berlin • New York. However. The evidence suggests that. spread and persistence (Mollison 1986). for seaweeds at least. which is a complex multi-stage process that can be arbitrarily. Valentine1.040 Review Mechanisms of invasion: establishment. Alternatively. Johnson2 Marine Research Laboratories.*. invasion process.Valentine@utas. Defining these key phases precisely is vital to adequately describe and understand the invasion process and to enable meaningful comparisons among different species. spread. With the possible exception of Caulerpa taxifolia. Very few commonalities in key life history traits emerge since each species possesses a unique set of traits that confers a high capacity for invasiveness. Hobart. In this paper. control options that primarily target the disturbance are unlikely to represent viable management options. 2002). 2000. Hewitt et al. understanding mechanisms of invasion may also be important in identifying both potential future invaders and potential recipient communities vulnerable to invasion (Mack et al. and which to leave alone (Hiebert 1997). spread and persistence of introduced seaweed populations Joseph P. management. preventing anthropogenically mediated disturbance to canopies of native seaweeds should be considered as a potential control option to minimise the risk of establishment of exotic species at high densities.2007. then there exists a greater range of management options that include targeting the cause of the disturbance rather than the alga itself. In contrast. but usefully broken down into the separate phases of arrival. managers must decide which species have immediate priority for control. GPO Box 252-05. GPO Box 252-49. life history characteristics. Codium fragile ssp. Tasmanian Aquaculture and Fisheries Institute. establishment. Australia. Fucus serratus) establishment and spread. Nyberg and Wallentinus 2005.. In addition to defining threat and options for management. in several cases.g. The rapid acceleration in spread of introduced seaweeds poses a major challenge for management of marine ecosystems. Tasmania. management may need to target the alga directly. 2007).

however. 6ˇ Zuljevic and Antolic 2000. Algal type* Opportunistic Stresstolerant Life span Short Long Algal species Biotically Caulerpa competent taxifolia Long Long1 (pseudoperennial) High2 High3 Fucus serratus Long8 Codium fragile Sargassum Undaria ssp. Codium fragile ssp. w32x . 22Fletcher and Fletcher 1975. This article focuses on five species that have been recognised as successful seaweed invaders which have been the subject of experimental studies examining invasion mechanisms. References: 1Meinesz et al. 2Boudouresque et al.24 Small9 Small and large29 Propagule size Small Dispersal shadow Large While recognizing that qualitative assessment of life history strategies in this way is subjective. 14Trowbridge 1998. 16Carlton and Scanlon 1985. 13Trowbridge 1999. is not considered to constitute either establishment or persistence. b Although larger than other Codium species.c High17 Large10 Small10 Small18. establishment and subsequent expansion of the species range. 10Arrontes 2002. 2005.19 Moderate24 High26 Large25 Small and large22.15 Long20 (pseudoperennial) Short26 (annual) Herbivore resistance Growth rate Reproductive episodes Capacity for vegetative reproduction Propagule number Low High Single High Low High High High9.C.6. 2007). and that classification by life history type. 29Forrest et al. 17Chapman 1999. the tabulation nonetheless clearly shows that invasive seaweeds manifest a wide range of life history attributes. 5Sant et al. 3Meinesz et al. 23Stæhr et al. 25Norton 1992. 26Schaffelke et al.352 J. Caulerpa taxifolia (Vahl) C. in the absence of the macroscopic form. the presence of microscopic stages. For seaweed species with an alternation of generations between microscopic and macroscopic forms. 11NIMPIS 2002b. Is a similar approach likely to be fruitful in the case of seaweeds? Examining life history traits of the few well studied inva- Table 1 Life history traits of selected invasive seaweeds in relation to the three primary strategies of plant evolution (adapted from Clayton 1990).13 (pseudoperennial) Moderate14 High8. viz. 15Dromgoole 1975.c Low8 Moderate20 Low27 High21 High28 Repeated Repeated Repeated4 Repeated10 Repeated11.16 Repeated22 Single26 (zygotes) (spores) No23 No28 Varies Varies Varies High Varies Varies Varies Varies Varies Varies n/aa n/aa Small and large3. 27Valentine and Johnson 2005a. see Hewitt et al. 2002.12.b Small and large16. The invasion process How important are life history characteristics in determining invasibility? Are there commonalities in the life history traits of invasive seaweed species that provide important insights into mechanisms of invasion? In the case of terrestrial plants.7 No8 Yes8. Sargassum muticum (Yendo) Fensholt and Undaria pinnatifida (Harvey) Suringar. 19Campbell 1999. correlative studies have also been included in the absence of experimental data. We attempt to provide a synthesis of current levels of understanding of the mechanisms facilitating successful seaweed invasions.12.P. c Inferred from studies of other species within the order Fucales. 1995. focusing on life history characters and the factors influencing the processes of establishment. spread and persistence (factors influencing arrival are addressed elsewhere in this issue. 2000. the attributes of invading species that render them ‘‘invasive’’ have frequently been investigated as a means of identifying future invaders (Mack et al. The significant research efforts that have been directed at understanding the invasions of these particular species provides sufficient basis for discussion of mechanisms that promote successful seaweed invasion. Silva. Spread involves dispersal (natural or human-assisted). 12Fralick and Mathieson 1972. *Definitions of ‘‘algal type’’ in accordance with Grime (1977). 9Clayton 1990. tomentosoides (van Goor) P. while persistence (sensu Johnson and Mann 1988) refers to turnover of more than one generation of macroscopic thalli. 4Smith and Walters 1999. a Not applicable. 21Norton 1977. does not reveal consistent patterns. 8Chapman et al. tomentosoides muticum pinnatifida Long11. 24 Deysher and Norton 1982. since invasive Caulerpa taxifolia reproduces by vegetative fragmentation. Agardh. 18Prince and Trowbridge 2004. Fucus serratus Linnaeus. 1993. 1996. particular emphasis has been placed on understanding mechanisms of invasion using evidence from experimental studies. 20Britton-Simmons 2004. 7NIMPIS 2002a. 2000). Where possible. qualitative or otherwise. 28Saito 1975.16 (vegetative (zygotes) (parthenogenesis reproduction only) only) Yes5.4 Moderate9.12. 2000. Valentine et al. 1996.: Mechanisms of seaweed invasion of an introduced seaweed species as the development of a population of macroscopic thalli in an area that did not previously support the species.

Sakai et al. Codium fragile ssp. Community vulnerability to invasion The properties of the recipient community can be of major importance in determining invasion success (Dunstan and Johnson 2007). Our overall conclusion is that. 1987. with the notable exception of Fucus serratus.J. Undaria pinnatifida sporophytes can grow at high densities on otherwise unstable cobble and shell substrata (Valentine and Johnson 2003) on which foliose native macroalgae rarely develop. Certainly. introduced species consistently ranked higher than native species.e. establishment and ecological impact (Nyberg and Wallentinus 2005). Levine and D’Antonia 1999. More recent work with Sargassum muticum examined the mechanisms underlying invasion resistance in greater detail (Britton-Simmons 2006). Experimental manipulations showed that increased availability of space with removal of crustose and turf algae is required for strong recruitment of S. and invasive species ranked higher than non-invasive species. pinnatifida is able to utilise these unstable substrata because of the high growth rates of the sporophytes which rapidly attain sufficient size to stabilise the loose material to which they are attached. This notion is contrary to the more conventional viewpoint that most invasive plants. exceptions abound and generalisations are only applicable to a relatively select group of invasive species (Mack et al. Native species coexisting with U. are opportunistic species (Kolar and Lodge 2001. It is more useful to relate invasibility to the availability of resources. or un-utilised niches has been proposed as a reason why some communities are particularly vulnerable to invasion (Mack et al. for the most part. These authors argue that resistance to invasion will be determined by the particular properties of component species and their community dynamic. Emerging evidence suggests that increasing invasibility may be universally associated with increases in resource availability and/or variance in resource availability (reviewed by Dunstan and Johnson 2007). in New Zealand. possessing life history traits entirely consistent with an opportunistic life history strategy. their overall impact on the recipient community through development of dense cover. Using this approach. It is necessary to reconcile this view with the results of a recent approach to predict macroalgal introductions by quantitative ranking of 13 seaweed species’ traits under the broad categories of dispersal. there were no consistent patterns. but that recruits did not survive unless the foliose understorey and canopy species were reduced to increase light levels. 2000). Fernandez et al. consistent with the tenet that invasiveness of seaweed species is poorly predicted from their life history characteristics alone. it is sometimes suggested that communities with low species richness tend to be invaded more readily than areas with high species richness (Trowbridge 1998. tomentosoides is predominately found in association with Corallina turfs where bare space for attachment of thalli is abundant (Trowbridge 1995). there is evidence of this for some invasive seaweeds. highlighting the fact that each species possesses a unique suite of characters (Table 1. muticum is realised by sequential pre-emption of key resources (space and light) by different functional groups at different stages of development of the invading alga. It is usually implied that reduced levels of interspecific competition are associated with lower diversity systems. While we acknowledge the limitations of comparing life history characteristics on the basis of subjective qualitative criteria. This work suggests that resistance to invasion by S. therefore. under-. 1990). pinnatifida in Tasmania are unable to colonise unstable substrata because they grow too slowly and. stress-tolerant and biotically competent strategies. an important factor contributing to high rankings for invasive species was their ‘‘ecological impact’’. it is nonetheless apparent that few consistent patterns emerge. U. for Sargassum muticum. and most exhibit a range of characteristics that include components of what is usually recognised as opportunistic. there is limited value in using the life history features of these seaweeds to predict traits that confer invasiveness. Invasive seaweed species clearly do not emerge with a common suite of life history characteristics. 2000). namely opportunistic.P. which is that while invaders have some traits in common. Similarly. Vermeij 1978). and competitive or biologically competent strategies (Grime 1977. 2001). there is evidence to indicate that it establishes in areas that usually support low cover of native algae (Critchley 1983. However. which makes invasion by other species more likely. An ecosystem level attribute frequently cited as an important factor determining invasion success in terrestrial systems is disturbance (Elton 1958. it is difficult to define a vacant niche until it is occupied (Trowbridge 1998). therefore. is that these invasive species have rapid growth rates and capacity for both short. Other attributes of potential recipient communities that may influence vulnerability to invasion include properties that create a high likelihood of escape from biotic constraints (Mack et al. stress tolerant. i. Cavers and Harper 1967. and not by an aggregate community property such as richness. Thus. Shea and Chesson 2002). Clayton 1990). provides a basis for detailed examination of traits that may contribute to invasion success (Table 1). Undaria pinnatifida is arguably the exception. Valentine et al. 2000). work with marine invertebrate systems show that in some cases invasion of patches significantly increases with diversity (Dunstan and Johnson 2004).and longdistance dispersal. These results are. Hobbs and Atkins w33x . Similarly. However. This dynamic is readily interpreted in terms of the availability of resources (in this case the resource is space) and variability in resource availability (see Dunstan and Johnson 2007). Crawley 1986. muticum. When the life history characteristics that contribute to this ecological impact were considered alone. The presence of vacant. This is consistent with a view emerging from detailed examination of invasive terrestrial plants. at least in terrestrial environments. However. The most consistent trait shared by most species. are subject to a higher risk of damage by movement of the substrata during heavy surge or wave action. For example.. and so in this sense arguments centred on the concept of niche invoke a circular logic.: Mechanisms of seaweed invasion 353 sive seaweeds in relation to the three primary strategies associated with plant evolution.

2002 Arrontes 2002 Ambrose and Nelson 1982 Deysher and Norton 1982 De Wreede 1983 Andrew and Viejo 1998 Floc’h et al. this phenomenon is contrary to the pattern in other (non-marine) systems where activities of native herbivores provide resistance to invasions by reducing the survival and abundance of invasive exotic species (Parker et al. 1996. Valentine and Johnson 2003. particularly for Sargassum muticum.P. and there have been several mechanisms proposed. Britton-Simmons 2006) and observations following natural canopy disappearance (Ambrose and Nelson 1982) indicate that S. tomentosoides. 2004. Evidence from experimental manipulations. Valentine and Johnson 2005a). 2006). 2003 Levin et al. enabling seasonal development of dense virtually monospecific stands of U. muticum by maintaining low light levels on the benthos. is overgrazing of native algae by a native sea urchin (Heliocidaris erythrogramma Valenciennes) to form so-called ‘‘barrens’’ habitat (Valentine and Johnson 2003. then it is clear that disturbance can also play an important role in facilitating establishment and spread of marine plants (Table 2). 1996 Valentine and Johnson 2003 Valentine and Johnson 2004 Edgar et al. since the presence of a native canopy does not prevent development of U. Disruption of the native algal canopy has been demonstrated to be a key factor facilitating establishment of introduced seaweeds. while Deysher and Norton (1982) suggested that canopy species can prevent S. Stable native algal canopies inhibit invasion. Andrew and Viejo 1998. tomentosoides Fucus serratus Sargassum muticum Undaria pinnatifida w34x . but establishes following decline of the kelp. While there is ample evidence that disturbance often plays a critical role in facilitating invasion of introduced plants in terrestrial systems. but removal of erect algal species enhanced establishment intensity Yes Yes Yes No. pinnatifida sporophytes appears to be inhibited mainly by competition for light. tomentosoides does not directly displace native kelp species wSaccharina longicruris (Pyl. Valentine and Johnson 2004). Manipulations by Britton-Simmons (2006) suggest that an intact canopy prevents establishment of S. 2004 Reference Codium fragile ssp. muticum requires the provision of free space to establish successfully. Experiments involving manipulation of native seaweed canopies (Deysher and Norton 1982. The most important disturbance. 2004. Observational studies also indicate that disturbance to the native algal canopy is a critical precursor to the establishment phase in the invasion of Codium fragile ssp. pinnatifida. its importance in facilitating the invasion of exotic seaweeds has not been assessed in detail. muticum germlings from reaching the substratum. which has occurred in recent decades after infestation with the Table 2 Summary of the role of disturbance in the establishment process for selected invasive seaweeds.354 J. but dense seagrass beds less vulnerable to invasion No. but dense seagrass beds less vulnerable to invasion No. Species Role of disturbance Establishment – required? Caulerpa taxifolia No. 2002 Chapman et al. 2002 Jaubert et al. pinnatifida gametophytes on the rocky reef substratum (Valentine and Johnson 2003). Undaria pinnatifida and Codium fragile ssp. C. fragile ssp. Development of U.: Mechanisms of seaweed invasion 1988). but disturbance accelerates establishment Yes Yes Yes Yes Yes Yes Yes Yes Nature of disturbance? Specific disturbance not tested (different seagrass densities observed naturally) Experimental thinning of seagrass canopy Experimental removal of erect algal species Stormwater discharge implicated as disturbance Kelp canopy loss (due to epiphytic bryozoan Membranipora) Sea urchins eliminated by disease Experimental canopy removal Natural canopy disappearance Experimental canopy removal Experimental canopy removal Experimental canopy removal Experimental canopy removal Experimental canopy removal Canopy dieback Experimental canopy removal deVillele and Verlaque 1995 ´ Ceccherelli and Cinelli 1999 Ceccherelli et al. Edgar et al. Clearly. combined with observations following natural disturbances to the integrity of the canopy. Johnson et al. which acts to free resources.) Kuntzex. De Wreede 1983. Mechanisms of establishment: the importance of disturbance If the few studies that have critically examined the role of disturbance in the invasion process for introduced seaweeds are broadly indicative. while the presence of a stable native canopy inhibits sporophyte development (Floc’h et al. Valentine et al. indicate that Undaria pinnatifida sporophytes also require disturbance to establish at high densities. tomentosoides in the Northwest Atlantic Ocean.

or by exploiting periods of low sediment following events of elevated surge (Valentine and Johnson 2005b). Observations of Fucus serratus in the western Atlantic Ocean indicate the likely importance of disturbance in the invasion process. 2002). and can significantly accelerate the establishment process. pinnatifida after overgrazing and subsequent destruction of native canopy-forming algae (Valentine and Johnson 2003. Clearly. the recruitment and recovery of native canopy-forming species. While the exact dispersal mechanisms among invasive species differ. muticum on other algae are mainly the result of shading. therefore. with the exception of Fucus serratus. Development of the sediment matrix appears to inhibit settlement and development of native macroalgal propagules and. in high density stands it occurs principally in stressed environments where resources (e. sea urchin grazing. Manipulative experiments in Tasmania indicate that the primary disturbance factor.b).O. Some authors hypothesise that C.. For this species. therefore. Manipulative experiments and observations of seagrass beds indicate that C. taxifolia drives community dynamics by accelerating the decline of native seagrass wPosidonia oceanica (Linnaeus) Delilex. once established. or ships’ sea chests. facilitates establishment of U. however. and varies substantially among species. since it occurs most abundantly on friable sandstone substratum (Chapman et al. including Codium fragile ssp. U. manifest adaptations for both short. A similar mechanism has been reported for Sargassum muticum which. Valentine et al. if disturbance is required for establishment then it follows that spread will also be dependent on the frequency and intensity of disturbance. Thus. or nutrient availability (Britton-Simmons 2004).: Mechanisms of seaweed invasion 355 invasive epiphytic bryozoan Membranipora membranacea (Linnaeus 1758) (Levin et al. tomentosoides. manipulation by removal of native macroalgal canopies on rocky reefs has shown that communities with a native canopy are more resistant to C. although the decline may be instigated by multiple disturbance agents (deVillele and Verlaque 1995). taxifolia invasion than those without a developed canopy (Ceccherelli et al. the mechanism is more complex than that described for Codium fragile ssp. While disturbance to native canopies is not required for establishment of F. An experimental study examining the invasion of F. a trait that not only aids natural spread. pinnatifida is thought to persist on sedimentaffected reefs due to either a greater tolerance of sediment stress.P. and in estuarine areas following dieback of eelgrass (Trowbridge 1998). Experimental manipulations of established C. serratus. Clarifying the role of disturbance in the process of establishment of C. It is able to exploit these windows of opportunity by virtue of the rapid growth of sporophytes. sedimentation rates.J. The dispersal characteristics of introduced seaweeds also have a major bearing on their capacity to spread. Anthropogenic transport of fragments can account for ‘‘leaping’’ of introduced species to geographically distant sites without an intermediate station (Ribera and Boudouresque 1995). nets. disturbance increases the probability of successful establishment. 2002) and in areas with frequent ice scour (A. 2002). each of the remaining species that have demonstrated large scale incursions possess efficient strategies for dispersal. Recent experiments indicate that the negative effects of S. tomentosoides and Sargassum muticum. Similarly. fragile ssp. a more complete assessment of the risk that this alga poses to native communities. 2003). in association with anchors. taxifolia occurs in many habitat types. light and space) are available because other species are rare. largely prevents recruitment and development of other algae (Ambrose and Nelson 1982). Chapman personal communication). tomentosoides stands that have established are selfmaintaining and able to persist in the absence of the disturbance mechanism that enabled initial establishment. U. Many of these invasive seaweeds also possess characteristics that make them particularly susceptible to dispersal aided by human activity. fragile ssp. tomentosoides have the capacity to propagate vegetatively via fragmentation. disturbance affects the rate at which establishment occurs. ´ Ceccherelli and Cinelli 1999). Sargassum muticum and Undaria pinnatifida. serratus on eastern Atlantic shores of Spain has further demonstrated the importance of disturbance in the invasion process (Arrontes 2002). 2005a).and long-distance dispersal via microscopic propagules and drift thalli. but also enhances the likelihood of human-assisted transport. 2002). rather than changes in water flow. a matrix of sediment and filamentous algae accumulates on the reef surface (Valentine and Johnson 2005a. This mechanism establishes a positive feedback to maintain dominance by C. which has poor dispersal characteristics (Table 1). C. tomentosoides canopies indicate that they inhibit recruitment of native kelps (Levin et al. fragile ssp. removal of the sea urchins is not sufficient to promote recovery of native species because following native canopy removal. Some species. as in sites subject to stormwater and sewage outfalls (Jaubert et al. Caulerpa taxifolia and C. and. Codium fragile ssp. However. requires further research.g. fragile ssp. its role in the persistence of invaders is complex. pinnatifida and the sediment matrix coexist and persist indefinitely. taxifolia can invade native beds in the absence of disturbance. tomentosoides has also been observed to establish on former sea urchin barrens following epidemics of Paramoeba invadens (Jones 1985) that eliminate sea urchins (Scheibling and Hennigar 1997). it appears that dense seagrass meadows are more resistant to invasion than are sparse meadows (deVillele and Verlaque 1995. taxifolia. Mechanisms of persistence: is continued disturbance important? While disturbance may be an essential process facilitating establishment and spread of introduced seaweeds. tomentosoides. Mechanisms of spread Mechanisms of spread are often tightly coupled with the processes facilitating establishment. There is conflicting evidence regarding the importance of disturbance in the establishment of Caulerpa taxifolia. This complex mechanism is a stronger posw35x . A positive feedback mechanism facilitating persistence has also been demonstrated for Undaria pinnatifida. For example.R. However. Others provide correlative ´ evidence suggesting that although C.

2004. 1999. and the presence of introduced species (Levin et al. A range of disturbances or physiological stresses can lead to a reduction in cover of native algal canopies. tomentosoides and S. Villouta et al. sea urchin grazing (Lawrence 1975. Recent work in Tasmania represents a case-study demonstrating the potential for system-level management of U. Harrold and Reed 1985. removal of both the sea urchins and U. fragile ssp. tomentosoides and S. pinnatifida stands. For example. high water temperatures (Tegner and Dayton 1987). all of which require disturbance for successful establishment. including physical damage by storms (Kennelly 1987. Invasion by C. Andrew 1993. 1990. tomentosoides. The likelihood that a system affected by an invasive seaweed can return to its original state is a matter of critical interest. efforts to minimise canopy disturbance may slow down the pro- . Johnson et al. muticum since removal of the alien species does not realise recovery of native canopy-forming seaweeds in the case of U. The phase-shift from native algae to dominance by introduced species as a result of positive feedback (particularly for Caulerpa taxifolia. There are significant opportunities for researchers to undertake studies designed to recognise and minimise the impact of human activities on canopy-forming species. 2001). In all cases. both of which can lead to reductions in cover of canopy-forming species (Coelho et al. Indeed. Many of these disturbances are influenced by human activities and there is significant evidence to suggest that there has been a world-wide decline of canopy-forming species over the last 30 years (Benedetti-Cecchi et al. Managing populations of J. muticum are not the preferred food of native grazers in their introduced range (Prince and LeBlanc 1992. 2000). 1992). altering rates of sediment accumulation and inhibiting the growth of native seagrass shoots by shading (deVillele and Verlaque 1995). the predicted effects of global warming include not only increased water temperatures. Factors influencing persistence have not been examined in detail for Caulerpa taxifolia. Insight from this work has the potential to provide management with a range of options to prevent and/or control seaweed invasions. Schroder et al. taxifolia results in significant alteration to the environmental characteristics of seagrass beds. Where disturbance can be linked to human activity. pollution (Hardy et al. tomentosoides outbreaks. there is correlative evidence that positive feedback mechanisms also exist for this species. sedimentation is increasing on rocky coasts around the world as a direct result of industrial and domestic discharges and as an indirect result of modifying coastlines and river catchments (reviewed by Airoldi 2003). taxifolia and S. pinnatifida. 2001). Pederson and Johnson 2006). provides a potential option for control of U. When a system manifests little capacity to recover after cessation of a mechanism responsible for a phase-shift. pinnatifida.. muticum. reduced abundances of lobsters as a result of fishing activity are sufficient to account for formation of ‘‘urchin barrens’’ (Pederson 2003. 2004). the system is said to demonstrate an ecological hysteresis (Hughes et al. For Codium fragile ssp. managers are provided with alternative options to targeting seaweed thalli directly. pinnatifida. Keats et al. Bulleri et al. Jackson et al. For example. there is strong evidence that the organisms demonstrated to facilitate the invasion (Membranipora membranacea and Paramoeba invadens) are themselves introduced species (Chapman et al. but also increased frequency and intensity of storms. 2002). deVillele and ´ Verlaque 1995. 2005. For Caulerpa taxifolia and Fucus serratus. taxifolia is known to produce toxic secondary metabolites that assist in competition for space (deVillele ´ and Verlaque 1995). or when the recovery trajectory differs from that observed during the decline. burial or abrasion by sediments (Airoldi et al. fragile ssp. Consequently. Valentine et al. Bellwood et al. usually associated with humanmediated disturbance (e. in the Tasmanian system. research has shown that C. indirect control options may exist by w36x focusing efforts to minimise anthropogenically-mediated disturbance. 1996.356 J. 1999. Ayling 1981. tomentosoides. therefore. Codium fragile ssp. Dayton et al. fragile ssp. In addi´ tion. tomentosoides and Undaria pinnatifida) is cause for concern. 1993). Similarly. edwardsii to maintain sea urchin populations at low levels. moreover. pinnatifida. In Tasmania. the spiny lobster Jasus edwardsii (Hutton 1875) is more important than reef fishes as a predator of sea urchins (Heliocidaris erythrogramma Valenciennes 1846) and. Phase-shifts to dominance by introduced seaweeds also have potentially serious implications for secondary consumers. C. 2002). Sargassum muticum and Undaria pinnatifida. which has facilitated establishment of dense U. and an enhanced inoculum of spores of native species. but may affect recovery of canopy forming natives in the cases of C. Johnson and Mann 1988. Moreover. was insufficient to regenerate native canopy forming species (Valentine and Johnson 2005a). C. with potentially dramatic and longterm implications for ecosystem structure and function. Phase-shifts in community structure providing for alternative stable states have been demonstrated previously for marine systems. fragile ssp. However. 2001. tomentosoides in the north western Atlantic Ocean. the advent of ¨ hystereses through positive feedback provides particular challenges for management. Mechanisms of invasion: potential ‘‘system management’’ control options Where disturbance to the native algal canopy is a necessary prerequisite for the establishment and persistence of invasive seaweeds at high densities.g. It is likely that overfishing of sea urchin predators is ultimately the single most important factor causing reduced native algal cover on the east coast of Tasmania.P. efforts to prevent introduction of these exotic species represents a potential control option to avoid further C.: Mechanisms of seaweed invasion itive feedback than arises in the case of C. diets based on consumption of exotics can result in lowered reproductive output of grazers (Scheibling and Anthony 2001). The available evidence suggests that focusing management efforts to prevent disturbance to the native canopy may represent a feasible control option for Codium fragile ssp. Scheibling et al. 2005). Airoldi and Virgilio 1998). Britton-Simmons 2004).

aspect annual) or annual invasive species. In these examples. management to control it by targeting the disturbance may be effective if the disturbance that facilitates establishment is also required for persistence. Where the existence of different ‘‘stable states’’ (reflected as dominance by native canopy-forming seaweeds or introduced seaweeds) can be demonstrated. pinnatifida. this kind of spatial variability may be a result of introduced species displaying characteristics not evident in their native range (Ribera and Boudouresque 1995). particularly in relation to establishment and spread. which reinforce dominance of invasive seaweeds (such as those described for Undaria pinnatifida. potentially overestimating the strength of positive feedback loops. Spatial variability in invasion dynamics is clearly an important consideration and can provide particular challenges to formulating management responses to invasions. pinnatifida to cessation of disturbance to native canopy species is scale-dependent. Propagule supply may also be influenced by the scale of the disturbance.g. it appears that the results from the small-scale experimental plots would have resulted in an underestimate of the threat posed by Undaria pinnatifida. there is no recovery of native canopy-forming algae following removal of sea urchins. The lack of long-term studies may represent a potential bias when examining persistence mechanisms. Unfortunately. Codium fragile ssp. the native species displace any U. and may reduce the ultimate density at which they establish. 2005). relates to effects of spatial scale. Valentine and Johnson 2005a). it is particularly important that future studies examine the factors that promote recovery of native canopy-forming species. Where there has been large scale destruction of the native canopy (spatial extent approximately 1. while the accumulation of sediment in the smaller experimental plots is insufficient to prevent recovery of native canopy-forming species. pinnatifida thalli that develop in response to the initial disturbance within two years (Valentine and Johnson 2003). present a significant challenge for management. studies are rarely conducted on a time scale sufficient to examine more than one turnover of a generation of macroscopic thalli.. storm scour). This can provide w37x . U..2 ha). Consequently. where the facilitating canopy disturbance is natural (e. practical control options are not available. However. native seaweeds and the sediment matrix Conclusion Our broad findings are that knowledge of life history traits provides only limited insight into the potential for invasion of exotic seaweeds. The sediment matrix and high cover of U. it should be stressed that wherever possible. Mechanisms of invasion: the importance of spatial and temporal scale Scale is well recognised as a fundamental aspect of ecology (Levin 1992) and must be considered when examining mechanisms of invasion and potential management options. The mechanism shaping this non-linear scale-dependent response is unknown. the response of U. In such instances the magnitude of invasion will depend on the frequency and intensity of natural disturbance events. ‘‘system management’’ is problematic. In this particular example. 2004. In relation to introduced seaweeds. Rueness 1989). Clearly not all disturbances can be prevented or controlled. Valentine et al. and control options will be restricted to targeting the seaweed directly. A possible explanation is that sediment accumulation following canopy disturbance is itself scale-dependent. when holes in the canopy are relatively small (16 m2). While the current synthesis demonstrates a degree of predictability in the response of invasive seaweeds to disturbance.: Mechanisms of seaweed invasion 357 cess of establishment and spread. particularly those with low dispersal abilities. potentially affecting recruitment processes for native canopy-forming algae. From a management perspective. and so ensure greater confidence in predicting invasion dynamics. it needs to be acknowledged that responses to manipulations (in experiments) or external forcings (in nature) may differ from one location to another. tomentosoides and Sargassum muticum).J. but that disturbance can play an important role in the invasion process. it is clearly preferable to sustain a resilient ecosystem than to attempt to rehabilitate it after a phase-shift has occurred (Hughes et al. For example.g. disturbance.e. Long-term studies are clearly required to examine whether native perennial species eventually exert dominance over pseudo-perennial (i.P. For example. Sargassum muticum occupies a wider ecological niche and grows much larger in European shores compared with Japanese populations (Norton 1977. Valentine and Johnson 2003) or at large scales as a result of overgrazing of native algae by sea urchins (Johnson et al. Where possible. or both (Valentine and Johnson 2005a). Greater development of the sediment matrix associated with the larger-scale disturbance may inhibit recovery of native algae. The temporal scale of observation may also have a large bearing on the ability to critically examine mechanisms of invasion. experiments should be replicated in space and time to establish generality in the response of invasive seaweeds to disturbance. Another layer of complexity in the dynamics involving interactions between Undaria pinnatifida. particularly for species with longer life spans. However. It should be emphasised that once an exotic species is established. the strong positive feedback mechanism seems only to operate for canopy removals at larger scales. experiments examining mechanisms of invasion should be conducted on a range of spatial scales to infer generality of results. since targeting the enabling disturbance after establishment is unlikely to represent an effective control strategy. particularly in relation to persistence. in manipulation experiments.. Thus. but would not be sufficient to prevent establishment from occurring. In contrast. These kinds of mechanisms have implications for assessing the threat of an introduced seaweed species. pinnatifida develop regardless of whether disturbance to native canopy species occurs at small scales (e. and there is no sea urchin grazing. the existence of positive feedbacks and ecological hystereses.

Cinelli. 133: 241–251. Benedetti-Cecchi and F. 60: 251–263. Effects of Posidonia oceanica canopy on Caulerpa taxifolia size in a north-western Mediterranean bay. Ecol. and habitat structure on reefs in temperate Australia. N. The invasive alga Caulerpa taxifolia is not a suitable diet for the sea urchin Paracentrotus lividus. Aquat. and J. J. L. Bot. Bot. Aquat. tomentosoides (Chlorophyta) in the North Atlantic Ocean. 2000. L. MuckleJeffs. Philos.358 J. W. S. Ecol. J. Ecology 62: 830–847. Mar. M. Reichard. P.S. Chapman. Phycol. L. Ceccherelli. Biol. Seastedt. Stress Recovery 7: 317–333. and M. 62: 421–445. J. In: (R. Spread of introduced Caulerpa species in macroalgal habitats.. D. Mar. Verlaque. Tegner. X. L. 1990. Gray.N. Ecological limits to the invasion of Sargassum muticum in northern Spain. 1999. Ecol. 1992. Folke and M. J. Chapman. Ambrose. Rijstenbil and M. Ottawa. Arrontes. deVillele. N.E. Temporal and spatial patterns of disturbance and recovery in a kelp forest community. 1999. Species introductions and changes in the marine vegetation of Atlantic Canada. 1999. 1999. Crawley. M. Oxford. M. I. 2004. Clayton. Biol. Ecol. A.T. Ceccherelli. 2003. The clear message is that ‘‘prevention’’ is easier and less costly than ‘‘cure’’. Britton-Simmons 2006. A.W. and F. Scheibling and A. Occurrence of Codium fragile subsp. P. F. Helgol. Cavers.V.L. Harper.: Mechanisms of seaweed invasion important options for management to control seaweed invasions. P. Andrew. resource preemption and the genesis of invasion resistance in a community of marine algae. This question will only be answered with carefully designed experimentation and analysis (Ceccherelli et al. G.K.F.S. 2002. E.P. 214: 137–150. Bot. 1996.T. The establishment and increase of Sargassum muticum (Yendo) Fensholt populations within the Solent area of southern Britain. Responses of turf-forming algae to spatial variations in the deposition of sediments. because other elements of community complexity may influence resistance (BrittonSimmons 2006). Britton-Simmons.E. R. Mar. T. Critchley. F. 240: 19–36. and M. J. and Paracentrotus lividus Lam. A. Mar. Studies in the dynamics of plant populations.E. 28: 155–165. Ecol. sea urchin grazing. it may be more practical and effective to target the disturbance rather than the alga directly. Crawley. Mar. Meinesz.M. M. Mar. The population biology of invaders. eds) Alien invaders in Canada’s waters. Dunstan and Johnson 2007). 1981. J. Aust. Edwards. Ecology 74: 292–302. Sediment deposition and movement over a turf assemblage in a shallow rocky coastal area of the Ligurian Sea.F.S. an aspect of seaweed invasions that has received scant attention to date.. 2006. Crawley. C. C. Impacts of anthropogenic stresses on the early development stages of seaweeds. Work in this area has been conducted only with Codium fragile ssp. Cinelli. 2002.. 15: 439–452. Lemee. particularly in relation to understanding the mechanisms that enable invasive species to outcompete native species following disturbance.R. Direct and indirect effects of the introduced alga Sargassum muticum on benthic. Trans.M. 25: 265–267. An investigation of the increase in number of population individuals. Bot. Campbell. succession and stability. 1967. pp. 16: 630–640. tomentosoides. Inhibition of giant kelp recruitment by an introduced brown alga. Rev. J. 2004. Hughes. 1996. 1987. Canadian Forest Service. Ecol. there is also considerable scope for research to examine the factors conferring resistance to invasion in native seaweed communities. Mar..H.B. Lonsdale. From introduced species to invader: what determines variation in the invasion success of Codium fragile ssp. 1998. Bot. R. 141: 1059–1067.M. Ser.. 2002. K. Piazzi and D. Williamson. tomentosoides (Chlorophyta: Bryopsidales) in marine embayments of south-eastern Australia. Ser.J. 1983. T. Ser. Nature 429: 827–833. K.J. particularly when positive feedbacks arise to maintain the dominance of invasive seaweeds.J. 55: 59–71. I. Prog. Nystrom. Prog. A. The role of biological disturbance in temperate subtidal encrusting communities. Mari and A. Claudi. The fate of seed and transplants introduced into various habitats. Mar.J. London B 314: 711–731. Blackwell Scientific.. Soc. G.L. 26: 539–545. w38x . This research would fruitfully examine nutrient dynamics and macroalgal physiology. P. 2002. Dayton. Coelho. 1986. Annu.T.. Viejo. Airoldi. Brown. Valentine et al. Bulleri. Airoldi. 165: 271–282. S. I. Ecol.H. Scanlon. G. Directing research to reduce the impacts of nonindigenous species. L. 52: 277–289.A. References Airoldi. Mar. Ecol. 241: 81–95. Grazing by the sea urchins Arbacia lixula L. Parker. 277: 61–78. Airoldi.J. Biol. C. Nantel and E. Atkinson. 1982. Biol.A. in the northwest Mediterranean. 41: 161–236. Relini and F. J. Prog. 429–454. USA. Oikos 113: 395–401. 1985. 53: 245–250. 133–148. P. Monogr. Ser. Exp. J. R. Smith. X. M. Changes and degradation ´ in a Posidonia oceanica bed invaded by the tropical alga Caulerpa taxifolia in the North Western Mediterranean. Cinelli. J. Mar. subtidal communities of Washington State.L. Carlton. However.J. Given the importance of disturbance and the properties of the recipient community (Dunstan and Johnson 2007) in the invasion process.. Fabiano and F. Cinelli. Virgilio. S. Bellwood. eds) Colonisation. Parnell and P. Boudouresque. 2002.M. There are significant opportunities to extend this line of enquiry to other species. J. Chapman. wetlands and forests. Exp. Balata. Hayes. There are significant opportunities for further research in this area. 35: 938–940. M. Prog. 280: 1–11. Spatial heterogeneity. 1993. Ayling. Biol. Bulleri. Cons. Biol. Edwards and A. Ecol.M. Mechanisms of range expansion in the intertidal brown alga Fucus serratus in northern Spain.J. Pannacciulli. Mar. What aspects of the native community provide this resistance? It is not simply a function of species richness (Dunstan and Johnson 2007).R. Byers. Mar. F... Moschella. Chornesky and D. Ecol. Confronting the coral reef crisis. Britton-Simmons. and B. L. R.O. this approach is not likely to be effective once an invader is established. Andrew. 1995. L. 1. 1998. tomentosoides (Chlorophyta) on the Atlantic coast of North America. Exp. Ecosyst.R. Oceanogr. J. and J. Where a facilitating disturbance is linked with human activity.E. Randall. The adaptive significance of life history characters in selected orders of marine brown macroalgae.M. and R. Progression and dispersal of an introduced alga: Codium fragile ssp.B. Mar.S. and has shown that invasion in this species is due in part to its ability to compete for and acquire nitrogen (Trowbridge 1998). Functional group diversity. The effects of sedimentation on rocky coast assemblages. Aquat. 38: 79–87. pp. Meeresunters. P. Benedetti-Cecchi.P. Bot. 2001. Nelson. Predicting the consequences of anthropogenic disturbance: large-scale effects of loss of canopy algae on rocky shores. What makes a community invasible? In: (M.

L. G. Pandolfi. Prioritizing invasive plants and planning for management. fish and macroinvertebrate communities on eastern Tasmanian reefs. Chisholm. Bazzaz. Petrik and T. Hiebert. Parker. 7: 265–279. Community-wide effects of nonindigenous species on temperate rocky reefs. The role of natural dispersal mechanisms in the spread of Undaria pinnatifida (Laminariales. pp. Trends.W. 111: 1169–1194. Bull. Progress in invasion biology: predicting invaders. and D. Aust. Johnson. Soc. 27: 293–301. Estes. Kidwell. 2007. A. Opposing effects of native and exotic herbivores on plant invasions. 1990.M.N. Studies on the recently introduced brown alga Sargassum muticum (Yendo) Fensholt I. Marchioretti. and C. 1985. New paradigms for supporting the resilience of marine ecosystems. Effect of disturbance and nutrient addition on native and introduced annuals in plant communities in the Western Australian wheatbelt.: Mechanisms of seaweed invasion 359 De Wreede. Mar. C.B. Mann. Johnson. T. 2004.M. J.A. Bellwood. H. Fernandez. and S. Exp. Mar. R. Paramoebidae). The ecology of invasions.M. Kolar. Ecology of Sargassum muticum on the north coast of Spain. 10: 689–710. prediction. Preliminary observations. Nyberg. 1992. Phycol.P.marine. L. eds) Proceedings of the International Echinoderm Conference. and I. 50: 326–337. Steneck and J. Introductions of seaweeds: accidental pathways and mechanisms. Komatsu. Edgar. J. Ecol. 2003. sea urchin grazing.R. Gutierrez and J. Levin. 1983.C. 2002. R. S.W. Erlandson. Valentine et al.. R. 13: 213–286. Amer. Modelling biological invasions: chance.H. Lodge. J. 1987.P. J. and K. Biol.M.A. Ecology and reproduction. Tremayne. Cooke. Winter fragmentation of Codium fragile (Suringar) Hariot ssp. J. M. Fletcher. Sliwa. R. 26: 41–53. Elton. Hesses and X. 2002b. pp. Phycol. Lange. Ecol.H. Ecol.G. J. Brown. Ecol. 18: 149–156. 2006. 9: 257–264. H. Phycologia 22: 153–160. Wilson.S. Date of access: 12/6/2005. 38: 499–508. In: (T. Harrold. T. Monogr. Evans and M. Prog. morphology and biomass of Caulerpa taxifolia in the Mediterranean sea. Valentine and H. 312: 67–87. Ripley. and T. 1975. 1992. Methuen. Date of access: 11/17/2005. Meinesz. Mar. Benichou.A. 2003. T. 158. 2000. 1958. Science 311: 1459–1461..L. Web publication -http://crimp.P. Botsford. Spread of the introduced tropical green alga Caulerpa taxifolia in northern Mediterranean waters. Meinesz.M. C. 13: 171–179. Codium fragile ssp tomentosoides species summary. L. Hydrobiologia 326/327: 217–222. S. S. Levin. 68: 181–193. sea urchins and algae facilitates spread of an exotic kelp in eastern Tasmania. M. Long-term changes in the marine macroalgae of three polluted estuaries in north-east England. Mar. W. Ser.J. Occurrence of Codium fragile subspecies tomentosoides in New Zealand waters. Floc’h. Bradbury. App. Mar. R. Wallentinus. M.D. 1993. and A. Trends Ecol. J. Dunstan. Rotterdam.M.S. Mollison. Burkepile and M. Dispersal and colonisation in Sargassum muticum (Yendo) Fensholt. B. Levine. Lemee.M. Physical disturbances in an Australian kelp community. Oceanogr. M. B.J. 1977. tomentosoides (van Goor) Silva (Chlorophyceae. Grime. Re-evaluation of the extent of Caulerpa taxifolia development in the northern Mediterranean using airborne spectrographic sensing.M. Luken and nimpis). R. Phaeophyta): regrowth and interaction with Rhodomelalarix (Ceramiales.C. Roy. Ecology 73: 1943–1967. Protozool. Peterson. 1972.. C. D’Antonia. C. J. Bjorndal. 213–220. Coyer. a pathogenic amoeba from the sea urchin. 56: 179–196. 2005. Norton.H. patterns of adaptation and stability of Nova Scotian kelp beds. in eastern Canada. and kelp forest community structure. epidemiology. The problem of pattern and scale in ecology. Mack. Zeal. Biol.C. Rico. S.A.R. Evans. Warner. Heinzeller. Oikos 87: 15–26. University of Tasmania.. Mar.. Rev.. Bourque. J. Keats. F. 16: 199–204.. 40: 145–153. Ecol. Steele. and control. Can species traits be used to predict marine macroalgal introductions? Biol. H. Nat. F. 2004. 32: 564–569. Effect of algal canopy clearance on plant. Bot. Mari. Fralick. Undaria pinnatifida (Laminariales. 5: 141–147. M.H. 1993.A.K. Science 293: 629–638. explanation. Hurd and C. A.K. 263: 75–82. 2002a. Campbell and B. 195–212. D. Schaffelke. C. C. 2000.S. Bot. J. Robin South and D. w39x . Hardy. Inv. Balkema. Kennelly. Jackson.D. Oecologia 138: 285–292.D.marine. R. J. R. Berger. Historical overfishing and the recent collapse of coastal ecosystems. R. B. Ecol. L. I. Siphonales) in New England. 46: 91–98. G.R. Morton and C. Ser. H. and C. 172: 81–91.A.P.W.S. NIMPIS.L. 2007. 1995.A. C. Invasion rates increase with species richness in a marine epibenthic community by two mechanisms. Biol.A. Lawrence. Steneck. Web publication -http://crimp. T. R. Strongylocentrotus droebachiensis. Hughes.A. Folke. Ecol. and L.H.X.M. Bot. P. D. 1997.M. Elton revisited: a review of evidence linking diversity and invasibility. Johnson. 58: 129–154. 1996. Hewitt. Nebelsick. 2001. Ecol. Mechanisms of invasion: can the recipient community influence invasion rates? Bot.J. C. D.. J. Rhodophyta). Effects of experimental reduction in grazing by green sea urchins on a benthic macroalgal community in eastern Newfoundland. J. Barrett. C. K. K.O. N.E.I. Jaubert. Evol..H. pp. Morrow and H. Pajot and V. de Vaugelas. 1986.csiro. Mar. Diversity. Phycologia 11: 67–70. J. Ecology 83: 3182–3193. Norton. 6–10 October 2003. 1990. Reed.. Appl. Freshw.P. J. Biotic invasions: causes. sp. Biol. Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. P. Paramoeba invadens n. NIMPIS. J. Hayes. P. Prog.L.M. W. J.R. ´ Molenaar and X. Mar.P. Pederson. Lonsdale. Hobbs.R.M. Exp.. Mar. Philos. New York. Mar. 2005. Hay.. Dunstan. Annu. and C. C. 1988. Samson. and C. Good. C. Minghelli-Roman.R.M. pp. 1988. Fletcher 1975. Caulerpa taxifolia species summary.J. Identifying potential marine pests – a deductive approach applied to Australia. J.R. Johnson. R. M. 1985.G. G.J. Munich.H.G. Clout and F. Ser. The growth and development of Sargassum muticum. Mari. R. 181. A. PhD thesis.E. Forrest.. 2004. New. Thieret. Jones. R. J.H. 1982.R. Mouret. Phaeophyta) 12 years after its introduction into the Atlantic Ocean. Evol.J.J.D. Bot. 314: 675–693. Biol.S. 50: 361–372. Simberloff. Ecol. Mar. Taylor. Temporal effects. In: (J. Sargassum muticum (Fucales. Norton. Blachier. and D. Lenihan. global consequences. On the relationships between marine plants and sea urchins. New York. 33: 423–428. J. 1975. Ecology 66: 1160–1169.S. eds) Assessment and management of plant invasions. S. Dromgoole. Mar. D. Prog. Mar. Springer-Verlag. Atkins. Ecol.. Hay. B. J. Poll. Dispersal by macroalgae. 1999.S. T. 2001. Hughes. Mathieson. Phycologia 39: 547–553. Br. Variations in the structure. Population dynamics of the sea urchin Heliocidaris erythtrogramma on the east coast of Tasmania. Deysher. 20: 380–386. Food availability. D. J.T. Leiden. Exp. C. J.. T.csiro. (Amoebida. A. J. Ecol. 1977. Tegner and R.A. Pederson.R.B. A most unusual barrens: complex interactions between lobsters. Kirby.. Exp. Phaeophyceae). Mar. Mar. 2003.N. J.E. L.

R. 17: 243–279. 21: 291–300. Syst. Oceanogr. 36: 1–64. Synchronus release of male gametes of Caulerpa taxifolia (Caulerpales. McCauley. Sci. B. Australia. I. 2003. 20: 307–319. and C. Evol.A.W. Ecol.F. Valentine. Persson and A. D. Bot. 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. M.E. 1998. C. O’Neil. 1997. Bristol. 304–320.) and the invasive alga Codium fragile ssp. J. Parker. 55: 223–230. Valentine. Aquat. Tohida and H.W. Cryptogam. pollution and introduced species. Valentine. Scheibling. Saito. Fish. Biopress Ltd. Destructive grazing. Junk. Hennigar and T. R. epiphytism. 35: 1007–1024. P. Chapman. Trowbridge.J. and P. 17: 170–176. Allendorf.A. Tegner. and S.H. Phycologia 39: 157–159.. Mar. 48: 106–115. Mar. Shea. Persistence of the exotic kelp Undaria pinnatifida does not depend on sea urchin grazing. Mar. J. Biol. Cinelli. W. 2005. Ecol. tomentosoides on Australian shores. Schaffelke. Mar. Walker.D. Rueness. P.D. Effects of the spread of the introduced Rhodophyceae Acrothamnion preissii and Womersleyella setacea on the macroalgal community of Posidonia oceanica rhizomes in the Western Mediterranean sea. K. Cambridge.P. 2005. Ann. Sant. Fiordland. Hay. Ecol. Valentine et al. and C.N. Scheibling. Ballesteros.A. Biol. Molofsky. Bull. Ser. 2006. Vol. and A.J. tomentosoides.. New Zeal. 2006. 47: 461–470. 39: 427–430. Trowbridge. Ecol. Establishment of the green alga Codium fragile ssp.L. accepted 12 June. J. E.E. S. Prog. Trowbridge. L.J.G. Chlorophyta) in the Mediterranean Sea. 2000. 56: 2300–2314.. ˇ Zuljevic. Ecol.P. and disease: the dynamics of sea urchin–kelp interactions in Nova Scotia. Chesson. Poll.R. C. M. 336: 120–134. M. and P.D. and C. Mar. 285: 43–55. L. D. Bot. J. J. J. R.N. J. M. Johnson.M.X. Kendrick.W. A. Rev. 2001. Biol. Lodge. Mar. 207: 79–88. Stæhr. Community ecology theory as a framework for biological invasions.L. Tasmania.J. 2004. Ann. 1995. A.A. Boudouresque. J. Walters. 1987. 2002. 32: 305–332. Hewitt. C.P. Hobart. N. O. Prog. 1978.D. Sakai. 1975. Johnson. Freshw..360 J. Sargassum muticum and other introduced Japanese macroalgae: biological pollution of European coasts. 2005a. Ser. Mar. and C. Biol. In: (F. R. Direct experi¨ mental evidence for alternative stable states: a review.E. Establishment of the introduced kelp Undaria pinnatifida in Tasmania depends on disturbance to native algal assemblages. 11. tomentosoides on New Zealand rocky shores: current distribution and invertebrate grazers. Bot. T.: Mechanisms of seaweed invasion Pederson. Feeding. J. Pederson. Oikos 110: 3–19. Villouta. Introduced marine plants. and C. Prince. J. 217–268.E. Anthony. N. Ecol. 1999. Rev. Received 19 January.J. Balch.S. and L. Valentine. Predation of the sea urchin Heliocidaris erythrogramma by rock lobsters (Jasus edwardsii) in no-take marine reserves. Mar. Laminariales) in Tasmania. A. and G. Agardh in the Mediterranean Sea: testing the boat transportation hypothesis.M. A. growth and reproduction of sea urchins (Strongylocentrotus droebachiensis) on single and mixed diets of kelp (Laminaria spp. 1999. Mar. Mar. pp. Reproduction in the green macroalga Codium (Chlorophyta): characterisation of gametes. Reproductive phenology of the introduced kelp Undaria pinnatifida (Phaeophyceae. Ser. Y. Mar. eds) Advance of phycology in Japan.S. In: (J. ´ 1996. Johnson.E. CSIRO Marine Research..W. 2001. J. Vermeij. G. Chadderton. An assessment of the potential spread and options for control of the introduced green macroalga Codium fragile ssp. Undaria. with special reference to macroalgae: mechanisms and impact. and C. Mar. 113: 159–163. Algol. Res. and C. C.I. J. Johnson.S. Recurrent outbreaks of disease in sea urchins (Strongylocentrotus droebachiensis) in Novia Scotia: evidence for a link with large-scale meteorologic and oceanographic events. Scheibling. Invasion of Sargassum muticum in Limfjorden (Denmark) and its possible impact on the indigenous macroalgal community. Krause-Jensen. Dayton. Effects of sea urchin (Evechinus chloroticus) grazing in Dusky Sound. J. Bot.M. pp.E. Can. Thompson and S. patterns of marine life. 1995. Exp. 83: 949–965. pp. J.G.C. Cohen. 1999. eds) Progress in phycological research. Weller. H. Adv. Ecol. Biol.S. pp. Piazzi. Pugsley and C. and B. 152: 155–165. 1989.P.. New Zealand. With. 2000.R. 139: 139–146. D. C.P. El Nino effects on Southern California kelp forest communities. and F. De Roos.G. Delgado. Round and D. Mar. Ecol. Antolic. Biogeography and adaptation. 2000. 20: 173–176. tomentosoides (Chlorophyceae) and four other seaweeds. 1992. Trowbridge. J. 332. Establishment of the introduced kelp Undaria pinnatifida following dieback of the native macroalga Phyllospora comosa in Tasmania.F.K. Prince. The population biology of invasive species. LeBlanc. Smith. The spreading of the introduced seaweed Caulerpa taxifolia (Vahl) C. Threats to macroalgal diversity: marine habitat destruction and fragmentation. Trends Ecol.. Hennigar. Rodrıguez-Prieto and E. Mar.M. 2004. Freshw. Australia. Fragmentation as a strategy for Caulerpa species: fates of fragments and implications for management of an invasive weed. R. J. 43. K. Res. Hirose. M. Mar.R. F. and W. Schroder. 41: 105–112. 2001. Ecology of the green macroalga Codium fragile (Suringar) Hariot 1889: invasive and non-invasive subspecies. Cabin. Thomsen. Ellstrand.L. Wernberg and D. Prog. 1998. Phycologia 44: 84–94. Comparative feeding preference of Strongylocentrotus droebachiensis (Echinoidea) for the invasive seaweed Codium fragile ssp. 295: 63–90. 2006 w40x . Harvard University Press. Exp. C. Ribera. Ecol. Holt. Johnson. 2005b.R. Campbell and C. The Hague. Mar. Baughman.

Symstad 2000. 2002). total levels of resource availability will vary. These findings cannot be explained solely by Shea and Chesson’s (2002) attempt to reconcile divergent observations of both positive and negative relationships between invasion rates and richness of the recipient community. 2002. Elton (op. the nature of interactions among species. Australia. 2000). so too will patterns of resource utilisation. GPO Box 252-05. communities with relatively more species and niches. based on the behaviours of several models. it needs to be emphasised that Elton stated his hypothesis as two separate ideas. However.g. Tasmania 7001. Dunstan1.1515/BOT.. This observation keeps sharply in focus the question of why it is that alien species often fail to establish or invade at new sites despite inoculation. that is. The ability of a community to resist invasions has been a subject of ongoing research since Elton’s (1958) seminal work. Stachowicz et al. spatial interactions. e-mail: Piers. Here. Wiser et al. Hector et al. patches) and the invasibility of those areas (e.* and Craig R. Based on qualitative observations across a diversity of habitats and ecosystems. species-poor communities. However. w41x . and the spatial arrangement of individuals on a landscape. We argue that seaweed communities adhere to this principle. the dynamics of some empirical systems do not support this idea. diversity or the average connectivity of the system per se. is that species-rich communities are more resistant to invasion than species-poor communities in otherwise identical habitats. These remarkably prescient ideas have remained part of the framework of ecological theory over the past 50 years. 1997. While the lines of evidence forwarded by Elton do not stand up to exacting scrutiny. other more quantitative evidence has emerged to support his ideas. dependent in part on the life history features of component species.041 Review Mechanisms of invasions: can the recipient community influence invasion rates? Piers K. Stohlgren et al. Tasmania 7001.. Keywords: invasion resistance.. even if the total amount of resource does not change. 1999. should be more prone to invasions than communities that are more stable and less prone to oscillations. Hobart. but from the ability of established species to utilise the maximum amount of resources in the long term and realise the smallest amount of variability in resource 2 School of Zoology and Tasmanian Aquaculture and Fisheries Institute. cit. Kolb et al. McGrady-Steed et al. invasions. 2004. we develop an alternative view that invasion success is related positively to variability in resource availability. Robinson et al. more prone to fluctuations) than in more complex communities. Elton’s (1958) principal conclusion was that the ‘‘balance of nature’’ in simple communities was more easily ‘‘upset’’ (i. Tilman 1997. Hobart. DOI 10. Most of the debate about invasions has focused on the idea that species diversity confers resistance to invasions. Johnson2 CSIRO Marine and Atmospheric Research. were more stable than simpler. 2001. It follows that.. University of Tasmania. Levine 2000. Cleland et al. but they are not as frequent as might be expected from a virtually constant supply of propagules from anthropogenic vectors (Carlton and Geller 1993). 1995. Kennedy et al. arguably with increasing frequency (Cohen and Carlton 1998. Introduction Invasion resistance and richness: the conventional view Two elements critical to the establishment and spread of invasive populations are the arrival of new propagules of the potential invader and the ability of the recipient community to resist their establishment. First. Secondly. The impetus to more fully understand the mechanism(s) of resistance of communities to invasion is as urgent as at any time..) suggested that communities with varying species abundances (i. He argued that the simple low diversity communities that could be more easily ‘‘upset’’ were more susceptible to invasion by alien species.e. with greater oscillations in species abundances). This variability can arise in many ways. Our overall conclusion is that the ability of a community to resist the establishment of new populations comes not from species richness. there is also a growing body of empirical evidence showing a positive relationship between richness and invasibility (e.Botanica Marina 50 (2007): 361–372 2007 by Walter de Gruyter • Berlin • New York.2007. The widespread view. GPO Box 1538. 1998.Dunstan@csiro. he suggested that more complex communities. initiated by Elton and later supported by both empirical and modelling studies.g. However.e. as abundances of species vary. Ruiz et al. resource limitation. Invasions into marine ecosystems continue to occur.g. Australia 1 * Corresponding author Abstract At least since Elton’s work in the 1950s it has been argued that properties of recipient communities influence invasion rates. Considerable empirical evidence has revealed a negative relationship between the species richness of particular areas of interest (e. his argument was compelling and provoked substantial debate. 1999. Consequently. reflecting the particular attributes of component species and their interactions. MacArthur (1955) suggested a similar line of reasoning. but reveal instead a positive relationship between species richness and invasion.

R. Shea and Chesson (2002) suggested that the divergence can be reconciled by considering the scale of observation. Rather. all based on analyses of real ecological systems. Johnson: Mechanisms of invasion Dunstan and Johnson 2004. 2005). water supply was the varying resource). observations at large scales across multiple habitat types will show a positive relationship between species richness and the number of aliens. including invasive aliens. competition was intense and new plants had a reduced rate of successful establishment. Here we suggest that this notion applies to ecological systems in general. Meiners et al. 2004. is that the positive relationship between richness and the likelihood of invasion stems from particular properties of component species and their interactions to generate particular patterns of resource utilisation and community dynamics. Brown and Peet 2003). Since the results of this suite of studies are diametric to the conventional view (after Elton 1958) and its modern synthesis (e. 2004. Jiang and Morin 2004). This implies that a community with one or two dominant species will be more resistant to invasion than those where the abundances of species are more even. Thus. These conflicting results. This hypothesis has been supported by recent empirical work (i. Shea and Chesson (2002) argue that at smaller scales. limit the establishment of the invader into the community. thus. Dunstan and Johnson 2004). Invasion resistance: an alternative viewpoint based on resource variability Shea and Chesson’s (2002) synthesis does not account for the mounting number of studies that find positive or varying relationships between richness and invasibility (as a function of the number of alien species present) at small scales within the same habitat type (Davis and Pelsor 2001. 1999. (2004) found that patterns of native and alien species richness were positively correlated within four sites located in grassland and desert biomes. who were principally concerned with invasions into plant communities. Communities with particular species were more resistant to invasion than others without these species. In any community. Shea and Chesson 2002). we suggest that the common unifying feature across all of these studies. which reduced the ability of invasive (and other native) species to establish and spread in the community. argued that there is no reason to suspect that richness per se should be correlated with invasibility. 2004. Thus. within the same habitat type. opportunities for invasion of patches dominated by relatively few large long-lived colonies/individuals were notably fewer than in patches characterised by a large number of small colonies/individuals.e. including poor habitats unable to support many species (native or alien).362 P. Dunstan and Johnson (2004) similarly found that the frequency of recruitment into an established marine epibenthic community increased with increasing species richness of patches. 2004. If the available resource fluctuates more rapidly than the established individuals are able to respond.g. They suggest that since environmental heterogeneity increases with scale. Invasion resistance: the importance of spatial organisation Closely related to the issue of variability in resource availability is that of spatial effects. Larger colonies were less likely to die (and so free up space for new recruits) than smaller colonies. When resources were limiting (in their study. independently of total richness. Levine 2000. As the broad thesis of this paper. Meiners et al. Because resident individuals will be unable to respond instantaneously to fully utilise a resource that becomes available (either through the resource increasing or the release of resources through the death of resident individuals). when there are pronounced fluctuations in resource availability there will be more opportunities for a new species to establish. These patterns may be explained by the spatial variation in resource use and supply (Davies et al. the relationship between richness and probability of invasion depended on the particular composition of the recipient community. the relationship between richness of the recipient community and resistance to invasion may be either positive or negative. Smith et al. depending on the nature of the limiting resource base and the mechanism(s) underlying its variability. . further colonisation will be limited by the availability of resources. observations at large scales will encompass several habitat types. competition was weak and establishment of new plants was significantly easier. They suggested that these patterns were w42x driven by the higher resource utilisation of the resident communities with one or two dominant species. When water was not limiting. and favourable habitats able support a large number of species (native or alien). (2000). At this point. species-rich patches will be more resistant to invasion than species-poor patches. Davis and Pelsor (2001) tested this hypothesis in a terrestrial plant community and found that resource supply was a critical determinant of invasion success.K. but not by the average conditions across large scales. The primary mechanism arose as a result of size-specific mortality. Cleland et al.. Davis et al. in line with Elton’s initial ideas. it is useful to examine the underlying mechanisms in more detail. The common element in these studies is the capacity of the established community to utilise resources and. which were inevitably more species-rich. within a habitat type. they also found that the relative abundance of alien species was negatively correlated with the richness of native species. This mechanism need not be directly related to richness. Cleland et al.. They identified two different mechanisms that underpin this pattern. Davis et al. Dunstan and C. (2004) found that invading species did not always respond in a monotonic way to increasing richness. species (whether alien or native) will tend to colonise until either the resources available are exceeded or environmental limits are reached. then ‘‘peaks’’ in resource availability will facilitate establishment of new individuals. However. (2000) first suggested that the magnitude of fluctuation in resources could be the key to determining the likelihood of establishment of new species into a community. Many communities. Conversely. Stohlgren et al. Levine 2000. which cover a diversity of ecosystem types. Meiners et al. including space. have provoked intense debate (Levine and D’Antonio 1999). so that the relationship between richness and invasibility is negative. Accordingly.

Again. so that multiple species with similar resource needs could not survive.g. the harder it is to find a stable equilibrium.. and considered further by Roughgarden (1974) and Abrams (1975). MacArthur and Levins (1967) and Roughgarden (1974) found that the success of an invasion was severely constrained by the size and shape of the utilisation curves. 1984. 1984.P. Thus far. However. invasion resistance declines with increased richness (e. are not in equilibrium.g. show a nonrandom spatial arrangement of species within and between habitats at most spatial scales. we explore the possibility that niches and limiting similarity are not necessary to explain the success or failure of an invasion into a system. Sousa 1979. and they were allowed to run to stable equilibrium after the addition of an invasive species whose resource utilisation was the average of the existing community. for a fixed resource limit. 1991) are usually based on a mean field approach. species (e. the identity of species adjacent to disturbed areas (and their reproductive state at the time of the disturbance). exist as dynamic mosaic of patches. by discarding the assumption of equilibrium it is possible to consider effects of fluctuating resource availability. His model simulates invasions into artificially constructed communities of differing sizes. If there is a single resource. 1981. 2004).. The extent of overlap of the resource utilisation curves of any two species defines the intensity of competition between them. This is. the niches of all species will completely overlap and the fate of an invasion will depend on other properties of the system. Modelling is useful as a powerful way to generalise empirical results. which may generate behaviours different from those reported thus far.g.. whether dominated by seaweeds or not. Fridley et al. at least in part. The methods were initially established by MacArthur and Levins (1967). Among the most frequently cited papers are those of Case (1990. Robinson and Valentine 1979. of course. Dayton et al. the more species there are. of course. and on the identity and phenology of local neighbours. then by definition. Valentine et al. and opportunties for dense patches of particular species to develop that limit colonisation by other. among others. 1984.. Case 1990. and it is assumed that two species with identical resource utilisation curves cannot coexist. 1991. Each species has a resource utilisation curve that defines the shape of resource utilisation over that resource dimension. Doak et al. The outcomes of models are. dependent on their inherent assumptions (e. but demonstrate some common behaviours. In both we examine whether invasibility is dependent more on particular properties of w43x . However. since communities can often be viewed as collectives of local ‘‘patches’’. and to more fully explore concepts. Byers and Noonburg 2003.g. and the invaders would be excluded under many scenarios. 1991) and later versions using a similar approach (Byers and Noonburg 2003) show that. Drake 1990. Johnson and Mann 1988. they have not been embraced widely by modellers. 1998. Empirical observation suggests that marine communities in general. They found that as the number of species increased. a gross simplification of the structure of natural systems. Secondly. results of models have supported the tenet that invasion resistance increases with species richness. Most communities.K. and patterns of interspecific interactions on invasion dynamics. 1984. Law and Morton (1996) also found that invasion rates decreased as they increased the number of species in their assembled systems. Dayton et al. reflect a particular history of resource variability. the resistance of the community to new species increased. their models relied on the stability of the Lotka-Voltera equations to define the success or otherwise of a new species entering a community. Case 1990. Invasion resistance: this paper Against this background. it follows that spatial pattern can potentially strongly influence broader scale dynamics. Sousa et al. While these kinds of spatially explicit mechanisms are well recognised by experimentalists. Sousa 1984).. The model communities assembled by Case (1990. In the first model we focus on the importance of resource variability and the interactions this may have with species richness and invasion resistance. 2007). invasion success declines as the number of species in the recipient community increases. Shigesada et al. 1991) extended the ideas of this early work and considered multispecies systems of more than three species. patterns of resource utilisation. These results are in accord with the patterns found by May (1972) who showed that the potential parameter space for multispecies Lotka-Voltera equations decreases as species number increases. even dominant. Law and Morton 1996. Pivotal to the construction of these models is the assumption that species consume resources from a single resource dimension.g. 1991) were constructed in such a way that they were always analytically stable. Hewitt and Huxel 2002). and exploring the effects and validity of assumptions is an important exercise. Johnson: Mechanisms of invasion 363 including seaweed vegetation (e.e. conventional models of invasion dynamics (e. The structure of these communities was limited by similarities in resource utilisation. Invasion resistance: approaches using modelling Models are useful tools to help develop and clarify thinking about invasion dynamics and the underlying processes. namely stable equilibria and limiting similarity. we developed two models to examine effects of fluctuations in resource availability. For example. in some cases. and seaweed communities in particular. Importantly. Chapman and Johnson 1990. which implicitly assumes a fully mixed and homogenous arrangement of individuals. In other words. Case (1990..R. In the second model we consider the importance of spatial interaction between adults and the influence of network topology (i. The two models make quite different assumptions about the dynamics of species. 1991). The models of Case (1990. Dunstan and C. These examples emphasise that the dynamics of a particular patch can depend in large part on spatial patterns in disturbance. and models have not reproduced the empirical finding that. it is well established that seaweed community dynamics can be strongly influenced by spatial patterns in disturbance. spatial structure. we question the two key assumptions that underpin these models. richness and connectivity) on the outcomes of invasions. Thus. A given mosaic will.

there will be 50 individuals of species x and if ry is 10 there will be 5 individuals of species y. competitive interactions may play an increasingly important role in preventing the establishment of an invader. if rx is 1. 7.000 times. The probability of mortality di can be either independent of the species resource consumption or inversely related to the resource consumption of the species r vive within a given habitat. up to 50 individuals of the new species are added to the system. After 2000 iterations of the model. 5. if a species (i) i consumed 100 resource units (rs100). Johnson: Mechanisms of invasion communities. depending on patchiness in the distribution of species. and the number of individuals of the new species at 2500 iterations is recorded. but over large areas of parameter space this would not change their qualitative behaviours. The model is a non-spatial individual-based system where individuals do not compete explicitly as adults. Methods Model 1: non-spatial individual-based model Our first simple model allows fluctuations in resource availability. particular individuals or patches will have more opportunity to respond to free space than others. The number of species at this point is uncontrolled and can vary between 2 and 20. either recruit or adult. It was also a deliberate choice that the models are schematic because this simplicity enables clear explication of the underlying principles. The community is initialised with 20 species and a total resource pool (K) of 1000. each species i is randomly allocated a resource consumption rate ri. a critical element of Model 1. then individuals are added until the system reaches K. increasing resource use will reduce the probability of mortality. and a spatially explicit environment. If a species goes extinct locally then no more offspring are produced. we relate the findings of these general models to the particular attributes of seaweeds in predicting broadscale patterns of their invasions. The time when the new species is added is arbitrary. mortalitysdi) and second. We introduce competition because any relationships between species richness and invasion evident from Model 1 might be altered by competition between adults. of any species. The number of species present at 2000 iterations. or all resources are consumed and no new offspring can recruit to the community. The model is run for two different scenarios. and adding species to the model at different times makes no difference to the final results (other than ts0). Davis and Pelsor (2001) showed that as resources became limiting. For any given combination of parameters the simulations are repeated 10. a new species invades the system. first where mortality is independent of the resource consumption of individuals (i. or on aggregate community measures such as richness. 3.9. Each individual consumes r resources from the total pool of resources K. In the latter case. If there are insufficient resources to support 50 individuals. This logic suggests that spatially explicit models of invasion dynamics may yield dissimilar dynamics from their mean field counterparts. depending on the random walk process that has occurred. The value of K is held constant for the duration of the simulation. its resource base is freed and added to the pool of free resources.R. Each species has a birth rate. but the total resources consumed varies as individuals reproduce and die. The variability of free resource is calculated as the variance in unconsumed resources between 1000 and 2000 iterations. This trade-off between births and deaths ensures that all species remain neutral in terms of their ability to sur100 1q w44x . the probability of mortality would be di2. Each species (i) has a resource consumption ri. In all simulations bis di /0. The number of individuals is varied to ensure that each species consumes the same total resource (50) when the model begins. Depending on resource availability. Mean resource variability. 100 1q Model 2: spatially explicit individual-based model This model introduces two complexities absent in Model 1. namely interspecific competition between adults. where mortality is dependent on resource r consumption (i. In other words.e. For species where di is reduced. and the particular location and timing of disturbance. species richness and number of successful invaders over the 10. Dunstan and C. which determines the likelihood of an individual producing a single offspring. The design of the models was deliberately kept simple so that we could search for general patterns and dynamics. and it cannot be displaced by another individual. competition increased and the establishment of invading species was limited. once an individual is established it is able to maintain its share of the resource base until it dies. The model rules are: 1. Thus. Offspring from all species are randomly assigned to the community until all new offspring have been assigned to the community. 1). that determines how much resource an individual requires to survive.. We are not attempting to develop accurate simulations of particular equilibrium or non-equilibrium scenarios for seaweeds. For each scenario. rather than following a random walk. For example.e. 2. For example.000 independent simulations are calculated. Each species has a death rate.364 P. but are looking for our models to deliver clear signatures of nontrivial general behaviours. As the strength of interspecific competition increases..K. which determines the probability of an individual dying. mortalitysdi ). drawn uniformly between 1 and 20. which so that dsdi . di (0. We could make the models more complex and ‘‘realistic’’ in many ways. bi. Finally. This ensures that the population will grow towards the carrying capacity. 6. When an individual dies. the magnitude of bi is reduced by a similar amount. 4. Since di ranges between 0 and 1. This model is made spatially explicit in part because it provides a mechanism to introduce resource variation.

so connectivity is set by the strength of the interaction. the two models as presented represent different ends of a spectrum.P. PrwY displaces and overgrows Xx. In comparing the dynamics of spatially explicit and equivalent mean-field models..K. and each disturbance event cleared a square of 49 cells. Garlaschelli et al. since patches were highly dynamic. Habeeb et al. and recruitment was open. Using this basic model architecture. Thus. 1999. with spatial organisation where ‘‘colonies’’ were allowed to form.. and all species could propagate vegetatively. Connectivity is usually defined on the basis of the number and strength of pairwise interactions (e.. These species were allowed to grow and the system spatially self-organise to occupy the entire landscape. which enables individual-based models of competition among species on a 2-dimensional landscape. viz.g. We allowed an initial recruitment of 18 ‘‘native’’ species to an empty landscape..e. Case 1990). with each species recruiting with equal likelihood. The likelihood of a disturbance event associated with any single cells10-4 per timestep. Johnson and Seinen 2002). Johnson 1997.5% of the landscape). a neighbour Cy is selected at random.zoo. such that an w45x . In this context. Indeed. s: indicates standoff.htm).g. that if mortality and recruitment rates were made very large and competitive interactions reduced. Effect of connectivity on invasion rates The prevailing paradigm is that communities characterised by high connectivity among species are more resistant to invasion than poorly connected communities (e. and updating of the landscape was synchronous. and the likelihood of Cy displacing Cx is given by PrwCy)Cxx. Recruitment was to empty space on the landscape made available by random disturbances which cleared clusters of cells on the landscape. Interactions among any two species X and Y were determined by three probabilities (sPr) that sum to unity. in any one time step 784 cells were cleared (. at the same rate irrespective of the presence and abundance of adults on the landscape. Model rules All spatially explicit models were undertaken using the Compete software (available at http:// www. Johnson 1997. all parameters relating to the biology of individual species and outcomes of interactions between species were identical in the two models. south. Johnson: Mechanisms of invasion 365 assume a uniform distribution of component species. the only instantaneous mortality that occurred was through disturbance. Durrett and Levin 1994.. The qualitative results do not depend on our simplifications to assign all species identical growth and recruitment rates and eliminate instantaneous mortality. When a cell Cx is occupied. on first. east and west). All models used a landscape of 400=400 cells with zero boundary conditions (i. without spatial organisation where the positions of cells on the landscape were randomised between each time step. Prwstandoff between X and Yx (Figure 1).. i.R. however. Growth into an empty cell with at least one occupied neighbour in the von Neumann neighbourhood is determined by selecting the state of a neighbour chosen at random. Effectively. the four adjacent cells to the north.g. Arii and Parrott 2004). PrwX displaces and overgrows Yx. a pair of species does not interact if their interaction is defined as a standoff.e. and all recruits of all species initially covering a total of 2% of the landscape. the landscape surface was toroidal to avoid edge effects). Note. the system is maximally connected in the sense that each species potentially competes with all others for space win an S species system there are S(S-1)/2 possible direct pairwise interactionsx. 2003. simulating the dynamics of a mean-field model.e. recruits continued to arrive at the landscape Figure 1 Possible outcomes of interactions between a pair of species X and Y. they develop as patches or colonies as a result of vegetative growth (e.. Johnson and Seinen 2002. We ran the model under two different scenarios. and second. continuously overgrowing and displacing one another. Dunstan and Johnson 2005).utas. Molofsky et al. then this model would behave similarly to Model 1. Dunstan and C. it is well established that spatially explicit models may demonstrate qualitatively different behaviours from otherwise identical non-spatial models (e. all species on the landscape had identical recruitment and growth rates. ): indicates overgrowth. 2005. which defines the probability of species Cy winning an encounter with Cx. species do not usually exist as individual cells except when they first recruit to the we examined the effect of connectivity in the network topology and species richness on the capacity of ‘‘alien’’ species to invade self-organised landscapes of native species. rule structures for overgrowth defined a probabilistic cellular automaton based on the von Neumann neighbourhood (i. Instead.g. In our models. In all simulations. Note that in spatial models of the kind used here.0. Borrett and Patten 2003. This does not mean that a given patch/colony was immortal. In all simulations.

Johnson: Mechanisms of invasion approximately consistent community structure was attained.. (1998) where fluctuations in the abundance of a single species are averaged out as species richness increases. This process is equivalent to the process proposed by Doak et al.0.R. and invasion success is correspondingly reduced (Figure 3E. Thus. determined at random. invasions are also more successful in communities where resource consumption is variable between species (Figure 3A). but in every case the number of standoffs in the interaction matrix was identical. and other factors.01 or 0. However. When mortality is independent of individual resource consumption. Case 1990. the strengths of interactions not involving 100% standoffs could vary at random. species-rich communities resist potential invaders more effectively than species-poor communities. the level of invasion of an alien species should be approximately constant for a fixed number of native species and connectivity in the recipient community.e.0 such that sum of all three probabilitiess1. there are fewer resources for the newly arriving individuals and it is more difficult for the invading species to establish. we also conducted Monte Carlo sets where reversals were permitted. Thus. the abundance of the invading species is negatively correlated with species richness (Figure 2A). where a species X displaces a species Y on all occasions in time and space. We recorded the cover of each alien species 500 time steps after the first opportunity for introduction. i. irrespective of whether mortality is dependent or independent of resource utilisation (Figure 2B). This landscape was then opened to potential invasion by two ‘‘alien’’ species. The loss of an individual from a species that requires few resources frees fewer resources than loss of an individual utilising a greater proportion of the total resources. In marked contrast to this pattern. with the recruitment rate of all species (native and alien) held at either 0. Stachowicz et al. When a species-rich community is invaded. it is highly unlikely that the outcome of interactions between any two species is binary. PrwY)Xx and PrwXsYx can take any value in the interval 0–1. each Monte Carlo series consisted of 1000 runs. Thus. Note. We define connectivity as the proportion of standoffs in the 190 possible pairwise interactions in a 20-species system. Again. Depending on differences in size. the more resources an individual utilises. we first ran sets of models where reversals in interaction outcomes were not possible. that the correlation between invasion success and resource variability is positive. For each level of connectivity. (2002) demonstrated that this mechanism reduced invasions in some subtidal marine invertebrate communities (but see Dunstan and Johnson 2006). Because the dynamics of both alien species were virtually identical. we ran cases where outcomes were binary (either species X displaces Y. Results Model 1: resource variability and the relationship between mortality and resource utilisation Although the model is intentionally simple.4 new individuals of each species recruited to the landscape each time step. Other aspects of the models were as described above. showing the same general relationships between species richness and invasion as other model communities (e.g. w46x and where reversals were possible. thus.001 per vacant cell per time step. Where interactions were not 100% standoffs. with the direction of win or loss determined at random.0. 1991.F). as outlined above. with all other interactions defined as a binary outcome (win or lose). both with recruitment rates identical to the native species. the network topology defined by the interaction matrix was determined randomly.K. in every encounter). For pairwise interactions that did not result in a standoff. if mortality rates are dependent on levels of resource utilisation. however. defined in terms of the number and strength of interactions. In nature. unlike the . is identical. it is more usual that reversals will arise. or Y displaces X. resource variability associated with mortality of an individual in a species-rich system is less than in a species-poor system (Figure 3D). Thus. while the number of 100% standoffs was identical in all runs. as occurs in communities where mortality is independent of resource utilisation. Dunstan and C. For all 20 species in this system. the dynamics demonstrate several important behaviours. thus. Effect of network topology on invasion rates If invasion rates are determined largely by the richness and connectivity of the recipient community as is suggested. We also compared the effect of differential recruitment rates. Where mortality is dependent on resource utilisation..366 P. the connectivity of each random configuration of the interaction network. We examined this premise using the models described above for a simple recipient community of 10 native species. where PrwX)Yx..e. in different runs within any given Monte Carlo series. since the total utilisation is always limited to 1000. When mortality is independent of individual resource consumption. each different run in any Monte Carlo series had identical connectivity. then for a given rate of propagule arrival. such that X will prevail in some circumstances and Y in others. determined randomly. with a single alien as a potential invader. the fewer the number of individuals that can be packed into the community. on average.01. Thus. the interaction matrix defining the network topology of the system was determined at random. species-rich communities have more species that consume fewer resources. where either PrwX)Yx or PrwY)Xxs1. Law and Morton 1996). i. the probability of recruitment to an empty cells0. physical environment. Note that where the outcomes of non-standoff interactions are binary. based on the number and strength of interactions (the usual way to define connectivity). the mean covers of the two invasive species were recorded after 200 time steps. Note that for these runs. then invasion success is positively correlated with species richness (Figure 2A).0. . the identity of other neighbours. A standoff between a species pair X and Y is defined as PrwXsYxs1. Thus. and where the number of standoffs in the interaction matrix was fixed (arbitrarily) at 45% and assigned randomly in each run. For each level of connectivity we conducted Monte Carlos of 1000 runs. The mechanisms underpinning these patterns reflect patterns of resource availability.0.

Both patterns arise in both models although they have very different underlying structures and assumptions. and species consuming a relatively large amount of available resources have lower mortality rates. This example shows clearly that. if connectivity is high (i. it is the species-poor communities that have the lowest resource variability and the least successful invasions (Figure 3B. 10% of random topologies) in which the alien species fails to establish at all. Case 1990.. or whether reversals occur in pairwise interactions that are not standoffs (Figure 5). This tendency is exacerbated because the self-organised patch size in systems with high connectivity is.K. in the non-spatial. In contrast. Note that repeated runs of the same network topology give virtually identical outcomes. Also. In marked contrast. Dunstan and C. become locally extinct.C). as a function of the maximum resource units consumed. consistent with the conventional view (e. When the number of standoffs in a network is high.g. Thus. despite repeated reintroductions of propagules. In ca. Model 2: effects of connectivity and network topology on invasion In all spatial models. depending on the local arrangement of species. the alien invaded to occupy )10% of the landscape at 500 time steps. Simulations with mortality dependent on resource utilisation are closed circles while simulations with mortality independent of resource utilisation are open triangles. case where mortality is independent of resource utilisation. the likelihood of invasion decreased with increasing connectivity of the community. the tendency to resist invasion is highly variable depending on network topology. but otherwise equivalent models. the resultant level of invasion can be highly variable. there is a high likelihood of an individual being adjacent to another species that can be overgrown. and in about 2% of cases the invader spread to occupy )50% of the landscape over the same time period. Dunstan and Johnson 2004. there is relatively little likelihood of a given patch of one species residing on the landscape adjacent to another species that it can overgrow.P. Johnson: Mechanisms of invasion 367 Figure 2 The correlation (Kendall coefficient) between (A) species richness and invasion success. larger than that in models with a high proportion of standoffs. This qualitative pattern was evident irrespective of whether non-standoff interactions permitted reversals or not. irrespective of the level of recruitment of the alien. These species retain a larger proportion of the available resource. Maximum resource units consumed defines the potential maximum number of resource units that can be consumed by an individual. on average. 2000.. the number of standoffs is low). at higher levels of connectivity. and there is no consistent relationship between invasion success and species richness. 1991). or being overgrown by a neighbour.e. the likelihood of invasion was notably higher in the spatial than in equivalent nonspatial systems (Figure 4). It is reasonable to expect that richness can be either positively or negatively correlated with invasions at a local scale depending on the nature of component species. and species-richness declines as those species that consume less.e. These patterns are also interpreted most readily in the context of resource availability. 2006). and (B) resource variability and invasion success. Variation w47x . While in most cases the alien species occupies )0% but F10% of the landscape after 500 time steps. 25% of cases. for a given fixed connectivity and richness of the recipient community. a given individual patch is more likely to overgrow other species or be overgrown by others than in communities where connectivity is lower. the likelihood of invasion at first increased with increasing connectivity (i. but the topology of the interaction network is allowed to vary. This is because species in speciespoor communities are more likely to be large consumers. effects of competition) before levelling off (Figure 4). increasing Discussion: invasions into marine algal communities General The key finding in the behaviour of both models presented here is that the likelihood of invasion increases with variability in resource availability in the recipient community. If connectivity and richness of the recipient community is kept constant. and external forces (Davis et al. but die fastest. there are many occasions (ca. the dynamics among species.R..

.) that spatial variability in resource availability was responsible for the positive correlation between richness of aliens and natives at large scales. but otherwise identical models.R. Non-spatial models show increased resistance to invasion with increasing connectivity.K. growth and mortality). respectively. Solid triangles and crosses are results for equivalent non-spatial. irrespective of whether non-standoff interactions allow reversals or not. Johnson: Mechanisms of invasion Figure 3 The relationships between invasion success. By consid- w48x . (2005). The probability of potential invaders attaining )2% or )5% cover after 200 time steps is estimated from Monte Carlo sets of 1000 runs. and that this pattern is generated as a function of temporal resource variability. At least in part. Figure 4 The effect of connectivity on levels of invasion in a model 20-species system. the precise topology of the interaction network has a large influence on the susceptibility of the system to invasion (Figure 5). for a given connectivity (and richness). however. These results are consistent with the behaviours of the real ecological systems reported by Davis and Pelsor (2001) and Dunstan and Johnson (2004). Dunstan and C. in resource availability is influenced not only by external environmental forcings.. while the spatial equivalents demonstrate decrease in resistance to invasion with increasing connectivity. Maximum resource utilisation (r) equals 15. If we exchanged variation in time (our models) with variation of resources in space. then even small fluctuations may release sufficient resource to enable a successful invasion. there will be more opportunity for successful invasions when there are large fluctuations in resource availability. characteristics of recruitment. if resources are limiting. Solid circles and squares show results for spatial models considering alien species that exceed 2% and 5% cover. and structure in the spatial arrangement of individuals. patterns of interspecific interactions among species. Notably. On average. our results are limited to a single patch but we have shown that both patterns of positive and negative correlations between native and alien species are possible at small scales. cit. They suggested (op. but can be strongly influenced by the population dynamics of component species (i. Dotted lines are results of spatial models in which interactions that are not 100% standoffs allow reversals in outcomes (indicated by ‘‘with reversals’’). species richness and resource variability for simulations with dependent mortality (A)–(C) and independent mortality (D)–(F). but at small scales (within a patch) natives and aliens were negatively correlated.e. it is not only system-wide patterns of interspecific relationships (e. Connectivity is defined as the percentage of 100% standoffs in the matrix of possible pairwise interactions among species. differences in demography and outcomes of interspecific interactions reflect interspecific differences in the capacity of species to utilise resources. connectivity) that are important but. our results would be similar to those of Davies et al. Clearly.368 P.g.

R. Reversals of this kind arise commonly in benthic marine systems (e.P. ering both our work and that of Davies et al. Seaweed communities Is there any reason to expect that seaweed communities may demonstrate any similarities with our models? In a broad sense.K. would utilise all the resource available until it ultimately utilises the maximum level of resource available. and (C) all non-standoff interactions have a unanimous winner and recruitment is low. Results are given for communities where (A) all non-standoff interactions have a unanimous winner and recruitment is high. We have not attempted to present a general theory of invasion dynamics. despite utilising the same resource and ‘‘competing’’ as recruits for limited resource. like other species. By relaxing assumptions about resource partitioning we have been able to demonstrate that both positive and negative correlations between invasion success and species richness are possible. multiple species can co-exist.. utilising information on species identities. resource supply and utilisation and propagule supply.g. even in these circumstances. require a wide variety of resources (e. that invasion success decreased with increasing richness of the recipient community. in line with the established view. Seaweeds. a single set of runs showed either significant positive or negative relationships between invasion success and richness depending on the magnitude of invasion that was considered (results not presented in detail here). The same principle has been demonstrated in spatial models of particular natural systems that proved to be good predictors of the global community dynamics of the real system (e. while non-zero values indicate the upper limit of a class covering 10 percentage points. while in others Y displaces X.e. ‘‘0 (DNE)’’s‘‘did not establish’’. If a higher threshold of invasion is considered (the alien covers G5% of the landscape after 200 time steps).. ‘‘80’’ indicates runs where the cover of the invader after 500 timesteps was )70% and F80%. and to identify which particular combinations of factors act to promote or resist invasions. the models of Levins and Macarthur (and. in general. However. the relationship between invasion success and richness is positive. Dunstan and Johnson 2005). e. In terms of classic niche theory. (2005) a more general theory of invasions should be possible. see introduction of Johnson and Seinen 2002. In these runs mortality was independent of patterns of resource use.g. Notably. On the y-axis. a species X competitively displaces Y. 1991) emphasise a deterministic framework with a hierarchical competition structure. the network topology is not strictly hierarchical and. It is worth noting that in the spatially explicit model (Model 2) we could devise run sets that showed. Both of the models presented here emphasise population stochasticity and resource utilisation either with (Model 2) or without (Model 1) competition between adults for space. Where competition for space is included. pathogens).. indicating runs where the alien species was absent from the landscape after 500 time steps. It remains to thoroughly test those principles deemed as general.g. predation. Other factors not included in our models will almost certainly affect the outcomes of invasions (e. all the species share the same niche as the overlap in resource requirements is 100%. Frequencies are determined from Monte Carlo sets of 1000 runs.. by extension. However. and are subject to a suite of evolutionary pressures similar to those of any other group of organisms which co-occur in a given habitat.g. seaweeds share many ecological characteristics with. (B) outcomes of non-standoff interactions are characterised by reversals and recruitment is high. A single species. Case 1990. furthermore. We highlight this point to emphasise that inconsistencies in the relationship between invasion success and richness of the recipient community arise at several scales of resolution of the system. propagule pressure. but have added to a developing list of considerations that is moving towards a more generalised and integrated viewpoint.. the models presented here are generalised schematics designed to elucidate patterns that may occur in seaweed (and other) communities.g. For low-level invasions where the invading alien species manages to cover at least 2% of the landscape 200 time steps after the first arrival of propagules. some run sets allowed reversals in outcomes whereby at some points in space/time. the relationship between invasion success and richness of the recipient community is negative.. without any other species present. with 45% of interactions in the network as 100% standoffs. Dunstan and C. Dunstan and Johnson 2005). In our model communities there is a single resource (i. just as in the configuration of Model 1 that yielded a similar result. w49x . space) that all species must utilise to survive. Johnson: Mechanisms of invasion 369 Figure 5 Levels of invasion of a community of 10 native species defined by the frequency of cover attained by an alien species 500 time steps after the first arrival of propagules. In contrast. connectivity is held constant. In all cases.

Phillips and Hurd 2003).g. Chapman 1984. Seaweeds manifest a variety of strategies in responding to variation in these resources. These strategies realise tradeoffs in competitive ability... seaweeds have evolved a plethora of strategies to optimise their survival. Species will respond to this variation and during periods of excess resource availability. nutrients. Dayton et al. Probyn and Chapman 1983).R. 1997). 1984. ongoing persistence of an introduced seaweed may require mechanisms to prevent natives from eventually regaining domination of space (e. shading the photosynthetic w50x tissue and preventing high recruitment rates and rapid growth. and it is usual that only a relatively small number of these resource dimensions (typically nitrogen. seaweed communities are unlikely to differ from many other kinds of communities. Zimmermann and Kremer 1986). However. Silva to invade when light (and space) resources became available.g.K.. ´ 1982.. 2002). with the smallest .. with less vulnerability to ‘‘mortality’’.g. recruitment potential and mortality.g. Small-scale variation in nutrient availability can also arise.g. Lobban and Harrison 1997).. influencing the survival of both juveniles (e.. examples in Lobban and Harrison 1997). Species able to efficiently and rapidly uptake available nutrients may locally limit the availability of the resource to newly arriving propagules (e. 1984. 1982). and that the patterns of resource variability will be an important determinant in the invasion success for a given density of alien propagules. In these generic properties. and it is through these windows of opportunity that alien species can initially recruit to the community.g. The critical point is that the ability of a community to resist the establishment of new populations comes not from species richness or diversity but from the ability of the suite of species that is present to utilise the maximum amount of resources over the long term. see also Valentine et al. Sousa 1984.)x which overgrows the kelp blades. 2001) and adults (Gerard 1982. (2) the pattern of utilisation of resources by the recipient community. and to form dense patches that effectively excluded re-establishment of the kelp (Chapman et al. 2002. 2007). For species such as the kelp Saccharina longicruris (de la Pylaie) Kuntze which realises a prodigious reproductive output (Chapman 1984) and uses stored nitrogen to achieve high growth rates under optimal light conditions when available nitrogen in the water column is low (Gagne et ´ al. space. Finally. Dunstan and C. Gagne et al. Rees 2003. we suggest that seaweed communities are also likely to demonstrate properties that our models suggest will realise positive relationships between invasion rates and species richness of the recipient community. and play a key role in shaping the mosaic of patches that so often arises in seaweed systems (e.. this dynamic was changed markedly with invasion of an alien bryozoan w(Membranipora membranacea (L. Valentine et al. Conclusion The success or failure of an invasion will depend on at least three aspects of the recipient community: (1) the amount of resource available across the resource spectrum.370 P. and consequently increase the risk of invasion. The weight of evidence suggests that larger and denser patches of a particular species are better able to locally monopolise resources. ranging from storage of nitrogen to be used for growth in times when nutrients are not available or light levels are more suitable (e. However. light and nutrients) and will vary in space and time. space) for survival. The role of environmental stresses or disturbances.g. Whether the invaders survive will be determined by continuity in resource supply and competition for those resources with other species in the recipient community. reflecting different underlying capacities to utilise resources and different strategies (in an evolutionary sense) in allocating them. This then enabled Codium fragile subsp. The particular dynamics of any community will release resources in space and time.g. tomentosoides (van Goor) P. longicruris appeared able to maintain its dominance of the system and that opportunities for invasion were remote (Johnson and Mann 1988). demonstrate differential capacity to utilise these resources in optimising their growth and reproduction. light. Johnson: Mechanisms of invasion trace and other elements.g. and so interactions in the availability of nitrogen and light may arise. Chapman and Johnson 1990).g. than smaller patches (e. and then using this nutrient directly for growth rather than storage (e. it is perhaps not surprising that individuals are able to rapidly capitalise on breaches in the canopy that locally release resources of light and space (Johnson and Mann 1988). depending on the species. Korb and Gerard 2000. Like other organisms. We therefore expect that the characteristics of the established individuals at a site will influence the patterns of resource variability at that site. This mechanism may be particularly prevalent at lower latitudes where nutrients may be limiting (Steneck et al. The resource spectrum is defined as the magnitude of the resource dimensions (e. growth and reproduction (e.. and also influences the growth of clonal species (Santelices 2004). It is worth noting that by this mechanism S. The availabilities of space and light are usually closely linked. light are nitrogen as limiting factors. This example highlights a complex suite of mechanisms that realised sufficient variation in resource availability to enable a significant invasion event. growth and reproduction in the face of variability in the availability of limiting resources. Dayton et al. vitamins. 2007).C. Valentine et al. Sousa 1984. grazing and other ecological interactions in creating space and facilitating establishment of alien seaweeds is well documented (e. light and space) are limiting. 2007). Hernandez-Carmona et al.. Seaweed communities will typically experience fluctuations in the availability of space. particularly as applied to patches. to a capacity for highly efficient uptake of nitrogen at low concentrations. and (3) the strength and pattern of interspecific competition and spatial organisation of the community. The most obvious is size-specific mortality. Spatial and temporal patchiness in the distribution of species able to commandeer nutrients in this way may generate small-scale patchiness in resource availability. Large-scale variation in nutrient availability often has a strong seasonal component.

and S. Oikos 87: 15–26. Reich. Seasonal ´ patterns of growth and storage in Laminaria longicruris in relation to differing patterns of availability of nitrogen in the water. Melbourne and K.R. 54: 253– 289.A. S. 2001. Methunem. Seaweed ecology and physiology. Cohen. Johnson 2006. Johnson. Theor. Dayton. 1984. 2003. 69: 91–101. Structure of pathways in ecological networks: relationships between length and number. P. Science 288: 852–854. Habeeb. 1990. M.O. 1982.R. The importance of being discrete and spatial. J. Patten.G. Patterns of invasion within a grassland community. J. 2004. Ecol. 88: 528–534. and P. Elsevier.R. Tilman and Proc. Invasion resistance species build-up and community collapse in metapopulation models with interspecific competition.R. Durrett. R.N.O. Biol. and V. Prog.K. Mar. Biol. and G. S. 4: 421–428.B. Chapman. Johnson. w51x . Currie. Ecol. Kennedy. and invasion resistance with patch size. Model. Hector.R. Laminaria saccharina (Chromophyta). 16: 819–831. 1997. Exp. R..K. Enters and C. T. A. Brown. D.M. Jiang. G. K. Borrett. 147: 213–233. R. Johnson. Smith. and I.J.M.A. Nat. P. Bigger. Popul.J.. S. Morin. 2000. D’Antonio. Sci. Fluctuating resources in plant communities: a general theory of invasibility. T. Johnson. R. Biol. Biol.. Science 261: 78–82. The role of nitrogen nutrition in high-temperature tolerance of the kelp. Parrott.M. A. Geller. 133–148. 2005. Nantele and E. Bowles.K. Cleland. pp. Davis. Gerrodette. J. J.K.P. Elton revisited: a review of evidence linking diversity and invasibility. Invasion success and community resistance in single and multiple species invasion models: do the models support the conclusions? Biol.. J.E. Dunstan. J.J. 1996. 1997. Theor.P. 2003. 2002. 42: 239–266. Limiting similarity and the form of the competition coefficient.R.E.F. Ecological roulette: the global transport of nonindigenous marine organisms. 33: 800–810. and E. Mann. Elton. L. Davies. J. Rice. Fridley.R. Roy. Oecologia 138: 285–292. Accelerating invasion rate in a highly invaded estuary.. D. S. 2003. Ven Tresca. 170: 173–184.R. Invasion rates increase with species richness in marine epibenthic communities by two mechanisms. Morton. pp. Biol.J. V. R. Drake.H. Mar. London. Pelsor.. J. S. D.D. 78: 99–109. Marvier. C. Harding.O. P. Lawton. Ecol. Claudi. Dunstan. and R. Carlton. Drake. Wotherspoon and C. Peet. Levine. 44: 221–229.E. 2001. Huxel. Invasion in space and time: non-native species richness and relative abundance respond to interannual variation in productivity and diversity. 2005. and M. Species introductions and changes in the marine vegetation of Atlantic Canada. Rosenthal and D. O’Malley and D. 2002. 1988. 2002. Knops. 2004.A. Keller. 99–208. Nature 417: 636–638.F. Biol. Lunt.K. References Abrams. Cambridge. Biol. T. Ecol. A. Ecol. Experimental support for a resource-based mechanistic model of invasibility. Bot. Biodiversity as a barrier to ecological invasion. 1991. 186: 221–233. pp. C. 2002. We see no reason to suppose that seaweed communities are an exception to this principle. eds) Alien invaders..T. P. J.A. Ecol. Ecol. and B. In: (R. Spatial heterogeneity explains the scale dependence of the native-exotic diversity relationship.. Andelman.. Ecology 84: 32–39. K.S. Dunstan. Ecology 84: 1428–1433.A.L. R. Gramling and D. and J. 227: 327–333. Mar. Hydrobiologia 192: 77–122. Amsterdam.R. Ecol.E. 90: 871–881. Reproduction. P. B.R. 1994. 1984.. Bruno. Chapman. M. 2004.S. P. Alpert.A.D. P. Ecology 87: 2842–2850.L. R. 2004. Thomson. Species diversity and biological invasions: relating local process to community pattern. Carlton. 58: 129–154. J. D.O. E. and P. Scheibling and A. C.D. Klomp and I. Gerard. J. Chapman. Theor. Holzapfel.K. 66: 27–35. Universal scaling relations in food webs. Am.D. 1998. 1998. 87: 9610–9614. In: (N.S. G. Patch dynamics and stability of some California kelp communities.H. B. and L. Lett. Johnson. Invasions 4: 263–271. Bazeley-White and J.J. 2002. Natl. Byers. 1990. K. Gerard. Selection for restraint in competitive ability in spatial competition systems. Nitrogen assimilation characteristics of polar seaweeds from differing nutrient environments. 2001. 1993. and C.L. Robledo and E. Diversity. 7: 947–957. Ecology 86: 1602–1610. Naeem. K.M. B. Effect of nutrient availability on Macrocystis pyrifera recruitment and survival near its southern limit off Baja California. Thompson. Disturbance and organisation of macroalgal assemblages in the northwest Atlantic. Case. Ecology 85: 3215–3222.A. Minnis. J. Ecol. pp. 2000. C.D. Johnson. Scale dependent effects of biotic resistance to biological invasion. 2004. A. Johnson. Inouye. 245–263. Linking richness. community variability. C.E. Vandermast. Carney. Levin. D. Caldarelli and L. Ecol.R. D. Davis.A. M. Growth and utilisation of internal nitrogen reserves by the giant kelp Macrocystis pyrifera in a low-nitrogen environment. Self-organizing in spatial competition systems. Monogr. C.C. 198: 83–92.R. 2005. and K. Dobson. A. Diversity and invasibility of southern appalachian plant communities. Ecology 77: 762–775. J.J. and C.F. Noonburg. Brown and J. Horner-Devine. Nature 423: 165–168. M. Mar. Ecol. Korb. Natural Resources Canada. Pietronero. Gerard. and R.M. and C. Lett. Monogr. Community diversity and invasion resistance: an experimental test in a grassland ecosystem and a review of comparative studies. E.M. Null models of exotic invasion and scale-dependent patterns of native and exotic species richness. A. 1958. Law. Garlaschelli. J. J. 8: 356–375. Johnson: Mechanisms of invasion 371 amount of variability. Chapman. Biol.. C. Monogr. P. R. K. Emergence of non-random structure in food webs generated from randomly structured reginal webs. Arii.M. P. K. and stability of Nova Scotian kelp beds. 151: 264–276. Phycol. Ecol. 46: 363–394. and J.M. 7: 1047–1057.. Ser. V. The statistical inevitability of stabilitydiversity relationships in community ecology. Case. Kolb.R. Model. 1982. Hernandez-Carmona. 143–153. S. Harrison. Theor.K.A. E. Soc. Grime and K.D. R. Harrison. Seinen. Gagne. Serviere-Zaragoza. The ecology of invasions by animals and plants. (London) Series B 269: 655–663. Doak.B. MuckleJeffs. M. 75: 467–487.H. Science 279: 555–558. Predicting global dynamics from local interactions: individual-based models predict complex features of marine epibenthic communities. Lobban. and C. Permanence and the assembly of ecological communities. Mar. Acad. J. Mann and A. Emery. Productivity gradients cause positive diversity-invasibility relationships in mircobial communities. Linn. J. Chesson.C. patterns of adaptation. A. Trebilco. Ecol. 1999. V. Proc. recruitment and mortality in two species of Laminaria in southwest Nova Scotia. and C. Howe.T. J. Invasion resistance arises in strongly interacting species-rich model competition communities.I. 1975. 2003. Cambridge University Press. Chapman. Hewitt.M.R.R.. T. J. Determining natural scales of ecological systems. Lett.A. 1997.H. eds) Frontiers in ecology – building the links. Ottawa. 1990. Soc.. Res. Levine. 2000. Dunstan and C. The mechanics of community assembly and succession. Popul.

2003.K. Sousa. L. Termoto. J. 29: 436–459. Stohlgren. and C. J. Meiners. D. 50: 351–360. Ecology 83: 2575–2590. R. 1955. B. Mar. J. 17: 170–176. G. M. Ser. Binkley. Prog. Whitlatch. Hurd. Exp. Morin. Allen. 1999. 49: 227–254.A. D. 2004.W. Bourque. Mar.. Ser. 1995 Invasibility of experimental habitat islands in a California winter annual grassland.J. Prog. Durrett. Theor. 1974... Will a large complex system be stable? Nature 238: 413–414. Levins. Invasions of coastal marine communities in North America: apparent patterns. K. Schell.H. and divergence of coexisting species. R. Ecology 36: 533–536. R. In situ growth and chemical composition of the giant kelp. Safety factors and nutrient uptake by seaweeds. M. Roughgarden. Species diversity and invasion resistance in a marine ecosystem.B. Erlandson. Dominance not richness determines invasability of tallgrass prairie. stability. 2002.J. 2002. and marine ecosystem function: reconciling pattern and process.D. R. processes and biases.M. Ecology 81: 99–109. recruitment limitation. McGrady-Steed. 1979. Shea. 1979. Fried. Chesson. MacArthur. M. 2000. Oikos 106: 253–262. A. Bot. Platt. Graham.P. Kremer.R. Monogr.C. Stachowicz. resilience and future. 55: 270–282. storage and utilisation in relation to shore position and season. Ecol. 1967. Ecol. A test of the effects of functional group richness and composition on grassland invasibility. J.R.H. 2004. 69: 25–46. and spatially variable patterns of succession. A comparison of ecological responses among aclonal (unitary). Species packing and the competition function with illustrations from coral reef fish. 2004. Schroeter and S. Hines.K. Phillips. 1983. J. D. 263: 29–42. N.T.W.J. D.372 P. M. The limiting similarity. Biol. 300: 31–64. T. and R. J. Biol. Community structure and forest invasion by an exotic herb over 23 years. R. 73: 243–271. G. Knapp. Estes and M. Rev. P. Bashkin and Y. Kalkhan.C. Sousa. 1984. 2006 w52x . Fluctuations of animal populations and a measure of community stability. Nitrogen ecophysiology of intertidal seaweeds from New Zealand: N uptake. Ecology 78: 81–92. Quinn and M.A.C. T. Smith. Local frequency dependence and global coexistence. and grassland biodiversity. T. W. G. Griffeath and S. Prog. Nat. 5: 163–186. Biol.A. Osman. S. convergence. Ecol. Mar. R. 1997. Valentine.J. M. Trends.B. Wilcox. Kelly and A. Am.A. Symstad. Harris and P. Nature 390: 162–165.F. clonal and coalescing macroalgae. J...J. Ecol. Magierowski and C. 2006. Kelp forest ecosystems: biodiversity. Santelices.R..P. S.. Biol. Biodiversity.V. Fofonoff. Mar. R.) C. J. Johnson: Mechanisms of invasion MacArthur. Whitlatch and R. Kawasaki and E. propagule availability. Y. Ecol.K. J. T.S. Intertidal mosaics: patch size. Theor. 81: 91–104. 1986.. Gaines. Ruiz. S.W.: physiological strategies in a nutrient stressed environment. K. Exotic plant species invade hot spots of native plant diversity. Ecol. J. Mechanisms of invasion: establishment. Robinson. 7: 121–126. Bull.T.. Rees.H. 1981. J. Probyn. B. Sousa. J. Ecology 76: 786–794. Experimental investigations of disturbance and ecological succession in a rocky intertidal algal community. Tilman. J. H. Newman. 1984. P.J.H.. P. 101: 377–385.M.D. Wonham and A. accepted 26 December. R.D. Exp. J.O. Dunstan and C. spread and persistence of introduced seaweed populations. and P. W.. The effects of interference competition on stability. 1998. Carlton. Clinton and K. Biol. J. Ag. invasion resistance. Ecology 79: 2071–2081. Ecol.W.J. Community theory as a framework for biological invasions. Johnson. Son. Beyond biodiversity: individualistic controls of invasion in a selfassembled community. J. Ecology 65: 1918–1935.C. Chapman.L. Theor.M. G.A. Picket. K. Ecol. 21: 97–133. Robinson. Stachowicz.. Math. Chong. Dushoff.. and A. Annu. Latitudinal variation in intertidal algal community structure: the influence of grazing and vegetative propagation. Cadenasso and S.L.F. invulnerability and invadability. Summer growth of Chordaria flagelliformis (O. 1999. Levin. Tegner.A. Monogr. Osman and R. J. 264: 31–48. and W.M.R. and J.P. Oecologia 48: 297–307.D. Valentine. Mar.J.H.B. 2000. Stanton. Steneck. Otsuki.L. M. Mar. Syst. Corbett. W. Biodiversity regulates ecosystem predicability. Popul. May. 1972. Biol. Ecol. Conserv. 2007. Received 7 January. J. R. Ser. Ecol. 27: 277–285. 2002. Muell. Evol. structure and invasion of a multi-species system. Molofsky. 31: 481–531. 1999.. Community invasibility. Popul. Shigesada. Lett. R. Science 286: 1577–1579. Zimmermann. The concepts of elasticity. Environ. 2003. Macrocystis pyrifera: response to temporal changes in ambient nutrient availability.N.V. 1997.J. Wiser.P.

but was not detected for many years in northern France. fishers. and divers). Even though the site of first sighting for A.2007.Botanica Marina 50 (2007): 373–384 2007 by Walter de Gruyter • Berlin • New York. Since this species is generally identifiable only with light microscopy. 1973. more frequent in areas that are most often visited by specialists. Caulerpa taxifolia (Vahl) C. This paper provides a general overview of these different approaches and the specific strategies adapted to the biological and ecological characteristics of particular species. cylindracea ˚ (Sonder) Verlaque. Farnham 1974) first detected the brown seaweed Sargassum muticum (Yendo) Fensholt in 1973 on the Isle of Wight (south coast of Britain). who often report any anomaly detected in the marine environment. Similarly. Universite de ´ Nice-Sophia Antipolis. details on the invasive capability of an introduced seaweed indicated by rates of spread are needed to assess potential impacts on native ecosystems. Small algae whose invasive character is unspectacular.M. The real date and site of introduction to the Mediterranean Sea are still not known. Huisman et Boudouresque originating from Australia was discovered in Libya in 1990. a SCUBA diving scientist working on marine phanerogams in California (San Diego) discovered Caulerpa taxifolia by chance. At the time of discovery in California. early reporting is not always the case. tracking. standardisation of geographical and density data is important. 1976). Parc Valrose. observations in the Mediterranean Sea have been spread widely in time and space. which has invaded the Mediterranean Sea. monitoring. Wollaston. and (c) assess their invasive potential. invasive seaweeds. Agardh var. thus. including mapping techniques and public awareness campaigns.. Introduction In recent decades. and identification of alien species and their vectors of introduction using both classical means (based on taxonomical and biogeographical knowledge) and molecular tools. active tracking near sources of introduction. or algae that are difficult to distinguish from native species (cryptic invasions) often go unnoticed for long periods before detection and reporting. Keywords: introduced species. in 2000. This is the case for a small member of the Ceramiales originating in Australia including Acrothamnion preissii (Sonder) E. Ribera Siguan 2003). (b) monitor their spread. 1977). two years before its discovery on the south side of the English Channel at SaintVaast-La-Hougue (France) (Cosson et al. However. This was immediately identified as the well known invasive Mediterranean strain (Jousson et al. The tracking of alien species before eradication or control measures are instigated requires special cartographic techniques. DOI 10. more than 1000 m2 of the lagoon were already covered by this species. This was the case for the green alga. Furthermore. Detecting alien invaders Passive and random detection The discovery of an alien species is often a matter of chance collection. clear directions are now emerging for optimal tracking strategies to (a) detect alien species as early as possible. preissii was Leghorn in Italy (Cinelli and Sartoni 1969). where the first sighting is often reported only several years after introduction. To identify the invaded ecosystems. and are identified through the perspicacity of a phycologist. 2000. and to describe the rate of spread and invasion dynamics. the real w53x . Agardh. Farnham (Farnham et al. even for large introduced and invasive species. The alga had probably been imported into Brittany or Normandy in the late 1960s from Japan on spat of the oyster Crassostrea gigas (Thunberg) (Gruet et al. dependent on the collection and meticulous analysis of samples by specialists. other approaches must be used. e-mail:meinesz@unice. Rapid detection is also important for identifying sources of introduction so that transport vectors can be restricted. thanks to the discerning eye of a phycologist sampling off Tripoli harbour (Nizamuddin 1991). Woodfield and Merkel 2004). sailors. Detection is.042 Review Methods for identifying and tracking seaweed invasions Alexandre Meinesz Laboratoire Environnement Marin littoral. This passive detection is aided by laypersons using the oceans for a living or for recreation (e. France. 06100 Nice cedex 2. Alien species occur perchance in sample collections. introductions of alien benthic algal species have increased dramatically in the oceans and in landlocked seas (Ribera and Boudouresque 1995. initially identified in the Mediterranean Sea by SCUBA divers when it covered barely 1 m2 of sea floor (Meinesz and Hesse 1991). for instance in the vicinity of marine research stations or in marine protected areas. Rapid detection of a species new to a geographic region can be crucial for eradication or control operations. including random sampling. they may be detected more quickly by amateurs than by professional biologists. In these endeavours. An invasion of Caulerpa racemosa (Forsskal) J. When an introduced species has a size or shape very different from those of native species.g.1515/BOT. mapping. Based on numerous case Abstract Tracking macroalgal invasions relies on a variety of approaches and techniques.

phycologists organised tracking campaigns for new introduced species. Around potential sites of elevated risk of introduction. Lane.. taxifolia and C.W. 2001). Classical techniques of identification and biogeographical knowledge of the range of the natural populations of the introduced alga are usually sufficient to establish status as an alien. a large green alga. including: • it should be new to the area studied (the original range should be clearly distinct). several authors have demonstrated that the invasive strain is monophyletic and genetically homogeneous. is also a means to ensure early detection of new alien species.g. For example. C. it then becomes more easily identifiable. were reported in the vicinity of aquaria (Meinesz and Hesse 1991.374 A. it is important to determine the frequency with which it was introduced into the different invaded areas and the subsequent pattern of spread. in the vast majority of cases. long confused with Codium tomentosum Stackhouse.. Once the introduced alga has been properly described and recognised. the site and date of first introduction into the North and Mediterranean Seas are unknown and debatable. Komatsu et al. For C. a site where several introduced species have been reported can become a focus of sustained interest for phycologists. thus. and this will depend on maintaining facilities with specialists in the taxonomy of algae and regional biodiversity. Meinesz: Tracking invasive seaweeds site of first introduction cannot be known with certainty. Coleman 1996. The molecular tools to track and identify alien invasive species are described elsewhere in this issue (Booth et al. 2000). Investing in ‘‘outreach’’ activity.g. it is clearly important to effectively monitor the arrival of introduced species. 1998). This suggests that there are only a few (at least two) separate introductions from the native populations localised in the North Pacific Ocean (Goff et al. Provan et al. Active detection Active detection is a dynamic process. genetic tools have proven very useful in establishing alien invader status. tomentosoides (van Goor) P. In the management and control of such alien species. 2007). However. In the vast majority of cases of algal introduction. for Codium fragile (Suringar) Hariot ssp. in the Mediterranean Sea and in Japan. 1997. 1995). the majority of them (43 taxa) most likely originating from the Pacific region and including some large phaeophytes we. this species had not yet been reported in the 1990s. Certain sites are particularly favourable for the introduction of species. When an invasive introduced algal species is reported. e. Silva. or aquaculture facilities where juveniles of shellfish species are imported. After the discovery of several introduced species of Japanese origin in the early 1970s. Saunders. These authors raised the possibility that the alga may have been carried from the Red Sea by currents (more than 2500 km from Monaco). Areschoug) C. A public awareness campaign about its possible arrival in Tunisia was organised in 1998 by local phycologists based on the distribution of well-illustrated brochures (Langar et al. and the potential impact of alien species. 2005). it is then sought in neighbouring regions or countries. Codium fragile ssp. tomentosoides. fragile ssp. Numerous examples of this kind of ‘‘detection dynamics’’ may be cited. once reported or given media exposure.g. in several cases outlined below. usually then arouses interest in the local and regional scientific community. In fact. and to date have discovered 45 introduced macroalgae. Thanks to this information campaign. Detection effort should also focus on the mode of introduction. more intensive observation means that introduced species may be discovered more easily. the suspected vector has not been contested.E. its origin and vectors of introduction Various criteria to recognise and designate a species as alien have been proposed. such as training members of the interested lay public about the shape and colour of native algae.. • there should be identifiable invasion dynamics (temporal and geographical).C. Areas within the vicinity of public aquaria built on the coast may also be actively investigated. where there is a major oyster farming facility. but two other hypotheses were formulated by scientists based in Monaco (Chisholm et al. Druehl et G. Saccharina japonica (J. A revealing example is the tracking of Caulerpa taxifolia in some areas of the Mediterranean Sea. the introductions of Sargassum muticum (see the compilation of 300 publications concerning this invader by Critchley et al. or was native to the Mediterranean Sea as a . Its status as an introduced species and mode of introduction seemed obvious at the time. shipping harbours where deballasting takes place. In this case. racemosa var. 1990) and of the two invasive Caulerpa species (C. Determining the alien character of a species. 1992. a fisherman reported the presence of the alga to an oceanographic centre in 2000 (Langar et al. Similarly. The newly discovered species. Similarly. 2003). cylindracea). e. It had never been observed previously in the Mediterranean Sea (Meinesz and Hesse 1991). tomentosoides This sub-species is a worldwide invader. and • sources of introduction in the area of first sighting should be identifiable. In Tunisia. Sargassum muticum and Undaria pinnatifida (Harvey) Suringarx (Verlaque 1994. Oyster spat has long been imported to Thau from Japan (from the Seto Inland Sea). Mayes. Caulerpa taxifolia This green alga was first discovered as an invader in 1984 beneath a public aquarium in Monaco where it was cultivated. the designation as alien (either through range extension or anthropogenically mediated introduction) is not contested. it is the mode of introduction that justifies the active detection of introduced species. With so much uncertainty. A spectacular case is that of the Thau lagoon on the French Mediterw54x ranean coast. and an active search can be organised. especially if the species is known to be potentially invasive with potentially deleterious impacts on the invaded environment. established. A dynamic of detection is. two cases of the introduction of Caulerpa taxifolia.

being first observed outside its native Asian range in the Mediterranean Sea in 1971 and later in the eastern North Atlantic Ocean in Brittany. 2000. demonstrated that the invasive strain in the Mediterranean Sea is identical to strains cultivated in the Monaco Aquarium. Durand et al. However. In contrast. cylindracea This species was first recognised as an invader in the Mediterranean Sea off Tripoli harbour. which rapidly invaded the coasts of most Mediterranean countries. that the invasive (Mediterranean. but it was finally determined that the invasive strains were genetically close to a population developing in a temperate region of Western Australia near Perth (Fama ` et al. other neighbouring oceans (Atlantic Ocean. Japan and California) and aquarium strain did indeed originate in Moreton Bay. It is often queried whether it arrived in ship ballast water. 2005). but implicate maritime traffic in promoting recurrent migration events from the native range to Australasia (Uwai et al. 2005). Indian Ocean) and from aquaria. The genus Caulerpa was unknown on the Pacific coasts of the USA and C. including those of Monaco and Stuttgart (which was the source of the strain cultivated in the Monaco aquaria since the 1980s). 1994. 2003). genetic analysis demonstrated clearly that this Grateloupia was misidentified. Undaria pinnatifida Debate on this species is often focussed on the vector. Meinesz: Tracking invasive seaweeds 375 ‘‘metamorphosis’’ of Caulerpa mexicana Sonder ex Kut¨ zing. Subsequently it reached most of the islands of the archipelago and became the most invasive alien macroalga on coral reefs throughout the main Hawaiian Islands. 2005. Grateloupia species Another example of the utilisation of genetic tools to elucidate the origin of an introduced and invasive alga is that of a rhodophyte identified initially as Grateloupia doryphora (Montagne) Howe. 2002a. This alga has also established in New Zealand. 2000. 2001. taxifolia and C. To settle the issue. 2002). 2002). Piazzi et al. even when collections from other areas of the Pacific Ocean and Australia were included. Valentine and Johnson 2003). taxifolia in San Diego and Los Angeles and to ban trade in Caulerpa species for aquaria. O’Doherty 2007). known on the eastern shores of the Mediterranean Sea (nearly 3000 km from Monaco) since 1945. 2000). and the vector is unknown. These analyses also make it possible to estimate the number of sources of introduction or distinct origins within an affected area.b. Ko` matsu et al. (1998) confirmed by genetic analysis that C. Genealogical analyses point to aquaculture as a major vector of introduction and spread in Europe. It was then established quickly. 2002. Caulerpa racemosa var. mexicana are two distinct species. It has invaded coastlines worldwide. Libya (Nizamuddin 1991). there is no certainty regarding the date and location of first introduction. with individual plants forming discrete clusters corresponding to geographic locality (Sherwood 2005. Australia (Jousson et al.b. on the basis of various molecular analyses. Fama et al. (1998) and Olsen et al. Meinesz and Boudouresque 1996). 1998). 2000. 307). This species was reported as introduced and invasive since 1973 in western Europe. Adelaide) (Millar 2001) led to the realisation that transport of vegetative fragments by boat traffic from Moreton Bay was an important vector of introduction (Schaffelke et al. Argentina and the American north Pacific coast (Silva et al.A. its arrival in California (San Diego and Los Angeles) immediately prompted genetic analysis (Jousson et al. known since 1925 on the southern coasts of the Mediterranean Sea (Hamel 1926). since 1997 in eastern North America and since 1982 in the Mediterranean Sea. However. ISSR analyses revealed highly structured Hawaiian populations of A. spicifera with a substantial range of both within. taxifolia had never been reported off temperate and tropical coasts of the Pacific Ocean. Spain and the Netherlands. DNA sequencing revealed no variation for the two markers. 2001. Meusnier et al. 2000). from hull fouling. taxifolia from the Red Sea. Verlaque et al.and among-population variation. Jousson et al. The problem posed by this species. racemosa. Several contradictory genetic analyses were published. 2002. 2003a. Schaffelke et al. and that it corresponds to G. This confirmation led the local authorities to attempt eradication of C. Verlaque et al. was to determine whether it was derived by hybridisation between several different varieties of C. but different from those originating in the Red Sea and the oceans neighbouring the Mediterranean Sea (Jousson et al. or whether it came from the Red Sea or from other oceans. turuturu Yamada. Genetic knowledge accumulated during the debate about the introduction of C. 2005). 2002. the appearance of new range extensions of Caulerpa taxifolia into southern Australia (Sydney. or from aquaculture facilities where this edible alga is cultivated (under the name of wakame). Acanthophora spicifera (Vahl) Børgesen Genetic tools were used to investigate the geographic origin of Hawaiian populations of this alga believed to have been introduced 50 years ago by way of a biofouled barge from Guam. Voisin et al. Genetic analysis of samples of C. 2003a. 2004. adjacent to the city of Brisbane. taxifolia in the Mediterranean Sea made it possible to quickly identify the invasive strain in California as the one that had developed in the Monaco Aquarium and in the Mediterranean Sea (Jousson et al. This genetical analysis can neither confirm the supposed origin nor secondary introductions in Hawaii. originally described from Japan (Gavio and Fredericq 2002. Knowing the temperature tolerances of the invasive strain of Caulerpa taxifolia in the Mediterranean Sea (Komatsu et al. Finally. with subsequent establishment in the United Kingdom. p. as is readily observable from their morphological differences (Meinesz et al. w55x . 1997) helped to identify a population of this species in subtropical Australian waters (Meinesz 2001. originally described from Pacific South America. Australia. and even the Canary Islands in the Atlantic Ocean (Verlaque et al. Wiedenmann et al. Given the history of Caulerpa taxifolia as a (controversial) invasive species.

Procaccini et al. the only one that appears to differ from the others is the population of C. producing only male gametes (without eyespots) (Meinesz et al. A certain number of species introduced into the Mediteranean Sea and referred to as Lessepsian (coming from the Red Sea via the Suez canal. Caulerpa taxifolia At the time of its initial discovery at Monaco and the first studies of this species (Meinesz and Hesse 1991). scalpelliformis (Brown ex Turner) C. Meinesz: Tracking invasive seaweeds Asparagopsis armata Harvey and A. numerous phases of gamete production have been observed. Lamouroux ˚ on the French Mediterranean coast (Meinesz 1979). Codium fragile var. genetic studies of alien algae can elucidate some evolutionary and genetic consequences for native and invading species (see Booth et al. may confirm or identify the mode of introduction. taxifolia. observations of the reproduction pattern of the strain introduced into the Mediterranean Sea showed that it is exclusively dioecious. genetic analyses usually support initial observations that use classical morphological and biogeographical criteria indicating that the species is indeed introduced. genetic tools would provide a basis for testing the opinions of Cormaci et al. A variety of case studies underline the importance of this kind of knowledge. disintegrates (this is a process of holocarpy). If we consider that the introduced strain has a single origin. Norris (sPolysiphonia setacea Hollenberg) and Antithamnionella elegans (Berthold) Price et John)x Tracking alien algae to determine their spread and invasiveness As soon as an alien species is detected and reported. genetic analysis has not been able to resolve disagreements regarding sites and modes of introduction. taxiformis (Delile) Trevisan Genetic tools were used to differentiate these introduced species in the Mediterranean Sea wthe tetrasporophyte stages (‘‘Falkenbergia’’) are difficult to distinguishx and to describe genetic variability within native and introduced strains (Andreakis et al. 2007). These mechanisms can account for the very rapid spread of this alga at some sites. these different cases demonstrate that. This characteristic had already been observed in Caulerpa prolifera (Forsskal) J.V. Thus. In contrast. taxifolia can be undertaken in the immediate vicinity of already identified sites to assess natural rates of vegetative spread. taxifolia was known to be monoecious (Goldstein and Morall 1970). Importance of knowledge of the biology of the alga Basic biological knowledge is important to estimate the potential for natural or anthropogenic dissemination. knowledge of the production pattern of spores or zygotes or of vegetative fragments or propagules that may be spread by currents or by man. This production of specialised propagules more easily disseminated than fragments of thallus increases the colonisation potential of an affected site (Renoncourt and Meinesz 2002). where there is debate. Chapman 1999). and there is a highly efficient system of vegetative reproduction in which the spherical branchlets of the thallus can break off and form vegetative propagules. duction occurs was raised. Caulerpa racemosa For this species. enable estimates of the number of secondary independent introductions. such as to harbours and fishing or mooring areas. The alga reproduces sexually (Panayotidis and Zuljevic 2001). Agardh ¨ and certain varieties of C. In this case. is essential to define the potential for spread. taxifolia that has developed in Tunisia. and searches for the alga can be undertaken within a wider radius where human activities are likely to have transported fragments. However. Nı Chualain et al. In summary. racemosa developing in the southern Mediterranean Sea. some Rhodophyta introduced into the Mediterranean Sea wWomersleyella setacea (Hollenberg) R. but the only sample examined was in poor condition (Jousson et al. This is the case for Caulerpa mexicana Sonder ex Kutzing. call for genetic investigation since they may represent relics of an algal flora originating in the tropical Atlantic Ocean. Similarly.E. 2005). this requires a good knowledge of patterns of reproduction and habitat use of the introduced alga. In the first instance. two modes of reproduction that might explain its very rapid spread have been described.. without any female gametes being detected. ´ ´ For some introduced species. Since then. taxifolia that have developed in the Mediterranean Sea are clonal. built by Ferdinand de Lesseps in 1855–69) by Por (1978). and then the application of a variety of monitoring techniques. assess the genetic diversity of introduced populations. (2004) who contested the status of 14 taxa considered by other authors as introductions into the Mediterranean Sea. and thus. 2005. For example. In the Mediterranean Sea. 2004. 2004. tomentosum reproduces parthenogenetically (Feldmann 1956. Tracking of C. Genetic analyses would appear to support this notion. the question of whether sexual reprow56x . Finally. Genetic analysis may inform us on the status of a species of interest (its identity and origin). depending on the biological and ecological characteristics of the species. all the signs are that sexual reproduction does not occur. which must have favoured its dissemination. Reproduction appears to be solely vegetative. e. emptied of its content. then all the populations of C. and a clear understanding of the phenology. C. racemosa should reveal a more rapid progression of cover over a more extensive area than has been demonstrated for C. by boats with fragments attached to their anchors. The reproductive cycle of the genus Caulerpa involves production of gametes. Zuljevic and Antolic 2000).g. 1994. C.376 A. Other invasive introduced algae Other invasive introduced algae have a variety of reproductive modes that influence invasion dynamics. 1998). On this basis we may predict a slow rate of dispersal attributable solely to ‘‘secondary’’ anthropogenic dispersal. Species are dioecious or monoecious. its spread and invasion dynamics must be determined. All the nuclei are associated with chloroplasts and when the gametes are released the thallus. since there is very little genetic differentiation among populations. tracking C.

tracking large algae has been greatly assisted by the community at large (e. fishers. Brochures or posters to inform the public helped monitor the spread of Sargassum muticum in various countries on the coasts of the north-eastern Atlantic Ocean.. Rindi et al..e. Mapping using point samples For most introduced species. more easily detected from aerial photographs or teledetection images. Athanasiadis 1996.e. 1994. Croatia. In some cases. Finally. Ministry of Fisheries and Biosecurity of New Zealand. usually at large scales. reflecting the fact that they are readily located and identified because of their large size. The first allows the localisation of populations (or individuals) from information obtained through a distributed (but usually haphazard) collection of point samples (by divers or by using a grab). Keeping the public informed has proven to be an effective means of collecting the information needed to estimate the overall extent of invasion in a region as vast as the Mediterranean Sea. Knowing whether a species is able to colonise a large or small range of habitats determines the choice of monitoring techniques for the alga. so their dissemination occurs only through natural (currents) or anthropogenic (mainly fishing nets in the case of these two algae) dispersal of thallus fragments. If this were the case.g. The second involves collecting and analysing two-dimensional images of the seabed. in the case of S. thus. or sonograms of the seafloor obtained by side scan sonar.000 brochures have been distributed since 1991 in six Mediterranean countries (Spain. Considering the timing of reports of species occurrences at different points in space can enable production of useful maps of the rate of spread. Caulerpa taxifolia and C. most sightings have been recorded as occurrences (plotted as points on distribution maps) without any estimation of the areas covered or concerned (e. plotting the dynamics of population expansion has been limited to drawing up a list of scattered sightings on relatively small scale maps (more than 1/5000). by the passage of SCUBA divers or towed or autonomous video cameras (ROV). More than 300. was banned in Normandy (France) on the basis of evidence that the alga could complete its reproductive cycle in the temperatures of the English Channel and the North Sea.g. Several government agencies have distributed brochures to the public including the Department of Conservation. This was the case for Undaria pinnatifida.. and to monitor their development. with similar brochures written in several languages in some countries (Cottalorda et al. Knowledge of the ecology of introduced species Understanding a species’ autecology is also essential for efficient tracking of range extension. the isothermic limits characteristic of certain species offer a basis for predicting the limits of spread. This effort to collect cartographical data with the assistance of an informed public was also supported by the mass media (we estimate that 2000 press articles relating to the invasion by C. Meinesz: Tracking invasive seaweeds 377 appear to be sterile (Cormaci et al. Cultivation of the giant kelp Macrocystis pyrifera (L. tendency to form dense aggregations in a narrow depth range and. Stuart 2004). or linear samples (i. sailors and other lay persons). which have been relatively easy to map. using aerial Similarly. SCUBA divers. muticum. Turkey). Stuart personal communication).. taxifolia and C. Tunisia. Conversely. For the two invasive species most extensively mapped in the Mediterranean Sea. numerous Internet websites have been developed to raise public awareness and collect information (almost 1500 press articles and 36 websites are listed on the website http:// www. These algae are. Italy. Farnham 1997.g. knowledge of the bathymetric limits attainable by an introduced species is useful to define the ‘‘search space’’ for tracking. For these algae that are easy to see and identify. This kind of monitoring effort can produce maps of the distribution of invasive algae over large areas (e. Collection of cartographic data through community observation Although discovery and monitoring of small or cryptic algae usually depends on observations by professional phycologists. However. spectral responses obtained from satellite teledetection. 1999). it was soon established that they are able to invade most benthic habitats from the surface to 50 m depth.caulerpa. floating thalli that often reach the surface. 2001). racemosa have been published by the media in Mediterranean countries). Properly informing the public made it possible to identify most of the Mediterranean sites affected by Caulerpa taxifolia and Caulerpa racemosa. Sargassum muticum and Undaria pinnatifida develop just at the level of the lowest tides with a vertical distribution range of -5 m. However. 1981). bathers. the temporal component of the dynamics (Figure 2). the English Channel and the North Sea. Brochures have generally been made available both in hard-copy and more recently on the Internet (M. Important public awareness programmes were intitiated in New Zealand to track Undaria pinnatifida.g.) C. This is the case for Sargassum muticum and Undaria pinnatifida. estimates of the thermal threshold for this species proved inaccurate. France. this kind of prediction can also fail. i. w57x . the cultivation of which in Brittany (France) was permitted on the basis that low water temperatures would not allow reproduction by spores.A. racemosa. Responses to requests to cultivate other large phaeophytes have been more conservative. These monitoring techniques always require confirmation by divers since the spectral responses of different communities or species are often very similar and vary with depth (in the case of spectrographic images) or type of bottom (in the case of side scan sonar sonograms).. since the alga spread rapidly in the natural environment. e. invading further to the North (on the southern shores of the United Kingdom) than had been anticipated. Collection of cartographic data by systematic monitoring Monitoring marine species involves two distinct types of observation (Meinesz et al.. then its development may have become uncontrolled (Boalch 1981). by compact airbone spectographic imaging (CASI). using transects). Figure 1). Ag.

For more severely affected areas (mostly in the form of multiple scattered colonies). . Another method of linear observation consists of towing a camera mounted on a benthic sled or hovering device that maintains an approximately fixed distance off the seafloor. often in water depths to 20 m. 1994. the English Channel and the North Sea (from Boudouresque 1994).378 A.g. In a minority of cases. albeit with marked seasonal fluctuations. 2005).25 m2) (Conklin and Smith 2005). This method has been utilised successfully in monitoring Caulerpa taxifolia in large bays at depths of 10–40 m. This technique is also used to actively search for algae in areas where there have been no previous sightings. The simplest and least costly strategy is to involve those members of the public who routinely observe the seabed in shallow waters. divers seek to delimit the area over which the colonies are dispersed. With this method. This has been the case for Caulerpa taxifolia. using a small boat towing a diver at the surface or underwater provides a suitable means. cylindracea in the Mediterranean Sea (see the 23 cartographic publications cited by Piazzi et al. including fishers. These techniques have been used extensively in monitoring the spread of Caulerpa racemosa var. in Hawaii was followed by monitoring 15 sites within a single bay (using quadrats of 0. Most of the 130 independent infested areas known to date along the French Mediterranean coasts were discovered by amateurs. Belt transects several tens of km long can be filmed in one day using this methodology (Belsher et al. where there is high confidence that detection is soon after initial establishment. swimmers and sailors. A GPS can be used to localise the area covered by the diver. The coverage depends on the lens used. 2001). which means the diver can detect colonies in a 20 m swath bisected by the transect. Meinesz: Tracking invasive seaweeds Figure 2 Example of a map of sightings of invasive species on small scales. 1998). and each population observed can be localised with precision. but given the variations in the height of the camera above the bottom. a band of only 2–4 m width can usually be monitored effectively. Scattered sighting (dots) of Sargassum muticum with no data on density or colony sizes (area). A diver can cover 2–5 km in 2 h while observing from the surface in this way. free divers can be towed on a surface buoy with a GPS device to continually record position. where major mapping operations have been undertaken on the coasts of all the countries affected in the Mediterranean Sea (26 cartographic publications were cited by Meinesz et al. scales between 1/500 and 1/5000). For this. In the Mediterranean Sea. Several methods have been used to describe the extent of its colonisation. Figure 1 Example of a map of sightings of invasive species on small scales. other types of assessment enable spread to be estimated and reported on larger scale maps (e. 2001. estimates of invaded areas at a regional scale together with assessments of density have been recorded on large scale maps (1/500–1/5000). transects 200–500 m in length (according to depth) can w58x be readily explored to search for or localise invasive Caulerpa. visibility is often more than 10 m. To find reported colonies. often very dense and extensive perennial populations.. based on density data for a series of transects (Thomsen et al. or to locate the alga in the vicinity of colonised areas. For Sargassum muticum. The abundance and spread of the invasive red alga Kappaphycus sp. but were subsequently checked and verified by scientists. 2003). divers. efforts to describe the density or coverage of invading algae are limited to relatively localised areas. Isocontours indicate the rate of spread of Sargassum muticum in the northeastern Atlantic Ocean. Mapping using linear observations For invasive species with large populations. This species occurs in large. From Farnham (1997).

Other representations are based on presence/absence within square grids of highly variable size. an international pool of experts (from France. Under these conditions. 2005). as the alga grows and spreads very quickly. (3) Level III is attained when dozens or hundreds of colonies of various sizes are dispersed over a surface area )10 ha. such as states. These studies suggest that long range dispersal events from initial points of establishment have a strong influence on the rate of the overall range w59x . and that are dispersed over an area -10 ha. Sargassum muticum. During this stage of the invasion. Its efficacy was tested on only one occasion in the case of Caulerpa in the Mediterranean Sea. in some densely covered areas. 1994. The use of isocontours for invasive species based on densities is frequently utilised in conjunction with temporal wave fronts of the invasion (Hengeveld 1989). see Figure 1). To compare data from one year to another and between neighbouring countries that have invested in monitoring the invasion. or concerned area.. (2) Level II refers to the next step of spreading. Spread modelling Numerous theoretical and empirical approaches for assessing and predicting the spread of invasive terrestrial species have been proposed based on the characteristics of the invasion dynamics observed during the first years of colonisation of an environment (Hengeveld 1989. Thus. Figure 2). each containing information on the incidence of the invasive species. Ribera 1994). 2001) (Figure 3). Standardisation of cartographic data Once monitoring techniques have been implemented. Since the beginning of the invasion in the Mediterranean Sea. the concerned area). in monitoring the invasion of Sargassum muticum in Europe (Critchley et al. it is possible to estimate the invasion dynamics of an alga (e. racemosa is established in 12 countries (in 2005). 1999. For Caulerpa racemosa var. II and III).. as was the case. Italy. this technique is likely to prove useful for detecting and estimating the area occupied by thalli at relatively high densities. is seen as a basis for considering the entire square invaded (and coloured uniformly on maps or recored as ‘‘present’’ in tables). country). The best method to estimate the extent of coverage is to delimit the perimeter enclosing all colonies (i. irrespective of density. No new records have been indicated by this costly method. By summing the colonised areas (Levels I. Meinesz: Tracking invasive seaweeds 379 Mapping based on two-dimensional images of the seabed When invasive species densely cover large areas in shallow waters (particularly between 0 and -10 m). Tunisia and Croatia) established a standardised method (Vaugelas et al. standardised criteria for the geographical assessment of the invasion are required. It is characterised by several colonies that occur within 250 m of each other. and it is also very costly. In the vast majority of cases. and indicating those cells that are colonised. Farnham 1997. Numerous examples of invasions by introduced species in the terrestrial environment have been described by dividing the landscape into a large number of discrete cells of similar or identical size. interpretation usually requires diving to ‘‘ground truth’’ the remotely sensed data. with a total covered area of more than 1000 m2. that cover a total area of more than 1000 m2. for example. invasions proceed so rapidly that only the linear coastal extent of colonies is a valid criterion for description. but it has been used in the Mediterranean Sea to indicate the number of countries affected by the inva- sion of the two species of Caulerpa. These guidelines for mapping C. and in monitoring the invasion of Acrothamnion preissii and Codium fragile in the Mediterranean Sea (Ferrer et al.g. it is relatively easy to estimate the surface area covered by the alga (referred to as the covered area) and to delimit the exact perimeter of the area of dissemination by SCUBA diving (the concerned area). Ruitton et al. this form of demarcation is less relevant. cylindracea in the Mediterranean Sea. regions or other administrative subunits (county. Spain. 2005) (Figure 5). 1983. For the sea. in which one or more colonies occurring less than 100 m apart occupy a total surface area of less than 1000 m2. taxifolia define three levels of invasion and associated descriptive terms for assessing an impacted area (Figure 4): (1) Level I is the first stage of colonisation.A. an evaluation of the overall status of a given region in terms of the area affected by the colonisation is obtained. Other spatial conventions have been proposed such as presence/absence within broader polygons. they can be detected by aerial photography or by using a compact airbone spectographic imager (CASI). Each sighting of the alien species within a square. several international teams have been involved in monitoring the spread of Caulerpa taxifolia in several countries. Rather. taxifolia. Satellite teledetection has been used to estimate the spread of Sargassum muticum (Belsher and Pommellec 1988) but. usually as maps or tables. the outer boundary. If the boundaries of the invasion can be described with reference to time. maps summarising the invasion of this alga typically show only the lineal extent of the invaded area along the shoreline (Piazzi et al. as regards C. it is both time-consuming and futile to measure the covered area. it becomes impossible (and in any case not very useful) to map the location of each colony with any precision. city. CASI is rarely used in detecting underwater alliens. In order to standardise the mapping. is estimated by identifying the positions of the peripheral colonies. again. Hastings et al. at least six Mediterranean countries are affected (in 2001) while C. Monaco. Since the responses of several species of the same genus are similar. the information collected must be recorded and visualised appropriately. At this stage. Meinesz et al. For example. 2003). which was unable to delineate the total area of infestation (Jaubert et al. 2005. or to measure the covered areas.e. sites of observation are recorded in point fashion (one point per area where occurrence has been observed) on maps. Comparison of the densely covered areas detected by CASI with larger areas that have been invaded and observed previously by divers in the same region is not possible.

This method seeks to ensure 100% coverage of the afflicted area. monitoring invasive algae must be carried out with a high level of precision. 2001). taxifolia cannot be monitored in its entirety during each campaign. Tracking for eradication purposes In a few rare cases. The success of eradication operations usually depends more on the precision of monitoring than on the eradication technique itself. is a useful example. between 40 and 60 SCUBA divers or skin divers combed the waters of the national park for three days to detect developing colonies. and divers using a guide-line deployed by a small boat using differential GPS. Williams and Grosholz 2002. the Parc National de Port-Cros authorities decided in 1994 to control the spread of Caulerpa taxifolia by eradicating the colonies as soon as they became established. whereas in an uncontrolled neighbouring island (Porquerolles) the invasion spread to cover several tens of hectares by 2004. Very precise monitoring is required if it is necessary to completely eradicate either the whole of an introduced population or all of a particular sub-population of developing colonies within a restricted area. 2000. the whole eradication investment may be rendered worthless within a few years. Report of occurrences with spatial extension for each spot. the extensive area of seabed favourable for the development of C. where more than 1000 m2 of C. Each year since 1994. At Port-Cros. Agua Hedionda lagoon near San Diego was covered several times by SCUBA divers along hundreds of transects 1 m apart. towed cameras and laser line scan.380 A. expansion. Permanent grids of ropes were deployed in the colonised areas in the third year of quarterly surveys. 2001. This technique made it possible to detect all colonies. colonies were discovered and eradicated. the occurrence of the alga at Port Cros has since been highly restricted. Each year. which were then successfully eradicated. Commencing in summer 2001. 2002) at a particular site. Off the French Mediterranean coast. Woodfield and Merkel 2004). 1997. different methods of tracking the algae for eradication purposes were tested in the turbid waters of these areas (visibility w60x is typically -2 m in Agua Hedionda lagoon). taxifolia (Woodfield and Merkel 2004). predictions are hampered by poor knowledge of both coastal currents and the spatial distribution of the subtidal habitats that an introduced species is likely to colonise. 1998. taxifolia were discovered in 2000 (Jousson et al. near San Diego (Agua Hedionda lagoon) and near Los Angeles (Huntington Harbor). Therefore. Invasion of Caulerpa taxifolia in the Mediterranean Sea (from Meinesz et al. a predictive spread model has been developed only for Caulerpa taxifolia (Vaugelas et al. The latter technique appeared to be the most effective in locating very small fronds of C. Even if the detection of the colonies is less than exhaustive. In the marine domain. For invasive algae. and included towed divers. Meinesz: Tracking invasive seaweeds Figure 3 Example of a map of sightings of invasive species on small scales. The eradication of Caulerpa taxifolia in southern California. those particular sites most favourable for the introduction (mooring areas in sheltered bays or areas where fishing . Hill et al. since if a few colonies have not been detected.

1999 and Meinesz et al. 2001). Their position can. Mediterranean Sea. Conclusion The manner of discovery of new invasions and their subsequent monitoring provides a basis for assessing the effectiveness of several different tracking protocols that have been attempted. 438419580N. 2005). the activity of phycologists with a good knowledge of the algal flora of their region. w61x . thus. nets are placed underwater) have been most closely inspected. 1996. the distance between divers is 5 m. Meinesz: Tracking invasive seaweeds 381 Figure 4 Configuration of the three levels of colonisation of Caulerpa taxifolia on large scale maps. cylindracea on large scale maps in terms of the linear extent of coast line affected (from Ruitton et al. Since the waters at PortCros are very clear (visibility often more than 10 m). A buoy attached to a weight by a rope is placed at each of the colonies detected. (after Vaugelas et al. with subsequent eradication (Cottalorda et al. 781895899 E). Robert and Gravez 1998). Colonisation Levels I–III are as outlined in Figure 4.A. be easily determined with a GPS. Example: the rade of Villefranche (France. led to relatively rapid detection of alien algal species. Monitoring methods based on groups of 6 to 10 divers swimming in line on a pre-established course holding a rope have been used. In Level III the position of the dozen or hundred main colonies involving more than 100 ha and covering much more than 1000 m2 is not presented. Robert 1996. Figure 5 Representation of the invasion of Caulerpa racemosa var. In the majority of cases. plus informing the lay public about potential invaders.

Dimet. Sargassaceae).L. T. Critchley.. E. Le Gall. Chapman. Dugornay and C. Phycol. Cottalorda. G. Fama. In: (M. ed. Meinesz. High ` levels of intra. C. Kooistra and G. Verlaque and Y.) Dynamique d’especes marines ´ ` invasive: application a l’expansion de Caulerpa taxifolia en ` Mediterranee. 2002a. Methodes moleculaires pour l’analyse ´ ´ d’especes invasives: l’exemple de Codium fragile. Napoli 37: 567–574. In: (Aca` demie des Sciences. 1991–2001: 11 years of campaigns for public awareness of the Caulerpa taxifolia problem. and often to ascertain their mode of introduction. Belsher.and inter-individual polymorphism in the rDNA ITS1 of Caulerpa racemosa (Chlorophyta). Acrothamnion J. genetic tools can be particularly helpful in illuminating the likely history of a given introduction.K. Dagault. Caisey. Paris. Boudouresque. Phycol. Blanc. Phylogeography and cryptic diversity in the invasive seaweed Asparagopis (Bonnemaisoniales. G. 8.. Ag. 1996. Ballesteros.C. Inv. T. A. M. T. Yillam. Ital. Coleman. Expansion de l’algue d’origine japonaise Sargassum muticum (Yendo) Fensholt. W. eds) Second International Workshop on Caulerpa taxifolia.-M. Coroller. In: (V. O. Fama. Zaninetti. Paris. 33: 551–562. and S.): 83. Cottalorda.. Meeresunters. D.R. M. Cottalorda. A. L’Europe ´ (Ifremer/ Icram). A. G. Furnari. Alien macrophytes in the Mediterranean Sea: a review. Above all.J. 2005. Sargassum muticum. Meinesz. Peleau. Charbonnel.. New Orleans (USA): 24. 1995. Acquisition de donnees sur l’expansion de ´ Caulerpa taxifolia et Caulerpa racemosa en rade d’Hyeres et ` en rade de Toulon (France). Hydrobiologia 326/327: 29–34. Eradication de la colonie de Caulerpa taxifolia decouverte en 1994 dans les ´ eaux du Parc National de Port-Cros (Var. Le Gall. Eur. Fucale). A bibliography of the invasive alga Sargassum muticum (Yendo) Fensholt (Fucales. J. J.C. M. de 1983 a 1987. Elements of cartography and changes of Caulerpa taxifolia in 1992 along the Alpes-Maritimes and Monaco coasts. R. Meinesz and G. Hawai’i and an experimental assessment of management options. J. In: (C. 105: ´ 109–166.. T. 15: 122–133. Acta 26: 161–166. Boudouresque.F. Menager. J.F. Peirano. F.K. pp.-M.T. Meinesz: Tracking invasive seaweeds To assess spread. Mediterranean Sea. C.H.-F. Coleman.. Linn. Wysor. Cormaci. References Andreakis. Di ` Giuseppe. A. Ecosystem research report No.. pp.T. J. F. F. Acad. Genetic polymorphism in Caulerpa taxifolia (Ulvophyceae) chloroplast DNA revealed by a PCR-based assay of the invasive Mediterranean strain. P. M. S. pp.F. Conference Marine Bioinvasions. Int. Biol. Pommellec.-F. Zool. ` Molecular phylogeny of the genus Caulerpa (Caulerpales. pp. 2001. M. Oceanol. J. Scabbia. Farnham and S.. A. GIS Posidonie. DNA analysis methods for recognizing species invasion: the example of Codium and generally applicable methods for algae. A. Devel. W.H. Pucci and T. (Rhodophyta. A. Biol. 1973–1981.-F. Giacone and S. Mereau. Donatella. J. Zucarello. Mingant. Fama. Morphology and classification of the Ceramioideae (Rhodophyta) based on phylogenetic principles. Goraguer. Raillard. J.T. Bot. Ribera. Chisholm. tomentosoides (Chlorophyta) in the North Atlantic Ocean? Helgol. 2003. P. 83–87. Bull. Yoshida and T. Duglet and C. Marcfeld. G. are relatively rare. Belsher. Boutbien. Puccini.H. N. F. Mar. Early discovery of major invaders followed immediately by exhaustive monitoring is the exception rather than the rule. eds) Fourth International Workshop on Caulerpa taxifolia. Dimeet.A. J. 1969. J.. 1994. Molecular approaches to the study of invasive seaweeds. 39: 273–284. Pubbli. de Vaugelas and E. Oceanol. From introduced species to invader: what determines variation in the success of Codium fragile ssp. 10: 657–667.M. C. M. Fugazzi. Robert. J. w62x . D. O. 33–55. Farnham. G. A. Durand. Rhodophyta. N. G. European Commission Directorate general XIII. J. such as that of the eradication of Caulerpa taxifolia in California. J. Sci. Chlorophyta) inferred from chloroplast tuf A gene. T. Morrell. J. Briand and ´ C. Do we really nead to grow Macrocystis in Europe? Proc.M. 2000. J. Phycologia 44 (4 Suppl. E. cartographic methods make it possible to measure the extent of the spread of an invasive alga and can assist in helping to predict potential impacts. A. Kooistra. Cosson. Olsen. 1996. Critchley. Normandie Fr. G. 2005. Belsher. 7: 1029–1039. France). Bertrand and N. Molecular data suggest a hybrid origin for the invasive Caulerpa racemosa (Caulerpales. J. Booth. ´ Campagnes oceanographiques Califa 1998 du N. 1996. Boudouresque. Biol. University of Barcelona. Marseilles.. 2007.S. Rhodophyta) from the Mediterranean Sea. 1997. 52: 277–289. Intern. Rhodophyta): genetic and morphological identification of Mediterranean populations. Millar and J. E. Bot. A. V. 1983. ` Gravez. Norton. 2001. Dini. Seaweed Symp. G. Asparagopis taxiformis and Asparagopsis armata (Bonnemaisoniales. P.. de Vaugelas. Sartoni. eds). Furnari. 35: 349–356. Environ. On three interesting marine red algae (Ceramiales. Boudouresque. C. P. Provan and C.A. 2004. B. J. M.W. 1994. Bot. Ceramiaceae): genere algale nuove per il mare Mediterraneo. Kappaphycus ssp. Mar.F. Giaccone.. Mar. Acquisition de donnees qualitatives et ´ quantitatives sur l’expansion de l’algue Caulerpa taxifolia (Alpes-Maritimes. 128: 1001–1006.M. Cah. Procaccini and W. J. Chlorophyta) in the Mediterranean Sea. staz. Athanasiadis. Lavoisier Publ. Cinelli. and J. A. Gomez and V. Cormaci.. Barcelona. Abundance and spread of the invasive red algae. H. 2004. Comparing standardised cartographic data over time and between different areas has proven extremely useful in this context. Procaccini and W. 50: 385–396. Nolan. Ass. Pawlowski. 1994. Biol. in Kane’ohe Bay. 29: ˆ ` 221–231. Biol. Evol. M. Principaute de Monaco et en Mer Ligure). 63: 799–811. it is necessary to match appropriate marine environmental monitoring techniques to the biology and ecology of the alga... Volto. A. Maggs. U. E. Jousson. Gravez. Smith. Manuel..T.W.C.. Boudouresque. 1999. 38: 1040–1050. Chiaverini and J. M.O. Andreakis. W. Le Parco.A. Jaubert and G. Eur.P. 1977. Stam and G. Kooistra. M.382 A. Thibaut. E.L. W. Although in a majority of cases classical identification and biogeographical knowledge provides an adequate basis for determining that particular individuals represent an alien algal species. Meinesz. Recent Res. Serio. Evol. and G. Les especes introduites dans les ` eaux cotieres d’Europe et de Mediterranee: etat de la quesˆ ` ´ ´ ´ tion et consequences. 15: 618–624. C. 149–155.. 1988. D. Procaccini. 1981. X. 2002b. Opera Botanica 128: 1–216. Caulerpa taxifolia in the northwest Mediterranean: introduced species or migrant from the Red Sea? C.-F. Soc. Belsher. Youenou. Emery. Acta 17: 443–451. 8–27. Alongi and D. A. 2002.M. E. Billard. P. G. Biol. Lunven. 1: 153–202. G. A. J. Sur la vegetation ´ ´ algale de l’etage littoral dans la region de Saint-Vaast-la´ ´ Hougue et la presence d’une espece japonaise nouvelle pour ´ ` ¸ les cotes francaises: Sargassum muticum (Yendo) Fensholt ˆ (Phaeophycee.R. Life Sciences 318: 1219–1226. A chronology of new European sites of attachment for the invasive brown alga.J. Phycol. Introduced species in European Coastal waters. L.F. and so successful prevention of spread as a result of early detection and tracking. Boalch. ´ ´ Conklin. Mar. Luxembourg.. sur ¸ les cotes francaises. 1990.

. C.T. J. A. S. Am. South Africa 17: 92 (abstract). J.R.. eds). ´ Meinesz. I. O. Djellouli. W.. Meinesz. Ecol. 37: 349–360. The spatial spread of invasions: new developments in theory and evidence. Ecol. Phylogenetic analyses of Caulerpa taxifolia (Chlorophyta) and of its associated bacterial microflora provide clues to the origin of the Mediterranean introduction. 2003. Notes taxonomiques ´ preliminaires sur Caulerpa taxifolia et Caulerpa mexicana. using molecular tools. Melbourne. Boudouresque. 2001. E. J. Zaninetti. Soc.. Portsmouth Dist. J.. Meinesz. M. Minghelli-Roman. leurs applications sur les cotes fran´ ˆ ¸ caises de la Mediterranee. Prog.T. D. The invasion of Caulerpa taxifolia in eastern Australia. Y. T. Taylor and D. Destombe. Harrison. pp. Seaweed Symp. A. Tracing species invasion in Codium. The Sargassum saga. 160. C. C. Temperature and light responses of alga Caulerpa taxifolia introduced into the Mediterranean Sea. II.-F. M.. Zuljevic. Gravez. Moore. Gravez. Boudouresque. A. Boudouresque. 3: 201–210. M. Meinesz and D. Morrow.. J. Chisholm. D.. Olsen and W.. Millar.L. Nat. Peirano. Holland. J. 2004. 146: 145–153. Ben Mustapha. Irvine. 378. a siphonous green alga. Int.. Davies.A. H. Sexual reproduction of the invasive green alga Caulerpa racemosa var. pp. C. Sci. B. J. T. A. But next time? Unsuccessful establishment of the Mediterranean strain of the green seaweed Caulerpa taxifolia in the Sea of Japan. Modeling and Simulation 1: 30–35. pp. Biol. 2001. El Abed.T. incipient species status for the invasive strain. Hill.F. El Abed. 1992. Thomson. 1997.T. E. Meusnier. Meinesz.A. Inv. 2000. Phycol. Grateloupia turuturu (Halymeniaceae. 1997. D. Bot. L. J.. Ecol. Eur. O’Doherty. and A.F. A. 1976. Mod.J. J. A. Lavoisier ´ ´ Publ. Langar. N. T. F. Meinesz and F. Nı Chualain. Gavio. and B. C. J. ´ ´ Meinesz. Cottalorda. Biol. I. Contribution a l’etude de Caulerpa prolifera ` ´ (Forskal) Lamouroux (Chlorophycee. Ser. Bul. Valero. Antolic. Chicago. Hesse..J. A. Pietkiewicz. T. Nat. Scourge of the Mediterranean – now appearing in California! Caulerpa taxifolia. A. J. Ripley. C. M. Mediterranean Caulerpa taxifolia and C. K. K. C. Mar. J. Cinelli. J. In: ´ (C. J. 1998.. Phycol. Meinesz. Jaklin. Agardh development in the NorthWestern Mediterranean Sea. Maggs. Thibaut and A. Oceanol. Biol. Millar and A. J. 1956. Paris. The invasive genus Asparagopsis (Bonnemaisoniaceae. ed. 105–114. 1979. Pawlowski. Panayotidis. Goldstein. Nat. Olsen. First International Workshop on Caulerpa taxifolia. Fletcher and L. 1974. Ribera and A.C. occidentalis in the Mediterranean Sea. Gruet. 34: 850–856. Life ´ ´ Sciences 319: 603–613. 2: 64–67. T. 2001.H. 2001. I. Bern. S. Mol. J. Caye. Acta 14: 415–426. H. The green marine algae of Libya. Meusnier. deVaugelas. A. Phycol. Sci. R. Tunesi. D. Jousson. Paris. Lemee and A. J. 2003. W.. Olsen. importe sur ˆ ´ ¸ la cote Atlantique francaise. Meinesz.J. W. In: (C. Ben Mustapha and A. W. Coquillard. L. Premiere signalisation de Caulerpa taxifolia (Vahl) C. Valero. Meusnier. Molecular evidence for the aquarium origin of the green alga Caulerpa taxifolia introduced to the Mediterranean Sea. La repro˚ ´ duction sexuee sur les cotes occidentales de la Mediterra´ ˆ ´ nee. In: (Academie des Sciences.-F. R.T. Komatsu.R. Coquillard. M. A. 1998. Liddle. Robert. B. A.M. ´ ´ 2004. C. P. Orestano. F. Acad. A.L. F. Woodfield. Ecol. 243: ´ ´ 305–307. Genetic population structure of the Hawaiian alien invasive seaweed Acanthophora spicifera (Rhodophyta) as revealed by DNA sequencing and ISSR analyses. 1970. Predicting invasive species expansion using GIS and simulation coupling.-F. and ecophysiology of Falkenbergia isolates. 1991. 2001. 79: 1279–1285. A. Belsher. Komatsu.. Prog. mexicana (Chlorophyta) are not conspecific. Ohba. J. Hengeveld. Freestone. Introduction et invasion de l’algue tropicale Caulerpa taxifolia en Mediterranee nord´ ´ occidentale. Mar. Malvadkar. Valero. Feldmann. Elga Publishers. Mar. Hill.F. Marchioretti. 3: 275–277. P. 109: 251–265. Especes invasives sur les cotes de la ` ˆ Manche et de l’Atlantique.K. Stam. 172: 275–280. Coleman. Jousson. H. 1981. 39: 83–92. G. Meinesz: Tracking invasive seaweeds 383 Farnham. An algorithmic model for invasive species: application to Caulerpa taxifolia (Vahl) C. Hori and H. The introduced green alga Caulerpa taxifolia continues to spread in the Mediterranean. K.1973.. Mar. A.L. Caulerpale). and S. Boele-Bos and W. Hist. M. J. Komatsu. R. Paris 32: 420. 1991. K. Silva. 2nd edition. Re-evaluation of the extent of Caulerpa taxifolia development in the Northern Mediterranean using airbone spectrographic sensing. Lambrinos. Oceanol. Destombe. M. Quelques algues rares ou nouvelles pour la flore mediterranenne. Di Guiseppe. 22: 117–121. Fredericq. Olsen. Bull.M. ´ ´ Hastings. Killer algae. Flora Mediterranea 4: 163–166. Mol. Ivesa. Ser. S. Eur. Meinesz. U. Blachier.A. 175: 660–672.. Chapman and Hall Ltd. Jaubert. Proc. GIS Posidonie.M.. Bot. Cah. 10: 931–946. R. London. L. Zechman. K. Djellouli. pp. Ann. pp. Ecol. Campagne de prevention et de sensibilisation a l’introduction ´ ` en Tunisie de Caulerpa taxifolia. Acad. 2002. Analysis of rDNA ITS1 indels in Caulerpa taxifolia (Chlorophyta) supports a derived.. Ecol. Sci. F. Coquillard. GIS Posidonie. Agardh ` en Tunisie. w63x .L. 2002. G. Nat. 17: 173–184. Hist. Phycol. Meinesz and V. H. C. Inv. Cape Town. Zavodnik and A. 2000.M. D. Stam and J. 2005. Nature 243: 231–232. I. Fr. 230. Farnham. El Abed. Boudouresque. Cuvelier and R.The true tale of a biological invasion. deVaugelas and A. 1926.C. A. J. 40: 1112–1126. Sci. Meinesz and C. Palluy.F. Sci. M. Methodes ´ recentes de cartographie et de surveillance des herbiers de ´ phanerogames marines. 15–35.M. Ceramiaceae) in the Mediterranean Sea: new record from the Balearic Islands. Stam. and S. G.W. Chiaverini. M.. Aussem. Sur l’origine de Caulerpa taxifolia en Mediterranee. A. A. W. The spread of Acrothamnion preissii (Sonder) Wollaston (Rhodophyta. Langar. Polymerase chain reaction-single strand conformation polymorphism analyses of nuclear and chloroplast DNA provide evidence for recombination. Prog. O. 1994. Meinesz. Ferrer. 2001. Mar. Mus. Acta 24: 199–203. D. E. A. Hill. 17–20. Massuti-Pascual. K. Elmendorf. Thibaut. N. Renoux-Meunier.W. Lett.-F. The University of Chicago Press. and C. L. 61: 223–233. Gomez Garretta. T. J. Modeling the ultimate seaweed expansion. F. 2002. Zuljevic.. Ser. B.. morphology. Boudouresque. Ishikawa. M. Yamaguchi. Marseilles. 1994.-M. T. A. Gode. Dugaw. Voytek and A.. V. Meinesz. Buckles. Invasive alga reaches California. Rhodophyta): molecular systematics. Heral and J. Nature 408: 157–158. A. Ecol. G. 1996. Tech. Laurent. Langar. Marseilles. 1998. deVaugelas. P.. multiple introductions and nascent speciation in Caulerpa taxifolia complex. A. Saunders and M. Thibaut and P. 11: 2317–2325.-F.D. A. Meusnier. M. M. Vie et Milieu 31: 27–34. ´ Bonhomme.A. Gametogenesis and fertilisation in Caulerpa. Dini. Farnham. 2007. Mer (Tunisia) 27: 1–8. Cuddington. Rhodophyta) is the correct name of the nonnative species in the Atlantic known as Grateloupia doryphora. New York Acad. Valero. ˆ Hamel. Simulation 76: 126–134. 1998.) ´ Dynamique d’especes marines invasive: application a l’ex` ` pansion de Caulerpa taxifolia en Mediterranee. A. Ben Mustapha and A. C. Sur la parthenogenese du Codium fragile ´ ´ ` (Sur. Zaninetti..) Hariot dans la Mediterranee. Desmarais. 8: 91–101.R. T. pp. Grau.. 1989. L. Premieres observa` tions sur l’introduction de la faune associee au naissain ´ d’huıtres japonaise Crassostrea gigas (Thunberg). Dynamics of biological invasions. 263: 75–82. Goff. Nizamuddin. Guiry. Attached Sargassum muticum found in Britain. Pawlowski. P. Morall.L. Stam. Y. eds) Third International Workshop on Caulerpa taxifolia. A Djellouli. L. Instit. Pac.

-M. W. eds) ´ Second International Workshop on Caulerpa taxifolia. G. France). Vogel. Sherwood. Les macrophytes marins introduits en Medi´ terranee: biogeographie. J. Cullioli.D. 2002. 2003a. Murphy and C. Uthicke. Cossu. and E. A. Review of research on Undaria pinnatifida in New Zealand and its potential impacts on the eastern coast of the South Island. Meinesz. 2003. A.S. Argyrou. maritime traffic effects. Viard. Antolic. D. J. GIS Posidonie. Blitzkrieg in a marine invasion: Caulerpa racemosa var cylindracea (Bryopsidales. Controle de l’algue Caulerpa ˆ taxifolia dans le Parc National de Port-Cros (Var-France). Verlaque. Meinesz: Tracking invasive seaweeds ¸ Piazzi. 2003b. Woodfield. N. Establishment of the introduced kelp Undaria pinnatifida in Tasmania depends on disturbance to native algal assemblages.R. and J. Durand. 2000. 2002. C. Asparagopsis taxiformis in the Mediterranean Sea. S. 26: 189–202. R. Huisman. Balata. pp. Cryptogam. Chlorophyta) invasion along the French Mediterranean coasts. Ruitton. B. Poster. S. 1996. M. 1978.M. Pergent. M. Inv. Luxembourg. Meinesz. eds). Invasion of Caulerpa racemosa var. Preliminary reports from the Caulerpa taxfolia invasion in southern California. M. C. M. Neill. C. 2005. Frada Orestano. F. R.): 4A. Boudouresque. Gravez. Verlaque. Lanfranco. 38: 325–329. accepted 18 April. Phycologia 44 (4 Suppl. Pathways of biological invasions of marine plants. Andreakis and W.C. Introduced marine plants. K. Rindi. Hill 1997. Stuart. 44: 204–210. M. Javel.A. Pol. Pillen. Phycologia 41: 533–535. Meinesz.H. S. Washington. The influx of Red Sea biota into the Mediterranean by way of the Suez canal. 295: 63–90. Merkel & Associates. Ecol.. The genus Grateloupia C. Engel and F. N. Gravez. 2004. Synchronous release of male gametes of Caulerpa taxifolia (Caulerpales. 4: 333–338. ´ Berlin. Received 20 January. Akcali. Cinelli. Silva. Boudouresque and Y. M. Ribera. ´ Verlaque. In: 10th Marine ˚ Research Conference. Mar. Van Klaveren. Inv.. Phycologia 44 (4 Suppl.-M. 2005. Por. F. Hirtshals (Denmark). Biol. Biol. A. Komatsu. Williams. Vaugelas. Vaugelas. Panayotidis. Tracking the invasive history of the green alga Codium fragile sp tomentosoides. M. 2005. P. 1994.A. S.S. M.. M. Brannock. Baumstark. L. A. F. Ecol. Meinesz and V. M. Ulvophyceae) in the Mediterranean Sea. Belsher. A. S. Morphology and reproduction of the adventive Mediterranean Rhodophyte Polysiphonia setacea. Le Parco. Wiedenmann. Chlorophyta) in the Mediterranean Sea.D. Prog.. pp. Stær and T.R. Fucales) in Draby Vig. T. P. A. 37–43.C. Using genetic techniques to investigate the sources of the invasive alga Caulerpa taxifolia in three new locations in Australia. B. 2005. Acta 17: 1–23. and K. Acad. Introduced species in European Coastal waters.. Verlaque. A. Renoncourt. A. Boudouresque and Y. 1995. J.M. Briand ´ ´ and C. Thomsen. Meinesz. DNA fingerprints of Caulerpa taxifolia provide evidence for the introduction of an aquarium strain into the Mediterranean Sea and its close relationship to an Australian population. 2001. pp. European Commission Directorate general XIII.. Coquillard and D.A. Lesseptian migrations. G. Recherche de l’algue Caulerpa taxifolia dans les eaux du Parc National de Port-Cros. 2002. Grosholz..N. Ruitton. F.. A. Rhodophyta) in the Thau Lagoon (France. Valentine.D. Oceanol. Cohen. de. Phycol. Procaccini. 2005. Gil-Rodriguez. Harris and J. Ribera. 6: 269–281. P. T. Algol. M. Pala. Zuljevic and G.D. Mar. Ballesteros. J. In: (M. Proposition for a standardisation of map representation of Caulerpa taxifolia expansion in the Mediterranean Sea. Voisin. 2003. Verlaque. Zuljevic. S. 12. Span. Chlorophyta). On the identity and origin of the Mediterranean invasive Caulerpa racemosa (Caulerpales. Calvo. pp. Javel. Chlorophyta) in the Mediterranean Sea: an assessment of the spread. 2001. Schaffelke. 14: 189–194. A. Phycologia 39: 157–159. 2005. Palluy. A. C. Ceccherelli. Carlton. R. 2004. Population genetic structure and geographic origin of the Hawaiian invasive seaweed Acanthophora spicifera (Rhodophyta). Cassar. Mol. Zuljevic.. Department of Conservation. Vie et Milieu 47: 397–400. J. R. Djellouli. Prog.F. Agardh (Halymeniaceae. In: (Ruiz G. P. pp. Alfonso-Carillo. Gravez. Nat. Acta 24: 29–49. Ballesteros. Boudouresque. B. Mar. Merkel. 2000. J. Bot. 45–49. Mediterranean): a case study of marine plurispecific introductions. USA 102: 5432–5437. Boudouresque. J.C. A computer simulation to evaluate the impact of Caulerpa taxifolia on Mediterranean biodiversity. Mar.A. Johnson.M. In: (C. J.. Boudouresque. Verlaque. Boudouresque. 8. M.R. Hydrobiologia 398/399: 91–100.-F. Exp. Sci. P. Provan. 233: 307–310. Biol.C. Gomez and V. D’Archino. 1994. Biol. 2007 w64x . 99–100. Limfjorden.H. Spatial and temporal distribution of Sargassum muticum (Phaeophyta. Durand. Bull. F. Pergent and M. and A. Murphy and S. 183–226. Inventaire des plantes introduites en Medi´ terranee: origines et repercussions sur l’environnement et les ´ ´ activites humaines. Ribera. Zavodnik and A. eds) Invasive species: vectors and management strategies. G. A. E. Europ.-F. J. M. C. First report of the Asian kelp Undaria pinnatifida in the northeastern Pacific Ocean. DOC Science International series 166. Kooistra. L. Morucci. Differential shuffling of native genetic diversity across introduced regions in a brown alga: aquaculture vs. Robert. Carlsbad. P. Uwai. Antolic.. San Diego. 40. The Caulerpa racemosa complex (Caulerpales. Ser. 43: 49–68. Cirik. 11: 187–268. Ballesteros. Phycologia 44: 477–496. 1999. de. P. Jaklin. Cottalorda. N. J. 128. A. Maggs. 50: 1061–1068. Woodfield. 1998. Phycol. 1999. Boo and H. L.. Formation of propagules on an invasive strain of Caulerpa racemosa (Chlorophyta) in the Mediterranean Sea. 138: 229–234. A. 2006. Marston. and V. Sandulli. Gravez. Antolic. M.. A.A. 2005. Nelson.L. Acta 22: 85–94. Peirano. E.-F. N.-F. A. Kawai. Res. Ribera Siguan. with special references to macroalgae: mechanisms and impact. Ecol. Bull. ` A. Nolan. Mar. E. Pol. T. Robert. Island Press.384 A. A. First assessment of the Caulerpa racemosa (Caulerpales. Checklist of the macroalgae of Thau Lagoon (Herault.R. Proc. ˇ Petrocelli. C.T. Tripaldi. R. Meinesz. F. Wernberg-Møller.F. 2002. M. Meinesz and W. eds). S. Le Parco. P. Cinelli. Oceanol. M.P.-F. Phycologia 44 (4 Suppl): A52–A53.H. Verlaque. F. Ecosystem research report No.): A94.L. E. Barcelona. C. 2005. B. V. 1998. J.A. Third International Workshop on Caulerpa taxifolia. Meinesz and F. Cinelli.. Goddard. pp. Oceanol. Eradication and surveillance of Caulerpa taxifolia within Agua Hedionda Lagoon. C. Mar. Springer. Genetic diversity of Undaria pinnatifida in Asia and New Zealand deduced from mitochondrial genes. C. Verlaque. S.M. Wellington. Marseilles. Mifsud. Third-year status report. cylindracea (Caulerpales. G.-F. and C. and C.. and B. pp. Villalard-Bohnsack and M. University of Barcelona. Chlorophyta) reaches the Canary Islands (NorthEast Atlantic). M.A. Guiry and F. A. a hot spot of marine species introduction ´ in Europe. In: (C. D.

yet invasions also provide many opportunities for ecological and evolutionary research (Sax et al. 1998. Over the past two decades. aquaculture (Farnham 1980.1515/BOT. Introduction Non-native species that become established into existing ecosystems and subsequently threaten biodiversity and/ or result in economic damage are referred to as invasive alien species (Shine et al. focusing on invader species for which the greatest amount of information is available. 2001). 2007). 2005) are currently in the forefront of invasion e-mail: c.g. such as microarray technology. it illustrates the potential changes that can occur. there has been no previous general review of the genetic or evolutionary aspects of invading alien seaweeds. invasion. in population structure and allele frequencies. 1998. Whilst this is necessarily a simplified model that does not take into account the possibility of multiple. include marine species and are relevant to the genetics of seaweed invasions. Grosholz 2002). Nevertheless. cryptic species. 2000). Belfast BT9 7BL. and (2) changes in genome organization at the species level through hybridization. Invasive alien species are now widely accepted as one of the leading threats to biodiversity. have successfully identified the species involved and their sources. Ribera and Boudouresque 1995. Queen’s University. Holland (2000). eloquently summarizes the key features of theoretical invasion genetics. We draw on studies of better-known aquatic and terrestrial organisms to point the way forward in revealing the genetic consequences of seaweed invasions. molecular studies of non-native seaweeds. Wilcove et al. To our knowledge. we briefly review these studies. yet marine research has lagged behind investigations of terrestrial and freshwater ecosystems (Grosholz 1996. Bohonak et al. de Rivera et al. after habitat destruction (Vitousek et al.. Non-natives without such effects are known as alien or non-indigenous species (Shine et al. briefly described here. including the exploitation of developments in bioinformatics (Lesk 2002). and points towards the utility of molecular genetic techniques in an integrated pest management approach. We review invasion processes.043 Review Molecular approaches to the study of invasive seaweeds David Booth. Cox ¨ 2004. and thus the phenotype.. We also highlight potential applications of more recent methodological and statistical approaches. Northern Ireland. it seems pertinent to outline invasion processes (Figure 1). Marine ecosystems are potentially in a high-risk category. DNA.000 species being transported daily (Ribera and Boudouresque 1995).Botanica Marina 50 (2007): 385–396 2007 by Walter de Gruyter • Berlin • New York. As yet. and in individual gene expression profiles at the levels of expressed messenger RNA (the transcriptome) and the proteins synthesized (the proteome). little research has been directed towards examining the genetic consequences of seaweed invasions.2007. 2007). 2005). Here we provide an overview of seaweed invasions from a genetic perspective.maggs@qub. some recent marine studies (e.e. and rationalize evolutionary and genetic consequences for the indigenous and invader species into two main groups: (1) changes in genepool composition. and assess the likelihood of predicting invasion w65x . Current studies of bioinvasions are idiosyncratic and narrowly focused (reviewed in Grosholz 2002) and future studies must draw on a wider variety of techniques in the field of ecological and evolutionary genetics. Valentine et al. Muller 2001. 2000). including cryptic * Corresponding author Abstract A wide range of vectors is currently introducing a plethora of alien marine species into indigenous marine species assemblages. Maggs* School of Biological Sciences. 1998) are vectors that introduce a multitude of alien marine species into indigenous species assemblages (Hewitt et al. 1999. resulting in an uncontrollable biological experiment of immense proportions (Mooney and Cleland 2001). 1997. Keywords: alien species. in population structure and allele frequencies. reviewing the genetics of marine invasions. sequential or coinciding metainvasions (Davies et al. however. Due to the convoluted nature of modes of invasion. and (2) changes in genome organization at the species level through hybridization. and in individual gene expression profiles at the levels of expressed messenger RNA and the proteome (i. Olsen et al. Shipping (Carlton and Hodder 1995. all proteins synthesized) and thus the phenotype. Minchin and Gollasch 2003). Jim Provan and Christine A. assignment tests and mixed stock analysis. DOI 10. establishment and subsequent outcomes (Cronk and Fuller 1995. 1994) and the aquarium trade (Jousson et al. a number of reviews. Kolar and Lodge (2001) describe evidence for characteristics that determine the success of an invasive species. with estimates of approximately 10. The consequences for the indigenous and invader species can be rationalized into two main groups: (1) changes in gene-pool composition. hybridization. However. Gurevitch and Padilla 2004). Mooney and Cleland 2001.

2003). showing possible outcomes following introductions of an invasive species into a new region. They highlight the rapidity of the invasion process. few studies deal with periods of more than ten years. Booth et al. 2001. Pikea (Maggs and Ward 1996). 1993). There are insufficient data to give algal examples demonstrating all the processes on this diagram (cf. Provan et al. whilst genetic variation can identify invaders. muticum is competitively excluding red algae. the majority of molecular studies to date have sought to identify the source of aliens.C. F. Meusnier et al. 2001). Silva (Goff et al. 1992. so a small reduction in fitness changes a population from slightly positive growth to negative growth (McGinnity et al. Sphaerotrichia divaricata (C. 2003). Verlaque et al. Do populations of alien species show greater genetic diversity or lower diversity than conspecific native populations? Have alien species usually arrived as multiple introductions? What are the genetic threats in the form of introgression and loss of adaptive alleles? Is it possible to identify genetic traits of successful invaders? Do invading seaweeds exhibit predominantly clonal . and note that successful invasions may be related to both the provenance and genetic responses of the invader. Schaf` felke et al. (2006) showed that it occupies a previously vacant niche on European coasts. 2002. Comparatively little work has been directed towards examining the consequences of seaweed invasions. 2002. 2003). Sanchez et al. Novak and Mack (2005) discuss genetic bottlenecks and how mating systems and genetic diversity influence invasions. but examples are provided where possible based on the following studies: Fucus evanescens vs. 1998. Prince and Trowbridge 2004). in Caulerpa (Jousson et al. Fama et al. where it can grow on soft sediments unlike native macroalgae. highlighting the point that. Asparagopsis (Andreakis et al. Codium fragile subsp. success. concluding that there are insufficient data available to support claims to this effect. our knowledge of introduced species dynamics breaks down. found that in Spain S. Agardh) Kylin (introduced populations of which are noninterfertile with native North Atlantic populations: Peters et al. (2005). Allendorf and Lundquist (2003) examined the population biology. Grosholz (2002) points out that at larger geographical scales and longer timescales. An extinction vortex is defined as a situation where recruitment is close to the replacement level. Codium fragile ssp. tomentosoides (Van Goor) P. Mooney and Cleland (2001) and Lee (2002) examine specific aspects of the impact of invasions on evolutionary genetics. tomentosoides (this subspecies is parthenogenetic: Trowbridge 1998. control of invasives should perhaps involve a ‘‘shoot first. In seaweeds. for example the inheritance of adaptively significant traits and the population genetics of native and non-native species. Sargassum muticum (Yendo) Fensholt wStrong et al.: Genetics of seaweed invasions Figure 1 Key invasion processes. 2005a. 2004) and Polysiphonia harveyi J. with particw66x ular focus on cryptic invasions. Because of the vast range of life history patterns and mating systems in seaweeds (which include representatives of at least three phyla).386 D. Bailey (McIvor et al. Gurevitch and Padilla (2004) reviewed evidence for invasive species as general or primary agents of extinction. Schaffelke and Hewitt 2007). evolution and control of invasive species. ask questions later’’ approach to eradication. perhaps due to competition for lightx. serratus (Coyer et al. many pertinent evolutionary and population genetic questions can be addressed by molecular approaches.

2004).D. predict. 2000). Due to the difficulty in identifying algae by morphology alone. 2002. little can be done to understand. Several recent studies have focused on this highly invasive ‘‘aquarium strain’’ of C. Goff et al. 1998. mexicana (Olsen et al. Provan et al. Vahl) C. Meusnier et al. 2001). Booth et al. The seaweed invasion that has received by far the most attention is that of Caulerpa taxifolia (M. A high level of similarity indicated conspecificity between Californian and English Pikea californica Harvey and a possible vector was identified in the form of Catalina flying boats. Interestingly. 1992). and isolation steps to yield concentrated plastid DNA. are there any general trends in these parameters for invasive seaweeds or is each example case-specific? The aims of this paper are to provide an overview of seaweed invasions from a genetic perspective. as is frequently observed in terrestrial and freshwater ecosystems (Elton 1958)? Do they show different mating systems (e. The vector for an invasion of Codium fragile (Suringar) Hariot into San Francisco Bay in the late 1970s (Silva 1979) was claimed to be boxes of live fishing bait from New England packed in algae that had been discarded into the Bay (Dawson and Foster 1982). 2001). Kusakina et al. Carlton 1996. 1992).: Genetics of seaweed invasions 387 reproduction. plastid DNA restriction fragment length polymorphism (RFLP) analysis was employed to address the origin of Pikea sp. microsatellite markers have been applied to identify the provenance of an introduction. Parker et al. Identification of invasive species and their provenance Arguably this step is fundamental to any research on invasive species as without a working knowledge of these elements. Australia. focusing on invader species for which the greatest amount of molecular information is available. by comparison to Californian and Japanese samples. taxifolia is closely related to strains cultivated in European aquaria prior to the first observations of the species in the Mediterranean Sea (Jousson et al. Schaf` felke et al. Malpeque Bay and Caribou Harbour respectively.. Recently. taxifolia on the Californian coast was later shown to be the aquarium strain also (Jousson et al. tomentosoides into Atlantic Canada in New Brunswick. In a similar study by Maggs and Ward (1996). none of which was the invasive genotype. but could not distinguish between an independent introduction from Japan and secondary transfer from introduced populations in the Atlantic Ocean (Goff et al. Phylogenetic analyses of the noncoding internal transcribed spacer sequences (ITS) of nuclear ribosomal DNA (rDNA) demonstrated that Mediterranean C. 2001. 2004). Ferraris and Palumbi 1996. The earliest attempts to identify sources of introduced seaweeds used plastid genome markers. and to draw on relevant studies of better-known marine and terrestrial organisms to point the way forward in molecular approaches to the study of seaweed invasions. more selfing) compared to non-invasive congeners? Overall. in the Isles of Scilly. but two other Queensland populations (Kissing Point and Kelso Reef) showed high diversity of ITS2 types. Where possible. Initially it was shown that the invasive alga is not conspecific with the widespread tropical species C. w67x . Ferraris and Palumbi 1996. Jarne and Lagoda 1996. 1999.g. (2002) found that the Brisbane population of C. England. we draw attention to evidence that may lead to answers to some of the questions posed above. 1994. The origin of this strain is believed to be Australia (Meusnier et al. 2001. Such analysis has now been largely superseded by polymerase chain reaction (PCR) methodologies to obtain informative haplotypes (Geller et al. this phenomenon has been reported for many marine species groups (e. Coyer et al. Meusnier et al. 2002. it is important to note for the assumptions of population genetic analyses that biological invasions are far from normal or equilibrium conditions (Davies et al. which cuts the circular plastid genome into fragments that form barcode-like patterns on gels. these studies exemplify the point that invasions can occur as multiple events or from multiple sources.g. A variety of diagnostic markers for the mitochondrial. 2001. from the species to the individual.. Bohonak et al. chloroplast and nuclear genomes can be used to classify organisms in a hierarchical fashion (Avise 1994. 1997. Identification of invasive species. tomentosoides. Depending on the level at which studies are aimed. Agardh into the Mediterranean basin (Meinesz 2007). However. 1998). Andreakis et al. They were able to adequately identify two of the three populations as being derived from tropical native stocks. Geller et al. (2006) used morphological data and inter-simple sequence repeat (ISSR) markers to identifiy three independent invasions of Codium fragile ssp. taxifolia and similar results have been obtained with various markers. Meusnier et al. Restriction patterns con- firmed the invader as the non-native subspecies C. it does require whole DNA restrictions. markers that range from hypervariable microsatellite DNA markers (which vary in length due to different numbers of nucleotide repeats) to conserved gene sequences can be deployed. (2002) used ITS in an attempt to determine the origins of three newly discovered populations of C. over 500 of which were manufactured in San Diego and transported to England during the Second World War. introductions may be cryptic in nature or composed of multiple morphologically similar species. Emerson et al. or mitigate the consequences. Whilst plastid genome RFLP produces favorable results due to its conserved nature (Soltis et al. (1997) and discussed below. 1998). Invasive C. sources and vectors Molecular markers A wide array of molecular markers is available to the phycologist today to discriminate invaders from native species. taxifolia in New South Wales. (1992) investigated the source of this invader using plastid DNA restriction fragment length polymorphism (RFLP) analysis. Fama et al. taxifolia was identical to the Mediterranean form. Similarly. as noted by Geller et al. Zuccarello and West 2003. McIvor et al. Schaffelke et al. Hillis and Moritz 1996). but for the third they did not have enough resolution to exclude the invasive aquarium strain. 2002. fragile ssp.

it is highly probable that such populations will have recently undergone a bottleneck (i. as has been achieved previously for exploited fish species (Hauser et al.: Genetics of seaweed invasions (2006) investigated Fucus serratus L. In addition to this. Hoss and ¨¨ w68x Paabo 1993). The application of molecular markers to herbarium material opens up new avenues of research. His prediction was borne out in a study of the red seaweed Polysiphonia harveyi Bailey. 2002. One came from Hokkaido. Booth et al. into the northern North Atlantic Ocean (Nova Scotia and northwestern Europe). Sufficient numbers of individuals (often more than 100) to allow for population genetics are available for some seaweeds: a wide range of species was preserved during the 19th and 20th centuries as multiple replicate herbarium samples known as ‘‘exsiccatae’’. as they allow the exploration of past events. which had already proven useful in distinguishing species and populations of red algae. The ability to isolate and amplify DNA from extinct ‘‘ancient’’ or archival specimens (Paabo 1989) is now commonplace. a reduction in genetic diversity that occurs in populations experiencing rapid. population growth rates and effective population size from gene genealogies in seaweeds.e. Increase in both abundance and distribution of this species was found at 138 sites surveyed along the coast of North Carolina. By incorporating historical information on the shipping trade with their population structure data they identified the sources of the introductions and dated them to the 19th and late 20th centuries. Invasions and population genetic structure Population genetics A key goal to be addressed by the molecular ecologist today is the identification and characterization of both indigenous species and invaders. such as modelling using Bayesian and coalescent methodologies to estimate mutation parameters. (2006) reported the detection of a semi-cryptic invasive species of Gracilaria in North America. and is also found in New Zealand and California. harveyi in New Zealand represents a cryptic invasion due to its morphological similarity with the native P. Using the framework of coalescent . The presence of P. 1998). originally described from North America and considered an alien in European waters. harveyi. While these estimates are all intrinsically interlinked. including cryptic invasions. in Iceland and the Faroe Islands. or nearby. population genetics studies can be used to estimate demographic parameters that can then be related to the stage and magnitude of invasion and the response of the indigenous species. Resolution of putative populations into management or evolutionary significant units (Moritz 1994) through an understanding of their biogeography or genetic structure. Given the nature of invasive algae. rbcL. particularly cryptic species such as Mytilus galloprovincialis (Lamarck) (Geller 1999). (2005a) after examination of eight indigenous and 15 introduced populations. 2001). most recent common ancestor estimates.. By sequencing the rubisco spacer they were able to discriminate vegetative Gracilaria vermiculophylla (Ohmi) Papenfuss from native taxa with ‘‘nearly identical’’ morphology. Analysis of haplotypes combined from chloroplast microsatellite loci and chloroplast sequences indicated a minimum of two separate introductions from the native populations in Japan. tomentosoides were reported by Provan et al. Whilst isolated ancient DNA molecules are replete with oxidative and hydrolytic damage (Paabo 1989. short PCR primers can be developed that ¨¨ amplify small sections of genes studied. From a minimum spanning network of P. such as effective population size Ne. strictissima J. The ability to identify such temporal samples allows for increased accuracy in determining the first introduction of a species. The processes involved at each stage of invasion can be elucidated through estimation of population statistical parameters. succession or displacement to post-invasion. McIvor et al. For seaweeds. Population parameters At each stage in the invasion process from introduction. Tracking invasions in space and time Herbarium and museum samples potentially hold a unique record when considering the introduction of an invasive species. and evidence of genetic impoverishment. Independent introductions into Europe of the green seaweed Codium fragile ssp. one into the Mediterranean and the other into the North Atlantic Ocean and Chile. (2001) employed the gene coding for the large subunit of rubisco. severe reductions in the number of individuals for one or more generations). Hooker et Harvey. two invasive haplotypes were identified that indicated two separate introductions into the North Atlantic Ocean from Japan. Freshwater et al. a variety of statistical approaches have been suggested for most genetic markers.388 D.D. 2003). with observations in locations over the past 170 years. both the invader and the indigenous populations can be examined for a range of parameters. Hutchinson et al. these problems can be minimized by using species-specific or lineage-specific primers. migration rates. The significance of bottlenecks for alien plant species has recently been reviewed by Novak and Mack (2005). although the 4–5% sequence divergence between the two allowed unambiguous discrimination of the two species (McIvor et al. A second haplotype invaded from Honshu into the southern North Atlantic Ocean (North Carolina). Tests for population bottlenecks involve assessment of the relationships between gene diversity and the observed number of alleles in bottlenecked versus nonbottlenecked populations (Luikart and Cornuet 1998. although pre¨¨ cautions must be taken to avoid contamination by DNA from contemporary samples (Willerslev and Cooper 2005). Cryptic introductions Geller (1997) predicted that multiple conspecific introductions would be detected by molecular investigations of aliens. with particular reference to the role of mating systems. has the potential to identify the routes of transfer in order to recommend mitigation steps. Luikart et al.

low genetic differentiation in Asparagopsis armata Harvey in the Mediterranean Sea for nuclear. possibly from a refugium in Brittany. These naturalized admixtures can then contain within-population diversity that exceeds the native range. Alien populations of seaweeds likewise tend to exhibit reduced genetic diversity. (2000) found a lack of variation at the DNA level for both isozymes and randomly amplified polymorphic (RAPD) DNA in New Zealand Hydrilla verticillata (L. mirroring the classical view from theoretical population genetics (e. it is necessary to embrace the paradox that the invader has gone through a population bottleneck (Allendorf and Lundquist 2003. found star-like topologies in minimum spanning trees of haplotypes that are normally indicative of sudden population expansions. through directional selection. Bottlenecks reduce variation throughout the whole genome due to drift. an invasive submerged freshwater weed. though the patterns in population structure were attributable to sequential colonization events and ‘‘edge’’ populations similar to those inferred by Comps et al. Provan et al. Tsutsui et al. however. Likewise. on a grander scale. but they can provide illumination for some invasion scenarios. with some introductions being the product of admixed genotypes from the native range. Conversely. Admixtures from multiple sources result in higher diversity within introduced than in natural populations in many plants (Novak and Mack 2005). Booth et al. Coyer et al. Avise 1994. A coalescent estimate of changes in effective population size revealed an expansion starting w69x .) Trin. at least in the short term. (2001). which was attributed to multiple introductions from highly differentiated sources. Hofstra et al. causing population admixture. (2005a) and Kusakina et al. indicated a much deeper and slower colonization. mitochondrial and plastid markers (Andreakis et al. Studying the postglacial distribution of Fucus serratus in Europe. Indeed Novak and Mack (2005) suggest that this process may foster invasions. (2001) also found higher levels of diversity in the indigenous Japanese populations of P. Both studies attributed this pattern to the inconsequential amount of sexual reproduction. Wang 2001. 1998. In this context. few alleles per locus and low genetic diversity. ex Steud. They found high levels of genetic diversity throughout the species range. harveyi than those in the Atlantic. 2004). Hudson 1991). (2006) in Codium fragile subsp. Clonal reproduction is characteristic of all these species. This mechanism can result in ‘‘patchwork quilt’’ patterns in population structure. 2000). a trend parallel to that noted by Provan et al. therefore. Genetic depauperacy Changes in population structure and reduced genetic diversity associated with the genetic bottlenecks of introduction and colonization have been widely observed. Williamson 1996. (2003) collected data for seven microsatellite loci. Reed and Frankham 2003). increased genetic diversity has been observed in a number of invasive species such as mollusc aliens (reviewed in Holland 2000). The genetic patterns characteristic of postglacial recolonization that have developed on millennial timescales may be detected with more rapidly evolving markers on the much shorter timescales of anthropogenic invasions. Postglacial colonization Postglacial colonization (reviewed in Hewitt 1999) reflects. the postglacial colonization process may represent a model with which to examine the nature of changes in gene-pools over space and time due to invasion.: Genetics of seaweed invasions 389 theory (Kingman 1982..f. In the invasive aquatic plant Phragmites australis (Cav. whereas selective sweeps.D. (2005b). Berthier et al. These have now been succeeded by more powerful temporal methods that employ samples distributed over several generations (Nei and Tajima 1981..g. reduced fitness or increased likelihood of extinction (Frankham and Ralls 1998. The potential explanation for this apparent paradox lies in the research of Voisin et al. Wang and Whitlock 2003) and by Bayesian temporal methods (Beaumont et al. Likewise. and may lead to introgression of adapted genomes (Cox 2004). Pellegrin and Hauber (1999) noted a low percentage of polymorphic isozyme loci. 2004) is thought to be the result of a recent invasion from Australia. bottlenecked populations can be discriminated as they tend to exhibit star-like haplotype networks. 2002). tend towards fixation of beneficial alleles and associated linked regions of the genome (Maynard Smith and Haigh 1974). Heterozygote deficiencies found in 50% of the populations in the Atlantic Ocean and North Sea were attributed to sweeps of temporal colonization. 2000). tomentosoides. The distribution of pairwise nucleotide mismatches. It is also possible to determine whether such a loss of diversity came about due to population bottlenecks or selective sweeps (Galtier et al. with the potential for subsequent recombination and the generation of novel genotypes that can adaptively radiate. 2002. (2005) on the invasive kelp Undaria pinnatifida (Harvey) Suringar. Beerli and Felsenstein 2001) and measures of genetic disequilibrium (Hill 1981. The aquarium strain of Caulerpa taxifolia found in the Mediterranean Sea (and off San Diego. Vitalis and Couvet 2001). There have been a few recent studies of postglacial recolonization of seaweed species in Europe. Refugial populations are equivalent to native populations in having high genetic diversity and the genetically impoverished colonies derived from the refugium have similar features to introduced populations. using a combined approach of nuclear and mitochondrial analysis in a phylogeographic analysis of the red seaweed Palmaria palmata (Linnaeus) Kuntze. McIvor et al. Yet to fully understand the genetic consequences of an invasion. High-resolution markers in non-coding regions of the mitochondrial genome showed increased genetic diversity in introduced populations relative to native populations. Observations of reduced genetic variation within invasive species and populations clearly do not equate with lower evolutionary potential. Earlier studies provided single point estimates of coalescent time (Beaumont 1999. the dynamics of the invader. 2003) and yet is still successful.) Royle. reviewed in Petit et al. By contrast. California) has severely reduced nuclear diversity within and between individuals compared with expectations for normal populations (Jousson et al.

¨ 2002). Bayesian admixture analysis of closely related F. The invasive strain is cold water tolerant compared to the native tropical strains. Meusnier et al. Agardh) Eubank -uvifera (C. mating systems and seed or propagule variation (Rejmanek and Richardson ´ . the aquatic plant Rorippa austriaca (Crantz) Bess. 2003). plastid and mitochondrial markers. 2002). nuclear ITS1 sequences. 2003) and Oncorhynchus sp. including the formation of a hybrid zone (Figure 1). Townsville. 2002). turbinata (J. (Bleeker 2004) and the fishes Gadus morhua (Linnaeus) (Nielsen et al. hybridization can work at the species and population levels by delivering additive genetic variation to depauperate gene pools (Soltis and Soltis 2000). F. In Australia. evanescens C. Agardh species complex. (2002) found only hybrids when both parents were above a threshold abundance level. vesiculosus (Engel et al. Agardh) J. ceranoides Areschoug are all closely related. Mediterranean populations showed no polymorphism with these markers. evaw70x nescens. highlighting the time scale over which such colonization events can occur under natural circumstances. Coyer et al. Natural hybrids were all the result of mating between female F. racemosa var. including that of the first florideophyte. serratus and F. Engel et al. but these suggestions have not been substantiated. evanescens is hermaphroditic. A recent study of the invasion of F. which is a relatively recent radiation. Agardh and an unknown tropical strain. (2003) utilizing ITS1. However. growth rate. Adaptive traits include dispersal characteristics. 1999) and micro˜ satellite allele frequencies (Wallace et al. evanescens was introduced into Oslofjord (S Norway) in the late 19th century and spread to Sweden. reaching the western Baltic by 1992 (Wikstrom et al. noting that hybridization processes generate ‘‘genetic substrate’’ from which traits can be selected in the invasion process. 2002). Later work by Verlaque et al. based on 18S rDNA sequences (Durand et al. In the context of invasiveness. evanescens male = F. 2005). Collen personal ´ communication). are thought to be important components of the speciation process (see Hewitt 2001). with the exception of Fucus. serratus. and resulting introgression of genes from one species into another. the oak tree Quercus sp. was also inter˚ preted initially as the result of recent hybridization between the native C. and F. Lee (2002) highlighted the role of genome architecture studies in investigating additive genetic variation. hybridization and sexual recombination do occur. Further availability of genomic data will undoubtedly open up new fields for exploring seaweed invasions. spiralis and F. evanescens (Coyer et al. individuals of C. 2005. Hybrid zones have been well studied in natural populations of various organisms including the bee Apis mellifera (Linnaeus) (Clarke et al. One individual from Kissing Point. and sexual reproduction occurs rarely. Huisman et Boudouresque and indicated a likely source population in Australia. Fucus serratus and F. 2004. Hybridization Hybridization between species. A second invasive taxon in the Mediterranean Sea (Verlaque et al. in native Australian populations.g. which can detect single base mutations (Wattier and Maggs 2001)x of the ITS and a non-coding intron in the plastid 16S rDNA gene to evaluate the extent of sexual reproduction in Mediterranean and Australian C. 2000). and hybrids were found to be dioecious. Australia showed a combination of two ITS2 profiles that were otherwise found in different individuals collected at the same site. Complete plastid genomes are already available for red. serratus and F. 2005). (Rubidge and Taylor 2004). Mooney and Cleland 2001. but there is no evidence that the invasive strain is the result of hybridization (Meusnier et al. However. The future for molecular studies of seaweed invasions Genomics Several genome sequencing projects are now underway for seaweed species. Billard et al.8S rDNA and ITS2 sequences clarified the taxonomic status of the invasive strain as C. Hybridization was asymmetric.. Chondrus crispus Stackhouse (J. (2002) exploited single strand conformation polymorphism w(SSCP). Booth et al. vesiculosus and F. (2006) using Bayesian microsatellite analysis confirmed hybridization between F. cylindracea (Sonder) Verlaque. SSCP polymorphism revealed several shared bands that constituted 10 different profiles. A subsequent study by Coyer et al. by transferring and generating novel adaptations (Ellstrand and Schierenbeck 2000. Fertile hybrids have been identified by morphology in several areas where the two species now occur together. Coyer et al. as a stochastic event. 2004). serratus female crosses were only 20% as successful as the reciprocal cross. with F. evanescens and male F. spiralis hybridizing naturally.: Genetics of seaweed invasions around the penultimate glacial maximum. Agardh into the native range of F. as evidenced both by intra-individual ITS sequence variation (Serrao et al. racemosa var. Fucus vesiculosus Linnaeus. The invasive strain of Caulerpa taxifolia has sometimes been interpreted as a hybrid (e. belonging to the Caulerpa racemosa (Forsskal) J. and investigated the population dynamics of the hybrid zone. F. with eight of 18 morphologically identified hybrids being F1. and by rearranging coevolved gene complexes into novel combinations through recombination in the introgressed F2 generation (reviewed in Soltis and Soltis 2000. 5. serratus provides interesting details of some key genetic processes in invasions. Using microsatellites. McGinnity et al. evanescens are naturally sympatric only in Iceland and NW Norway (Coyer et al. 2002). taxifolia populations. There is little evidence of natural interspecific hybridization in seaweeds.390 D. Makowka 2000). 2006) provides additional molecular evidence for this hybridization. green and brown seaweeds. Arnold 2004). (2002) demonstrated that individuals with hybrid morphology were indeed genetic hybrids. life history variation. This corresponded well with culture results in which F. spiralis Linnaeus and F. F. (Craft et al. taxifolia with the invasive genotype are up to six times larger and much more robust than the other genotypes. serratus is dioecious whereas F. Both processes have also been identified as elements of biological invasions.

Lee (2002) also noted the role of gene-environment interactions (reviewed in Pigliucci 1996) and commented that invasive species are able to adapt to environments that are significantly different from that of their endemic range. 2004). With the advent of amplified fragment length polymorphism (AFLP) analyses. However. and sequenced to generate expressed sequence tags (EST). 2004. Petit et al. tomentosoides may lie in desiccation tolerance (Schaffelke and Deane 2005). These tests allow the determination of an invader’s origin on the basis of the most likely population in which its multilocus genotype originated (Rannala and Mountain 1997).: Genetics of seaweed invasions 391 1996. affordable high-throughput genome scans and QTL mapping have become available to molecular ecologists (see Liu and Cordes 2004). This approach could be applied to the study of invading seaweeds as AFLP studies have already been pioneered in red algae (Donaldson et al. it is clear that a better knowledge of genomic arrangements. as these features may be associated with the underlying causes of success or failure of particular algal introductions. microsatellite (Buetow et al. 2000) and in kelps (Erting et al. These findings were attributed to the role of either divergent selection on a small proportion of the genome or differential introgression following secondary hybridization. affording detection of invasive and potentially invasive types. 2003) and single nucleotide polymorphism (SNP) maps (International SNP Map Working Group 2001). (2001) utilized 306 AFLP loci to examine speciation in parapatric morphs of the winkle Littorina saxatilis (Olivi). 1998. 2001). This library of expressed sequences can be plotted onto a microarray. 1997. An affordable approach that is already being employed by phycologists uses the technique of subtractive hybridzation (Su et al. Cluster analysis of all loci grouped organisms by morph. Finally. phenotypic plasticity and associated adaptive traits could be fundamental to the future study of invasions. and thus may be linked to adaptively significant genes. both studies come with strong caveats. and that in Caulerpa taxifolia the invasive strain is cold-water tolerant compared to the native tropical strains (Meusnier et al. and screening of gene expression in tissues and types of organisms (Schena et al. and is increasingly used to study fundamental questions in ecology. Clements et al. relatively simple microarray studies could reveal the genes involved. AFLP maps are now commonplace and are recognized as a powerful tool in predicting heterosis. and hybridizing the microarray. Post-genomic research is now commonplace in model species and human gene expression studies. reviewed in Gibson 2002. Although not yet developed in seaweeds. 1995) using a Bayesian method (Rannala and Mountain 1997. samples were grouped by site instead. Wilding et al. Although adaptive genetic traits have not yet been sought in any invasive seaweeds. 2001) to generate libraries of cDNA that are enriched for unique sequences and eliminate those common to both transcriptomes (the suite of transcribed cDNA sequences). phenotypic plasticity and gene-environment interactions (reviewed in Morin et al. more commonly. whereas when these variable loci were excluded from the analysis. 2004) that have been highlighted as key traits in successful invaders (Grosholz 2002. Tests involve either frequency (Paetkau et al. these ESTs can be used to search protein databases using programs such as BLAST and subsequently isolate the gene expressed to a cellular location or biochemical pathway (Gene Ontology Consortium 2004). Wu et al. there are notable examples of such studies in marine invertebrates and freshwater fishes. Booth et al. 2004). Knowledge of genomic architecture has gone hand in hand with the development of whole genome sequences and linkage studies in the form of chromosomal (Montgomery et al. These maps are used in the study of commercially important or model organisms and are associated with large institutes (or. 2000. The combined approach of examining QTLs with AFLP genome scanning represents an ideal methodology for examining adaptively significant traits and phenotypic plasticity in invasive species (Rogers and Bernatchez 2005). Microarrays Microarrays represent a novel way to determine the nature of gene-environment-phenotype relationships that could provide a tool to better understand how some seaweeds become invasive. Wilding et al. Assignment tests can reveal gene flow from invasive species Assignment tests have also recently been applied as an index to estimate population differentiation and admixture (for details see Paetkau et al. Microarrays are essentially arrays of known probes fixed to a matrix that can allow subsequent hybridization of the expressed messenger RNA in the form of cDNA. If we consider that a key trait in the invasion success of Codium fragile subsp. Another approach in the identification of quantitative traits or adaptively significant genes is the use of microarray technology. Pearson et al. Campbell and Bernatchez (2004) employed this approach also in assessing the role of selection and differential adaptation in sympatric pairs of Coregonus clupeaformis (Mitchill) (whitefish) ecotypes. quantitative trait loci (QTL). Lee 2002). (2001) found that 5% of the loci studied exhibited unusually high levels of differentiation. Whilst there is little possibility that there is an ‘‘invasiveness’’ gene and although microarray studies have limitations in terms of reduced sensitivity to low levels of gene expression. Gene expression in response to environmental parameters can then be examined by reverse-transcribing expressed RNA. Approximately 3% of some 440 AFLP loci screened deviated from expectations.D. Upor down-regulation of genes in response to the chosen parameter can be visualized by fluorescence levels for each EST. investigating genome evolution and determining the proportion of the genome involved in adaptive functions (Klein et al. 2004). they may offer a valuable insight into the nature of gene-environment interactions. 2004). 1995. namely that the tests for neutrality assume that loci studied are unlinked. Ranz and Machado 2006). and may identify the gene pathways involved in producing invasive phenotypes. groups of institutes) and research grants. Pritchard w71x . 2000).

1994. J. Biol. predominantly fishes. USA 98: 4563–4568. and L. References Allendorf. Genetics 162: 2025–2035. Population biology. Likelihood-based estimation of the effective population size using temporal changes in allele frequencies: a genealogical approach. 2002. Approximate Bayesian computation in population genetics. we have provided here a summary of valuable technical approaches. this analytical approach seems to be much more robust with regard to incomplete sampling or missing stocks.H. Among the advantages of the pseudo-Bayesian procedure is that w72x baseline groups are not necessarily required to be in Hardy-Weinberg equilibrium. Asparagopsis taxiformis and Asparagopsis armata Bonnemaisoniales. pp. Valero. Sci. Mixed stock analysis Through admixture analysis it is possible to determine the genetic constitution of the mixed groups of populations or species (Utter and Ryman 1993). 1995). Conclusion In conclusion. Beaumont.A. Detecting population expansion and decline using microsatellites. Zhang and D. Chapman and Hall. It is clear that future studies of hybridization. Whilst assignment tests use population allele frequencies to ‘‘assign’’ individuals. 2001). Furthermore. Secondly. and in the stock mixture. P. J. for each locus. works by sequentially improving a computed ‘‘guess’’ until convergence at a maximum likelihood perceived to be the best estimate. Examining the adaptive genetic traits that underlie the success of a particular invasive species may yield valuable information that can then be used to produce predictive models.C. Rhodophyta: genetic and morphological identification of Mediterranean populations.392 D.M. Procaccini and W.W. Acknowledgements Our genetic studies of invading seaweeds have been funded by ALIENS (EVK3-CT-2001-00062) and the Esmee Fairbairn Foun´ dation (Marine Aliens project). Although potentially useful. 2004. GSI uses complex algorithms to estimate the relative contributions of the putative populations in order to make up the multilocus genotypic frequencies observed in the mixed stock (Fournier et al.: Genetics of seaweed invasions et al. the main one being the assumption of Hardy-Weinberg equilibrium for the baseline samples (Pella and Masuda 2001). N. 2001. W. there must be a reasonable understanding of the individual stocks (i. uses Bayesian likelihood functions to generate a prior probability density based on the relative frequencies of the alleles present in both the baseline samples. 2004. This methodology is known to have a number of limitations. and J. 17: 24–30. for several decades and may prove invaluable in studying invasive conspecifics.L. G. spiralis and F. G. Maximum likelihood estimation of a migration matrix and effective population size in n subpopulations by using a coalescent approach. This must be linked with the existence of detectable temporally stable genetic differences among those groups and methodologies to detect them. E. M. even with a low likelihood. Genetic isolation between three closely related taxa: Fucus vesiculosus. P. 2002. 2000) or the likelihood-based Markov Chain Monte Carlo approach (Chikhi et al.. Serrao. Assignment tests are best suited to detect potential immigrants and gene flow rather than to determine proportional contribution of stocks in a group of ‘‘unknowns’’. Engel and ˜ M.F. The conditional maximum likelihood estimate. In these cases. Beaumont. Dauguin. . whilst it is critical to identify the source of the invading alga to fully characterize the biological niche it occupies.A. Pearson. M. The pseudo-Bayesian analytical procedure. Arnold. Natl. to a given sample included in the baseline (even if this is not the true population of origin). Debevec et al. Avise. J.C. the individual is classified as a population sample of only two genes. Phycol. Beerli. Berthier. there must be reliable methods for estimating the proportions of the various groups in the population. Mixed stock analysis has become powerful enough to allow the determination of the relative contribution to a mixture of native source populations (Galvin et al. Phycol. E. Conserv. New York. evolution and ecology of invasive species.J. 2005. Andreakis. phenotypic plasticity. Cornuet and G.. Felsenstein.. 2000).. Genetics 153: 2013–2029. First. London. 1984.A. Billard. 38: 1–12. meaning that large amount of data must be collected. 1994). Proc. J. Booth et al.e. 1999. 41: 900–905. F. Acad. Balding. these tests tend to be most powerful when a large number of informative markers (i. Kooistra.L. 511. Transfer and origin of adaptations through natural hybridization: were Anderson and Stebbins right? Plant Cell 16: 562–570. they can be modified to implement both genetic distance and allele-sharing based measures. C. C. The most fundamental of these is that every individual is assigned. which is likely given the cosmopolitan or wide distribution of many seaweeds. populations) that are potentially contributing to the system. however.. The application of genetic stock identification procedures has allowed the evaluation of mixed stock in a variety of species. 2003. 40 or more loci) are used (Bowcock et al. M. ceranoides. Since there has been relatively little work carried out on the genetics of invasive algae relative to other invasive groups. which is readily implemented in the statistical package SPAM (Statistical Program for Analyzing Mixtures. recently implemented by Pella and Masuda (2001) in the computer program BAYES. natural history and evolution. Beaumont.. gene-environment interactions and differential gene expression will play a role in determining what makes an organism invasive. Luikart. Lundquist. F. Finally.R. Genetics 160: 741–751. Pella and Masuda 2001).A. M. Eur. Molecular markers. Recent advances in computational science and molecular tools have prompted the development of two analytical procedures.e. it is also necessary to determine the potential genetic changes that will occur following invasion. assignment tests have a number of drawbacks.

C. Daugbjerg and P. L. Gomory. 2002. Cardina. 2: Ecosystems.E. 226. Berkeley. (Phaeophyceae. 47: 186–199. 89: 1792–1798.L. Saunders. and K.W. Ecology 86: 3364–3376. Millar and J. Geller.F. 2004. Puck. Gates. Grosholz and G. Galtier. 121: 721–730. Donaldson. Carlton. Price.V. D. 1958. Mol. J.H. Systematics Association Special Volume No. Chopin and G. Ludwigsen.B. Phycol. Hamner. Plant Syst. Bruford and M. N.. J.R. 2005. 1982. Kidd and L. C. N. SPAM Version 3. Riddell and C.T. The Africanization of honeybees Apis mellifera L.J. Biotic resistance to invasion: native predator limits abundance and distribution of an introduced crab. J.2: statistics program for analyzing mixtures. and J.L. Thiebaut and R. Appl. S. Dini. Koenig. Jivoff. Nolan. DC. S. Walton. Stam and J.F.W. Genetic polymorphism in Caulerpa taxifolia (Ulvophyceae) chloroplast DNA revealed by a PCR-based assay of the invasive Mediterranean strain. European Commission Ecosystem Research Report. D. Fish Biol. 1997. Coyer. E. Cryptic invasions of the crab Carcinus detected by molecular phylogeography. 246: 35–44. Farnham. and prediction in marine invasion ecology. 2006.. Decline of a native mussel masked by sibling species invasion. 2006. 15: 122–133..K. A. A microsatellite-based multipoint index map of human chromosome 22. Genetics 158: 1347–1362. Doohan. Ralls. S. Ellstrand. Eur.. Chlorophyta) in the Mediterranean Sea. 1994. Natl Acad. Bot. Villablanca and G. J. 400. 39: 243–256. Comps. Geller. E. Olsen. Ferguson.S. Elton. N. Ruiz-Linares. pp. Q. G. O’Farrell and T. Durand. Roderick. J.D. Invasion genetics of New World medflies: testing alternative colonization scenarios. Florideophyceae). F. Molecular zoology: advances. Pedersen. 2003.. w73x .T. J. 1999. L. W.E. Boudouresque.F. C. High resolution of human evolutionary trees with polymorphic microsatellites. Genetic variation and self-incompatibility within and outside a Rorippa hybrid zone (Brassicaceae). Donaldson. J. B. animals. Biol.W.P. Chapman and Hall. J. Conserv.C. Yang. W. J. Meinesz.. Meinesz. Biol. 181. M. E. Fucus serratus and Fucus evanescens (Heterokontophyta: Phaeophyceae) in a 100-year-old zone of secondary contact.T. Montgomery. Biol. Biol. J. M. Can. 41: 235–246. Evolution 56: 1462–1474. Whitfield. 2001. Peters. F. Craft.. Barton.. Dawson. A.J. In: (C. PCR-based detection of mtDNA haplotypes of native and invading mussels on the northeastern Pacific coast: latitudinal pattern of invasion. T. R.. Bowcock. B.. John Wiley and Sons.J. Letouzey.S. Appl.J. eds) Introduced species in European coastal waters. J. J. 2004. Genetic entities and ˜ mating system in hermaphroditic Fucus spiralis and its close dioecious relative F. Davies. Nature 368: 455–457.E. Evol. 241. Evol. Spielman and B. P. Roderick.B. 15: 618–624. Hybridization of the marine seaweeds. P. Briand and C. Origin of Fucus serratus (Heterokontophyta. pp. W. 1996. Powers. Verlaque and Y.F.A. process. USA. Bernatchez. pp. E. Booth et al. 10: 365–370. Nucleotide diversity within and between four species of Laminaria (Phaeophyceae) analysed using partial LSU and ITS rDNA sequences and AFLP. J.. K. Conservation biology – inbreeding leads to extinction. Budarf. 14: 17–21. Biol. In: (J. USA 97: 7043–7050. B. Studies on aliens in the marine flora of southern England. 104: 379–398. Carlton. Geller. D. Phycol. 2004. A.H. Debevec. Biogeography and dispersal of coastal marine organisms: experimental studies on a replica of a 16th-century sailing vessel. 13: 661–664. O. Booth. Cox... Olsen.E. microbes. Fournier.L. Ashley and W.F. Diverging trends between heterozygosity and allelic richness during postglacial colonization in the European Beech. Estimating stock composition in mixed stock fisheries using morphometric. J.M.M. Rinderer. W. M. Molecular data suggest a hybrid origin for the invasive Caulerpa racemosa (Caulerpales. Foster. Chopin and G. and electrophoretic characteristics.. D. 119: 243–249. Soc. 2000. Busack. Duggan.D. Introduction of marine benthic algae into Atlantic European waters.W. Frank. J. M.. Peters. Campbell. B. Mol. Serrao. Zaninetti. McKinnell. 2004. Jordan. Cavalli-Sforza. Coyer. J. Adaptability of plants invading North American cropland.A. Conserv. Seeb. S. C. 6: 256–262. Emerson.D. Fama. Seashore plants of California. 91: 509–510. Am.A. A. A. Quezada-Euan and B. 1980. Determining the source of newly founded populations: multilocus genotyping in nonequilibrium population genetics. Cronk. J.D. 2002. T.Y. Trends Ecol.B. 2005. Stam and J. Vol. F. 2000. Amplified fragment length polymorphism (AFLP) as a source of genetic markers for red algae. The ecology of invasions by animals and plants. J. 2000.B. K. Postice age recolonization and differentiation of Fucus serratus L. 14: 2033–2046. Revealing the ´ demographic histories of species using DNA sequences. Evol. Manuel. Pawlowski. pp. Coyer.A.L.A. Hines and P. B. J. N. J.A. J. Masuda. 2001. 2001. F.W. Evol. F. Invasions 3: 103–111. Ecosyst. Sci. Stam and J. Biol. J. 2004. 2003. Palumbi.L. Fish. New York.M. A. 1998. Beacham. Pattern. Invasions 8: 631–637. 269: 1829–1834. 41: 400–408. Davies. Paradis and C. Villablanca and G. Genomics 18: 329–339. Fucaceae) populations in Iceland and the Faroes: a microsatellite-based assessment.G. and L.A. Carlton and D. G. Limited hybridization between Quercus lobata and Quercus douglasi (Fagaceae) in a mixed stand in central coastal California. Petit. London. Evol. Mar. 1995.T.B. J. Minch. Lond.H.R. London. strategies and protocols. Ferraris.A.J. 21: 945–956. Clarke. R. M. P. de Rivera. 2000. Chikhi. University of California Press. Daguin and E. 32–36. J.. 78: 97–106. J. Alien species and evolution: the evolutionary ecology of exotic plants. 1995. Phaeophyceae). S...L. D. Generic scan using AFLP markers as a means to assess the role of directional selection in the divergence of sympatric whitefish ecotypes. K. Eur. Boudouresque.: Genetics of seaweed invasions 393 Bleeker. Bohonak. Agric. D. Depaulis and N. M. Erting. J. Freshwater.B. C. 1994. Fuller. 1984. A. Ecol. Williams and P. pp. 1998. Phycol. M. 1995. J.S. A. Le Parco. Thebaud. Nature 392: 441–442. Greene.F. N. and M. Hodder. W.D. of the Yucatan: a study of a massive hybridization event across time. Murphy and C. Irvine and W.R. Biol. Plant invaders: the threat to natural ecosystems. New York. M.C.. and J. Di Tommaso. F.D. Mar. G. Saunders. C. 12: 1817–1829.S. A. Env. 16: 707–716..G. E. A. Porter. Distribution and identification of an invasive Gracilaria species that is hampering commercial fishing operations in southeastern North Carolina. N. B. B. Genetics 157: 389–397. 17b.. Ecol. D.. L. vesiculosus (Fucaceae.T. J.C. R.E.X. and S..M. J. Mohler.. A. pp.X.W.H. Ruiz. R. Genetics 155: 981–987. Sci. Oldroyd. 1996. J. Mol. Proc. Engel. Hoarau. Ruiz.L.E. C. Ecol.F. Clements. Galvin. Emanuel. 12: 25–35. eds) The shore environment. pp. Trends Ecol. Swanton. 2002. J. E. G. Aquat. Hybridization as a stimulus for the evolution of invasiveness in plants? Proc. An assessment of the AFLP method for investigating population structure in the red alga Chondrus crispus Stackhouse (Gigartinales. Mol. Washington.R. meristic. Methuen and Co. Pella. Genetic stock identification of Atlantic salmon using single locus minisatellite DNA profiles. Biol. Olsen. Island Press. Frankham. Schierenbeck. Academic Press. and K. Fucaceae) populations in Northern Europe. Biol. T. Buetow.K. 875–914. Reynolds and L. T. 2002..F. 2002.. 580. Farnham.K. Hered. and interacting native species. Taggart. 1999. Evol. Di ` Giuseppe. Jousson. 2001. Estimation of admixture proportions: a likelihood-based approach using Markov Chain Monte Carlo. Tomfohrde. Farnham.T. R. W. 1994..K. Cross.L. Phycol. Beaumont. Detecting bottlenecks and selective sweeps from DNA sequence polymorphism.M.

M. w74x . Wayne and the SNP workshop group. R. Trends Ecol.A. Montgomery. Di Guiseppe.A. N. D. J. Ser. Trends Ecol. Ecol. M. Olsen and W. I. Trends Ecol. Hofstra. Ale and J. Linn. J. Gibson. 32: 176–193. B. Fitness reduction and the potential extinction of wild populations of Atlantic salmon. Lesk. Fouling and ships’ hulls: how changing circumstances and spawning events may result in the spread of exotic species. Provan and M. life history and molecular studies. Prodohl. Mol.H. Meinesz and C.L. Haigh. Ecol. Childs. Oxford. pp. incipient species status for the invasive strain. 19: 208–216. Carvalho. J. N. Evol. Hewitt.. Evol. Oxford University Press.. 2001. Biol. C.W. Bot. Nature 409: 945–946. Molecular evidence for the aquarium origin of the green alga Caulerpa taxifolia introduced to the Mediterranean Sea.42 million single nucleotide polymorphisms. Evol. Mar. A. 1999. USA 98: 5446–5451. Olsen. E. C. Allendorf. The hitch-hiking effect of a favourable gene. 10: 931–946.T. 2004. J.. Estimation of effective population size from data on linkage disequilibrium. Mar. Soc. 1–44. L. and J. Monterey Bay National Marine Sanctuary fact sheet: Caulerpa taxifolia. 2004. In: (D. B 270: 2125–2132. Muller. Grosholz. G.394 D. H. Meusnier. Res. G. I.E. Trends Ecol. Microarrays in ecology and evolution: a preview. from molecules to populations and back. Schlueter. Acad. W.. Valero. J. J. RAPD profiling and isozyme analysis of New Zealand Hydrilla verticillata. Evolutionary genetics of invasive species. Mol. P.R. E. Hillis. P. 50: 373–384. 2001. L.. Progr. Eur. Cross. Taggart and T. Steele and F. The evolutionary impact of invasive species. 2003. 2001. K. Hynes. 38: 209–216. Voytek and A. C. Z. Boudouresque. Adam. Hill. Sunderland. Aquaculture 238: 1–37. Sinauer Associates. Polymerase chain reaction-single strand conformation polymorphism analyses of nuclear and chloroplast DNA provide evidence for recombination. Lodge. Roga. McIvor. 2007. Proc. Cordes. Gurevitch. 17: 386–391. P. 1996. A high-resolution map of human chromosome 12. R. J. Morin. 1996. 2002. Roy. Booth et al. DNA marker technologies and their applications in aquaculture genetics. Progress in invasion biology: predicting invaders. 49: 1–9. Adcock. A. Campbell and B. Ecological and evolutionary consequences of coastal invasions.B. 12: 228–237.J. J. Methods for identifying and tracking seaweed invasions. J. B. Zaninetti.D. J. 172: 275–280. D. Carvalho. Microsatellites. J. Invasion history and genetic population structure ¨ of riverine macroinvertebrates. J. Mullet. Genetics of marine bioinvasions. 39: 83–92. Cleland. Luikart. Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. R. O’Hea. Usefulness of molecular markers for detecting population bottlenecks via monitoring genetic change. Ecology 77: 1680–1686. Makowka. 11: 17–24. C. Report to the Monterey Bay National Marine Sanctuary. 9: 373–375. Goff.D. W.W..M. Mol. Liu. D. C. 10: 789–807. 1998.A. Natl. Genet. Nucleic Acids Res. W. Acids Res. D. 11: 2317– 2325. a siphonous green alga. Gode. Maynard Smith. Dini. Res.. Coleman. Ecol. Luikart. Stam and J. 16: 199–204. Nature 408: 157–158. L. Kristie and M.L. C. J. p. S. 1996. 2003. 1992. 1981. Cotter. C.J. Gene genealogies and the coalescent process. Zoology 104: 346–355..J. O’Maoileidigh.S. 1996. J. Genet.. Stanhope. Hauser. Phycol. Trends Ecol. G. Am. Natl.M. 1993. Valero. Genome Res. G. J. Mass. 79: 1279–1285. 2002. Clayton. M. USA 99: 11742–11747. 1991.T.T. 2000. Evol. eds) Oxford surveys in evolutionary biology. F. G.I. Temporal analysis of archived samples indicates marked genetic changes in declining North Sea cod Gadus morhua. B 270: 2443–2450. Hewitt. J. R.M. Millar and A. L. Meusnier. G. G. P.: Genetics of seaweed invasions Gene Ontology Consortium. 68: 87–112. Silva.E. 2003. 11: 424– 429. 2000. 2001. Rhodophyta) in England and the North Pacific. J.. A. Kusakina. Schaffelke. 1994. Cooke. 2000. Bot. M. 2002.E. 2004. B. 50: 326–337. C.F. Meinesz. 2002. 1998. Tracing species invasion in Codium. 17: 22–27. The coalescent. Acad. M. Pawlowski. and S. Morishige.T.B. Salmo salar. Loss of microsatellite diversity and low effective population size in an overexploited population of New Zealand snapper Pagrus auratus.K. 2001. Cornuet. Mol. and J. Hoss. Klein. Dong.M.-M. and B. Proc.. Cartinhour. O. A. as a result of interactions with escaped farm salmon.F. 1982. comparative morphological. eds.J. Olsen. pp. Soc. Phycol.J. Sci. Evol. Baker. R. and E.C. Kolar.E.E. Smith. Mol. Pawlowski. Maggs. Minchin. Luikart. Rogers and G. multiple introductions and nascent speciation in Caulerpa taxifolia complex. 32: D258–261. 2002. W. Introductions of seaweeds: accidental transfer pathways and mechanisms. Morphological and molecular evidence for multiple invasions of Codium fragile in Atlantic Canada. Defining evolutionary significant units for conservation. J. 2004. C. Evol. Aquat.A. L. Invasive alga reaches California: the alga has been identified that threatens to smother Californian coastal ecosystems. F.N. Destombe and M. 2002. 2007. 2001. Hudson.. Conserv. Liddle. A.E. S. Phylogenetic analyses of Caulerpa taxifolia Chlorophyta and of its associated bacterial microflora provide clues to the origin of the Mediterranean introduction. D.D. W. 66: 153–166. Trends Ecol. Biol. Nature 409: 928–933.A. volume 7. Stam. J. 2000.L. using molecular tools. Meusnier.R. E. Oxford. and D. 7: 963–974. Padilla.F. Dadswell. van Oosterhout. Jarne. 2001. Antonovics. P. Ward. P. Ecol. Stam. J. Moritz. Moritz.M. Analysis of rDNA ITSI indels in Caulerpa taxifolia (Chlorophyta) supports a derived. McGinnity.L. The Gene Ontology GO database and informatics resource. Mar. P. 10: 537–549. hybrid zones and phylogeography – or seeing genes in space and time. SNPs in ecology.. J. 2000. and J. Lee.T. Jousson. Zechman.W. M.A. Woodfield. Ecol. 376. Bot. Holland. R. D.R... Ramirez and G. Valero.C. Kingman. Proc. Zaninetti..J.G. G. Soc. Ulanch.D. The genus Pikea (Dumontiaceae.K. 10: 911–919. Hutchinson. Mar. Biofouling 19: 111–122. Hydrobiologia 420: 63–71. P. Destombe.F. Postglacial recolonization of European biota. Klein. Obert. Mol. rbcL sequences reveal multiple cryptic introductions of the Japanese red alga Polysiphonia harveyi. Sci. G.M. A high-throughput AFLP-based method for constructing integrated genetic and physical maps: progress toward a sorghum genome map. Nucl. Meinesz. Ferguson. Ecol.L. Grosholz. and S. DNA extraction from Pleistocene ¨¨ bones by a silica-based purification method.L. Evol. 655. 23: 23–25. D. pp. and P. Hewitt. I. Sherwin. evolution and conservation. Are invasive species a major cause of extinctions? Trends Ecol. 1. 2001. Proc. 19: 470–474.R. Mooney. ´ Bonhomme. M. Lond. Snyder. Futuyama and J. F. Green and K. Maggs. L. 1974. Stochastic processes and their applications 13: 235–248.D. Bot.W.J. Oxford University Press. A map of human genome sequence variation containing 1. and G. 2004. International SNP Map Working Group. M. Molecular systematics. Ecol. Gollasch.L. Lagoda. Desmarais. Speciation. O. Paabo. et al. Contrasting rates of spread for introduced species in terrestrial and marine systems. 1998. and D. London Ser. Introduction to bioinformatics. Jousson. 21: 3913–3914. C. K. 2006. S. Bot.

and R. Ribera. Phragmites australis (Cav. Conserv. Hydrobiologia 260/261: 31–36. tomentosoides. Machado. 2001. Chloroplast microsatellites: new tools for studies in plant ecology and evolution. 2003. Bot. D. Mar.S. 44: 204–210. E. Sanchez. Ecol. N. Slade. S. 1996. Stachowicz and S. IUCN. Proc. C. Murphy and S. Stam. Z. pp. Shine. J. Reduced genetic variation and the success of an invasive species. Acad. 17: 230–237. 1999. Evolution of the ˜ Fucaceae (Phaeophyceae) inferred from nrDNA-ITS.K. Utter. 1992. and D. D. Ecol. Hybrid zone structure and the potential role of selection in hybridizing populations of native westslope cutthroat trout (Oncorhynchus clarki lewisi) and introduced rainbow trout (O. Bayesian methods for analysis of stock mixtures from genetic characters. Booton and P. Environmental Policy and Law Paper no. 1995. Progr. Ecol. 1979.M. Meldrup and P. Tracking the invasive history of the green alga Codium fragile ssp. Murphy and C. Genetic assignment methods for the direct. Phylogeography of the red seaweed Palmaria palmata reveals a Pleistocene marine glacial refugium in the English Channel. Impacts of introduced seaweeds. Ecology 79: 361–382. Introduced marine plants. 287–311. Sci. I.O.D. mexicana (Chlorophyta) are not conspecific. 99: 151–167. 4: 347–355. and R. B. 97: 7051–7057. San Francisco. Inference of population structure using multilocus genotype data. What molecular markers can tell us about populations: choosing and using a molecular marker. Brown. J. Trowbridge. D. 14: 189–194. M. Schena. Calvert.J. Invasions 7: 557–565. Gundling. 1997. Rogers. Chapman and Hall.J. Science 270: 467–470. Valero. Deane. 1993. Genetics 155: 945–959.) San Francisco Bay: the urbanized estuary. Boele-Bos and W. Rubidge. In: (D. 13: 735–3749. ¨¨ molecular cloning and enzymatic amplification. real-time estimation of migration rate: a simulation-based exploration of accuracy and power. R. and F. 16: 142–147.E. Biol. Ecol. Pella. and Doyle.A.A. Genetic markers and mixed-stock fisheries. Serrao and M. Brawley. California. The role of genetic and genomic attributes in the success of polyploids.E. M. Bull. 2004. 47: 461–470. How organisms respond to environmental changes. Stachowicz and S.J. 1999. Gaines. J. 2003. B. Soltis. Case. Pritchard. 41: 942–949.E. J. 2005... J. with special reference to macroalgae. pp.) Trin. and C. J. 2001. Mol. 2005. Natl. Wattier and C. Introduction. Phycol. 1981. Mol.M. and D.L. Acad. Invasive alien spe¨ cies: a guide to designing legal and institutional frameworks on alien invasive species..L. Fuerst. S. 138. ed. Mar. R. Acad. Mack. J. Pigliucci. Provan. Switzerland. Correlation between fitness and genetic diversity. Fisheries 18: 11–21. Evidence of a hybrid zone in Atlantic cod Gadus morhua in the Baltic and the Danish Belt Sea revealed by individual admixture analysis. Schaffelke. American Association for the Advancement of Science. Integrating QTL mapping and genome scans towards the characterization of candidate loci under parallel selection in the lake whitefish Coregonus clupeaformis. Acad. Serrao. w75x . Frankham. B.. Ann. 36: 1–64. 197: 117–137. Petit. Shalon. 50: 397–417. R.P. 2004.S. Colonization and modification of soft substratum habitats by the invasive macroalga Sargassum muticum. Prog..J. Fishery Bull. Gaines. Sci. Ecol.A. and J. What attributes make ´ some plant species more invasive? Ecology 77: 1655–1660. evolution and biogeography. Richardson. Hauber. Paabo. and C. S. 1997.L. Bialozyt.D.J. 13: 55–65. Stephens and P. Natl. E. Rev.A. Novaczek. Soltis. Evol. Taylor. P. Natl. M. Genetic bottlenecks in alien plant species. Meusnier. Desiccation tolerance of the introduced marine green alga Codium fragile ssp. Evol. tomentosoides – clues for likely transport vectors? Biol. Mediterranean Caulerpa taxifolia and C.D. Phycol.. 2002. 1998.M. 2000. In: (D. 35: 382–394. Gaines. Provan. Proc. A. and D. pp. 201–228. 2003. Bernatchez. Alice and S..A. D.W.E. Grønkjær.D. Mol.S.T. Provan. Booth et al. 2001. J. Pellegrin. Evol. Bot.. Hansen. Novak. J. and L. Ryman. Mar. eds) Species invasions: insights into ecology.F.Z. W. D. Su. Ruzzante. Mountain. 2006. H. Genetic drift and estimation of effective population size. 2000. 1–7..F Sax. 34: 850–856. Maggs.L. Phycol. Intraspecific sterility barrier confirms that introduction of Sphaerotrichia divaricata (Phaeophyceae. 14: 351–361. Genetics 98: 625–640. Stirling and C. Strobeck. Schaffelke.J. Suppression ˜ subtractive hybridization for studying gene expression during aerial exposure and desiccation in fucoid algae. eds) Molecular systematics of plants. 40. 117–150. 1996. Powell and P.F. Fernandez and J. 2005. Uncovering evolutionary patterns of gene expression using microarrays. ´ ´ Ecology and genetics of tree invasions: from recent introductions to Quaternary migrations. from phenotypes to molecules and vice versa. Schug. Boudouresque. M. Bot. Parker. Soltis. A. and D. Prince. D. R. Aquat. 36: 359–366. ex Steudel. 21: 29–37. Long-term changes in the structure of intertidal assemblages after invasion by Sargassum muticum (Phaeophyta). Phycol. Natl. characterization. Tajima. Milligan. Sci. Ecol. pp. Ecol. T. Phycol. Forest Ecol.A. J. and N. Sax. D. Soltis. B. In: (Conomos. Peters. 12: 1497–1508. Hollingsworth.A. Ancient DNA: extraction. 63: 241–259. M.A. L. Suarez. 11: 187–268. Hampe.H. Pearson.J. Rejmanek.A. Isozyme variation among populations of the clonal species. Natl. Shi and P. M. Chordariales) into the Mediterranean was from Japan. Rannala. USA 86: 1939–1943. Biol. and C. 2006. R. pp.B.J.D.M. Subtraction hybridization identifies a transformation progression-associated gene PEG-3 with sequence homology to a growth arrest and DNA damage-inducible gene. Soltis and B. E... 1993. Estoup. Sax. 2007. Cancela. M. Silva.. USA 94: 9125–9130. P.D. Dring and C. The benthic algal flora of central San Francisco Bay. 2005a. P. 1998. E. Sci. Reproduction in the green macroalga Codium (Chlorophyta): characterization of gametes. J. Acad. Mar. A. G. Influence of mating systems and introduction dynamics. J.. D. Olsen. P.. Holway and T. Mol. W. Strong. New York. D. 1995.C.C. Mol. J. Kawai and I. C. Uthicke. 1998.. Detecting immigration by using multilocus genotypes. Using genetic techniques to investigate the sources of the invasive alga Caulerpa taxifolia in three new locations in Australia. 14: 793–805. Proc. Sunderland. Tsutsui.A.. I. M..H.F. Sinauer Associates. 321: 87–97.M. Paetkau. In: (D. Quantitative monitoring of gene expression patterns with a complementary DNA microarray. 97: 5948–5953. Stachowicz and S.J.N. Fisher. Burden and A. J. Schaffelke. Hewitt. 1995. Garnier-Gere and A.G. USA 94: 9197–9201. Poll. 2000.M. Trends Ecol. Y.: Genetics of seaweed invasions 395 Nei. Sci. S. S. Masuda.D. MA. Maggs. and E. Ser. 1989. I. Mol. Mass. Donnelly... Ranz. Mol.V. Eur. P. Res. mykiss). Oceanogr. 2005b. 2005. eds) Species invasions: insights into ecology. D. mechanisms and impact.J.. Ecol. Davis and P. Microsatellite analysis of population structure in Canadian polar bears. Managem. Arrontes. M. N.D. Trends Ecol.A.S. evolution and biogeography. Snow. N.A.. F.B. J.F. J. Nielsen. 11: 168–173. Trends Ecol. Proc. Ecology of the green macroalga Codium fragile (Suringar) Hariot: invasive and non-invasive subspecies.G. Proc.. M. Soltis J. Sinauer Associates. M. 2005. Sunderland. Mar.E. Maggs. C. Paetkau. G. and C. 2004. Reed. 2004. Williams and L. and M. Trowbridge. P.

J. G. C. pp..L. A pseudo-likelihood method for estimating effective population size from temporally spaced samples. 2005. Wu. A. 2001. Johnson. Couvet. Willerslev. spread and persistence of introduced seaweed populations.L..C. L. 2001.H. Bot.C.. 21: 1–16. Southern Sweden. Bot. Zuccarello. S. Williamson. and A. T. 45: 50–517.C. 2001. R. Differential gene exchange between parapatric morphs of Littorina saxatilis detected using AFLP markers. Maggs. West. Chlorophyta). 2000.A. Quantifying threats to imperiled species in the United States.M. Huisman. 2005. Phillips and E. 78: 243–257. Adv. D.. Losos. Proc. Theor. Genetics 163: 429–446. Acad. D’Antonio. Biol. Magierowski and C. On the identity and origin of the Mediterranean invasive Caulerpa racemosa (Caulerpales. Kautsky. Boudouresque. Determining the affinities of salt marsh fucoids using microsatellite markers: evidence of hybridization and introgression between two species of Fucus (Phaeophyta) in a Maine estuary. C. Phycol. Li. Proc. 38: 325–339.F. Gravez. Introduced species: a significant component of human-caused global change. Boudouresque and Y.396 D. J.L.S. 244. Genet. J. Klein and A. Fang. Natl.A. B 272: 3–16. Li and Z. A. Differential shuffling of native genetic diversity across introduced regions in a brown alga: aquaculture vs. Wallace. L.. and C. 2000. A. von Wachenfeldt and L.. R.L.R. J. 2005. Cooper. M. Phycol. R. Ancient DNA. New Zeal. J.P. Whitlock. Bioscience 48: 607–615. Eur. 102: 5432–5437. 14: 611–619. 35: 171–212. Genetics 157: 911–925. Viard. C. Loope. 2006 w76x . C.and two-locus identity measures. (Phaeophyceae) in Øresund. Le Parco. Mar. Wang.S. Res.J.F. Mathieson. Appl. 2001. Dubow. 50: 351–360. M. A. 2003. J. M. C. M. accepted 23 November.F..: Genetics of seaweed invasions Valentine. Chapman and Hall. 2007. Evol. Phycol. Vitalis. Res. London. 1996. Estimation of effective population size and migration rate from one. E. Wilding. Hu. Verlaque..R. 43: 49–68. and J. Multiple cryptic species: molecular diversity and reproductive isolation in the Bostrychia radicans/B. J.A. Westbrooks. 2003.M. and D. Y. J.B. C. Ecol. Sci. Zeng. Genet. Verlaque. Mar.. Ulvophyceae) in the Mediterranean Sea. M. Grahame.S. Han.M. J. and M.K. R. Durand. Engel and F. J. Mar. Voisin. Mechanisms of invasion: establishment. Wilcove D. 100: 1249–1256. Roy. London Ser. Wattier R. Butlin and J. Intraspecific variation in seaweeds: the application of new tools and approaches. The Caulerpa racemosa complex (Caulerpales. Estimating effective popu- lation size and migration rates from genetic samples over space and time. 40: 1013–1027.J. Ag. 2003. Rejmanek and R. 1998. moritziana complex (Rhodomelaceae. 2004. Rothstein. Soc. Wang. Wikstrom. M. 1997. maritime traffic effects. Estab¨ lishment of the exotic species Fucus evanescens C. An integrated genetic map of Populus deltoides based on amplified fragment length polymorphisms. Vitousek P. 39: 948–959. Meinesz and V. Booth et al. Rhodophyta) with focus on North American isolates. J. Biological invasions. 2002. Bot. Received 23 December. J. Bot..

rapid response and control to reduce the likelihood of negative impact effects. overfishing. more awareness of the problem and increased survey effort are likely to have increased the detection of introductions (Ruiz et al.. 2000. introduced macroalgae. Wilkinson 2004). 1994). 1999. However. PMB 10. habitat alteration and destruction. Introduction It is now widely accepted that global marine biodiversity and resource values of the world’s oceans are threatened by anthropogenic influences. 2000. see also Costello and Solow 2003). reflecting increased global trade and changes in economic activities. toxic effects on other biota.. Hewitt 2003b).gov. The assessment of ecological impacts of alien marine species has been recognized as a research priority in recent years. hence. and reduced abundances/biomass of native macrophytes. predict and measure impacts of introduced seaweeds. developw77x . the Asian clam wPotamocorbula amurensis (Schrenck)x in San Francisco Bay (Nichols et al. 2002. Evidence is now also mounting that synergistic effects with other stressors play an important role for the establishment and spread of marine aliens species. Knowledge of socio-economic impacts of invasive seaweeds is poor. Olden et al. Olden and Poff 2004. 2000. has increased over the last 20 2 National Center for Marine and Coastal Conservation. ecological impacts. both for ecological effects and for associated economic costs (Parker et al. Australian Maritime College. 1999. PMB 3. 2004. Perrings et al. The predominant impacts were changed competitive relationships in the recipient habitat. eradication and control programs. Hewitt2 Australian Institute of Marine Science. there are still very few rigorous studies of the impacts of aliens (Ruiz et al. This is in contrast to the perception that invading macroalgae have potentially serious impacts. the comb jelly wMnemiopsis leidyi (A. e-mail: b. or introduced species in general. Australia (Ross et al. Changes in biodiversity. There was no information about evolutionary effects or changes of ecosystem processes. eradication. The rate of marine introductions. Grosholz et al. the management of species incursions needs to remain focused on early detection. We collated costs associated with control/eradication activities and for national spending on marine biosecurity in Australia. In particular. Rosebud. a process by which ecosystems will become dominated by generalists and opportunistic species. DOI 10. 1999. This pattern has already been observed in some locations affected by environmental degradation and species’ invasions (McKinney and Lockwood 1999). An alternative view is that most marine alien species have negligible impacts on their recipient environment. Vitousek et al. Reise et al.E. effects on fish and invertebrate fauna. and. including introductions of seaweeds. Hewitt 2003a. Australia. however. Formal assessment frameworks for impacts of marine aliens. 2006) with current global estimates of introduced macroalgae ranging from 163 (Ribera Siguan 2002) to 260 species (J. and the predatory sea star Asterias amurensis (Lutken) in Tasmania and Victoria. Townsville MC QLD 4810. Keywords: control. or are merely an addition to the ecosystem (Farnham 1980. covered only a fraction of their introduced distribution and generally were conducted over short time scales. economic impacts. are scarce. However. Ruiz et al. Perrings et al.044 Review Impacts of introduced seaweeds Britta Schaffelke1. Until we are able to understand. global climate change and the introduction of alien marine species are identified stressors.g. Smith unpublished data). Victoria 3939. Grosholz 2002). Prevention of impacts is the driving force for costly surveillance. e. 1999. 1999). Pimentel et al. Carlton 2000). there are some well-known examples of catastrophic effects of marine alien invaders on recipient ecosystems. The threats posed are often inferred from estimates of introduction status and observations of negative impacts in other invaded areas. and habitat change were also identified. resultant space monopolization. The mechanisms underlying the manifestation of impacts are uncertain and inferences about common patterns were hampered because impact studies were available for only a few introduced seaweeds. especially in coastal regions (Norse 1993.2007. Australia 1 * Corresponding author Abstract We analyzed 69 publications on the impacts of introduced seaweeds.* and Chad L. Ecosystem alterations due to global change coupled with species introductions are thought to result in ‘‘biotic homogenization’’ (e. especially when aliens attain high abundances in a particular ecosystem. Occhipinti-Ambrogi and Savini 2003). New Zealand and the United States. Agassiz)x in the Black Sea (Kideys 2002). indicated by high abundances of invaders.g. The current knowledge of impacts of alien macroalgae is even sparser than for other taxonomic groups of aliens. because they may alter ecosystem structure and function by monopolizing space. ¨ 2003). for any negative impacts (Ruiz et al.1515/BOT. Ribera Siguan 2002. 2002. 1997.Botanica Marina 50 (2007): 397–417 2007 by Walter de Gruyter • Berlin • New York. Marine macroalgae (seaweeds) are a significant component of marine alien taxa (Schaffelke et al.

g. reports to government agencies. 1999. An additional 13 case studies reported effects of alien macroalgae on fish and invertebrate fauna in the recipient environment. Sargassum muticum (Yendo) Fensholt and Undaria pinnatifida (Harvey) Suringar. These existing studies of impact address only a small fraction (. Codium fragile (Suringar) Hariot ssp.. Some original publications cited elsewhere proved difficult to obtain (e. e.. The predominant effect of alien macroalgae reported in the case studies were changed competitive relationships in the recipient habitat (43 case studies.. herbivores. Hewitt 2003b). Trowbridge 1998. Six examples of toxic effects on other biota were reported for Caulerpa species. Boudouresque and Verlaque 2002. and they are also able to attain high . We categorize reported impacts and classify the quality of the information (e. changed structure. Caulerpa taxifolia (Vahl) C. for light or substratum) – Space monopolization – Change in community composition • Effects on higher trophic levels (e. Schaffelke et al. Levin et al. associated fauna. unpublished proceedings). Economic and societal impacts: • Direct – Costs of loss of ecosystem functions or values – Impacts on environmental amenity – Impacts on human health • Indirect – Management costs (government/non government) – Costs of research into introduced species – Costs for eradication and control measures – Costs for education/extension campaigns.. 2006x. sediment accumulation) • Change of ecosystem processes (e.g. were reported in nine case studies. Agardh. the occurrence of fertile hybrids between an alien and a native congener (Table 1). such as changes in productivity or habitat complexity (e. Ribera Siguan 2002. 2000). tomentosoides. These are cited as the original author(s’) based on the secondary source (e.g.g. Sargassum muticum and Codium fragile ssp. hybridization).. Documented impacts of seaweed invaders are known mostly from a few. unless they explicitly addressed interactions between the species.g.398 B. • Genetic effects – Within a species (e. We were unable to find quantitative information about evolutionary effects or about changes in ecosystem processes caused by seaweed introductions. For the purpose of this review we consider potential impacts into the following categories: Ecological and evolutionary impacts: • Direct and indirect competition with native biota (e. One case study reported a genetic effect. Schaffelke and C. resultant space monopolization and reduced abundances/biomass of native macroalgae or seagrasses. observational information..5%) of the current estimate of the total number of globally introduced macroalgal species (circa 260).. Table 1). seven case studies report such changes. Hewitt: Impacts of introduced seaweeds ing into ecosystem engineers.1980s to 2005) that present data on impacts of alien seaweeds. In this review we synthesize and analyze current knowledge of impacts of alien seaweeds using published sources. with most cases reporting decreases in the number and abundance of species (Table 1). These were generally indicated by high abundances of the alien species. introgression) – Between species (e. tomentosoides (Van Goor) Silva. Walker and Kendrick 1998. Wear and Gardner 1999.6. Parker ¨ et al.. to examine whether certain species are more likely to cause significant impacts than others.g. Three case studies found no significant impacts of the alien seaweed studied. alteration of trophic structure). 2002. Results reported in multiple publications but leading to the same conclusion with regard to impact were listed as one case study. reviews and publications offering only distributional or observational data were omitted..g. Wallentinus 2002. Our aim is to find patterns of impacts.. with all relevant references. data from manipulative field experiments). The majority of case studies focused on Caulerpa taxifolia. and to identify mechanisms contributing to the observed impacts. followed by Undaria pinnatifida. based on observations or assumptions. addition or loss of canopy species). well-studied. generally a decrease in richness of native macroalgal species in invaded areas compared to non-invaded areas. Impacts or risks of impacts have been variously categorized (e. Gollasch and Leppakoski 1999. Ecological impacts Methods We examined 69 publications (.g.g. w78x The 60 collated case studies report ecological impacts for only 17 species of introduced seaweeds (Table 1).. Ruiz et al. however. toxicity) • Habitat change (e. high profile species we. and altering foodwebs. Occhipinti-Ambrogi and Savini 2003. mainly. Ribera and Boudouresque 1995.L. These species are the geographically most widely distributed alien macroalgae..g. Changes in biodiversity.g.g. Studies that reported results from several alien species were listed as separate case studies for each species. While there are potentially other kinds of economic impacts (see list above). Less clear is the occurrence of habitat change.g. 1999. this was the only type of socio-economic impact for which there were sufficient quantitative data. Grosholz 2002. cited in Sinner et al.. coupled with significant environmental and economic consequences (Thresher 2000). Information about economic impacts was collated from quantitative assessments of cost or effort for control and eradication measures. Of particular concern is their potentially rapid spread beyond initial points of introduction through efficient dispersal.

removal) CC Italy (Med. Agardh Sur (comp) G Overgrowth increased shoot density of Cymodocea nodosa (Ucria) Ascherson and decreased shoot density of Zostera noltii Hornem. increasing total algal biomass Acanthophora spicifera O. amplified by nutrient enrichment. Method O. Hewitt: Impacts of introduced seaweeds 399 Negative effect on shoot density of Cymodocea nodosa. and longevity of leaves. Schaffelke and C. Australia May 1976 Caulerpa racemosa (Forsskal) ˚ J. Gepp et E. diversity and abundance of native macroalgae Piazzi et al. 2002 Bonnemaisonia hamifera Hariot O (Serial collections) E (removal) CC SM R Increase in abundance. Agardh. Sur. Hering G Increase in abundance since first record in 1920s to become dominant species in several locations in New South Wales. no influence of nutrients E (enrichment. 2002 R Competitively superior to native Laurencia nidifica J. Vahl) C. High abundance at some sites. mortality of sparse seagrass beds De Villele and Verlaque 1995 ` Caulerpa taxifolia G B. Gepp O. Sur CC USA (Hawaii) R Most common introduced seaweed in Hawaii. 2001a Caulerpa taxifolia (M. health of Posidonia oceanica (L. Sur SM USA (Atlantic coast) Gulf of Maine Australia (Pacific coast) Italy (Med. Agardh G Invaded areas: decrease in number. now common component of community (24% maximum cover) Harris and Tyrell 2001 Caulerpa filifomis (Suhr) K.S. Sur SM USA (Hawaii) Smith et al. Elba) R Co-occurrence in previously monospecific Halophila hawaiiana Doty et Stone meadows Smith et al. In long-term. Vahl) Børgesen O. common in intertidal and tide pools.L. Tuscany coast) CC Italy (Med. width. Elba) Ceccherelli and Cinelli 1997 Cecherelli and Sechi 2002 w79x . species co-exist.Table 1 Summary information of case studies of impacts of alien macroalgae.) Delile. in mixed meadows Ceccherelli and Campo 2002 Caulerpa racemosa Sur (comp) G Reduced species number. E SM HC USA (Hawaii) Russell 1992 Effect Location Reference Species Summary Acanthophora spicifera (M. After 3 years of competition. Tuscany coast) CC Italy (Med. displaces native macroalgae (but no data given) Avrainvillea amadelpha (Montagne) A.

Ligurian Sea) USA (Pacific coast. Fish density and biomass slightly lower in invaded sites Caulerpa taxifolia G Colour change of a number of fish species inhabiting C. 2002 Williams and Grosholz 2002 Tippets 2002 Merino et al. taxifolia meadows Caulerpa taxifolia G Biomass of Ruppia maritima L. C. 1996 Lemee et al. 1994 (in Boudouresque et al. 1995). mainly Polychaeta on C. ´ Pedrotti et al. sediment organics and pollution between the two areas) Caulerpa taxifolia G No evidence of decrease in Posidonia oceanica abundance. 1996. Caulerpa taxifolia G Caulerpenyne and C. 20x lower in invaded patches Caulerpa taxifolia G Reduced abundance of invertebrates compared to Zostera marina L. San Diego) USA (Pacific coast. 1997 ´ Lab Lab TO TO Boudouresque et al. taxifolia. Ligurian Sea) Jaubert et al. 1998a–c. 1999 Sur (comp) HT Francour et al. Ligurian Sea) Effect Location Reference Relini et al. taxifolia and seagrass patches well isolated. San Diego) Arigoni et al. Ligurian Sea) CC HT France (Med) Boudouresque et al. taxifolia extracts inhibit or delay the proliferation of phytoplankton strains Caulerpa taxifolia G Consumption by sea urchins results in impaired gonadal development and loss of spines Caulerpa taxifolia Caulerpenyne and C.L. Important economic fish species absent in C. 2000 Sur (comp) Sur (comp) CC France (Med. taxifolia compared to Cymodocea nodosa meadows species composition changed. indication of no significant competition 400 B. Schaffelke and C. Amade and Lemee 1998. Relini et al. Pesando et al. 1993. no change in fish feeding habits. ´ Pedrotti and Lemee 1999 ´ (Table 1 continued) Species Summary Caulerpa taxifolia G Higher density and diversity of invertebrate epifauna and fish in C. recruitment. 1995 Sur (comp) Sur (comp) Sur (comp) Lab CC HT TO HT France (Med. taxifolia extracts inhibit development of sea urchin eggs . Ligurian Sea) France (Med. 1992 Verlaque and Fritayre 1994 Sur – France (Med. 1997 also found large difference in water quality. 1996. taxifolia meadows Caulerpa taxifolia G Less biomass and diversity of native algal and invertebrate species Caulerpa taxifolia Diversity higher in non-invaded area (note: Chisholm et al. reproduction.w80x Method Sur (comp) HT HC Italy (Med. Hewitt: Impacts of introduced seaweeds Caulerpa taxifolia G No clear effect on composition and species richness of ichthyofauna. Lemee et al.

sea urchin larval and fish toxicity. racemosa inhibit membrane extrusion pump (protective mechanism against toxins) in mussel and sponge. mortality in molluscs fed with treated algae G Schroder et al. Ligurian Sea) Canada (Atlantic coast. tomentosoides G Levin et al. Tuscany coast) Piazzi et al. tomentosoides G Codium now dominant. Nova Scotia) CC HC HT USA (Atlantic coast. 1994 (in Boudouresque et al. more pronounced in C. Wollaston Sur (comp) O. 1999 Italy (Med.(Table 1 continued) Method Lab TO Dini et al. cover and diversity of native species lower in invaded areas. Tuscany coast. Balata et al. 2003. herbivory assays). 1996 Chapman et al. taxifolia extracts and caulerpin from C. making sponges less resistant to tributyl tin G Piazzi and Cinelli 2003 G R 50–100% cover of benthic macroalgae is introduced. racemosa patches. taxifolia areas G Paul and Fenical 1986 Caulerpa taxifolia Caulerpa racemosa Lab TO G Laboratory testing of Caulerpenyne: antibacterial and antifungal properties. 1998 ¨ Caulerpa taxifolia Caulerpa racemosa Sur (comp) CC G C. establishment only after previous disturbance of canopy-forming kelps. compared to invaded controls. Schaffelke and C. establishment only after previous disturbance of canopy-forming kelps. Native algal abundance decreased.E. 2002 w81x Codium now dominant. setacea in C tax patches Italy (Med. harbor area) Caulerpa taxifolia Caulerpa racemosa Womersleyella setacea (Hollenberg) R. Norris Acrothamnion preissii (Sonder) E. 1995). Avoidance of treated feed pellets by fish. No turf in C. Less abundance of juvenile fish in invaded patches O. E (removal. 2004 Effect Location Reference Species Summary Caulerpa taxifolia Sur (comp) CC G Caulerpenyne changes behavior of marine ciliate possibly causing mortality G Caulerpa taxifolia Caulerpa racemosa Lab TO G Reduced cover and number of native species colonized by one or both Caulerpa species. Ricci et al.M. More Womersleyella in C. Gulf of Maine) Bellan-Santini et al. some W.L. racemosa patches. Sur . then preventing recruitment of native kelps. Hewitt: Impacts of introduced seaweeds 401 Codium fragile ssp. then preventing recruitment of native kelps. Native algal abundance decreased B. 2002 Codium fragile ssp. Sur HT CC HC R Caulerpa taxifolia G Richness and species number of invertebrates (mainly amphipods) slightly reduced in invaded areas France (Med.

dominant species at some sites Heterosiphonia japonica Yendo R Most common species in sheltered and semiexposed subtidal (6 to )12 m). serratus L. but high annual variation Codium fragile ssp.Y. Sur SM USA (Hawaii) Smith et al. spicifera leading to higher total algal biomass on some reefs Hypnea musciformis R Epiphyte on other macroalgal species. no gonadal development on Codium diet Fucus evanescens C.V. overgrowing benthos such as rhodoliths Hypnea musciformis (Wulfen) J. No competition with native seaweeds. 2004 O. Schaffelke and C. tomentosoides G Shift in abundance over 25 years from kelpdominated to Codium and introduced red algae-dominated plus native opportunistic species wDesmarestia aculeata (Linnaeus) J. 2004. ¨ Wikstrom et al. Sur CC HC USA (Atlantic coast. 2006 ¨ O. 2002. Gulf of Maine) Harris and Tyrell 2001 Effect Location Reference Lab HT Scheibling and Anthony 2001 Lab G Sweden (Baltic Sea) Sweden (Baltic Sea) Coyer et al. different epifauna composition and lower abundance of amphipods compared to native species 402 B. Dawson R Increase in distribution. 2002 O. Agardh B Fertile hybrids with F. Sur SM USA (Hawaii) Smith et al. (as Eucheuma striatum F. Conklin and Smith 2005 (Table 1 continued) Species Summary Codium fragile ssp.L. dominant species at some sites. Lab SM USA (Hawaii) Smith et al. dense mats attached to reef substrata . higher total algal biomass at some sites Kappaphycus species R Dominant at some sites. Lamourouxx. Lamouroux R Often epiphytic on introduced Acanthophora spicifera. Hewitt: Impacts of introduced seaweeds Gracilaria salicornia (C. Schmitz) R Higher invertebrate diversity compared to noninvaded reef site. Smith et al. Sur SM HT HC USA (Hawaii) Russell 1983 O. tomentosoides G Not preferred by sea urchins. Conklin and Smith 2005 Norway (North Sea coast) SM HC USA (Hawaii) Husa et al.V. Sur SM O. together with A. 2002. Fucus evanescens B Lower biomass and fewer species of epiphytes and grazers. 2002 Sur (comp) CC HT Wikstrom and Kautsky 2004. forms large monospecific blooms at some sites and/or grows intermingled with dense Ulva fasciata Delile Kappaphycus spp. observation of coral mortality after smothering. Sur Russell 1992 O. Agardh) E.w82x Method O. Sur.

H. decrease of Laminaria digitata (Hudson) J.V. Bailey) M. Gulf of Maine) Harris and Tyrell 2001 HT USA (Hawaii) Woo 2000 cited in Conklin and Smith 2005 Effect Location Reference Species Summary Kappaphycus species R Overgrowth of reef-building corals.) J.V. Sur O. Lamouroux and Fucus vesiculosus L. Bailey) O. Stæhr et al. Sur CC France (Atlantic coast) E (removal) SM USA (Pacific coast) Curiel et al. Fewer sea urchins at invaded sites Britton-Simmons 2004 Sargassum muticum B High abundance in tidepools caused decreased abundance of leathery and foliose macroalgae Viejo 1997 De Wreede 1983 Sargassum muticum O.) C. muticum stands Sargassum muticum E (removal). cleared areas. Agardh dieback. Agardh Sargassum muticum B Most abundant species in lower indertidal and subtidal. Adriatic Sea.(Table 1 continued) Method O. 1998 R 100% cover in one location Sargassum muticum (Yendo) Fensholt Sur CC B Decreased cover and native algal species number under S. Guiry et G. marina den Hartog 1997 Sargassum muticum B Ambrose and Nelson 1982 B.-G. Choi. seasonal S. Sur (comp) CC Italy (Med. Lamouroux abundance Cosson 1999 Sargassum muticum B Colonization of areas previously colonized by Zostera marina. muticum canopy at high density during peak of M. Lab E E (removal) CC CC HT B Canopy reduced cover of native species. Kim. Sur SM USA (Atlantic coast. Saunders (as Polysiphonia harveyi J. esp.W. no re-colonization by Z. Laminaria saccharina (L. inhibiting re-colonization . Hewitt: Impacts of introduced seaweeds 403 w83x Recruitment after Macrocystis pyrifera (L. Schaffelke and C. pyrifera recruitment.-S. Venice) Denmark (Limfjord) USA (Pacific coast) Spain (Atlantic coast) CC Canada (Pacific coast) CC France (Atlantic coast) O. Sur B Sargassum rapidly colonized exp. canopy then decreased recruitment of Rhodomela larix (Turner) C. leading to partial mortality Neosiphonia harveyi J. 2000 Sargassum muticum B Increased abundance of native kelp and understorey species after experimental removal of canopy.L.

Sur SM Curiel et al. (cited in Sinner et al. competition with Sargassum muticum assumed R Womersleyella setacea Acrothamnion preissii R Reduced functional diversity of seagrass rhizome epiphytes at sites invaded by turf species compared to unaffected sites . pinnatifida after experimental reduction of native canopy. echinoderms). but with changed native community composition Undaria pinnatifida B Establishment of U. recovery to near control-level after 1 year B Undaria pinnatifida Sargassum muticum B Dominant component in Venice lagoon. accumulation of fine sediment. Sur (comp) E (removal) E (removal) CC CC CC Italy (Med. Venice) Argentina (Patagonia) Australia (Tasmanian east coast) Australia (Tasmanian east coast) SM Australia (Tasmanian east coast) O. 2001 Italy (Med. 1998 Casas et al. low cover of Corallina and turfs. Italy. molluscs. 2004 Curiel et al. Agardh ` Undaria pinnatifida B High density of U. Piazzi et al. 2002 (Table 1 continued) Species Summary Undaria pinnatifida (Harvey) Suringar B No detectable effect on native algal assemblage over 3 years Undaria pinnatifida B No detectable effect on native algal assemblage Undaria pinnatifida B Wellington Harbour: U. Queen Charlotte Sound: increase in subcanopy species diversity (algae. pinnatifida cover 404 B. pinnatifida after experimental removal of native canopy. 1998 O. pinnatifida at high abundance after dieback of canopy-forming Phyllospora comosa (Labillardiere) C. pinnatifida subcanopy invertebrate assemblages different. recovery after 2 years. many ascidians. Adriatic Sea. 2004 Valentine and Johnson 2003 Sur (comp) SM Valentine and Johnson 2004 E (removal) Edgar et al. possibly because of increased habitat complexity Undaria pinnatifida B Decreased cover of understorey species under 100% U. 2000) Battershill et al. Adriatic Sea.L. Spain (several sites in W-Med) Piazzi and Cinelli 2000. Sur (comp) CC HT New Zealand – New Zealand Wear and Gardner 1999. Venice) Sur CC HC France. polychaetes and hydroids. Schaffelke and C.w84x Method Sur (BACI) – New Zealand Forrest and Taylor 2002 Effect Location Reference Sur (BACI) O. Hewitt: Impacts of introduced seaweeds Undaria pinnatifida B Decreased species richness and diversity of native seaweeds Undaria pinnatifida B High density of U.

in the Mediterranean Sea. New Zealand*). New South Wales. subcategories: space monopolization (SM). The Netherlands. S. the underlying mechanisms of the ecological impacts of these four species are discussed in detail below (also refer to Table 1). especially in sparse meadows (De Villele and Verlaque 1995). introduced to the: Mediterranean Sea (France. Tunisia). taxifolia. NE Atlantic Ocean (Belgium. Sweden). pinnatifida introduced to the: Mediterranean Sea (France. Portugal: Azores. Gsgenetic effects. In contrast. especially under nutrient enrichment (Ceccherelli and Cinelli 1997). SW Pacific Ocean (Australia: Tasmania. Sweden). N Ireland. fragile ssp. e. Maryland. 1995. Posidonia oceanica. tomentosoides. Norway.L. New Zealand). Caulerpa taxifolia A large research effort has addressed the ecological impacts of Caulerpa taxifolia in the Mediterranean Sea. France*. Australasia (Australia: Tasmania*. The presence of C.B. Italy*). taxifolia. field survey with temporal comparisons before/after invasion wSur (BACI)x. Spain. France. N Ireland. NE Pacific Ocean (USA: California and Oregon). Denmark*. NE Pacific Ocean (Canada: British Columbia*. Spain*. is negatively affected by competition with C. Rsred algae (Rhodophyta). introduced to the: Mediterranean Sea (Croatia. field experiment (E). France. Bsbrown algae (Phaeophyceae). Germany. Great Britain: England. or become the dominant benthic species in some locations. Ireland. Netherlands. Spain). laboratory experiment or assay (Lab). Scotland. SW Pacific Ocean (Australia: South Australia. Portugal. Rhode Island). taxifolia colonization and growth by providing physical w85x Airoldi et al. It is important to note that case studies of impacts of the above species are available only for small portions of the geographical ranges that have been invaded (see countries or regions marked by an asterisk in the following list): C. where known. England. NE Atlantic Ocean (Belgium. Victoria. Impact categories: competition with native biota. North Carolina. NW Pacific Ocean (Japan – failed introduction). Airoldi 1998 Italy (Med. oceanica facilitates C. introduced to the: Mediterranean Sea (France). HTseffects on higher trophic levels (HT). Italy*). New South Wales). Great Britain: England. whereas long-term experiments suggested that the two species are likely to coexist and that high nutrient availability will not change competitive relations (Ceccherelli and Sechi 2002). Ligurian Sea) SM Dominant species Sur Reference Effect Location Summary Method Sur (comp) Womersleyella setacea Acrothamnion preissii R R (Table 1 continued) Womersleyella setacea Species R SM CC Italy (Med. change in community composition (CC). New York. Maine*.B. NW Atlantic Ocean (Canada: Nova Scotia* and Prince Edward Island.: While the number of alien seaweed species is higher in other areas. S Atlantic (Argentina*). leading to decreased productivity and shoot mortality. Gsgreen algae (Chlorophyta). The Netherlands. We briefly discuss case studies of red algal introductions to the Hawaiian Islands. Denmark. field survey comparing invaded and non-invaded sites wSur (comp)x. no significant impact shown (–).. Italy*. USA: Washington and Oregon*: Mexico: Baja California. U. C. MedsMediterranean Sea. habitat change (HC). a small but well-studied area with a relatively high number of abundant alien seaweeds (N. taxifolia had a negative effect on shoot density of the seagrass Cymodocea nodosa in short-term studies. Hewitt: Impacts of introduced seaweeds 405 Methods: field survey (Sur). observational study (O).g. Massachusetts. Victoria. Monaco. Tuscany coast) Piazzi and Cinelli 2001 . Species co-occur and compete with one another. the proportion subjected to impact-related studies is relatively higher for Hawaii). USA: Connecticut. P. Mexico: Baja California). Schaffelke and C. the dominant seagrass in the Mediterranean Sea. Spain. France*. subcategory toxicity (TO). NE Pacific Ocean (USA: California. The nature and. NE Atlantic Ocean (Belgium. muticum. Ireland. Wales. overall space monopolization is independent of the respective dominant species abundances. NE Pacific Ocean (USA: California*). Germany. Norway. Scotland.

Edgar et al. At low grazing pressure. 1999). Critchley et al. 1998. recently proposed as C. pinnatifida is facilitated by increased substratum availability created by disturbance (Valentine and Johnson 2003. Since the early 1990s. usually evident as reduced cover and richness of native seaweeds and marine plants. see also Valentine et al. Information about impacts in the southern states of Australia is at present primarily anecdotal (Glasby et al. Forrest and Taylor 2002. Reduced abundances and sometimes reduced richness of native seaweeds have been found in invaded areas (Viejo 1997. racemosa var. However. pinnatifida abundance but not enough to prevent canopy establishment (Valentine and Johnson 2005a). Curiel et al. taxifolia.L. pinnatifida have been removed by manual clearing (Valentine and Johnson 2003. 1998a–c. 2003). 2004). Bellan-Santini et al. Manipulative field experiments demonstrate that the establishment of U. 2007). rather than shade (Ceccherelli and Cinelli 1998. Sea urchin grazing can significantly reduce U. De Wreede 1983) and eelgrass (den Hartog 1997). 1998. 2005). taxifolia typically show reduced biomass and diversity of native macroalgae and invertebrates and low fish abundance (Boudouresque et al. 2000. The distribution and abundance of P. . other studies have detected either no significant differences in diversity or cover of native macroalgal assemblages in invaded versus non-invaded areas (Wear and Gardner 1999. 1992. 2000). cit. taxifolia (Williams and Grosholz 2002). In summary. nodosa and Zostera noltii decreased shoot density of the former species but increased density of the latter (Ceccherelli and Campo 2002). taxifolia had negative effects on sea urchin larvae and protists in the laboratory (Table 1). In Italy. Italy. muticum. taxifolia (Piazzi et al. Toxic secondary metabolites of C. indirectly supporting the persistence of the introduced seaweed. racemosa var. Francour et al. Forrest and Taylor 2002) or. but whether similar effects manifest in the field is unknown. Sinner et al. racemosa var. 2004). 2000. racemosa var. cit. biomass of the seagrass Ruppia maritima was 20 times lower in meadow patches colonized by C. 1995. The introduced turf assemblages also promote growth and spread of introduced Caulerpa. The reduced abundance of native seaweeds has lead to decreased abundance of the sea urchin Strongylocentrotus droebachiensis (op. overgrowth by C. Where they co-occur. Native species abundance and diversity are lower than in uninvaded areas (op. whereas areas with a higher complexity and species diversity were less conducive (Ceccherelli et al. however. Britton-Simmons 2004). 2001b. Curiel et al. depending on habitat. the two introduced Caulerpa species also interact with two introduced turf-forming red algae. not changed in the Bay of Menton (French Mediterranean Sea) over 7 years since C. In contrast. Schaffelke and C.). On the Tuscan coast. C. a second Caulerpa species has been spreading in the Mediterranean Sea. Stæhr et al. Impacts of introduced Caulerpa taxifolia in other parts of the world are scarcely known.b. 1998. and sometimes the diversity of understorey species (Battershill et al. muticum is the most likely factor preventing re-growth of native species (Britton-Simmons 2004). oceanica-dominated areas seem well separated. 1987). introduced Caulerpa species have monopolized benthos in some areas of the Mediterranean Sea. However. Re-establishment of native assemblages after 1 to 2 years has been observed where high abundances of U. it forms predominantly seasonal canopies that act to decrease cover. The four species form a mosaic of largely introduced assemblages. with different species dominating.). oceanica has. Verlaque and Fritayre 1994. 2004). U. cylindracea reduced diversity and abundance of native macroalgae. Edgar et al. with C. taxifolia patches than in Zostera marina meadows (Tippets 2002). C. This species was also recently recorded as introduced in a water body in South Australia (Collings et al. Piazzi and Ceccherelli 2002). 2001a). albeit without supporting data (Fletcher and Fletcher 1975). cylindracea having the most pronounced effect (Balata et al. taxifolia was introduced. 1999). albeit with changed species composition (Valentine and Johnson 2003). The seasonal canopy of S. 2002). 2005). 2004). Hewitt et al. and through increased competition have caused significant changes to community composition. Underwater light measurements support the notion that shading by S. Hewitt: Impacts of introduced seaweeds protection. 2004. Recruitment and establishment of this species is often facilitated by disturbance creating available substratum (Ambrose and Nelson 1982. Casas et al. Sites on the French Mediterranean coast colonized by C. and in mixed meadows of C. implying minimal competition at larger geographic scales (Jaubert et al. Italian studies (only about 50 km from the French study sites) report higher biomass and diversity of invertebrates and fish in C. muticum then prevents re-establishment of native macroalgae (Ambrose and Nelson 1982. cited in Sinner et al. pinnatifida persists while native canopy-forming seaweeds recover poorly. Valentine and Johnson 2004). Deysher and Norton 1982. cylindracea has higher growth rates and is competitively superior to C. U.406 B. an increase in subcanopy species diversity (Battershill et al. Colonization by either species reduced diversity and abundance of native macroalgae compared with uninvaded areas. which avoids consumption of S. pinnatifida seems not to inhibit recruitment of native understorey species (Valentine and Johnson 2005a. taxifolia meadows (presumably as a result of increased habitat complexity). 1998). cylindracea (Verlaque et al. especially turf and encrusting species (Piazzi et al.and P. Undaria pinnatifida Undaria pinnatifida populations dominate space in many regions where the species has been introduced (e. the species was reported to have profoundly altered the coastal ecology. 1996).g. Sargassum muticum Shortly after the discovery of Sargassum muticum on the south coast of England. but a significant lack of some important economic species that require open sand habitats (Relini et al. Once established. In California. 2000. and abundance of invertebrates was w86x lower in C. Womersleyella setacea and Acrothamnion preissii (Piazzi and Cinelli 2003). due to build-up of sediment in areas where native canopy-forming species are lost. more rarely..

taxifolia in California included immediately available emergency funds (the incursion was considered an environmental emergency similar to an oil spill) to commence the eradication and substantial funds for ongoing monitoring.) Le Jolis in California (Table 2). However. (2004) for Ascophyllum nodosum (L. Kaneohe Bay. Several red algal species (Acanthophora spicifera.L. natural sea urchin/kelp dynamics are disrupted by the spread of the introduced bryozoan Membranipora membranacea (Linnaeus). detailed breakdowns of costs are reported in three recent studies: Anderson (2005) for Caulerpa taxifolia in California. the number of which is possibly further reduced by decreased kelp abundance (op. control and eradication efforts (Table 2). However. Chapman et al. all paid by the vessel’s insurer (Wotton et al. 2002). tomentosoides (Harris and Tyrell 2001. Mayes.) have established at high abundances and are spreading on Hawaiian coral reefs (Smith et al. for Codium fragile ssp. In both cases. Alien and native bloom-forming macroalgal species now form a mosaic with overall high total algal cover sustained by low and spatially variable grazing rates (Stimson et al.5 million for the containment of C. 2002. tomentosoides in the NW Atlantic Ocean have been facilitated by interactions with other introduced species. Economic impacts Information about economic impacts of alien seaweeds is generally rare. research and public awareness (Anderson 2005. tomentosoides does not occur in the NE Atlantic Ocean. While changes in abundance are likely to occur over decades. pinnatifida from a sunken trawler in New Zealand were for (failed) salvage attempts (85% of total costs).. cited in Conklin and Smith 2005). Ecological impacts of established C. Levin et al. Quantitative assessments of their ecological impacts and competitive relationships between each other and with native benthos are. Chapman et al.US$ 55. only consume C. local authorities. defoliation and gap formation in New England and Nova Scotian Saccharina latissima (L. Trowbridge (1998. (2004) for Undaria pinnatifida in the Chatham Islands. fragile ssp.x beds (Harris and Tyrell 2001. These species monopolize space and increase overall macroalgal productivity and biomass on coral reefs (Table 1).g.g. Avrainvillea amadelpha. The total sum of )US$ 7. The introduced seaweeds exacerbate the problem of persistent macroalgal blooms in some locations. scientists and other stakeholders. 2002). and Eucheuma spp. (2000. tomentosoides in the NE Atlantic Ocean ever attained higher abundances in the past. are collated in Ribera and Boudouresque (1995). The introductions to the NE Atlantic Ocean occurred more than 30 years earlier than those in the NW Atlantic Ocean (reviewed in Chapman 1999). Levin et al. Space monopolization by C. cit. C. The costs of the successful eradication of U. so direct comparisons are potentially problematic. Periodic overgrazing by sea urchins (Johnson and Mann 1988) provided a disturbance to native seaweeds enabling establishment of C. Direct impacts of marine macroalgae are largely unquantified. 2002)..000 year-1 (Van Beukering and Cesar 2004). Schaffelke and C. fragile ssp. fragile ssp. tomentosoides when no other seaweeds are available (Sumi and Scheibling 2005) and have impaired gonad development on a diet of only this species (Scheibling and Anthony 2001). and Miller et al. Hawaiian macroalgal invasions At least 21 seaweed species have been introduced to the Hawaiian Islands. in situ treatment of gametophytes and small-sized sporophytes on the ship’s hull (13%) and regular monitoring of the ship’s hull and adjacent shoreline (2%).) Lam. Costs differ widely between reports (Table 2). Levin et al. New Zealand. Zucarello personal communication). 2002). indeed the paucity of estimates of economic values in the marine sector in general has been identified as a significant gap (Colgan 2004). there were unquantified costs for involvement of government agencies. but in most instances it is not obvious how estimates were calculated. both accidentally and intentionally for seaweed aquaculture (Godwin 2001. Impacts on amenity and recreational value can be expected in situations where high abundances of introduced seaweed occur. see also Anderson 2007 for further details on the eradication process). G. 2002. summarizing effects on fisheries and aquaculture due to fouling of nets. fragile ssp. Kappaphycus spp. e.). unlike impacts of macrophytes in freshwater systems. 2001) and supported by sediment nutrient levels that remain elevated (Stimson and Larned 2000). Druehl et Saunders was Laminaria saccharina (L. Wotton et al. there is unfortunately no information as to whether C. tomentosoides Establishment and impacts of Codium fragile ssp. Hypnea musciformis. tomentosoides) and Sinner et al. Removal of beach wrack derived from Hypnea musciformis blooms in a coastal town in Hawaii costs . for Undaria pinnatifida). not available. One component of the economic impacts of invasive seaweeds is the cost of rapid response. e. fragile ssp. but there are no quantitative data. Cases of observed or anecdotal reports of economic impacts. w87x . Gracilaria salicornia. Sea urchins (Strongylocentrotus droebachiensis) prefer kelp as a food source. Hewitt: Impacts of introduced seaweeds 407 Codium fragile ssp.) Lane. ropes.B. 2004). tomentosoides recruits into these gaps and persists by inhibiting recruitment of kelp zoospores. 2002. tomentosoides in this manner has resulted in reduced abundance of native macroalgae and of juvenile fish (Harris and Tyrell 2001. floats and other maritime equipment. tomentosoides in other parts of the introduced range have not been studied. more importantly. The authors also predict a significant longterm economic benefit to the local economy via improved real estate values were the algal blooms controlled. Conklin and Smith 2005. which overgrows kelp blades and leads to reduced growth. fragile ssp. fragile ssp. and Chapman (1999) suggested that high native floral diversity and grazing pressure prevent high abundances of C. which began in the 1960s with the establishment of high abundances of the native Dictyosphaeria cavernosa (Forsskal) Børgesen after disturbance and chronic nutri˚ ent enrichment (Smith et al. tomentosoides in this region. 1981). Smith et al. however. Space monopolization by C. fragile ssp. Overgrowth of reef-building corals has been observed (Woo 2000.

the government agreed to a significant investment in enhanced marine biosecurity delivery in the 2004/05 budget. As a consequence. DAFF) and Natural Heritage Trust funding (shared between DAFF and the Department of Environmental Heritage). In the United States. The New Zealand public good science funding agency. Where no monetary value was available.NZ$ 6.g. Conversion factors used: *1 AU$s0.3 million year-1 s .000 year-1 . by reduction of nutrient inputs.AU$ 2. at dive sites that were previously attractions because of their high benthic diversity. the establishment of a National System for the Management of Marine Pests is estimated to cost AU$ 7 million over the three-year period 2004–2007 (. this underestimates total marine biosecurity expenditure of FRST. 1986 Hurley 1981 cited in Critchley et al. Hewitt personal communication). Estimates are generally unavailable for the indirect costs of invasive or potentially invasive seaweeds. representing . Maui.8 million year-1). Australia. 2004 Reference Miller et al. containment and ongoing monitoring of incursion in California. given significant overlaps in research focused on biodiversity and biosecurity. We were unable to find other estimates of revenue loss caused by incursions of invasive seaweeds. Forestry and Fisheries.38 US$ t-1 (wet weight) )US$ 1. Hewitt personal communication).US$ 1. N.L. In Australia. the Foundation for Research. Removal of biomass from beaches Removal from coral reefs in Hawaii Manual removal by volunteers (group size unknown) Estimated costs for mechanized removal (only applied at experimental scale) Successful eradication from a sunken vessel at the Chatham Islands.L. 1986 Wotton et al.US$ 4. except in cases where there is a direct response to a particular invasion.000 over 3 years (5 person day 800 m-2 month-1) Hewitt et al.6 million over 5 year US$ 5–23 m-2 US$ 46 million US$ 4 million over 3 years US$ 55.408 B. Sargassum muticum Sargassum muticum** Undaria pinnatifida*** South Australia.US$ 0. Parker personal communication). This total is derived from a combination of appropriation funds within the Commonwealth Government (Department of Agriculture. e. Science and Technology (FRST).9 million year-1 (. ***1 NZ$s0.8 million year-1) towards marine biosecurity research (C. National Sea Grant allocates an estimated US$ 2. Hewitt: Impacts of introduced seaweeds Table 2 Economic costs associated with eradication and control efforts for invasive seaweeds.76 US$.8 km-2) in the State Caulerpa taxifolia* Hypnea musciformis Kappaphycus spp. application of sea salt Estimated cost to treat all colonized areas (. as may arise.88 US$.4% of total biosecurity expenditure (Hewitt and Bauckham . Species Ascophyllum nodosum Caulerpa taxifolia Caulerpa taxifolia* Summary Eradication by manual removal from small incursion area (total of 174 thalli) Rapid response.2 person h m-2 10–70 kg wet weight trip-1 . New Zealand has also recently adopted a Biosecurity Strategy (Biosecurity Council 2003) in which Marine Biosecurity was identified as a priority. an estimate of effort is given.L.9 million Neverauskas pers.2 million year-1 (.. comm. Van Beukering and Cesar 2004 Conklin and Smith 2005 Critchley et al. freshwater treatment Kihei coast. has explicitly allocated NZ$ 1. 2005 Undaria pinnatifida* )US$ 23. Hawaii. or by impacting recreational boating or fishing activities (Critchley 1983). leading to an increase in marine biosecurity expenditure of almost 300% to .9 million year-1. 2004 Anderson 2005 Glasby et al. **1 GB£s1.66 US$. w88x Costs of management activities are usually not separated by taxonomic group. USA (2000–2005) New South Wales. Schaffelke and C.4 million year-1 towards research and outreach associated with marine invasions (C. However. New Zealand (heat treatment and monitoring) Manual removal at experimental scale Cost/effort US$ 4680 US$ 7. 2005 Original figures were converted to US$ using exchange rates on 10/09/2006. These include associated costs of research and education/ extension activities.

Dunstan and Johnson 2007. structures providing artificial substrata and altered temperature regime due to effluents) often leads to higher incidence and abundance of invaders (reviewed in Carlton 1996. whereas uninvaded sites or sites with low invader abundance are less polluted (Chisholm et al. Caulerpa taxifolia. Anthropogenic disturbance leading to changes in resource availability (e. Gollasch and Leppakoski 1999). US Fish and Wildlife Service. and the establishment of invasive species and their proliferation to high abundances with associated impacts (Davis et al. and changing competitive relationships in the native assemblage. Avoidance by herbivores may be an important mechanism that causes shifts in community composition. However. Discussion Our review of available published literature showed that quantitative assessments of ecological and economic impacts of invasive seaweeds are still scarce. even in the absence of the original disturbance (Valentine et al. resources which C. high nutrient availability. although ¨ this view has been challenged recently (discussed in Dunstan and Johnson 2007). The data are urgently required to adequately inform and guide the management of invasive or potentially invasive species. Hewitt et al. Impacts of alien species cannot be viewed in isolation from the preceding stages in the invasion process. C. In the majority of reported cases. because the factors determining success of establishment and further spread may be site. Recipient habitats with low cover and diversity of native species (either chronically or after acute disturbance) often have a higher incidences and abundances of alien species (e.g.g. Lemee ´ w89x . 2007). Hewitt: Impacts of introduced seaweeds 409 2004. tomentosoides in Australia are generally found in engineered environments. high fecundity). 2000. Table 1). Schaffelke personal observations). ¨ Undaria pinnatifida often forms dense stands on artificial substrata (e. e. for both marine and terrestrial ecosystems. high growth rates. which may be due to impacts of the invader or the pollution. 2004b). and individual State natural resource management agencies. Control of introduced macroalgal biomass by herbivory is often ineffective.or time-specific (Grosholz 1996). taxifolia can utilize.g. A good example of this is the significant impact of introduced Codium fragile ssp. low diversity algal turf assemblages and seagrass meadows promoted the establishment of high abundances of introduced Caulerpa species in the Mediterranean Sea (Cecherelli and Cinelli 1998. or both. These preceding stages and the manifestation of impacts through high abundances and space monopolization reflect characteristics of i) the recipient environment (e.g. 1996. Influence of the recipient environment The analysis of the invasion history of a species is often used to predict whether that species would become invasive elsewhere. Ceccherelli et al. Highly abundant Caulerpa taxifolia has been found on sediments enriched with nutrients and organic matter from urban wastewater. Schaffelke and C. Branch and Steffani 2004). 1997). The less polluted sites also have higher cover of native macrophytes. resource availability.. tomentosoides on western Atlantic coasts. 2000.. Extensive blooms of other introduced Caulerpa species have also been linked to local nutrient enrichment by sewage inputs. Ruiz et al. compared to the relatively benign effect of this species on benthic communities in the east Atlantic Ocean (see above. bund walls and riprap (B. either because invasive seaweeds are not preferred by native grazers (examples in Table 1. the mechanisms causing these community changes are mostly unknown (but see Valentine et al. Gollasch and Leppakoski 1999). Valentine et al. While this is proportionally much less than the economic contribution of primary marine industries to New Zealand’s GDP. impacts observed in one location often do not predict the effects in another location.. Hayes and Sliwa 2003. Parker et al.. 2002) has not yet been demonstrated for introduced seaweeds. 2003 for discussion of this issue for better-studied higher plant introductions). There are indications for a relationship between disturbance. Gurevitch and Padilla 2004). it is a large improvement over previous investment. US Geological Survey. parvifolia Harvey. 2007). which may lead to resource variability in the recipient habitat..g.g. although biogeographic limits of many macroalgae are known to be temperature-controlled (Breeman 1988). brachypus var. recently discovered in Florida. ollivierii Dostal in the ´ Bahamas (Lapointe et al. 1996) and abundant populations of C. However. Closer examination of these two factors and of interactions between invaders may suggest the underlying mechanisms for the observed community changes. The lack of these data. positive feedback mechanisms can enable invasive seaweeds to persist and flourish. Nevertheless. Williamson 1999. 1999...g. Boudouresque et al. The management of marine introduced species in the United States is vested within a large number of Federal and State agencies including the US Coast Guard. Once established. The mechanisms underlying impacts of alien seaweeds are uncertain (see Levine et al. wharfs. 2007 and Dunstan and Johnson 2007). Biological interactions also play a major role in controlling high abundances and space monopolization. 2002) and proliferation of several invading seaweed species is facilitated by reduced native macroalgal cover (see Table 1. 2007). We were unable to find any quantitative information about societal impacts of seaweed invasions. For example. Identifying all expenditure on managing marine introductions is beyond the scope of this review. namely successful establishment and spread (for further discussion see Valentine et al. is generally bemoaned in the invasion biology literature (e. 1999. and C. impacts are typically expressed as community dominance of the invader through monopolization of space. e. water and sediment pollution.. and hence likely to cause negative impacts (Lodge 1993. MacDougall and Turkington 2005. 2005a. jetties.B.L. marinas. Valentine et al. disturbance. Facilitation of introductions by climate change (Stachowicz et al. competition and community composition) and ii) the invader (e. fragile ssp. Floc’h et al. 2007).b). and. Mack et al.g.

Davis and Pelsor 2001. undisturbed. and in California by the disturbance of native eelgrass beds by the mussel Musculista senhousia (Benson) and the anemone Bunodeopsis sp. Schaffelke et al. 2000. Nyberg and Wallentinus (2005) compared species traits (relating to dispersal. will eventually replace C. In New Zealand. but see Lohrer and Whitlatch 2002). Undaria pinnatifida. Piazzi and Ceccherelli 2002). Scientists have tried to circumvent this dilemma through the experimental removal of established invading kelp for comparison with unmanipulated invaded control sites. 2007). Howe (currently accepted synonym: G. species most likely to be successful invaders. it is as yet unknown whether C. deemed unethical and in New Zealand it is illegal. The impact studies assessed here cover only a small part of the introduced distributional range for even the best-studied introduced seaweeds (see above). Results. (2003) suggest a weight-of-evidence approach to overcome the lack of pre-invasion data. . However. However.A. The manipulated sites are used to simulate species composition in communities that have not been invaded. tomentosoides. or whether the two species will facilitate one another. Trowbridge 1996. Edgar et al. as discussed above. In situ experimental introduction of species for impact studies is. and inferences about common patterns impossible. may be difficult to interpret because the experiment may reset the assemblage to an earlier successional stage.410 B. which is different from the initial. Asexual reproduction and fast growth also have the potential to enable alien seaweeds to quickly colonize available space. For example. 1995) or preferred by only a few grazers (C. tomentosoides. 2007). tomentosoides by the invasive bryozoan Membranipora membranacea. studies are only initiated after an incursion has already occurred and use comparisons of sites colonized and not colonized by alien species (see Table 1 for examples). Such an approach has not yet been applied to assess impacts of seaweed incursions. For example. where two introduced w90x Caulerpa species co-occur. and hence. Forrest and Taylor (2002) found no differences in native species richness and abundance due to the establishment of Undaria pinnatifida using a control-impact design. Williams 2002). In that analysis (op. Known impacts of other species are limited mostly to single studies at small geographic scales. taxifolia. Dunstan and Johnson 2007. Prince and LeBlanc 1992. and these differences may have resulted in the lack of the alien species establishment in uncolonized sites. 1998. ultimately leading to impacts. Gavio and Fredericq 2002). Re-establishment of native species is possible but full recovery may take several years (Valentine and Johnson 2003. taxifolia. Another example is the facilitation of space monopolization by Codium fragile ssp. however. detailed field observations and field surveys at various spatial scales in invaded and uninvaded areas. Interactions between invaders Multiple invasions into one location can synergistically disturb an ecosystem and facilitate the establishment of further alien species – a process that has been termed ‘‘invasional meltdown’’ (Simberloff and von Holle 1999. turuturu Yamada. shading by the canopy-forming Sargassum muticum was an important mechanism that reduced native biodiversity in invaded areas (Levin et al. A number of species’ traits known from well-studied invader seaweeds are likely to facilitate establishment of high abundances. tomentosoides. Indeed. 1996. traits observed in an invasive species are often also found in conspecifics or congenerics that are not known to be invasive (Paula and Eston 1987. Fucus evanescens. Codium fragile ssp. In the Mediterranean Sea. Undaria pinnatifida. Schaffelke and C. and significant differences in community composition could thus be the result of confounding artifacts. species’ traits alone are unlikely to help predict the likelihood and impacts of invasions (Valentine et al. Examples for facilitation of establishment and growth of one alien seaweed by another is the promotion of Caulerpa taxifolia in the Mediterranean Sea by invasive red turf algae (Ceccherelli et al. 2002). Role of species’ functional traits Functional traits may influence whether some species are more likely to cause significant ecological or economic impacts. and on sufficient inoculation pressure (Davis et al.L. Francour et al. 2004). cit. typically. racemosa. 1995). U. Trowbridge 1995. Ross et al. making comparisons difficult. However. The outcome of either scenario could be more serious ecological impacts than presently observed. establishment and impact) between European alien and native species. pinnatifida significantly limited their ability to draw inferences. Asparagopsis armata Harvey and Grateloupia doryphora (Montagne) M.). likely to have significant negative impacts were Codium fragile ssp. and so it is illegal to disseminate or transport this species. Hewitt: Impacts of introduced seaweeds et al. which is competitively superior (Piazzi et al. Caulerpa taxifolia.. Valentine et al. both of which are alien (Reusch and Williams 1998. 2001a. Uncolonized sites may be inherently different from colonized sites. Typically. Vroom and Smith 2001). Thornber et al. they suggest that the lack of benthic community data before establishment of U. pinnatifida is classified as an ‘‘unwanted organism’’ under the Biosecurity Act of 1993. 2004) and may be impaired by the lack of native species in the immediate vicinity to provide for sufficient recruitment of spores. 1999. community (Valentine and Johnson 2003). Establishment of high abundances more likely depends on characteristics of the recipient environment that result in traits of aliens being advantageous for recruitment and growth. Limited inference space Evidence of impacts of alien marine species is often hampered by the lack of suitable baseline data prior to invasion. Traits relevant to the manifestation of impacts were size (most invasive green and brown macroalgae were larger than their native counterparts) and growth strategies (invasive species more often form dense covers and inhabit a larger depth range than native species). fragile ssp. in some instances no change of herbivores’ feeding habits was observed (C. 2002). and assessed impacts of a predatory seastar using information from small-scale experimental manipulations.

There is also some dispute about how much area of the Mediterranean Sea is colonized by C. for detailed information about intentional seaweed introductions). Hewitt 2002. Long-term monitoring of Caulerpa taxifolia in the Mediterranean Sea (Meinesz et al. Maggs and Stegenga 1999). Other costs (e. McIvor et al. Even though rhodophytes are the most prevalent group of alien macroalgae (Ribera Siguan 2003). taxifolia is not slowing down. i. Rhodophytes are often inconspicuous and difficult to identify to species level. however. The potential for harvest of commercially valuable seaweeds. and alleviating impacts (Stimson et al. However. Invasive Undaria pinnatifida is harvested commercially in Australia (Tasmania) and. Meinesz et al. Born et al.. Wallentinus 2002. Hewitt: Impacts of introduced seaweeds 411 Caulerpa taxifolia is the one introduced seaweed for which ecological impacts are well documented (Table 1). reducing invader abundance. but does have limited abundance or impact information for specific sites.. The species has been cultured in France since 1983.g. ecological impacts of this group are known from only a handful of species. Hewitt 2003a). 2007. most impact studies are conducted over periods ranging from only weeks to at most a few years. however. mainly those introduced to the Hawaiian islands (Table 1).e. where C. Aquaculture imports and transfers are the main vectors for invading seaweeds in Europe (Ribera Siguan 2002. However. which Stockwell et al. However. for de-fouling of maritime structures) are perceived to be ongoing costs regardless of the presence of introduced species (Sinner et al. In contrast. However. at least briefly. 2007). contrasting results were found (see above and Table 1). Impacts of invaders may also change through time..g. and urbanized embayments. gametophytes vs.e. hull antifouling) are significant for commercial and recreational shipping sectors. 2004. We have presented figures for a limited set of countries. the reasons for this are unknown. 2001). 2002. taxifolia. costs for eradication and control (Table 2). the use of tributyltin in antifouling paints will be phased out globally by 2008 and costs of hull maintenance may increase. cited in Wallentinus 2002).L. Meinesz 2007) is focused on tracking the distribution and spread of this invader. herbivore preferences may change over time from native to alien seaweeds.ices.. the costs of compliance with the Code are unknown. tetrasporophytes of Asparagopsis armata. Interestingly. The economic costs of species invasions must also include other societal costs such as management and research. The ICES Code of Practice for the Introductions and Transfers of Marine Organisms (updated 2003. Most alien marine species are found in the coastal zone (Carlton 1996). tomentosoides in the Mediterranean Sea and off the coast of Maine (USA) indicate that this species peaked about a decade after first discovery and then declined (reviewed in Trowbridge 1998). 2000). Observations of Codium fragile ssp. and are possibly underestimated. 2007).g. It is debatable whether reported impacts are inherent. whereas remote sensing results suggest that C. (2001) estimated a colonized area in the Mediterranean of 131 km2. Schaffelke and C.. taxifolia reaches very high abundances (see Table 1). or cryptic invasions of sibling species that are morphologically indistinguishable from previously introduced species or native species (e.B. available at http://www. Other reasons may be density-dependent thresholds in survivorship or exponential growth after a lag phase. they are unusually not considered to be specific to alien marine species (Hassall & Associates Pty Ltd. While environmental disturbance facilitating establishment of aliens may be greater in these environments. is generally viewed as a positive impact (see Pickering et al. and hence possibly impacted. Hewitt et al. Even though costs for vessel maintenance (i. Economic impacts The data are too limited to even roughly assess the economic impacts of invader seaweeds. The management regimes currently under consideration for hull fouling in Australia and New Zealand may lead to specific. 2007. 2003). Coyer et al. Hewitt et al. However. 2004a). We have indications of some costs involved with seaweed invasions. are from two highly urbanized coastal regions in France and Italy. The wider ecological consequences of genetic effects of seaweed invasions (the only example we found is the formation of fertile hybrids between the native Fucus serratus and the alien F. Pickering et al. taxifolia cover along the south coast of France may have been overestimated by a factor of ten (Jaubert et al. invading marine species often persist at low levels and later start to increase in abundance and spread. Ruiz and Hewitt 2002. 2002). species-specific consequences or whether they would be manifested only in disturbed environments. this monitoring indicates that areas of highest cover and colonized area are close to the initial incursion point (along the Ligurian coast) and that the spread of C. albeit with limited success (Ribera and Boudourw91x . and there is currently no quantitative information about invasive seaweed abundances or impacts on decadal or longer time scales. and alien marine species-associated additional costs of maintenance. 2002) are currently unknown. there may have been separate introductions of morphologically dissimilar generations (e. and where impacts are most likely. one or more significant introduction vectors are generally present (Ruiz et al.g. in Spain (Cremades 1993. it is impossible to identify the proportion of these expenses that apply to seaweed invasions only. e. An economic assessment of the impacts of seaweed invasions should cover all potentially affected values including use and non-use values (Perrings et al. A commercial harvest policy is in place in New Zealand. estuaries and ports are considered to be ‘‘hot spots’’ of introductions (Hewitt and Martin 2001. they also have a high inoculation pressure. (2003) attribute to either an initial period of adaptation or a change to previously functional environmental controls such as competition or herbivory. prescribes quarantine and disinfection procedures to alleviate this pathway. either accidentally or intentionally introduced. 2001. Booth et al. Ruiz and Hewitt 2002. 2000. The majority of studies.. also see Nunes and van den Berg 2001 for a review of economic valuation of biodiversity). evanescens. For example.

412 B. Schaffelke and C.L. Hewitt: Impacts of introduced seaweeds

esque 1995, Fletcher and Farrell 1999). In Argentina this species was first considered to be a new resource (Casas and Piriz 1996), but is now rather viewed as an ecological and economic threat to native seaweed resources (Casas et al. 2004). Introductions of seaweeds for aquaculture are common practice, especially of tropical carrageenophytes (Zemke-White 2004). Impacts of these introductions are poorly understood and are inferred from knowledge about impacts from red algae introduced to Hawaii for aquaculture trials (see Table 1 and Smith et al. 2002). A quarantine protocol for introductions of tropical seaweed has been established, targeting epiphytes and epifauna (Sulu et al. 2003); however, costs for these quarantine measures are unknown. The risks of intentional seaweed introduction have not yet been evaluated with cost-benefit analyses, and such analyses would be difficult to perform currently due to lack of data about impacts. The potential of future introductions of genetically modified seaweeds for aquaculture may add another dimension of uncertainty to this issue. Management of impacts Prevention of impacts is the driving force for costly surveillance, eradication and control programs. Managing the impacts of introduced seaweeds goes hand in hand with management strategies aimed at preventing new introductions in the first place and at controlling or eradicating established invading species (Hewitt 2003a, Hewitt et al. 2004b). Clearly, impacts will be avoided if species are prevented from arriving through a range of pre-border management options (op. cit.). Similarly, impacts are likely to be minimized if eradication/control measures are in place to limit the establishment and/or prevent high abundances of established invasive species wfor a description control measures for invading seaweeds see Wotton and Hewitt (2004) and Anderson (2007)x. Research needs Biological invasions have human causes and consequences (Perrings et al. 2002, Hewitt 2005). Future research on impacts of alien seaweeds (and other alien marine species) should focus on multidisciplinary research with biological, social and economic approaches. As impacts are intricately linked to the transport and establishment of alien marine species, much more knowledge is needed about the mechanisms involved in these preceding two stages of the invasion process. Frameworks need to be developed to better predict which species are likely to invade which habitats. The mechanisms that lead to high abundances of introduced seaweeds need to be identified, including the role of anthropogenic disturbance and climate change as confounding factors. The spatial and temporal variability of impacts need to be explored, which will improve the understanding of ecosystem vulnerability and adaptation. This knowledge will support implementation of Article 8h of the Convention of Biological Diversity (prevention, control and eradication of introduced species which threaten ecosystems or species). Without the capacity to measure and predict impacts of alien marine species, w92x

scarce funds for research and management are unlikely to be allocated where they are most needed.

We were unable to find sufficient substantial quantitative information about the impacts of alien seaweeds to detect common patterns. Even though a number of studies have shown significant ecological impacts, the underlying mechanisms are largely unidentified and impacts may be specific to the invaded system or the period of time since establishment and/or past disturbance. In addition, knowledge about socio-economic impacts is extremely scarce. Currently, decisions about management of alien invasive seaweeds are mostly unsupported by best science. Until we are able to understand, predict and measure impacts of alien seaweeds on various spatial and temporal scales, the management of species incursions needs to remain focused on early detection, rapid response and control to reduce the likelihood of impact manifestation.

We thank Craig Johnson and Anthony Chapman for the invitation to contribute to this special issue and for their helpful comments on the manuscript. We also thank Marnie Campbell, Jennifer Smith, Sven Uthicke and two anonymous reviewers for constructive comments and discussions.

Airoldi, L. 1998. Roles of disturbance, sediment stress, and substratum retention on spatial dominance in algal turf. Ecology 79: 2759–2770. Airoldi, L., F. Rindi and F. Cinelli. 1995. Structure, seasonal dynamics and reproductive phenology of a filamentous turf assemblage on a sediment influenced, rocky subtidal shore. Bot. Mar. 38: 227–237. Amade, P. and R. Lemee. 1998. Chemical defense of the Medi´ terranean alga Caulerpa taxifolia: variations in caulerpenyne production. Aquat. Toxicol. 43: 287–300. Ambrose, R.F. and B.V. Nelson. 1982. Inhibition of giant kelp recruitment by an introduced brown alga. Bot. Mar. 25: 265–267. Anderson, L.W.J. 2005. California’s response to Caulerpa taxifolia: a model for invasive species rapid response. Biol. Invasions 7: 1003–1016. Anderson, L.W.J. 2007. Control of invasive seaweeds. Bot. Mar. 50: 418–437. Arigoni, S., P. Francour, M. Harmelin-Vivien and L. Zaninetti. 2002. Adaptive coloration of Mediterranean labrid fishes to the new habitat provided by the introduced tropical alga Caulerpa taxifolia. J. Fish. Biol. 60: 1486–1497. Balata, D., L. Piazzi and F. Cinelli. 2004. A comparison among assemblages in areas invaded by Caulerpa taxifolia and C. racemosa on a subtidal Mediterranean rocky bottom. Mar. Ecol. 25: 1–13. Battershill, C., K. Miller and R. Cole. 1998. The understorey of marine invasions. Seafood New Zealand 6: 31–33. Bellan-Santini, D., P.M. Arnaud, G. Bellan and M. Verlaque. 1996. The influence of the introduced tropical alga Caulerpa taxifolia, on the biodiversity of the Mediterranean marine biota. J. Mar. Biol. Assoc. UK 76: 235–237.

B. Schaffelke and C.L. Hewitt: Impacts of introduced seaweeds 413

Biosecurity Council. 2003. Tiakina Aotearoa-Protect New Zealand: the biosecurity strategy for New Zealand. Wellington, New Zealand, Ministry of Agriculture and Forestry. pp. 63. Booth, D., J. Provan and C.A. Maggs. 2007. Molecular approaches to the study of invasive seaweeds. Bot. Mar. 50: 385–396. Born, W., F. Rauschmayer and I. Brauer. 2004. Economic eval¨ uation of biological invasions – a survey. UFZ Discussion Papers. UFZ Center for Environmental Research, Leipzig, Germany. Online: (22/02/2005). pp. 30. Boudouresque, C.F. and M. Verlaque. 2002. Biological pollution in the Mediterranean Sea: invasive versus introduced macrophytes. Mar. Pollut. Bull. 44: 32–38. Boudouresque, C.F., A. Meinesz, M. Verlaque and M. KnoepfflerPeguy. 1992. The expansion of the tropical alga Caulerpa taxifolia in the Mediterranean. Cryptogam. Algol. 13: 144– 145. Boudouresque, C.F., A. Meinesz, M.A. Ribera and E. Ballesteros. 1995. Spread of the green alga Caulerpa taxifolia (Caulerpales, Chlorophyta) in the Mediterranean: possible consequences of a major ecological event. Sci. Mar. 59 (Suppl. 1): 21–29. Boudouresque, C.F., R. Lemee, X. Mari and A. Meinesz. 1996. ´ The invasive alga Caulerpa taxifolia is not a suitable diet for the sea urchin Paracentrotus lividus. Aquat. Bot. 53: 245–250. Branch, G.M. and C.N. Steffani. 2004. Can we predict the effects of alien species? A case-history of the invasion of South Africa by Mytilus galloprovincialis (Lamarck). J. Exp. Mar. Biol. Ecol. 300: 189–215. Breeman, A.M. 1988. Relative importance of temperature and other factors in determining geographic boundaries of seaweeds: experimental and phenological evidence. Helgol. Meeresunters. 42: 3199–3241. Britton-Simmons, K.H. 2004. Direct and indirect effects of the introduced alga Sargassum muticum on benthic, subtidal communities of Washington State, USA. Mar. Ecol. Progr. Ser. 277: 61–78. Carlton, J.T. 1996. Pattern, process, and prediction in marine invasion ecology. Biol. Conserv. 78: 97–106. Carlton, J.T. 2000. Global change and biological invasions in the Oceans. In: (H.A. Mooney and R.J. Hobbs, eds) Invasive species in a changing world. Island Press, Washington DC. pp. 31–53. Casas, G.N. and M.L. Piriz. 1996. Surveys of Undaria pinnatifida (Laminariales, Phaeophyta) in Golfo Nuevo, Argentina. Hydrobiologia 326/327: 213–215. Casas, G., R. Scrosati and M.L. Piriz. 2004. The invasive kelp Undaria pinnatifida (Phaeophyceae, Laminariales) reduces native seaweed biodiversity in Nuevo Gulf (Patagonia, Argentina). Biol. Invasions 6: 411–416. Ceccherelli, G. and D. Campo. 2002. Different effects of Caulerpa racemosa on two co-occurring seagrasses in the Mediterranean. Bot. Mar. 45: 71–76. Ceccherelli, G. and F. Cinelli. 1997. Short-term effects of nutrient enrichment of the sediment and interactions between the seagrass Cymodocea nodosa and the introduced green alga Caulerpa taxifolia in a Mediterranean bay. J. Exp. Mar. Biol. Ecol. 217: 165–177. Ceccherelli, G. and F. Cinelli. 1998. Habitat effect on spatio-temporal variability in size and density of the introduced alga Caulerpa taxifolia. Mar. Ecol. Progr. Ser. 163: 289–294. Ceccherelli, G. and F. Cinelli. 1999. Effects of Posidonia oceanica canopy on Caulerpa taxifolia size in a north-western Mediterranean bay. J. Exp. Mar. Biol. Ecol. 240: 19–36. Ceccherelli, G. and N. Sechi. 2002. Nutrient availability in the sediment and the reciprocal effects between the native seagrass Cymodocea nodosa and the introduced rhizophytic alga Caulerpa taxifolia. Hydrobiologia 474: 57–66.

Ceccherelli, G., L. Piazzi and D. Balata. 2002. Spread of introduced Caulerpa species in macroalgal habitats. J. Exp. Mar. Biol. Ecol. 280: 1–11. Chapman, A.S. 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, A.S., R.E. Scheibling and A.R.O. Chapman. 2002. Species introductions and changes in the marine vegetation of Atlantic Canada. In: (R. Claudi, P. Nantel and E. MuckleJeffs, eds) Alien invaders in Canada’s waters, wetlands and forests. Natural Resources Canada, Canadian Forest Service, Science Branch, Ottawa. pp. 133–148. Chisholm, J.R.M., F.E. Fernex, D. Mathieu and J.M. Jaubert. 1997. Wastewater discharge, seagrass decline and algal proliferation on the Cote d’Azur. Mar. Pollut. Bull. 34: 78–84. Colgan, C.S. 2004. Measurement of the ocean and coastal economy: theory and methods. National Ocean Economics Project, USA. (18 April 2005). Collings, G., G. Westphalen, A. Cheshire, K. Rowling and M. Theil. 2004. Caulerpa taxifolia (Vahl) C. Agardh eradication efforts in West Lakes, South Australia. SARDI Aquatic Sciences Publication RD02/0161–8, South Australian Research and Development Institute, Henley Beach. pp. 34. Conklin, E.J. and J.E. Smith. 2005. Abundance and spread of the invasive red alga, Kappaphycus spp., in Kane’ohe Bay, Hawai’i and an experimental assessment of management options. Biol. Invasions 7: 1029–1039. Cosson, J. 1999. On the progressive disappearance of Laminaria digitata on the coasts of Calvados (France). Cryptogam. Algol. 20: 35–42. Costello, C.J. and A.R. Solow. 2003. On the pattern of discovery of introduced species. Proc. Natl. Acad. Sci. USA 100: 3321–3323. Coyer, J.A., A.F. Peters, G. Hoarau, W.T. Stam and J.L. Olsen. 2002. Hybridization of the marine seaweeds, Fucus serratus and Fucus evanescens (Heterokontophyta: Phaeophyceae) in a 100-year-old zone of secondary contact. Proc. Roy. Soc. London 269:1829–1834. Critchley, A.T. 1983. The establishment and increase of Sargassum muticum (Yendo) Fensholt populations within the Solent area of southern Britain. II. An investigation of the increase in canopy cover of the alga at low water. Bot. Mar. 26: 547–552. Critchley, A.T., W.F. Farnham and S.L. Morrell. 1986. An account of the attempted control of an introduced marine alga, Sargassum muticum, in Southern England. Biol. Conserv. 35: 313–332. Critchley, A.T., P.H. Nienhuis and K. Verschuure. 1987. Presence and development of populations of the introduced brown alga Sargassum muticum in the southwest Netherlands. Hydrobiologia 151/152: 245–255. Curiel, D., G. Bellemo, M. Marzocchi, M. Scattolin and G. Parisi. 1998. Distribution of introduced Japanese macroalgae Undaria pinnatifida, Sargassum muticum (Phaeophyta) and Antithamnion pectinatum (Rhodophyta) in the Lagoon of Venice. Hydrobiologia 385: 17–22. Curiel, D., P. Guidetti, G. Bellemo, M. Scattolin and M. Marzocchi. 2001. The introduced alga Undaria pinnatifida (Laminariales, Alariaceae) in the Lagoon of Venice. Hydrobiologia 477: 209–219. Davis, M.A. and M. Pelsor. 2001. Experimental support for a resource-based mechanistic model of invasibility. Ecol. Lett. 4: 421–428. Davis, M.A., J.P. Grime and K. Thompson. 2000. Fluctuating resources in plant communities: a general theory of invasibility. J. Ecol. 88: 528–534. den Hartog, C. 1997. Is Sargassum muticum a threat to eelgrass beds? Aquat. Bot. 58: 37–41. De Villele, X. and M. Verlaque. 1995. Changes and degradation


414 B. Schaffelke and C.L. Hewitt: Impacts of introduced seaweeds

in a Posidonia oceanica bed invaded by the introduced tropical alga Caulerpa taxifolia in the north western Mediterranean. Bot. Mar. 38: 79–87. DeWreede, R.E. 1983. Sargassum muticum (Fucales, Phaeophyta): regrowth and interaction with Rhodomela larix (Ceramiales, Rhodophyta). Phycologia 22: 153–160. Deysher, L.E. and T.A. Norton. 1982. Dispersal and colonization in Sargassum muticum. J. Exp. Mar. Biol. Ecol. 56: 179–195. Dunstan, P.K. and C.R. Johnson. 2007. Mechanisms of invasions: can the recipient community influence invasion rates? Bot. Mar. 50: 361–372. Edgar, G.J., N.S. Barrett, A.J. Morton and C.R. Samson. 2004. Effects of algal canopy clearance on plant, fish and macroinvertebrate communities on eastern Tasmanian reefs. J. Exp. Mar. Biol. Ecol. 312: 67–87. Farnham, W.F. 1980. Studies on aliens in the marine flora of southern England. In: (J.H. Price, E.G. Irvine and W.F. Farnham, eds) The shore environment. Vol. 2: ecosystems. Systematics Association Special Volume N. 17 (b). Academic Press, London and New York. pp. 875–914. Fletcher, R.L. and P. Farrell 1999. Introduced brown algae in the North East Atlantic, with particular respect to Undaria pinnatifida (Harvey) Suringar. Helgol. Meeresunters. 52: 259– 275. Fletcher, R.L. and S.M. Fletcher. 1975. Studies on the recently introduced brown alga Sargassum muticum (Yendo) Fensholt. I. Ecology and reproduction. Bot. Mar. 18: 149– 156. Floc’h, J.Y., R. Pajot and V. Mouret. 1996. Undaria pinnatifida (Laminariales, Phaeophyta) 12 years after its introduction into the Atlantic Ocean. Hydrobiologia 326/327: 217–222. Forrest, B.M. and M.D. Taylor. 2002. Assessing invasion impact: survey design considerations and implications for management of an invasive marine plant. Biol. Invasions 4: 375–386. Francour, P., M. Harmelin-Vivien, J.G. Harmelin and J. Duclerc. 1995. Impacts of Caulerpa taxifolia colonization on the littoral ichtyofauna of the North-Western Mediterranean Sea: preliminary results. Hydrobiologia 300/301: 345–353. Gavio, B. and S. Fredericq. 2002. Grateloupia turuturu (Halymeniaceae, Rhodophyta) is the correct name of the nonnative species in the Atlantic known as Grateloupia doryphora. Eur. J. Phycol. 37: 349–359. Glasby, T.M., R.G. Creese and P.T. Gibson. 2005. Experimental use of salt to control the invasive marine alga Caulerpa taxifolia in New South Wales, Australia. Biol. Conserv. 122: 573–580. Godwin, L.S. 2001. Hull fouling of maritime vessels as a pathway for marine species invasions to the Hawaiian Islands. Proceedings of the 24th Meeting of the Marine Facilities Panel of the United States Japan Cooperative Program in Natural Resources, November 4–10, 2001: 1–10. Gollasch, S. and E. Leppakoski. 1999. Initial risk assessment of ¨ alien species in Nordic coastal waters. Nord 1999: 8. Nordic Council of Ministers, Copenhagen. pp. 244. Grosholz, E.D. 1996. Contrasting rates of spread for introduced species in terrestrial and marine systems. Ecology 77: 1680–1686. Grosholz, E.D. 2002. Ecological and evolutionary consequences of coastal invasions. Trends Ecol. Evol. 17: 22–27. Grosholz, E.D., G.M. Ruiz, C.A. Dean, K.A. Shirley, J.L. Maron and P.G. Connors. 2000. The impacts of a nonindigenous marine predator in a California bay. Ecology 81: 1206–1224. Gurevitch, J. and D.K. Padilla. 2004. Are invasive species a major cause of extinctions? Trends Ecol. Evol. 19: 470–474. Harris, L.G. and M.C. Tyrrell. 2001. Changing community states in the Gulf of Maine: synergism between invaders, overfishing and climate change. Biol. Invasions 3: 9–21. Hassall & Associates Pty Ltd. 2002. Introduced marine pests. Scoping the socio-economic impacts. Report prepared for the Department of Agriculture, Fisheries and Forestry, Canberra, Australia. pp. 75.

Hayes, K.R. and C. Sliwa. 2003. Identifying potential marine pests – a deductive approach applied to Australia. Mar. Pollut. Bull. 46: 91–98. Hewitt, C.L. 2002. The distribution and diversity of tropical Australian marine bio-invasions. Pac. Sci. 56: 213–222. Hewitt, C.L. 2003a. Marine biosecurity issues in the world oceans: global activities and Australian directions. Ocean Yearbook 17: 193–212. Hewitt, C.L. 2003b. The diversity of likely impacts of introduced marine species in Australian waters. Records of the South Australian Museum Monographs Series 7: 3–10. Hewitt, C.L. 2005. New Zealand marine biosecurity research directions to underpin management. New Zeal. Sci. Rev. 61: 73–77. Hewitt, C.L. and A. Bauckham. 2004. Changes to marine biosecurity. Biosecurity Magazine 53: 13. Hewitt, C.L. and R.B. Martin. 2001. Revised protocols for baseline port surveys for introduced marine species – design considerations, sampling protocols and taxonomic sufficiency. CRIMP Technical Report Number 22. Hobart, Tasmania, Australia, CSIRO Marine Research. pp. 46. Hewitt, C.L., M.L. Campbell, R.E. Thresher, R.B. Martin, S. Boyd, B.F. Cohen, D.R. Currie, M.F. Gomon, M.J. Keough, J.A. Lewis, M.M. Lockett, N. Mays, M.A. McArthur, T.D. O’Hara, G.C.B. Poore, D.J. Ross, M.J. Storey, J.E. Watson and R.S. Wilson. 2004a. Introduced and cryptogenic species in Port Phillip Bay, Victoria, Australia. Mar. Biol. 144: 183–202. Hewitt, C.L., J. Willing, A. Bauckham, A.M. Cassidy, C.M.S. Cox, L. Jones and D.M. Wotton. 2004b. New Zealand Marine Biosecurity: delivering outcomes in a fluid environment. New Zeal. J. Mar. Fresh. Res. 38: 429–438. Hewitt, C.L., M.L. Campbell, F. McEnnulty, K.M. Moore, N.B. Murfet, B. Robertson and B. Schaffelke. 2005. Efficacy of physical removal of a marine pest: the introduced kelp Undaria pinnatifida in a Tasmanian Marine Reserve. Biol. Invasions 7: 251–263. Hewitt, C.L., M.L. Campbell and B. Schaffelke. 2007. Introductions of seaweeds: accidental pathways and mechanisms. Bot. Mar. 50: 326–337. Husa, V., K. Sjøtun and T.E. Lein. 2004. The newly introduced species Heterosiphonia japonica Yendo (Dasyaceae, Rhodophyta): geographical distribution and abundance at the Norwegian southwest coast. Sarsia 89: 211–217. Jaubert, J.M., J.R.M. Chisholm, G. Passeron-Seitre, D. Ducrot, H.T. Ripley, L. Roy and G. Passeron-Seitre. 1999. No deleterious alterations in Posidonia beds in the Bay of Menton (France) eight years after Caulerpa taxifolia colonization. J. Phycol. 35: 1113–1119. Jaubert, J.M., J.R.M. Chisholm, A. Minghelli-Roman, M. Marchioretti, J.H. Morrow and H.T. Ripley. 2003. Re-evaluation of the extent of Caulerpa taxifolia development in the northern Mediterranean using airborne spectrographic sensing. Mar. Ecol. Progr. Ser. 263: 75–82. Johnson, C.R. and K.H. Mann. 1988. Diversity, patterns of adaptation, and stability of Nova Scotian kelp beds. Ecol. Monogr. 58: 129–154. Kideys, A.E. 2002. The comb jelly Mnemiopsis leidyi in the Black Sea. In: (E. Leppakoski, S. Gollasch and S. Olenin, eds) Inva¨ sive aquatic species of Europe. Distribution, impacts and management. Kluwer Academic Publishers, Dordrecht. pp. 56–61. Lapointe, B.E., P.J. Barile, M.M. Littler, M.M and D.S. Littler. 2005a. Macroalgal blooms on southeast Florida coral reefs: II. Cross-shelf discrimination of nitrogen sources indicates widespread assimilation of sewage nitrogen. Harmful Algae 4: 1106–1122. Lapointe, B.E., P.J. Barile, M.J. Wynne and C.S. Yentsch. 2005b. Reciprocal invasion: Mediterranean native Caulerpa ollivieri in the Bahamas supported by human nitrogen enrichment. Aquatic Invaders 16: 2–5. Lemee, R., D. Pesando, M. Durand-Clement, A. Dubreuil, A. Mei´


Comparative feeding preference of Strongylocentrotus droebachiensis (Echinoidea) for the invasive seaweed Codium fragile ssp. D. 2002. 40: 1028–1031. 2004. Red algal exotics on the North Sea coasts.. P. J. 48: 177– 192. LeBlanc. Intentional introductions of commercially harvested alien seaweeds. Environ.B.A.A. Skelton and R. Antolic. Belsher. Ferrua.L. Prince. Ecol. M. Feeding behavior of Paracentrotus lividus in the presence of Caulerpa taxifolia introduced in the Mediterranean Sea. 2001. RbcL sequences reveal multiple cryptic introductions of the Japanese red alga Polysiphonia harveyi. 46: 542–551. racemosa in the Mediterranean Sea: interspecific interactions and influence on native macroalgal assemblages.P. Norse. Nunes. A.H. Fenical. 8: 133–137. Effects de l’expansion des Rhodophyceae introduites Acrothamnion preissii et Womersleyella setacea sur les communautes algales des rhizomes ´ de Posidonia oceanica de Mediterranee occidentale. 50: 338–350. 1986. Ecology 83: 719–732. Cinelli. 1987. Effects of caulerpenyne. McKinney. W.M. Mari. Cryptogam. A. Cinelli.-M.. C. Ecological and evolutionary consequences of biotic homogenization.. Cinelli. 6 (online) URL: http://www. 19: 282–283. order Caulerpales. Ruiz.E. Thibaut. V. Grigulis ` and S. 383. Acta 19: 255–262.J. P. V.P. Are invasive species the drivers or passengers of change in degraded ecosystems? Ecology 86: 42–55. Lockwood. L. Pollut. C.. J. Piazzi. L. Soc. Girard. Community-wide effects of nonindigenous species on temperate rocky reefs. Eur. P. Langar.. Cinelli. H. Cryptogam. USA) by the Asian clam Potamocorbula amurensis. Pedrotti. Turkington. 34: 157–169. Issanchou and P. Lemee. Zuniga and D. Piazzi. A. 2003. C. N. J. Petrik and T. Environmental and economic costs of nonindigenous species in the United States. J. 225: 189–195. 21: 291–300. B. K. Boudouresque. L. Mar. Evol. Telopea 1: 136–138. Hewitt: Impacts of introduced seaweeds 415 nesz.. 37: 69–76. A. 2004. Ecol. E. M.S. Pickering. Mar.M. Guerriero and F. C. E. Mar. Bioscience 50: 53–65.R. Biotic homogenization: a few winners replacing many losers in the next mass extinction. 2003. and J. ´ Microalgae: a model to investigate the ecotoxicology of the green alga Caulerpa taxifolia from the Mediterranean Sea. Zuljevic. D. P. L. K. Gobert. R. de Vaugelas. Levine.. van den Bergh. I. Menager and S. Invasions 1: 3–19. 1999. Meinesz. Douglas.C. California. Goodell. Levin. D.M. Meinesz.. 10: 911– 919. Balata.S. Mar. M. pp. Ecol. Eston. Dalmazzone. Island Press. 1996. and F. global consequences. Wallentinus. Ser. Poff. Shogren. Trends Ecol.R. Appl. Ceccherelli. Mar. Mar. the major toxin from Caulerpa taxifolia on mechanisms related to sea urchin egg cleavage. Invasions 3: 201–210. Mar. Tunesi. Byers and L. S. McIvor. Lonsdale. D. Distribution and dominance of two introduced turf-forming macroalgae on the coast of Tuscany. 44: 509–520. F. 44: 13–25.. 2001. Acta. 2000.M. Algol. T. ´ 1996. A new record and eradication of the northern Atlantic alga Ascophyllum nodosum (Phaeophyceae) from San Francisco Bay. M. Impact: toward a framework for understanding the ecological effects of invaders. Bull. L. Preliminary survey of toxicity of the green alga Caulerpa taxifolia introduced into the Mediterranean. Watkinson. Evol. Ecol. 2001. M. J.A. Appl. Global marine biological diversity. Biol.. D’Antonio. Lemee.E. R.B. Cryp´ ´ togam. Clarifying biotic homogenization. D. Effects of Cau´ lerpa taxifolia secondary metabolites on the embryogenesis. 39: 203–222. Grau. and D. G. 5: 485–493. J. Orestano. Proc. D. Washington. Ben Mustapha..J. L. and G. A. 1993. and R. Mar. MacDougall. H. Chang. Amade and J.B. Malestroit. von Holle. 2005. L. J. E. B. A strategy for building conservation into decision making. Nichols. and control. C. Changing dominance of an algal species wCaulerpa filiformis (Suhr) Heringx.A. Effects of competition between two introduced Caulerpa. Lonsdale.. Economic valuation of biodiversity: sense or nonsense? Ecol. Evans. Ruitton. 1992.E. Miller. M. Massuti-Pascual. E.L.L. Pietra. M. J. and W. Balata. 1996. 1999. Methods for identifying and tracking seaweed invasions. Perrings. Evaluation of benthic macroalgal invasion in a harbor area of the western Mediterranean Sea. Ceccherelli and F. Zavodnik and A. K. and N. L. 1993. J. J. Williamson. V. Meeresunters. Moyle. R.L. 2007. Olden. D. II. Maggs.D. D. El Abed. Trends Ecol. P. Lemee. Mar. Boudouresque. Econ.. Parker. X. 50: 373–384. ´ A. Algol. Simmons and A. Comparative study of the growth of the two-occurring introduced green algae Caulerpa taxifolia and Caulerpa racemosa along the Tuscan coast (Italy.L. 19: 18–24. D. Pesando.H.L. Maggs.M.M.D. 30: 405–410. epidemiology. Occhipinti Ambrogi. Piazzi. 2002. Simberloff. Italy. Mol. 52: 243–258. A. and F. F. Remarkable invasion of San Francisco Bay (California. Oceanol. A. P. Chemical defense in tropical green algae.M. Trends Ecol. Delfino. Phycol. The introduced green alga Caulerpa taxifolia continues to spread in the Mediterranean. 38: 223–231. C. C. J. Invasions 7: 265–279. 2000. Fausch.A. 2002. Ecol. 1993.. 35: 139–155. T. 2001b. 2004.D. Sulu. Progr. Toxicol. L. Good. 10: 689– 710. J. Paul. D. J. J. 66: 95–101. E. Marchi and R. B. and V. 2003. Cottalorda. 1994.M. and H. Peirano. J. northwestern Mediterranean Sea in relation to different habitats and sedimentation. Phycol. Biological invasion risks and the public good: an economic perspective. Piazzi. 2002. W. Provan and M. Schemel. Ceccherelli and F. Bazzaz. Djellouli. 210: 149–159.D.F. Balata and F. Cecchi and F. N. Ecology 83: 3182–3193. Cooccurence of Caulerpa taxifolia and C. A. Clout and F. Williamson.J. Cinelli. Mack.M. Ivesa.K. Meinesz. Bot. and F.. 2003. R.S.D. Lavorel. Helgol. 24: 233– 243. 22: 459–466. W. Effect of microalgae treat´ ed with natural toxins on the nutrition and development of filter-feeding sea-urchin larvae. Lond. Dukes. and J. C. Barbier. and W. Ecol. Phycol. Phycol. R.S. Nyberg. Morrison. tomentosoides w95x . Coyer. J.. Mar. T. Ser. G. Progr. R. 1999.G.D.M. P. Conservation Ecol. B. Bot. Threat to macroalgal diversity: effects of the introduced green alga Caulerpa racemosa in the Mediterranean. M.L. Mechanisms underlying the impacts of exotic plant invasions. Ser.A. Lemee. Bot.M. 2005. C. Lohrer. Piazzi. Ser. Displacement of a former community.N. western Mediterranean). L. C. Cosentino-Manning and G. 2001. Amade. Simberloff. muticum? Bot. Can species traits be used to predict marine macroalgal introductions? Biol. D.L. J. A. Olden. and I. N. Mar. Douglas and K. Cinelli. Thompson and L.D. Trends Ecol. Biotic invasions: causes. Pesando.. Cinelli. Lach. Stanhope. Evol. Paula. 14: 450–453. Biol.J. Wonham. Pimentel. Biological invasions: lessons for ecology. Pedrotti. Progr. A.B.A. Algol. Cinelli. 19: 245–253. Stegenga. Poff. 2001a. Are there other Sargassum species potentially as invasive as S.M. Progr. L. and R.F. P. Aquat. Evol. Interactions among aliens: apparent replacement of one exotic species by another.. Whitlatch. 2000.L. Piazzi. 270: 775–781. Lodge. Savini. R. USA. Oceanol. Eur. L. A. M. A. Chiaverini. 1999. Jaklin. Res. DC. 2002. Environ. Kareiva. Goldwasser. and R. Vila. M. Lemee. 1997. Schaffelke and C. 1976.J. Piazzi. larval development and metamorphosis of the sea urchin Paracentrotus lividus. Biological invasions as a component of global change in stressed marine ecosystems. consecol. 2007. Piazzi. May. Epiphytic macroalgal assemblages of Posidonia oceanica rhizomes in the western Mediterranean.

B.L. Mar. France. 113: 159–163. 35: 270–395. nutrient levels. C. 124: 215–218. Leppakoski. pp.. J. 2006. Kurelec and W.H.. Confronto tra la fauna epifitica di Caulerpa taxifolia e Cymodocea nodosa.W. Report to Ministry of Fisheries. Biol. N.. 2000.A. 1999. 291–310.1007/s10811-006-9074-2).J. D. S. Evol. 1992. B. M.B. D. Introduced marine plants. A. G. Distribution. R. Biol. Stimson. Schroder. M. Syst. B. Torchia. 207: 79–88.J. H. Island Press. 5: 119–126.. Invasions 1: 21–32. 1999. Williams. C. Ruiz.T. Key threats from marine bioinvasions: a review of current and future issues. Natl. Schaffelke and C. 84. Mar. 31: 481–531. G. Meeresunters. R.S. Progr. Hassanein. M. R. Wonham and A.. Behavioral modifications imposed to the ciliate protist Euplotes crassus by caulerpenyne: the major toxic terpenoid of the green seaweed. Helgol.. and S. 578.E. Progr. Smith. pp. The effects of Caulerpa taxifolia on invertebrate abundance in Agua Hedionda Lagoon. Hewitt: Impacts of introduced seaweeds (Chlorophyceae) and four other seaweeds. T. 58: 325–343. B. In: (J. Pedersen. B. A strategy for managing the Asian kelp Undaria: final report. Gravez.185–195. Role of grazing by sea urchins Strongylocentrotus droebachiensis in regulating the invasive alga Codium fragile ssp. Relini and G. Evers and A. ICES J.M.S. Ecology of the invasive red alga Gracilaria salicornia (Rhodophyta) on O’ahu. Mueller.N. Ann. 2002. T. Pac. Most. Limnol. and Hypnea cervicornis J. Noumea. Ruiz. Kinlan. 44: 950–972. Invasion of Sargassum muticum in Limfjorden (Denmark) and its possible impact on the indigenous macroalgal community. tomentosoides.T.. Reise. and biases. Biologia Marina Mediterranea 5: 185–195. Selective grazing of the isopod Idotea baltica between Fucus evanescens and F.T. Relini. L. Ribera Siguan. Williams. M. and S. Massachusetts Institute of Technology. J. Acad. Ecol. Population ecology of the invasive kelp Undaria pinnatifida in California: environmental and biological controls on demography. 1999. New Zealand. Kinnison. M. 35: 290–303. Squair and C. Stachowicz. Appl. Ribera Siguan..F. 2002.L. Ag.T. Russell. Sauvage. S. C. S. Stimson. Kumar. T. Dini. P. Ecol. Reusch. Progr. J. ¨ H. J. M. Smith.J. vesiculosus from Kiel Fjord (Western Baltic). Relini. Leppakoski. Anthony.R. G. with special reference to macroalgae: mechanisms and impact. Laws. Ag. tomentosoides in Nova Scotia. and Hypnea musciformis (Wulfen) J. Exp. Sci.X. Badria.H. 11: 187–268. Conklin. 24–36. 183–226. Protistol. C. Trends Ecol. and their association with two native species. Fofonoff. Ser. V.B. Sea Grant College Program. R. C. D. Sulu. G. Palluy. Ser. Phar. M.A. Oecologia 113: 428–441.-F. Acanthophora spicifera (Vahl) Boerg. A.A. 1998c. Boudouresque. Macrophyte canopy structure and the success of an invasive marine bivalve. Ecol. Hawai’i. pp. 136. Fofonoff and A. Batel. Hines. Ecol. M. J.J. Torchia. Ser. GIS Posidonie Publications. Zool. pp. Hewitt. Kluwer Academic Publishers. Introduced macroalgae: growing concern. Ag.E. Olenin. Fish biodiversity in a Caulerpa taxifolia meadow in the Ligurian Sea. 1999.B.T. Wolff. T. 2002.M. Pathways of biological invasions of marine plants. J. R. In: (E. impacts and management. G. Boudouresque. Larned and E.. 1983.L. Ital. 2005. processes. 2000. Mar. Res. Schaffelke. Relini.E. Hay and T. Sci. Oceanogr.416 B.P.J. Johnson and C. 2001. 2004. J. (online first. M. Pickering. Ribera. Gollasch and ¨ S. G. Hunter and C. impacts and management. 1998b. Ayyad.E. Secretariat of the Pacific Community.T. Nitrogen efflux from the sediments of a subtropical bay and the potential contribution to macroalgal nutrient requirements. ed. In: (C. Hines.) Marine Bioinvasions.. January 24–27. Walsh. 268: 69–80. and introduced algae on the distribution and abundance of the invasive macroalga Dictyosphaeria cavernosa in Kaneohe Bay.E. M. D. S.V.. 2004. Hawaii.L. 1981. Carlton. Hewitt. 139: 139–146. Cawthron Report No. S. eds) Third International Workshop on Caulerpa taxifolia.A. Relini. Hendry and M.. Washington. Mar. Taylor. Laurencia nidifica J. The ecological invasion of Hawaiian reefs by two marine red algae. 1998. Gollasch and W. Kaneohe Bay sewage diversion experiment: perspectives on ecosystem responses to nutritional perturbation. 1995. pp. Biol. 2000. K. Nelson. J. Dordrecht. pp.A. J. Distribution. Dordrecht. Meinesz and F. C. Environ. Krause-Jensen. 2002. Sci. Biol. Tippets. Simberloff.. C.H. Wernberg and D.. Boston. USA 99: 15497–15500. K. Stæhr. 18: 94–101. Smith. R. Ruiz. Molinari.. Non-indigenous species as stressors in estuarine and marine communities: assessing invasion impacts and interactions.M. Reusch. Kappaphycus seaweed in the Pacific: review of introductions and field testing proposed quarantine protocols. 1999. Hewitt and J. Thomsen. growth and reproduction of sea urchins (Strongylocentrotus droebachiensis) on single and mixed diets of kelp (Laminaria spp. Oikos 84: 398–416. Gollasch and S. and S. 252: 159–180. Pac. J. Ross. 2001. Phycol. von Holle. Scheibling. Ecology of the imported red seaweed Eucheuma striatum Schmitz on Coconut Island. 2002. 2000. W. eds) Invasive aquatic ¨ species of Europe.A. R. Distribution and reproductive characteristics of nonindigenous and invasive marine algae in the Hawaiian Islands. Scheibling. Larned.L. Smith. DOI: 10. 2000. and B. Torchia.G. Sci.. 529–547.E.J. Stachowicz. 57: 1421– 1427. Prog. 1995.M. and S. Mar.J. Conklin. Positive interactions of nonindigenous species: invasional meltdown? Biol. Wiens. Forrest and M.. G. Thresher. Cawthron Institute. 56: 299–315. Carlton. Russell. Pac. Smith. C.J.H. Osman. E.A. Torchia. ICES Marine Science Symposia 194: 110–125. Sci. pp.M. Pederson.F. Caulerpa taxifolia.R. Oahu. J. The role of fishing gear in the spreading of allochthonous species: the case of Caulerpa taxifolia in the Ligurian Sea. Effects of herbivory.M. Mar. Rev. Introduced marine species of the North Sea coasts.L. Eur.M. 2003. 1998. Toward understanding patterns of coastal marine invasions: a prospectus. 37: 87–108.C. Olenin.. Feeding. Mar. Invasions 5: 3–21. S. M. D. J.. P. E. Variable responses of native eelgrass Zostera marina to a non-indigenous bivalve Musculista senhousia. Report for University of California at Berkeley Environmental Sciences w96x . Hawaii. Hunter. Terwin. Sci. Kluwer Academic Publishers. Biol. and C. Contemporary evolution meets conservation biology. 1999. Toxicol. 1998a. eds) Invasive aquatic species of Europe. and C. Invasion of coastal marine communities in North America: apparent patterns. 2003. 65 (Suppl): 465–470. California. C. Ecol. Assessing the ecological impacts of an introduced seastar: the importance of multiple methods. 292: 203–212. Fish and epiphytic fauna on Caulerpa taxifolia and Cymodocea nodosa at Imperia (Ligurian Sea). Stockwell.B. Graham and J. Ricci.W. Mar. Inhibitory effects of extracts from the marine alga Caulerpa taxifolia and of toxin from Caulerpa racemosa on multixenobiotic resistance in the marine sponge Geodia cydonium. In: (E. Brock and T. J.P.) and the invasive alga Codium fragile ssp. Coral Reefs 19: 343–357. Pac.H. Sumi. Proc. Review of non-native marine plants in the Mediterranean Sea.E. Phycol. Whitlatch and R. 2003. 2003. Relini and G. Linking climate change and biological invasions: ocean warming facilitates nonindigenous species invasions. Sinner. Relini and G. Schaffelke. 52: 219–234. In: (G. Ruiz. A. C.L. Relini and G. Smith. F. Thornber. Capovani and F.. P... 2000. Kimmerer. Walhorn. Proceedings of the First National Conference. and R. M. eds) Invasive species: vectors and management strategies..L.

Wotton. J. Zemke-White. tomentosoides on New Zealand rocky shores: Current distribution and invertebrate grazers. Grosholz.D. 465–476. pp. 50: 351–360. Mar. Am. impacts and management. J. P. accepted 22 November. 2004. On the identity and origin of the Mediterranean invasive Caulerpa racemosa (Caulerpales. Mediterranean algal communities are changing in face of the invasive alga Caulerpa taxifolia (Vahl) C. ¨ ´ 2006.H. Kendrick. pp. The role of science in management of Caulerpa taxifolia in the United States. Trowbridge. Johnson. Trowbridge. Threats to macroalgal diversity: Marine habitat destruction and fragmentation. J.M. Acta 17: 659–672. Marine biosecurity postborder management: developing incursion response systems for New Zealand. Eradication success Down Under: heat treatment of a sunken trawler to kill the invasive seaweed Undaria pinnatifida.D. Smith. Fresh. 2004. Ecography 22: 5–12.C. Melillo. Wikstrom. Vitousek. Sci.R. J. Huisman. and H. Biol. 8. Assessment of the current knowledge on the environmental impacts of seaweed farming in the tropics. 19: 283–284. Olenin.. Valentine.. Biol. S. 83: 949–965. Australia.-F. Chlorophyta). Biol. 2002. M. J.M. Valentine. 27–52. 285: 43–55. Biol. In: (S. Ser. S. L. 2005. Stuart and D. P. R.M. Kautsky. Invasion of a habitat-form¨ ing seaweed: effects on associated biota. Mar.R. In: (E. Valentine. 2002. La Jolla.D.M. 89: 525–531. Online URL: http://socrates. Proceedings of the AsiaPacific Marine Science and Technology Conference.A. 1997. Hewitt. California. 126: 193–204. M. 2002. D. eds) Marine science into the new millennium: new perspectives and challenges. eds) International Caulerpa taxifolia Conference Proceedings. 2005b. California Seagrant College Program. January 31–February 1. 1998. 1999.L. Lubchenco and J. J. M. Ecol. N.D. I. The effects of colonization by Sargassum muticum on tidepool macroalgal assemblages. Valentine. Johnson. 2002. 2006 w97x .A. Ecol. Malaysia. and C. 2004. C.P. UK 77: 325–340. T-047 (CDROM). Establishment of the introduced kelp Undaria pinnatifida following dieback of the native macroalga Phyllospora comosa in Tasmania. and P. Trends Ecol. spread and persistence of introduced seaweed populations. 2003. Ho. D. Le Parco. Mar. berkeley.J. Williams. Magierowski and C. 2004.J. Johnson. Establishment of the introduced kelp Undaria pinnatifida in Tasmania depends on disturbance to native algal assemblages. 12–16 May 2002. 2003. Mechanisms of invasion: establishment.R. 38: 325–339. C. Mokhtar and L. Establishment of the green alga Codium fragile ssp. C. Johnson.Hj. USA. J. and G. Bot. Vroom. M.M. Mar. Van Beukering. Persistence of the exotic kelp Undaria pinnatifida does not depend on sea urchin grazing.P.P. Valentine. Rev. Wotton. Oecologia 148: 593– 601. The challenge of siphonous green algae. 36: 1–64. Grosholz.D. Progr. Exp. Publication No. 49: 844–849. and C. E. Durand. Mar. Mar. Wilkinson. Fritayre. Berkeley. R. 1998.M.pdf (22/ 02/2005).M. Kautsky and H.: An Ann. Mar. V. Ecol. pollution and introduced species. Bot. Human dominition of Earth’s ecosystems.M. 295: 63–90. Ecological economic modeling of coral reefs: evaluating tourist overuse at Hanauma Bay and algae blooms at the Kihei Coast.L. 38: 553–559. Johnson. Phycol. Cesar. J. Pavia.R. Received 22 December. 48: 106– 115. Williamson. Assoc. pp. S.L.B. Dordrecht. and C. 1996. 1994. Fergus. Introduced versus native subspecies of Codium fragile: How distinctive is the invasive subspecies tomentosoides? Mar. Bull. Chong. C. Bot. C. J. 58: 243–260. Boudouresque and Y. Ser. Wallentinus. Mar. Williams. Eur. eds) Invasive aquatic species of Europe.A. Pollut. 233: 307–310. 2001. O’Brien. ¨ S. Introduced marine algae and vascular plants in European aquatic environments. Res. Verlaque.. New Oceanogr. Pac. Kuala Lumpur. and C. San Diego.I. D. Phang. Mar.L. Trowbridge.L. Increased chemical resistance explains low herbivore colonization of introduced seaweed.C. 2004. Invasions 6: 141–150. pp. and L. D. Invasions. 2004. Science 277: 494–499.D. W. Evol. Progr.J. Schaffelke and C. University of California. 2004. In: (E. Leppakoski. California. The long history of the biotic homogenization concept. and C. Hawai’i. 1995. Hewitt: Impacts of introduced seaweeds 417 Senior Seminar. Biol. Mar. 55: 223–230. and E.. 2007. Res. Ecology of the green macroalga Codium fragile (Suringar) Hariot 1889: invasive and non-invasive subspecies.A. J. and C. P. Mooney.P.P. C. Preliminary reports from the Caulerpa taxifolia invasion in southern California. Agardh. Williams. H.. S. Viejo. Kluwer Academic Publishers. M. 1997. Wikstrom.R.B. Fresh. S. Sci. Ooi. CA. Steinarsdottir. Verlaque. Distribution. Ecol. 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. Gollasch and S. 2005a. 12. Mar. 41: 105–112.S. J. Oceanol.S. Walker. J.

2006). basic and applied research on management of freshwater macrophytes has a rich and long history spanning over 100 years (Sculthorpe 1967. Use of heat.g. marinas.g. and pertinent research is sparse (Schaffelke et al.2007. either based on economic criteria or criteria that result in tolerable effects on the environment. USA. salt. estuaries and lagoons. ‘‘management’’ and ‘‘control’’ refers to methods used to mitigate or reduce the negative impacts resulting from an invasive species.) will not be discussed here. and have utilized parallels between the marine and freshwater physical environments to propose practical approaches for control of seaweed invasions.e. wharfs. In contrast to typical fouling species.Botanica Marina 50 (2007): 418–437 2007 by Walter de Gruyter • Berlin • New York. Undaria. non-chemical methods. due to often harsh and highly variable physical conditions in marine environments. through effective management Abstract Seaweeds have invaded ecosystems along the coasts of many countries where they can displace native algae and seagrasses. This will require better communication among researchers and managers working to reduce introductions and negative impacts of these seaweeds. there is no such extensive network of researchers and practitioners whose purpose is the improvement of management methods for invasive seaweeds. efficacious methods for controlling seaweed infestations. to glean what is applicable from the freshwater environment. Caulerpa. through use of bottom paints. off the Florida coast).1515/BOT. efforts to control alien invasive seaweeds have been extremely limited. DOI 10. films. short of complete removal. national. rapid response actions. Codium. Similarly indicative is the lack of any examples of invasive marine algae in the relatively recent summary of invasive species as a global issue (Mooney and Hobbs 2000). Anderson USDA-Agricultural Research Service. herbicide. Introduction This article focuses on control of alien marine macroalgae as invasive species of tidal ecosystems that may be natural or altered habitats such as harbors.. and vessel hulls and to reduce drag on ships. Control of fouling species (e. management approaches are taken when complete extirpation of . regional and even local societies organized to deal expressly with nuisance freshwater plants. Gallagher and Haller 1990. etc. I have highlighted a few examples where management has been achieved at some measurable level. coatings. eradication. There are guides.. CA 95616. w98x Goals of seaweed control: management or eradication I have chosen to use the terms ‘‘management’’ and ‘‘eradication’’ from the well established vernacular of ‘‘pest control’’ in general. safe and effective chemical treatments. Usually.J. Actions aimed at management usually presume an unending infestation (i. self-sustaining). Thus. which now infests over 20. Nutrient inputs from near-shore sources have exacerbated the spread of some species (e. AERF 2005). and the lack of efficacious methods. Furthermore. but one that may be reduced to some acceptable level. To counter the increase in seaweed introductions and the spread of these species. On the other hand.. Pieterse and Murphy 1990). bays.000 ha of Mediterranean subtidal zones. but has yet to result in any operational programs. Keywords: biocontrol. copper. Given the paucity of verifiable... where feasible. The most widespread and notorious cases have been introductions of Caulerpa taxifolia. therefore. Though there are obviously important physiological and ecological differences between freshwater angiosperms and seaweeds. while there are several international. it will be useful to adapt. particularly related to logistics of prevention. biological control. chlorine. e-mail: lwanderson@ucdavis. Biological control by herbivorous mollusks and sea urchins has been investigated. and removal. mechanical control and prevention (e. containment. Davis. Though there is a long history of attempts to prevent or reduce the attachment of ‘‘fouling’’ marine species (including algae). Exotic and Invasive Weed Research. The goal of management is to reduce impacts to an acceptable level. methods that have proven successful in controlling freshwater weeds. One Shields Ave.g. New methods will need to be developed as well. there are many physical similarities in the habitats. management. these actions are directed primarily to protect the integrity of pilings. Few attempts to control seaweed invasions have been successful. freshwater and various mechanical (removal) approaches have been successful in reducing or eradicating some infestations. Invaded areas are usually gradients from naturally occurring littoral zones toward highly modified and artificial habitats formed by construction of physical barriers and substrata to accommodate maritime activities. reduce biodiversity and impair habitat of fish and invertebrates. manuals and practical management plans and strategies for freshwater ‘‘weeds’’. It is important.045 Review Control of invasive seaweeds Lars W. and an associated industry that encompasses aquatic herbicide development and use.

. business or a ‘‘wildfire’’ provides apt clarity. or has occurred elsewhere in very similar ecosystems. the scale or scope of an existing infestation should not necessarily preclude eradication. ‘‘Management’’ of fire alone is clearly not a tenable approach and it explains the tremendous efforts directed at both prevention and detection of fires. the importance of rapid. but cannot be permitted if eradication is to be achieved.J. Silva might be a feasible management approach for keeping well-defined intertidal areas free of further intrusion (Trowbridge 1999). some level of propagule ‘‘bank’’ may be tolerated in management projects (e. the ultimate expense of over $US 7 million for eradication must be weighed against potential impact on the environment and economic activity had this species been allowed to spread to susceptible sites along the Pacific coast. In addition. tomentosoides (Van Goor) P.000q ha infested. The simple analogy of responses to a fire in a home.g. Similarly. enforcement of regulatory constraints). Thus. target species biology. Australia National Task Force w99x .000 h-1 cm-2 surface area of sorus tissue. highly efficacious methods become available even after significant spread. and that successful eradication programs necessitate a zero-tolerance goal. The rapid increase in costs.g. likewise. (2005) report that Undaria pinnatifida can release zoospores at rates up to nearly 150 million per hour per sporophyte. For example. Notwithstanding the importance of rapid response (i. ‘‘control’’ and ‘‘eradication’’ interchangeably. then an overall strategy for full eradication may be feasible. as well as the feasibility of achieving it. it is much more difficult to argue as forcefully to block all possible pathways of introduction. In contrast.g. the rationale used to arrive at a decision to embark on a management or an eradication program must reflect the overall (generally long-term) goal. concomitant intensity of surveillance required for successful eradication usually far exceed (at least initially) that needed for management alone. as well as the competitive interactions between native species and an invasive alga. it might be possible to curtail further spread. A firm commitment to that goal also unequivocally defines for all stakeholders the expectations. Agardh in the Mediterranean Sea by constantly removing new phalanxes of the population spreading at the broad edges of the infestation. the ability to sustain a management program for many years needs to be assessed. eradication) to ‘‘new infestations’’. and that zoospore releases occurred over a three-month period.e. or when costs of eradication cannot be borne. Eradication of an invasive alga. (2006) recently reported that infestations of Caulerpa taxifolia in Botany Bay (New South Wales. This is dependent on site characteristics. and any other viable part or propagule. experience suggests this is not the case. and the potential impacts on non-target species. I have emphasized propagule removal because those unfamiliar with the practical aspects of eradication often use ‘‘management’’. One might argue that there is a continuum of goals (and attendant effort) between eradication at one end and ‘‘management’’ the other. A decision to eradicate as opposed to ‘‘manage’’ must also provide a scientifically driven endpoint that once attained. 2005. and available containment/eradication methods. The clear identification of a successful endpoint also justifies effective surveillance costs and provides incentives to preclude any further introductions (e. Finally. if sufficient opportunity for native organisms to sustain pre-invasion populations can be provided by simply suppressing populations of an invasive seaweed. In long-term ‘‘management’’ programs.W. Likewise. via biological control). scope of resources. and may even necessitate access to private property for extensive periods. York et al. For example. An example of management would be the efforts to contain further spread of Caulerpa taxifolia (Vahl) C.. then eradication may not be warranted. effective responses to algal introductions is supported by dispersal rates and capacities of marine macroalgae that can exceed by orders of magnitude those modeled for invertebrate larvae (see figure 3 in Kinlan et al. However. presupposes very early detection. General principles of management and eradication In the past few years. causes a significant reduction in further costs. plans and strategies for effective responses to invasive species have been developed by various countries (e. then the potential for eradication of large infestations may be greatly improved. cutting or physical removal of Codium fragile spp. Thus. While this would be a Herculean task given some 20. These interactions are usually poorly understood unless the invasion is a reoccurrence in a well-understood ecosystem. coupled with rapid. they are quite different. Australia) were associated with lower species richness of fishes.L. the thoroughness of removal and requisite. For example. long-term impacts of not controlling or eradicating invasive seaweeds must be considered. costeffective responses whose goal is to completely remove. if some populations can be contained and eradicated locally.. Wright 2005). For example.. reduced ‘‘public access’’ to the infested site. the successful eradication of Caulerpa taxifolia in California exemplifies the highly intense and initially costly type of program required for complete extirpation of an invasive marine alga (Anderson 2005). There are also equally important social ramifications associated with management versus eradication goals because the latter will almost always require significant changes in behavior. and time frame needed. and the potential non-target impacts of these typically tardy responses have been noted for invasive species in general (Rejmanek and Pitcairn 2002). Schaffelke et al. reduced fish abundance when compared with sites containing native seagrasses.C. These authors also outline release rates from other studies on laminarian species ranging from 2000 to 800. Thus. or kill all of a species’ vegetative parts. and why action analogous to ‘‘eradication’’ of the fire is the expected goal. If new. This approach encompasses nearly all current attempts to deal with invasions of aquatic organisms. and at one site. because their detection has usually occurred far too late for complete removal (eradication). However. Anderson: Control of invasive seaweeds 419 the target species is deemed not feasible.

. A general model for ‘‘invasive species response’’ can be adapted from other existing pestprevention and control plans cited above. I have summarized these actions in Figure 1.W. and usually expensive. with the common understanding that multiple routes and changes may be necessary to attain the goals of the project. a consistent hallmark of successful programs has been an underpinning from. sustaining public (stakeholder) confidence. one cannot simply initiate or direct a given set of actions and presume the outcome.. Given the limited tools available to manage or eradicate invasive seaweeds. Anderson: Control of invasive seaweeds 2000. Keppner 2002. Instead. Therefore. Only through that foundation can adequate. Finally. what reasonable set of objectives can be established to address seaweed infestations? How will success be measured? Who is responsible for coordinating control actions and where do the resources come from? Marine communities typically manifest complicated interspecific interactions.420 L. inevitably. pest-management or eradication projects tends to create a high level of public and political interest. agencies and public stakeholders. Thresher and Kuris 2004. The ascending. it is essential to implement an adaptive management approach because. improvements in methods.J. objective assess- ments of all actions be made. which presumes that efforts directed at ‘‘prevention’’ have failed. thus.g. and from successful control and eradication projects (e. These efforts also often require commitment of resources for several years. US Fish and Wildlife Service 2005). These response plans and successful projects share several essential components. Hewitt et al. while at the same time. Under the best circumstances. arrowed lines in Figure 1 represent this principle.g. In addition to adequate resources (funding. sound science. the process requires a culture of flexibility among collaborating individuals. developing credible. Establishing criteria for success Undertaking complex. CDFA 2005. Kuris and Culver 1999. 2004. 2004. hopefully. Anderson 2005). although specific methodologies must be tailored to fit both the target seaweed species as well as the invaded habitat. resulting in a new infestation. these criteria can be defined very early in the project. and the invasive algal species that pose a threat to them have multiple pathways of introductions. defensible and quantifiable measures of progress is not only essential for evaluating actions. it is also crucial to attaining a recognizable endpoint. unforeseen problems arise and new knowledge gained from monitoring and assessments of treatment actions will lead to adjustments and. technically challenging. 2002. Biosecurity Council 2003. and reliance on. FICMNEW 2003. Wotton and Hewitt 2004) and US state and federal agencies (e. equipment. expertise). w100x . In short. The clear choice between ‘‘management’’ and ‘‘eradication’’ needs to be made very early since that Figure 1 Generic scheme for developing response to invasive seaweed infestations. Bax et al.

2005). search grids were rotated slightly between diver passes to ensure better surveillance). use of GPS-established transects. California. In the California project described. USA. California). w101x . $US 7 million). Sprsspring. drove public outreach and education. Though this may seem obvious.e. given the track record of this species in temperate waters of the Mediterranean where it had spread to over 20. or monitoring methods. the projected criteria for successful eradication was three full growing seasons following the last known real ‘‘find’’. taxifolia infested site in Huntington Harbor. The importance of post-treatment monitoring cannot be overemphasized. but without divers’ knowledge. two critical activities must be implemented: treatment actions and reliable evaluation of their field efficacy. 2001).5–1.000 ha since 1985 (Meinesz 1999. success was nearly as good even for smaller patches. The history of surveillance and occurrence of C. When the growth rate of C. The approach taken with the USA Caulerpa taxifolia project provides a good example. For example. chemicals) in the environment. Based upon the surveillance and criteria established. and multiple offset survey grids (i.0 m in diameter. Sumssummer. declaration of eradication was made in July 2006 (California Department of Fish and Game 2006). Field efficacy was evaluated by removing sediment cores from treated areas and providing adequate growth conditions for any viable propagules (Anderson et al. or placement of solid chlorine-releasing pellets (see Anderson 2005).. nor can it be ignored when estimating the costs of such projects. though when visibility was especially good. Continued QA/ QC for post-treatment monitoring was accomplished through SCUBA diver training. This approach also answered a question that was later crucial to determining the duration of monitoring required. Once a goal is established. Approaches to management and eradication of invasive seaweeds Invasive seaweeds are able to establish in a variety of marine environments ranging from relatively placid Figure 2 Surveillance history and presence of Caulerpa taxifolia at Agua Hedionda Lagoon. A similar pattern has been observed in the other C. which was determined by assessing their ability to locate various sizes of plastic ‘‘Caulerpa’’ placed randomly within the search areas. Note: lack of plants was the result of containment under PVC tarpaulins followed by injections of sodium hypochlorite. USA. the decision to eradicate the population was made within two weeks of discovery (Anderson 2005).L. the specific evaluative. 80% was associated with post treatment monitoring. The clarity this brought to subsequent actions facilitated acquisition of resources. what is the minimum size of a ‘‘colony’’ that would be detected 100% of the time in a single multi-diver grid survey even with poor visibility? The answer was between 0. The process is analogous to establishing quality assurance/quality control (QA/QC) requirements for monitoring contaminants (e. taxifolia was considered.g.J. Equally important were routine evaluations of divers’ ability to detect Caulerpa.. By adding an additional year of surveillance for conservative assurance. Anderson: Control of invasive seaweeds 421 decision will drive different efforts with very different expected endpoints. the consistency of their validity and assured objectivity are not trivial matters. in the early discussions of options for dealing with the first US infestation of Caulerpa taxifolia (in Agua Hedionda Lagoon. viz. of the total cost (ca. It also became clear that trying to answer that question by field experiments or ‘‘monitoring growth’’ was not compatible with the process of eradication. taxifolia in Agua Hedionda is shown in Figure 2.W. the likelihood of a missed colony going undetected for two years was virtually nil. and eliminated discussions such as ‘‘What is an acceptable level of growth and occurrence of Caulerpa taxifolia?’’.

a number of containment devices and w102x methods may be needed. Each invasion presents unique constraints and opportunities and. Wright and Davies 2006). jetties. effectively and constructively. In addition. Some of these approaches have been successful on varying scales of infestations in marine systems. Therefore. however. Therefore. Conducting physical (or chemical) manipulations and surveillance in these types of environment pose tremendous logistic problems.. However. they will ultimately also circumscribe proposed management or eradication efforts. Clearly. yet monitoring efforts are minimal whether at points of origin or at recipient habitats. Table 1 summarizes possible strategies and methods for containing seaweed infestations. therefore. At present. Wallentinus 2002. or movable locks. These types of action almost always raise serious social. Miller and Chang 2004. those undertaken most quickly and with least delay from the onset of the infestation generally have been most effective and. socioeconomic and political conditions. taxifolia fragments to prevent spread of colonies was recently demonstrated through modeling of their growth. The importance or urgency of ‘‘containing’’ an infestation. such as physical access and quarantine? Answers to these questions will not only affect containment approaches.W. This is also the case for freshwater ecosystems. rather than a single massive one. poses very difficult problems for containment or treatments. or by judicious removal of propagules (Smith and Walters 1999).g. should be least costly (Rejmanek and Pitcairn 2002). However. For example. The difference in the outcome is as much a function of how the methods are used as in the choice of a specific method. biological. containment is a crucial and integral part of the entire strategy.J. 2005. in the long run. The methods described. Several strategies that have been successfully used for freshwater weed management or eradication could be adapted to marine systems. less than 0. including. potential dispersal capacity must be curtailed immediately as a first response. These species also have a variety of growth forms. complete closure or quarantine of an infested site may be necessary. retaining walls in marinas. The importance of containing (or removing) C. economic. even when discovered early. The cost and probable effectiveness of a given method must be weighed against the risks of not containing the infestation. may have utility whether the goal of the response is long-term management or eradication. and to reduce opportunities for further spread within the site. likely impacts (if known).000 m-2 and that 30 to 45% of newly established stolons in several infested sites were derived from these types of fragments. These may range from simple enclosures (e. .. or dredging. SCUBA or snorkel diving. or at least suggested here. anchoring. rocky substrata with uneven surfaces.g. Due to the patchiness of many infestations. Treatment and control action for management or eradication The following sections describe specific methods for management or eradication of invasive seaweeds. Schaffelke et al. Ceccherelli and Piazzi 2001. rather than quickly attempting a particular management or eradication method depends upon the lag-time from introduction to ‘‘discovery’’. the physical and biological characteristics of an invaded site will very often determine the methods that may be feasible to use. Similarly. having management and eradication tools readily available is essential for adequate responses to these invasions when they are finally detected.. the first and most prudent action will usually be effective containment of the site to allow time for notification of appropriate stakeholders and for initial. and the resources at hand. The modeling showed that multi-seasonal removal of propagules could dramatically reduce the size of infestations. Wright (2005) has shown that fragmented fronds of Caulerpa taxifolia may reach densities of 6. Thus. the most problematic invaded sites are open coastal areas having high-energy wave action. Ribera Siguan 2002. our ability to detect introductions of invasive seaweeds (and most other aquatic invasive species as well) is poor. anchored plastic sheeting) to the complicated installation of large robust structures (e.g. fishing. Large containments would most likely rely on use of natural or existing constructed boundaries such as coves. There are numerous and varied pathways for such incursions. any activities that may compromise containment must be curtailed. as appropriate.422 L. each will require creative problem solving tailored to the prevailing physical. such as Sargassum muticum (Yendo) Fensholt. In some circumstances. and subjected to strong currents. whether through physical containment. and nearly all have been used for control or eradication of freshwater invasive plants. The objective is simple: to prevent movement of viable parts of the invasive alga outside a delineated perimeter. Ruitton et al. Containment of invasive seaweed infestations There are no ready-made products or protocols for invasive seaweed management or eradication. A number of questions invariably arise with any discussion of containing the affected area: Who has jurisdiction of the site? Who ‘‘owns’’ the site? What legal and administrative processes are required to restrict access to the site? Who will be affected by such restrictions and how will communications be handled with these stakeholders? Who has authority to enforce restrictions. legal and even political issues that must be dealt with quickly. the likely rate of spread. Some have been successfully used for relatively small areas (e. rational. cement pipes or metal dikes) to surround the infested site. and certainly in eradication programs. swimming. in most cases. science-based evaluation of the potential impacts or threats from the infestation. boating. coupled with various ‘‘removal’’ scenarios (Ruesink and Collado-Vides 2006. As with all pest control actions. possibly in conjunction with additional solid barriers. groins. and reproductive and dispersal capacities (Zuljevic and Antolic 2000. 2006). Anderson: Control of invasive seaweeds lagoons. bays and estuaries to highly energetic and variable open coastal systems. These potential seaweed ‘‘control’’ actions are separated into containment and treatment approaches.2 ha covered with PVC tarpaulins). seaweeds having pelagic occurrences.

as well as very small multicellular stages. polyethylene sheeting). 2005b). even hand-removal can be effective as with the successful extirpation of Ascophyllum nodosum (L. or where a narrow access channel can be closed off (e. Anderson 2005. solid or fine-mesh material (e. Adequate.L.W. This decreases potential for further disturbance dispersal and isolates site for human activities References/Comments Merkel and Woodfield 2003 (tarpaulins). no references for marine systems Drain or ‘‘De-water’’ site Madsen 2000. Ivesa et al. coarse sand or other dense material. dense material cover: proposed. these systems are typically deployed in relatively placid. Often the systems have to be tailored to specific bathymetric. rigid material. or concrete dikes.g. containment of these reproductive structures during mechanical operations may be impossible under most circumstances. or to cover infested vessel hulls After isolating and sealing the area. The size and mass of these materials would necessitate shipboard hoists and coordinated diver-assisted placement. Cover infested area with adequate depth (thickness) of gravel. trial and error.J. Anderson: Control of invasive seaweeds 423 Table 1 Physical containment methods for invasive seaweed infestations. Sand. but extending to the bottom where the lower edge is sealed with sand or gravel bags. no reference found Isolate by solid perimeter barriers Proposed. Ideally. accessible. lentic environments in contrast to tidally influenced and potentially high-energy wave conditions where invasive seaweeds have become established. burying. nylon or stainless steel. steel or aluminum cylinders could be used for small colonies. table 6 in Madsen 2000). large. This may only be practical in upper tidal zones. no reference found for marine systems Isolate by flexible barrier Madsen 2000 (freshwater systems). containment cylinders could be off-loaded adjacent to the infested areas and later placed where needed Install weighted fine mesh or solid flexible curtains to surround the infestation. Notwithstanding these difficulties. as evidenced by the regrowth of Kappaphycus species in hand-cleared areas of Kaneohe Bay. jagged rocks). CDFA 2000 Prevent movement into/outside and within sites Mechanical These methods consist of various physical manipulations in or around infestations. or other dense materials. Lighter material can be anchored using weights placed near the bottom of the cylinder. polyvinyl chloride. secure anchorage may be achieved using either weighted materials (sand/rock/gravel bags/chains) or metal or fiberglass rods driven into the substrate. sediment-types and logistic constraints on mobility of large pieces of equipment.. Conklin and Smith (2005) point out how difficult it is to manually remove all propagules. either allow tidal flux to drain water or pump out.. no reference found for marine systems Merkel and Woodfield 2003. with the objective of either removing. small harbor or marina) Quarantine site. This method is probably only practical when little or no tidal or currents affect the site. Since seaweeds often produce microscopic gametes and zoospores. when conditions are favorable. 2006). Hawaii. The most effective methods incorporate some means for collection and removal of plant fragments after cutting or dislodging from the substratum. These are similar to oil spill containment skirts. CDFA 1990 (freshwater sites). Practical limitations include size of infestations and the type of bottom contours (smooth sandy or mud bottom vs. but there are nearly always large numbers of viable propagules released.. The difficulty in physical removal is also illustrated in the recurrence of a population of Caulerpa taxifolia in the Croatian coastal harbor at Malinska within two years after it was initially ‘‘removed’’ by pumping (dredging) (Zuljevic 2001. In addition. In deep areas of high surge or surface swells. Alternatively. and redesign.) Le Jolis from a relatively localized infestation in San Francisco w103x . Strategy Cover and isolate infested area(s) with solid or flexible materials Methods and constraints Physically cover infestation with either weighted. Successes of these freshwater mechanical systems can be ascribed to many factors such as the many decades of development. or other dense. flexible. There is a long history of mechanical uses in freshwater plant and algal infestations (e. or simply complete burial (Glasby et al.g. Dispersal of propagules can be reduced somewhat by using floating curtains. or killing established seaweed. material can be gravity-fed through flexible hosing or pipes that allow SCUBA divers to place the material accurately Insert linked steel plates (sheet piling). Conveyor belt transport sys- tems can remove the bulk of cut plants.g. including the substratum.

Therefore. and because it can disperse via fragments as well as numerous microscopic zoospores. The effort took 3 days. As with the US Caulerpa taxifolia project. Campbell and Burridge 1998. the practicality of each method w104x will be dictated by the characteristics of the infested environment (see Dunstan and Johnson 2007) and as well as the morphology and phenology of the invasive seaweed. Confrancesco 1998). its tolerance of cool waters (e. the feeding behavior of Lobiger serradifalci Calcara produces viable fragments of C. To contain the infestation. pinnatifida in the United States (Thornber et al. which sank in Hanson Bay. filiformis. It is also important to note that. and clearly field conditions may influence grazing behavior (Alcoverro and Mariani 2004). mechanical removal) could spread an infestation (Valentine and Johnson 2003. Davis et al. Expanded exploration coupled with adequate host preference testing could yield more candidate agents.424 L.. These were laboratory studies. Thibaut and Meinesz 2000. a shell-less species feeds well on two invasive Caulerpa species. officinalislaced discs. Biological control Although there are several examples of biological control programs for exotic freshwater macrophytes (e. 2001. Four species of sacoglassans that have received most attention as potential agents for control of C. 2002).e. Wallentinus 2002). Anderson: Control of invasive seaweeds Bay. divers removed the two existing sporophytes within days of the sinking. The presence of C. with the sea urchin Helopcidaris tuberculata Lamarck).g. evaluation of these collateral impacts must be thoroughly evaluated in light of any advantages accruing from these ‘‘non-chemical’’ approaches. sea urchins.W. however. due to physical disruption of the benthic habitat by any of these methods. Floc’h et al.. Thibaut et al. New Zealand (Ministry of Fisheries. The most likely candidates for control agents are herbivorous sacoglossan mollusks. with monitoring following for a few months. efficacious. making it ill suited for biological control. (2005) examined feeding preferences in some generalist herbivores. Management of this species is particularly difficult since it can establish on a range of substrata and temperature conditions. Fletcher and Manfredi 1995. introduced agents must be sufficiently host-specific. and Australia (Sanderson 1990. and well-suited to the conditions of their new habitat. 2005). including mollusks. 2004). divers’ search and surveillance transects were carefully planned. microscopic gametophytes) to prevent further release of spores. Coquillard et al. 1996. SCUBA divers performed systematic removal of nearly 5000 sporophytes in monthly efforts spanning 1997–1999 (Hewitt et al. 2000. or Corallina officinalis L. Thus.g. Zuljevic et al. 1985. and further surveillance over a longer period. nodosum ecad mackayi (Turner) Cotton thalli and fragments were physically removed. 2001. Valentine and Johnson 2003). Parma microleptis Gunther. but without fully dedicated funding and long-term wellexecuted programs (probably 5 or more years). Over 170 ‘‘free living’’ A. These authors emphasized the ‘‘low probability that consumers will control these invasive algae’’ due to the low preference for C.J. Argentina (Piriz and Casas 1994. filiformis. thus. in a recent and particularly well-documented southern Tasmanian infestation (Tinderbox Marine Reserve). Another interesting example of using physical (hand) removal for seaweed control are responses to some infestations of the Japanese-native alga Undaria pinnatifida (Harvey) Suringar. Martin and Cuevas 2006) and several European Atlantic and Mediterranean coastal areas as well (Boudouresque et al. Generalist herbivores such as fish may reduce biomass to some degree. and continued to remove sporophytes (produced from attached. Salinas et al. yet did appear to deter consumption in some cases (e. adverse effects on non-target organisms are virtually unavoidable. success is not likely. no successful programs have been reported for marine algae. 2004). As in all approaches using classical biological control. This project also exemplifies the importance of understanding the reproductive biology of target seaweeds. Notwithstanding limitations of mechanical and hand removal methods. Mediterranean Sea) is poor. 2004). For example. However. and fish assemblages (i. Turbo torquatus Gmelin favored the C. 1996). or possibly sea urchins such as Strongylocentrotus droebachiensis (OF Muller) (Secord 2003. removal of sporophytes before releases of zoospores is a strategic action to reduce recruitment. Meinesz 2001). 1996. temperate Asian range over the past 30 years to diverse habits in the USA (Silva et al. The only discouraging aspect of this effort is that over two months passed between the discovery of the infestation and actions taken to remove it. Turbo undulatus Lightfoot (gastropoda) showed a significant preference for Ulva species and Sargassum species and least preference for C. Furthermore. as with any management or eradication strategy. taxifolia are listed in Table 3. Australia (Sanderson and Barrett 1989. 2004). Mexico (Aguilar-Rosas et al. studies of biological control of invasive seaweeds have barely begun.. bagged and disposed at a landfill offsite. When offered mixed diets of live algae.. uifasciata Steindacher and Chromis hypsilepis Gunther). New Zealand in 2000 (Wotton et al. Sumi and Scheibling 2005). but . Compared with research on freshwater exotic weed biological control agents. though Elysia subornata (Verrill). currently. filiformis extracts had marginal effects. The Mediterranean infestations of Caulerpa taxifolia have generated the greatest interest in this approach due to widespread and dense populations (Meinesz 1999. This kelp (Laminariales) has expanded dramatically from its native. 2005). P. so relatively indiscriminate disruption (e.g. There are other ongoing attempts to understand and curtail the spread of U. disturbances of native agal assemblages appear to facilitate its dispersal. However. California (Miller et al. Similarly. Localized heating (708C for 10 min) was eventually used (over one year later) to destroy attached gametophytes. New Zealand (Hay and Luckens 1987). Sanderson 1990. taxifolia. This knowledge was critical in the successful eradication of U. I have listed (Table 2) approaches that are probably most amenable to management or eradication of seaweeds. Marine Biosecurity New Zealand 2001)..g. Some feeding trials employed artificial diets such as agar discs containing extracts of Caulerpa filiformis (Suhr) Hering. pinnatifida on the metal hull of the trawler Seafresh I. In these tests.

Newroth 1979. These methods have been used in freshwater systems to remove Myriophyllum spicatum in Canadian lakes.g. Poorly consolidated substrata may preclude this due to high turbidity generated during dredging Due to scale of equipment. Van Way 2006 (freshwater system). or into holding/settling tanks. hydroraking within contained area Madsen 2000. At this juncture. However. then high.. 2005 may not provide the requisite selectivity needed to differentially reduce problematic invaders. In addition.....g. there are inherent and largely unknown risks with the introduction of yet another exotic marine species (i. but certainly needs to be considered. tomentosoides Van Goor and found that there have been at least two independent introductions from native sources. loosened algae would need to have been removed via suction dredges or diverassisted dredges. Newroth and Soar 1986. the ability of algal species to produce ‘‘repellent’’ compounds has long been recognized and certainly restricts w105x . This is suitable for small to moderate scale infestations (e. deployment and logistics make this costly and complicated. How this might affect host specificity of herbivores is unclear. In order to better select and ‘‘match’’ a potential biological control agent.) Complete drying of site (plus removal of dried seaweed) Proposed for marine systems.. 0. hydraulically powered rotating head with rigid or flexible tines that are directed along the substrate. This has potential for clearing large areas in relatively shallow water. as Secord (2003) correctly points out. it is prudent to move with extreme care and thoroughly investigate not only host-range. or passed through sufficiently fine mesh to retain algal fragments and other propagules.L. and herbivore/host interactions.e. Bugbee and White 2004 (Hydroraking was used in conjunction with herbicides.g. California Department of Agriculture 1990 (freshwater system) Large-scale hydraulic dredging (e. but if it were coupled with transient de-watering or focused heating of infested surfaces. Anderson: Control of invasive seaweeds 425 Table 2 Potential mechanical methods for control or eradication of invasive seaweeds.1–2 ha) that are fairly shallow (less than 5 m depth). lethal temperatures could be achieved quickly in localized areas References/Comments Zuljevic 2001. and nontarget assessments are often limited temporally and spatially. This would probably be done as part of a large-scale containment installation that is sufficient to permit pumping out water behind retaining walls.g. this approach is limited to near-shore areas having adequate storage volume (e.g. floating curtains or solid walls). or where floating barges can receive dredged spoils. These authors used chloroplast microsatellite analysis to determine silmilarities and origins of several invasive populations of Codium fragile spp. a control agent). 8–15 cm diameter dredge opening) Conditions and constraints Dredged material is either pumped onshore. Unless the site can be contained (e. and not suited for rough water conditions These systems usually include an articulated. but also secondary and tertiary effects resulting from new species introductions. this approach will result in spread of propagules and usually creates very poor visibility. (2005). which interferes with monitoring and surveillance Efficacy requires extensive air-exposure for drying and probably removal of sediment containing the seaweed. This approach could also be timed to coincide with extremely low tides if the infestation is limited to the upper tidal zones The high heat capacity of water makes this method problematic. no references found for marine systems. tanks). 30–60 cm diameter dredge opening) Proposed only.. California Department of Agriculture 1990 (freshwater systems) Heated or superheated water/steam Wotton et al. Following rotovation. sea urchins) via augmentative approaches coupled with protective exclosures may offer the most conservative and acceptable opportunities for biological control (Conklin and Smith 2005). Methods Small-scale diverassisted dredging (e.g. However.W. more genetic analyses of invasive seaweeds are needed such as those reported by Provan et al.J. Madsen 2000. though largescale dredging is commonly done in marine harbors and marinas to remove sediment Rotovation. Use of native hebivores (e. power and disposal needed.

benthic Pelagic Pelagic Benthic Tropical/subtropics. Agardh ˚ Coquillard et al. prolifera. Zebrasoma flavescens Bennett. preferred native: Graciliaria coronopifolia J. tomentosoides Turbo undulatus Lightfoot Temperate (SE Australia) Various herbivorous fish: Acanthurus blochii Valenciennes. triostegus L. medium feeding rate Feeds on individual pinnules. stores caulerpenin. 2005 Table 3 Characteristics of some potential biological control agents for invasive seaweeds (modified from Anderson 2002b. 18–26 8–12 Kappaphycus species 12–25 C. C.J. 2001 Thibaut and Meinesz 2000 Thibaut and Meinesz 2000 Conklin and Smith 2005 Scheibling and Anthony 2001. kleptoplasty. poor feeding in warm waters Generalist Sargassum species Generalists. Control agent: (species) Provenance Target species Lobiger serradifalci Calcara (w/shell) Mediterranean Caulerpa taxifolia Elysia subornata Verill (w/o shell) Tropical C. C. -15 is lethal C. Thibaut et al. taxifolia . taxifolia Tripneustes gratilla (L.) (sea urchin) Tropical (Hawaii) Kappaphycus species Strongylocentrotus droebachiensis (sea urchin) Northerntemperate (Nova Scotia) Codium fragile ssp. 2005 Benthic Tropical. Sumi and Scheibling 2005 Incisions on all parts. taxifolia C. C. high feeding rate (10= others) Incisions on all parts. C. Agardh Thallus consumption. 2004. taxifolia Oxynoe olivacea Rafinesque (w/shell) Mediterranean C. Codium as only source did not support gonadal development Thallus consumption Davis et al. low feeding rate Thibaut and Meinesz 2000 Host-specificity (feeding ‘‘preferences’’) Feeding characteristics References Pelagic Direct. veliferum Bloch. stores caulerpenin. Thibaut personal communication 2002). low feeding rate Thallus consumption Pelagic 14–22 Preferred Laminaria species. prolifera (Forsskal) ˚ Lamouroux. Anderson: Control of invasive seaweeds Oxynoe azuropunctata Jensen (w/shell) Tropical C. Chromis hypsilepis Gunther Tropical Sargassum species. Parma microlepis Gunther. taxifolia. Caulerpa species Gracilaria salicornia (C. Dawson. taxifolia 17–25 C.w106x Larval development Optimal temperature range for feeding (8C) 17–25 Incisions lead to holes and fragments.. Agardh) E. T. A. Davis et al. Z. Smith et al. racemosa 17–25. benthic Direct. 2000. C. racemosa (Forsskal) J. taxifolia 426 L. 18–26 Thallus consumption Paul and Hay 1986.Y. hold-fasts.W. taxifolia.

freshwater). There are also some long chain akyl-type algicides. The only systemic herbicide that appears to have been examined for control of invasive seaweeds is fluridone (Anderson unpublished data). Whether longer exposures could kill this or other macrophytic marine algae is questionable. recent introduction. Fluridone inhibits a key enzyme (phytoene desaturase) in the higher plant carotenoid biosynthesis pathway. stolons or rhizoids are protected from chemical exposures by bottom sediments or encrusting epiphytes. Glasby 2004. This approach might be quite useful for localized treatments of invasive seaweeds. though there are very few published reports available. Australia (Creese et al. Symptoms in Caulerpa taxifolia from exposures to these chemicals vary from complete chlorosis and necrosis and loss of integrity (e. USA). In fact. Chemical control Chemicals used for control of plants and algae are called ‘‘herbicides’’.. has been marketed since the mid-1980s for control of susceptible. there are no algicides registered expressly for use in marine ecosystems in the USA (Don Stubbs. and (3) use of freshwater pumped from the Torrens River into saline ‘‘West Lakes’’ in South Australia (Di w107x . since some of these anchoring structures such as rhizoids of Caulerpa species can absorb and translocate nutrients.g. Even for freshwater aquatic weed control... including algicides. It is generally not considered an algicide because it has little effect on most problematic freshwater algae. 1982). Figure 3B. Furthermore.g.g. but fronds may appear to remain intact (e. Algicides are generally considered a sub-set of herbicides that are used to kill or reduce the growth of algae. presumably. Use of freshwater is included since. unless the infestations could be covered first to help retain effective concentrations of the compound. the available active ingredients are quite limited (Madsen 2000. such as changes in oceanic temperature regimes and related population shifts. Anderson: Control of invasive seaweeds 427 the pool of candidate herbivores (e. Carmel. these symptoms appear fairly quickly after a few hours (chlorine) to a few days (copper. but is worthy of further investigation. The pellet formulation sinks to the substratum where it releases the active ingredient over a few days to several weeks. acetic acid). anchored seaweeds may survive treatments if holdfasts. the onset of symptoms is generally earlier. chlorine). and effects are more pronounced at higher doses (e. as amended 1974. acetic acid. However. among those products cleared for use in freshwater systems.W. a kind of ‘‘chemical mowing’’ might be achieved. that is. and ozone (the latter is usually generated on-site). carfentrazone). both in affecting invasive species and. the need for a very long contact time (several weeks) might preclude the use of fluridone in high-energy zones.g. depending upon the formulation. Ceccherelli and Sechi 2002). The variability is due to specific physical conditions within the infested sites. chlorine (in various forms). 2005a). As with most algicides. but these are primarily registered for use as anti-fouling agents in cooling tower systems. Merkel and Woodfield 2003. AERF 2005). triclopyr. diquat. While the physical appearances vary. or other systems where water is recirculated. McConnel et al.D). 2005. ability to achieve adequate contact time. Although contact herbicides would be expected to provide the most rapid control of seaweeds. not algae (e. 2. Thus. if they were suceptible. their potential control agents (Stachowicz et al.J. 2002). However. which are a sub-set of all chemicals used to control or mitigate ‘‘pests’’. Partial chlorosis was observed at the elongating (distal) fronds in small scale tests using explants of C. 2004. registered for use by the US Environmental Protection Agency (and similar regulatory entities in other countries). aesthetic and human-health impacts of freshwater algae and freshwater plants (‘‘aquatic weeds’’).L. they only affect parts of the algae that are directly exposed to the active ingredient. there are several aquatic herbicides. its action is to chemically overwhelm physiological mechanisms that maintain normal osmotic balance in marine algae. chelated copper) to conditions where necrosis and chlorosis occur. 1996. However. endothal. and in some cases. they might also be capable of absorbing and moving systemically active compounds to susceptible points such as active meristematic regions (Williams 1984. Southern California Caulerpa Action Team 2006). particularly with the pelleted (solid) formulation. which contains fluridone. Due to a long history of economic. weedy freshwater angiosperms and is normally used for 6 to 8 weeks at very low doses (6 to 50 ppb).. and acrolein. Field-level efficacy using chemicals has ranged from poor (copper sulfate) to fairly successful (freshwater) to highly effective (chlorine). Glasby et al. fluridone. These active ingredients include copper (both inorganic and organo-chelated forms). many active ingredients are targeted primarily for control of angiosperms (flowering plants). 2002a. loss of integrity (freshwater. 1996. SonarTM (SePRO Corporation. taxifolia that were exposed to 50 ppb fluridone for 12 d (Figure 3G).g. Further complicating this approach is the overall uncertainty of future environmental conditions. 2003). (2) large applications of granular sodium chloride in New South Wales. Chisholm et al. agricultural. more broadly termed ‘‘pesticides’’ (FIFRA. except for products used as marine antifouling boat bottom paints. eradicate these infestations. or surface coatings. A summary of these chemicals is provided in Table 4. the use of chemicals to control seaweeds has been extremely limited both in the USA and in most other countries. I have included some laboratory scale studies as well. US Environmental Protection Agency personal communication 2005).. anchored parts would necessitate continued re-treatments. This strategy is used in both freshwater and terrestrial weed control with soil/sediment-active herbicides. establishment and detrimental impacts of invasive seaweeds have prompted attempts to use chemicals to manage. like high concentrations of NaCl. Freshwater algicides currently registered for use are ‘‘contact’’-type herbicides. Notwithstanding the lack of commercially available marine algicides. but regrowth from viable.C. Probably the three most successful examples to date of field-scale chemical treatments (all to control or eradicate Caulerpa taxifolia) relied on different methods: (1) chlorine (sodium hypochlorite) in the USA (Anderson 2001.4-D. and availability of resources to continue treatments.

5 mg l-1 Osmotic stress. The colonies of C. then liquid sodium hypochlorite (approximately 12% solution) was injected through ports near the top (Figure 3H). killed fronds/rhizoids Burridge and Gorski 1998 Burridge and Gorski 1998 Burridge and Gorski 1998 Sea Nine 211 (Rhom Hass) Salts (NaCl) Freshwater Laboratory U. solid tablets (Trichloro-STriazinetrione) Liquid (sodium hypochlorite) Liquid/CuSO4 saturated textile mats Liquid (copper sulfate solution) Liquid chelate (copper alkanolamine complex) Direct exposure as liquid formulation to Gracilaria salicornia (C. radiata (zoospores) Undaria pinnatifida Effect Kills fronds Inhibition of photosynthesis Killed fronds/rhizoids Killed fronds/some rhizoids Inhibition of photosynthesis. no growth of C. Williams and Schroeder 2004. 2005). The tarpaulins were left in place for the duration of the project. Zostera marina L. It is important to note that both sites in California were in relatively shallow water (2–4 m) and in highly protected areas where natural. Dawson Ecklonia radiata (C. pinnatifida. but only a small proportion was actually infested (cumulatively less than 0. Agardh) J. Huntington Harbor. The Agua Hedionda Lagoon site in Carlsbad. killed fronds Partially effective Killed fronds Negative growth rates References Glasby 2004. E. taxifolia were first contained under PVC (polyvinyl chloride) tarpaulins. radiata Burridge and Gorski 1998 Laboratory/field Laboratory/field Granular (50–200 kg/m-2) Direct contact Creese et al. contained a patchy distribution of colonies over approximately 2. 2004 Glyphosateq Imazapyr Laboratory Glyphosate Diuron Simazine Furanone Laboratory Laboraory Laboratory Little effect on zoospores Little effect Killed gametophyes at )10 mg l-1 Killed gametophytes at )1.W. Smaller colonies found later were treated with solid chlorine-generating tablets and immediately covered with vinyl tarpaulins. California. These applications.J. California was approximately 57 ha. 2004. 2004 Di Fava 2003. localized kill Osmotic stress.2 ha). Smith et al. parts of some tarpaulins were removed in situ and recolonization of benthic organisms was noted.428 L. Anderson: Control of invasive seaweeds Table 4 Examples of chemicals used to control marine macroalgae. 2003 Anderson 2002a. The other USA site. Agardh E. 2000 Creese et al. coupled with intensive post treatment surveillance. Agardh) E. high-energy waves and surge were negligible. sediment core samples were removed from beneath w108x some of the tarpaulins and placed in conditions in a growth chamber that would facilitate growth of viable algal propagules. 2004). even though the uninfested sediments removed from the site supported growth of inoculated fronds (Anderson et al.. In the USA effort. Anderson (unpublished) Thake et al.g. though other benthic fauna and flora (e. No regrowth was observed from any of these cores. Collings et al. Chemical Acetic acid Aluminum Chlorine Site Laboratory Laboratory Field Method of application Liquid/direct exposure Liquid/direct exposure Liquid (sodium hypochlorite solution). Forrest et al.4 ha. As with the removed sediment cores. taxifolia for six years and resulted in successful eradication at the two USA sites (Anderson et .) eventually colonized exposed areas. Y. 2005. but were removed in the seventh year in 2007. Perlich 2004 Laboratory Copper Laboratory/field Laboratory Laboratory Uchimura et al. have eliminated live C. Collings et al. 2004 Anderson (unpublished) Smith et al. 2004 Fava 2003. 2004. several large and small colonies that were discovered in 2000 at two separate locations were first contained under vinyl tarpaulins (sealed along the bottom with gravel-filled bags). Following the assessments of the sediment cores. taxifolia was observed up to five years after initial containment and treatments. Merkel and Woodfield 2003. To assess the efficacy of these treatments.

These authors noted.J. Australia was variable. The decision was made to dilute the water in West Lakes.W. it took nearly four months to dilute and displace the deep layers and w109x . (F) fronds 7 days after initial 90 min exposure to 2% (vol/vol) acetic acid. al. Frond lengths range from 5 to 15 cm.g. 2006. Mesocosm tests with some herbicides (e. South Australia resulted in excellent kill rates of Caulerpa taxifolia where flushing was complete (Collings et al.0 ppm copper (Cutrine Plus) for 8 days. 80 psu) showed that either low (10 to 17 psu) or high salinity should be lethal. The efficacy of salt applications in New South Wales. Southern California Action Team 2006. 65. Anderson: Control of invasive seaweeds 429 Figure 3 Responses of Caulerpa taxifolia to chemical treatments. (H) example of frame and tarpaulin covering used to contain and treat C. hydrogen peroxide) and altered salinity (e.g. This probably restricts the utility of this method to relatively shallow waters where the salt can be directed properly onto the target colonies without too much dilution (Glasby 2004). however. 2004). 25. taxifolia with sodium hypochlorite solution in the California infestations (Agua Hedionda) during 2000 and 2001. Because seawater is denser than the freshwater pumped from the Torrens River. (C) fronds exposed to 1. (E) fronds (on left) exposed to freshwater continuously for 7 days (controls on right). but in several sites complete kill was achieved after 50 to 200 kg m-2 sodium chloride was applied on top of the colonies (Creese et al.. This infestation was discovered in 2002 and consisted of a range of sparse to dense colonies in a fairly narrow tidal-lake system that was amenable to hydraulic control. (G) fronds (left) exposed to 50 ppb fluridone for 12 days (controls on right). copper sulphate. 10. that rates above 50 kg m-2 also resulted in long-term (one to six months at least) negative impacts on some native flora such as Zostera capricorni Aschers. California Department of Fish and Game 2006). (B) unexposed (control) fronds. Other benthic fauna (on sediment surfaces and infauna) were also adversely affected by the higher rates of salt application.35 psu to less than 10 psu.. 2004). Transporting and applying large masses of salt required some specialized equipment and logistic support.L. The replacement of seawater with freshwater in West Lakes. Exposed fronds were maintained at 208C under 300 mmol m-2 s-1 cool-white flurosescent light (L:D 14:10). (D) fronds exposed to 10.0 ppm copper (Cutrine Plus) for 8 days. 17. taxifolia exposed to ‘‘household’’ concentration (5% vol/vol) of sodium hypochlorite for 24 h in sea water. Over 2000 megaliters of water were pumped into the infested site to reduce the salinity from . arrow indicates typical chlorosis symptoms. since a source of freshwater was relatively close (Torrens River). (A) Example of of C.

430 L.W.J. Anderson: Control of invasive seaweeds

to achieve sufficiently low, lethal salinity near the bottom. During the pumping and freshwater exposure period (ca. five months: July 2003 to December 2003) some efficacy sampling was conducted which showed that none of the C. taxifolia exposed to the low salinity was capable of regrowth (Collings et al. 2004). As expected, other stenohaline, non-target organisms were killed as well. However, recovery of these species over time was anticipated, since adjacent areas where freshwater intrusion was limited should have provided sources for recolonization. Figure 3E shows typical symptoms of C. taxifolia resulting from exposure to freshwater. These examples illustrate that site-specific physical conditions (hydraulic, bathymetric etc.) may allow for effective containment and control actions that might not be practical elsewhere. There are also limitations to the effective use of available algicidal chemicals to manage or eradicate seaweeds. The high levels of salts, coupled with high pH of seawater tend to lower the efficacy of inorganic copper products. Such conditions shift equilibria away from the most active, ionic (dissolved and dissociated) forms of Cu toward complexes such as carbonates, which then become less available to enter target algal tissues. This may be overcome partially by using higher application rates, but costs then become restrictive and there may be potential non-target impacts on fish and invertebrates. Recently Arnold (2005) also pointed out that even moderate levels of dissolved organic carbon (DOC, in ranges from 0.5 to 10 mg C l-1) can increase EC50 values for copper for sensitive species and/or stages such as mussel (Mytilus galloprovincialis Lamarck) embryos and larvae. It is likely that under some conditions of moderate to high DOC (or fronds that are laden with detritus or epiphytes), applications of copper will be less effective. Thake et al. (2003) showed the low pH of cytosol in Caulerpa taxifolia tends to retain metals such as aluminum (and presumably copper) in their more reactive ionic form (e.g., Al3q), thus, leading to disruption of photosynthetic electron transport and probably other physiological reactions. These authors reported total inhibition of photosynthesis following exposures of C. taxifolia fronds to 1 mM aluminum chloride. Thus, it is not surprising that in laboratory exposures, chelated copper was lethal to C. taxifolia fronds with exposures of a few days to 1 or 10 ppm copper (e.g., Figure 3C,D). This response suggests that proper formulations of metals may provide a tool for management and perhaps eradication under conditions that permit adequate duration of exposure (Anderson et al. 1982). Interestingly, some higher plants such as the marine angiosperm Poisidonia oceanica (L.) Delile and freshwater angiosperms such as Potamogeton species are far less sensitive to acute exposures to some metals (Al and Cu, respectively) than are target invasive weeds. As Thake et al. (2003) point out, this selectivity might provide a benefit in releasing populations of less susceptible native plants (or algae?) following successful removal or suppression of the target seaweeds. However, studies are needed to ascertain more precise dose/responses of both target seaweeds and desirable plants, other algae, and non-target animals. Table 5 lists several potential aquatic herbicides that may be efficacious against some target invasive seaw110x

weeds. Though there are certainly many other compounds that may affect seaweed growth, only those with prior US EPA registration for freshwater uses were included since these at least have been reviewed for environmental fate and some non-target effects. It is important to note, however, that additional studies on efficacy must be coupled with thorough assessments of environmental impacts, including non-target organisms as well the dissipation and fate of these chemicals in marine ecosystems. Lack of these data is a major impediment to the development of effective chemical controls for invasive seaweeds. Management by resource limitation One could argue that if critical resources for growth were lacking at a given point of introduction (spatially and temporally), then successful invasions would not occur, or at least would be greatly confined (see Dunstan and Johnson 2007). Indeed, Blumenthal (2005) has argued that both responses to increased resources as well as ‘‘release from enemies’’ should be examined when trying to assess the invasiveness of alien plants. He points out that high-risk species include those freed from coevolved host-specific herbivores, pathogens or competitors, and especially risky are those also able to capitalize on newly available resources. Conversely, insufficient light or nutrients, substratum instability (spatial opportunity), intolerable temperature and salinity ranges are obvious conditions that could preclude establishment of seaweeds. Soluble dyes (e.g., Aquashade ) that attenuate photosynthetically active radiation (PAR) have been used to reduce growth of freshwater macrophytes and algae. Unfortunately, light and most other resources are not easily controlled in marine, near-shore environments, or even within lagoons or small estuaries. Tidal fluctuations, shifting sediments and the large scale of marine systems make these approaches impractical under most circumstances. In fact, just the opposite often occurs as a result of development along coastal zones. Construction of marinas and harbors usually provide low-energy, protected areas as well as increased nutrients, while at the same time, serve as entry points from various pathways of introduction (Bax et al. 2002). Some marinas, aquaculture facilities and other engineered embayments could be manipulated to some extent to reduce light availability and restrict nutrient inputs. These strategies require thoughtful design since they must mitigate impacts from runoff, percolation, sedimentation and other nutrient loading sources and pathways. Thus, land use practices must be integrated into an overall management objective. It is clear, however, that for invasive species such as Caulerpa taxifolia, which have low light requirements (Komatsu et al. 1997), deepening most marinas would be impractical, particularly where annual sediment inputs gradually elevate the bottom. Furthermore, since most marinas and aquaculture facilities have large floating surfaces (docks, nets or screen structures) and artificial depth-gradients that span surfaces to the bottom (e.g., pilings, bulkheads, retaining walls), the opportunity for settlement of algal propagules is high, regardless of depth.

L.W.J. Anderson: Control of invasive seaweeds 431

Table 5 Herbicides with potential for controlling invasive seaweeds (WSSA 2002). Herbicide (trade name) Aquathol-K/ Hydrothol 191 Active ingredient Endothall Type C Mode of action Inhibits protein/lipid synthesis, membrane disruption, electron transport uncoupler Photosynthesis inhibitor, lipid peroxidation Photosynthesis inhibitor Cell membrane disruption Free radical generation, lipid oxidation Concentration use range (ppm) 0.5–5 Approximate half-life (freshwater) 3–7 days





90 daysq

Velpar Shark Reward

Hexazinone Carfentrazoneethyl Diquat


0.25 0.1–0.5 0.1–0.37

4–5 months 1–5 days Few h (water), months (soil); binds to clay (biologically inactive) 30 daysq




Photosynthesis inhibitor, lipid peroxidation Inhibits cell division, inhibits cell wall synthesis Disrupts cell membranes (general biocide) Oxidant, general bioside





0.5–2.0 (also soil use at 2 to 6– 10 kg ha-1 active ingredient) 1–15

30–80 days


Acrolein (2-propenal) Chlorine gas, sodium hypochloride


1–4 h

Chlorine (various forms)



1–6 h

C: contact type herbicide; S: systemic type herbicide.

Spatial limits to establishment: Limiting or altering ‘‘suitable’’ space for colonization might be considered as a resource management approach. However, what drives spatial competition among native and invasive seaweeds is poorly understood, and even less known are the physical conditions of benthic environments (shapes, textures, elevations, composition) that would predictably favor a native species over an introduced seaweed. At the extremes, such as loose, unstable sand versus wellanchored rock, exclusion of some species could be achieved, but the problem is, of course, the likelihood of excluding desirable native flora as well. Nutrient limitation: Increases in available nutrients from sediments can certainly support or increase algal population biomass to problematic levels. Lapointe (1997) demonstrated that in some cases, sources of increased nutrients include groundwater discharges, which suggests that improved land-based nutrient management might reduce growth of invasive seaweeds. In studies on Kaneohe Bay, Hawaii, Larned (1998) concluded that nutrient sources in low energy protected sites were primarily benthic, whereas growth at higher flow sites relies on continuous water-column inputs. Stimson and Larned (2000) also reported that efflux of dissolved inorganic nitrogen (DIN) in Kaneohe Bay, which supports abundant Dictyosphaeria cavernosa (Forsskal) Børgesen, was near˚

ly 500 mM m-2 d-1. Pore water levels there were also higher than in less alga-infested sites. In an attempt to assess the role of benthic nutrients and herbivory on species biomass and distribution, Lapointe et al. (2004a) used cages (to exclude or include grazers) placed at increasing distances from high DIN inputs in the Bahamas. They found, using C:N ratios, that biomass was positively correlated with proximity to near shore, high DIN input, but that the composition of species seemed to result from herbivore preferences. In another study in the Florida Keys, Lapointe and coworkers (Lapointe et al. 2004b) showed through analysis of 15N/14N that populations of the red alga Laurencia intricata Lamouroux and the green alga Cladophora catenata (L.) Kuetzing utilized landbased sources of nitrogen. These sources included both large-scale movement from agricultural inputs via the Everglades as well as sewage discharges. They also found a correlation between rainfall events and increased abundance of epiphytic algae on Thalassia testudinum Banks ex Koenig. Taken together, these studies and others suggest that reduction in land-based inputs (e.g., sewage/waste disposal, runoff) could reduce growth of some seaweeds. These are complex problems since they usually encompass effects of large-scale commercial and industrial development, their associated waste-management infraw111x

432 L.W.J. Anderson: Control of invasive seaweeds

structures, as well as increased near-shore private home development. Establishing causal relationships between nutrient sources and observed increases in intertidal and subtidal algal infestations, or increases in algal biomass, can take many years. Reversing these effects can take even longer due to time lags between detection of the nutrient source(s), and implementation of effective alternative treatments. These systems are further complicated if shifts in herbivores occur, which may in turn impede the recovery of native algal populations even after nutrient inputs have been curtailed. Climate change: Further confounding and overriding effects of specific resource availability on the establishment and competitive success of invasive seaweeds, there is now a well-established multi-decade trend in increasing temperature of marine waters (Stachowicz et al. 2002). At least for some invertebrates that have been studied (e.g., acidians), it is clear that the present warming conditions have led to more favorable environments for non-native species compared to native species, and that the critical influences appear to be increased temperature maxima and minima now being experienced at the colonizing sites. Further evidence for the potential expansion of species to formerly ill-suited habitats was provided by Root et al. (2003). These authors showed in a meta-analysis of over 140 studies covering diverse taxa winvertebrates, amphibians, birds, trees, other plants (but not algae)x, that phenological indicators (e.g., onset of reproductive stages) as well as species densities were consistent responses to global warming, particularly in the higher latitudes. Adding more evidence of changing oceanic conditions, Bryden et al. (2005) have recently detected altered circulatory velocities in the northern Atlantic region (Atlantic overturning) that may reduce transport of warm waters to the upper latitudes along European coasts. The net result of all these perturbations seems uncertain, except that benthic organisms would seem to be in line for significantly different future environments. Perhaps there are parallel changes occurring in seaweeds, such as changes in morphology and reproductive modes or timing that foreshadow population shifts. The architectural plasticity exhibited by seaweeds suggests that this is certainly possible (Carruthers et al. 1993, Collado-Vides 2002). How this malleability is manifested in marine communities, including competitive interactions with introduced species, will be interesting to see. Just as alarming, and certainly pertinent to growth of invasive seaweeds, is the increase in atmospheric CO2, which will probably double before the end of this century. How this, and a concomitant reduction in pH and calcium carbonates in marine waters may affect seaweed growth is unsure. It is likely to lead to stresses and reduction in coral cover on tropical reefs (Tanhua et al. 2007, Chem. Eng. News March 16, 2005). Will these changes increase potential habitat for algal species? There is no a priori reason to believe that responses to these temperature and CO2 trends are not occurring in seaweeds, and that tropical species may find suitable conditions in higher latitudes over the next 50 to 100 years. Thus, increases in temperature, coupled with more available carbon (dissolved CO2), regardless of direct land-based nutrient w112x

inputs, could exacerbate the invasiveness of some algal species. Although control and management of invasive seaweeds may be somewhat ameliorated by reductions in nitrogen and phosphorous loads that end up in coastal waters, these approaches will likely be limited to very specific locales, and perhaps, ultimately, be far overshadowed by more widespread global climate and oceanic changes.

Research needs and solutions
Worldwide, pest control is a multibillion dollar industry, with a diverse range of markets that include agricultural pests, domestic and commercial structural pests, aquatic (freshwater) and riparian weeds, rangeland weeds, health related pests, and forest pests. It is not difficult to understand how these markets drive research in private industry as well as in various national, state and local agency programs: there is a tremendous profit motive, and successful production of food and fiber depends on efficient, cost-effective pest control methods. For example, in the USA alone, there are over 300 active ingredients registered as herbicides, but only 9 registered as aquatic herbicides, and about 40 active ingredients registered as algicides, although there are no active ingredients registered for control of marine algae (Don Stubbs, US Environmental Protection Agency personal communication). In addition, there are hundreds of non-chemical devices marketed for weed control in non-marine environments. It is clear that, at least for the last 50 years, the economic incentive for development of seaweed control methods (chemical or non-chemical) has been absent. As noted previously, only products aimed at preventing ship hullfouling organisms seem to have generated private support for research. Simberloff et al. (2005) recently pointed out this disparity between the federal funding levels of research for agriculturally related pests compared to pests that primarily impact natural ecosystems. These authors also point out the lack of consistent funding for control actions that could lead to eradication. The reponses to introductions of Undaria pinnatifida noted earlier illustrate the gaps in both strategic responses to, and adequate resources for mitigating invasive seaweeds. The current situation parallels closely circumstances during the late 1940s and 1950s when freshwater weeds began to cause serious impacts and pose threats in various aquatic sites in the USA and other countries. Recognizing the limits of private industry and the lack of market incentive, USA federal and state agencies, and like entities in the UK, Australia, and Canada developed public-supported research programs to develop new, effective control methods for aquatic weeds (Sculthorpe 1967, Gallagher and Haller 1990, Anderson 2003). Today, public agencies still undertake most of the research and provide technology transfer related to aquatic and riparian weed management. Aside from some significant economic losses to the aquaculture industry such as Codium-impaired production and harvests in coastal Canada (Colautti et al. 2006), invasive seaweeds primarily impact large, natural, open

light.. use of best disposal methods Overload osmoregulatory systems Increase herbivory pressure and impacts Interfere with growth/reproduction Produce lethal conditions. herbicidal and fully integrated approaches for controlling freshwater weeds.J. recovery conditions Ensure specificity Susceptibility to osmotic stress Host-specific herbivores (biological control) Natural product effects (allelopathy) Temperature stresses Susceptibility. fate and metabolism of herbicides in seawater and marine sediments Biotic and abiotic reproductive controls Control strategy Block photosynthesis. inhibit transport. a network of international. Second. there are hundreds of scientists and aquatic plant management specialists who have useful experience with non-chemical (including biological control). there is now considerably more opportunity to adapt current knowledge. replanting options Susceptibilty.g. there is almost no support for private. Thus. mariculture. And. With a multitude of national and state priorities for marine research. canopy) w113x . practices and products used for various freshwater angiosperm and algae control to the management and even eradication of invasive seaweed infestations. lastly. disrupt electrolyte regulation Block dispersal and reproduction capacity Potential method(s) Sediment injection. In the USA. differentially block carbon sources Curtail inputs. aquaculture. First. However. selectivity by isolating heated area Susceptibility of photosynthetic pathways in native algae or seagrasses Differential effects on native algae Identify conditions favoring native algae or seagrasses Light requirements (quality/irradiance)..g. compared to conditions in the 1950s.g. disrupt reproduction Block photosynthesis. translocation ability. nutrient. revegetation methods Susceptibility to osmotic shock. bottom-dwelling fish (e. localized pelleted formulations. carbon sources and carbon metabolism Nutrient responses Interspecies interactions (competition) Deprive essential nutrient(s) Out-compete invader (space. containment and treatment Alter nutrients. it is reasonable to ask how these Table 6 Research needed for development of seaweed management and eradication. private university and stateuniversity affiliated marine laboratories could house programs aimed at a wide range of control research. government or academically based research on control methodologies. alter carbon availability Ability to reestablish natives. EPA. there already is a foundation of specialized equipment. Third. radio frequency heating Burial with various materials.. national and regional scientific societies already exists whose focus is on management of freshwater aquatic plants and algae in a wide range of habitats.. re-planting options. provide conditions/resource for growth Non-target effects Benthic organisms.W. or even on basic studies on the interactions of invasive seaweeds and native communities. alter photoperiod Cutting. environmental safety and utility in control projects. all of which could be evaluated for efficacy. NOAA-Fisheries). uncouple respiration.L. Research area Chemical efficacy. sculpins). hydroacoustics). Research could be supported through in-country (governmental) funds as well as sponsorship through multinational industries (e. Anderson: Control of invasive seaweeds 433 habitats that are usually under governmental stewardship. rotovating.. there are many coastal research facilities throughout the world that already have most of the infrastructure and support systems needed to conduct seaweed control research. aquarium). dozens of candidate herbicides and newly developed surveillance methods (e. chemical exposure (e. sequester nutrients Facilitate space for native growth.g.g. scraping. plant growth regulators). native seagrasses and native algae Native seagrasses and native algae Viability of vegetative structures Prevent dispersal. federal (e. dredging coupled with removal off site Contain and expose to freshwater or hypersaline conditions Augmentative releases (culture and release) Augment biomass of allelopathic (native) species Localized hot water or steam. and which are not directly associated with a highvalue income-generating activity.

Invasions 7: 1003–1016. K. 1: 34039. San Diego. Carlton 2001. ACT. Internatl.W. inadvertent introductions by aquarium hobbyists will probably increase as well.J. 2nd edition. R. during the Clinton administration. FL. 1999.E. A review of aquatic weed biology and management research conducted by the United States Department of Agriculture/Agricultural Research Service. 43: 1–9. California’s reaction to Caulerpa taxifolia: a model for invasive species rapid response. Biological control of killer alga. Anderson. Dechoretz. Marquis-Smith. G. Avila-Serrano and R. L. R. global changes in seawater temperature maxima and minima appear to be allowing range extensions of some sessile species. Anderson. CA: 169–189.434 L. Proc. systematic effort to develop technologies expressly for control and eradication of invasive seaweeds. Aquatic plant management: best management practices in support of fish and wildlife habitat. In the USA. and efficacy of copper in Hydrilla verticillata.. resources could be directed toward developing seaweed control. Buschbaum et al. Aquatic Ecosystem Restoration Foundation. With these increases.W. marine ecology. Anderson. 2000. including phycology. Summary and conclusion The ability to control invasive seaweeds will become more important as both the pathways of introduction expand along with increased ship movements and other near-shore activities. Mooney and K. Paznokas and B. the importance of. Aguilar-Rosas. signed February 3. Mar. Weed Sci. L. G. Arnold. Aquat.R. L. 2005. Key Biscayne. Proc. 2003. Note: arrows indicate the interaction of all critical inputs and knowledge base. Plant Manage. and threat from invasive species was recognized in a Presidential Executive Order No. Caulerpa taxifolia. 2005.W. Mariani. 2006. Anderson. L. as well as a range of effective and safe control and eradication technologies. Australia National Taskforce on the Prevention and Management of Marine Pest Incursions. Control III: 79– 85.W. Integrated Environ. 78. it will be essential to develop well-coordinated national and statesponsored research projects that focus on identifying likely invasive species and habitat characteristics that facilitate invasions. Biol. B. Manage. 2005. First record of Undaria pinnatifida (Harvey) Suringar (Laminariales. Merkel. 1999.J.W.. L. Assess. Sci. Population growth will also bring with it higher land-based w114x . Darmstadt and D. W. 14th Int. and scientists working on freshwater plant/algae management and marine pest management. R. Further compounding these events. Figure 4 provides a simple graphic representation of how these disciplines must eventually interact to provide integrated management and eradication approaches. Posthumus. Tan. Report of the National Taskforce on the Prevention and Management of Marine Pest Incursions.J. or strains that are better suited to the new conditions. Pest Manage. Waters. like seaweeds.J. California Confer.) Specifically. The fact that some early responses to these types of invasions have been successful is particularly encouraging in that there has not yet been any concerted. marine fisheries. 2005. L. Caulerpa taxifolia in the United States: rapid response and eradication program. Anderson. On Aquatic Invasive Species. W. Effects of dissolved organic carbon on copper toxicity: implications for saltwater copper criteria. L. What has been lacking is a strategic plan that truly focuses federal (and state) agency resources and expertise on invasive species.S.W. but some native species as well. Aguilar-Rosas. Alcoverro. Canberra. Caulerpa taxifolia Conf.W.J. 35: 263–269. 2006. 59: 801–813. 2004. 2006). Anderson. Anderson. 1986. Phaeophyta) on the Pacific coast of Mexico. Effect of three formulations of uptake. Caulerpa taxifolia: new marine algal invader in U. 2002a. Over the past eight years. R. on Biol. Woodfield. 13112. Merkel. L. USA: 45–46 (abstract). implementation of that directive has begun to result in ‘‘cross-cutting’’ federal agency budgets that can address particular invasive species needs. Bot. Ecography 27: 361–365.J.J. Bayer. Marcos-Ramirez. W. B. Successful eradication of Caulerpa taxifolia in California through rapid response and team approach. 2004. To meet the inevitable increase in invasion episodes. Walters et al. Woodfield. Conf. a fully vetted review of research priorities could be generated through one or more workshops with participants from several disciplines.W. T.J. Anderson: Control of invasive seaweeds Figure 4 Diagrammatic summary of the key components required for successful response to invasive seaweed infestations. and these will likely include macrophytic algae. 2001. Hoffman. N. and S. Coastal human populations worldwide have been increasing tremendously over the past 100 years and this trend will continue. and this will surely accelerate growth and spread of not only exotic algae. Any such plan needs to provide for a rational risk and benefit assessment as well (Maguire 2004. pp.. nutrient loading in some coastal areas. 47: 255–258. R..J. I have compiled a list of research needs or gaps.W. Ideally. AFFA. and because habitat conditions are changing in ways that will often favor success of new introductions (Thresher et al. Mooney. based upon the kind of information that has been useful in developing technologies for the management of freshwater weeds (Table 6). J. 2002b. References AERF: Aquatic Ecosystem Restoration Foundation. that have not received adequate attention to date. Anderson. Aquatic Invaders 12: 1–6. Use of sediment bioassays to verify efficacy of Caulerpa taxifolia eradication treatments. Patterns of fish and sea urchin grazing on tropical Indo-Pacific seagrass beds. L.

Clonal architecture in marine macroalgae: ecological and evolutionary perspectives. Gorski. 26–39. and L.K. with a description of a new species. Mouret. Jaubert. Kappaphycus spp.R. pp. Jr. Overview and future direction of biological control technology. Thibaut.M.. California noxious and invasive weed action plan. Clout.R. Fungicide. General guidelines for the establishment and evaluation of invasive species early detection and rapid response systems Version 1. History and devlelopment of aquatic weed control in the United States.few. 1987. Gallagher. 2004. 2005. 24 (http://ficmnew.. Nature 438: 655–657. Z. 1998.J. Schaffelke. Colautti. pp. Aquat.K. T. H. A. Amundsen and H. A. Science 310: 243–245. Invas.E. Laminariales) on the South Coast of England. Gueugnot. Response of common SE Australian herbivores to three suspected invasive Caulerpa spp. Australia. McEnnulty. Bot. Weed Sci. Proceedings of the international conference on eradication on island invasives. Plant Manage. M. Grimont and J. pp. pp. Mar. Mar. on Aquat. pp. Rodenticide Act. Rev. B. 49: 379–381.B. Experimental use of salt to control the invasive marine alga Caulerpa taxifolia in New South Wales. Introduced species in U. Gland.L. Laminariales) en Mediterranee. S.J. J. D.. 44: 209–213. Mar. Creese and P. Carlton. P. Tiakina Aotearoa – Protect New Zealand: the biosecurity strategy for New Zealand.L. Collings. Campbell. and R. Chisholm. Cheshire. N. Phaeophyta) 12 years after its introduction into the Atlantic Ocean. 146: 859–868. Cox. Creese. Species: 159 (abstract). Bauckham. Collado-Vides. Dunstan. van Overdijk. Burridge. Caulerpa taxifolia eradication research and monitoring: milestone report to PIRSA marine habitat. July 12. In: (C. 1996. 4. N. Biol.E. 38: 429–438. Culture studies on two morphological types of Caulerpa (Chlorophyta) from Perth. Piazzi. R. pp. Boudouresque. Bot. and C. A. Willing. Tolerance of the invasive marine alga Caulerpa taxifolia to burial by sediment. CDFA (California Department of Food and Agriculture) 2000.W. Hewitt. Modeling 135: 1–16. C.G. 50: 361–372. Bot. CA. A.M. 148: 743–754. Phaeophyta) in Golfo Nuevo. Glasby. eds) Turning the tide: the eradication of invasive species. In Kan’ohe Bay. Cassidy. Man-made marinas as sheltered islands for alien marine species organisms: establishment and eradication of an alien invasive marine species. Eurasian milfoil and water lily in Lake Quonnipaug with herbicides and hydroraking 2002. P. Glasby. D. A. Saier. CSIRO. 1998.. D. Coastal waters: environmental impacts and management priorities. C. Invasions 7: 1029–1039. 1996.M. G. Di Fava. Invas. B. 1993. Buschbaum. Thresher.D. Aquat. Benkendorff and D. Pew Oceans Commission.W. C. Res. Hewitt. G. D. 2005.. 2003. Bot. The use of biocidal agents as potential control mechanisms for the exotic kelp Undaria pinnatifida. 2003.M. as amended 1974. Mar. and T. C. R. 1996. Efficacy of physical removal of a marine pest: the introduced kelp Unda- w115x . Marshall. Mazel and Y. 2002. White.N. Walker and J. Ceccherelli. M.L. Floc’h. G.T. Primary Industries and Resources (PIR) South Australia. C.I.A. ´ Bryden. 2004.M. G.M. E. 16. Ecol. Glasby. Species: 156 (abstract). 1998. pp. Update 7 (September. Australia. 2005a. CRIMP Technical Report No. Mechanisms of invasion: can the recipient community influence invasion rates? Bot. Undaria pinnatifida (Laminariales. Interrelated causes of plant invasion. Bull. Argentina.A. K. 2006. Mar. Dispersal of Caulerpa racemosa fragments in the Mediterranean: lack of detachment time effect on establishment. 2003..few. 82: 71–81. J. P. on Aquat. F.D. -http://www. Control of Cabomba.. and P. Burridge. C. J. 2005. Coquillard. K. Wellington. 2005b. Blumenthal. pp. How an introduced seaweed can affect epibiota diversitiy in different coastal waters. 1985. 38: 355–358. New Zealand Marine Biosecurity: delivering outcomes in a fluid environment. Biol.T.. R. pp. Conservation 122: 573–580. Chapman and B. MacIsaac. Blakemore. Victoria.T. Eradicating and preventing the spread of the invasive alga Caulerpa taxifolia in NSW. Hydrobiologia 326/327: 217–222. Luckens.S. Bugbee. Conf. 13th Int. Slowing of the Atlantic meridional overturning circulation at 258 N. Bailey. California Department of Fish and Game. Campbell. Hill.. Coquillard.J.C. pp.B. and J. J. 64. Fletcher. 27. Westphalen. 2006. CDFA (California Department of Food and Agriculture) 1990. The occurrence of Undaria pinnatifida (Phaeophyceae. Res. Station: 1–18. Rowling and M.T Gibson. 2004. (http://ficmnew. 13th Int. 1996. 36: 49– 53. pp. R.I.S.maf.T. Evol. and amended versions.. Cofrancesco. Longworth and S. New Zealand. Characterised and projected costs of nonindigenous species in Canada. Abundance and spread of the invasive red algae. 2002. The spread and attempted control of the invasive seaweed Caulerpa taxifolia in New South 2001. UK. T.A.R. 1974. Veitch and M.R. Hawaii and an experimental assessment of management options.M. and M. Glasby. Hydrobiologia 474: 57–66. Jones and D. 104. Nutrient availability in the sediment and the reciprocal effects between the native seagrass Cymodocea nodosa and the introduced rizophytic alga Caulerpa taxifoila. A. Ageron. Hayes. Freshw.R. H.. Bot. Ministry of Agriculture and Forestry. Mar. Piriz. 18. J. Hay. 2007. K. R. 25: 329–332. Davis. Huisman.L. Conf.R.G. Pajot and B.L. Cunningham. Vector management tools for invasive marine species: reducing the spread of biofouling pests with aquaculture transfers. Australia.J. 2005. A national early detection and rapid response system for invasive plants in the United States. Nature 381: 382. L’algue japononnasie Undaria pinnatifida (Phaeophyta.N. 15: 531–545. Simulations of the mollusc Ascoglossa Elysia subornata populations dynamics: application to the potential biocontrol of Caulerpa taxifolia growth in the Mediterranean Sea. Haller. Manfredi. Biol.H. Gibson and S. Kay. Occurrence of Undaria pinnatifida (Phaeophyta: Laminariales) in Port Phillip Bay. T. C. J. Ecol. 28.F. J.L.A. Biol.. Freshw.R. E. Amended. Mar. Johnson. Ward.F. 63. Connecticut Agricult. 34. C. control and eradication division of plant industry. 7 USC 136. Dauga. K. 2004. 2004. 56. IUCN SSC Invasive Species Specialist Group. Western Australia. 2005. Smith.M. 1990. Conklin.S.J. Annual report. Exp.J. Hydrobiologia 326–327: 2134–215. Carruthers.L.R. Invasions 8: 45–59. Knoepffer-Peguy. 2005. Switzerland and Cambridge. Murfet. N. ‘Roots’ in mixotrophic algae. Gerbal and M. Theil. Declaration of Caulerpa Eradication/Ceremony/Carlsbad.M. Anderson: Control of invasive seaweeds 435 Bax. Roberston and B. Biosecurity Council. 2006. Forrest. N. FICMNEW (Federal Interagency Committee for the Management of Noxious and Exotic Weeds).L. Phycologia 24: 364–366. 2004. Sechi. C.govt. 36: 589–596.C.. Mar. G. 2006.. Biol. 5: 115–192. Wotton. SARDI Aquatic Sciences Publication RD02/0161–8. FICMNEW (Federal Interagency Committee for the Management of Noxious and Exotic Weeds). S. 2002.. Davis and T. P.R. The Asian kelp Undaria pinnatifida (Phaeophyta: Laminariliales) found in a New Zealand harbor. N. Z. Dodgshun and K. CDFA (California Department of Food and Agriculture). T. 1995. and N. (US) Federal Insecticide. Proc. Ceccherelli. G. and J. M. New South Wales Fisheries Final Report Series No. Arlington Virginia. and J. Parry and R. 2003. and W. Moore.. L. 2000.A. A. J. 2004. 50. 2002. 2001. FIFRA. T. R. Surveys of Undaria pinnatifida (Laminariales. 2003) Information about Caulerpa taxifolia eradication. L. 36. J. pp.

F. Koenigstein). 13th Int. Press. Hewitt. The biology of aquatic vascular plants. 11: 139–148. Reproductive phenology of the introduced kelp Undaria pinnatifida (Phaeophyceae.R and R. Biol.versus phosphorous-limited growth and sources of nutrients for coral reef macroalgae. and R. Hall. pp.. Tasmania: Hobart. Newroth. G. First record of Undaria pinnatifida (Laminariales. Ruesink. Piazzi. and R.. 146: 145–153. M. Occurrence of Undaria pinnatifida in Golfo Nuevo. A pilot project to examine the options for controlling and eradicating the introduced macroalga Undaria pinnatifida.P. Kluwer Academic Publishers.E.. Laminariales) en Asturias (mar Cantabrico). Ceccherelli and F. Undaria pinnatifida (Harvey) Suringar on the east coast of Tasmania. G. Salinas. Soar. C. 2002.A. Invasions 5: 117–131. Mar. N. B. 49. Chem.L. California. Provan. Dept. Switzerland and Cambridge. Chang. S. Buckles. 38. 2004b. 2000. Keppner.C. 2005. and G. pp. Hewitt. Mar Ecol. Modeling the increase and control of Caulerpa taxifolia. eds). Ministry of Fisheries. Casas. Cuevas. and S. Boletin del Instituto Espanol de Oceanographia 12: 77–79.. Scheider. Oxford Univ. J. Scheibling. 1999. 132: 409–421. S. Molecular Ecol.S. What can decision analysis do for invasive species management? Risk Anal. Invasions 7: 251–263. 1999. 2006. Sanderson. pp. and M. Ecol.436 L. impact and management. pp.A. J. Anderson: Control of invasive seaweeds ria pinnatifida in a Tasmanian Marine Reserve.. Lakeline 20: 22–34. Ruitton. Second year status report to SCCAT (Southern California Caulerpa Action Team). an invasive marine macroalga. 1996. Australia. Nutrient thresholds for bottom-up control of macroalgal blooms on coral reefs in Jamaica and southeast Florida. Argentina. Phycol. Croatia) Aquat. Edward Arnold. Invert. Madsen. Nota sobre la presencia de Undaria pinnatifida (Harvey) Suringar (Phaeophyceae. 2003. Pergent and M. tomentosoides. P. Merkel. and J.N. S. Biol. Effects of seconday metaboliites from marine algae on feeding by the sea urchin.S.D. Perlich. L. P. 1979. 18: 529– 541. A prevention program for the Mediterranean strain of Caulerpa taxifolia. Invasions 8: 1399–1402. R. 2001. Advantages and disadvantages of aquatic plant management techniques. When is eradication of exotic pest plants a realistic goal? In: (C. Exumas. Mar.P. Chief Technical Officer. Aquat.L.J. of Sea Fisheries. 2006. B. J. Mar. 249–253. D. 2005.T. P. Kinlan. Meinesz. The ecology and management of nuisance aquatic vegetation. L. Univ. The true tale of a biological invasion. Root. NZ. IUCN SSC Invasive Species Specialist Group. Dordrecht.J. Invasive aquatic species of Europe: distribution. Marine Biosecurity.. A preliminary survey of the introduced macroalga. McConnel. Collado-Vides. 2004a. K.W. Miller. Bot. eds) Turning the tide: the eradication of invasive species. 2001.A. Gollasch and ¨ S. Kakuk. B. Bull. Barile. J. 2001. Shipboard demonstration of chlorine dioxide as an effective ballast water treatment on the M/V Atlantic Compass. 2nd edition. Fish and Wildlife Service. H.M. S. 291–310. Unpublished Report to CSIRO Marine Research. 34. 2001. J. Prog. 42: 1119–1131. 457. Review of non-native marine plants in the Mediterranean Sea. Ivesa.. Ser. Yentsch. Secord. ‘‘Fingerprints’’ of global warming on wild animals and plants. Biol. Argentina. 1990. Lytechinus variegates. P. A. Pitcairn. Piriz.T. J. Fuertes. Pieterse. Culver. Gland.. J. Phaeophyta) in Southern Patagonia. Ecol. Rejmanek. M. Undaria (Undaria pinnatifida).M. 1994. pp.. UK.J. Hobart. pp.M. Llera and C. Vegetation patterns and spontaneous regression of Caulerpa taxifolia (Vahl) C. 2006. 2005. Diversity Distrib. Limnol. Cosentino-Manning and G. Eradication and surveillance of Caulerpa taxifolia within Agua Hedionda Lagoon. Hobbs. 15. A. 2006. Temperature and light responses of the alga Caulerpa taxifolia introduced into the Mediterranean Sea. Jaklin and M. Wellington. 1996. J. J. pp.R. Komatsu.E. Prog. 139: 139–146. Maguire. 1990. Phycologia 44: 84–94.W. Veitch and M. 8: 1437–1453.) and the invasive alga Codium fragile ssp. Tracking the invasive history of the green alga Codium fragile spp. B. Verlaque. Mar. C. Lapointe.C. tomentosoides. Leppakoski. 33: 153–157. California.E. Anthropogenic nutrient enrichment of seagrass and coral reef communities in the Lower Florida Keys: discrimination of local versus regional nitrogen sources. Mooney. 2000. Nitrogen. Ser. 308: 23–58.X. Poll. Feeding. Propagule dispersal and the scales of marine community process.C. Olenin. 2004. Biol. pp. M.M.S. Biological control of marine invasive species: cautionary tales and land-based lessons. Laminariales) in Tasmania. J. Littler and B. growth and reproduction of sea urchins (Strongylocentrotus droebachiensis) on single and mixed diets of kelp (Laminaria spp. B. Barrett.J. Lapointe. Ribera Siguan. Clout. Chlorophyta) invasions along the French Meditteranean coast. O. 2002. Hughes. Biol. Oceangr.R. 1989. Chicago. Cays. Targett and J. 2003. S. Biol.L. Woodfield. 360. Australia. Gainers and S. A. A survey of the distribution of the introduced Japanese marcoalga Undaria pinnatifida (Harvey) Suringer in Tasmania. 1982. 24: 859–868. Chicago Press. Threat to macroalgal diversity: effects of the introduced green alga Caulerpa racemosa in the Mediterranean. London. Newroth. First assessment of the Caulerpa racemosa (Caulerpales. Cinelli. 1998. and C. 17: 12–19.E. 298: 275–301. In: (E. Lapointe. Biol. A. Barile and W. 1997.J. 593. Eurasian watermilfoil management using newly developed technologies. Mar. N. 40: 1028–1031. The University of Chicago Press. Applied Phycology Forum 10: 4. Appl. J. S. Ecol. Anthony. 14: 189–194. Invasions 8: 309–325.E. Australia. Daley. Schaffelke. Meinesz and D. UK. A. and N. J. Bot. w116x .. Phycol. Pounds. pp. Island Press. 2004. New Zealand. Sanderson. Murphy. pp. T. J. 50: 1061–1068.S. A. U. Littler. (Reprinted 1985. pp. Biol. J. A. L.J. Invas. Species: 54 (abstract). Meinesz. 9. M.H. Agardh in Malinska (Northern Adriatic. Matzie.A Maggs. D. K. Lester. 1967. 378. Exp. An introduced sabellid polychaete pest infesting cultured abalones and its potential spread to other California gastropods. M.M. T. 2004. J. 2002. J. Smith and C.. Murphy and C. Ruiz. December 1998. and K. 1986. Invasive species in a changing world. A. T. Larned. Conf. Carlsbad. The relative importance of nutrient enrichment and herbivory on macroalgal communities near Norman’s Pond Cay. 210: 149–159. Introduced macroalgae – a growing concern. Technical Report No.M. Price. Bahamas: a ‘‘natural’’ enrichment experiment. Javel. Plant Manage. 2003. Nature 421: 57–60. Rosenzweig and A. Devescovi. Mar. C. Exp. Killer algae. Killer algae. Proceedings of the international conference on eradication on island invasives. on Aquat. Biol. USA. Ecol. Meinesz..A.D. P. A. 610. 1997. B. Campbell and C. J.Mar. Culioli. British Columbia aquatic plant management program. Koeltz Scientific Books. Sanderson.L.H. Schaffelke. S.. NALMS International Symposium on Applied Lake and Watershed Management 5: 245–251. 2005. 85: 324–330.J.R. Sculthorpe. 118: 391–403. Martin.R.J. Kuris. A new record and eradication of the Northern Atlantic alga Ascophyllum nodosum (Phaeophyceae) from San Francisco Bay. and L.

pp. Demographic feedback between clonal growth and fragmentation in an invasive seaweed. De Agnelis.D. Ser. Appl. Chlorophyta) us Jadranu. Phycol. San deaux. 272: 69–76. and S. Hunter. Kuris. Bot. Windle. Report No. C. 88 (access via http://sccat. Thibaut. Amade. U. 147: 559–569. Valentine. T. Ecol. Mar.L. 20. Stachowicz. Proc. Johnson.C. Thake. Campbell.R. 295: 63–90. 2000. Mar. Campbell. California. Uchimura. Paris. and C. Introduced species policy. J. accepted 2 August. Zuljevic. R. J.H. Agardh (Caulerpales.J. KS. WSSA Publications. Mangialazo. Hewitt. Nat. M. Mar. Synthesis: introduced and cryptogenic species in Port Phillip Bay. Martin.H. 1999. In: (C. Eradication success down under: heat treatment of a sunken trawler to kill the invasive seaweed Undaria pinnatifida. Acad. C. 2006. Biol. D. eds). and L. Phycologia 39: 157–159. Baccou. Kq and Naq for the destruction of Caulerpa taxifolia: Differential effects of photosynthetic parameters. tomentosoides in Nova Scotia.C. Ecol. Front. Thornber. Invasions 4: 333–338. P. J. J. 46: 17–23. Prog. K. Environ. A. Whitlatch and R. Antolic. Potential use of Cu2q. C. 29: 374–379.M. Hill. 81: 343–344.T. Trowbridge. Linking climate change and biological invasions: Ocean warming facilitates nonindigenous species invasions. D. Randone and G. Goddard.. D.F. Meinesz. Williams. 2005. 3: 12–20. 312: 223–234. R. M. 43. D.. Res. Herfort. Stachowicz. T. Thresher and R.L.T. I.C. Cohen. Johnson. J. 2003. Stuart and D. and S.L. Graham and J. Sc. Oceangr. Hewitt and M. Exp.J. Lawrence. Biol. A. Southern California Caulerpa Action Team (SCCAT). Meinesz. Olenin. Mar.M. Zagreb. Mar. S.M. Role of grazing by sea urchins Strongylocentrotus droebachiensis in regulating the invasive alga Codium fragile spp. Anderson: Control of invasive seaweeds 437 Silva.R. C. R. Melnick and Vidal.E.. J. Thesis. management. Ribal. R. M.. impact and management.. A. U. 493. Fragmentation as a strategy for Caulerpa species: fates of fragments and implications for management of an invasive weed. Options for managing invasive marine species. 104: 3037–3042. University of Zagreb. D.K.W. Res. H. 2004. Larned. Charrier. J. Pacific Sci.R. P. Schroeder. Sci. Susceptibility of the invasive seaweed Caulerpa taxifolia to ionic aluminium. Wright. Biol. Ecology of the invasive red alga Gracilaria salicornia (Rhodophyta) on O’ahu. 2004. and C. S.E. and A. Simberloff. Tanhua.R.R. Ierardi.H. tomentosoides on Australian shores. and C. Booth. Hawi’i. 27–52. A. Scheibling. Establishment of the introduced kelp Undaria pinnatifida in Tasmania depends on disturbance to native algal assemblages. A. Pease. 323: 477–488. Eradication of the invasive seaweed Caulerpa taxifolia by chlorine bleach. eds) Marine biological invasions of Port Phillip Bay. Mar. pp. Wotton.. Ecol. Osman. Zuljevic. Wright.J. 252: 159–180. Thresher.A. Marine biosecurity postborder management: developing incursion reponse systems for New Zealand. 2001. R. 58: 325–343. Walters. 2003. Uptake of sediment ammonium and translocation in a marine macroalga Caulerpa cupressoides. 2002. J.H. J. B. Mato. Ser. pp. R.N. 55: 223–230.J. Kinlan. Ecol. Bull. 2000. Sandeaux and J. J. Mar Biol.S. 134. and B. N. 2001. 1999.L. PZSN 1.. L. Ecology 87: 1744–1754.. 292: 203–212. Limnol. 2002. Hobart. Elysia subornata (Molusca) a potential control agent of the alga Caulerpa taxifolia (Chlorophyta) in the Mediterranean Sea. Friis.B. pp. and A. Synchronous release of male gametes of Caulerpa taxifolia (Caulerpales. Biol. Z.L. J. Herbicide handbook. Elloukal and A. Differences between native and invasive Caulerpa taxifolia: a link between asexual fragmentation and abundance in invasive populations. 2007 w117x . L. J. York. Nitrogen efflux from the sediments of a subtropical bay and potential contributions to macroalgal nutrient requirements. 2001.W. pp.. Waugh and D. Squair and C.R. A. 2005.. Biol. 2005.H. and A. Ass..T. C. U. Introduced marine algae and vascular plants in European aquatic environments. Kortzinger. 2004. First report of the Asian kelp Undaria pinnatifida in the northeastern Pacific Ocean. WSSA (Weed Science Society of America). B. C.E.S. S. Invasions 6: 295–300. Fergus. 283–295. M.W. Pojava i sirenje vrste Caulerpa taxifolia (Vahl) C. Freshw. Mar. Mar.. Smith. Nat. Australia. A. M. Valentine. 2005.E. Ecol. 1984.L. Are the Mediterranean ascoglossan molluscs Oxynoe ulivacen and Lobiger serradifalci suitable agents for a biological control against the invading tropical alga Caulerpa taxifolia? C.M. 2005. 2000. Woodfield. Smith. Most. Received 29 December. 1999. Victoria. Acad. I. Ser. C.W. Population ecology of the invasive kelp Undaria pinnatifida in California: environmental and biological controls on demography. 2004. 12: 15–23. Ser.B. P. Wallentinus. T. 2006. E. R. Mar. Kluwer Academic Publishers. 99: 15497–15500. 2002. Leppakoski. C. J.N. Wallace.M. 2006. Zuljevic. 268: 69–80. Prog.L.M. Ecol. 49: 844–849. J. M. Thibaut. Smith. Conklin. 2004. CSIRO Marine Research Report. Thibaut. Terwin. Fish assemblages in habitats dominated by Caulerpa taxifolia and native seagrasses in south-eastern Australia.K. J. Dordrecht.L.B. In: (E. Gollasch and S. Mar. K. Stimson. 38: 553–559. Mar. Establishment of the introduced kelp Undaria pinnatifida following dieback of the native macroalga Phyllospora comosa in Tasmania. Mar.T. Wotton. National management plan for the genus Caulerpa. 2005.J. Parker and P.P. Poll. Exp. Ass.R. O’Brien. CSIRO Marine Research. J. 2004. 81: 497–504. 2007. Proc. T. Harris and J. Fish and Wildlife Service. pp. Progr. Biol. Acad. Freshw. Williams. Thresher. S. ¨ S. Centre for Research on Introduced Marine Pests Tech. and future research needs. Mar.D. Hewitt. Meinesz. Chlorophyta) in the Mediterranean Sea. An estimate of anthropogenic CO2 inventory from decadal changes in oceanic carbon content. Sauvage. and R. Invasive aquatic species of Europe: distribution. pp. T.E.P. 135. 20: 307–319.L. Davis. 2002. T. Sea slug disperses the invasive Caulerpa taxifolia. An assessment of the potential spread and options for control of the introduced green macroalga Codium fragile 8th edition. Final report on eradication of the invasive seaweed Caulerpa taxifolia from Agua Hedionda Lagoon and Huntington Harbour. Ecol Prog. Glasby and B. Ecol. Sumi. Sci. 2000. A. Sci.

Sectoral and selected regional and sub-regional efforts are also highlighted. it should be noted that states such as Australia and New Zealand are recognized as leaders in terms of domestic law and policy responses (Doelle 2003. non-native species. While a comprehensive analysis of law and policy responses at the global and regional level is not possible here. Introduction As demonstrated in a number of the articles in this Special Issue. We conclude with law and policy recommendations. with the terms alien species. we describe key global and selected regional efforts to deal with invasive species to demonstrate the challenge of developing a comprehensive and coordinated response to the threat of invasive species. particularly in relation to intentional introductions. examples of efforts in North America and Europe are offered to illustrate challenges and opportunities for regional responses to invasive seaweeds. Here we provide an overview of law and policy responses to aquatic alien invasive species generally and invasive seaweeds more specifically. In fact. Key global regimes considered include the 1982 United Nations Convention on the Law of the Sea.Doelle@dal. Here we use the terms ‘‘invasive species’’ or ‘‘invasive seaweeds’’ unless the context requires otherwise. As a result. Finally. the scope of the problem only gained widespread attention of law and w118x policy makers in the 1990s. DOI 10. Some of these activities also involve intentional transfer of invasive seaweeds.046 Review Invasive seaweeds: global and regional law and policy responses Meinhard Doelle*. In section 2 we point out that at least two global regimes provide an international framework for States to take action preventing the introduction and spread of aquatic invasive species. McConnell and David L. more difficult regulatory problems posed by unintentional pathways for species transfer and introduction. aquaculture. law and policy efforts have tended to be generic and focused on managing pathways rather than on the problems posed by particular species or organisms. Although concern about the issue of introduction of alien species was evident in the late 1970s. e-mail: Meinhard. aquaculture. climate change. On the aquatic side. Moira L. attention appears to have been focused more on intentional introductions of fish species and on specific sectoral pathways or vectors for the unintentional transfer of these and other species including pathogens. Halifax. Contributions from the Food and Agriculture Organization and the International Maritime Organization are also considered in the global context. and the opening of new canals and waterways. invasive species pose almost incalculable economic. Similarly. Concern about invasions is not limited to biodiversity per se but extends to its broader socio-economic impacts on agriculture. Dalhousie University. the Ramsar Convention and the Bonn Convention on Migratory Species. most notably the need to approach the issue of invasive seaweeds in a manner consistent with the precautionary principle. regional. the 1992 Convention on . Although these efforts in part impact on the problem. precaution. habitat loss. forests. B3H 4H9. viz. national responses are not considered. fishing activities. At a regional level. fisheries. VanderZwaag Marine & Environmental Law Institute and Dalhousie Law School. and has taken the form of border control or quarantine measures. Keywords: global. we do not attempt to distinguish between various species but simply use the term ‘‘seaweed’’. and other human activities dependent on the stability of living resources in a particular ecosystem.1515/BOT.2007. the aquarium trade. socio-cultural and human health security risks. As explained in the other articles in this Special Issue. often interchangeably. such as seaweeds. non-indigenous species. and alien invasive species are generally considered to top the list of biodiversity threats. To date. 2004). 2004). In the process. however. NS. the Convention on Biological Diversity. However. the introduction of alien invasive species poses one of the most serious threats to both terrestrial and marine biodiversity. We are primarily concerned with the. Most of the effort in policy development to date has been on terrestrial invasive species.Botanica Marina 50 (2007): 438–450 2007 by Walter de Gruyter • Berlin • New York. the fragmented nature of the response at the global and regional level is exposed. or harmful aquatic organisms used. invasive seaweeds nevertheless pose a serious threat in the context of unintentional transfer and introduction through * Corresponding author Abstract We consider law and policy responses to invasive seaweeds at global and regional levels. Hewitt et al. arguably. Estimates of the cost of responding to this problem around the globe vary widely. alien invasive species. terminology varies greatly in both law and academic literature on this topic. law and policy. Canada. 1. One estimate of the cost to the US economy is US$137 billion per year (Murray et al.

including invasive seaweeds.’’ 2. directly or indirectly. The implications of building a national response on these principles are explored in the last part of this article. devotes just one article specifically to the problem of ‘‘introduction of species.1. Consistent with precaution. The 1971 International Convention on Wetlands of International Importance especially as Waterfowl Habitat (Ramsar Convention) and the 1979 Convention on Migratory Species of Wild Animals (Bonn Convention) tangentially aim to curb the introduction of alien species in the context of specific area and species conservation. This article is. The two main sectoral responses at an international level to the problem of transfer and introduction of invasives as an unintentional consequence of ships’ operations (ballasting and hull fouling) and fisheries and aquaculture are also outlined. as yet. hazards to human health. UNCLOS imposes a general duty on all States to protect and preserve the marine environment (Article 192). Firestone and Corbett 2005). alien or new. the date of submission of this article. in most cases very costly and. control and containment are risky at best. precaution and prevention rather than eradication or containment or control is the way to deal with activities that are likely to be a vector or pathway for the introduction of invasive species. or the intentional or accidental introduction of species. of substances or energy into the marine environment. in many cases. the only effective defense against invasions: eradication. on Parties to UNCLOS to take steps to address the problem of transfer and introduction of alien or new species into the marine environment is clear. ineffective. Article 1 of UNCLOS defines ‘‘pollution of the marine environment’’ as: ‘‘(4) w«x the introduction by man. Global responses to invasive organisms such as seaweeds While numerous international instruments and institutions are concerned with invasive species (McNeely et al. which. we would like to emphasize that the materials are current up to 10 January. 2. UNCLOS. General legal framework Considered the ‘‘Constitution of the Oceans’’. Doelle et al. Article 196(1) states: ‘‘States shall take all measures necessary to prevent. based on the view that the harm arising from this problem. addresses the issue of State obligations to protect and preserve the marine environment from pollution from both land and ocean- Although this distinction may have some implications for national level regulatory responses. threatened or endangered species and other forms of marine life from all sources of pollution wArticle 194(1) (5)x (Firestone and Corbett 2005). 2001). which results or is likely to result in such deleterious effects as harm to living resources and marine life. to a particular part of the marine environment. or whether this constitutes some other category of environmental harm (McConnell 2002. and shipping. impairment of quality for use of sea water and reduction of amenities. including estuaries. Four main global agreements The four global agreements of special relevance to controlling invasive marine species fall into three sub-categories.1. reduce and control pollution of the marine environment resulting from the use of technologies under their jurisdiction or control. including both socioeconomic and biodiversity impacts and costs. An overview of regional responses set out in section 3 is followed with a generic discussion of what could be done at the national level to implement the principles developed internationally as the basis of an effective response to the threat. there has been a general recognition internationally that prevention is the best and. which may cause significant and harmful changes thereto. It proposes the adoption of a precautionary and integrated approach to regulatory design and implementation at a national level to address the problem of invasive species.’’(emphasis added) There has been some debate as to the precise meaning of this provision. with its 320 articles and nine annexes. this chapter briefly discusses four of the main global agreements targeting invasives and highlights sectoral attempts by the Food and Agriculture Organization (FAO) and the International Maritime Organization (IMO) to address the problem of introductions of alien species in the contexts of fisheries and aquaculture. based activities. under Article 196(1). The question is whether on a strict reading it can be interpreted as meaning that the introduction of potentially harmful alien species is pollution of the marine environment. including fishing and other legitimate uses of the sea. hindrance to marine activities. the part that deals with preservation of the marine environment. respectively. this problem needs not be replicated at a national level. which is found in Part XII of UNCLOS.: Law and policy responses to invasive seaweeds 439 Biological Diversity (CBD). In cases of doubt. therefore. 2. provides the general legal framework for addressing the problem of marine invasive species.1. Note: As the law in this area is constantly changing. alien or new’’. the obligation. inter alia. which may cause pollution or significant and harmful changes to the marine w119x .M. The 1992 CBD casts a wide net to address the impacts of introduction of ‘‘alien species’’ warticle 8(h)x on broad biodiversity protection. 2006. are such that prevention-oriented strategies are the best regulatory approach. Precaution has emerged as a key principle in the response to the problem of invasive species at both the global and regional level. We argue that even though the global and regional law and policy responses are. neither comprehensive nor coordinated. This obligation includes a duty to prevent pollution of the marine environment and to protect and preserve rare or fragile ecosystems as well as the habitat of depleted. particularly in connection with international shipping. UNCLOS. An environmental impact assessment requirement is also set out in Article 206 for activities. more often than not. In addition to this specific provision on species introduction. and the 1982 United Nations Convention on the Law of the Sea (UNCLOS).

Inadequate national implementation of international obligations and limited national capacity were identified as key impediments for addressing the introduction and spread of invasive alien species (paragraphs 17. States shall take all measures necessary to ensure that activities under their jurisdiction or control are so conducted as not to cause damage by pollution to other States and their environment. Technical and Technological Advice 2005). The Convention also establishes a continuing obligation for States to protect and preserve the marine environment through global and regional cooperation. standards and recommended practices and procedures consistent with this Convention. they shall. which might be the foundation for filling regulatory gaps in addressing invasive seaweeds. Article 8(h) calls on Parties to ‘‘prevent the introduction of. Article 194(2) includes an obligation regarding protection of the environment of other States. habitats or species. States would be urged to develop joint contingency plans for responding to seaweed invasions (Article 199). Biodiversity protection The CBD. met in New Zealand in May 2005 and issued an informative report (Subsidiary Body on Scientific. the CBD can be seen as building upon and elaborating the State obligations set out in UNCLOS concerning conservation and preservation of the marine environment. Habitats or Species). as they are described Similar wording as to state responsibility is found in Article 3 of the CBD. on a regional basis. in 1998 adopted a program of work with one of five thematic areas being devoted to invasive alien species (CBD Secretariat. taking into account characteristic regional features.’’ To the extent that it deals specifically with marine biodiversity. and that pollution arising from incidents or activities under their jurisdiction or control does not spread beyond the areas where they exercise sovereign rights in accordance with this Convention. assess the potential effects of such activities on the marine environment w«x. the Guiding Principles urge a three-stage hierarchical approach involving prevention as a first priority. control or eradicate those alien species which threaten ecosystems.’’ in the CBD (and in later discussion. 2. through an Annex (Guiding Principles for the Prevention. For example. Article 22 (2) of the CBD specifically notes this relationship: ‘‘Contracting Parties shall implement this Convention with respect to the marine environment consistently with the rights and obligations of States under the Law of the Sea. Firestone and Corbett 2005). The AHTEG emphasized the need for capacity building efforts including technology transfer and training in relation to invasive species. the Group initiated discussions about the numerous legal issues including how to define damage to biological diversity and how to value damage to biodiversity (CBD 2005). The Expert Group noted that liability regimes for damages caused by invasive species may be an important issue and recommended that the issue be raised at the Experts Meeting on Liability and Redress under the Convention scheduled for October 2005.’’11 States might also be obliged to notify other States of the potential for invasive seaweeds to cause transboundary damage (Article 198).1. for the protection and preservation of the marine environment. has one provision specifically aimed at addressing the issue of introduced invasive species or alien species. in Decision VI/23 (2002) on alien species that threaten ecosystems. undated).: Law and policy responses to invasive seaweeds environment. 2 w120x . then numerous other UNCLOS provisions would apply (McConnell 2002. This language may capture intentional introductions of seaweed for cultivation: ‘‘When States have reasonable grounds for believing that planned activities under their jurisdiction or control may cause substantial pollution of or significant and harmful changes to the marine environment. the COP urged Parties to develop national invasive alien species strategies and action plans and to develop regional strategies where appropriate. having agreed in 1995 to a program of action called the Jakarta Mandate on Marine and Coastal Biological Diversity. The use of the term ‘‘may’’ emphasizes the need to take action where a material risk is indicated. An Expert Group has linked this obligation to invasive species (Subsidiary Body on Scientific. 35).’’ It may also have implications for assessing the effect of any approaches adopted to address unintentional introductions. Technical and Technological Advice 2005). ‘‘Article 194 Measures to prevent.2. established at the request of the Conference of the Parties in Decision VII/13 (2004).’’ If indeed introduction of alien species (under Article 196) can be considered a form of pollution. States would have an obligation to ensure that alien species that may/can harm do not spread beyond areas of national jurisdiction wArticle 194(2)x. setting out 15 guiding principles for the prevention and mitigation of impacts of alien species. in formulating and elaborating international rules. calling for preventative and precautionary approaches to addressing the causes of biodiversity losses. Besides embracing the precautionary approach and ecosystem approach for dealing with invasive species. The program of work has become a ‘‘living tree’’ spawning numerous initiatives to address the threat of introduction of alien species to ecosystems. as appropriate. reduce and control pollution of the marine environment w«x 2. Article 197 provides: ‘‘States shall cooperate on a global basis and. States might also be liable for transboundary invasions of invasive species (Article 235). followed by eradication and containment. For example. as far as practicable.2 The Group of Legal and Technical Experts on Liability and Redress in the Context of Paragraph 2 of Article 14 of the Convention. The Ad Hoc Technical Expert Group on Gaps and Inconsistencies in the International Regulatory Framework in Relation to Invasive Alien Species (AHTEG). Doelle et al. met from 12 to 14 October 2005 in Montreal and while finding it premature to recommend development of a liability protocol. The Decision also adopted.440 M. 1 The Conference of the Parties (COP). directly or through competent international organizations. Introduction and Mitigation of Impacts of Alien Species That Threaten Ecosystems. habitats or species. ‘‘marine alien species’’).

2.2. Article 9. especially for deliberate introductions of species. where a risk assessment approach is followed and w121x . Range States (of a migratory species listed in Appendix I as endangered) are required to endeavor: ‘‘To the extent feasible and appropriate to prevent. urged Parties to: prepare inventories of alien species in wetlands. Iran in 1971 and has been amended by two Protocols (in 1982 and in 1987) (Ramsar Convention 1971). urged Parties to: undertake risk assessments of alien species which may pose a threat to the ecological character of wetlands. The Convention establishes quite general obligations on Parties in relation to invasive species. Appendix II). For migratory species listed in Appendix II.1 urges States to minimize the harmful effects of introducing non-native species or genetically altered stocks used for aquaculture. Appendix I) and listed migratory species having an unfavorable conservation status or which would significantly benefit from international cooperation (Bonn Convention. the Guidelines proceed to suggest moderated versions of the precautionary approach. adopted at the 7th Conference of Contracting Parties in 1999.1. and.1. Article 12 calls for strengthening national research capacities and for assessing the impacts of environmental changes on fish stocks and aquatic ecosystems. reduce or control factors that are endangering or are likely to further endanger the species.M.3.8 urges States to protect and rehabilitate all critical fisheries habitats in marine and freshwater ecosystems. and cooperate in preventing and controlling transboundary invasions including those in shared coastal/marine zones (Ramsar Conference 2002). a non-binding document setting out principles and standards for fisheries and aquaculture practices.: Law and policy responses to invasive seaweeds 441 The AHTEG urged Parties to take seriously their responsibilities under Article 3 of the Convention. Doelle et al. The Code may. Perhaps of greater relevance in addressing invasive species than the Code of Conduct itself is the development of the non-binding Technical Guidelines on the Precautionary Approach to Capture Fisheries and Species Introductions (FAO 1996). The potential impact of invasive seaweeds on the ecology of habitats of protected species would raise concerns relevant to this obligation. regarding the use of alien species in aquaculture or in relation to the problem of transfer of invasive species through ships. Pursuant to Article III (4)(c) of the Convention. as were other potential pathways for the introduction of invasive species including scientific research. establish control and eradication programs. review existing legal and institutional measures relating to invasive species control. Various export controls were listed as examples.2. It directly addresses the introduction of non-native species only in the context of aquaculture and intentional introductions. be relevant to the issue of intentional and unintentional introductions of invasive seaweeds through its general habitat protection and research exhortations. In particular agreements are encouraged to include provision for protection of habitats from disturbances. through Decision VII/5 (2004) on marine biological diversity. that is.’’ ‘‘Range States’’ are defined in the Convention to include states that exercise jurisdiction over any part of the range of the migratory species and states whose flag vessels are engaged outside national jurisdictional limits in taking the migratory species. It committed Parties to establish nature reserves on wetlands and to include at least one wetland on the List of Wetlands of International Importance.3. After noting in paragraph 104 that a strictly precautionary approach would not permit deliberate species introductions and would require strong measures to prevent unintentional introductions. recommended that Parties use native species and subspecies in aquaculture. or a similar code. adopt legislation and programs to prevent the introduction of ‘‘new or environmentally dangerous alien species’’ (Ramsar Conference 1999). exotic species detrimental to the migratory species’’ wArticle V(5)(e)x. The 1979 Bonn Convention is aimed at protecting endangered migratory species (Bonn Convention. not allowing activities within their jurisdiction or control to cause damage to the environment of other States or areas beyond national jurisdiction. Specific area and species conservation The Ramsar Convention was signed in Ramsar.3 proposes that States adhering to the Code consult with the neighboring States before introducing non-indigenous species into transboundary aquatic ecosystems. or controlling or eliminating. It has largely addressed the issue of invasive species. The FAO and invasives in the fisheries and aquaculture sectors The FAO has accepted a Code of Conduct for Responsible Fisheries (FAO 1995). ‘‘including strict control of the introduction of. While the COP. Resolution VIII. including strictly controlling introduction of. tourism and the aquarium trade. already introduced exotic species. the Guidelines suggest ‘‘controlled introductions’’ where proponents of introductions shall be required to demonstrate caution through following the non-binding ICES Code of Practice on the Introduction and Transfer of Marine Organisms. including notifying potential importing countries about particular species that may be invasive and prohibiting the export of some species.14 on invasive species and wetlands. Rather than prohibiting intentional new species introductions. Article 9. including transboundary impacts. or control of already introduced. The Guidelines equivocate over what a precautionary approach should mean to species introductions. through hortatory resolutions.18. where necessary. identify the presence of invasive alien species in wetlands and for listed sites to report to the Ramsar Bureau the nature of the invasion. however. Range State Parties are encouraged to conclude Agreements to restore or maintain migratory species at a favorable conservation status. The AHTEG highlighted the many specific gaps and inconsistencies in the international regulatory framework. Resolution VII. Global sectoral initiatives 2. 2. 2. Article 6. the Expert Group noted there are no specific binding international requirements addressing impacts. The exclusion of certain ships from IMO regulatory treaties was also viewed as a gap. adopted at the 8th Conference of the Parties in 2002. fouling of ships and on other equipment and vessels.

2. are transferred between countries in other ways related to ships’ operations. the ship’s sea chest (Cawthron 2004). It can be seen as a specific delineation of State obligations under both UNCLOS and the CBD.’’ wemphasis addedx This vector will be partly regulated at an international level by the BWM Convention 2004. discussed in the next section. albeit on board a ship. along with ballast water. or biologically contaminated fishing gear. the most significant vectors for seaweed NIS appear to be: 1) aquaculture w«x. developed by the IMO member States. Concerns have been expressed about these other unintentional or operational vectors in various fora. such as invasive seaweeds. and as codified by UNCLOS. It is an important step forward in addressing concerns about the introduction of potentially harmful organisms (including invasive species) by transport in ballast water and in sediment in the bottom of ships’ ballast water tanks. cargo packaging and loading equipment. 2) shipping. by ballast water discharge. commensurate with the severity of potential adverse impacts’’ (paragraph 129). For unintended introductions. aquarium trade. in that it includes more coastal State responsibilities and rights in the regulation of this sector. be seen as complementary to the international obligations in the Anti-fouling Convention. the associated Guidelines for implementation (IMO. 1. The BWM Convention 2004 is based. Doelle et al. This approach can. may create hazards to the environment. on a 1997 Resolution of the IMO General Assembly. more commonly known as MARPOL 73/78. 2004. property or resources. or into fresh water courses. As the foregoing quote indicates.’’ The BWM Convention 2004 is one of the newer generation of IMO regulatory Conventions. human health. paragraph 8. either as targeted species or as unintentional hitch-hiker associates w«x Besides canals and waterways. A. attaching to the anchor and other parts of a vessel as well as cargo. Section B. These may be considered. 2) aquaculture enterprises. 2) noted that: ‘‘w«x the major pathways or vectors of introducing marine NIS wnon-indigenous speciesx into non-native waters are: 1) shipping transport. w«x Seaweeds appear to be much less likely than other marine NIS to be introduced through the discharge of ballast water but are very likely to be moved along the coast as fouling organisms on ships’ hulls or other marine gear. These include attaching to the ship’s hull (a process called fouling).442 M. is under the auspices of the IMO. for example. This involves a combination of initial and on-going compliance inspections. 868(20). Guidelines 2004). 4 A ‘‘flag State’’ is generally the State in which a ship is registered (although a ship can be on more than one registry. 3 This comment highlights a regulatory gap. A recent study of invasive seaweeds on the Pacific Coast of North America (Murray et al. However. either in ballast water or as hull fouling organisms. it can only fly one flag at a time). 5 w122x . as distinct from intentional transfers of alien species. to meet its mandate of securing ‘‘safer shipping and cleaner seas’’ by regulation of the shipping industry through the implementation of standards for many of the flag State obligations found under UNCLOS (Articles 91.: Law and policy responses to invasive seaweeds pilot/experimental introductions supported. as: ‘‘w«x aquatic organisms or pathogens which. Regulation B-3). States often have a ship owning/regulation interest (flag State) and a coastal State interest (coastal and marine environment and resource management) and a port State role (a specific regulatory/enforcement role vis a vis the other two interests). coastal zoning and alternative discharge options. certification. It is implemented through a multifaceted phase in system for the standards linked to the date of construction (before or 2009 or 2012) and the size of the ship’s tanks (Annex. The Guidelines also suggest the development of an accessible database on ballast or fouling organisms that have an impact upon fisheries and the creation of a network of experts charged with identifying introduction problems and areas of impact (paragraph 131). largely related to the dynamics of international institutions and lawmaking. a ‘‘flag State’’4 has the primary responsibility for regulating the operation of ships flying its flag. The Guidelines encourage the development of effective non-biocidal antifouling paints or treatments to reduce the risk of introduction from ship fouling (paragraph 137). and.5 The regulatory system set out in the BWM Convention 2004 adopts the formula that is now well established in many Conventions developed by the IMO to help prevent many different ship-based sources of marine pollution. impairment of biological diversity or interfere with other legitimate uses of such areas. The IMO and the regulation of shipping as a vector for invasive species Shipping has been recognized as one of the primary vectors for the national and international transfer of ‘‘harmful aquatic organisms’’. potentially harmful organisms. This Convention. which are defined in Article 1. It is part of a web of regulatory Conventions. pp. 94). in part. mostly as fouling organisms attached to hulls and other ships’ parts. On the ratification by 30 States whose combined merchant fleets constitute not less than thirty-five percent of the gross tonnage of the world’s merchant shipping fleet. in part.2. but so far there is no specific international regulatory develThe term ‘‘coastal State’’ is a shorthand term usually used to refer to the interest of a State in protecting its coastline and resources in the waters under its jurisdiction. which took many years to negotiate. to adopt and implement national laws to address this problem. Under international law. as unintentional transfers in the sense that they are by-products of the operation of shipping. discussed above. irrespective of where they operate in the world. It means that not all aspects of shipping that can serve as vectors for the unintentional introduction of harmful organisms are regulated under the BWM Convention 2004. of the International Convention on the Control and Management of Ship’s Ballast Water and Sediment 2004 (BWM Convention 2004). it is suggested that it may not be an effective regulatory response to either prevention of or reducing the risk of spread of invasive seaweeds by ships. 2. such as the International Convention for the Prevention of Pollution from Ships 73/78. when it comes into force3. Guidelines for the Control and Management of Ships’ Ballast Water to Minimize the Transfer of Harmful Aquatic Organisms and Pathogens. the Guidelines recommend that authorities should ‘‘establish regulations to reduce these risks. if introduced into the sea including estuaries. when finalized.

The BWM Convention 2004. These guidelines are being evaluated by the National Introduced Marine Pest Coordination Group for implementation in either a voluntary or regulatory framework.. By way of introduction. Doelle et al. however. this section considers regional efforts to respond to the threat of invasive species.6 For example. it can be an important component to ensure the effectiveness of international regimes. be an effective response. Chatham Islands and transiting to Fiordland (South Island). Asia and the Pacific. may. Invasive Alien Species. surface. such as seaweeds that attach to the exterior of the ship and its equipment (hull fouling). Technical and Technological Advice 2005. commercial fishing. passenger cruise. perhaps ironic. In addition. Instead. New Zealand has developed a Voluntary Code of Practice for vessels departing the two main Islands for the sub-Antarctic Islands. may result in increased fouling of ships and the subsequent transport of non-indigenous species. In addition. It is important to recognize that there are regional efforts to address invasive species in most regions of the world (McNeely et al. petroleum and slow moving barges) to underpin a risk evaluation has commenced. Port area authorities are expected to identify and warn ships of areas where ballast should not be taken up or discharged.: Law and policy responses to invasive seaweeds 443 opment. and to adjoining countries. or devices on a ship to control or prevent attachment of unwanted organisms. to the extent that seaweeds are transported and introduced through ballast water and sediment discharges. paint.2. the regional approach has the advantage of allowing law and policy responses to be tailored to the unique circumstances of each region.2) will also include coastal/ port responsibilities. it is not yet entrenched as an acceptable port or coastal State practice under a specific international agreement. and given the regional nature of the problem in many respects. to avoid the spread of species along the coastline within a country.’’ 6 pathogens. as well as any particularly sensitive areas or activities. This may then result in use of less effective surface treatments and increased hull fouling and risk of transport of organisms such as invasive seaweeds. In comparison to global efforts. However. and SBSTTA/6/ paragraphs 20–22. the Convention’s Guidelines (IMO. 20 December 2000. over time. although it could perhaps be supported on the basis of more general UNCLOS or CBD obligations to protect the marine ecosystems. infestations or known populations of harmful aquatic organisms. Options for Future Work.7 3. and West Asia. 2001). concern has been expressed in the Report of the AHTEG meeting. The Workshop was proposed by a member of the US Navy. Naval Surface Warfare Center and a member of the USCG Environmental Standards Division. the International Convention on the Control of Harmful Anti-fouling Systems on Ships 2001 (Anti-fouling Convention)..g. SBSTTA VI/8. The need to raise the issue with respect to the United Nations openended Informal Consultative Process on Oceans and the Law of the Sea (INICPOLOS) was also noted at paragraph 70(g). It also allows States within a region to cooperate in the absence of global consensus. once it comes into force and is implemented at a national level. e. a comprehensive research program examining hull fouling across all international vessel sectors (recreational. Furthermore. Even where this may not be a viable regulatory response for all vectors. The Anti-fouling Convention is aimed at eliminating harmful biocides such as tributyl tin (TBT) used in the coating. complication in connection with the transport of invasives. More recently. it is worth considering the effectiveness of regional efforts to deal with aquatic invasive species generally and invasive seaweeds more specifically. 7 w123x . to address the issue in connection with the Antarctic Treaty area. The process of identifying the ‘‘harmful aquatic organisms’’ in or near coastal and port waters can be taken into account in evaluating ‘‘risky ships’’ by the next port. surface treatment. regional efforts in North America and Europe are used to illustrate what has taken place to date.g. A further. discussed elsewhere in this article (Subsidiary Body on Scientific. McConnell 2002). Comparative regional coordination and cooperation In the absence of a comprehensive global response to invasive seaweeds. have advantages over both global and national responses to invasive species. gap-filling approach to dealing with related issues in the meetings relating to the CBD (e. A complete overview of regional efforts on this issue is. and to consider the challenges and opportunities associated with a regional approach to invasive species such as seaweed. regional approaches may have The Northern Territory of Australia has recently implemented mandatory hull fouling checks on recreational and fishing vessels seeking entry into any of the enclosed marinas. Although a few countries have adopted regulations to address transport of organisms such as invasive seaweeds by hull fouling. To this end. a regional approach can. not possible here. Regional approaches have potential advantages over national efforts in that they may be better able to tailor responses according to ecological boundaries as opposed to political ones. hull fouling has been the most important means by which shipping has transported non-indigenous species w«x impending limitations on the use of the most effective antifouling paint worganotin basedx and on the conduct of hull cleanings. in theory. commercial merchant.M. once adopted. at paragraphs 64–70). regulation of ships on international voyages should be coupled with regulation of domestic and any regional trade fleets. international shipping. These include areas of phytoplankton blooms. which could help prevent the risk of ships encountering seaweeds that may attach to hulls and equipment. arises as a result of the fact that the problem may be exacerbated by the adoption and implementation of another recent IMO marine environmental protection Convention. In particular the AHTEG noted the need to encourage the IMO to address the issue and also. including An electronic list serve posted a notice in early July 2001 of a proposed ‘‘Planning Meeting: Workshop on Ship Fouling and Biological Invasions in Aquatic Ecosystems’’. Subcommittee on Bulk Liquids Cases 2004 2. Latin America and the Caribbean. North America. outbreaks. The proponents note that: ‘‘Historically. in 2000 concern was expressed about this piecemeal. Regions recognized by the United Nations Environment Program (UNEP) include Europe.

identification and response to invasions. and Mexico. The other main area for discussion was the response to the threat of aquatic invasive species through regulatory and voluntary measures to prevent and respond to invasions. including one with representation from British Columbia. Western regional panel on aquatic nuisance species The Western Regional Panel on Aquatic Nuisance Species was initially called for in Section 1203 of the US National Invasive Species Act of 1996 (NISA). Possible areas of cooperation include joint processes for prediction. North American cooperation Cooperation in the North American context means cooperation among Canada. the International Joint Commission has been active in promoting cooperation on the response to aquatic invasive species in the Great Lakes Region. 2004). On the regulatory side. Beyond this. one involving the Great Lakes system. and other related interests. industry. An interesting issue with respect to regional and sub-regional cooperation in North America is the role of First Nations peoples. the CEC recently commissioned a report on the status of seaweed invasions on the Pacific coast of North America (Murray et al. (2) A directory of legal and institutional frameworks for the prevention and control of invasive species. With respect to invasive seaweeds. As discussed below. participants identified five priority areas for regional cooperation: w124x (1) A North American Invasive Species Information Network. particularly given the confusing jurisdictional picture with respect to environmental and aboriginal issues in Canada and the US. Any regional cooperation involving all three countries is likely to involve the Commission for Environmental Cooperation (CEC) established under the (1992) North American Free Trade Agreement (NAFTA) to encourage cooperation on environmental issues of interest to the three countries. voluntary measures. 3. and makes some general science and policy recommendations.1. are ongoing. however. Regional cooperation in North America: the CEC The CEC has been actively involved in coordinating action of aquatic invasive species since it held a workshop on the topic in March 2001 (CEC Proceedings 2001). 49. (3) Identification of invasive species and pathways. Topics discussed at the workshop included cooperation with respect to science and information sharing. (4) Tools for raising awareness. and one involving the Gulf of Maine. The Panel was set up following a meeting in autumn 1996. The Western Regional Panel is considered in more detail below as an example of sub-regional cooperation in the North American context. academia.2. 3. consistent rules to discourage intentional and unintentional behavior that may lead to invasions was seen as important to help reduce the risk of invasions in a manner that equally distributed potential costs involved in eliminating high risk activities. state and provincial governments in Canada and the United States. In addition. there are opportunities for cooperation on aquatic invasive species in freshwater ecosystems. its statutory base is federal legislation in the United States. and awareness raising. An interesting aspect of the Panel is that it includes jurisdictions from two countries. there are members from aboriginal organizations. In addition. 3. there has been limited action on invasive species to date. one involving the Pacific Ocean. considers the environmental threats of identified invasions. The Report.1. 50). 2001 workshop. (5) Tools to provide economic incentives to take voluntary action to reduce the risk of invasions (CEC Proceedings 2001. most notably the Great Lakes system. there are no concrete results to report.1.: Law and policy responses to invasive seaweeds the advantage of minimizing competitiveness otherwise associated with law and policy responses that either prohibit or increase the cost of certain economic activities. It also dictates its goals. and the role of states and provinces in the US and Canada respectively. however. At the March. as well as public awareness issues. Canada (Annual Report. p.1. specifically ballast water and hull fouling. Sub-regional cooperation in North America Sub-regional cooperation is generally ecosystem driven and often involves various levels of government with responsibility for a threatened ecosystem.1. The following sections consider whether there are indications that regional efforts in Europe and North America have been able to materialize on these theoretical advantages. In the Gulf of Maine. there are at least three examples of sub-regional cooperation. including prediction and modeling work. and to some extent the Arctic Oceans. institutions for inter-jurisdictional cooperation are well established in the form of the Gulf of Maine Council. there are opportunities for bilateral or sub-regional cooperation on the Pacific. Within the CEC. The focus of these efforts has been on invasions resulting from shipping.1. at 1). particularly those of potential concern to more than one country. The US National Invasive Species Act of 1996 goes beyond requiring the establishment of the Panel. They include the following: . the United States of America. In North America. which is currently in draft form. 2000–2001. voluntary measures were seen as serving to bring about the desired behavior to reduce or eliminate the risk of invasions without the need for regulations. Membership of the Panel includes representatives from federal. regulation. At this workshop.444 M. Doelle et al. It was made up of representatives from four existing advisory groups on invasive species. representatives of interested departments and agencies from the three member states identified a number of objectives as well as some specific steps to be taken to improve regional cooperation on this issue. discussions on how to achieve regional cooperation through information sharing. however. conservation groups. 3. Efforts to implement these priorities are ongoing. With respect to actions that require no outside motivation. the Atlantic.2. referred to above in section 2 on shipping. With respect to the Great Lakes.

the plan focuses on information sharing as an initial step toward more effective responses within the Gulf of Maine. The Bern Convention has certainly been the main legal instrument to guide regional cooperation on this issue. and in various aquatic ecosystems at risk of invasions more specifically. and report back to the Standing Committee on progress.2.1. Article 11(2)(b) requires each party to ‘‘strictly control the introduction of non-native species’’. This provision.2. The CEC is still in the early stages of trying to engage the member states in taking a coordinated approach to the problem. research and information sharing. has caused the parties to the Convention to consider the need for regional action on the issue. and the importance of legal. It is to be expected. other aquatic nuisance species program activities in the western region that are not conducted pursuant to the NISA. been documented in marine ecosystems throughout Europe. and the 1992 Helsinki Convention on the Protection of the Marine Environment of the Baltic Sea Area. 4.: Law and policy responses to invasive seaweeds 445 • Identify priorities for the Western Region with respect to aquatic nuisance species. and the Caspian Sea. The work of the Panel to implement these goals is ongoing. and control program to prevent the spread of the zebra mussel west of the 100th Meridian. • Coordinate. This has led to the preparation of a European Strategy on Invasive Alien Species prepared on behalf of the Standing Committee under the Bern Convention (Bern Convention 1979). National level law and policy options One clear message from the foregoing overview of international efforts on invasive species is that regional and global efforts are fragmented in terms of both regulatory w125x . The Strategy was endorsed by the Standing Committee in Recommendation 99 at the December meeting (Standing Committee Proceedings 2003). Observers (nonparties) are also invited to implement the Strategy. The Strategy furthermore highlights the role of regional cooperation. Doelle et al. including the Mediterranean Sea. where possible. that efforts at regional cooperation may have advanced further in Europe than in other parts of the world. 3.2. 3. too early to assess guiding principles let alone evaluate law and policy responses to the threat of invasions. The bottom line in North America is that it is too early to tell whether opportunities associated with regional approaches will materialize. As pointed out in other papers in this issue. There are efforts underway in the Mediterranean Sea. The Strategy is largely based on work carried out on invasive species under the CBD. the work of the Panel is in its early stages. Similarly. • Make recommendations to the US Federal Task Force on Invasive Species regarding an education. but it does include provisions in Article 11 that bring the issue within the mandate of the Convention. aquatic invasions have. and endorses the hierarchy of prevention.1. perhaps more than anywhere else. 3. prevention. and generally cross references work done under the CBD throughout the document. eradication and control. Specifically. The Strategy accepts as its basis the precautionary and ecosystem approaches. eradicate or control aquatic invasions have so far not been brought forward by the Panel. Based on the 2000/2001 Annual Report (the most recent report available). such as the 2003 Framework Convention for the Protection of the Marine Environment of the Caspian Sea (Article 12). With respect to aquatic invasive species. Recommendation 99 recommends that all parties to the Bern Convention implement national strategies in light of the European Strategy endorsed by the Standing Committee. the Gulf of Maine Council on the Marine Environment has been the main vehicle for regional cooperation on marine environmental protection. therefore. has resulted in considerable pressure for regional and sub-regional cooperation in Europe. in combination with numerous invasions documented in various ecosystems in Europe. In fact. the current action plan (Gulf of Maine Action Plan 2001) provides for awareness raising and improved management as the two pillars of its aquatic invasive species strategy. • Provide advice to public and private individuals and entities concerning methods of preventing and controlling nuisance species infestations. On the management side.2. Such efforts at multi-jurisdictional cooperation are generally carried out under regional agreements.M. 3. and the Caspian Sea.2. Areas covered include awareness raising. policy and institutional frameworks. The Convention initially did not deal in any detail with invasive species. it is not surprising that there are a number of sub-regional efforts to deal with aquatic invasions. the Baltic Sea. Concrete law and policy recommendations on how to prevent. • Submit annual reports to the Task Force. the focus to date has been on education and awareness raising. It adopts the terminology from the CBD. The Strategy was presented to the Standing Committee at its December 2003 meeting in Strasbourg. but have been coordinated through the 1979 Bern Convention on the Conservation of European Wildlife and Natural Habitats. Regional cooperation in Europe under the Bern Convention Efforts at regional cooperation on aquatic invasive species in Europe generally have been based on global efforts under the CBD. which came into force in 1982. the 1995 Protocol concerning Specially Protected Areas and Biological Diversity in the Mediterranean Sea. voluntary cooperation and coordination. The focus so far has been on information sharing. Sub-regional cooperation in Europe Due to the significant number of invasions and the multitude of jurisdictions with a stake in responding to those invasions as well as taking measures to prevent future ones. monitoring (including inspection). subregional efforts are in the early stages.2. the Baltic Sea. Gulf of Maine Council On the Atlantic coast of North America. for some time. European initiatives on aquatic invasive species The multitude of jurisdictions in Europe generally.

This means any effective strategy on invasive species will consider available preventative measures first. Assuming this approach works for well established activities with clear utility resulting in unintentional introductions. they can involve changes to the activity that leads to the invasion to make it safe. In case of pathways where current conditions do not reasonably allow for measures to prevent the risk of invaw126x sions. a combination of measures to reduce the risk and motivate further efforts to reduce and even. 4.446 M. Few countries have developed integrated strategies on invasive species that consider long-term local and global harm and benefits of the activities involved and the invasions linked to those activities. eliminate the risk in the future would constitute a second level of response. Given the limited success in addressing the problem globally and regionally. and about other vectors such as those associated with the aquarium trade and fishing. eradication. prevention has proven to be the only effective way of avoiding the invasion from becoming permanent. Prevention is the most effective way of slowing the increasing rate of invasions. the availability of an alternative method of achieving the utility of the activity. implementation of international agreements is only the starting point at a national level. such as the BWM Convention 2004. • Use of the funds generated from the process of internalization for early identification. other than through border control measures that are acceptable under international law. or with a mandate to protect ecosystems or components of ecosystems threatened by invasions. A country that has taken this issue more seriously than most is New Zealand (Wotton and Hewitt 2004). They can serve to motivate those who benefit from the activity responsible for the risk to look for ways to reduce or eliminate that risk. The overall message from international efforts on this issue seems clear. the international character of many of the activities inherently places some limits on the ability to regulate. It is at the national level. An effective national response clearly has to go beyond the implementation of international commitments. In the context of both unintentional and intentional transfer of invasive species. usually either associated with the utility of the activity involved. can be effective in reducing the risk of invasions that may result from ballast water and sediment discharge. General considerations This section will consider in very general terms the issues facing domestic law and policy measures. it is important to take into account the unique characteristics of the activity involved. difficult to prove. The example of international shipping is one involving an unintentional introduction from a long-established activity which most would consider as providing an essential service to society. In many cases. control. how would the response have to be adjusted . therefore. Furthermore. the responsibility is assigned to agencies with a focus on a particular aspect of the problem. Another would be the allocation of responsibility for compensation for damages arising from invasions that do occur in spite of measures to those who benefit from the activity. that we can expect to see the results of the global and regional efforts to develop effective responses to the threat of invasions. and by funding eradication. this can be problematic because a causal connection can be difficult to establish in that an invasion may not be apparent for many years and. A national level precautionary approach to regulatory system design is needed. In using this example as a starting point for the discussion of possible national level responses.: Law and policy responses to invasive seaweeds responses and at an institutional level. An effective national level response to the risk of invasions from vessel traffic might therefore consist of the following components: • Identification of reasonable measures to reduce the risk of invasions from ship traffic. Responses to risks that are deemed unavoidable as a result of the utility of the activity and the absence of alternatives have the potential to serve a dual function. However. including the utility of the activity. This means that the prohibition of shipping is generally not considered a reasonable response to this threat. control or containment of invasions to reduce the long-term damage. including those set out in international agreements. if baseline data on the relevant ecosystem are not available. • Identification of the residual risk. implementation of international agreements. or it can involve prohibition of the activity. As was discussed in section 2. Whether either of these options can reasonably be implemented with respect to a particular pathway will depend on a number of factors. Doelle et al. They can also serve to fund efforts for responding to invasions that do take place by funding efforts to identify responses as early as possible. One part of the answer would be to motivate research and development on ways to prevent invasions resulting from shipping. An example might be invasions from hull fouling and ballast water. This means that a clear identification and understanding of the problems and gaps found in the international system and the implications for national implementation is needed. obligations and principles developed under the various international instruments described elsewhere in the article. This leaves the question of what can or should be done about other risks related to shipping. In many States. Such measures can fall into two categories.1. • Regulation and enforcement to ensure all reasonable measure to reduce or eliminate the risk are being taken. and the cost of implementing alternatives. it is left to national governments to implement specific law and policy measures to implement the general principles that have been developed at a global and regional level. It will not come as a surprise that the problem of fragmentation does not stop at national borders. perhaps. It is assumed for purposes of this overview that the starting point for national measures will be those commitments. • Internalization of the cost of the residual risk (erring on the side of overestimating the risk and the resulting cost). and containment.

Other countries have focused on imposing decision-making responsibilities on existing departments and agencies. For purposes of this discussion of appropriate law and policy responses. the less the utility of an existing activity. Examples might be mariculture in closed systems on land. Doelle et al. Institutional issues Having considered the range of decisions that may have to be made at a national level to implement an effective response to invasive species. While interpretative debates have surrounded the precautionary approach (VanderZwaag 1998. The reason for considering them separately is not to diminish the importance of applying a precautionary approach in case of existing activities. but with decision makers whose primary mandate is as closely as possible connected to the prevention of invasions. 4. A precautionary approach here would suggest that decision-making responsibility should not rest with regulators of the activity involved. Even so. The fundamental choice is between the creation of a new decision-making agency and the use of one or a combination of existing decision makers. unless the species by its nature is known not to be invasive. In principle. Some countries. It is important to first define the boundary between intentional and unintentional introductions. to how to ensure motivation to reduce the risk and to ensure that the cost of any invasion is born by those who benefit from the activity that is creating the risk. w127x . implement directly. a precautionary approach to invasive species would generally result in the prohibition of intentional introductions in the sense of an introduction of a non-native species without any barriers to prevent its spread. the greater the pressure to respond to the threat by prohibiting the activity. In between is a range of activities whose classification really depends on the level of effort applied to prevent the escape and/or establishment of an invasive or alien species. a strong version of precaution would place the burden of proof on the proponent of an activity to meet some requisite standard of proof (Hildreth et al. These generally include departments of fisheries. and the higher the risk associated with it. should be based on an approach that seeks to fulfill international responsibilities to protect the global environment. In the mariculture context for example. existing frameworks may need to be modified to facilitate appropriate decisions on issues ranging from whether to allow an activity. as opposed to in the open sea without barriers to prevent the spread of the species. or in cages. Principle 10 in the CBD Guiding Principles for the Prevention. aquaculture. by delaying or preventing the activity until or unless it can be proven to be sufficiently safe by its proponent. Having said this. one could consider all non-native mariculture to be intentional. transportation. and agriculture. The other includes decision makers with an environmental protection and conservation focus. the main difference is that there is an opportunity to implement the precautionary approach in a more direct manner. something that is generally accepted to be difficult to establish. These generally include departments responsible for environmental protection. The first consists of regulators of the sectoral activities that pose a risk of invasions. the issue is one of whether a strategy has been developed whereby the risk of an invasion can be identified and how well it can be evaluated. This leaves the issue of intentional versus unintentional introductions. such as New Zealand. such as ‘‘no significant’’ threat to ecosystem health. have created new agencies to either oversee the national implementation by existing agencies. and the United States. or a combination of both. it is possible to consider the introduction to be unintentional. Introduction and Mitigation of Imports of Alien Species. but to highlight the opportunity to do so for new activities in a manner that avoids the difficult question of how to turn back the clock and eliminate an activity that has become accepted and relied upon within a society. reducing and controlling invasive species receives sufficient weight when compared to the pre-existing mandate of the decision maker. depending on the level of effort made in a particular operation to prevent the spread of a species used in mariculture.M. Existing decision makers typically fall into one of two categories. 4.: Law and policy responses to invasive seaweeds 447 to deal with differences in these basic characteristics? Clearly. and agencies responsible for processes such as environmental approval and environmental assessment processes. It is not surprising that one of the main challenges with the reliance on existing decision-makers is how to ensure that the objective of preventing. discussed above. whether the activity is a new or existing activity. resource conservation. Alternatively. This problem also arises in the context of environmental decision-making superimposed on government decision makers through environmental assessment processes that are based on the self assessment model. the decision-making responsibility will have to fit within an existing institutional framework. Ellis and FitzGerald 2004.3. fish stocking is the clearest example of an intentional introduction. such as shipping. how should these decisions be made? Inevitably. ideally operating within an integrated framework.2. it is suggested that nothing turns on where the line between intentional and unintentional introductions is drawn. 2005). suggests that the burden of proof should be with the proposer of intentional introductions of potentially invasive species to show the introduction will be unlikely to threaten biological diversity. On the other hand. Regulatory tools A domestic regulatory response to prevent the transfer of harmful aquatic organisms and pathogens should be based on a principled approach with sustainability as the ultimate objective. Introductions from ships clearly fall into the unintentional category. Australia. this decision would be made based on the same precautionary approach. Rather. biodiversity. Scott 2005). With respect to new activities. what conditions to impose on an activity to minimize the risk of invasion. The following principles initially developed in the shipping context provide a sound basis for a national response to invasive seaweeds more generally: • Responses to an ecological problem in the context of an international activity.

Doelle et al.448 M. An alternative use of the same range of economic instruments is to motivate those engaged in the activity to find ways to reduce or eliminate the risk. and then designing and implementing effective enforcement mechanisms to ensure that legal obligations are observed. There are a number of alternatives to the traditional command and control approach that have evolved over time. uniform and consistent manner in each port. security requirements. They are of interest here in particular with respect to activities that are permitted to continue in spite of an ongoing risk of invasions. be based on scientific research and an analysis of both local and global ecological implications of any action. Anyone who complies with the standards set in the regulation is entitled to engage in the activity in question. setting out those requirements in law. The traditional tool for environmental protection is generally known as command and control. based on a ‘‘polluter-pay’’ model. all regulatory determinations must. imposing penalties for not following those requirements. Requirements should be put in place that are environmentally safe. or the least possible. technology or the development of new related concerns. or the establishment of a liability fund. including the regulated sectors and other sectors. • Reducing unnecessary costs to the public and the regulated industry. • Minimizing uncertainty for all affected parties. Responses should allow for and explicitly encourage continuous technological and operational improvement to better protect the marine ecosystem. and requiring that the cost be paid by those who benefit from it. This process is often referred to as ‘‘internalizing the cost’’. It will be important to develop local and regional contingency responses and compensation plans for all those negatively affected by the activity. practicable. Responses should encourage the involvement of all parties affected by the issue (and any decisions about regulating the issue). sustainability and integration of agency responses. might include: • Preventing the problem at the earliest possible point and with the highest level of effectiveness possible. The common thread is the objective of quantifying the cost of the risk of invasion. based on the internationally accepted standards such as the IMO Guidelines and the BWM Convention 2004 and any guidance developed under it. with preference given to measures designed to ensure either no. Another common form of regulating activities is through standards imposed through regulations. Requirements operating at a national level also need to take into account ecosystem differences within each country. Having now considered the substance of the decisions that would have to be made at the national level as well as some basic choices about the decision maker. Of most interest in this context is what has become known as economic instruments. • Maximizing accountability – internationally. this leaves the question of the regulatory tools that may be used to implement the decisions made. There should be a focus on measures to prevent the uptake of harmful organisms and pathogens at the source as well as preventing their introduction. • Ensuring transparency. regionally and nationally. including legislation. • Maximizing opportunities for risk assessment and prevention. and allows regulators to specify conditions for approval on a case by case basis. and must be applied in a fair. as much as possible. it only does so Goals to be achieved in designing a regulatory system. It will be important to ensure that there is ongoing review and monitoring to evaluate the impact of any action that is taken. This refers to the general process of identifying what should or should not be done. Risks to the ecosystem8 should be minimized by designing and adopting measures that are commercially and practically viable and that encourage compliance rather than avoidance and conflicts. It will be important to ensure transparency. presumably due to the utility of the activity and the absence of an alternative that would eliminate the risk without eliminating the utility. as much as possible.: Law and policy responses to invasive seaweeds • • • • • • • • • • • integrates economic and ecological protection concerns and is based on international cooperation to develop rules and technological or other solutions to environmental problems arising out of the globalization of the economic system. • Ensuring flexibility to respond to and incorporate developments in scientific information. Economic instruments provide the opportunity to ensure that the cost of the risk of invasion is borne by those who engage in or otherwise benefit from the activity. This includes the environment or ecosystem of the enacting State and other States and common areas as noted in Guiding Principle 4. in helping to develop a solution. which requires individuals who wish to engage in an activity to seek approval. For example. A common regulatory tool is the permitting process. While this can be achieved by internalizing the cost. A precautionary approach should be adopted for both regulatory design and implementation. and to accommodate local ecosystem conditions and requirements in a harmonized manner (McConnell 2002). 8 w128x . long-term negative impact on the environment. • Avoiding unnecessary conflicts between shipping and other coastal zone users and amongst regulatory agencies. • Maximizing administrative efficiency and cooperation through holistic approaches and integrated management. This can be done through user fees. Compliance should be encouraged by making use of a range of modern regulatory devices such as economic incentives and voluntary compliance agreements. requirements for insurance. designed to minimize cost and delays to the shipping industry and. Here those engaged in activities are required to meet the standard set in the regulation rather than to be forced to individually apply for permission.

‘‘Cawthron reveals unwelcome ‘Octopus Garden’’’. Sub-Committee on Bulk Liquids and Gases. Online: -http://www.M. 963 (1972). Ocean Dev. Globallast.M. At the same time. 2005.M. Coastal and port environments: international legal and policy responses to reduce ballast water introductions of potentially invasive Ocean Yearb. 1340 U. 15 (1980).helcom. J. European Strategy on Invasive Alien Species.L. Similarly at the regional 1340 U. Willing. 21 I. Online: -http://conventions. and J. L. w129x .N. Online: -http: //www.M. 1995.asp). North American Agreement on Environmental Cooperation. Conclusion: the need for a precautionary integrated approach to regulatory design and implementation decisions The development of an effective law and policy response to the threat of invasive seaweeds is still in its early stages. Bern Convention on the Conservation of European Wildlife and Natural Habitats Standing Committee. Council of Europe – ETS no.htm). Convention on Biological Diversity of the United Nations Conference on the Environment and 2001–2006.coe. J. Online: -http://www. Online: -http: //www. FAO. Treaties/Html/104.default. Firestone.htm).fi/ Convention/en_GB/text/). Law 36: 291–316. Gulf of Maine Council on the Marine Environment. Convention on Wetlands of International Importance especially as Waterfowl Habitat. International Convention for the Prevention of Pollution from Ships (MARPOL 1973) Options for Future Work. 2003. September 14.3. M. March 2001 CEC Workshop Proceedings. 104. Online: -http://globallast. Other sources Cawthron Institute. 874 (1992). Some jurisdictions have made significant progress. 1979. available online at -http://www.J. Convention on Migratory Species of Wild Animals.cawthron. Ellis. Mar. R. programmes/areas/marine/default. 1995. rather than the internalization of the cost. Global Ballast Water Management Programme website.fao. 2003. Langlas.T. Online: -http://www.FAO. 1992. Cox. Res. Int.M. December 31 I.coe. Coast. A.C. September 19.htm). M. Convention-FrameworkConventionText.M. Development of Guidelines for Uniform Implementation of the 2004 BWM Convention. Int.htm). Convention on the Protection of the Marine Environment of the Baltic Sea Area. biodiv. Corbett. UNEP/CBD/COP/8/27/Add. Rio Declaration on Environment and Development. Hildreth.L. CBD Secretariat. 49: 779–800. Resolution A. 2004.M. 32 I. not based on the cost of responding to invasions. Law and policy responses to invasive species in North America. 38: 429–438. Efforts to move towards an effective global response are ongoing. June much remains to be done. 1996. Press release. International Convention on the Control of Harmful Anti-fouling Systems on Ships (Anti-fouling Convention). Protocol concerning Specially Protected Areas and Biological Diversity in the let alone at the global level. 2. 1480 (1993). Jones and D. Online: -http:// www.S. February 2. Invasive Alien Species. While these efforts do show some promise. Mar. The precautionary principle in International Law: lessons from Fuller’s internal morality. November 2. Online: -http://globallast. 1261 (1982). FAO Technical Guidelines on the Precautionary Approach to Capture Fisheries and Species Introductions No. 2004.. April 9. Freshw. IMO AFS/CONF/26 (2001). Online: -http://www. 2005. Roles for a precautionary approach in marine resources management. Action Plan.caspianenvironment.N. ICES. Law 18: 261–294. North American 5. The quiet invasion.biodiv. November 4. Workshop to Identify Cooperative Opportunities for Preventing the Introduction and Spread of Aquatic Invasive Species. 32 I. There is little indication to date of the specific issue of invasive seaweeds as a distinct challenge that has been identified in many jurisdictions or regions.asp). 1992. 6. 32 I. If the primary objective of an economic instrument is therefore the ultimate elimination of the risk. 818 (1992). IMO Doc. 2003. 1997.gulfofmaine.L. Note by the Secretariat. December 10.imo.T. 2002. New Zealand marine biosecurity: delivering outcomes in a fluid environment. imo. United Nations Convention on the Law of the Sea. 605 (1993).imo. BLG 9/11. Doelle et al.M. 2005. 17 February 1978 Protocol. SBSTTA VI/8 and SBSTTA/6/ paras 20–22. 19 I. 2005. the current state is one of fragmentation. 2004. The Framework Convention for the Protection of the Marine Environment of the Caspian Sea. while others are just starting to take the problem of invasive species seriously. Online: -http://www. Online: -http://www. November 12. C.L.L. 1982. McGill Law J. ‘‘Jakarta Mandate Marine and Coastal Biodiversity – Introduction’’.: Law and policy responses to invasive seaweeds 449 if the cost cannot be passed on easily and if the cost is sufficiently high to create a motivation to invest in finding ways to reduce or eliminate the risk. law and policy makers do have a solid basis of principles and potentially powerful regulatory tools to draw upon. and A. June 13. Jarman and M.ices. NZ J. Online: -www. Code of Conduct for Responsible Fisheries. December 184 (1973).L.L. IMO. February 1. References International agreements and documents Bern Convention on the Conservation of European Wildlife and Natural Habitats. 1992. 1973. Bauckham.L.asp). IMO. 1979. June 23. 1992. 1993. Online:-http://www. Code of Practice on the Introduction and Transfer of Marine Organisms. International Council for the Exploration of the Sea. A. 31 I. 2004. Online: -http://www. J.htm). International Convention on the Control and Management of Ship’s Ballast Water and Sediment.868(20) Guidelines for the Control and Management of Ships’ Ballast Water to Minimize the Transfer of Harmful Aquatic Organisms and Pathogens. Report of the Group of Legal and Technical Experts on Liability and Redress in the Context of Paragraph 2 of Article 14 of the Convention on Biological Diversity. 11 I. the price will be set based on what is required to motivate research and development. June 1. 19: 33–61. CBD show_cdr. Cassidy. Wotton.G.S. Online: -http://www. FAO. June 10. Precautionary approach to capture fisheries and species introductions. December Hewitt. IMO BWM/ CONF/36 (2004). North American Free Trade Agreement.M.S. 20 December 2000. 289 (1993).

Doelle et al.18 on Invasive Species and Wetlands. Wotton. Mooney. 121 2002 Final CIESM Portal Programme. 50–85. December.ku. International Maritime Organization No.htm).htm. 104–332. http://www. The EU Northern Dimension. Resolution VIII. http://www. US National Invasive Species Act of 1996.loc. Online: -http://globallast. Johan Schei and J. The Nordic Environmental Action Plan 2001–2004.L. M. Switzerland and Cambridge. available online at -http://thomas. Freshw. Caspian Environment Programme (CEP). Environ. -http://www.ramsar. htm) Law and res_vii. U. Globallast Monograph Series. sns. Ramsar Convention COP8. SBSTTA 2000 and other SBSSTA docs and COP q app. Global Strategy on Invasive Received 10 January. pp. L. Shifting the burden of proof: the precautionary principle and its potential for the ‘‘democratization’’ of risk. 50. J. McConnell. Technical and Technological Advice. Online: -http: //www. Z..html. J. Baltic Sea Transportation System Projects. key_res_viii_18_e. The precautionary principle in environmental law and policy: elusive rhetoric and first embraces. Resolution VII.ramsar. Convention on Biological Diversity. http://www. Internet resources Baltic Marine Biologists (BMB).) 2005. Resolution VII. 2000–2001 Annual Report.icais. Scott. Fernandez. D. http://www. IUCN Gland. helcom/declarations. Convention on Biological Diversity. 2006 w130x . Online: - 110 Stat 4073.smf. Zertuche-Gonzalez. UNEP/CBD/SBSTTA/11/INF/4.helcom.ramsar. GloBallast Legislative Review. Online: -http:// www. 2002. L. London.14e.helcom. http://www. Online: -http://www.pdf).org/pdf/21Tuesday/C/tues_c_ e_am/Hans_Herrmann. Notes of Standing Committee to the Bern Convention. http://europa. accepted 23 November. Western Panel on Aquatic Nuisance Species. D.htm). H. Global Ballast Water Management Programme. caspianenvironment.E.14 on Invasive Species and Wetlands. -http:// globallast. Online: -http://www. Ramsar Conference. 1999.14e. and Mar. 1998. Ramsar Conference. Subsidiary Body on Scientific. Baltic Sea Regional Project (BSRP).: Law and policy responses to invasive seaweeds Commission for Environmental Cooperation.gda.coe.A. external_relations/north_dim. Commission on Environmental Cooperation (presentation) 2004. J..pdf). VanderZwaag. Resolution VIII. 2003. Environmental Threats.N. Report of the Ad Hoc Technical Expert Group on Gaps and Inconsistencies in the International Regulatory Framework in Relation to Invasive Alien Species. Online: -http://www. Neville. UBC Press. http://www. J.pdf. Online at -http://www. No. P.ciesm. 8: 355–375. Pub. 38: 553–559. Online: http://www. norden.K./temp/.ramsar. 2002. http://www. In: (Law Commission of mainnemo. SBSTTA helcom/projectsmeetings/GEF-BSRP. N. Vancouver. The Nordic Council. cgi-bin/query/D?c104:13:. Law Practic.14 1999.htm. S.pdf). Status. 23rd Meeting.mdbsexmOl0::). Nordic Network on Introduced Species (NNIS). McNeely.cec. Marine biosecurity postborder management: developing incursion response systems for New 2001. Ramsar Convention COP7. 2006. Online: -http:// www. 2003 HELCOM Bremen Declaration. D. http://www. Working Group 30 on Non-indigenous Estuarine and Marine Organisms (BMB WG 30 NEMO). asp. Hewitt. and Policy Considerations for Invasive Seaweed for the Pacific Coast of North America. 2005.450 M.

g.2007. DOI 10. 2007). by shipping have focused on treatment of ballast water (e.Botanica Marina 50 (2007): 451–457 2007 by Walter de Gruyter • Berlin • New York. and whether apparent patterns of larger numbers of alien seaweeds in Australia. for example. As is the case with most establishments of alien species. They can account for a significant proportion of the total flora (e. most engineering efforts to control translocation of marine species. particularly in light of the intent to phase out use of tributlytin (TBT) and related organotins in antifouling paints by 1st January 2008 because of their deleterious effects on the marine environment. including algae.johnson@utas. University of Tasmania. mechanical hull scrubbers) have presumably not been cost effective.. These observations pose two challenges. However. or with physical properties that inhibit settlement of marine organisms. or where systematic surveys of susceptible areas (ports) have been implemented (Australia and New Zealand). Cangelosi et al. New Zealand and the Mediterranean. Despite redoubled efforts to develop new antifouling paints based on chemical biocides less toxic than organotins. there has been an accelerated effort to detect introduced seaweeds to the extent that up to .1515/BOT. we established the scope of this topic around a series of questions. Ribera and Boudouresque 1995) and up to . In defining challenges for the future and suggesting how those challenges might best be tackled to optimize returns on research Just as is the case for invasions of terrestrial systems (Mack et al. preventing invasions of seaweeds in the first place is much less costly than attempting control of post-establishment.97%) of seaweed introductions are accidental. usually for aquaculture. there is at least a qualitative correlation between the number of alien species recorded in IUCN bioregions and the effort given to looking for them. consequences of invasions and human responses to the threat and occurrence of invasion. which also provided a framework for integrating the different contributions and a means of highlighting deficiencies in knowledge and understanding (Johnson and Chapman 2007). but there are likely to be ongoing appeals for future introductions. authorities and the public alike has driven a large effort to detect alien species (Mediterranean). Johnson School of Zoology and TAFI. hull fouling remains a significant problem. but far fewer alien species in tropical waters. Particularly in the last decade. are real. particularly in Africa and Asia. Hobart. Intentional introductions A minority of species (-3%) has been introduced intentionally. reveal the greatest number of alien seaweed species.40% of all alien species (Schaffelke et In the introduction of this special issue of Botanica Marina. overfishing and pollution associated with w131x . it is useful to revisit those questions under four main headings dealing with species introductions per se. 2007). the great majority (. but it begs the question about the real number of established alien seaweeds. 2007). Given large ecological pressures on coral reefs as a result of.260 species world wide have now been identified as alien to their native range (Hewitt et al. 2007). The 1999 IMO Assembly resolution called for complete prohibition on the application of TBT and other organotin compounds by 1st January 2008. the invasion process. namely ascertaining the veracity of current knowledge about the extent of alien and invasive seaweeds. Gollasch et al. this poses large challenges. Australia. Indeed. This pressure is most acute in developing nations in tropical and subtropical regions where aquaculture of seaweeds is often seen as an alternative (and sustainable) economic activity to either growing species that require large inputs of artificial feeds or extractive harvesting in wild fisheries (Pickering et al. 2007). This is hardly surprising. The International Maritime Organization’s (IMO’s) International Convention on the Control of Harmful Anti-fouling Systems on Ships prohibits the use of TBT and will enter into force 12 months after 25 States (representing 25% of the world’s merchant shipping tonnage) have ratified it.047 Conclusion Seaweed invasions: conclusions and future directions Craig R.. given that hull fouling is the principal culprit. 2006) in a given area. Introductions of alien seaweeds The questions posed • What are the major modes of introduction of invasive seaweeds? • Is there tangible pressure for ongoing intentional introductions? Accidental introductions Introduced seaweeds have been detected in most marine bioregions of the world. 2007. the exceptions being some tropical areas and the polar latitudes (Hewitt et al. both of which have typically had a large impact on the environment and which may be ecologically and economically unsustainable in the long term. Tasmania 7001. Regions where interest among phycologists. Engineering solutions (e.. 2000).g.g. GPO Box 252-05. and whether there are meaningful responses to reduce the risk of introductions through hull fouling. However. and hull fouling of ships is by far the most important vector (Hewitt et al. e-mail: craig.

452 C.R. Johnson: Seaweed invasions: conclusions and future directions

aquaculture of species that require addition of nutrients (McManus 1997, Jackson et al. 2001, Hughes et al. 2003, Feng et al. 2004, Azanza et al. 2005), there is considerable ecological as well as socio-economic pressure to identify alternative and more sustainable livelihoods for human coastal populations. Aquaculture species that do not require exogenous inputs of nutrients, such as shellfish (Bell and Gervis 1999, Feng et al. 2004) and seaweeds (Feng et al. 2004, Pickering et al. 2007) are attractive on environmental grounds. Nonetheless, in many places in the Pacific where they occur, these relatively low-impact activities are still largely in an experimental phase (Bell and Gervis 1999, Pickering et al. 2007), although there are notable exceptions (Doty 1977, Trono 1999, Feng et al. 2004, Pickering et al. 2007). The reasons behind failed attempts to develop seaweed culture usually have a strong cultural and/or socio-economic basis (McManus et al. 2002, Pickering 2006, Pickering et al. 2007).

The invasion process
The questions posed • Are there common life-history or genetic traits of successful invaders? • Why do some species become invasive while others do not? • Is it possible to predict the next pest seaweed? • Are there common mechanisms underpinning seaweed invasions? • Why do some communities appear to be more susceptible to incursions than others? • Do the traits of the recipient community influence invasion rates? As is the case with terrestrial plants (e.g., Crawley 1987, Mack et al. 2000), there is no consistent set of lifehistory or morphological traits, or particular taxonomic affinities, that define invasive seaweeds (Valentine et al. 2007). Thus, it remains unclear why some species are highly invasive while other, even closely related, species (e.g., Trowbridge 1998) are not. By corollary, the most reliable means of identifying a ‘‘next pest’’ seaweed is through reference to existing patterns of invasion rather than consideration of species’ traits in isolation. If there are any broad traits common to most (but not all) invasive seaweeds, it is the capacity for rapid growth and means of effecting both short and long-distance dispersal (Valentine et al. 2007), but many seaweeds manifest these properties without showing any sign of being invasive. Moreover, even the same species can be invasive in one area but not in another (e.g., Trowbridge 1998, Chapman 1999) or, in the same area, at one time but not another we.g., Undaria pinnatifida (Harvey) Suringar, CR Johnson, pers. obs.x. Collectively, these observations suggest that invasion might have as much to do with the properties of the recipient community as of the invader itself and, of course, this has been a topic of much debate since Elton’s (1958) first discussion of the idea (e.g., Levine and D’Antonio 1999, Levine 2000, Stachowicz and Tilman 2005, Fridley et al. 2007). w132x

The results of Dunstan and Johnson’s (2007) models substantiate the suggestions of Davis et al. (2000) and Davies et al. (2005) that resource availability is a critical determinant of invasion success and, in particular, that the likelihood of invasion increases with variability in resource availability. For nearly all seaweed species where there is empirical evidence of the mechanism of invasion, disturbance to native species in the recipient community is a key feature (Valentine et al. 2007). Caulerpa taxifolia (M. Vahl) C. Ag. in the Mediterranean may be the only seaweed where invasion does not depend on disturbance breaking a native species’ monopoly on resources (see Valentine et al. 2007), but even here resistance to invasion is greater in areas where cover of native seagrass or macroalgae is high (deVillele and Verlaque ´ 1995, Ceccherelli and Cinelli 1999, Ceccherelli et al. 2002), and there is evidence that high density stands do indeed depend on disturbance to limit the growth of native species (deVillele and Verlaque 1995, Jaubert et ´ al. 2003). Thus, it appears that invasive seaweeds are not especially competitive; competitive displacement of native seaweeds de novo by alien invasive seaweeds occurs rarely, if at all. At least in some quarters, a similar view is emerging for terrestrial plants (Bruno et al. 2005). To date, theoretical considerations and empirical observations are consistent with the idea that the risk of seaweed invasion is related to variability in resource availability (Dunstan and Johnson 2007, Valentine et al. 2007), but further carefully designed and executed experiments are required to more rigorously test these ideas. If variability in resource availability through disturbance, or any other mechanism that causes morbidity or mortality of native seaweeds, is ultimately shown to be the key predictor of invasion success, then this may explain apparent anomalies such as why a species is invasive in one area but not another, and why some communities appear more easily invaded than others. It would also explain why risk of invasion might not be predicted by the richness of the recipient community (Dunstan and Johnson 2007). The pattern of fluctuation in resource availability at any given locale will depend at least on the properties of the occupying native species and interactions among them, patterns of disturbance, and variability in physical properties such as temperature, wave action, and nutrient loading. Complex responses to several experiments suggest that considerations of invasion dynamics need to address separately the different stages of invasion since the mechanisms facilitating ongoing persistence of an invader may be different from those underpinning its initial establishment and spread (Valentine et al. 2007). Disturbance to native canopy-forming algae to provide space is necessary for Sargassum muticum (Yendo) Fensholt and Codium fragile ssp. tomentosoides (van Goor) P.C. Silva to establish at high densities, and presumably to spread beyond initial establishment. Having established a closed canopy, both species can effectively inhibit re-establishment of native seaweeds, at least in the short term (reviewed by Valentine et al. 2007). In Tasmania, Undaria pinnatifida also requires disturbance to native seaweeds to establish at high densities but, once established, it does not require ongoing disturbance to

C.R. Johnson: Seaweed invasions: conclusions and future directions 453

maintain its dominance. This is because a matrix of sediment and filamentous algae builds up on the substratum when native canopy-forming species are removed. This matrix inhibits development of native canopy-forming seaweeds, even in the absence of both disturbance (sea urchins) and Undaria pinnatifida and when the inoculum of spores from native seaweeds is enhanced (Valentine and Johnson 2005a,b). However, this effect is scale dependent. If native canopy forming seaweeds are removed in small patches (16 m2) then U. pinnatifida establishes and the sediment matrix develops, but within two years the native seaweeds displace the invader to recover dominance (Valentine and Johnson 2003). However, when native algae are removed on a much larger scale, U. pinnatifida establishes, the sediment matrix develops, and native canopy forming seaweeds do not recover (Valentine and Johnson 2005a). The explanation for this non-linear response is unclear. Moreover, it is difficult to estimate the prevalence of nonlinearities of this kind because too few experiments are undertaken to detect them. They certainly add complexity to the nature of invasion dynamics. Similarly, shortterm responses to manipulations at small scales may not be evident over longer periods or at larger scales. If all patches where Codium fragile ssp. tomentosoides (Chapman et al. 2002, Levin et al. 2002) or Sargassum muticum (Britton-Simmons 2004) established were able to inhibit recruitment of native seaweeds indefinitely, then patches of the invader might be expected to persist and maintain their dominance of ‘‘captured’’ sites. This mechanism would result in the gradual but inexorable displacement of native seaweeds over large scales, but this has not been observed for either species. The complete dynamic is more complex than is indicated by short-term experiments. Clearly, detailed and enlightened understanding of invasion processes requires careful experimentation and observations over the long term. There is yet much to be done to fully comprehend the nuances of the invasion dynamics of seaweeds. But even with a more complete knowledge, it is unlikely that particular seaweed invasions will ever be predictable. In this, invasions by seaweeds are no different from those of other kinds of organisms (Gilpin 1990).

Consequences of invasions
The questions posed • What are the ecological, genetic and economic consequences of seaweed invasions? • Can we expect existing and, in particular, emerging techniques in genetics and genomics to provide a much deeper understanding of seaweed invasions? If there is issue about the real nature of worldwide biogeographic patterns of alien seaweeds, the uncertainty about the impacts of alien species is even more profound. It could be argued that, since the direct impacts of very few alien species have been considered at all (;17 of the ;260 alien species identified) while even fewer (;4 species) have been studied in any real depth with appropriate effort given to both experimental work

and surveys (Schaffelke and Hewitt 2007), it is premature if not wholly invalid to attempt any general synthesis of the impact of alien seaweeds. However, it seems clear that, like most other groups of alien species including terrestrial plants (e.g., Williamson and Fitter 1996, Gurevitch and Padilla 2004, Bruno et al. 2005), the great majority of alien seaweeds are not highly invasive and are unlikely to become pests. Indeed, the highly skewed attention to a minority of alien seaweed species arises because effort has focussed on those few that appear most likely to be problematic. While there are undoubtedly as yet undetected ecological impacts of alien seaweeds, it is just as certain that a greater number of species would have been investigated more fully to date if there were clear signs of them becoming invasive as opposed to establishing as another ‘‘background’’ alien species. Of those that have been investigated, effects have varied from significant reductions in both abundance and diversity of native species at a local scale, to no detectable effect, to local enhancement of invertebrate and fish biomass and/or diversity (see Schaffelke and Hewitt 2007, Table 1). In several cases, the introduced seaweed seems to simply increase the standing biomass of total algae. No invasive seaweed has had what could be described as massive effects on biodiversity on a large scale. While it is clear that some seaweeds have significant ecological impacts, at least locally, current evidence suggests that their impacts might not be as great as several marine animals, particularly some filter-feeding marine molluscs we.g., the Asian clam Potamocorbula amurensis (Schrenck), Nichols et al. 1990, and New Zealand screwshell Maoricolpus roseus (J.R.C. Quoy et J.P. Gaimard, A. Reid and C.R. Johnson, unpublished datax, and generalist predators in pelagic (e.g., the ctenophore Mnemiopsis leidyi, Shiganova 1998, Daskalov 2002, 2003) and benthic (e.g., Northern Pacific seastar, Asterias amurensis A. Agassiz; Ross et al. 2003) habitats. All of these animals have the capacity to effect deleterious impact on richness, diversity and ecosystem functioning over large spatial scales. Of course, comparing the impact of seaweeds in one area with that of animals in another is problematic because it is not possible to distinguish impacts as a property of the invader from impacts related to the nature of the recipient community. However, the pattern of greater impacts by animals than plants is sometimes evident in the same system. In Tasmania for example, despite the relatively rapid spread of Undaria pinnatifida and its capacity to form a closed canopy in dense stands (Sanderson 1990, Valentine and Johnson 2003, Hewitt et al. 2005), its overall effect has arguably been small compared to that of introduced benthic marine animals such as A. amurensis (Ross et al. 2003), M. roseus and the European green crab Carcinus maenus (Linn.) (Thresher et al. 2003). C. maenus has a voracious appetite for small bivalves including mussels, oysters and cockles, and appears to displace a similarly sized native crab species, Paragapsus gaimardii (Milne Edwards) (Walton et al. 2002). If these patterns are found to hold more generally, then it will parallel the pattern from terrestrial systems where invasive animals, particularly generalist predators, w133x

454 C.R. Johnson: Seaweed invasions: conclusions and future directions

have greater direct impacts than plants. In other words, invasive top-down effects may be more important than invasive bottom-up effects in changing the configurations of recipient benthic communities. There remains much to do to properly understand the impacts of invasive seaweed species. Their socio-economic impacts have hardly been addressed at all (Schaffelke et al. 2007). Not only have the impacts of few species been examined thoroughly, but most studies have focussed on the direct impacts on the abundance and diversity of natives. In considering effects on diversity, most work has examined local alpha diversity, while beta and gamma diversity have been ignored. In many cases, local alpha diversity might decrease while gamma diversity increases. For example, in Nova Scotia Codium fragile spp. tomentosoides has been spectacular in its displacement of the previously dominant kelps (largely Saccharina longicruris (Pyl.) Kuntze; see Johnson and Mann 1988 was: Laminaria longicruris Pyl.x) in patches. This green alga does so by capitalizing on disturbances from grazers, or in response to dieback of kelp as a result of smothering of their photosynthetic tissue by the introduced bryozoan Membranipora membranacea Linn. (see Chapman et al. 2002). Native seaweeds, particularly kelps, are less abundant in areas taken over by Codium, and so at a local scale alpha diversity is reduced. A similar phenomenon has been observed in the Gulf of Maine further to the south (e.g., Levin et al. 2000). While Codium can form meadows of 100s–1000s of square meters in extent, in Nova Scotia replacement of kelps at this scale has occurred mostly in two bays (Mahone and St Margarets Bay), but only in wave sheltered areas in shallow water (F8 m; R. Scheibling, pers. comm.). Thus, gamma diversity may well have increased. Descriptions of impacts on diversity and abundances are a useful starting point, but at least as important are the effects on ecosystem functioning and dynamics. However, these aspects are rarely examined, no doubt because of the effort and, in some cases, technology required. How are primary and secondary production, and resistance and resilience stability (sensu Dayton et al. 1984) affected by invasives? What is the nature of indirect effects, and of synergistic effects of co-occurrence of several alien seaweeds? The only measurable effect of the establishment of some alien species is apparently to increase total algal cover and local richness (see Schaffelke and Hewitt 2007). But do relatively benign alien species like this simply accumulate indefinitely in a linear manner, or is some threshold attained where effects become non-linear? Can otherwise noninvasive seaweeds become highly invasive in the face of significant interactions with anthropogenic modifications to the marine environment, e.g., disturbance and eutrophication? Is there any evidence of ‘‘invasional meltdown’’ (Simberloff and Von Holle 1999; see also Simberloff 2006) whereby establishment of some alien species increases the likelihood of subsequent incursions? Are there significant evolutionary consequences for the invader in establishing in new areas, and for native species as seaweed floras become increasingly homogenized with ongoing accumulation of aliens? These are all important questions that are poorly addressed, not only for seaweeds but for invaded sysw134x

tems in general. But they are also difficult questions to tackle, and typically require complex experimental fieldbased studies, often over several years combined with empirical surveys at several scales. We are hopeful that researchers will have the courage to address these questions in the near future. With the rapid emergence and uptake of new techniques in molecular genetics, there is every chance that some of the evolutionary questions, particularly those relating to interactions between genotype, phenotype and environment, might be resolved before the ecological ones (Hofmann et al. 2005, Booth et al. 2007). This would be a welcome development given that the genetic consequences of seaweed invasions, including effects on gene pool composition, genome organization and mating systems, are currently so poorly appreciated (Booth et al. 2007).

Human responses to the threat and occurrence of invasions
The questions posed • How have seaweed invasions been tracked, and can existing approaches be improved? • Is it possible to predict the course of an invasion? • What are sensible approaches to reducing risk of further introductions? Responses to the threat of alien invasive seaweeds have included (1) attempts to mitigate the risk of alien species becoming established in the first place, (2) the development and application of science and technology to better predict ‘‘next pests’’, more rapidly detect alien species before they have opportunity to spread, and better understand the space-time dynamics of invasions, and (3) attempts to eliminate or control invasive seaweeds when they do establish in a new locale. The earlier intervention occurs in the chain of events described by uptake at a donor site ™ translocation by a vector ™ release at a donor site ™ establishment at donor site, the easier and less expensive it usually is to thwart potential introductions. Ships have long been recognized as vectors for translocation of marine species (e.g., Ostenfeld 1908) but, as we emphasized earlier, practical responses to minimize translocation of species by ships have focused largely on ballast water (e.g., Cangelosi et al. 2007, Gollasch et al. 2007), despite the fact that hull fouling is a major source of introduction of seaweeds and many other kinds of marine organisms (Hewitt et al. 2007). Particularly as TBT-based antifouling is phased out, and given the cost of engineering solutions to hull fouling, translocation of alien seaweeds by shipping is likely to be with us for a long time to come unless hull scrubbing or other hull treatment is forced through regulation, which seems unlikely, at least in the medium term (see Doelle et al. 2007). This is despite the economic incentive to reduce drag, and thus fuel costs, by minimising hull fouling. Notwithstanding the problem of hull fouling, international and most national policy and law makers are acutely aware of the risks associated with translocation of marine species. They also recognise the fragmented nature and lack of integration of existing reg-

D. In this context we note that a plethora of techniques has been brought to tracking seaweed invasions (Meinesz 2007). which might sensibly be based on risk management principles. In this context it is interesting that modelling seaweed invasions and various options for their control has not featured in responding to establishment of alien seaweeds. Ecol. Britton-Simmons.. Johnson: Seaweed invasions: conclusions and future directions 455 ulations aimed at controlling translocation of marine species across national borders (Doelle et al. but little attempt has been made to use this information in models. Harmful Algae 6: 547–566. Models would be of particular value if they could be calibrated against the known dynamics of initial range expansion. Prorocentrum minimum bloom and its possible link to a massive fish kill in Bolinao. R. 13–40. model the epidemiology of spread.g. Keller.. Cangelosi. 50: 385–396. Nantel and E. and to cooperate with other nations in effecting this goal. and account for the spatial structure of populations in considering control options (e. Spread of introduced Caulerpa species in macroalgal habitats. Reid. wetlands and forests. 255: 259–270. New Zealand. L. eds) Species invasions. Biol. and F. predicting the course of seaweed invasions and thus improving strategic responses to invasions and informing optimum allocation of effort for surveillance. Direct and indirect effects of the introduced alga Sargassum muticum on benthic.J. Gerrodette. 2007. Fridley. 2004.D. K. Effects of Posidonia oceanica canopy on Caulerpa taxifolia size in a north-western Mediterranean bay. the role of disturbance. a potential problem in early detection is looming rapidly. Chapman. Takayama. Stachowicz and S. D. Balcer. Fukuyo. 1999.. Currie. Piazzi and D.R. succession and stability. MuckleJeffs. J.W. molecular genetics skills. Coda We have identified a raft of questions and challenges that will. R. Seaweed ecologists are occupied with many of the questions that are more broadly considered in invasion biology. N. No task is more pressing how- w135x . Rapid response to new introductions requires being able to identify an alien species as soon as it establishes. With declining funding for taxonomy and fewer taxonomists being trained worldwide (Godfray 2002. Elith et al. Crawley. Gervis. Int. J. D. J. New species for coastal aquaculture in the tropical Pacific – constraints. M. Prog. P. Maggs.J. M. Chapman. 2007). V. 2006). From introduced species to invader: what determines variation in the success of Codium fragile ssp. Patch dynamics and stability of some California kelp communities. campaigns to completely eradicate alien invasive seaweeds. eds) Colonization. Sinauer Associates. 7: 207–223. 1999. Sax. pp. J. Pangasinan.J. T. Species introductions and changes in the marine vegetation of Atlantic Canada.M.J. Reavie. Canadian Forest Service. Daskalov.L.F. Blackwell Scientific.A.. L. Long-term changes in fish abundance and environmental indices in the Black Sea. Mar.D. Rosenthal. J. help shape research efforts into invasive seaweeds into the future. Booth.K..M. Exp. will arise through a heady mix and purposeful integration of in situ fieldbased experiments. 2005. how the likelihood. and this surely must include modelling. but also the existence of appropriate taxonomic and. Mar. 429–453. 225: 53–63. Exp.E. There are limited options to control invasive seaweeds once the opportunity for eradication has passed (Anderson 2007). There exist a plethora of both well-established and emerging techniques to predict species’ distributions (Guisan and Zimmerman 2000. not only of seaweed invasions but of invasion dynamics in the broad. P. Bruno. Mays. nature and impact of invasions are influenced by propagule pressure.D. Ser.g. What makes a community invasible? In: (A. 50: 418–437. References Anderson. Ecol. Aquacult. 2002. Bot. and in helping assess various options for control.O. Daskalov. R. 2007. 133–148. Ser. and M. Dayton. In: (D. Given problems with remotely sensing invasive seaweeds. prospects and considerations... Mar.. 280: 1–11. Crawley and P. B. The high cost of obtaining these kinds of data from field-based monitoring begs optimum use of the information. Overfishing drives a trophic cascade in the Black Sea. Prog. hopefully. Yap and H.C.D.J. A. Molecular approaches to the study of invasive seaweeds. Bell. J. Edwards. Ecol.M. G. 1984. eds) Alien invaders in Canada’s waters. pp. This omission is puzzling given that modelling could be highly beneficial in providing understanding of the epidemiology of invasions. Oxford. Ven Tresca.G. Balata. Sturtevant and X. G.F. Azanza. 277: 61–78. Harmful Algae 4: 519–524. Hopkins and Freckleton 2002). Mar. if expensive.D. D. but in every case this has relied on early detection (Anderson 2007). A. K. Insights into ecology. and biology of the invader. Gaines. 2007. Canada and Germany needs to be replicated globally. There have been successful. 2005) which might be a hallmark of many marine invasions (Kinlan and Gaines 2003). Ecol. subtidal communities of Washington State. J. Bromberg and M. Biol. Researchers must take all opportunities to urge their governments to establish regulatory frameworks that minimize the risk of translocating species among bioregions. A. Ser. pp.. Ceccherelli G.V. Meeresunters.D. evolution and biogeography. increasingly. Monog. Gao. and ecological theory. Control of invasive seaweeds. Prog. R. Insights into biotic interactions from studies of species invasions. Ecol. Russell et al.D. Mar. Sunderland. 54: 253–289. ever than the need for better integration of research on invasive seaweed species with ‘‘mainstream’’ theory on ecological invasions. This requires not only implementation of some kind of screening procedure. Chapman. 52: 277–289. 2002. tomentosoides (Chlorophyta) in the North Atlantic Ocean? Helgol. Ottawa. Cinelli. USA. Northern Philippines.S. 240: 19–36. the nature of the recipient community. Mar. The lead taken in establishing pertinent legislation by the governments of Australia. 1999. Claudi. Y.R.S. 2005. Ecol. Scheibling and A. Provan and C. 2003. E. Bot. In: (R. Travis and Park 2004).J. M. there is necessarily a large ‘‘on ground’’ effort if an accurate estimate of the pattern of range expansion of an invasive seaweed is to be ascertained (Meinesz 2007). Gray. 1987.A. 2002. including the effects of unpredictable long-distance dispersal events (e.H. The critical gains in understanding. The response of zooplankton and phytoplankton from the North American Great Lakes to filtration. empirical observation at a range of scales. Bertness. G. L. Mar. Ceccherelli.

W. Species diversity and biological invasions: relating local process to community pattern. 2007.F. 2007. Hou. Card. Oikos 87: 15–26. E. et al.. and stability of Nova Scotian kelp beds. Rice. J. Campbell. D. Propagule dispersal in marine and terrestrial environments: a community perspective. Inouye. H. PLoS Biology 3: 382–388. E.F. 1988.R. 33: 153–157.cbcrmlearning. Science 301: 929–933. Hughes. and R. et al. Dunstan.L.. Ecol. M.E.B. Pickering. AC007E/AC007E00. 2004. Ling and C. C. J.S. and D. Mar. Von Holle.. 2007. Nichols. Invasion of the Black Sea by the ctenophore Mnemiopsis leidyi and recent changes in pelagic community structure. J. Mar. Evol. Jaubert. Feng. R. Fisheries 14: 1–10. and A. Padilla.N. 88: 528–534. Appl. Gurevitch. J. S. 2000. R. Coyer. 18: 227–234. Fish. 2007.): S121–S127. C. and S. Grime and K. Marchioretti. 19: 470–474.A. J. Phycol. patterns of adaptation. D.C. A.M. Connolly. pp. D.M. 1990. P. Community-wide effects of nonindigenous species on temperate rocky reefs. 11: 187–268.. Appl. London. 2002.T. David. Bot.. Tilman and B. www.R. epidemiology.456 C. J. Invasions 5: 3–21. C. Bot. A. deVillele. T.T. Ecology 86: 1602–1610. Harmful Algae 6: 585–600. C. B. 1990.C. M. 2003. 2000. Mack. Prog. Introduced marine plants. Mar. M. K. L. and N. Coral Reefs 16 (Suppl.T.P. P. McManus. Ser.. Nature 417: 17–19. S. T.B.. J. The ecology of invasions by animals and plants.X. Cadavos. Campbell and B. Simberloff. Voigt. The invasion paradox: reconciling pattern and process in species invasions. Bot. Godfray. 2005. 2007. Ser.X. Climate change. C. K. Hewitt. Freckleton. Tropical marine fisheries and the future of coral reefs: a brief review with emphasis on Southeast Asia.K. J. Harrison. Bot.L. 2000. Thompson. Kyo. Melbourne and K.H. Ribera.L. USA) by the Asian clam Potamocorbula amurensis. Johnson and C. Phycol.A. Levin. Remarkable invasion of San Francisco Bay (California.W. Rev. Conserv.C. Fielman. Elton. M. 1998.. Pickering. Hewitt and Y. McManus. Burnaford and K.A. 50: 338–350. Development of mariculture and its impacts in Chinese coastal waters. Modelling 135: 147–186. Clout and F.J. Are invasive species a major cause of extinctions? Trends Ecol. 2002.D. Moore. Biotic invasions: causes. Hewitt. Ross. Predictive habitat distribution models in ecology.C. Berger. 2005. Smith.M. 2002. and C. Invasions 7: 251–263.J. Ostenfeld. 20: 305–311.J. Anim. Davis. Dudık. Roberston and B.W. Res. Minghelli-Roman. M. On the immigration of Biddulphia sinensis Grev.H.. Bot. human impacts..R.M. (2001). M. Mar. Historical overfishing and the recent collapse of coastal ecosystems. Biol. Stachowicz.O. Ping. Hewitt. E. Displacement of a former community. 58: 129–154. Lonsdale. Monogr. Naeem.P. M. II. 50: 373–384. 7: 305–310. Bazzaz. G. Gaines. Schaffelke. J. B. Mar.K. 2007. Chapman. 50: 438–450. 150–179. Introduced macroalgae – a growing concern. Russell. Seabloom. Shiganova. M.htm. Boudouresque.. Challenges for taxonomy. Bot. ´ Guisan. J.M. Seaweed invasions: introduction and scope. 361–372. Thompson and L.E. 18: 529– 541. Mar. N. Project Report SCS/ 77/WP/60.H.R. In: (E. Hofmann. D. 263: 75–82.Y. S. 2007. J. McConnell and D. Schaffelke. Good.W. Morrow and H.. D’Antonio.L. C. Hewitt.D. South China Sea fisheries development and coordinating programme.L. Folke.J. Elton revisited: a review of evidence linking diversity and invasibility.H. M. Oceanogr. The Bolinao community-based coastal resources management project (initial phase): Towards an interdisciplinary approach. B. global consequences and control. Science 288: 852–854. M. H. L. Gilpin. Evol. CBCRM Resource Center. T.P. C. Jackson. Ferrier. 2005. Anderson. J. 50. A preliminary survey of the distribution of the introduced macroalga. Appl. Mar.fao. B. Doelle. Ecography 29: 129–151. Botstord. et al. Science 248: 88–89. Gollasch.. and K. Spatial heterogeneity explains the scale dependence of the native-exotic diversity relationship. dela Cruz and A. B. Smith. and M.E.L. M. A. Schemel. Sulu. Childs and L.D. Ecol. Mar. Undaria pinnatifida Harvey Suringer on the East Coast of Tasmania. L.I. Novel methods improve prediction of species’ distributions from occurrence data. Bot. 2002. 2003.A.M. Australia. 50: 321–325. Science 293: 629–637. and C. A. Real. Schaffelke. Seaweed resources and their culture in the South China Sea region. 1995. S.D. Advances in seaweed aquaculture among Pacific Island countries. Fish Biol. Zimmerman. eds) Seeds of hope: a collection of case studies on communitybased coastal resources management in the Philippines. Y.P. C. 1997. Petrik and T.. 1999. Johnson. M. Predictive spatial dynamics and strategic planning for raccoon rabies emergence in Ohio. D. Meinesz.L. Ecol. Johnson: Seaweed invasions: conclusions and future directions Davies. 1995.. Ecology 88: 3–17. Re-evaluation of the extent of Caulerpa taxifolia development in the northern Mediterranean using airborne spectrographic sensing. Kirby. 2007. Ecol.P.S. Chesson. M. with special reference to macroalgae: mechanisms and impact. 36 pp. Biol. and the resilience of coral reefs.J. Levine. T. C.D. Genomics-fueled approaches to current challenges in marine ecology. 10: 689–710. Methuen. 2006. 1908. J.R. 2004. University of the Philippines. Skeleton and R. Diversity. 50: 397–417.K. Smith and C. N. Fridley.D. R. dela Cruz. Schaffelke. Fluctuating resources in plant communities: a general theory of invasibility. Impacts of introduced Introductions of seaweeds: accidental transfer pathways and mechanisms. Phycol. M. Johnson. Mar. VanderZwaag. 5: 245–249. Hewitt. and its occurrence in the North Sea during 1903–1907. Ecological prediction.E.-F. T. Mann. Meddelelser fra Kommissionen for Havundersogelser. Domingo. Graham. B. Ecol. Prog.. 2005. Critical review of the IMO international convention on the management of ships’ ballast water and sediments.H.H. J. Fukuyo. Changes and degradation ´ in a Posidonia oceanica bed invaded by the tropical alga Caulerpa taxifolia in the North Western Mediterranean.M. Ecology 84: 2007–2020. Kinlan. Murfet. http://www. T. Doty. Johnson. 2000. Chisholm. J. J. 50: 326–337.L. 66: 95–101. L. 2007.W. Levine. 2003. Mar. Sax. pdf. D. F. 1958.R..E. Bellwood. Bourque. and C.A. Ferrer.L. Grosberg. Guisan. w136x . R. Trends Ecol. 2006. J. Elith. Mechanisms of invasion: can the recipient community influence invasion rates? Bot. Invasive seaweeds: global and regional law and policy responses. Ecol.J. Intentional introductions of commercially harvested alien seaweeds. Bjorndal. P. Verlaque. FAO. Methods for identifying and tracking seaweed invasions. P. J. Declines in the number of amateur and professional taxonomists: implications for conservation. Evans. B.J. J.A.A.A. A. M.S.R.M. Sanderson. 2006. F. 1977. Bot. K.R. X. and C. C.. Ecology 83: 182–3193. 2003. 1990. Dragsund.P. Stohlgren. 38: 79–87. Ferrer. Baird.. Ripley. Efficacy of physical removal of a marine pest: the introduced kelp Undaria pinnatifida in a Tasmanian Marine Reserve. S.L. Hopkins. M. J. C.R.D. Plankton 1: 1–25. L.H. Prog.P.. W.. Mar. M. J. McEnnulty. Assessing the ecological impacts of an introduced seastar: The importance of multiple methods.

272: 171–189. Ruiz. 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.. 1998. 41–64. In: (D. 285: 43–55. predation upon a venerid clam. M. C. and A. Stachowicz and S.P.D. The varying success of invaders. Valentine. 1999. Bot. Trono. Oceanogr. Gurney. Exp. Persistence of the exotic kelp Undaria pinnatifida does not depend on sea urchin grazing. Mar. Johnson.R.P. Valentine. C. Diversity of the seaweed flora of the Philippines and its utilization. Spatial structure and the control of invasive alien species. Johnson.R. Johnson: Seaweed invasions: conclusions and future directions 457 Simberloff.J. Fitter. Johnson. 2006. Prog. 2004. Tilman. Mar. unfortunate metaphor. 50: 351– 360. evolution and biogeography. Gaines. R. W. Mechanisms of invasion: establishment. Biol. Invasion dynamics of the European shore crab.P. R. C. important phenomenon. Biol.M. Williamson.M. Carcinus maenas. Sax. C. Stachowicz. 9: 912–919. Hydrobiologia 398/99: 1–6. Ecol. Proctor and G. G. 2007. Species invasions and the relationships between species diversity.P.D. Invasions 1: 21–32.R. in Tasmania (Australia). Rodriguez and N. J.R. MacKinnon. w137x . Invasional meltdown 6 years later. 2003. Walton. Valentine. J.J.C. Thresher. 7: 321–330.F. 48: 106– 115. Simberloff. Mar. and ecosystem functioning. 2002. Ruiz. Johnson. J. Von Holle. Trowbridge. Park. 1996. Rodriguez. Walton. Valentine. and C. Biol. R. L. Katelysia scalarina. 2005a. J.F.H. Ecol. 1999.J. and B. eds) Species invasions insights into ecology. Mar.C. Carcinus maenas. J. J. Ann. Sinauer Associates. 2003. L. or both? Ecol. 2005b. Effect of an invasive crab upon a marine fishery: green crab.R. Biol. and D. Ecology of the green macroalga Codium fragile (Suringar) Hariot 1989: invasive and non-invasive subspecies. and C. Sunderland. and K. J. Ecology 77: 1661–1666. Ecol. pp. W. Mar. D. G. MacKinnon. Rev 36: 1–64. J. 2005. Exp. Lett. 295: 63–90. 142: 867–876. Positive interactions of nonindigenous species: invasional meltdown? Biol. Conserv. D. Bot. in Australia. spread and persistence of introduced seaweed populations. community saturation. Mar. and C.. Bax.J. Magierowski and C. Travis. C. Anim.C. Ser. J. Establishment of the introduced kelp Undaria pinnatifida in Tasmania depends on disturbance to native algal assemblages.. Mar. Proctor.


USDA-Agricultural Research Service Exotic and Invasive Weed Research One Shields Ave. Marine Research Laboratories Tasmanian Aquaculture and Fisheries Institute University of Tasmania GPO Box 252-49 Schaffelke. David School of Biological Sciences Queen’s University Belfast BT9 7BL Northern Ireland E-mail: d. National Centre for Marine and Coastal Conservation Australian Maritime College Private Mail Bag 10 Rosebud. Tasmania 7001 Australia E-mail: Joseph.J. CA 95616 USA E-mail: lwanderson@ucdavis. David Provan. Marine & Environmental Law Institute and Dalhousie Law School Dalhousie University School of Zoology and Tasmanian Aquaculture and Fisheries Institute University of Tasmania GPO Box 252-05 Hobart.booth@qub. CSIRO Marine and Atmospheric Research GPO Box 1538 Hobart.O. Anthony R. Lars W. Regina H. School of Zoology and Tasmanian Aquaculture and Fisheries Institute University of Tasmania GPO Box 252-05 Hobart. Christine A. School of Biological Sciences Queen’s University Belfast BT9 7BL Northern Ireland E-mail: c. School of Marine Studies The University of the South Pacific Private Mail Bag Suva Fiji Islands E-mail: pickering_t@usp. Victoria 3939 Australia E-mail: . NS Canada B3H 4H9 E-mail: achapman123@gmail. Marnie L.Author information Joseph P.mcconnell@dal. Chapman.maggs@qub. Craig Valentine. Solomon Islands Center The University of the South Pacific Britta CRC Reef Research PO Box 772 Townsville. Tasmania 7001 Australia E-mail: Regina. Chad Magierowski.Magierowski@utas. Timothy D. Reuben J. Tasmania 7001 Australia E-mail: Craig. Victoria 3939 Australia E-mail: alloceans_ecology@yahoo.O. Moira L. Marine & Environmental Law Institute and Dalhousie Law School Dalhousie University Tasmania 7001 Australia E-mail: Piers. Piers K.Valentine@utas. Box 460 Honiara Solomon Islands E-mail: sulu_r@usp. NS Canada B3H 4H9 E-mail: Meinhard. Queensland 4810 Australia E-mail: Queensland 4810 Australia E-mail: Maggs. Meinhard Marine & Environmental Law Institute and Dalhousie Law School Dalhousie University Halifax. Box 1539 Townsville. NS Canada B3H 4H9 E-mail: David. National Centre for Marine and Coastal Conservation Australian Maritime College Private Mail Bag 10 Booth. Department of Biology Dalhousie University McConnell. Jim School of Biological Sciences Queen’s University Belfast BT9 7BL Northern Ireland E-mail: j. Posa International Ocean Institute Regional Center for Australia and the Western Pacific P. Alexandre Laboratoire Environnement Marin Littoral Université de Nice-Sophia Antipolis Parc Valrose 06100 Nice cedex 2 France E-mail: Dunstan. NS Canada B3H 4H9 E-mail: moira.


23. 131 diclobenil. 88. 53. 59 AFLP analysis 71 AHTEG 120. 81. 66. 8. 124. 118. 101. 68. 90. 134 Antithamnionella elegans 56 Antithamnionella spirographidis 13 Antithamnionella ternifolia 13 aquaculture (mariculture) 2. 12. 50. 111 carrying capacity 44 cartography 53–64 CASI spectrographic imaging 57. 8. 59. 26. 91. 13. 18–30 Commission for Environmental Cooperation → see CEC community composition change 78. 90. 34. 77. 82. 62. 71. 9 bottleneck. 134. 132. 90. 13. 70. 58. 111. 13. 99. 25. 87. 25. 122. 10. 84. 119. 67. 121 Bonnemaisonia hamifera 13. 10. 24. 59. 33. 119. turbinata 70 Caulerpa scalpelliformis 56 Caulerpa taxifolia 3. 47. 21. 72 benthic sled 58 Bern Convention 25. 103. 132. 11. 50. 24. 84. 133 Conference of the Parties (COP) 120. 108. 56. 71. 106. 6–17. 112. 10. 121 Code of Practice for Introductions and Transfers of Marine Organisms 11. 119. 12. tomentosoides 2.Fouling Systems on Ships 4. 13. 101. 32. 88. 127 Convention on Harmful Anti. 129 biodiversity protection 119. 133. 20 cryptic invasions 3. 60. 38. 21. 4. 54. 53. 114. 35. 70. 70. genetic 3. 132 aquarium trade 6. 84. 57. 90. 104 Bonn Convention 118. 101. 123 algal types (strategic resource allocation) 2. 66. 90. 113 biosecurity (→ see also quarantine) 6. 78. 89. 69 burden of proof 18. 107. 118. 131. 105. 56. 49 conserved gene sequences 67 Constitution of the Oceans 119 containment of introductions 9. 85. 119. 26. 109. 111 Acrothamnion preissii 53. 86. 71. 87. 79 boring organisms 7. 78. 61. 23. 27. 66. 80. 88. 124. 37. 87–89. 8. 90. 68. 21. 99. 123. 42. 32. 8. 31. 132. 85–86. 99. 54. 31. 10. 34. 126. 8. ecological 1. 50. 79. 122. 113. 92. 70. 122. 79. 34. 66. 24. 37. 69. 54. 123. 67. 49. 37 aluminum to control introductions 108. 35. 8. 110. 33. 35. 56. 55. 79. 66. 120 biodiversity → see species richness biogeographic region (bioregion) 1. 108. 78. 135 Convention on Biological Diversity (CBD) 4. 77. 33. 131 COP → see Conference of the Parties copper to deter introductions 7. 110 amphipods 26. 44. 21. 102. 28. 125. 104. 8. 104 Caulerpa mexicana 55. 20. 25. 24. cylindracea 53. 108. 65. 24. 62. 18–30. 37. 100. 132. 133 command and control protection 128 commercial seaweeds 19. 8. 57. 85. 7. 67. 132. 89 community dynamics. 81. 92. 126 contingency response 120. 133 Asparagopsis 20. 8. 67. 45. 55. 9–10. 43. they are marked in bold face) aboriginal issues 124 Acanthophora spicifera 21. 57. 57. 41. 121 connectivity 41. 66. 119. 113. 102. 120–128. 56. 88. 114. 99. 112. 84 Ascophyllum nodosum 4. 89. 66. 82. 11. 55. 57. 118. 134 barren grounds 34. 107. 91 Asparagopsis taxiformis 56 assignment tests (genetic) 71–72 Avrainvillea amadelpha 79. 90. 65. 38. 6. 26. 4. 35. 43. 131 acetic acid to control introductions 107. 61. 87 adaptive radiation 66 aerial photography 57. 18. 110. 103. 46. 107. 108. 28. 80. 36 Bayesian methodology 68. 46. 47. 12 ballast water 1. 22. 78. 91. herbicide 107. 54– 55. 68. 128 canopies of algae 21. 113. 22. 35 dispersal 4. 104–107. 3. 91. herbicide 107. 98. 71. 110. 107. 85 decline in canopy algae (global) 36 Desmarestia aculeata 82 detection of aliens 3. 133. 55. 100. 44. 125 Ceramium 10 Chara connivens 9 chlorine to control introductions 98. 133 carfentrozone. 81 caulerpin 81 CEC 124. 12. 82. 134. 87 BACI sampling 84. 54. 54. parvifolia 89 Caulerpa filiformis 79. 109 acrolein. 45. 91 Asparagopsis armata 56. 127. 7. 4. 23. 135 developing (less-developed) countries 2. 112 alien species. 35. 25. 121. 80. 87. 131. 19. 6. 56. 102. 70. definition 54 allele frequency 65. herbicide 111 diquat. 31. 58. 80. 9. 121 Codium fragile ssp. 91. 69. 131 Corallina 33. 7. 134 comb jelly 77. 44. 10. 108. 36. 31. 91. 131. 27. 60. 10. 56. 72 allelopathy 113 alpha diversity 134 alternative stable states 36. 122. 18. 77. . 121. 31. 59. 126 ascidians 9. 36. 135 biological control of introductions 22. 24. 47. 35. 133. 36–38. 104 “cottonii” cultivar 19. 56. herbicide 107. 105. 38. 33. 125. 20. 121. 132 caulerpenyne 80. 27. 131. 105. 49 complexity of communities 31. 23. 131. 121. 99. 36. 69. 70. 3. 132 competitive reversals 46. 37. 13. 4. 67 Caulerpa ollivierii 89 Caulerpa racemosa var. 91. 119. 27. 87. 13. 10. 84. 35. 86. 123. 59. 99. 34. 35. 98. 78. 92. 50. 43. 113. 78. 101. 26. 11. 34. 33. 46. 69. 43. 120. 128. 36. 103. 34. 20. 32. 69. 71. 45. 82. 87 accidental/unintentional introductions 1–3. 135 disturbance (ecological) 3. 10. 118 clonal reproduction. 82 algicide 107. 59. 87. 131. 38. 91 ctenophore → see comb jelly Cymodocea nodosa 79. 77. 36. 55. 27. 9. 119. 109. 62. 9. 53. 87. 102. 90. 50. 69 Code of Conduct for Responsible Fisheries 4.Subject index Special Issue Seaweed Invasions (Note: Grouped entries refer to expansive treatment of a topic. 48. 128 control of introductions 1. 98. 123. 12. 13. 49. 120. 22. 92. 88. 13. 106. 33. 118. 122. 86. 89. 84. 89. 59 Caulerpa brachypus var. 87. 41. 109. 104. 79. 11. 104 asian clam 77. 24. 68. 45. 122. 32. 120. 11. 22. 55. 123. 9. 90. 53. 134 compensation plans 128 competition 3. 111 disease 11. 19. 20. 118. 86. 12. 56. 36. 7. 127 BWM Convention 2004 11. 110 coral reef degradation 18. 126. 47. 87. 112. 83. 42. 4. 35. 72. 82 ancient DNA (herbarium) 68 anemones 90 Antarctic Treaty area 123 anti-fouling compounds 4. 60. 27. 87. 58. 66. 85 bait 8. 33. 98–117. 59. 67 balance of nature 41 ballast dry/semi-dry 7. 111 ciliates 81 climate change 4. 12. 110. 10. 33. 10. 65. 37. 86. 91. 21. 77. 83. 106 Caulerpa racemosa var. 81. 81. 10. 54. 78. 122. 85. 81. 77. 50. 58. species 50. 21.

65. 69. 112. 111 health. 38. 11. 134 experimental approaches 1. 20. 70. 102. 113. 134. 110. 65–76. 70. 121. 33. 91 Fucus serratus 3. 108. 107. 110. 26 Hizikia fusiformis 19 homogenization. 82. 35. 131. 126. 119. 83. 19 Gigartina skottsbergii 19 global sectoral initiatives 121–123 global warming 36. 105. 55. 126. 20. 35. 128. 105. 50. 44. 104. seaweed 2. 105. 118. 121. 37 ICES Code of Practice on the Introduction and Transfers of Marine Organisms 24. 81. 112. 83. 22. 25. 90. 86. 106. 65. 127 heat to kill invaders 8. 90 grazing/herbivory 3. 134 genetic consequences of invasion 2. 131 fitness 66. 81. 118. 12. 91. 45. 98. 53. 135 levels of invasion 48. 99. 21. 66. 44. 114. 67. 36. 113. 10. 66. 18. 113. 89 feedback mechanisms 11. 55. 127. 37. 120. 112. 124. 98. 8. 127. 132. 119. 55. 27. 91–92. 99. 24. 86. 40. 81. 23. 135 Eucheuma denticulatum 18. 22. 107. 78. 67. 89. 134. 89. 33. 62. 71. 31. 71. 132 limiting similarity-model assumption 43 “live” rock 10 live seafood trade 6. 132. 98. 87. 54. 4. 41. 10. 133 ecological theory 1. in water 12 hull fouling 1. biotic 77 hull cleaning. 104. 112. 23. 87. 118–130. 98. 68. 104. 110. 113. 69 fluridone. 99. 34. 93. 92. 135 expressed sequence tags 70 extinction 44. 59. 91. 118. 14. 77. 134 Laminaria japonica → see Saccharina japonica land-based aquaculture 11. 6. 90. 111. 21. 91 Fucus spiralis 70 Fucus vesiculosus 70. 90 Grateloupia doryphora 55. 6. 55. 20. 86. 69. 133. 111. 21. 22. 27 Law of the Sea (UNCLOS) 4. 85. 91. 65–76. 107. 19. 67 ITS sequences 67. 78 invasibility of communities 13. 7. Heterosiphonia japonica 13. 37. 9–11. 33. 25. 120. 114 Fucus ceranoides 70 Fucus evanescens 3. 13. 108 Gulf of Maine Action Plan 125 Gulf of Maine Council 124. 50. 135 diuron. 123 legal issues 3. 2. 121 IMO (International Maritime Organization) 118. 102. 58. 135 establishment of introductions 2. 36. 9. 110. 77. 23 Eucheuma striatum 82 eucheumoids 19. 98–117. 111. 91. 12. 80. 70. 53. 3. 77. 13. 134. 131 Jakarta Mandate 120 Kappaphycus alvarezii 10. 20 European initiatives on invasives 125 evolutionary consequences of invasion 56. 101. 33. 112. 55. 135 economic incentives 128 economic instruments 128 economics 1. 26. 70. 121. 110. 60. 9. 90. 132. 41. 85. 118. 82. 10. 32. 134 effective population size 68. 27. 62. 13. 83. 121 Halophila hawaiiana 79 hand removal of introductions 103. 24. 121 FAO Guidelines for Responsible Fisheries 24. 122. 92. 55. 89. 109. 25. 121. 128. 11. 134 genetic impoverishment/depauperacy 68 genetic integrity 66 genetics 2. 120. 133. 86. 103. 67. 119. 11. 70–71. 77. herbicide 107. 124. 20. 36. 67 eradication of introductions 3. 3. 135 genomics 2. 20. 131. 55. 26. 110. 135 industry. 34–35. 86. 127. 65. 36. 26. 50. 22. 84. 10. herbicide 111 environmental forcing 37. 71. 91. 82. 35. 41. 12. 91 FAO Technical Guidelines on the Precautionary Approach to Capture Fisheries and Species Introductions 121 fecundity of algae 10. 118. 11. 25. 91. 119. 37. 88 Hypnea musciformis 21. 41. 88. 129. 125. 31. 110. 112. 36. 87. 99. 125. 112. 98. 102. 102. 10. 23. 37. 102. 113. 49. 134 invasive species response model 100. 78 hydrogen peroxide as control agent 109 hydroids 84 Hypnea 19. 104. 31. 33. 8. 109. 22. 60. 41. 11. 107. 110. 78. 118. 90. 18. 104. 132 endothall. 34. 65. 119. 131. 21. 37. 67. 85. 113 dry dock hull cleaning 11. 77. 42. 89. 32. 92. 24. 77. human 78. 78. 88. 105. 82 heterozygote deficiency 69 hexazinone. 67. 3. 25–28. 107. 127. 12. 27. 43 invasion process 1. 102. 50. 88. 66. 59 liability (legal/financial) 120. 133 ISSR markers 55. 13 Lomentaria hakodatensis 13 Macrocystis pyrifera 25. 118. 77–97. 103. 47. 128 life history 2. 89 fish 8. 87. 34. 31. 11. 22. 87. 70 IUCN “100-of-the-worst list” 21 IUCN 7. 121. 56. 118–122. 110. 12 drying for control/eradication 105 Ecklonia radiata 108 ecological consequences of invasion 1. 61. 71. 62. 12. 32. 20. 79. 107. 6. 83 functional traits of seaweeds 6. 59. 82. 77. 123. 134. 38. 34. 131. 121. 122. 33. 26. 28 kelp forest 3. 34. 8. 53. 122. 106. 121. 134 green crab 133 growth rates of introduced species 32. 35. 4. 112 glyphosate to control introductions 108 Gracilaria coronopifolia 106 Gracilaria edulis 22 Gracilaria salicornia 21. 87. 18–30. 78. 112. 109. 87. 27. 83 management by resource limitation 110 . 3. 119. 46. 134 ecosystem 20. 89. 13. 88 hystereses. 133 fishing 4. 18. 68. 2. 90. 24. 121. 57. 109 freshwater to control introductions 10. 92. 33. 32. 23. 69. 132. 33. 78. 42. 120. 86. 69 FAO 19. 35. 19. 70. 87. 104 haplotype network 69 Hawaii 10. 90 Grateloupia subpectinata 13 Grateloupia turuturu 13. 132. 118–120. 89. 82. 123. 33. 134 hybridisation 3. 87–89. 50. 118. 54. 78. 133. 55. 25. 78. 31. 112. 82. 18–30. 72. 121. 56. 31. 122–126. 24. 98. 77. 105. 18–30. 133. 7. 70. 123. 23. 82. 2. 78. 131 impact assessment 119 impacts of introductions 1–3. 57. 122. 68. 78. 106. 126. 113 herbicides 98. 66. 32. 69 Elton 41. 119. 31. 107. 42. 132. 27. 98. 91. 90. 80. 85. 23. 65. 131 International Convention for Management and Control of Ships’ Ballast Water and Sediments → see BWM Convention 2004 International Convention for the Prevention of Pollution from Ships 73/74 → see MARPOL 73/74 introgression 66. 14. 58. 27. 10.Subject index 81. 65. ecological 31. 32. 119. 6. 22. 34. 56. 9. 103. 24. 48. 112 insurance 128 intentional introductions 1. 105. 91. 90 furanone. 36. 36. 128. 113 142 freshwater weeds 98. 98. 125 Gymnogongrus crenulatus 9 habitat change 4. 78. 24. 101. 114 invertebrates 8. 108 Gracilaria vermiculophylla 68 Grateloupia 9. 126. 111 drainage to eradicate introductions 103 dredging for control/eradication 102. 133. 36. 90. 68. 86. 92. 120. 24. 78. 2. 124. 32. 133 Gigartina 10. 21. 2. 82. 72. herbicide 111 “hitch-hikers” 2. 86. 128. 81. 27. 88. 88. 131–133. 107. 87. 56. 98. 66. 18. 27. 36. 70. herbicide 108. 91. 13. 37. 127. 15. 81. 3. 21. 37. herbicide 108 gamma diversity 134 gastropods 104 gene pool composition 65. 6. 11–13. 26. 9. 65. 92. 125. 106. 2. 3. 87. 78. 133 invasional meltdown 90. 26. 66. 90. 92. 77. 135 legislation 4. 99. 84. 25. 48 equilibrium view of communities 43. 87. 21.

113. 133. 86. 53. 37. 22. 101. 23. 134 PCR 67. 24. 65. 24. 23. 102. 69. 131 polychaetes 26. 2. 80. 49. 26. 33. 23. 13. 79. 87 multiple introductions 3. 9. 122. 109. 110 Pikea californica 67 plastid genome 67. 81. 105. 32. 43. 100. 133 selection pressure (evolutionary) 8. 87. 26. 88. 98. 58. 85. 114. 89. 112. 104. political 1. 59. 123. 103. 112. 57. 65. 57. 71 shipping 4.34. 90. 124 public education (outreach) 3. 33. 66. 43. 28. 54. 23. 104. 65–76. 20. 135 mapping (→ see also cartography) 53–64 maritime equipment 8. 124. 50. 86. 135 143 . 108 Sargassum muticum 9. 18–28. 32. 10. 72. 35. 77. 21. 4. 12. 12. 125. 121. 35. 13. 124. 9. 54. 31. 132–135 recruitment 8. 12. 24. 90. 46. 132 sediments 4. 132. 126. 3. algal 4. 109. 107. 36. 135 proportion of aliens in flora 1. 38. 37. 58. 68.Subject index management of introductions 28. 85. algal 2. 84. 26. 132. 9. 135 regulatory tools 127 remote sensing 3. 125. 50. 69. 98–100. 44. 111. 84. 103. 59. 89. 47. 24. 12. 99. 85. 77. 43. 67. 108. 114. 133–135 prevention of introductions 11. 124. 67. 99. 86. 53. 79. 31. 53. 22. 110. 113. 72. 23. 21. 68. 134 resource (commercial wild stock) 6. 68. 122. 11. 31. 88. 83. 57. 4. 38. 135 scientific research. 118–130 pollution 36. 128. 11. 25. 83. 87. 57. 45. 37. 91. 37. 19. 91 Phloiocaulon 8 Phyllospora comosa 84 physiology. 86. 105. 41–52. 92. 53–64. 133 predator impacts 133 predicting introductions 2. 50. 79. 107. 13. 21. 43. 132. 69. 48. 26. 49. 89. 47. 118–130. 90. 35. 14. 68. 124. 127. 110 sampling design 3. 46. 21. 65. 9. 108. 71. 102. 86. 102 sea star 77 sea urchins (→ see also barren grounds) 22. 92. 104. 24. 111. 28. 23. 60. 113. 18. 77. 131 oyster culture associates 9. 27. 82. 34. 25. 36. 50. 104. 110. 70 population structure 65. 47. 90. 135 mortality 42. 133 seagrass 10. 127. 101. 43. 98. 122. 35. 48. community 42. 50. 71 microarrays 71 microsatellite DNA 67. 70. 126. 80. 31. 41. 87. 78. 12. 66. 42. 70. 47. 68 permitting process 128 persistence of introduced species 21. 65. 3. 42. 27. 35. 56. 92. 47. 105. 121. 120. 134 mechanical methods to control introductions 98. 102. 6. 60. 59. 60. 54. 86. 108. 27. 112. 87. 57. 98. 135 molecular markers 67. 84. 131. 11. 92. 23. 102. 35. 42. 70. 88. 99. 133. 25. 133 refugial population 69 regional coordination and cooperation 123–125 regulations. 83. 33. 35. 6. 121 random walk 44 rate of invasion 1. 100. 41. 80. 6. 44. 22. 37. 28. 47. 77. 11. 37. 44–49. 9. 18. 132 pharmaceuticals 19 phase shift (community) 36. 47. 131 mechanisms of invasion 1. 113. 31. 57. 57. 44. 50. 127. 19. legal. 23. 26. 102. 122. 85. 37. 87 MARPOL 73/74 122 mating system 66. 45. 107. 43. 99. 77. 45. 90 national level law and policy 125 Neosiphonia harveyi 83 network topology 43. 85 postglacial colonization 69 precautionary approach/principle 23. 67. 10. 46. 68. 98. 20. 54 ozone treatment 107 Pacific islands 20. 6. 49. 134 niche 13. 18. 119. 127. 27. 12. 132 overfishing 4. 91. 129 predation 2. 105. 19. 128 risk mitigation 2. 66. 42. 91. 105. 38. 56. 37. 22. 48. 110 Posidonia oceanica 80. 72 non-spatial model 44. 118. 59. 104. 132. 86. 120. 50. 134. 118 Ramsar Convention 118. 61. 134. 132 mosaic. 71. 90. 126 rbcL 68 recipient community. 49. 126. 9. 81. 10. 112. 87. 6. 77. 26. 68 molluscs 77. 89. 112. 69 Porphyra yezoensis 9. 34. 101. 35. 36. 85. 28. 28 risk of introduction 2. 36. 24. 104. 33. 80. 11. 33. 128. 80. 36. 110. 104. 118–130. 38. 87. 131. 6. 118. 119. 78. 88. 54. 8. 50. 88. 21. 54. 49 resource supply 42. 32. 101. 50. 102. 56. 118. 60. 80. 107. 48. 53. 11. 104. 118. 68. 11. 106. 134 messenger RNA 65. 101. 84. 69. 22. 4. 27. 33. 102. 124. 31. 125. 38. 132 resource (ecological) use 13. 50. 23. 12. 71. 48. 121. 35. 13. 104. 50. 110. 92. 78. 9. 89. 103. 11. 25. 87. 125. 89. 134. 99. 81. 81. 7. 13 Palmaria palmata 69 parapatric speciation 66 patch structure/dynamics 3. 99. 66. 78. 2. 101. 128. 28. 70. 47. 132. 19. 88. 54. 59 scale (spatio-temporal) 1. 35. 57. 26. 48. 133 satellite teledetection 57. 127. 105. 66. 49. 135 molecular approaches 3. 125 Punctaria 8 QTL mapping 71 quarantine 2. 4. 48 North American cooperation 124–125 North American Invasive Species Network 124 nutraceuticals 19 nutrients (resource for algae) 13. 12. 99. 121. 24. 37. 11. 100. 72. 27. 37. 3. 31–40. 42. 87. 58. 86. 107. 98. 105. 23. 36. 92. 10. 83 Polysiphonia strictissima 68 population dynamics 47. 54. 119. 123. 119. 90. 91. 35. 98. 133 monitoring 4. 11. 104 mixed stock analysis 72 mode of introduction 2. 60. 131–135 restriction fragment length polymorphism 67 rhodoliths 82 Rhodomela larix 83 risk assessment 2. 43. 26. 41. 91. 132. 88. 128. 86. 43. 26. 22. 70 policy responses to alien species 1. 27. 68. 65. Polysiphonia brodiaei 13 Polysiphonia harveyi (=Neosiphonia harveyi) 13. 32. 66. 132. 7. 55. 57. 89. 49 next pest 2. 77. 9. 134. 114. 89. 113. 48. 92. 70. 80.48. 34. 31–40. 49. 133 Membranipora membranacea 34. 28. 19. 121 screw shell mollusc 133 SCUBA survey 53. 102. 49. 100. 126. 35–36. 22. 45. 37. 114. 46. 66. 91. 69. 27. 45. 111. 36. 41–52. 105 microscopic stages 8. 37. 10. 69. 41–52. 68. 36. 126. 9. traits of 2. 131 modelling invasion 41. 120. 57. 25. 69. 102. 79. 106 “sacol” cultivar 20 salt to control introductions 88. 25. 10. 128. 135 scale dependence 1. 90. 8. 110. 18. 135 rotovation for control/eradication 105 ROV (remotely operated vehicle) 57 Ruppia maritima 80. 36. packing material as a vector 6. 82. 92. 54 sacoglossans as control agents 104. 65. 25. 78. 110. 123. alien escapes from 7. 44. 47. 101. 65. 120. 28 Posidonia oceanica 35. 113 resilience stability 134 resistance stability 134 resistance to invasion → see also invasibility 12. 2. 42. 46. 8. 68. 20. 36. 69. 103. 98. 47. 133. 37. 114. 111. 78. 102. 86 Saccharina (Laminaria) japonica 9. 32. 101. 66. 110. 22. 50 resource variability 3. 46. 108. 3. 84. 62. 10. 105. 92. 44. 90. 92. 21. 54. 112. 131 propagules 7. 13. 89. 78. 127 resource (ecological) availability 3. 91 reproduction. 69. 3. 87. 49. 80. 49. 83. 128. 46. 131 proteome 65 public awareness 21. 119. 31–40. 50. 41. 35. 110. 103. 122. 89 response to introductions 1. 10. 110. 53.

25. 66. Womersleyella setacea 56. 82. 111 SNP maps 71 socio-economics 19. 13. 90 spatial organization (individuals) 41. 98. 26. 65. 86 United Nations Environment Program (UNEP) 123 United States Federal Task Force on Invasive Species 125 United States National Invasive Species Act 124 vacant niche 33. 86. 12. 21. 35. 35. 27. 68. 19. 45. 22. 21. 86. 13. 98. 83. 133 subtractive hybridization 71 surveillance 92. 91. 122. 20. 12. 82. 78. 107. 56. 100. 84. 10. 85. 37. 21. herbicide 108. 78. 21. 41. 101. 104. 65. 118. 31. 57. 84. 8. 89. 122. 125. 86. 69. 89. 133 understorey (algal) 33. 54 top-down vs. 92. 49 species co-existence 49. 99. 132. 92. 102. 90. 45. 100. 21. 25. 118. 12. 53. 6. 120. 34. 19. 132. 80. 22. 118. 23. 133. 133. 89. 36. 112. 81. 135 stability of communities 34. 134 synergisms 77. 35. 60. 35. 91. 21. 48. 108. 100 tributyl tin 4. 11. 28. 44. 24. 119. 42. 105. 84. 71 transport → see vectors treatment options for control/eradication 6. 125. 98. 43. 90. 131. 33. 135 TBT → see tributyl tin Thau lagoon 9. 27. 78. 23. 47. 70. 41. 41–52. 27. 83. 134 strategies and action plans (legal/ political) 120 stress tolerance 33 Striaria attenuata 13 substratum 9. 135 survey 1. 85. 22. 101. 81. 102. 86 Zostera capricorni 109 Zostera marina 10. 32. 118. 23. 54. 19. 41. 3. 78. 100. 132. 55. 81. 78. 50 spatially explicit model 43. 109 144 . 36. 132. 80. 105. 55. 77. 4. 91. 132. 131. 65. 91. 134 “spinosum” cultivar 20 spread modelling 59 spread of introduced species 2. 104. 13. 25. 3. 127. 89. 32. 55. 84. 78. 134 sources of introductions 3. 101. 85. 58. 21. 45. 11. 135 transcriptome 65. 54. 62. 53. 12. 91. 90. 88. 11. 54. 33. 26. 33. 37. 85. 134 trophic structure 13. 34. 133 taxonomic training 135 taxonomy 28. 90. 8. 9. 128 space monopolization 77. 43. 119. 67. 113. 89. 85. 22. 134 system management 37 Tasmania 3. 77. 134. 99. 68. 79 species richness/diversity 3. 33. 31. 126.Subject index side scan sonar 57 simazine. 55. 110. 90 Ulva fasciata 82 unavoidable risk 126 Undaria pinnatifida 2. 134 vegetative propagation 3. 37. 77. 10. 18. 54. 2. 66. 104. 54. 86. 86. 123. 23. 91. 18. 121. 35. 88. 36. 26. 25. 132. 18. 70. 77. 127. 10. 99. 6. 89. 84. 77. 103. 84 voluntary compliance agreements 128 von Neumann neighbourhood 45 watch lists 2. 56 Venice lagoon 83. 12. 87. bottom-up invader effects 134 toxicity of invaders 9. 8. vectors of introduction 4. 105. 120. 133. 7. 86. 102. 59–60. 114. 79. 25. 67. 22. 13. 53. 108. 119. 122. 99. 86. 134. 42. 87. 34. 81. 21. 91. 104. 87. 68. 36. 108. 38. 123. 78. 53. 9. 102. 18. 81. 89. 55. 87. 53–64. 78 turfing algae 3. 86 tracking introductions 1. 21 Western Regional Panel 124. 33. 10. 56. 9. 70. 32. 72. 123. 24. 77. 85.

Sign up to vote on this title
UsefulNot useful