Botanica Marina 50 (2007): 338–350 � 2007 by Walter de Gruyter • Berlin • New York. DOI 10.1515/BOT.2007.039

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2007/8

Review

Intentional introductions of commercially harvested alienseaweeds

Timothy D. Pickering1,*, Posa Skelton2 andReuben J. Sulu3

1 School of Marine Studies, The University of the SouthPacific, Private Mail Bag, Suva, Fiji Islands,e-mail: pickering_t@usp.ac.fj2 International Ocean Institute Regional Center forAustralia and the Western Pacific, P.O. Box 1539,Townsville, Queensland 4810, Australia3 Solomon Islands Center, The University of the SouthPacific, P.O. Box 460, Honiara, Solomon Islands

* Corresponding author

Abstract

The two main drivers for intentional introductions of com-mercial macroalgae are (1) increasing global demand formacroalgae and macroalgal products, and (2) increasingneed for alternative and sustainable livelihoods amongcoastal communities in less-developed countries (parti-cularly to reduce degradation of coral reefs) and in theless-developed rural areas of more-developed countries.The macroalgal species that form the basis for commer-cial aquaculture (mainly Saccharina japonica (J.E. Are-schoug) C.E. Lane, C. Mayes, Druehl et G.W. Saunders,Porphyra species, Undaria pinnatifida, Kappaphycusalvarezii, and Gracilaria species) are thus the ones mostlikely to be intentionally introduced to other places. Thehighest-profile cases of ‘‘invasive’’ macroalgae havemainly resulted from unintentional introductions, partic-ularly via shipping. Two cases are species importantcommercially for aquaculture, U. pinnatifida and K. alva-rezii, although the global spread of U. pinnatifida beyondAsia has been caused mainly by shipping. K. alvarezii hasbeen intentionally introduced to many countries for aqua-culture and has been reported as invasive in one localityin Hawaii; however, more recently it has emerged thatEucheuma denticulatum is in fact the main culprit at thislocality. While environmental problems from intentionalintroductions have been few compared with those fromunintentional introductions, it does not appear that com-mercial species are, as a group, inherently any more orless risk-prone than most unintentionally introduced spe-cies. Only a minority of alien species may ever becomeinvasive, but it is difficult to predict which will becomepests. In principle, international norms allow states tointentionally introduce exotic species for commercial pur-poses, provided that environmental threats can be avoid-ed. In practice, the burden of proof and duty of careabout environmental threats and protection of biodiver-sity is nowadays much higher than before. States cannottake it for granted that alien species may be introduced;new proposals should follow formal risk assessment and

monitoring processes that are science-based, andshould be strongly justifiable in terms of ability to provideexpected economic benefits.

Keywords: commercial macroalgae; introductions;invasive; translocations.

Introduction

We review intentional introductions of commercially har-vested macroalgae for stock enhancement or cultivationin a geographical location that is outside the nativerange. This includes both introductions from one countryto another (sometimes called ‘‘exotic introductions’’) andintroductions to a location outside the native range butwithin the same country (sometimes called ‘‘transloca-tion’’; Stickney 2002).

Aquaculture and shipping are the two main vectors forintroduction of alien marine species generally, and thisalso applies to macroalgal introductions (Schaffelke et al.2006, Trowbridge 2006). Introductions of macroalgae viashipping can usually be regarded as unintentional. In thecase of aquaculture, introductions of macroalgae can beeither intentional or unintentional. Unintentional introduc-tions attributable to aquaculture may result from escapeof target species from ‘‘secure’’ culture facilities, or fromintroduction of non-target species (‘‘hitchhikers’’ or‘‘stowaways’’) associated with the target species or withgear and equipment used for culture or transportation ofthe target species (Maggs and Stegenga 1999, Reiseet al. 1999). Almost half of the unintentional macroalgalintroductions documented in Europe are thought to be aresult of transfer of shellfish for aquaculture (Wallentinus2002).

Economic and social imperatives forcommercial-macroalgal introductions

Two main drivers can be identified for intentional intro-ductions of macroalgae, viz. increasing global demandfor commercially important macroalgae and macroalgalproducts, and increasing need for alternative and sus-tainable livelihoods among coastal communities in ruraland less-developed areas.

While attention nowadays is often focused more uponthe adverse impacts of alien species, introductions havebeen regarded historically as a valid means to improveproduction and economic benefits from fisheries andaquaculture. Large industries generating thousands ofjobs and millions of dollars in income are now basedupon aquaculture of alien species, for which relevantcommunities perceive their advantages as outweighingany disadvantages. These introductions took place, how-

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ever, in an era when awareness about possible environ-mental risks, and the unpredictability of risk, was muchlower.

An overview of the history and recent status of globalseaweed utilization is provided by a range of books andreviews, such as Bird and Benson (1987), Critchley andOhno (1998), McHugh (2002, 2003), FAO (2004), and Crit-chley et al. (2006). The main macroalgal species nowbeing commercially cultivated (and hence likely to beintentionally introduced to other places) are Saccharinajaponica J.G. Areschoug, Porphyra species, Undaria pin-natifida (Harvey) Suringar, Kappaphycus alvarezii (Doty)Doty ex P.C. Silva, and Gracilaria species.

Macroalgae form a large component of global aqua-culture production in terms of tonnage but, since theyare of lower value than other aquaculture products suchas crustaceans or molluscs, a disproportionately smallercomponent of value. It might then be expected that theeconomic imperatives behind efforts to introducemacroalgae beyond their native range will also be lowerthan for other aquaculture species, nevertheless there isunsatisfied demand globally for macroalgae andmacroalgal products. This is one basis for continuedinterest to introduce or expand macroalgal cultivation ina number of places around the world.

The demand for macroalgae and their products stemsfrom their uses as food or food constituents, and aspharmaceuticals or nutraceuticals. The great majority ofseaweed production is for food (as a sea vegetable) orfor food additives like carrageenan, agar or alginates(phycocolloids), and these are the main traditional usesof macroalgae. In FAO (2004) the situation is summarizedthus:

‘‘The seaweed industry provides a wide variety ofproducts that have an estimated total annual productionvalue of US$ 5.5–6 billion. Food products for human con-sumption contribute about US$ 5 billion to this figure.Substances that are extracted from seaweeds – hydro-colloids – account for a large part of the remaining billiondollars, while smaller, miscellaneous uses, such as fertili-zers and animal feed additives, make up the rest. Theindustry uses 7.5–8 million t of wet seaweed annually,harvested either from naturally growing (wild) seaweed orfrom cultivated (farmed) crops. The farming of seaweedhas expanded rapidly as demand has outstripped thesupply available from natural resources. Commercial har-vesting occurs in about 35 countries, spread between thenorthern and southern hemispheres, in waters rangingfrom cold, through temperate, to tropical.’’

Only in the cases of species like Kappaphycus alvareziior Gracilaria where large-scale propagation can be veg-etative (so life cycles do not need to be manipulated inshore-based facilities) does aquaculture of macroalgaeas sources of industrial raw materials seem justified(McHugh 2002). Even then, very low-wage economiesneed to be chosen. For example, socio-economic con-ditions appear right for K. alvarezii aquaculture in remoteouter islands of the Fiji Group or Kiribati, but not in themain centers of these countries where there are a rangeof other competing livelihoods (Namudu and Pickering2006). Even in China, aquaculture of macroalgae for algi-nates does not appear economical compared with

mechanical harvesting of natural resources (Jensen1993).

Emerging new uses for macroalgae are as pharmaceu-ticals and nutraceuticals. A pharmaceutical is a sub-stance used in the treatment of disease, whereas anutraceutical is a product isolated or purified from plantsor other foods that is taken in a dosage (non-food) formin order to provide a physiological benefit and/or protec-tion against disease. Also known as ‘‘dietary supple-ments’’ or ‘‘nutritional supplements’’, nutraceuticalsrepresent a middle ground between pharmaceuticals(‘‘drugs’’) and so-called ‘‘functional foods’’. These arelower-volume but potentially high-value uses ofmacroalgae.

Macroalgal species which are now known to containeither pharmaceutical or nutraceutical agents are verywidely represented among the Chlorophyta, Phaeophytaand Rhodophyta. Just a few of the species listed inreviews by Baker (1984) or Smit (2004) include Saccha-rina japonica, Undaria pinnatifida, Gelidium species,Agardhiella tenera (J. Agardh) F. Schmitz, Gigartinaskottsbergii Setchell et N.L. Gardner, Gracilaria species,Caulerpa species, Hypnea species, Hizikia fusiformis(Harvey) Okamura, Sargassum species, Kappaphycusalvarezii, and Codium fragile (Suringar) Hariot. This widerange of species (far wider than the range of popular edi-ble species, and many of wide geographical range) plusthe still-emerging state of research and actual products,makes it very difficult to discern the extent to which phar-maceutical or nutraceutical uses of macroalgae maybecome a driver toward further intentional introductionsof macroalgae.

Meanwhile, demand for the main food and food-con-stituent macroalgal species is large and continuing toincrease. Of all the macroalgal biodiversity potentiallyavailable however, very few species are used commer-cially for these purposes, and even fewer are cultivated.Commercial demand is met by the handful of macroalgalspecies for which large markets already exist, and forwhich either natural stocks are abundant and accessible,or their agronomic traits lend them to large-scaleaquaculture.

It is a general rule that aquaculture (compared with wildfisheries) is based upon relatively few species. This scar-city of suitable species for aquaculture then results intrade and translocation. This occurs either when appro-priate native species do not occur in a country, or whenthere is insufficient information about the culture require-ments of native species to enable commercialization(Stickney 2002). The most likely target species for inten-tional introductions of macroalgae will, therefore, beeither one of the select few high-value, aquaculturedfood species like Porphyra or Undaria pinnatifida, or eas-ily propagated food-constituent species like Kappaphy-cus alvarezii. Such a small group of likely targets shouldgreatly ease the research and risk-assessment demandsposed by intentional introductions of macroalgae foraquaculture, compared with the host of candidate spe-cies that would need to be anticipated in the case ofunintentional introductions.

A second major driver for intentional introductions,particularly of the eucheumoids ‘‘cottonii’’ (Kappaphycus

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species) and ‘‘spinosum’’ (Eucheuma denticulatum (N.L.Burman) F.S. Collins et Hervey), has been demand fornew sustainable livelihoods for coastal communities inless-developed countries, as alternatives to unsustain-able practices that cause degradation of tropical near-shore environments. Providing alternative livelihoods asa means to alleviate poverty and reduce pressure on wildmarine resources is now a major strategy in global initia-tives to protect coral reefs (e.g., the International CoralReef Initiative).

In many countries of Asia, Africa, the Caribbean Seaand the Pacific Ocean, cultivation of macroalgae is wide-ly perceived as one of the most benign types of aqua-culture activity in terms of environmental impacts, andone worth promoting to lessen exploitive pressure onfisheries/reefs and to lessen destructive practices likedynamite fishing (Zertuche-Gonzalez 1998, Ask 1999).For example, the environmental non-government organi-zation (NGO) ‘‘The Nature Conservancy (TNC)’’ has work-ed with park authorities to establish a Kappaphycus sea-weed farming industry in Komodo National Park in Indo-nesia (Howard 2003). The Swedish-funded CORDIOprogramme (Coral Reef Degradation in the Indian Ocean)has identified Kappaphycus aquaculture as one alterna-tive livelihood suitable for some parts of the Indian Oceanregion (Souter 2000, Howard 2003), as have Malaysianacademics seeking to protect the coral reefs of PulauBangii in Sabah (Koh et al. 2002).

‘‘Cottonii’’ and ‘‘spinosum’’ cultivars have now beenintentionally introduced to over 20 other countries bothwithin and outside the native range of eucheumoids (Ask2003, Ask et al. 2003a). A recent review of the history ofKappaphycus introductions in Pacific island countries(Sulu et al. 2004) lists eleven countries in the regionwhere this species has been introduced at one time oranother. There have been multiple introductions to somecountries like Fiji, Kiribati and the Solomon Islands, eitherto introduce new cultivars like sacol, or as part of effortsto revive defunct Kappaphycus aquaculture projects incountries where self-sustaining populations did notestablish.

Kappaphycus farming has been promoted by govern-ments and NGOs because it requires a low level oftechnology and investment, can be operated at thehousehold level, has relatively little environmental impact,does not require refrigeration or high-tech post-harvestprocessing within the country, and is normally compatiblewith traditional fishing and other subsistence uses of theinshore environment. It is a potential source of incomeand employment in rural areas with few other income-generating opportunities, and in particular is an activitythat can provide income for women (South and Pickering2006).

Alternative views about the claimed benefits and envi-ronmental impacts from Kappaphycus alvarezii introduc-tions for aquaculture have been expressed, for exampleby Zemke-White (2004) and Zemke-White and Smith(2006). Nevertheless the prevailing general perceptionthat eucheumoid aquaculture is a good alternative toother much-less sustainable coastal livelihoods in coralreef areas is likely to continue to be a driver for intentional

introductions of the economically-important cultivars ofeucheumoids, both within and outside their native range.

Though strongest in tropical least-developed coun-tries, similar interest in macroalgal aquaculture liveli-hoods also exists in the less-developed rural provincesof more-developed countries. In Ireland, two objectiveswere set for recent seaweed aquaculture developmentinitiatives; one is to meet growing market demands formacroalgae, while the other is to create jobs in ‘‘periph-eral communities in coastal areas’’ (Werner et al. 2004).Arguments for or against such development based upon‘‘utility’’ in terms of contribution to national GDP by thenew seaweed industry tend to under-value their potentialeconomic impact. This is because, although benefits indollar terms will certainly be small relative to GDP, evensmall increases in the income of marginalized or periph-eral communities can make a big difference to peoples’lives. For this reason, seaweed aquaculture projects inAsia, Africa and Pacific islands often enjoy political andcommunity support out of proportion to the potentialcontribution to GDP.

The nature of commercial seaweed species:are they more or less risk-prone with respectto establishment and impact of feralpopulations in exotic locations?

Species that readily establish and which threaten otherspecies or habitats or ecosystems in exotic locations aretermed ‘‘alien invasive species’’, however, the term canbe subjective because it depends upon the investigator’sperspective of what constitutes ecological and/or eco-nomic harm. Not all alien species are ‘‘invasive’’, despitethe recent proliferation of studies using these termssynonymously. Invasive species form high-densitypopulations in which the species are structurally and/orfunctionally major components of the invaded commu-nities (Trowbridge 2006).

Trowbridge’s (2006) review of non-native macroalgaelists approximately 250 species reported to have beenintroduced to new geographic regions worldwide, butnotes marked regional asymmetries including the factthat some regions are much better studied in this regardthan others. Of these species, relatively few havebecome serious ecological pests, although several havebecome very widely distributed and abundant in theirnew habitats. A species of the red seaweed Asparago-psis introduced to the North Sea, probably from Australia(Elton 1958), and the introduction of Asian Undaria pin-natifida to France, New Zealand, Australia, Mexico andArgentina (Hay 1990) are well known examples.

At least three macroalgal species are now regardedinternationally as serious pests, but none of them are ofinterest for aquaculture or commercial harvesting: AsianSargassum muticum (Yendo) Fensholt introduced to thePacific seaboard of North America and to northernEurope; the introduction of a variety of Caulerpa taxifolia(M. Vahl) C. Agardh, possibly from northern Australia, tothe Mediterranean Sea (Meinesz and Boudouresque1996) and most recently to southern California; and theintroduction of Codium fragile ssp. tomentosoides from

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Europe to the Atlantic seaboard of North America(Carlton and Scanlon 1985) and to Australia (http://www.epa.vic.gov.au, Publication 67, April 1999). Char-acteristics and impacts of these species that render them‘‘invasive pests’’ are reviewed by Zemke-White and Smith(2006).

How many alien seaweed species proliferate andbecome aquatic nuisances? Trowbridge (2006) citesBoudouresque and Verlaque’s (2002) report that 8 of 84macroalgal species introduced to the Mediterranean Seaare now ‘‘invasive’’; that of 113 species introduced toEurope as a whole, 27 are ‘‘invasive’’ and 9 are ‘‘veryinvasive’’ (Wallentinus 2002); and that of 19 species intro-duced to Hawaii, 5 have become ‘‘successful’’ (Smith etal. 2002). This is a relatively small yet significant propor-tion of the macroalgal species introduced. In makingsuch comparisons, the potential for differences of inter-pretation about ‘‘invasive’’ must be borne in mind. Soshould the fact that a species can be ‘‘invasive’’ in someplaces but not in others (Trowbridge 2006). It does meanthat the issue of macroalgal ‘‘invasiveness’’ must be tak-en seriously, along with other risks (including the unpre-dictability of risk), whenever intentional macroalgalintroductions are contemplated.

Two indicators of risk for commercially-cultivatedmacroalgae is whether or not any species important foraquaculture is prominent either in the literature on inva-sive macroalgae, or in any of the ‘‘watch lists’’ of invasivespecies maintained by government agencies, environ-mental NGOs, or inter-governmental organizations. Cur-rently, Undaria pinnatifida, and Caulerpa taxifolia appearon the ICUN Global Invasive Species Database’s ‘‘100-of-the-Worst’’ list (ICUN Invasive Species SpecialistGroup, http://www.issg.org). These species and Sargas-sum muticum and Codium fragile ssp. tomentosoidesmake up the four high-profile macroalgal ‘‘invaders’’prominent in the scientific literature. According to Trow-bridge (2006), public-awareness ‘‘watch lists’’ or publicitymaterials about marine invasives currently feature U. pin-natifida (in Europe, USA, Australia, New Zealand, Mexi-co), S. muticum (in Europe), Caulerpa taxifolia (in theMediterranean Sea, California), and (in Hawaii) exoticRhodophyta like Kappaphycus alvarezii, Acanthophoraspicifera (M. Vahl) Børgesen, Eucheuma denticulatum,Gracilaria salicornia (C. Agardh) E.Y. Dawson, and Hyp-nea musciformis (Wulfen) J.V. Lamouroux. Of the aboveten species there are two, U. pinnatifida and K. alvareziithat are important commercially for aquaculture.

Environmental risks in culturing Undaria pinnatifida

Undaria pinnatifida is one of the main commercially har-vested and cultivated species in Asia, and has had itsrange extended by intentional introductions and trans-locations for aquaculture in China (Wu and Pang 2006)and to Atlantic France from Mediterranean France (Floc’het al. 1991), but particularly by unintentional introductionsto Europe, USA, Australia, New Zealand, Mexico andArgentina (see literature reviewed by Casas et al. 2004).The main vector for spread of U. pinnatifida to all of thenew locations outside of Asia has been via shipping (asbiofouling on hulls), with one exception, viz. the contro-versial case of an intentional translocation to establish a

new seaweed aquaculture industry in Brittany (Floc’h etal. 1991). U. pinnatifida has microscopic gametophytestages, and is not known to propagate vegetatively. Asdescribed by Floc’h et al. (1991), translocation to Brittanyfirst occurred in 1983 prior to consideration of risks bythe ICES Working Group on Introductions and Transfersof Marine Organisms during 1984–1989. The decisionwas based upon the hypothesis that, while suitable forsporophyte growth, water temperatures of the NorthAtlantic Ocean would be too cold for the life cycle to becompleted in nature, so that cultivation in coastal watersof laboratory-produced propagules would be ‘‘controlla-ble’’. This hypothesis subsequently proved to beincorrect.

In recent reviews, Schaffelke et al. (2006) and Zemke-White and Smith (2006) point out that Undaria pinnatifidais not considered invasive in some places (such as theMediterranean Sea), nor is it always associated withdeclines in native species richness and abundance.However, it is considered invasive on the Atlantic coastof Europe and has been linked with reduction of nativeseaweed diversity in places like Argentina and New Zea-land. Characteristics of U. pinnatifida that contribute toinvasiveness are its rapid colonization of new or recently-disturbed hard substrata, wide seasonal windows forpropagule dispersal owing to the potential for multiplesporophyte generations within a population, and a pro-pensity for colonizing floating objects (Hay 1990, Valen-tine and Johnson 2003, Valentine and Johnson 2004).These characteristics mean that U. pinnatifida is easilyspread over long distances as biofouling on vessels ormarine equipment. It has a microscopic gametophytestage which, once established in the wild, is virtuallyimpossible to eradicate. Its sporophytes can form largethalli (1–3 m) of a type that can be considered ‘‘invasive’’in the sense of forming high-density populations that arestructurally and/or functionally major components ofinvaded communities. Note, however, that in TasmaniaU. pinnatifida is unable to displace native algae in theabsence of disturbance and that formation of high den-sity stands depends on disturbance to limit native can-opy-forming algae (Valentine and Johnson 2003, 2004).Furthermore, ongoing persistence of U. pinnatifida athigh densities on natural substrata requires persistentmechanisms to limit native canopy forming algae (Val-entine and Johnson 2005a,b). There are no reports tosuggest that U. pinnatifida is regarded as invasive withinAsia in locations outside its natural range. One possibleexplanation is that the species here has commercial val-ue that places it in high demand.

Environmental risks in culturing Kappaphycus

The eucheumoid Kappaphycus alvarezii, introducedintentionally to over 20 countries and territories including11 in the oceanic Pacific (Eldredge 1994, Ask et al.2003a, Sulu et al. 2004, Zemke-White 2004), has beenpublicized as ‘‘invasive’’ in one of those places. K. alva-rezii was intentionally introduced to the Kaneohe Bayarea of Oahu in Hawaii for aquaculture experiments inthe 1970s, and Smith et al. (2002) report that, unlike theother non-indigenous macroalgae they surveyed, K. alva-rezii is still restricted to this one locality; from the original

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point of introduction it has spread at the rate of approxi-mately 260 m year-1 (Rodgers and Cox 1999). However,K. alvarezii is considered ‘‘invasive’’ in Kaneohe Baygiven its high abundance (up to 80% cover) on somepatch reefs in this nutrient-enriched bay where it over-grows corals. For this reason it became the subject of aresearch program and public-awareness campaign toeradicate it and prevent further spread. The publicity gen-erated about K. alvarezii at Kaneohe Bay has led to bansor restrictions upon introduction of this species for aqua-culture in countries of the Caribbean Sea and CentralAmerica (Oliveira and Paula 2003, Alan T. Critchley per-sonal communication).

The situation at Kaneohe Bay in Hawaii contrasts withthe mainly anecdotal evidence (some of which isreviewed by Ask et al. 2003a and Sulu et al. 2004) fromother places where Kappaphycus alvarezii has beenintroduced for aquaculture. Many Pacific island countriesattempted to cultivate Kappaphycus aquaculture duringthe 1980s and 1990s but did not move on to commer-cialization of this species (Luxton 2001) except in Kiribati,Fiji and, most recently, in the Solomon Islands (Pickering2006). In some of these places, the abandonment of K.alvarezii aquaculture trials resulted in the thalli dying out,while in other places there are small residual populationssuch as in some parts of Tonga (Luxton 2001), Fiji Islands(Ask et al. 2003b) and Solomon Islands (Suluet al. 2004). In these oligotrophic reef environments, K.alvarezii may be said to ‘‘persist’’ but it is not ‘‘prolifer-ating’’ (Ask et al. 2003b, Sulu et al. 2004). For example,during a survey of commercial seaweeds in the Kaba andKiuva area of Fiji in 1995 (where K. alvarezii had beenfarmed continuously from 1986 to 1993) only a single K.alvarezii thallus was found (Pickering and Mario 1999); itwas a large (3 kg), unattached callus-like mass with fewapical growing points and exhibiting damage consistentwith grazing by siganid-fish and sea-urchins (e.g., Tri-pneustes gratilla Linnaeus). A farm still operates at Kiuva;this enterprise is destroyed occasionally by severe stormevents; the farmer does not know of any residual K. alva-rezii population in the area, so must move quickly torecover any drifting farmed plants for re-planting beforethey are washed away completely, or else must bring innew cuttings from farms in other parts of Fiji (Timothy D.Pickering personal observations).

Currently, Fiji has two emerging problems with nui-sance algae (May 2005, http://www.etravelblackboard.com/index.asp?ids38688&navs21). However, the spe-cies implicated are native to Fiji and the problems aremost likely linked to anthropogenically driven nutrientloading of near-shore waters by sugar cane agriculture,tourism and piggeries (Lovell et al. 2004). In recent yearsSargassum species have greatly increased in abundanceon many coral reefs, for example along the tourism-developed Coral Coast of Viti Levu. Gracilaria edulis (S.G.Gmelin) P.C. Silva has also become abundant amongsub-tidal seagrass beds adjacent to hotels like the FijianResort on the Coral Coast, and resorts like Beachcomberand Treasure Island in the Mamanuca Group (Timothy D.Pickering, personal observations). Beach-cast material iscreating stench and requires removal and burial at therate of 4 t (wet wt) per day at the two latter resorts alone.

K. alvarezii has not been implicated in any of these pro-blems with seaweeds in Fiji.

The information presented by Smith et al. (2002) indi-cates that, of the five non-indigenous invasive speciessurveyed in their Hawaiian study, the entity they refer toas Kappaphycus alvarezii has the least invasive charac-teristics. Reproductive K. alvarezii plants are rare innature, so the species propagates almost entirely byvegetative fragments. Smith et al. (2002) states that theability to fragment readily, disperse widely before recruit-ment, and re-attach successfully, are all hallmarks of ahighly invasive vegetatively propagating species. K. alva-rezii, on the other hand, is a robust species, negativelybuoyant and so unable to disperse long distances, andfragments do not have the capability of re-attaching tothe substratum. K. alvarezii plants rely on either entan-glement or their sheer weight to stay in place, though thefate of many plants is to become washed away into unfa-vorable habitats and perish. While K. alvarezii can slowlyspread laterally from a point of introduction by fragmen-tation, unlike Undaria pinnatifida it has a very low prob-ability of spreading as a component of biofoulingcommunities on vessels. This suite of characteristics canaccount for its apparent inability to spread over long dis-tances or between islands (Smith et al. 2002).

There are additional factors in the Kaneohe Bay casethat must be taken into account in any discussion of therisk of Kappaphycus alvarezii introductions for aquacul-ture. First, Kaneohe Bay is an urbanized and nutrient-enriched environment, in response to which severalmacroalgal species including natives, for example Dic-tyosphaeria cavernosa (Forsskal) Børgesen (Smith et al.2002), have become ecologically dominant. Second, thelevel of herbivory that might otherwise act as a biologicalcontrol is low in Kaneohe Bay, owing to low numbers ofsea urchins like Tripneustes gratilla (Zemke-White andSmith 2006) as a result of heavy fishing pressure, and tosiganid fishes being completely absent from the Hawai-ian islands (Woodland 1990). K. alvarezii is a palatablemacroalga and siganid fishes are known to exert consid-erable grazing pressure on both farmed and free-livingplants elsewhere (see, for example, Ask 1999, Luxton2001). Thirdly, recent molecular (Zuccarello et al. 2006)and chemical evidence (the plants yielded iota, not kappacarrageenan; E. Ask, personal communication) now indi-cates that the K. alvarezii epithet has been misapplied inmuch of the literature about the Kaneohe Bay problem,because of the misidentification of Eucheuma denticu-latum (another eucheumoid also introduced in the1970s). According to Zemke-White and Smith (2006), thedominant invader in Kaneohe Bay is in fact E. denticu-latum, and K. alvarezii is not nearly as abundant as pre-viously thought. Further, Zuccarello et al. (2006) havefound that K. alvarezii from Kaneohe Bay is a lineagegenetically distinct from the K. alvarezii currently culti-vated around the world. While the problems caused atKaneohe Bay by proliferations of algae such as K. alva-rezii are certainly not trivial, in terms of environmentalrisk, these took almost three decades to develop and arestill at a local, rather than an international or even nationalscale, when compared with other high-profile invasivemacroalgae like Sargassum muticum, Caulerpa taxifolia,Codium fragile or Undaria pinnatifida.

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Do commercial species of macroalgae poseenhanced environmental risks?

Regarding the question ‘‘are commercial species more orless risk-prone’’ than other macrolagae, the answer isthat two of the main commercially-cultivated specieshave gained a high profile for invasiveness, one well-jus-tified and one less-justified. While Undaria pinnatifida iscertainly used for aquaculture in Asia and in France, itsdispersal and rapid establishment globally has beenmainly unintentional due to shipping or to aquaculture ofother organisms, owing to its propensity for spore settle-ment onto floating objects. Laminaria and Porphyra spe-cies have similar reproductive (and hence potentiallybio-fouling) characteristics, and have been unintention-ally introduced to places by the same vectors, but arenot reported to be ‘‘invasive pests’’ in the sense of Trow-bridge (2006).

The characteristics of Kappaphycus alvarezii render itmuch less likely to become invasive, but this species isnot completely without risk as is shown by the KaneoheBay experience. From the information currently available,it is possible to construct cases either in favor (for exam-ple, Zertuche-Gonzalez 1998, Oliveira and Paula 2003) oragainst (for example, Zemke-White and Smith 2006)introduction of K. alvarezii for aquaculture. This will con-tinue to be controversial, and is destined to become aclassic example of the differential application of the Pre-cautionary Principle available to states under interna-tional law when competent authorities weigh up thebenefits and risks of intentional exotic-species introduc-tions. Points raised both for and against are based onarguments ranging from established empirical observa-tion to hypothetical scenarios. Verification of the variousclaims made about socio-economic benefits (for exam-ple, Ask 1999) or environmental risks (for example,Zemke-White and Smith 2006) regarding K. alvareziiintroductions for aquaculture will be fertile ground for fur-ther research.

Advocates for and opponents against intentional Kap-paphycus alvarezii introductions will agree, however, thatanytime a species is introduced intentionally, it must haveclear socio-economic benefits. There are now many cas-es of K. alvarezii having been introduced, often withoutquarantine protocols in place, for aquaculture projectsthat were under-financed, or commercially, socio-eco-nomically or institutionally unsound, or without guaran-teed markets, and so these ventures were set up to failfrom the outset (Ask 2003). By so doing, these statesexpose themselves to the full extent of potential environ-mental risk, without capturing any of the anticipatedsocio-economic benefits against which they had bal-anced this risk. The guidelines and advice provided byMcHugh (2002) and Ask (2003) for anyone contemplatingestablishment of new eucheumoid cultivation projectsare worthy of careful consideration.

The record so far shows that intentional introductionsof commercial macroalgae for aquaculture have causedfew serious effects (Eucheuma denticulatum, not Kap-paphycus alvarezii, at Kaneohe Bay has recently emergedas the main example). The bulk of problems caused byinvasive macroalgae have arisen from unintentional intro-

ductions, either by shipping, or by ‘‘hitchhiking’’ withother organisms introduced for aquaculture (Oliveira andPaula 2003). But what of the future? What new speciesmay be targeted for intentional introductions, and whatspecies already introduced may result in unforeseen pro-blems emerging over longer time-frames?

Environmental risk associated with the introduction ofany commercial macroalgae is, as for any exotic-speciesintroduction, always uncertain. Schaffelke et al. (2006),Trowbridge (2006) and Valentine et al. (2007) review var-ious factors that might assist to better predict whichmacroalgal species may become invasive and underwhat circumstances. These include possible connectionsbetween invasiveness and the latitude of introduction,species diversity of the receiving community (but seealso Dunstan and Johnson 2007), nutrient status ofreceiving waters, degree of anthropogenic modificationof environments, propagule pressure (for example, atnodes for inter-regional vectors such as ports), grazingpressure by herbivores, and the invading species’ envi-ronmental tolerances, growth and reproductive charac-teristics. No useful generalizations have emerged fromconsideration of these factors, apart from propagulepressure, suitability of the habitat, and previous successin other invasions (www.issg.org). These three factorsappear useful to predict whether a macroalga introducedunintentionally will establish and survive. However, thesefactors are all ‘‘givens’’ in the case of an intentional intro-duction for aquaculture (after all, no one will want tointroduce a species for aquaculture that is not going tosurvive) so they are not necessarily predictors of whethera commercial macroalga will become an ‘‘invasive pest’’in the sense of causing negative environmental or socio-economic impacts.

Risk management and risk mitigation ofintentional introductions of commerciallyharvested exotic macroalgae

Environmental, political, regulatory and moralimperatives

Intentional introduction of species, whether for aquacul-ture, the aquarium trade, scientific research or other pur-poses, will always have an element of associated risk.Any introduction poses a potential threat to the ecosys-tem, and two important unknowns are the impact of thealien species on the recipient community, and its per-formance in the new ecosystem.

Decisions about introduction of species rest with thegovernments of sovereign states and not with scientists.Competent authorities will take into account not only sci-entific advice but also social, economic and political con-siderations in assessing whether to accept or rejectproposals for introduction. States are not unfettered inthe exercise of their sovereign right to introduce specieshowever, and must have regard to international normsand to possible responses from the international com-munity or neighboring states.

Policies and norms concerning introduction of speciesare found in a number of the international conventions,

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guidelines and codes of practice that have stemmedfrom the Law of the Sea Convention and Chapter 17 ofAgenda 21. While these are described more fully byDoelle et al. (2007), here we highlight the FAO TechnicalGuidelines for Responsible Fisheries 5: AquacultureDevelopment (FAO 1997) because these explicitly con-template intentional introductions of commercial species.While conventions are binding upon those states that aresignatories, the FAO guidelines are not legally binding butdo carry moral force as an embodiment of internationalnorms.

The FAO Technical Guidelines principles on speciesintroductions include:

• Article 9.2.3 ‘‘States should consult with their neigh-boring states, as appropriate, before introducing non-indigenous species into transboundary aquaticecosystems’’; and

• Article 9.3.2 ‘‘States should cooperate in the elabo-ration, adoption and implementation of internationalcodes of practice and procedures for introductionsand transfers of aquatic organisms’’.

It is implicit in these guidelines that states do notregard intentional introductions of species as completelyprohibited. It is expected, however, that decisions wheth-er or not to introduce should be made in accordance withcodes of practice regarding risk assessments, safe-guards and procedures to avoid environmental threats.This leaves states to grapple with application of a pre-cautionary approach, given that any introduction willhave risks against which prevention is the best defense.Doelle et al. (2007) note that prevention of unintentionalintroductions by placing a prohibition on some activitieslike shipping is simply not possible owing to its utility tosociety, while for other less-compelling activities likeintentional introductions for aquaculture, decision makerswould have to engage in the difficult task of weighing therisk against the utility of the proposed activity. Inso doing, they are likely to also take into account theopportunity costs of not allowing the activity.

Demand to introduce species for aquaculture cantherefore be expected to continue, and the main issuefor resource managers is to have in place mechanismsto assess risks and benefits and, if the decision is affir-mative, strategies to manage the introduction in a waythat maximizes the benefits and avoids, remedies or miti-gates the risks. While international instruments like theFAO Guidelines can be criticized for being non-bindingand for pitting ‘‘utility’’ against ‘‘prevention’’, the factremains that the burden of proof and duty of care regard-ing environmental threats is now much higher than it wasuntil a decade or so ago. States should be urged, per-suaded, pressured and cajoled into adopting and imple-menting these guidelines.

The FAO Guidelines hold up the ICES Code of Practiceas a model for those states or regions that have not yetadopted any guidelines for species introductions (FAO1997). This Code of Practice seeks to address (1) inad-vertent coincident movement of harmful organisms (thatis, non-target species), (2) ecological and environmentalimpacts of the target species, and (3) the genetic impactof alien species (ICES 1995).

The annotations to Article 9.3.2 in FAO (1997) encap-sulate the international norms on introduction of speciesas follows:‘‘Basic elements of codes of practice such as ICESinclude:

• A proposal to introduce a particular species in a par-ticular area for a particular purpose,

• An independent review of the proposal by competentauthority, the review should include ecological andsocio-economic risk assessments, and

• Rejection, revision, or acceptance of the proposal.

Once an introduction has been approved, governmentsshould request aquaculturists to:

• Create a fish health management program includingquarantine and disease diagnosis,

• Monitor and evaluate ecosystem and socio-economiceffects,

• Notify international organizations and neighboringStates.

A country’s ability to carry out the elements of the codewill depend upon the state of knowledge on its humanand aquatic communities and on the financial and humanresources available. Faunistic and floristic surveys oflocal aquatic ecosystems can help determine what localspecies may be affected by aquaculture developmentand what local species may be utilized instead of import-ing an alien species. Socio-economic information on thefishing sector and on the fish-consumers will also helpidentify those people benefiting or at risk from aquacul-ture development. In addition, marketing surveys canhelp determine the cost-effectiveness and target con-sumer for a proposed introduction.’’

Managing intentional introductions in practice

These guidelines provide a useful framework for statesto adopt when contemplating intentional introductions foraquaculture, and many states should, as a first step,base their policies upon them. For marine macroalgae,however, risk mitigation and management of intentionalintroductions has often been poorly implemented(Zemke-White and Smith 2006), and this can be attri-buted to a variety of reasons. First, most of the inten-tional introductions of macroalgae predated thedevelopment of current norms on exotic speciesintroductions.

Second, financial and human resources in many coun-tries (particularly less-developed countries) are insuffi-cient to fully implement all the measures now deemedappropriate. These countries need assistance from theirmore developed counterparts or regional/internationalorganizations to increase their capacity for compliancewith international norms. For the same reason, there is adearth of floristic surveys for some regions, and so it canbe problematic to ascertain the status of a species asalien or otherwise and to assess the impact of an inten-tional introduction once it establishes as a feral popula-tion. A significant problem is that information on thebiology of most marine taxa is relatively limited, and thisincreases scientific and public uncertainty about the out-comes of control actions (Thresher and Kuris 2004).

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Ribera and Boudouresque (1995) noted that it is relativelydifficult for many regions of the world to recognize whichspecies have been introduced, mainly because currentspecies inventories are incomplete or recent, andbecause many authors are reluctant to specify whethercertain species are introductions. For those regions thatare relatively well-known, introductions comprise 4–5%(Mediterranean Sea) to 2–3% of the known flora (Riberaand Boudouresque 1995).

Third, states in several regions lack the capacity forbaseline ecological studies prior to introductions, or forfollow-up monitoring (Schaffelke et al. 2006). Accordingto Zemke-White and Smith (2006) there are no publishedreports that any baseline floristic studies have been takenprior to the introduction of macroalgae for aquaculturepurposes, and there is little literature on effects that theseintroductions may have had on the recipient community’sstructure or function. In the case of Kappaphycus alva-rezii, the reasons given for this were usually either thatfunds were not available for the research, or funds werenot allocated because K. alvarezii was not seen as amajor environmental threat, so was not given high rank-ing among research priorities (Zemke-White and Smith2006).

Fourth, while impacts of the high-profile invasive spe-cies have engaged many researchers’ interest after theyhave become established, and numerous studies onthese species are now completed, there has been verylittle research to support development of appropriatequarantine protocols for intentional or unintentionalmacroalgal introductions associated with aquaculture(Ask et al. 2003a, Sulu et al. 2004). This is an issue thatthe Aquaculture Programme of the Secretariat for thePacific Community has begun to address on behalf of itsmember states (Sulu et al. 2004), but there is scope toimprove recommended protocols further, and extendthem to other target species.

Fifth, most cases of post-introduction monitoring havebeen done over relatively short time-scales following anunintentional or intentional introduction (Trowbridge2006), whereas surveys decades after introduction mayyield different outcomes because the impact of an alienspecies may change over time (Schaffelke et al. 2006).

This whole issue is difficult because, in many cases,the capacity to predict environmental effects is poor,reflecting the fact that invasion biology is a complex andrelatively new area of study (Trowbridge 2006). Under-standing one introduction does not necessarily enableprediction of other introductions of the same species,because of site- or time-specific factors and lack of eco-logical principles with general application (Schaffelke etal. 2006). Proposers of introductions relying upon con-tainment measures must do so on the assumption thatthere will be escape and establishment in the wild (Stick-ney 2002). Further, eradications of macroalgae onceestablished are very difficult and expensive, and havebeen successful in only very few cases where theresponse was rapid and the timeframe since introductionvery short (for example, of Undaria pinnatifida from thehull of a sunken vessel at Chatham Is., New Zealand;Schaffelke et al. 2006). Thresher and Kuris (2004) havenoted that eradication of marine invasive species in gen-

eral has a low probability of success once the invadersare well established.

The only certain way to ensure there is absolutely norisk from a macroalgal introduction is not to introduce it,and instead develop suitable native species for aquacul-ture. For many countries, however, suitable native spe-cies will either be unavailable or have agronomic ormarketing constraints. States balance ecological riskagainst socio-economic benefits, and no state has ruledout the possibility that at some time, in some place, therewill be some species appropriate for introduction.

While introductions are governed by internationalnorms, a further problem, as pointed out by Ribera andBoudouresque (1995), is that texts in various conventionsand agreements are generally couched as recommen-dations, and no authority is designated to assess risks‘‘w«x which leaves the door wide open to whatever inter-pretation the country concerned considers (rightly orwrongly) to best suit its interests.’’ While states are nowclearly expected to move in the direction of giving teethto recommended practices and protocols, the factremains that only a few countries (Australia, New Zea-land, USA, Canada, Germany, Great Britain and Switzer-land) have adopted implementing legislation relating todeliberate introductions of alien species. It is no coinci-dence that 51% of marine macrophytes introduced intoEurope were first introduced in France where legislationcontrolling introductions of alien species is relatively lax.

Progress is being made, however. In Europe alone, atotal of 124 alien species (some of which are macroalgae)have been introduced in association with aquacultureactivities (Zenetos and Strefaris 2004). These authors(op. cit.) note that the rate of introductions has beendeclining recently, suggesting that European Unionmeasures are becoming more effective. The Berne Con-vention in 1979 provides that ‘‘w«x each contracting partyundertakes w«x to strictly control the introduction of non-native species’’. EU directives legislate for the protectionof ecosystems against the adverse effects of aquacul-ture-related introduced organisms (for detail see Zenetosand Strefaris 2004). The Convention on Biological Diver-sity recommends a hierarchical approach, based primar-ily on the prevention of unwanted introductions. Statesin other regions need to be encouraged to adopt similarmeasures, and if necessary should be provided withassistance to develop capacity for their implementation.

Identifying low- and high-risk species

Schaffelke et al. (2006), and Trowbridge (2006) havereviewed the risks associated with invasive macroalgalintroductions, and noted that there is no correlationbetween particular groups (Orders) and the levels ofassociated risk. There are few well documented exam-ples of risk assessment for intentionally introducedmarine macroalgae: well documented case histories,such as those for Kappaphycus alvarezii, Porphyra, Sac-charina japonica and Macrocystis pyrifera (L.) C. Agardhillustrate the fact that the issue of risk came after, ratherthan before, the introductions. While environmentalthreats from intentional introductions of commercialmacroalgae have been few compared with those arisingfrom unintentional introduction by other vectors such as

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Table 1 Criteria to determine the potential risk factors of deliberately introduced macroalgae.

Low-risk High-risk

• Does not cause serious impacts to the environment • Causes serious impacts to the environment• Reproduction and life-cycle non aggressive • Aggressive reproduction and life-cycle• Life-cycle stages can be controlled or manipulated • Complex life-cycle that is difficult to control or manipulate• Not known to out-compete local species when released • Grows rapidly in a new environment and displaces local

species in the wild• Relatively easy to remove/discard if no longer desired • Out-competes local species for space and habitat• Lacks mechanisms or strategies (e.g., vegetative • Possesses mechanisms aiding dispersal such as

propagation) aiding its dispersal vegetative propagation• Causes minimal economic and health costs • Potential high cost of eradication• Has natural predators to help keep it in check • Lack of natural predators in its new environment

shipping, this should be attributed more to the muchgreater propagule pressure posed by, and much greaterdifficulty in regulating, those other vectors. The histori-cally lower threat posed by intentionally introduced spe-cies is not a result of their being intrinsically any more orless risky than unintentionally introduced species.

The determination of low- vs. high-risk speciesremains largely arbitrary for marine macroalgae. In Table1 we suggest some of the criteria potentially useful in thedetermination of low- vs. high-risk species. A number ofintentionally introduced algae, however, do not match allcriteria in either category, possessing intermediate char-acteristics of both low- and high-risk species.

The introduction of Eucheuma/Kappaphycus from thePhilippines into Hawaii, and later into the Pacific Islands,demonstrates the complexity of this issue (summarizedin Sulu et al. 2004). While K. alvarezii (but now known tobe Eucheuma) is regarded as a serious pest at one loca-tion in Hawaii (Zemke-White and Smith 2006), K. alvareziihas failed to establish in many localities in the PacificOcean where it was introduced (Eldredge 1994, Ask etal. 2003a, Sulu et al. 2004). Thus, site-specific informa-tion is needed since the same species may behave quitedifferently in different environments.

Risk assessment procedures have resulted in someproposals for introduction of commercially valuable spe-cies to be declined. For example, plans to introduce thegiant kelp Macrocystis pyrifera into Europe in the 1950sand 1970s were dropped because of public protests anda recommendation from ICES (Boalch 1981). It is possi-ble that this species could otherwise have colonized theEuropean Atlantic coast from Spain to Norway, withunpredictable consequences.

While it is possible to identify macroalgal species thatpose higher or lower levels of risk in terms of undesirableenvironmental or socio-economic impacts, for exampleby utilizing criteria like those in Table 1 or like thosereviewed by Schaffelke et al. (2006) and Trowbridge(2006), no introduction of commercial macroalgae will becompletely without risk and it may be difficult to predictwhat the actual consequences will be.

Quarantine and farm procedures to minimize risk

Quarantine procedures address the issue of inadvertentcoincident movement of harmful organisms, that is, unin-tentional introduction of non-target species (sometimestermed ‘‘hitchhikers’’). For example, Sulu et al. (2004)showed that Kappaphycus alvarezii shipped to new loca-

tions may contain fauna such as copepods, amphi-pods, isopods or polychaete worms, smaller seaweedsattached as epiphytes, a microscopic epibiota possiblyincluding harmful dinoflagellates, and potentially any dis-ease organisms within the seaweed tissues. They alsoshowed, however, that relatively simple propagule selec-tion, treatment (e.g., washing with seawater) and quar-antine procedures can greatly reduce this risk.

Quarantine can thus play a vital role in reducing therisk of introductions of unwanted species and pathogensassociated with host aquaculture species. States areurged to develop quarantine protocols for the species ofmacroalgae most likely to be proposed for introduction.Unfortunately, very little research has been directed atdevelopment of quarantine protocols for macroalgae,and hardly any protocols or guides to best practice areavailable for macroalgae. Those states that have paidattention to quarantine matters have usually resorted toad hoc approaches.

A detailed case-history of quarantine for Kappaphycusalvarezii aquaculture and transportation to various coun-tries in the Pacific Islands region is provided by Sulu etal. (2004). While there are a small number of exampleswhere quarantine measures have been applied to K. alva-rezii (Ask et al. 2003a, Sulu et al. 2004), it is clear that inthe majority of cases no quarantine protocols have beenapplied. However, a modicum of forethought to the appli-cation of simple and low-technology protocols can go along way toward reducing ecological risk.

For seaweeds like Kappaphycs alvarezii with a relative-ly simple growth habit, quarantine procedures such aswashing, physical surface cleaning, mild chemical treat-ment or washing in freshwater may be effective in theremoval of larger fauna and flora, although the completeremoval of micro-organisms or endophytes is virtuallyimpossible (Sulu et al. 2004). An alternative is to trans-locate just apical tips of the plant and then grow theseat the new location using tissue culture methods. Thiswas the procedure followed by Brazilian authorities whenthey introduced K. alvarezii. They imported axenic cul-tures, cultured apical tips in agar, grew plants, then grewa second generation of cultures from those plants beforereleasing K. alvarezii into the sea. The process took aboutfour years and required fairly sophisticated laboratoryfacilities (Oliveira and Paula 2003).

For quarantine of whole plants of Kappaphycs alvarezii,placement in holding tanks using closed water systemsfor an observation period can allow detection of ‘‘hitch-

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hikers’’ or disease on the imported plants, and this canbe done in relatively simple land-based tank systemswith daily water exchange provided by pumping seawa-ter from an adjacent shore, as was done in Fiji in 1984(Sam Mario, personal communication). Water exchangedfrom this kind of quarantine system should be chlorinatedand discarded at least 500 m from the coastline to ensurethat no aquatic organisms escape into the local ecosys-tem. Zemke-White (2004) recommends that plantsshould be maintained for at least two weeks in a con-tained system, and that during that time they should bechecked for the growth of microalgae and animals on thethalli. The health of K. alvarezii plants can greatly deteri-orate in enclosed systems over two weeks, however. Thisobservation time could be safely shortened to 7–10 daysif washing and/or chemical-dip treatments precede theobservation period (Sulu et al. 2004).

Ribera and Boudouresque (1995) stress the impor-tance of raising public awareness of the risks involved inspecies introductions. Good examples of public aware-ness initiatives are the brochures distributed to peoplearriving in Australia explaining the main Australian quar-antine regulations, published in 49 languages, and themassive public awareness campaigns carried out inSpain, Italy and France on the invasion of Caulerpa taxi-folia (see Meinesz 2007). The Aquaculture Programme ofthe Secretariat for the Pacific Community is now raisingawareness among member countries about the need forquarantine protocols in aquaculture (www.spc.int/aqua-culture), and is taking steps to develop guidelines forbest practice.

Once a species has been introduced and the quaran-tine period has ended, particular farm procedures maysometimes be applied to further minimize environmentalrisk. These are usually directed at containment of theintroduced macroalga, to confine it to the aquaculturesite and prevent it from becoming established in the wildas self-sustaining populations or spreading to other are-as. One practice has been to propagate the targetmacroalga under controlled conditions onshore, thencarefully select grow-out sites where environmental con-ditions are suitable for growth but not for reproduction(usually by virtue of unsuitable temperature and/or day-length regimes). This approach was not successful incontaining Undaria pinnatifida on the French Atlanticcoast, because estimates of the temperature limits forreproduction of this species were incorrect. Proposersand resource managers would be prudent to assume thatany marine species, once introduced, will not be suc-cessfully contained, and ought to address all issues ofenvironmental risk at the pre-introduction risk assess-ment stage of any proposal.

Risk of spreading the introduced macroalga to otherareas away from the farm can be reduced by taking carethat seaweed farm equipment (ropes, floats etc.) or ves-sels do not harbor the macroalga through entanglementor biofouling before they are taken to other places. Thereis a growing literature on ways to reduce the risk of unin-tentional translocation of Undaria pinnatifida, Caulerpataxifolia and Sargassum muticum. For example, Gun-thorpe et al. (2001) report on tests of protocols to avoidspreading U. pinnatifida via mussel-farming equipment in

Australia, and the resultant guidelines are being built into publicity materials and awareness campaigns.

One component of environmental risk from introduc-tion of a macroalgal species for aquaculture is the risk ofadverse effects from the farm activity itself. Usually thesecan be avoided, remedied or mitigated by appropriatefarm management practices. For example, Kappaphycusalvarezii plants in off-bottom culture can abrade anddamage living corals that they contact (Zemke-White andSmith 2006). This can be avoided through selection offarm sites on clean-bottomed sandy areas away fromeither corals or seagrasses (Ask 1999), which brings thetwin benefits of avoiding damage to corals, and reducingherbivory of the cultivated macroalga by fishes which areoften much more abundant around corals and in sea-grass beds.

Conflicts between risk mitigation and commercialproduction

The intentional introduction of organisms for the purposeof aquaculture requires a balance between minimizingecological impact (i.e., risk), and maximizing economicgain (Watson et al. 2000). The rapid depletion of naturalfish stocks through over-fishing in most parts of theworld is placing increasing pressure on governments toseek alternative means of production, and as a conse-quence aquaculture is increasing (FAO 2004). Depletionof natural stocks of seaweeds is a much less significantissue because many stocks are inaccessible to fishing(e.g., because they are located on exposed rocky coastswith high wave action). However, this very inaccessibilitycan be one driver for increased production through aqua-culture in order to meet demand. The majority of marineplant aquaculture (and thus the movement of organismsfrom country to country) is centered in SE Asia. Seedstock from this region has been used to establish aqua-culture operations elsewhere, with the majority of therecipients being developing countries. For most of thesedeveloping countries, economic potential has almostalways taken precedence over ecological concerns. Themajority of these countries lack legislation regardingintroductions or it is sketchy, they lack the capacity toconduct meaningful baseline surveys or monitoring, orthey perceive aquaculture of an alien macroalga aspreferable to alternatives such as continued unsustain-able livelihoods or destructive practices associated withcoral reefs.

In these countries, where there are real or potentialconflicts between risk mitigation and commercial pro-duction, the ‘‘utility’’ of commercial productionoften takes precedence. In other countries with greatercapacity for coastal-management and weaker economicimperatives (for example, Australia, New Zealand, USA),further intentional introductions of non-indigenousmacroalgae are now almost impossible. As mentionedearlier, in the example of the proposed introduction ofMacrocystis pyrifera to Europe, deliberate introductionscan be prevented in the face of public pressure and sci-entific advice, and potentially serious ecological impactscan be averted. These will always be political rather thanpurely scientific decisions. However, expectations areincreasing that states should exercise a much greater

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duty of care and impose a greater burden of proof uponproposers of introductions than was the case twenty oreven ten years ago. The aquaculture sector is a relativelyeasy target for regulators compared with the shippingsector (Hewitt et al. 2004) which continues to be the mainvector for macroalgal introductions owing to technicalconstraints and powerful lobbyists.

For the majority of deliberate seaweed introductions,the risks have proved to be relatively small and conflictsbetween risk mitigation and commercial production havenot been an issue. Monitoring should be an importantpart of risk mitigation however, such as that being carriedout with introductions of Porphyra yezoensis Ueda fromJapan to the Atlantic coast of the USA (Watson et al.2000).

In cases where commercial production does not takeprecedence, the conflict becomes one where communi-ties may have an opportunity cost imposed upon themeither by an appropriate introduction being declined, orwhere permission for the introduction is granted but withonerous conditions attached. A hypothetical examplemight be if a jurisdiction were to require four years ofhigh-technology tissue culture before Kappaphycus alva-rezii propagules can be released from quarantine, asoccurred in Brazil (Oliveira and Paula 2003), in order tocompletely eliminate the risk of introducing associatedmicrobiota, compared with a two-week low-technologyquarantine protocol (Sulu et al. 2004) that might perhapsreduce the risk by 99%.

Conflicts about macroalgal introductions, where theyexist, can best be solved through transparent andaccountable decision-making processes by competentauthorities in which there is wide and meaningful con-sultation and participation by relevant stakeholders.

Decision support tools and other formal riskmanagement frameworks

Governments are cautious with aquaculture enterprisesinvolving the introduction of exotic species into a newenvironment, due to potential adverse impacts on nativeflora and fauna (see Doelle et al. 2007). In addition, mem-bers of the World Trade Organization (WTO) are requiredto use formal risk analysis to justify any restrictions oninternational trade based on risks to human, animal orplant health (WTO 1994). The risk analysis process takesinto account risk management and appropriate actionsnecessary to mitigate the risks’ impacts.

Orr (2003) describes a detailed risk analysis reviewprocess for non-indigenous aquatic organisms, devel-oped by the US Aquatic Nuisance Species Task Force in1996. The review process provides a standardizedmeans for evaluating the risk of introducing non-indige-nous organisms into a new environment and, if neces-sary, determining the correct risk management stepsneeded to mitigate that risk. However, the process hassome uncertainties about methodology, human error orthe biology and environmental requirements of the organ-isms, and it should be seen as a constantly evolving sys-tem that takes into account new information derived fromresearch. Orr (2003) provides a copy of the OrganismRisk Assessment Form (including uncertainty reference

codes) which is the main decision support tool of thatassessment.

A risk management framework should result from a riskanalysis process. The US system provides the necessaryguidelines and tools for the development of a risk man-agement framework for marine macroalgae, although thecomplex infrastructure and taxonomic expertise requiredfor the task is lacking in most countries where seaweedsare brought in for aquaculture purposes. Even (or per-haps, especially) under circumstances where there is lackof knowledge, limited capacity and low funding, thebenefits in developing a risk management frameworkinclude identification of the core values that need to beprotected, and prioritization in the delivery of controlmechanisms and in contracting of scientific research(Hewitt et al. 2004). A risk management framework is auseful tool to identify gaps in knowledge or shortcomingsin capacity, and to highlight the most pressing issues.

Acknowledgements

The authors are indebted to Alan T. Critchley, Erik I. Ask, G.Robin South, Cameron Hay, A.R.O. Chapman and Craig John-son for providing comments on this manuscript, and to ShitalSwarup for assistance with literature searches and interloans.

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Received 31 January, 2006; accepted 17 April, 2007