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Editorial

Aquarium species: Deadly invaders

The introduction of exotic species is, arguably, a moresignificant anthropogenic stressor than eutrophication ortoxic chemicals (Chapman, 1995) and, along with habitatdestruction, is the leading cause of extinctions and resul-tant biodiversity decreases worldwide. In the marine andsome freshwater environments (e.g., the North American

Great Lakes), ballast water (transport and discharge) is amajor potential source for new species introductions, andhas rightly received much attention (Rulz et al., 2003; Mat-heickal and Raaymakers, 2004). However, an arguablymore important source of species introductions into aqua-tic environments, and one which has received surprisinglylittle attention to date, is the world-wide aquarium trade.

The purpose of this editorial is twofold. First, we pro-vide information regarding the proven and potential futureimportance of the aquarium trade in marine exotic speciesintroductions to the detriment of receiving ecosystems. Sec-ond, we suggest that the aquarium trade should be subjectto risk assessment to assist in minimizing any adverse

effects of accidental introductions, and outline how thismight be done. Our focus is on the marine environment;however, the freshwater environment is arguably evenmore at risk from aquarium introductions than the marineenvironment (Wabnitz et al., 2003).

The worldwide aquarium trade is a multi-billion dollarindustry (Wabnitz et al., 2003), with many species availableby mail order or over the internet. Hundreds of organismsare used in reef aquariums. Every day tropical species,mainly from the Indo-Pacific, the Red Sea and the Carib-bean, are put aboard planes for shipment overseas. Amongthose species are predators that reef aquarium hobbyists

consider undesirable because of their predatory nature,but which arrive as ‘‘hitchhikers’’ in live rocks. Examplesinclude the mantis shrimps Lysiosquilla and Odontodacty-

lus, the crabs Thalamita and Atergatis, the fire wormHermodice, and the snail Heliacus. These undesirables,when found, either by hobbyists or by store owners are,too often, discarded into nearby coastal marine waters.

In other cases aquarium species escape from tanks (e.g.,during drainage of water from the tanks, or due to break-age), or they may be released for various reasons: they havegrown too large, their owners want to replace them, or

their owners are tired of maintaining the aquarium. Inthe case of live rock entering a new marine environmentthe problem is even more serious, since there can beentire communities of animals and plants colonizing therock, including several species able to reproduce asexually.Aquarium species are also released for religious purposes

(Severinghaus and Chi, 1999). For instance, Japanese Bud-dhists purchase and release small living aquatic creatures inan ancient ceremony called ‘‘Hojo-e.’’, an expression of atonement and pity. Similar Buddhist releases occur else-where, including the west coast of Canada (PMC, personalobservation).

Clearly not all aquarium species released to the wild willsurvive, nor will all of those that survive be able to repro-duce or ultimately become pests. However, if sufficientnumbers of individuals are released together, they may beable to reproduce (either sexually or asexually), and subse-quently compete successfully for habitat with native speciesestablished in those waters. If that occurs, the ecology may

dramatically change, with unpredictable consequences. De-spite growing efforts to detect invading species, many spe-cies, particularly smaller invertebrates and plants, remainunnoticed until it is too late to stop their spread.

Williamson (1996) has suggested the ‘‘three tens rule’’:10% of imported species will be introduced into new envi-ronments; 10% of these will become established; 10% of these will become pests. This rule essentially suggests that0.1% of all aquarium species will actually become intro-duced pests. However, this percentage may be overly opti-mistic. For instance, Holdich (1999) notes that crayfishintroductions into Europe as pests greatly exceed this per-

centage. In addition, even a single successful introducedspecies can wreak havoc on local ecologies.Padilla and Williams (2004) note that a ‘‘third of the

world’s worst aquatic invasive species are aquarium orornamental species.’’ They emphasize the need for in-creased attention to this threat, which represents ‘‘the sec-ond leading cause of extinctions around the world’’, andwhich is potentially much greater than for ballast water(Table 1).

Padilla and Williams (2004) provide a case history of the ‘‘killer alga’’ Caulerpa taxifolia, which was originally

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introduced to the marine environment via wastewater fromthe Oceanographic Museum at Monaco where it was usedfor aquarium decoration. It subsequently spread throughthe Mediterranean displacing native species and is alsonow spreading in California (Jousson et al., 2000) and Aus-tralia (Davis et al., 1997). Another example of an aquariumspecies that has become a successful marine invader is theIndo-Pacific lionfish Pterois volitans (Whitfield et al.,2002). Lionfish currently comprise a reproducing popula-

tion along the southeast coast of the US where they posenot only an ecological risk, but also a risk to humans.The warm marine waters off Florida are host to otherinvaders from aquarium releases (Rulz et al., 2003), includ-ing the following Indo-Pacific reef fishes: the Moorish idol(Zanclus cornutus), the sailfin tang (Zebrasoma desjardinii ),the yellow tang (Z. flavescens), the bursa triggerfish (Rhin-

ecanthus verrucosus), the racoon butterflyfish (Chaetodon

lunula), the orbiculate batfish (Platax orbicularis), and theimperator angelfish (Pomacanthus imperator) (http://nas.er.usgs.gov/fishes/index.html).

Risk assessment was originally developed to deal with

chemical pollution. It is only slowly being adapted to otherstressors including introduced species. Approaches forconducting risk assessments of ballast water species exist(Simberloff and Alexander, 1998; Haugmon et al., 2002).However, although there has been a risk assessment of dis-eases potentially introduced into Australia with live orna-mental finfish (AQIS, 1999) we are not aware of anyexplicit published risk assessment of the overall potentialeffects of marine aquarium species introductions. We sug-gest that there is a need for such assessments, as does theInternational Council for the Exploration of the Sea(ICES, 2001). We further suggest that such assessmentsshould comprise the following:

Problem formulation ( for both primary aquarium species

and potential  ‘‘hitchhiking ’’ species): Information on sourcelocations and final destinations relative to possible releases;life-history information relative to their ability to surviveand reproduce in other areas as well as their dispersal capa-bilities; any information on releases of similar species suc-cessfully surviving and reproducing and the resultingconsequences; any information on potential parasites ordiseases associated with these species.

Exposure assessment: Complementary information onwater quality (temperature and other parameters) in thesource and potential receiving environments for spe-

cific aquarium species and possible ‘‘hitchhiking’’ species

including parasites or diseases. Such information should in-clude some form of ‘‘safety factors’’ as tolerance ranges canbe surprisingly large (e.g., Logan et al., 1996).

Effects assessment: Complementary information on life-history characteristics and habitat requirements for specificaquarium species and possible ‘‘hitchhiking species’’including parasites or diseases, and similar species in poten-tial receiving environments.

Risk characterization: Probabilities of released species

surviving, reproducing, thriving, and competing successfullywith resident species to the extent of becoming pests, and thepotential significance of such successful introductions.

Such assessments would not be trivial, but neither arethe potential consequences of unintended species introduc-tions. Clearly, there would be minimal concern for inlandareas, or for areas with cold winters (though this maychange in the not-so-distant future if global warming is areality), or for areas that are remote, with few inhabitants.Non-trivial risks can probably be assessed as either moder-ate or high. The subsequent focus would be on areas as-sessed as at high risk.

Some potential risks will readily become apparent withminimal research. For instance, the Monaco shrimpLysmata seticaudata occurs in the warm waters of Portugaland the Mediterranean basin. These shrimp are hermaph-rodites, with a very short larval development time (Caladoet al., 2005), thus the likelihood that they will be able toreproduce and spread in other warm marine waters is high.They are currently being sold within the EU, but it isexpected they will shortly also be sold elsewhere (e.g., theUS, Japan).

In areas where the risks are high, additional informationregarding numbers of different species sold would allowdetermination as to whether or not reproducing popula-tions following release are reasonably possible. Such deter-minations could also be done during the ExposureAssessment. It is likely that the end result of such riskassessments would be the determination of specific areasat potential risk – under current exposure conditions (i.e.,current sale and transport). The next step would be tomonitor future sales and transport and regularly (yearly)evaluate changes relative to probabilities of successful, if unintended introductions.

As suggested by Padilla and Williams (2004), one aspect of prevention could include only allowing trade in species thateither could not survive in the wild in their host area, or that,

if they were to escape, could be completely removed. The lat-

Table 1Comparison of ballast water and aquarium species characteristics relative to successful invasions

Species characteristics Ballast water species Aquarium species

Size Generally small, often microscopic Generally large (although ‘‘hitchhiking’’ species can be smallor even microscopic)

Life-stage Generally young (larvae or spores) Generally adults at or capable of reaching reproductive statusCondition Variable Generally healthy; weaker individuals usually weeded out

Potential distribution Coastal, along ship routes and near or in harbors Only restricted by presence of humans with aquaria

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ter case would require the posting of bonds equal to the esti-mated costs for such removals, if necessary. Determinationof appropriate species and of appropriate costs for suchbonds would require information from risk assessments.

In summary, we strongly suggest that there presentlyexist high risks to the marine (and freshwater) environment

from the commercial aquarium trade. That is the point of this Editorial – to point out a present and future risk thatdeserves immediate consideration. Given the size of thisindustry, and the fact that it is promoted by some conser-vation biologists as a means of saving ecosystems such asthe Amazonian rainforest (Norris and Chao, 2002) andcoral reefs (Bunting et al., 2003), it cannot be curtailed,only controlled. And such control will require the informa-tion that only appropriate risk assessments can provide.

References

AQIS (Australian Quarantine and Inspection Service), 1999. Import RiskAnalysis of Live Ornamental Finfish. Canberra, Australia.

Bunting, B.W., Holthus, P., Spalding, S., 2003. The marine aquariumindustry and reef conservation. In: Cato, J.C., Brown, C.L. (Eds.),Marine Ornamental Species – Collection, Culture and Conservation.Iowa State Press, Des Moines, pp. 109–124.

Calado, R., Figueiredo, J., Rosa, R., Nunes, M.L., Narciso, L., 2005.Effects of temperature, density, and diet on development, survival,settlement synchronism, and fatty acid profile of the ornamentalshrimp Lysmata seticaudata. Aquaculture 245, 221–237.

Chapman, P.M., 1995. Ecotoxicology and pollution–key issues. Mar.Pollut. Bull. 31, 167–177.

Davis, A.R., Roberts, D.E., Cummins, S.P., 1997. Rapid invasion of asponge-dominated deep-reef by Caulerpa scalpelliformis (Chlorophyta)in Botany Bay. Aust. J. Ecol. 22, 146–150.

Haugmon, G.P., Behrens, H.L., Anderson, A.B., 2002. Risk based meth-odology to assess invasive aquatic species in ballast water. In: Spajic,L.D., Leppakoski, E., Gallasch, S., Olenin, S. (Eds.), Aquatic Species of Europe. Kluwer Academic Publishers, Dordrecht, pp. 467–476.

Holdich, J. (Ed.), 1999. Crayfish in Europe as Alien Species: How to Makethe Best of a Bad Situation? CRC Press, London.

ICES (International Council on the Exploration of the Sea), 2001. WorkingGroup on Introductions and Transfers of Marine Organisms Report.Available from: <www.ices.dk/reports/ACME/2001/wgitmo01.pdf>.

Jousson, O., Pawlowski, J., Zaninetti, L., Zechman, F.W., Dini, F., DiGuiseppe, G., Woodfield, R., Millar, A., Meinesz, A., 2000. Invasivealga reaches California. Nature 408, 157–158.

Logan, D.J., Bibles, E.L., Markle, D.F., 1996. Recent collections of exotic aquarium fishes in the freshwaters of Oregon and thermal

tolerance of oriental weatherfish and pirapatinga. Calif. Fish Game 82,66–80.

Matheickal, J.T., Raaymakers, S. (Eds.), 2004. 2nd International BallastWater Treatment R and D Symposium, IMO London, 21–23 July2003: Proceedings. GloBallast Monograph Series No. 15, London.

Norris, S., Chao, N.L., 2002. Buy a fish, save a tree. Conser. Prac. 3, 30– 35.

Padilla, D.K., Williams, S.L., 2004. Beyond ballast water: aquarium andornamental trades as sources of invasive species in aquatic ecosystems.Front. Ecol. Environ. 2, 131–138.

Rulz, G.M., Carlton, J.T., Ruiz, G.M. (Eds.), 2003. Invasive Species:Vectors and Management. Island Press, Washington.

Severinghaus, L., Chi, L., 1999. Prayer animal release in Taiwan. Biol.Conser. 89, 301–304.

Simberloff, D., Alexander, M., 1998. Assessing risks to ecological systemsfrom biological introductions [excluding genetically modified organ-isms]. In: Calow, P. (Ed.), Handbook of Environmental Risk Assess-ment and Management. Blackwell Publishing, Oxford, UK, pp. 147– 176.

Wabnitz, C., Taylor, M., Green, E., Razak, T., 2003. From Ocean toAquarium. UNEP World Conservation Monitoring Centre, Cam-bridge, UK.

Whitfield, P.E., Gardner, T., Vives, S.P., Gilligan, M.R., Courtenay,W.R., Jr., Ray, G.C., Hare, J.A., 2002. Biological invasion of the Indo-Pacific lionfish Pterois volitans along the Atlantic Coast of NorthAmerica. Mar. Ecol. Prog. Seri 235, 289–297.

Williamson, M., 1996. Biological Invasions. Chapman & Hall, London.

Ricardo CaladoCCMAR, Universidade do Algarve,

Campus de Gambelas,

8000-117 Faro,

Portugal 

Templo Aqua tico,

Rua de Santa Marta,

No. 27, 1150-291 Lisboa,Portugal 

Tel.: +351 21 355 9030; fax: +351 21 357 1211

E-mail address: rjcalado@hotmail.com

Peter M. ChapmanGolder Associates,

195 Pemberton Avenue,

North Vancouver, BC,

Canada V7P 2R4

Tel.: +1 604 986 4331; fax: +1 604 662 8548

E-mail address: pchapman@attglobal.net

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