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Oysters as Vectors of Marine Aliens, with Notes on Four Introduced SpeciesAssociated with Oyster Farming in South AfricaAuthor(s): T.M. Haupt, C.L. Griffiths, T.B. Robinson & A.F.G. ToninSource: African Zoology, 45(1):52-62. 2010.Published By: Zoological Society of Southern AfricaDOI: http://dx.doi.org/10.3377/004.045.0101URL: http://www.bioone.org/doi/full/10.3377/004.045.0101

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Oysters as vectors of marine aliens, with notes onfour introduced species associated with oyster

farming in South AfricaT.M. Haupt

1, C.L. Griffiths

1*, T.B. Robinson1

& A.F.G. Tonin2

1

Centre for Invasion Biology and Marine Biology Research Centre, University of Cape Town,

Rondebosch, 7700 South Africa2

Striker Fishing (Pty) Ltd, P.O. Box 558, Saldanha Bay, 7395 South Africa

Received 18 September 2009. Accepted 7 November 2009

Translocated oysters are well known to act as vectors of marine alien species, but to date thistopic has received scant attention in South Africa, despite the fact that oysters have beenimported into this region since 1894. Surveys of oyster farms in South Africa revealed fournewly-recorded alien species: the black sea urchin, Tetrapygus niger, from Chile; the Europeanflat oyster, Ostrea edulis (thought to be extinct since its intentional introduction in 1946);Montagu’s crab, Xantho incisus, from the North Eastern Atlantic seas of Europe, and the brachio-pod Discinisca tenuis from Namibia. Oyster imports are the most likely vector of all thesespecies. The biological attributes of each species, the possible threats posed by their introduc-tion, and the needs for additional control measures to limit or prevent further introduction andspread of alien species via oyster culture are discussed.

Key words: marine alien species, oyster culture, South Africa.

INTRODUCTIONMany commercially-cultured shellfish, particularlymussels, oysters, clams and scallops, have beenintentionally transported around the globe in orderto establish or enhance aquaculture ventures(Chew 1990). However, shellfish imported in thisway can also facilitate the introduction of alienspecies. These may include the introducedaquaculture species themselves, epi- or infaunalorganisms associated with them, disease microor-ganisms and multicellular parasites (Carriker1992; Naylor et al. 2001).

The oyster trade in particular, has been responsiblefor the distribution of many unwanted species(Minchin 1996; Ruesink et al. 2005). Oysters havebeen widely transported since Roman times, dueto their inherent ability to withstand long journeysout of water (Andrews 1980). Modern transportmethods, such as airfreight, have allowed for theirfurther and faster dispersal across the globe.

According to Minchin (1996) and Wolff & Reise(2002), the main reasons for the importance ofoysters in the translocation of alien species are thelong history of the trade and the large quantities ofoysters shipped. Another contributing factor isthat oysters do not bury into the substratum, thusremaining exposed to colonization by foulingorganisms, which are also difficult to remove due

to the rugose nature of oyster shells (Minchin 1996;Wolff & Reise 2002). Awareness of the potentialrisks associated with the accidental translocationof such fouling organisms has grown significantlyin many countries, but large quantities of shellfish,especially oysters, are still being traded withoutapplication of adequate biocontrol measures(Wolff & Reise 2002).

Overall, oysters have been introduced to 79countries outside their native ranges, 66 of theseintroductions being of the Pacific oyster Crassostreagigas (Ruesink et al. 2005). As a result, this species isnow one of the most cosmopolitan of all marineinvertebrates (Ruesink et al. 2005). C. gigas is large-bodied, long-lived and able to adapt to a widerange of environmental situations (Chew 1990).The importation of C. gigas to various countrieswas mostly driven by the diminishing populationsof native shellfish due to over-harvesting, diseaseand adverse weather conditions (Chew 1990;Miossec & Goulletquer 2007; Padilla & Gray 2007).

Ruesink et al. (2005) documented a total of 78alien marine algae, invertebrates, and protozoanspecies introduced to nine regions (Argentina,Gulf U.S.A., Baltic Sea, New Zealand, Australia,eastern U.S.A., western U.S.A., French Atlantic andNorth Sea) through oyster culture. Regions inwhich a wider variety of oyster species are cul-tured also have a larger number of associated alien*Author for correspondence. E-mail: charles.griffiths@uct.ac.za

African Zoology 45(1): 52–62 (April 2010)

species (Ruesink et al. 2005). In northwesternEurope, at least five alien species have been intro-duced via imports of C. virginica: the slipper limpetCrepidula fornicata, the American tingle or preda-tory oyster drill Urosalpinx cinerea, the false angelwing Petricola pholadiformis, the polychaeteClymenella torquata, and the ostracod Eusarsiellazostericola (Andrew 1980; Wolff & Reise 2002).C. gigas imports occurred on an even larger scaleand more than 20 invasive species accompaniedoyster imports in France alone. However, onlyfour of these have spread and become established:the anthozoan Aiptasia pulchella, the polychaeteHydroides ezoensis and the barnacles Balanusalbicostatus and Balanus amphitrite (Grizel & Heral1991). Grizel & Heral (1991) also reported twoJapanese algae species, Laminaria japonica andUndaria pinnatifida, which have become estab-lished after the importation of C. gigas to a Medi-terranean lagoon. Other invasive species, such asthe parasitic copepods Mytilicola orientalis andMyicola ostrea, as well as the brown alga Sargassummuticum, have also been introduced via C. gigasimports to both North America and Europe(Andrews 1980; Wolff & Reise 2002). M. orientalisand M. ostrea were found in batches of importedC. gigas oysters in 1933 and subsequently werefound to have established populations (Holmes &Minchin 1995). Critchley & Dijkema (1984) foundthat inconspicuous stages of Sargassum muticumcan be transferred with half-grown oysters.

In western North America, the local establish-ment of C. gigas spat and the development ofhatcheries resulted in its widespread cultivationalong the Pacific coastline (Quayle 1969;Drinkwaard 1999). This took place over severaldecades enabling opportunities for alien speciesaccompanying C. gigas to become established(Andrews 1980). In the past, shipments of oysterswere not checked for invasive species and boxescontaining C. gigas spat could hold up to 22 speciesof molluscs (Hanna 1966). Molluscs introduced viashipments of oysters include Cecina manchurica,the Japanese false cerith Batillaria attramentaria, theconvex slippersnail Crepidula convexa, C. fornicata,the eastern white slippersnail Crepidula plana, theJapanese oyster drill Ceratostoma inornatum/Ocenebra japonica, the Atlantic oyster drill Urosalpinxcinerea, the channelled whelk Busycotypuscanaliculatus, the eastern mudsnail Ilyanassaobsoleta, Japanese nassa Nassarius fraterculus,European ovatella Ovatella myosotis, Musculistasenhousia, the ribbed mussel Geukensia demissa, the

Chinese jingle Anomia chinensis, the Atlantic rangiaRangia cuneata, the Baltic macoma Macoma ‘bal-thica’, the Japanese trapezium Trapezium liratum,the Japanese littleneck Venerupis philippinarum,Gemma gemma, the false angelwing Petricolapholadiformis, softshell Mya arenaria and Lyrodustakanoshimensis (Carlton 1992). Nine of these spe-cies originated from Japan and 13 from the Atlanticcoast of North America (Carlton 1992). Venerupisjaponica is by far the most significant alien molluscspecies associated with oyster imports. This clamhas become widely distributed and is used forhuman consumption in its introduced range(Andrews 1980). Non-molluscan species includetwo serious Japanese parasites of oysters: the flat-worm predator Pseudostyochus ostreophagus, aswell as Mytilicola orientalis, which is also evident inEuropean waters (Andrews 1980).

Marine alien species that have been imported withcultured oysters may have significant ecologicalimpacts in areas where they have become estab-lished. Amongst many other factors, they are ableto alter the trophic structure of the invaded areaand change the disturbance regime (Vitousek1990). It has been suggested that large densitiesof these alien species could interfere in trophicenergy flow (Minchin 1996). In western NorthAmerica, studies of all but one of the introducedmolluscs, O. myosotis, have demonstrated dramaticimpacts on native communities. They are known tocompete with native species and alter the physicalappearance and ecological structure of the invadedhabitat (Carlton 1992). In addition to free-livingassociated species, parasites of introduced oysterscan also infest native species. In Australia, intro-duced parasites of oysters include the mudwormsPolydora websteri and Boccardia knoxi (Nell 2002).High infestations of these worms are associatedwith increased mortality and reduced condition intheir mollusc hosts (Lleonart et al. 2003; Simon et al.2006). These burrowers penetrate the inner surfaceof mollusc shells, which the host then repairs withnacre, forming a blister (Stephen 1978), whichwhen punctured, releases anaerobic metabolites,such as hydrogen sulphide. This lowers themarket value of oysters considerably (Handley1995).

Examples of diseases associated with importedoysters, and that have effects on native communi-ties, also exist (e.g. Malpeque Bay disease inCanada 1914, Delaware Bay disease on the Mid-Atlantic coast of North America 1957) (Andrews1980). C. gigas was blamed for the outbreak of a

Haupt et al.: Oysters as vectors of marine aliens 53

protozoan Bonamia ostreae, which reduced produc-tion of O. edulis in the Netherlands and elsewherein northwestern Europe in 1981 (Chew 1990;Nehring 2006). This disease resulted in a seriousdecline of O. edulis and was most prevalent inmature oysters that suffered mortalities of 50–80 %(Minchin & Rosenthal 2002). It is currently presentin Spain, France, Britain and Ireland (Balseiro et al.2006).

From the above, it is evident that considerableresearch has been carried out on the introductionof alien species associated with oyster imports inforeign countries, although more work is requiredto determine the possible ecological impacts ofsome of these species. In South Africa, however,this problem has been recognized, but little or noattention has been afforded to documenting it.

South Africa lies on one of the world’s majorshipping routes and has thus been exposed tomarine introductions for centuries (Griffiths et al.2009b). However, despite the considerable researchundertaken on marine invasions in Australia, theUnited States of America and Europe (Orensanzet al. 2002), this topic has only recently receivedattention in South Africa. The most recent pub-lished reviews of marine alien species in SouthAfrica are those of Robinson et al. (2005) andGriffiths et al. (2009). Both studies recognizedapproximately 20 confirmed alien species from theregion, most of which are restricted to shelteredbays, estuaries and harbours. Only the Mediterra-nean mussel Mytilus galloprovincialis and therecently reported barnacle Balanus glandula (Laird& Griffiths 2008) are known to have spread exten-sively along the open wave-exposed coastline. Thenumber of marine introductions recorded inSouth Africa is small compared to other regions ofthe world – for example, 298 marine alien speciesare recorded along North American shores (Ruizet al. 2000). However, large areas of the South Afri-can coast remain relatively unexplored for alienspecies and the taxonomy of certain marinegroups, specifically alien species, is also poorlydeveloped (Robinson et al. 2005). It is thus likelythat the presently recorded introduced speciesunderestimates the real numbers present. Indeed,an unpublished study by A. Mead et al. (pers.comm.) has already resulted in the recognition ofat least 70 additional marine alien species in SouthAfrica.

The South African oyster industry relies on com-mercially importing spat of the Pacific oysterCrassostrea gigas. This activity might very well

have led to the unintentional introduction ofmarine aliens. Oyster farms in this region have notpreviously been sampled in a directed effort todetect such bioinvasions. This study thereforeexamines marine alien species that might havebeen introduced via the oyster trade in these areas

METHODSThree oyster farms in South Africa, Alexander Bayand Saldanha Bay (West coast) and Knysna (Eastcoast), were surveyed for marine alien speciesassociated with oyster culture. Due to the variablenature of the three farms, sampling techniquesdiffered substantially. For example, in AlexanderBay, the layout of the farm allowed for a completesurvey of the oyster operation, as the culture damsare isolated from the sea, whereas the oyster farmsin Saldanha Bay and Knysna form part of aharbour and estuary respectively, which did notenable complete surveillance within the scope ofthis study. Thus, sampling of the latter two farmstargeted only Crassostrea gigas oysters, oysterbaskets and other structures associated with thefarming operation itself. Recent surveys of alienspecies occurring in the general habitats ofSaldanha Bay and Knysna Estuary have beenconducted by Robinson et al. (2004) and Griffithset al. (2009). A list of the introduced species foundin these areas is included below.

Alexander BayThe survey of Alexkor Ltd. in Alexander Bay was

carried out in March 2007. Two dams exist on thefarm, of which only one is in operation. Both damswere surveyed and each dam was divided intofive sites. At each site, five samples of each type. i.e.push-net (soft-substratum), core (soft-substratum)and general (hard-substratum, i.e. rocks, oystersand oyster racks) were collected. Push-net sampleswere carried out using a large net with a woodenboard placed horizontally at the front, to displaceorganisms from the sandy bottom into the net. Thepush-net was dragged along the sandy bottom for10 m at each site. Contents were then transferredto a 1 mm mesh seive and after most of the sandand debris were washed away, the remainingsamples were transferred to sorting trays. Coresamples were carried out using a speciallyadapted box-coring spade (20 × 10 cm). At eachsite, the spade was pushed into the sandy bottomthree times with the contents being placed in aseive. General samples involved collecting anyorganisms on hard substrata such as rocks, oysters

54 African Zoology Vol. 45, No. 1, April 2010

and oyster racks at each site. Soft substrata or hardsubstrata were not found at every site, in thesecases, only the possible types of sampling werecarried out. Trek-net samples were also carried outby pulling a net (20 m long with 1cm mesh) threetimes at appropriate locations (i.e. deep sandybottomed areas) in each dam.

Saldanha BayThe survey at the Striker Fishing Oyster Company

in Saldanha Bay was carried out in August 2007.Thirty market size oysters (>50 g total wetweight), from the same stock of Chilean oysters,were collected. Oysters of each set were made upof three sub-samples of 10 oysters each, taken fromthree separate baskets on the same culture rope.A scrape of organisms residing on each of threeoyster baskets were also collected to represent anyspecies not residing on the oysters.

Knysna EstuaryThe survey at the Knysna Oyster Company was

carried out in August 2008. At Knysna, oysters aregrown on racks in 6 mm mesh bags. Racks aredistributed in different areas of the estuary. ThirtyC. gigas oysters were collected in total. These weredivided into three sub-samples of 10 oysters each,taken from three different sites in the estuary. Thefirst site was situated deep into the estuary andaccommodated juvenile oysters purchased fromJeffrey’s Bay Nursery, which were approximately2–3 months old. The second site was nearby thelatter, however, oysters were approximatelysix months old and formed part of a pilot studywhich would determine the growth rate of oysterswhich are not relocated to Port Elizabeth. Thethird site was situated closer to the mouth of theestuary, where oysters were exposed to greatersalinities. This site accommodated juvenile oystersof 2–3 months, which were purchased fromJeffrey’s Bay Nursery. A scrape of any additionalorganisms residing on the mesh bags and on theracks were taken at each site.

Sample processingSamples collected from Alexander Bay, Saldanha

Bay and the Knysna Estuary were preserved in70 % ethanol and brought back to the laboratory atthe University of Cape Town. Oyster samplescollected from Saldanha Bay and Knysna werethoroughly searched for organisms on and in thegrooves of oyster shells. Organisms were identi-fied to species level.

RESULTSTen alien species were recorded in Alexander Bay,while 15 occurred in Saldanha Bay and seven inthe Knysna Estuary. These are listed in Table 1 andthe newly discovered species elaborated uponbelow.

We record here those alien species thought tohave been introduced as a result of oyster importa-tion. Other, previously-known marine alienspecies, as listed in Table 1, have been discussed inearlier papers by Robinson et al. (2005) andGriffiths et al. (2009). Three new introducedmarine species were found during our surveys,while a fourth, the crab Xantho incisus, was sent tous from the Kleinsee oyster nursery along the Westcoast, where it was apparently introduced withimported oyster spat from France. These fournewly-recorded species are described and illus-trated below.

Tetrapygus niger Molina, 1782(Class Echinoidea, Family Arbaciidae)

The natural range of the black sea urchin T. niger(Fig. 1a) is along the temperate Pacific coast ofSouth America from northern Peru to the Strait ofMagallanes in southern Chile. No previous historyof invasion exists for this species. It is identified byits typically depressed purplish test, which isdifferent to the round, green test of Parechinusangulosus, the only common coastal urchin nativeto the West coast of South Africa. T. niger was firstcollected from Alexander Bay oyster farm (Fig. 1a)in 2007. A breeding population of hundreds ormore individuals, consisting of both juveniles andadults, was recorded. Individuals were scatteredon the bottom and in oyster baskets within thetwo oyster dams on the farm, being particularlycommon amongst C. gigas within oyster baskets.

Ostrea edulis Linnaeus, 1758(Class Bivalvia, Family Ostreidae)

The European flat oyster O. edulis (Fig. 1b) origi-nates from Europe and has a global distributionfrom Norway to Morocco in the North EasternAtlantic, extending into the Mediterranean. Addi-tional naturalized populations exist where thisspecies has been introduced for aquaculture pur-poses (e.g. eastern North America, Canada andBritish Columbia). It is identified by its roundedshell, which differs from the flat shells of nativeAfrican Ostrea species. In South Africa, O. eduliswas first recorded in the Knysna Estuary in 1946,with subsequent introductions known to have

Haupt et al.: Oysters as vectors of marine aliens 55

occurred in Saldanha Bay and St Helena Bay in the1980s and 90s. Recent publications loisted thesepopulations as being locally extinct (Robinson et al.2005). During the course of this study an estab-lished population was rediscovered at the Alexan-der Bay oyster farm (Fig. 1b) along the West coastin 2007. Both adults and juveniles occurredamongst C. gigas oysters and on stones and otherstructures within both dammed ponds of theoyster farm, indicating the presence of a signifi-cant breeding population.

Xantho incisus Leach, 1814(Phylum Crustacea, Family Xanthidae)

Xantho incisus (Fig. 1c), commonly known asMontagu’s crab, is native to the Mediterraneanand North Eastern Atlantic coast. No previousinvasion history exists for this species. The large,dark-coloured chelae, contrasted with the palerbody colouration, distinguishes X. incisus from

other South African crabs found along the AfricanAtlantic coast. A single individual was collected onthe banks of the Kleinsee oyster nursery (Fig. 1c) inJanuary 2008. The species was first noted in 2006but no further specimens have been collected bythe oyster operators.

Discinisca tenuis Sowerby, 1847(Phylum Brachiopoda, Family Discinidae)

Discinisca tenuis (Fig. 1d) is reported in the litera-ture as native and endemic to Namibia, althoughshells have frequently been found washed ashorein Alexander Bay, close to the Namibian bordernear South Africa. No previous history of invasionexists for this brachiopod. The unusual transpar-ent, hairy, fringed shell makes this species readilydistinguishable from other native South Africanbrachiopod species. The first record of livingD. tenuis was made in Saldanha Bay in 2008(Fig. 1d). Numerous individuals were found

56 African Zoology Vol. 45, No. 1, April 2010

Table 1. Alien species recorded at Alexander Bay, Saldanha Bay and Knysna oyster farms.

Taxon Alexander Bay Saldanha Bay Knysna

CNIDARIASagartia ornate �

POLYCHAETABoccardia proboscidea �Polydora hoplura �

CRUSTACEABalanus glandula �Carcinus maenas �Monocorophium acherusicum �Jassa slatteryi � �

BRYOZOABugula neritina � � �

BRACHIOPODADiscinisca tenuis �

MOLLUSCACrassostrea gigas � � �

Littorina saxatilis � �Mytillus galloprovincialis � � �Ostrea edulis �

ECHINODERMATATetrapygus niger �

ASCIDIACEAAscidiella aspersa �Botryllus schlosseri � �Ciona intestinalis � �Diplosoma listerianum � � �

Microcosmos squamiger � �

Haupt et al.: Oysters as vectors of marine aliens 57

Fig.1.Appearance and location of Tetrapygus niger (a), Ostrea edulis (b), Xantho incisus (c) and Discinisca tenuis (d)in South Africa.

a

b

c

d

attached to the shells of C. gigas oysters grown insuspended culture. An average of one individualper oyster was found in a batch of 150 oystersinspected. Several previous surveys of the faunaof Saldanha Bay (Day 1958; Chrisie & Moldan1977; Robinson et al. 2004; Awad et al. 2005) failedto detect this conspicuous species, making itunlikely that it occurred naturally in the region atthat time. We therefore deduce that this is a recentintroduction with the cultured oyster importsfrom Walvis Bay, Namibia.

DISCUSSIONNumerous alien species have been recorded ineach of the three sheltered sites examined, withSaldanha Bay having the larger number of intro-ductions (Table 1). In Alexander Bay, which isisolated from any boat traffic or internationalharbours, these introductions are almost certainlydue to movements of oyster stock, whereas bothSaldanha Bay and Knysna have a long history ofuse as harbours in addition to their roles as centresof aquaculture. The geographical and historicalpatterns of introduction to these and other SouthAfrican sites are discussed in detail elsewhere(Robinson et al. 2005; Griffiths et al. 2009a,b), thusthe following discussion is confined to the fouralien species recorded in the course of this study.

Tetrapygus niger is the most abundant sea urchinin its area of origin along the central Chilean coast(Rodriguez & Ojeda 1993). The most likely vectorof this species into Alexander Bay oyster farm isthe introduction of juveniles along with spat ofCrassostrea gigas imported from Chile. The farm isisolated from any boating harbours and shippingactivities making it most unlikely that shippingwas the vector for this introduction.

A population of Ostrea edulis also occurred in thesame oyster dams at Alexander Bay. It was firstintroduced to the Knysna Estuary in 1946(Korringa 1956) and has since been considered tohave become locally extinct (Griffiths 2000; Robin-son et al. 2005). The population occurring at thefarm could have been introduced along with con-signments of C. gigas spat from Chile or France, butit is more likely this oyster was deliberatelytranslocated from other farms elsewhere in SouthAfrica, where it may have survived undetectedsince the early years of experimental oyster farm-ing in the region.

Oyster imports from France might also haveresulted in the introduction of the alien crab speciesX. incisus, found at Kleinsee oyster nursery. Like

Alexander Bay, Kleinsee is isolated from any inter-national harbours or boat traffic which could act asalternative vectors.

The discovery of the brachiopod D. tenuisfurther down the West coast in Saldanha Bay is thefirst example of an alien marine species in SouthAfrica originating from a neighbouring country.Individuals were found attached to shells ofC. gigas. The most likely vector of this species isC. gigas oyster spat translocated from the oysternursery in Walvis Bay, Namibia. No evidence wasfound of this species occurring on substrata otherthan oysters, indicating that the species may notyet have established self-sustaining populations.This species has recently been noted on oysters forsale at a Cape Town supermarket reputedlysourced from cultures in Algoa Bay and originallycoming from spat purchased from Alexander Bay.This suggests the species may be more widelydistributed.

Possible impacts

The impacts of alien species fall into one of threecategories: they may have no detectable or signifi-cant effect, they may be advantageous if they arecommercially exploitable, or they might have neg-ative ecological or economical impacts (Griffiths2000). Of particular concern are species known tobe a problem either in their area of origin, or inother invaded habitats.

Some echinoid species are already known tohave a significant ecological impact as they play animportant role as habitat engineers. Paracentrotuslividus has been described as an important habitatmodifier of immediate sublittoral areas in Europe(Kitching et al. 1983). Himmelman et al. (1971)discussed Strongylocentrotus droebachiensis in theNorth Western Atlantic causing a series of changesin the dynamics of the biota and in the NorthEastern Pacific there are studies on S. franciscanusand its influence on offshore kelp-beds (Dean et al.1983). Similarly, T. niger is a well-known ecosystemengineer and has become an economic and eco-logical pest in its areas of origin. In northern Chile,T. niger is the most conspicuous benthic grazer andhas recently quadrupled in abundance, resultingin catastrophic effects on associated flora (Vasquez& Buschmann 1997; Vega et al. 2005; V. Haeusser-mann, pers. comm.). Larvae of this species settle inbeds of the kelps Lessonia nigrescens and L.trabeculata, which are regularly exported fromChile as raw materials for alginate production(Vasquez & Santelices 1990; Rodriguez & Ojeda

58 African Zoology Vol. 45, No. 1, April 2010

1993). These kelps are an important food resourcefor T. niger, and make up 68 % of its diet (Rodri-guez 2003). Increased grazing from the urchins hasreduced the recruitment of both Lessonia speciesand has modified the morphology of L. trabeculataby grazing on the holdfast. This weakens individ-uals, making them susceptible to drag forces andincreasing mortality from water movement(Vasquez & Santelices 1990). Ojeda & Santelices(1984) showed that in the absence of the dominantcanopy species L. nigrensis, algal species such asGelidium chilense are unable to increase their cover,or monopolize the substratum, due to predationby T. niger. The increase in abundance of T. nigerhas also resulted in local extinctions of the kelpMacrocystis integrifolia due to overgrazing (Vegaet al. 2005). These ecological impacts illustrate thepossible impacts of T. niger along the west coast ofSouth Africa, which is also dominated by extensiveand commercially valuable kelp-bed ecosystems(Branch & Griffiths 1988).

A well-established population of O. edulis occursin the same oyster dams at Alexander Bay. AlthoughO. edulis has been deliberately introduced to SouthAfrica several times (Korringa 1956), the origins ofthis particular population are unknown. Globallythis species has been used to boost aquaculture inmany regions (Askew 1972; Mann 1983; Shpigel1989; Chew 1990; Drinkwaard 1999) and the nega-tive impacts of these introductions have beenextensively documented. These include the geneticloss of native oyster species due to the exchange ofO. edulis oyster stocks and the potential of O. edulisas a vector for the oyster disease Bonamia ostreaeand oyster pathogen Marteilia refringens in Europe(van Banning 1991; Cigarria & Elston 1997; LeRoux et al. 2005). If the population size of O. edulisescalated it could compete with C. gigas, which iscultured in the dams. Densities of C. gigas, how-ever, currently far outweigh those of O. edulis. Ifpopulations of O. edulis manage to establish in sur-rounding coastal waters, impacts such as competi-tion with native bivalve species could also occur.

Literature on the crab X. incisus focuses on itsbiology, distribution, spatial and temporal settle-ment patterns and association with other fauna,rather than its impacts as an invader (Crothers1970; Wirtz 1997; Flores et al. 2002; Flores & Paula2002). The discovery of this crab in South Africathus appears to be its first record as an alienspecies. Being a powerful predator this speciescould cause considerable damage to the shellfishindustry by consuming C. gigas or other shellfish.

Although no such incidents have been recorded,further studies should be conducted to determinethe density, distribution, habitat and diet at thissite in order to determine whether the crabs arelimited to the oyster farm, or have spread intosurrounding coastal waters. This is, however,unlikely given the isolation of this particular damfrom the open sea.

Literature on the brachiopod D. tenuis is limited.Its distribution and biology are noted by Branchet al. (2005) and its occurrence in Namibia dis-cussed by Brunton & Hiller (1990), Hiller (1990)and Nemliher & Kallaste (2002). It is unknownwhether D. tenuis has managed to spread to sub-strata other than that of cultured C. gigas oysters inSaldanha Bay. Brachiopods are sessile filter-feeding organisms and might therefore competewith native fauna for food and space. Theirunsightly appearance may also have a negativeimpact on consumers of shellfish farmed in thebay. Although oysters are cleansed prior topurchase, not all associated fouling organisms areremoved and D. tenuis are especially resistant, asthey are flat and attach via threads to the oystershells.

Because the ecological impacts of these alienspecies are unknown in the South African context,precautions should be taken to prevent theirfurther spread in South African waters. At present,the populations of T. niger and O. edulis arethought to be restricted to the oyster dams atAlexander Bay. Juveniles of both species werefound during sampling indicating that the popu-lations are able to successfully reproduce in theirnew environment. Of concern is the possibility ofthese species establishing outside of the oysterdams on the open coast. The cleansing procedureof the oysters at the farm entails jet-spraying withseawater to remove any fouling species. This water,along with any excess debris and fouling species, isreturned to the surrounding sea via an unfilteredand untreated run-off system. The occurrence ofthe urchins and oysters outside the oyster dam, aswell as their density inside the dams, remains to bedetermined. Should either species be detected inthe open ocean, a suitable eradication programmeto eliminate them and prevent their spread shouldbe urgently initiated. Olenin et al. (2007) haverecently published a method for quantifying alienimpacts and this might be considered in terms ofthe potential risks of T. niger to the South Africankelp beds and their associated and specializedbiota. In the interim, measures to prevent the

Haupt et al.: Oysters as vectors of marine aliens 59

60 African Zoology Vol. 45, No. 1, April 2010

transfer of T. niger and O. edulis from the dam tothe open sea should be initiated.

The density of X. incisus in Kleinsee is notknown, as to date, only a single dead specimen onthe littoral fringe of the cultivation dam has beencollected. Setting out crab traps would be the bestway to determine their density and also controland even eliminate this species, without any harmto the cultured oysters.

The brachiopods D. tenuis are not easily removedfrom oyster shells due to their flat and inconspicu-ous nature. Thus, a more thorough cleansingregime, for example soaking oyster spat in fresh-water or heated seawater before translocation tofarms, should be instituted to prevent furtherintroductions along with imported Namibianspat.

This study emphasizes the increasing roleplayed by the oyster industry in introducingmarine alien species to South Africa. The ICES (theCode of Practice of the International Council for theExploration of the Sea) are used to prevent intro-ductions in certain countries where oyster cultureis practiced. Some basic rules are the periodic in-spection (including microscopic examination) ofmaterial prior to importation, disinfection, andquarantine in the receiving country (ICES 2005).South Africa is not a member of the ICES but it isaffiliated to the organization. The Code of Practicehas not been rigorously followed with regard tooyster spat import, as South African operations arenot required to quarantine, disinfect or treat spatin any way. However, the hatcheries from whichspat are imported are required to produce healthcertification approved by their authorities. This islargely aimed at preventing the spread of oysterdiseases, rather than alien introductions. Unfortu-nately, there is no industry-wide initiative inSouth African marine aquaculture to address alienintroductions. Oyster operations are thereforeadopting their own approach. Larger spat whichmay have been exposed to the natural environ-ment in the country of origin and have a high like-lihood of contamination by organisms are nolonger being imported. Nurseries also importsmaller spat than in the past, and these have beencultured in a controlled hatchery environment,isolated from the natural environment andthereby at low risk of alien species contamination.It is a primary objective of at least one of thesenurseries to develop a hatchery in South Africa.Until then, a suitable eradication programme topermanently eliminate these newly recorded

marine alien species, and possible others that stillremain undetected, should be considered

ACKNOWLEDGEMENTS

The manager of Alexander Bay oyster farm,Schalk de Waal, is thanked for his assistance andinsight. We thank Andre van Wyk, a resident ofKleinsee who provided the specimen of X. incisusand the manager of Kleinsee oyster nurseryQuiryn Snethlage who provided information onthis species. Financial support was provided bythe DST/NRF Centre of Excellence for InvasionBiology.

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Responsible Editor: J.H. van Wyk

62 African Zoology Vol. 45, No. 1, April 2010