polydorid polychaetes on farmed molluscs: … polychaetes on farmed molluscs: distribution, spread...

AQUACULTURE ENVIRONMENT INTERACTIONSAquacult Environ Interact

Vol. 7: 147166, 2015doi: 10.3354/aei00138

Published online September 17

INTRODUCTION

Shell middens dating to as early as 12 000 BC inEurope, America, Japan, Australia and South Africaindicate that molluscs have been harvested exten-sively for millennia (e.g. Bailey & Milner 2002, Og -burn et al. 2007, Erlandson et al. 2008, Haupt et al.2010, Habu et al. 2011). Oysters were highly re -

garded by the classical Romans who imported oys-ters from as far away as Britain, despite the proposalof a law in 115 BC to curb this practice (Andrews1948). This demand undoubtedly prompted attemptsat culturing oysters and resulted in the successfulestablishment of oyster beds in a lake off thegreater Bay of Naples in 105 BC (Andrews 1948). Atabout the same time, Aboriginal Australians were

The authors 2015. Open Access under Creative Commons byAttribution Licence. Use, distribution and reproduction are un -restricted. Authors and original publication must be credited.Publisher: Inter-Research www.int-res.com

*Corresponding author: [email protected]

REVIEW

Polydorid polychaetes on farmed molluscs: distribution, spread and factors contributing

to their success

C. A. Simon1,*, W. Sato-Okoshi2

1Department of Botany and Zoology, Stellenbosch University, Matieland Private Bag X1, Stellenbosch, South Africa2Laboratory of Biological Oceanography, Graduate School of Agricultural Science, Tohoku University, Sendai 981-8555, Japan

ABSTRACT: Species of the Polydora-complex (i.e. polydorids) are the most common shell-boringpolychaetes found on cultured molluscs. However, which species become problematic depend ontheir ability to reach mollusc farms and flourish under culture conditions. We therefore hypo -thesise that the planktonic larval phases of pest polydorids on molluscs grown on-shore will beshort (as is typical of adelphophagic larvae, which can maintain large local populations) whilethose of polydorids on molluscs grown off-shore will be long (as is typical of planktotrophic larvae,which can disperse long distances to farms). Principal component and discriminant analyses ofinformation extracted from the literature partly supported this hypothesis by identifying larvaldevelopmental mode and pest species as contributing more to pest status than host species andculture mode, with differential influence on pest status in different situations and potential biasthrough incorrect identification of polydorid species. 2 analyses confirmed that pest statusdepended on host culture method and pest larval mode. Pest polydorids producing adelphophagiclarvae in on-shore systems may reflect the development of large local populations on hosts withculture periods >2 yr. The many records of pests in off-shore and near-shore systems with pestspecies producing planktotrophic larvae may reflect shorter host culture periods and the higherincidence of planktotrophy among polydorid species in general. Polydora websteri, P. uncinata, P.hoplura and P. haswelli are the most frequently recorded and widespread pest species globally,although the taxonomy of these and shell-boring P. ciliata and Boccardia polybranchia need to beclarified. The positive relationships between the numbers of alien shell-borers and pests, and thenumber of hosts cultured per country confirm that mollusc aquaculture is an important vector andreservoir of alien pest polychaetes.

KEY WORDS: Alien species Aquaculture Larval developmental modes Molluscs Off-shore On-shore Polydorid pests

OPENPEN ACCESSCCESS

Aquacult Environ Interact 7: 147166, 2015148

farming oysters by catching spat on cultch (Ogburnet al. 2007). The continued demand for oysters andother molluscs has led to the overexploitation of nat-ural stocks and consequent attempts to replenish de - pleted stocks with animals imported from elsewhereand the establishment of culture systems (e.g. Wolff& Reise 2002, Ruesink et al. 2005, Og burn et al. 2007,Haydar & Wolff 2011, Castell 2012, Lucas 2012). InJapan, China and Korea the culture of molluscsbegan about 500 yr ago (Kusuki 1991 in Ruesink etal. 2005) while in Europe and North America itstarted in earnest in the 1700s and 1800s (Wolff &Reise 2002).

Modern culture of molluscs is often associated withlarge-scale movement of stock (Wolff & Reise 2002,Ruesink et al. 2005, McKindsey et al. 2007). At least 5species of oysters and 2 species of clams have beenimported to, and moved among, countries in westernand northern Europe for aquaculture purposes sinceas early as 1570 (Wolff & Reise 2002). On the westcoast of North America, most of the cultured speciesare exotic or alien (McKindsey et al. 2007) while inChile a thriving abalone industry relies on stock orig-inally imported from California and Japan (Morenoet al. 2006). Similarly, the South African oyster indus-try relies on the regular importation of spat from theAmericas and Europe and the local movement ofstock from nursery to grow-out facilities (Haupt etal. 2010, 2012). Up to 18 oyster species have beentranslocated to 73 countries or regions, with the Paci -fic oyster, Crassostrea gigas, translocated to morethan 50 (Ruesink et al. 2005, Lucas 2012). Gastropodsare moved less frequently and there is a tendency forindigenous species to be cultured (Castell 2012, butsee Culver et al. 1997 and Moreno et al. 2006).

The cultivation of high densities of molluscs canhave far-reaching ecological effects, creating habi-tats for other organisms, providing them with pro-tection against predators, reducing physical andphysiological stress and enhancing settlement andre cruitment (e.g. Pregenzer 1983, Ruesink et al.2005, McKindsey et al. 2007, Lucas 2012). This isparticularly important when the molluscs are cul-tured in environments where they are creating hardsubstrates where none existed before, such as inmuddy or soft-sediment environments and sus-pended culture (Ruesink et al. 2005, McKindsey etal. 2007), thus providing settlement substrates forlarvae that might have been otherwise lost. Thearrangement of the molluscs and their shell struc-ture may further contribute to the production of dif-ferent microclimates for preferential settlement bylarvae; for example, large numbers of planktonic

polydorid larvae settled in the inner, rather thanouter, valve of scallops in suspended culture inJapan (Teramoto et al. 2013). Thus, cultured mol-luscs are often associated with infestations by dis-ease agents and fouling organisms (e.g. Bower et al.1994, Wolff & Reise 2002, McKindsey et al. 2007,Haydar & Wolff 2011, Castell 2012, Lucas 2012).This, together with the extensive movement of mol-luscs, particularly of oysters, has led to aquaculturebeing considered one of the main vectors of trans-port of exotic species. For example, Wolff & Reise(2002) estimated that more than 20 species of ani-mals were imported to Europe with C. gigas alone,and they concluded that oysters are more importantvectors than either hull fouling or ballast water, aconclusion supported by McKindsey et al. (2007).

There are many reviews of the diseases of cul-tured molluscs and of the exotic species transportedwith these animals, but they seldom focus on shell-boring polychaetes in any detail (Bower et al. 1994,Mor ten sen et al. 2000). The most common shell-borers are members of the Polydora-complex, oftenre ferred to as polydorids (e.g. Blake 1969b, Morenoet al. 2006, Radashevsky et al. 2006, Sato-Okoshi etal. 2008, Boon zaaier et al. 2014). While there arerare in stances where high infestations by polydoridsoccur under natural conditions (e.g. Poly do ra bre-vipalpa in the scallop Patino pecten yesso ensis andPolydora uncinata in the oyster Crasso strea gi gas[Sato-Okoshi & Abe 2012], and Di poly dora con -vexa, D. con cha rum and D. alborectalis in the scal-lop Patino pecten yessoensis in Japan [Sato-Okoshi1999]), high in festation by a few polydorid speciesis observed more frequently in mollusc culture sys-tems where intensive commercial culture may leadto the development of ecosystems which may en -courage the proliferation of pests. For example, inSouth Africa, Chile and Australasia, farmed mol-luscs were typically infested by fewer species thanare present on wild molluscs occurring close tofarms (e.g. Sato-Okoshi & Takatsuka 2001, Simonet al. 2006, Sato-Okoshi et al. 2008, Simon et al.2010, Simon 2011, Boonzaaier et al. 2014, Sato-Okoshi et al. 2015). Similarly, molluscs grown inon-shore culture systems were infested by fewerspecies than those grown off-shore (Simon, 2015).This suggests that either only some species areprone to becoming pests in culture, or that the cul-ture environment creates favourable conditionswhich only enable some species to become pests.In cases of high infestation levels, shells are dam-aged by the boring activity of the worms whichnegatively impact condition in the hosts as they

Simon & Sato-Okoshi: Polydorid polychaete pests on cultured molluscs

divert energy from growth to shell repair (Kojima &Imajima 1982, Lleonart et al. 2003, Simon et al.2006). In extreme cases infestation has been impli-cated in causing high mortalities (for ex ample, upto 50% of abalone stock in Tasmania, Lleonart etal. 2003) and the collapse of oyster culture con cernsin Hawaii and Australia (e.g. Bailey-Brock 1990,Ogburn et al. 2007).

The main aim of this review was 2-fold. In the firstinstance, the literature was explored to determinewhether pest species, larval developmental mode,host species and culture method influence the peststatus of polydorids on cultured molluscs. The secondaim was to provide the first review of polydorid pestson cultured molluscs on a global scale. Such a reviewwill help to (1) highlight which species are mostproblematic globally, (2) alert importers of molluscsto the species that are problematic in the countriesfrom which their molluscs originate, (3) trace the pos-sible source of new alien pest species, (4) determineif any species show host specificity and (5) highlightproblems in species identification.

MATERIALS AND METHODS

Reviewing the literature

A review of the literature reporting shell-infestingpolydorids in cultured or commercially harvestedmolluscs was conducted and the following informa-tion extracted: location, the polydorid and host spe-cies, culture method (classified as on-shore, inter-tidal, near-shore [bottom and subtidal] and off-shoresuspended), pest status (rare, common and pest) andlarval developmental mode (planktotrophic, adel -pho phagic, lecithotrophic and poecilogonous). Aspecies was classified as pest, when it was called assuch by the author, when the author demonstrated asignificant negative impact on the host or wheninfestation exceeded 10 worms per individual (seeKojima & Imajima 1982). It was classified as com-mon if many of the hosts were infested, but theauthor did not consider it a pest or had not demon-strated a negative impact on the host (this usuallyapplied to small species which were often present inhigh densities without negatively affecting the host,or if the boring activity of the worm was not destruc-tive), or if the infestation level was 0.9. These were run through a descriptive dis-criminant analysis (DA) to detect differences in peststatus depending on host, culture method, pest spe-cies and larval developmental mode.

A 2 analysis was used to test the hypothesis thatthe larval development of pests depends on the cul-ture system in which the molluscs are reared, usingonly those records from the literature which indi-cated both the pest status and larval developmentalmode of the polydorids in question, and previouslyunpublished data collected by the authors.

Simple linear regressions were used to determinewhether there was a relationship between the num-ber of hosts cultured and the number of shell-infesting, non-indigenous polydorids and non-indigenous pest polydorids recorded per country,and between the number of shell-boring, non-indige-nous polydorid species and the number of shell-bor-ing, non-indigenous pest polydorids re corded oncommercially reared hosts, per country. For the latterana lysis, cryptogenic species, species which had onlybeen identified to genus level and references to P. cil-iata (this species is not a shell-borer and will be dis-cussed in more detail in Problems with taxonomybelow) were omitted as their alien statuses could notbe confirmed.

149


WHY DO ONLY SOME POLYDORID SPECIESBECOME PESTS?

Culture methods

Molluscs are cultured in a variety of ways whichdiffer in terms of location, production costs, feedingand exposure of the molluscs to water movement andair (Appleford et al. 2012, Castell 2012, Lucas 2012).In on-shore systems, animals may be grown in bas-kets, cages or bags suspended in outdoor raceways,ponds or dams, or indoor tanks; water is usuallypumped in from the sea, through the farm and backto sea, while the molluscs are usually constantly sub-merged (Appleford et al. 2012). Alternatively, ani-mals may be grown in on-bottom culture where spator hatchery-reared seed are sowed directly onto theseabed or suspended off long-lines or floating rafts incages or bags subtidally or in the off-shore (Nell2001, Appleford et al. 2012, Castell 2012, Lucas2012). These will also be submerged permanently,but are subject to prevailing water currents whichwill depend on depth and distance from the shore.These systems can be utilised for most molluscs. Cer-tain bivalves may also be grown in the intertidal; spatare captured on sticks, nets or in bags which are seton frames or trestles or they may be sowed directlyonto the rocks (Nell 2001, Appleford et al. 2012,Lucas 2012). These animals are exposed during lowtide. Animals in near- and off-shore and intertidalculture are seldom fed. Thus, depending on the cul-ture method, molluscs will experience different lev-els of water movement and exposure during tidalcycles which could, in turn, influence their exposureto larvae of fouling organisms. Additionally, thedegree of feeding of the molluscs may influence theamount of food available to shell-boring worms,which could further affect their populations.

Larval developmental modes

The success of shell-boring pest polychaetes canprobably be attributed to favourable conditions onfarms relative to the natural environment. Simon etal. (2005) suggested that the enhanced reproductiveoutput and recruitment of the pest sabellid poly-chaete Terebrasabella heterouncinata could proba-bly be attributed to the high availability of potentialhosts and suspended organic matter derived fromdegraded abalone food and faeces, which may havebeen further influenced by the nature of the abalonefeed (Simon et al. 2002). Similarly, the high volumes

of faeces and pseudofaeces produced by culturedbivalves (Lucas 2012) may also contribute to the suc-cess of pest polychaetes. Furthermore, the success ofpests may be related to their life history strategies;polydorids usually have high fecundity, with somespecies producing >5000 planktotrophic larvae perbrood, and an average of approx. 2574 (Blake 1969a,Sato-Okoshi et al. 1990, Blake & Arnofsky 1999)which may result in high propagule pressure. How-ever, not all worms that become established on farmsbecome pests (e.g. Dipolydora capensis on farmedabalone in South Africa) (Simon et al. 2006, Simon &Booth 2007, Boonzaaier et al. 2014, Simon 2015). Thediscrepancies between the shell-boring polydoridworms that could be im ported onto mollusc farmsand those that do become established, and betweenthe degrees to which the different species flourish,may be related to differences in the larval develop-mental modes among polydorids (Simon 2015).

Polydorids lay their eggs in capsules brooded in thematernal burrows, but species differ with respect tothe size, number and feeding mode of larvae pro-duced; females may produce many planktotrophiclarvae, few adelphophagic larvae which feed on un-fertilised nurse eggs in the brood capsules, or fewlecithotrophic larvae which are nourished by endo -genous yolk (Gibson 1997, Blake & Arnofsky 1999,Blake 2006). Planktotrophic larvae usually emergefrom the maternal burrow when 3 to 8 chaetigerslong, while adelphophagic and lecitho trophic larvaeemerge when 5 to 19 chaetigers long (Blake 1969a,Blake & Arnofsky 1999). Some species are poecilogo-nous, thus producing different types of larvae as de-scribed above, either by the same individual, or dif-ferent individuals within the same population (Gibson1997, Blake & Arnofsky 1999, Blake 2006, David et al.2014). However, irrespective of the size at emergencefrom the maternal burrow, the larvae of most speciesmetamorphose when they are 15 to 20 chaetigers and900 to 1600 m long (Blake & Arnofsky 1999, David &Simon 2014). This also coincides with the size atwhich larvae usually become too heavy to swim ac-tively and sink in preparation for settlement (Hansenet al. 2010). Thus, the time spent in the water columndepends on the difference between the size at emer-gence and the size at metamorphosis; depending onwater temperature, planktotrophic larvae can spendup to 85 d in the water column before settling, whilelarger adelphophagic or lecithotrophic larvae can set-tle within a day of emergence (Blake & Arnofsky1999). Thus the larval developmental modes of spe-cies will ultimately affect the ability of their larvae toreach molluscs in culture.


Predictions

We hypothesised that species which become pestsdepend on their larval developmental modes and theculture methods applied to the hosts for 3 reasons: (1)molluscs farmed in off-shore and on-shore conditionsare exposed to different levels of sea water move-ment, (2) the duration of the planktonic phases of dif-ferent polydorid species differ and (3) competent lar-vae are of a similar size. In on-shore culture systems,larvae produced in wild source populations mayenter farms with water pumped onto the farm, but,irrespective of the duration of their planktonicphases, only competent larvae can infest the mol-luscs and remain in the system. If the adult wormsthen produce larvae with an obligate protractedplanktonic phase, these will be lost from the systemvia the outflow. Thus resident worms will probablynot contribute to the establishment of large local pop-ulations on farms and we can predict that worms withthis life history strategy will not become very abun-dant in on-shore systems. By contrast, if the larvalplanktonic phase is short or absent, resident wormswould contribute to the establishment of a large localpopulation as the larvae remain on the farm, infest-ing the same or nearby hosts (David et al. 2014, seealso Simon 2005 concerning T. heterouncinata). Wecan therefore predict that species producing larvaethat emerge at a very late stage of development willdominate in on-shore culture systems.

In near-shore or off-shore culture systems, molluscswill be exposed to the prevailing currents and plank-ton which can include high densities of spionid(including polydorid) larvae (e.g. Omelyanenko &Kulikova 2002, Abe et al. 2014). The plankton willpresumably include larvae that may have long orshort planktonic phases, but probably more of theformer; of the larvae captured off-shore in OnagawaBay by Abe et al. (2014), 3 of the 5 spionids identifiedto species level are known to produce planktotrophiclarvae (Blake & Arnofsky 1999, Teramoto et al. 2013),while Polydora uncinata, a species known to producelarvae with short planktonic phases and found wildin this bay (Sato-Okoshi & Abe 2012) were absent.Thus we can predict that in off-shore and near-shorecultures molluscs will be infested primarily by spe-cies producing larvae with long planktonic phases.However, if species which produce lecithotrophic oradelphophagic larvae are introduced to off-shoreculture systems by way of infested molluscs, then wecan expect these worms to remain on these farms andflourish (for example, it has been suggested that thesudden appearance of P. uncinata in oysters in sus-

pended culture in South Korea was a consequence ofthe introduction of new oyster stocks from a differentsource population [Sekino et al. 2003, Sato-Okoshi etal. 2012]).

Results and discussion

Influence of pest species and larval developmentalmode, and host species and culture method

on pest status

Eightyinstancesofinfestation(fromtheliteratureandunpublished data collected by the authors of thepresent study) included informationof the larvaldevel-opmental modes of the pest and the culture method ofthe hosts (the pest and host species in cluded in thisanalysis are in bold in Table 1). These records included23 species of poly dorids infesting 19 host species(Table 1). Ap proximately half of the records werefrom off-shore culture systems, a third from on-shoresystems, a quarter from near-shore systems and only5% from intertidal culture systems (Table 2). Further-more, when all the records are considered (i.e. not justthose included in the PCA analysis), we found thatmost species (14) were in off-shore culture systems, 9in on-shore, 8 in near-shore and 3 in the intertidal.

The PCA extracted 4 components but only 2 hadeigenvalues >0.9 which explained a total of 62.45%of the variation in the sample. Discriminant analysesof these components showed that the model wasvalid (Boxs M = 6.65, p > 0.05) and that component 1(larval developmental mode and polychaete species)explained 92.6% of the variance in pest status. Withthe exception of P. hoplura and P. websteri, the poly-dorid species considered here only ever producedone type of larva in all records (different develop-mental modes were also recorded for Boccardiachilensis, which was not included in the analysis,Table 1). Thus larval developmental mode and poly-dorid species may to a large extent be surrogates ofeach other. Furthermore, 22% of the species (P. ona-gawaensis, P. uncinata, P. has welli, P. websteri and P.hoplura) accounted for 58% of the records. However,this analysis cannot account for species which mayhave been misidentified; consequently the impor-tance of pest species may have been overestimated.Component 2 (host and culture method) contributed


Species name Type region Country where Host infested present on cultured molluscs

Boccardia

B. acus New Zealand New Zealand Crassostrea gigas, Tiostrea chilensis

B. atokouica New Zealand New Zealand C. gigas

B. chilensis Chile Australia, New Zealand C. gigas, Mytilus edulis, Saccostrea cucullata, T. chilensis

B. knoxi New Zealand Australia, New Zealand C. gigas, Haliotis rubra

B. polybranchia Australia Australia, France C. gigas, M. edulis

B. proboscidea West coast of USA Australia, Japan, C. gigas, Haliotis midae South Africa, USA (Hawai)

B. pseudonatrix South Africa Australia, South Africa C. gigas, Saccostrea commercialis, H. midae

B. semibranchiata France (Mediterranean) France, Spain C. gigas

BoccardiellaB. hamata East coast of USA China, Japan C. gigas, pearl mussels

Dipolydora D. alborectalis Sea of Japan, Vostock Bay Japan Patinopecten yessoensis

D. armata Atlantic Ocean, Madeira Japan, South Africa Haliotis discus hannai, Haliotis diversicolor, H. midae

D. bidentata Sea of Japan, Japan C. gigas, P. yessoensis Peter the Great Bay

D. capensis South Africa South Africa H. midae

D. cf. giardi South Africa South Africa H. midae

D. concharum New England to Japan P. yessoensis Newfoundland

D. giardi Spain Chile, Japan Argopecten purpuratus, C. gigas, Ostrea chilensis

D. huelma Chile Chile Haliotis rufescens

D. keulderae South Africa South Africa C. gigas, H. midae

D. normalis South Africa South Africa H. midae

D. socialis Pacific Ocean, Chile Chile O. chilensis

PolydoraP. aura Japan Japan, Korea C. gigas, H. discus discus, Pinctada fucata

Table 1. Global distribution of shell-infesting and pest species that are associated with cultured or commercially harvested mol-luscs. Excludes species identified just to genus level. Pest status in native and invasive range given as pest (p), common (c), or rare(r). Larval developmental mode: adelphophagy (ad), lecithotrophy (le), planktotrophy (pl), poecilogony (po). Culture environment:

Simon & Sato-Okoshi: Polydorid polychaete pests on cultured molluscs 153

Pest status Pest status No. of pest Larval Culture Reference in native outside of records developmental environ- range native range (total records) mode ment

p 1(3) po int, off-s, nr Handley (1995), Handley & Bergquist (1997), Dunphy et al. (2005)

c 0(1) ? off-s Handley (1995)

p & c 1(6) ad, pl int, off-s, Skeel (1979), Pregenzer (1983), Handley (1995), nr Handley & Bergquist (1997), Nell (2001), Dunphy et al.

(2005)

p p 4(4) pl off-s, nr Handley (1995), (2000), Lleonart (2001), Nell (2001),Lleonart et al. (2003)

c p 1(2) ? int, off-s Pregenzer (1983), Ruellet (2004), Royer et al. (2006)

p, c, r 5(8) po int, on-p Bailey-Brock (2000), Sato-Okoshi (2000), Simon et al. (2006), Simon & Booth (2007), Simon et al. (2010), Walker (2014)

c, p r? 1(6) ad off-s, on-p Sato-Okoshi et al. (2008) (as Boccardia knoxi), Simon etal. (2010), Sato-Okoshi & Abe (2012), Walker (2014),Simon (2015), S. De Lange, C.A. Simon & L.G. Williamsunpubl. data

r 0(2) ? int Ruellet (2004), Martinez et al. (2006), Royer et al. (2006)

c 0(2) pl off-s Sato-Okoshi (2000), Zhou et al. (2010)

p 2(2) pl off-s Mori et al. (1985), Sato-Okoshi (1999)

p 1(2) ? on-p Simon (2011), W. Sato-Okoshi unpubl. data

p c 1(2) pl off-s, nr Sato-Okoshi (1999), W. Sato-Okoshi unpubl. data

c 0(1) pl on-p Simon et al. (2006), Boonzaaier et al. (2014)

r 0(1) ? on-p Boonzaaier et al. (2014)

c 2(2) pl nr Mori et al. (1985), Sato-Okoshi (1999)

c 0(4) pl off-s Sato-Okoshi (1999), Sato-Okoshi & Takatsuka (2001)

p 1(1) ? nr Vargas et al. (2005)

r 0(2) ? off-s, on-p Simon (2011), Boonzaaier et al. (2014)

r 0(1) ? on-p Simon (2011)

r 0(1) ? off-s Sato-Okoshi & Takatsuka (2001)

p 4(4) pl off-s, on-p Sato-Okoshi & Abe (2012), Sato-Okoshi et al. (2012)

intertidal (int), near-shore bottom and subtidal (nr), off-shore suspended (off-s), on-shore pond or tank (on-p). Pest status columns:pest status is only in relation to the infestation of cultured or harvested molluscs; blank spaces indicate that pest status is not

known. ?: unknown. Species names in bold were included in the principal component analysis

(continued on next page)


Species name Type region Country where Host infested present on cultured molluscs

P. bioccipitalis California Chile Mesodesma donacium

P. brevipalpa Sea of Japan, Vostock Bay China, Japan H. discus hannai, P. yessoensis

Brazil Brazil C. gigas, Crassostrea rhizophorae

P. ciliata England India, France, Germany, C. gigas, M. edulis, Ostrea madrasensis, P. fucata, Italy, UK Tapes philippinarum

P. cornuta East coast of USA USA Crassotrea virginica

P. curiosa Pacific Ocean, Japan P. yessoensis Kurile Islands

P. ecuadoriana Ecuador Brazil C. gigas, C. rhizophorae

P. cf. haswelli Australia? Brazil C. gigas, C. rhizophorae

P. haswelli Australia Australia, Korea, Japan, C. gigas, M. edulis, O. chilensis, New Zealand Pecten novaezelandiae, Perna canaliculus, P. fucata, S. cucullata, H. discus discus

P. hoplura Bay of Naples Australia, Belgium, France, C. gigas, M. edulis, H. midae, Haliotis Holland,New Zealand, tuberculata coccinea, H. rubra, South Africa, Spain Haliotis laevigata (Canary Islands)

P. onagawaensis Japan China, Japan C. gigas, Chlamys farreri, P. yessoensis, H. discus hannai

P. rickettsi Southern California Argentina, Brazil, Chile Aequipecten tehuelchus, A. purpuratus, Nodipecten nodosus, C. gigas, H. rufescens

P. uncinata Japan Australia, Chile, Japan, C. gigas, H. discus discus, H. discus hannai, Korea H. diversicolor, Haliotis diversicolor supertexta, Haliotis gigantea, Haliotis roei, H. laevigata

P. websteria East coast of USA Australia, Brazil, Canada, C. gigas, C. rhizophorae, C. virginica, M. edulis, China, Japan, Namibia, P. yessoensis, Placopecten magellanicus, P. fucata, Mexico, New Zealand, Pinctada imbricata, S. commercialis, South Africa, USA, S. cucullata, Saccostrea glomerata? Ukraine, Venezuela

PseudopolydoraPs. dayii South Africa South Africa H. midae

Table 1 (continued)

aPreliminary data from Williams (2015) suggest that specimens identified as Polydora websteri in southern Africa, Japan andAustralia are molecularly distinct from specimens from the east coast of America, and he consequently referred to them as


Pest status Pest status No. of pest Larval Culture Reference in native outside of records developmental environ- range native range (total records) mode ment

p 1(1) ? nr Riascos et al. (2008)

p 7(7) pl nr, off-s Imajima & Sato (1984), Sato-Okoshi (1999),Sato-Okoshi & Abe (2012), Sato-Okoshi et al. (2013),Teramoto et al. (2013)

r 0(2) le int Radashevsky et al. (2006)

p, r p 5(7) ? int, off-s Kent (1979), Velayudhan (1983), Ghode & Kripa (2001), Boscolo (2002), Ruellet (2004), Buck et al.

(2005), Royer et al. (2006), Brenner et al. (2009)

p 1(2) ? int Gaine (2012) (as P. ligni)

r 0(1) le off-s Sato-Okoshi (1999)

p 1(2) pl int Radashevsky et al. (2006)

? ? ?(2) pl ?, int Radashevsky et al. (2006)

c p, c, ? 8(13) pl, ? off-s, int, Skeel (1979), Pregenzer (1983), Read & nr, on-p Handley (2004), Read (2010), Sato-Okoshi et al. (2012), Walker (2014), Sato-Okoshi & Abe (2013)

p p, c, r, ? 11(20) ad, ad & pl int, off-s, Korringa (1951) in Wolff & Reise (2002), Skeel (1979), on-p Pregenzer (1983), Handley (1995), Lleonart (2001), Nell (2001), Lleonart et al. (2003), Ruellet (2004), Royer et al. (2006), Simon et al. (2006), Kerckhof et al.

(2007), Simon & Booth (2007), Bilbaa et al. (2011),Boonzaaier et al. (2014), Walker (2014), Simon (2015),S. De Lange, C.A. Simon & L.G. Williams unpubl. data

p 6(6) pl off-s Sato-Okoshi et al. (2013), Teramoto et al. (2013), Williams (2015)

p 6(7) pl nr, off-s Sato-Okoshi & Takatsuka (2001), Radashevsky & Cderas (2004), Vargas et al. (2005), Diez et al. (2013)

p p 16(15) ad off-s Sato-Okoshi (1999), Radashevsky & Olivares (2005), Sato-Okoshi et al. (2008, 2012), Sato-Okoshi & Abe (2012), W. Sato-Okoshi unpubl. data

c, p c, p, r 12(26) ad, po, pl, ? int Loosanoff & Engle (1943), Hartman (1954), Skeel (1979), Bailey-Brock & Ringwood (1982), Bergman et al. (1982), Pregenzer (1983), Sato-Okoshi & Nomura (1990), Bower et al. (1992), Handley (1995), Handley & Bergquist (1997), Sato-

Okoshi (1999), Nell (2001), Diaz & Liero Arana (2003),Sabry & Magalhes (2005), Sato-Okoshi et al. (2008,2013), Litisitskaya et al. (2010) in Surugiu (2012), Read(2010), Simon (2011) (as P. ciliata), Sato-Okoshi & Abe(2013), Simon (2015), Williams (2015), De Lange et al.(2011), authors unpubl. data

r 0(1) pl on-p Simon et al. (2009)

Table 1 (continued)

P. cf. websteri. However, since this separation has not been clarified, we here refer to all as P. websteri


the records of C. gigas were from off-shore culturesystems, 6 were on-shore, and 2 were from the inter-tidal. For Patino pecten yessoensis, 8 records eachwere from near-shore and off-shore culture systems.Furthermore, Haliotis discus discus and H. midaewere cultured in the same way in 4 out of 5 and 5 outof 6 records, respectively. Seven species wererecorded 2 or more times and were always culturedin the same way. The importance of host species andculture method is also highlighted when the inci-dence of pests were considered for the most fre-quently recorded species. In all of the records ofPatinopexten yessoensis in the near-shore and 71%of the records in the off-shore, the polydorids wereconsidered pests. Similarly, 71, 67 and 50% of the re -cords of polydorids infesting C. gigas in the off-shore,on-shore and intertidal, respectively, were of pests.

Although the PCA and discriminant analyses iden-tified 2 components which described the variability,the Wilks lambda values were not statistically signif-icant (Wald = 0.951, 2(4) = 3.84, p = 0.428; Fig. 1). Thisindicates that polydorid species, culture system, lar-val developmental mode and host species all con-tribute to pest status, irrespective of the actual peststatus but that different variables were important fordetermining the pest status under different condi-tions. This was further explored using only the re -cords of pests (which made up 79% of the records),with 2 analyses showing that the frequency of theinstances of pests depended on mollusc culture system and the larval development of the worms(2(6,55) = 30.12, p


maternal burrows coupled with their high survival,even if the number of larvae per brood is low(Simon 2005, David & Simon 2014). Since relativelyfew adelphophagic larvae are produced per broodand since they usually emerge just before theysettle (e.g. Blake & Kudenov 1981, Gibson 1997,Blake & Arnofsky 1999, Blake 2006) at a size whentheir swimming or dispersal ability is reduced(Hansen et al. 2010), their ability to reach off-shoreculture systems in appreciable numbers wouldprobably be hampered. In spite of this, P. hopluraand P. uncinata, for which only adelphophagy hasbeen widely recorded (e.g. Wilson 1928, Read 1975,Lleonart 2001, Sato-Okoshi 1998, 1999, Sato-Okoshiet al. 2008), were identified as important pests in 5off-shore systems. In at least 3 of these instances thehosts did not develop from natural spatfall and hadbeen transported from nursery systems (Lleonart etal. 2003, Simon 2015). It is therefore possible thatthe worms had reached the culture systems artifi-cially, and, once established, a large local popula-tion could develop in the same way as proposed foron-shore culture systems. It is, however, still possi-ble that the hosts had been infected by free-swim-ming larvae (Williams 2015). The absence of pestswith adelphophagic or lecithotrophic larvae in thenear-shore and intertidal is unexpected; if thesource population is inter- or subtidal, the relativeproximity to the cultured subtidal molluscs shouldenable infestations by such larvae.

Planktotrophy

Planktotrophic larvae are particularly well suitedto infest molluscs in the off-shore for 3 reasons.Firstly, they are produced by the thousands perbrood and should therefore be common componentsof the plankton. For example, Abe et al. (2014) re -corded up to 5000 larvae m3 of P. onagawaensis atup to 5 m depth in Onagawa Bay. Secondly, these lar-vae usual ly spend 3 to 4 wk in the water column (e.g.Blake & Arnofsky 1999, David & Simon 2014, Davidet al. 2014) which would increase their opportunitiesfor reaching off-shore systems. Finally, plankto -trophic larvae are usually active swimmers until theybecome too heavy and are ready to settle (Hansen etal. 2010). Together with movement by water cur-rents, these characteristics should enable plankto -trophic larvae to reach molluscs in off-shore culturein high enough numbers to become problematic eventhough larval mortality may be high. Intensive cul-ture in near-shore and off-shore systems may further

enhance the successful recruitment of planktotrophiclarvae by providing substrates which would other-wise not be available in the area.

Buck et al. (2005) and Brenner et al. (2009) con-cluded that the dilution of polydorid larvae due todistance from near-shore source populations signifi-cantly reduced the susceptibility of mussels, Mytilusedulis, in off-shore suspended culture to infestation.These distances (11 to 27 km) were, however, con-siderably greater than, for example, in South Africaand Japan (1 km, Williams 2015; W. Sato-Okoshipers. obs.), and probably other countries too, andcould ac count for the different findings. Buck et al.(2005) also suggested that the short planktonicphase of the polydorid, which they identified as P.ciliata (2 wk planktonic phase, as described by Daro& Polk 1973; but see also Problems with taxonomybelow), also played a role. Undoubtedly, here theeffects of a short planktonic phase and the greatdistance off-shore were further exacerbated by asmall source population where only 1.7 to 2.7% ofthe samples were infested by a mean of up to 6worms per infested shell (Buck et al. 2005, Brenneret al. 2009). Larger source populations that arecloser to the culture systems and composed of spe-cies with longer planktonic phases would pose agreater risk (e.g. P. brevipalpa infesting wild andcultured Patinopecten yessoensis in Abashiri Bay[Sato-Okoshi & Abe 2012], and P. onagawaensisfound on farmed scallop and wild abalone in thesame localities [Sato-Okoshi & Abe 2013]).

Poecilogony

Poecilogony is a rare reproductive dimorphism(Chia et al. 1996, David et al. 2014). A perceivedadvantage to poecilogony for pest polydorids is thatthey may benefit from dispersal by the plankto -trophic larvae to the off-shore systems, and the laterdevelopment and maintenance of local populationsby the adelphophagic larvae (Chia et al. 1996, David& Simon 2014, David et al. 2014). However, the typeof poecilogony could affect the ability of a species tobecome established in off-shore systems as a con -sequence of the final number of larvae that meta -morphose. Poecilogony was recently described forP. hop lura from South Africa, with females producingeither planktotrophic or adelphophagic larvae(David et al. 2014). Purely planktotrophic broods ofP. hoplura contain more than a thousand larvae whilepurely adelphophagic broods contain a mean of 20(David et al. 2014). In Simon (2015), all the develop-


ing broods observed in the off-shore containedplanktotrophic larvae, while all those from the on-shore populations contained adelphophagic larvae.The larval type of females not brooding at the time ofsampling was not determined, so it is possible thatthey produced different types of larvae, since mixedpopulations have been found (David 2015). This sug-gests that in South Africa at least, off-shore popula-tions may have been established by planktotrophiclarvae and then maintained by later generations offemales producing adelphophagic larvae. By con-trast, poecilogonous species producing both larvaltypes simultaneously appear not to capitalise on thedual advantages of different larval types, as evi-denced by the low number of records of poecilo -gonous pests in off-shore culture systems. This mightbe a consequence of inter-sibling competition. Inmixed broods of Boccardia proboscidea, plankto -trophic larvae are often cannibalised by theiradelpho phagic siblings, reducing the number of dis-persive larvae entering the water column (David &Simon 2014). Furthermore, planktotrophic larvae inmixed broods lack swimming chaetae which mayinhibit their swimming abilities compared to that oflarvae from pure broods (Gibson 1997). This mightalso apply to other species which produce mixedbroods.

The high incidence of pests with planktotrophiclarvae may be because the larvae are produced insuch high numbers that they out-compete specieswith adelphophagic larvae. Alternatively, or addi-tionally, it may reflect the fact that many polydoridspecies produce planktotrophic larvae. Of the spe-cies included in this review for which the larvaldevelopmental modes are known, 62.5% produceplanktotrophic larvae, 8.3% each produce adelpho -phagic or lecithotrophic larvae or are poecilogo-nous, with a further 12.5% having different modesin different records (Table 1). These proportionsare very similar to those found among the Boccar-dia, Boccar di ella, Dipolydora and Polydo ra species;59, 21 and 3% produced plankto trophic,adelphophagic and lecithotrophic larvae, respec-tively, while 16% were poecilogonous (Blake &Arnofsky 1999). These proportions are also similarto that of individual records of polydorids in differ-ent culture systems (Table 2): planktotrophy (68%),adelphophagy (16%), lecitho trophy (2%) and poe-cilogony (14%). Thus the high incidence of pestspecies producing planktotrophic larvae in theintertidal, near-shore and off-shore may be a pro-portionate representation of species with plank-totrophic larvae among the polydorids. However,

the disproportionately high number of records foradelphophagic and poecilogonous developmentamong species recorded as pests in on-shore facili-ties supports the hypothesis that some se lectiondoes occur there (e.g. P. hoplura, B. pro bos cideaand Boccardia pseudonatrix in South Afri ca [Simon2015], P. uncinata and B. pseu do natrix [as B. knoxi,Sato-Okoshi et al. 2008] in Australia and P. uncinatain Japan [Sato-Okoshi et al. 2015]).

Host and culture system

The link between larval development and peststatus of worms in different culture systems may befurther enhanced by the culture period of the hostsin the different systems. Thus the dominance of spe-cies with larvae that emerge at a late stage of devel-opment in on-shore culture systems may also berelated to the fact that 16 of the 22 records in on-shore facilities included in this study were of slow-growing aba lone which remain in culture for >4 yr(Castell 2012). This would facilitate the accumula-tion of many polydorids (Pregenzer 1983) and overmany generations; e.g. B. proboscidea start repro-ducing within about 1 mo of settling and live forapprox. 1 yr, during which time they produce manysuccessive broods, leading to almost constantrecruitment on farmed abalone (Simon & Booth2007; see also Sato-Okoshi et al. 2015, for moreexamples). Thus, when hosts remain in culture forseveral years, exponential growth of the worm pop-ulation can be expected if conditions re main thesame or effective remedial measures are not taken.Conversely, 18 of the 39 records of off-shorecultures were of oysters and mussels that re main inculture for


GLOBAL SPECIES DIVERSITY, DISTRIBUTION,HOST SPECIFICITY AND TAXONOMY

Movement of pests with molluscs in aquaculture

Reviews that consider polydorids in general, andshell-infestors associated with cultured molluscs inparticular, usually have a regional focus: Chile (Sato-Okoshi & Takatsuka 2001, Moreno et al. 2006), SouthAfrica (Simon et al. 2006, Boonzaaier et al. 2014,Simon 2015), Japan (Sato-Okoshi 1999, Sato-Okoshi& Abe 2013), Korea (Sato-Okoshi et al. 2012), China(Zhou et al. 2010, Sato-Okoshi et al. 2013), Australia(Blake & Kudenov 1978, Sato-Okoshi et al. 2008,Walker 2011, Walker 2014), New Zealand (Read2004) and the United States of America (e.g. Blake1969b). These often indicate the presence of speciesthat are outside of their natural distribution ranges,but there is no comprehensive global review of theshell-boring polydorid pests of cultured molluscs.

The movement of molluscs for aquaculture hasbeen implicated in the inadvertent spread of manyalien species, including polychaetes (e.g. Wolff &Reise 2002, McKindsey et al. 2007, Ruesink et al.2005, Haupt et al. 2012, inar 2013). In particular,Haupt et al. (2012) demonstrated that even aftercleaning, oysters still harboured polydorid shell-borers after translocation. Yet the records which con-firm oysters and abalone as the vectors of transporta-tion are limited; Polydora websteri and Boccardiaproboscidea were transported from mainland USA toHawaii (Bailey-Brock & Ringwood 1982, Bailey-Brock 2000), P. uncinata from Japan to Chile (Rada-shevsky & Olivares 2005), and probably P. websterifrom Namibia to South Africa (Simon 2015, Williams2015), while the sabellid Terebrasabella heterounci-nata was transported from South Africa to Californiaand further (Culver et al. 1997, Moreno et al. 2006).In some instances aquaculture may not have beenthe vector of introduction of a pest to a new region,but is responsible for its spread within its introducedrange (e.g. Simon et al. 2009, Haupt et al. 2012,Williams 2015). Despite this close association be -tween polydorid polychaetes and cultured molluscs,reviews of the contribution which aquaculture makesto the movement of aliens pay little or no attention topolydorids (e.g. Wolff & Reise 2002, Ruesink et al.2005, McKindsey et al. 2007).

This neglect might be because molluscs would betreated against polydorids in general rather than anyspecific species (Royer et al. 2006), rendering theidentification of individual pest species meaninglessto many farmers. The neglect would be further exac-

erbated by the many taxonomic problems associatedwith polydorids (Sato-Okoshi et al. 2015). However,the failure to identify species means that their spreadbeyond their natural distribution ranges is often onlynoticed after they have become established and arethen almost impossible to eradicate (Bailey-Brock1990).

Results and discussion

A total of 178 records from the literature andauthors un published data identified 38 polydoridspecies (8 Boccardia spp., 1 Boccardiella sp., 11 Di -poly dora spp., 17 Polydora spp., 1 Pseudo polydorasp., excluding those that had only been identified togenus level), infesting 36 cultivated or commerciallyharvested mollusc species in 25 countries on all con-tinents except Antarctica (Table 1). Half the speciesconsidered in this review are, or have the potential tobe, problematic alien species. The most virulent ofthese are undoubtedly P. websteri, P. uncinata, P.haswelli and P. hoplu ra, which collectively infest 21hosts in 17 countries. Among these species, P. unci-nata was always considered a pest (in 15 records)while P. hoplura, P. websteri and P. has welli wereconsidered pests in approximately half of theinstances where they were reported with culturedmolluscs (Table 1). Twelve species were re corded in2 countries and 21 in only one. Eighteen species wereassociated with commercially important molluscsonly within the native range of the polychaete, 8were recorded within and outside of their nativeranges, and 9 were recorded only outside of theirnative ranges. From among these species, where theproportion of records as pests exceeded 50%, themaximum total number of records was 8. Thirteenspecies were never recorded as pests (Table 1).Among the species infesting only 1 host, only Boccar-dia semibranchiata, infesting Crassostrea gigas, wasrecorded in more than one country (France andSpain). Of the species that infested more than 2 hosts,11 were restricted to either one country, or oneregion (e.g. P. onagawaensis has only been found inChina and Japan, and P. aura has only been found inJapan and Korea, while P. rickettsi which, althoughrestricted to South America, was recorded in Chile,Argentina and Brazil).

inar (2013) suggested that 36 of the 292 alienpolychaete species that he reviewed were probablymoved by aquaculture, including 1 sabellid and 15polydorid shell-borers. However, he undoubtedlyunderestimated the full extent of the distribution of

159


these pests as he only considered records whereworms were specifically identified as alien; for exam-ple, he did not list P. hoplura as an alien in Australia,although it had already been recorded there severaltimes (Blake & Kudenov 1978, Hutchings & Turvey1984, Lleonart et al. 2003). Our tally has increasedthe number of known alien shell-infesting polydoridsto 17, with the addition of Boccardia chilensis and Di -po ly dora concharum. Furthermore, the alien rangesof 9 species have been extended (Boccardiella ha ma -ta, Boc car dia polybranchia, Boccardia pseudonatrix,D. armata, D. concharum, P. ciliata, P. haswelli, P.hoplura, P. rickettsi and P. websteri) while Boccardiasemibranchiata and P. hoplura should be consideredcryptogenic, rather than alien, on the Atlantic coastof Europe (cf. inar 2013 and Haydar & Wolff 2011).

Relationship between aquaculture and the spread ofalien species

Although there are few instances where the move-ment of molluscs for aquaculture was the confirmedvector for the transport of polydorids, this reviewconfirms the conclusions of previous authors thataquaculture is an important vector and reservoir ofexotic species, including polychaetes (e.g. Wolff &Reise 2002, inar 2013). Linear regressions showedsignificant positive relationships between the num-ber of hosts cultured in a country and the number of(1) shell-infesting, (2) non-indigenous polydo rids and(3) non-indigenous pest polydorids recorded percountry (Table 3). Furthermore, a positive significantrelationship was found between the number of non-indigenous shell-boring polydorid species and thenumber of shell-boring non-indigenous pests re -corded on commercially reared hosts, per country(Table 3). For the latter analysis, cryptogenic species(such as P. hoplura in France and Belgium) wereomitted, as were species identified only to genuslevel and references to P. ciliata because their alienstatus could not be confirmed. In spite of a small sam-

ple size, these analyses provide a telling indictmenton the role which aquaculture plays in the spreadand flourishing of alien pest polydorid species. Thisconclusion is further reinforced by the fact that themost non-indigenous pests were recorded in Japan,which also cultivated the most hosts (e.g. Sato-Okoshi & Nomura 1990, Sato-Okoshi 1999, Sato-Okoshi & Abe 2012, 2013). Additionally, all of thepest polydorids associated with cultured oysters inAustralia (Walker 2014), 5 of the 6 species in Chile(Moreno et al. 2006) and 3 of the most importantpests in South Africa (Boonzaaier et al. 2014, Simon2015, Williams 2015) are alien.

Host specificity

Although host species was identified as a factor indetermining pest species, shell-infesting polydoridsare usually not host-specific (Moreno et al. 2006, Sato-Okoshi et al. 2008, Simon 2011, 2015). This is sup-ported by this review. Eight of the 37 species infestedmore than 4 hosts, with P. websteri, P. haswelli, P. un-cinata and P. hoplura recorded on 6 or more hosts(Table 1). Eleven and 13 species were re corded on 2hosts or one host, re spectively, when unidentified spe-cies are ex cluded. The species which were recordedon only one host may in fact represent a restricted dis-tribution range of the worm since some of these spe-cies were recorded only in one country or region each(e.g. B. semibranchiata, D. albo rec talis), while othershave been recorded on other hosts which are not com-mercially important (e.g. D. socialis, D. concharum,Blake 1971). Similarly, 10 species infested only bi-valves but this might reflect the situation on farmsrather than host specificity (Table 1); for example, P.websteri has only been recorded on bivalves in cul-ture, but also on gastropods in the wild (Blake 1971)while, D. armata has only been found on farmedabalone, but is not restricted to gastropods in the wild(e.g. Sato-Okoshi 1999). One exception is D. capensis,which has been recorded widely on wild and farmed

gastro pods in South Africa butnever on oysters, even whenpresent on aba lone close by (Si-mon 2011, 2015). The physicalstructure of the host may, how-ever, affect its susceptibility toinfestation. For example, the ru-gose nature of the shell of C. gi-gas is believed to contribute to itseffectiveness at creating habitatsfor other organisms (Haydar &

Equation (n) R2 p

Polydorids vs. hosts y = 0.24 + 1.24x (25) 0.651


Wolff 2011). Similarly Haliotis midae is infested bymore species (Boonzaaier et al. 2014) than any otherhaliotid included in the present study and this may bea consequence of the rugose nature of its shell com-pared to that of other haliotids (Fig. 2).

Problems with taxonomy

An important outcome of this review is that it hashighlighted the species for which identifications are(probably) problematic. Since its initial identificationas a pest of oysters by Haswell (1885), B. poly-branchia has been recorded as a pest of C. gigas inFrance (Ruellet 2004, Royer et al. 2006) and My ti lusedulis in Australia (Pregenzer 1983). There is, how-ever, much confusion in the literature around thisspecies (Blake & Kudenov 1978, Simon et al. 2010)and it probably includes several morphologicallysimilar species. Additionally, it has not beenrecorded with oysters in Australia since 1983 (Pre-genzer 1983, Walker 2014), while the photographprovided in Ruellet (2004, their Fig. 50), though notvery clear, more closely resembles B. proboscidea,which has also been recorded on the Atlantic coastof Spain (Martinez et al. 2006), in Roscoff, France (T.Struck & C. A. Simon unpubl. data) and Belgium(Kerckhof & Faasse 2014). It is therefore possible thatthe identifications of this species as a pest are incor-rect. Similarly, P. ciliata was originally described insediment (Johnston 1838) and its identification as ashell-borer is therefore very controversial. Blake(1971) and Blake & Kudenov (1978) suggested that P.ciliata infesting cultured molluscs on the east coast ofNorth America and in Australia were probably P.websteri. Later, Mustaquim (1988) demonstrated thatshell-boring P. ciliata in Europe were molecularlydistinct from non-boring forms; yet P. ciliata has beenidentified as a shell-borer several times since 1988, in

Europe, India and China (our Table 1, Gao et al.2014), thus perpetuating earlier errors.

Recent morphological and molecular analyses sug-gest that extensive revision to 3 important pest spe-cies is necessary. Here we identified P. websteri asthe most wide-spread shell-boring polydorid. How-ever, recent molecular analysis suggested that P.websteri from near the type locality is molecularlydistinct from conspecifics in southern Africa, Japanand Australia, suggesting that at least these latterrecords represent a different species which Williams(2015) referred to P. cf. websteri. Additionally, it isun certain whether P. websteri in Brazil (Sabry &Magalhes 2005) should be referred to P. haswelli(see Rada shevsky et al. 2006). Thus the records con-sidered here of P. websteri may actually representseveral species. To further complicate matters, pre-liminary molecular investigations also suggest that P.ona ga wa ensis may be synonymous with P. websteri(Williams 2015). Additionally, studies by Read (2010),Walker (2014) and Williams (2015) provide compell -ing arguments for synonymising shell-boring P. has -welli with P. neocaeca and P. uncinata with P. hop lu -ra. If they are right, the known distribution of thesespecies will change considerably, and P. hoplura willbe the most widespread pest in the world.

The literature reviewed here also included 7 Poly-dora, 2 Boccardia and 3 Dipolydora species identifiedonly to genus level. Given the frequency with whichpolydorids may be moved with aquaculture and ship-ping (inar 2013), it is imperative that pest polydoridworms be identified properly. This will increase ourunderstanding of the actual movement and distribu-tion of shell-infesting polydorids and help identifynew alien species in time to enable eradicationbefore the worms become established. It is clear thatpolydorids can be difficult to identify, especially formany aquaculturists who lack taxonomic trainingand access to the literature. For example, South Afri -

Fig. 2. (A) Haliotis midae, (B) H. gigantea and (C) H. discus hannai showing the difference in the rugosity of the abalone shells (scale bars = 2 cm), which can influence the species susceptibility to infestation by polydorid species


can farmers initially assumed that locally culturedabalone were infested by a Polydora species, whenthey were, in fact, infested by P. hop lu ra, B. probos -cidea and D. capensis (Simon et al. 2006, Simon et al.2010). It is therefore imperative that an alternativemeans to identify worms is developed, and that amolecular database of polydorids, using commonDNA markers such as 18S rRNA, 28S rRNA and COI,be generated. Such a database will facilitate therapid identification of pests, even when regional tax-onomic expertise is lacking.

CONCLUSIONS

Observations of the larval developmental modes ofpolydorid pests of cultured molluscs in South Africa(Simon 2015) suggested that molluscs grown in on-shore culture systems are more likely to be infested byspecies producing larvae which leave the maternalburrow at a late stage of development while those inoff-shore culture systems would be infested byspecies producing larvae with a longer planktonicphase. Our review of the literature reporting the peststatuses and larval developmental modes of poly-dorids infesting cultured (or commercially harvested,wild) molluscs suggest that these observations arevalid on a more global scale. However, a more com-plete analysis is hampered by several confoundingfactors. (1) Polydorids are usually investigated onlywhen they become problematic, and many countriesare therefore presumably not experiencing problemswith infestations. For example, Crassostrea gigas iscultured in more than 50 countries (Ruesink et al.2005, Castell 2012), but we found records of infestationfor just a third of that. This does not necessarily meanthat oysters in the remaining countries are free ofpolydorids, just that they have not been investigated.Thus the rare and common polydorid species wouldprobably have been under-represented in the analy-sis. (2) Polydorids are sometimes investigated duringtargeted research by taxonomists, but the pest statusof the worms may not always be indicated (e.g. Blake1971, Walker 2014). Furthermore, the positive rela-tionship between the numbers of shell-boring poly-dorid species and cultured hosts examined percountry may be influenced by the level and number oftaxonomic studies conducted in different countries.For example, since the 1990s, one of the authors (W.Sato-Okoshi) has re corded 15 polydorid species asso-ciated with 9 cultured mollusc species in Japan (e.g.Sato-Okoshi & Nomura 1990, Sato-Okoshi 1999, Sato-Okoshi & Abe 2012, 2013). Similarly, many polydorid

species (in cluding non-indigenous and pest species)have been recorded in South Africa (14; e.g. Boonza-aier et al. 2014, Williams 2015), Australia (9; Blake &Kudenov 1978, Skeel 1979, Sato-Okoshi et al. 2008,Walker 2014), New Zealand (7; Handley & Bergquist1997, Read & Handley 2004, Read 2010), Chile (6;Sato-Okoshi & Takatsuka 2001, Moreno et al. 2006)and Brazil (5; Radashevsky et al. 2006). In contrast,only 4 polydorid species have been re corded in China,on 5 hosts (Zhou et al. 2010, Sato-Okoshi et al. 2013).Since China is the leading producer of molluscs glob-ally, culturing at least 11 species (Castell 2012, Lucas2012), this is undoubtedly an underestimate of theshell-boring polydorids in that country. (3) Certain cul-ture methods have been used more frequently thanothers. Among the re cords considered here, off-shoresuspended culture was the most frequently used (for 14species in 24 countries), followed by near-shore culture(13 species in 13 countries), on-shore (11 species in 13countries) and intertidal culture (5 species in 12 coun-tries). The apparent preference for off-shore sus-pended culture may have biased the analyses.

To fully understand regional polydorid species di -ver sity and the risk of species becoming pests orbeing moved along with their hosts, polydorid infes-tations must be surveyed under cultured and naturalconditions. Species which are benign in their nativeranges may become pests when translocated to a newregion or exposed to novel hosts, as did B. pro-boscidea in South Africa. While we provide strong ev-idence suggesting that larval developmental modedetermines which species will become pests (particu-larly in on-shore systems), other life history character-istics may also play a role, such as the life span andthe timing and duration of the reproductive and set-tlement periods (i.e. the longer the more severe theinfestation). Such information will enable aquacultur-ists to predict which species could become problem-atic while knowl edge of the timing of the settlementof juveniles will allow the timeous implementation ofcontrol measures.

Acknowledgements. The authors thank Natasha Mothapofor her advice and help with the statistical analyses andAndrew David and Matt Bentley for their valuable com-ments on the manuscript. C.A.S.s visit to Japan was fundedby the HB & MJ Thom and Oppenheimer Memorial Trusttravel grants and research funds were provided by theNational Research Foundation (Thuthuka Programme). Thefunding bodies made no contribution to the development ofthe study, the interpretation of the data or the preparationand submission of the manuscript. C.A.S. also thanks thestaff and students of the Laboratory of Biological Oceanog-raphy, Tohoku University, Sendai, for their hospitality dur-ing her stay.


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