Polydora uncinata (Polychaeta: Spionidae) in Chile: an accidental

transportation across the Pacific

Vasily I. Radashevsky1 & Carolina Olivares2,*1Institute of Marine Biology, Russian Academy of Sciences, Vladivostok 690041, Russia; 2Departamentode Biologıa Marina, Universidad Catolica del Norte, Casilla 117, Coquimbo, Chile; *Author forcorrespondence (e-mail: che@ucn.cl)

Received 19 August 2003; accepted in revised form 1 April 2004

Key words: abalone, aquaculture, blister worms, Chile, oysters, Pacific, Polychaeta, Polydora uncinata

Abstract

A Polydora species was found boring in shells of the abalone Haliotis discus hannai cultivated in land-based tanks in Coquimbo, Chile. Spionid polychaetes of Polydora and related genera have been reportedfrom Chile but no worms similar to those found in abalone have been described. The abalone pest cor-responds in morphology to Polydora uncinata Sato-Okoshi, 1998, a shell-boring species which was origi-nally described from Japan and never reported from outside the country. It is suggested that occurrenceof the species in Chile resulted from its accidental transportation from Japan. Adult worms were mostlikely transported to Coquimbo with imported abalone brood stock. Prevalence of abalone infestationby worms in Coquimbo varied substantially among cultivation tanks, reaching values as high as 98.8%.Up to 42 worms were found in one shell. The worms often caused formation of nacreous blisters whichcovered up to 50% of the inner shell surface. Egg capsules with developing larvae were present in femaleburrows. Larval development was entirely lecithotrophic, with larvae feeding on numerous nurse eggs,staying inside egg capsules until 16–17-segment stage and hatching shortly before metamorphosis. Poly-dora uncinata is redescribed based on individuals from Coquimbo to alert zoologists in case of accidentalrelease of worms into Chilean coastal waters. Regardless of how the species was transported to Chile, itsrelease to the natural ecosystem may have negative unforeseen impacts on the native fauna.

Introduction

Since 1987, 11 shipments of adult abalone Halio-tis discus hannai Ino, 1953 have been transportedto aquaculture facilities in Coquimbo, Chile,from four provinces on the Pacific side of Hon-shu Island, Japan (Resolutions No. 1281/87, 58/88, 975/89, 1518/89, 1367/91, 814/95, 1599/96,900/98, 829/00, 1008/02, 2873/02 of Ministerio deEconomıa, Fomento y Reconstruccion). Impor-ted abalone were maintained in a land-based sys-tem in Coquimbo and used as brood stock toprovide offspring to other land-based centers inthe country. Progeny of these abalone were also

used in a pilot experiment aimed at introductionof the molluscs into coastal waters for furthercommercial cultivation (Resolution No. 220/02 ofMinisterio de Economıa, Fomento y Reconstruc-cion). Abalone from tanks in Coquimbo werestudied by the authors and numerous individualsof a polydorid polychaete were found boring inabalone shells. These worms differed substantiallyfrom polydorids so far reported from Chile(Hartmann-Schroder 1962; Carrasco 1974; Roz-baczylo et al. 1980; Blake 1983; DiSalvo andMartınez 1985; Rozbaczylo 1985; Basilio et al.1995; Sato-Okoshi and Takatsuka 2001; Rada-shevsky and Cardenas 2004) and were identified

Biological Invasions (2005) 7: 489–496 � Springer 2005

as Polydora uncinata Sato-Okoshi, 1998. ThisPolydora species was originally described fromthe Pacific coast of Honshu Island as a borer ofshells of both wild Omphalius rusticus (Gmelin,1791) and cultivated Pacific oyster Crassostreagigas (Thunberg, 1793), and has not beenreported from outside of Japan (Sato-Okoshi1998).

Commercial oyster industry and aquaculture ingeneral is one of the means by which cultivatedand associated species can be dispersed outwardfrom their native regions through human’s activ-ity (Carlton 1975, 1987; Cohen and Carlton 2001;Naylor et al. 2001). Lists of species introduced bythese means usually include polychaetes, and spio-nids are always among them. It is likely that fourtube-dwelling spionid species have been intro-duced to California in entrapped sediment thataccompanied adult and seed oysters: Polydoracornuta Bosc, 1802 and Streblospio benedicti Web-ster, 1879 in association with the American oyster,Crassostrea virginica (Gmelin), transplanted fromthe Atlantic coast of North America, plus Pseudo-polydora kempi (Southern, 1921) and Pseudopoly-dora paucibranchiata (Okuda, 1937) along withthe Pacific oyster, C. gigas, transplanted fromJapan (Carlton 1975). A boring spionid Polydorawebsteri Hartman in Loosanoff and Engle, 1943was introduced to the Hawaiian Islands alongwith spat and young oysters purchased fromhatcheries on the east and west coasts of NorthAmerica (Bailey-Brock and Ringwood 1982; Bai-ley-Brock 1987). Tube-dwelling Polydora nuchalisWoodwick, 1953 was probably introduced to theHawaiian Islands with shipments of shrimp fromwestern Mexico to stock ponds at one of theaquaculture farms (Bailey-Brock 1990). Boccardiaproboscidea Hartman, 1940 was introduced to anoyster culture farm in the Hawaiian Islands withshipments of Ostrea edulis Linnaeus, 1758 fromMaine (Bailey-Brock 2000). Three boring spio-nids, Polydora websteri, Polydora hoplura Clap-arede, 1869 and Boccardia chilensis Blake andWoodwick, 1971 infesting commercial bivalveswere possibly introduced to New Zealand (Hand-ley 2000). Similarly, Boccardia berkeleyorum Blakeand Woodwick, 1971 known from California andVancouver Island was recently reported from gas-tropod shells in the Philippines, likely representingan accidental introduction to the Indo-West Paci-fic (Williams 2001).

Boring polydorids, also called blisterworms ormudworms are known pests which can cause seri-ous damage to molluscs, both cultivated and liv-ing in natural ecosystems (Haswell 1885;Whitlegge 1890; Lunz 1941; Loosanoff and Engle1943; Hewatt and Andrews 1954; Owen 1957;Galtsoff 1964; Mohammad 1972; Blake andEvans 1973; Kent 1979; Skeel 1979; Lauckner1980, 1983; Wargo and Ford 1993; Handley1995, 1998; Blake 1996; Handley and Bergquist1997; Lleonart et al. 2003a, b). Many of themcan rapidly become established and reach epi-demic proportion in aquaculture facilities. Forexample, an infestation of P. websteri in culturedoysters contributed to the collapse of a highlyintensive aquaculture industry at Kahuku,Hawaiian Islands (Bailey-Brock and Ringwood1982; Bailey-Brock 1987). Cumulative mortalitylevels of 50% or more associated with two spio-nid mudworms, Boccardia knoxi (Rainer, 1973)and P. hoplura, were reported by various sea-based abalone culture facilities within Tasmaniaduring the mid-1990s (Lleonart et al. 2003a, b).

The purpose of the present study is to describethe Polydora worms from abalone shells in Co-quimbo, compare them with type material ofP. uncinata from Japan, report an accidentaltransportation of P. uncinata to Chile, and alertzoologists to the potential for accidental releaseof worms into Chilean coastal ecosystems.

Materials and methods

Live abalone were collected from land-based cul-tivation tanks in Coquimbo (29�59¢ S, 71�22¢ W),Chile monthly from November 2002 throughApril 2003. Blister coverage was estimated visu-ally. Abalone shells were broken into small frag-ments with pliers and polychaetes were removedunder a stereomicroscope in the laboratory. Theworms were relaxed in isotonic magnesium chlo-ride, measured and examined alive with lightmicroscopes. Drawings were made using a cam-era lucida and images were taken using a digitalcamera. After examination, a part of adultworms was fixed in 10% formalin solution, rinsedin freshwater and transferred to 70% ethanol.Fixed material was deposited at the MuseoNacional de Historia Natural, Santiago deChile (MNHN An 2010-2012, 3 specimens) and

490

Senckenberg Museum, Frankfurt am Main, Ger-many (SMF 13492, 18 specimens). Type materialof P. uncinata deposited in the Natural HistoryMuseum and Institute, Chiba, Japan (NHMICCBM-ZW 902, 3 paratypes) was also examined.

Results

Systematic account

Spionidae Grube, 1850Polydora Bosc, 1802Polydora uncinata Sato-Okoshi, 1998 (Figures1–4)Polydora uncinata Sato-Okoshi, 1998: pp. 278–280, Figure 1; 1999: p. 835.

Description of the Chilean material

Largest specimen 32 mm long and 1.2 mm wideon segment 7 for 117 segments. Body pale in life;fixed specimens usually with secretory cells visibleas small dark spots scattered on dorsal side ofposterior segments. Fine continuous black lineusually present on palps along edges of ciliatedfood groove in small individuals; up to 12 pairsof black bars present on each palp in large indi-viduals; bars arranged regularly on distal 1/2–2/3

of palp (Figure 2A); occasionally, pigmentationon palps absent.

Prostomium weakly incised anteriorly, thusincision occasionally seen only in ventral view.Caruncle extending posteriorly until end of seg-ment 2 or middle of segment 3. Short nuchalantenna present on caruncle. Four eyes usuallypresent, including one pair of anterior and onepair of posterior eyes; occasionally eyes absent.Palps extending posteriorly for 10–20 segments;with longitudinal food groove lined with finefrontal cilia; latero-frontal motile compound cilia(cirri) and short papillae with non-motile cirribordering food groove; papillae with non-motilecirri also scattered on lateral and abfrontal palpsurfaces.

Segment 1 with small postchaetal lamellae inboth rami; notochaetae absent; short capillariespresent in neuropodia. Single (occasionally two)recurved heavy spines and 2–6 slender capillariespresent in notopodia of posterior postbranchiatesegments (Figures 2B and 2C). Spines firstappearing in juveniles on segment 18, synchro-nously with formation of segment, and develop-ing on all following segments; spines lost fromanterior notopodia as growth proceeding andstarting from more posterior segments in biggerworms (Figure 3). In adults spines usually starting1–3 (occasionally 4–17) segments after posterior

Figure 1. Map showing suggested path of Polydora uncinata across the Pacific.

491

branchiate segment; in one individual, spinesstarted on last branchiate segment. Notopodialpostchaetal lamellae reduced on branchiate seg-ments but slightly enlarged on posterior,abranchiate segments, thus appearing like bran-chiae (Figures 2B and 2C). In largest individualwith 117 segments, branchiae terminating on seg-ment 102 and recurved spines starting on seg-ment 104.

Segment 5 greatly modified, almost twice aslarge as segments 4 or 6, without postchaetallamellae, with 3–6 dorsal superior winged capil-laries (Figure 2E), up to 7 major modified spines

alternating with pennoned companion chaetae,and 3–7 ventral winged capillaries (Figure 2D).Dorsal superior and ventral capillaries shorterand fewer than those on adjacent segments.Major spines arranged in a slightly curved diago-nal row; spines falcate, with large lateral flange(Figure 2F); upper and inner part of the flangethinner than lower and outer one, often brokenbasally in anterior old spines, thus the wholestructure appearing as a large tooth.

Hooded hooks in neuropodia from segment 7,up to 12 in a series, not accompanied by capillar-ies. Hooks bidentate, with shaft slightly curved,

Figure 2. Polydora uncinata (SMF 13492): (A) anterior end, dorsal view, left palp omitted; (B) posterior end, dorsal view; (C) pos-

terior segment with heavy recurved spine and enlarged notopodial postchaetal lamella, anterior view; (D) ventral capillary chaeta

of segment 5; (E) dorsal superior capillary chaeta of segment 5; (F) major falcate spine and pennoned companion chaeta of seg-

ment 5; (G) bidentate hooded hook from neuropodium of segment 7; (H) bidentate hooded hook from neuropodium of a posterior

segment.

Figure 3. Polydora uncinata. Relationships between the arrangement of branchia (in segment numbers, referring to the last branchi-

ate segment) and the total number of segments (filled circles), and the arrangement of heavy recurved spines in notopodia (in seg-

ment numbers, referring to the first spine-bearing segment) and the total number of segments (empty circles).

492

with weak constriction on shaft in anterior seg-ments (Figure 2G) and greater constriction inposterior segments (Figure 2H).

Branchiae from segment 7, full-sized from seg-ment 8–10, gradually diminishing in size alongposterior half of body and absent on 5–20 poste-riormost segments (Figure 3). Branchiae flat-tened, with surfaces oriented parallel to bodyaxis, free from notopodial postchaetal lamellae.Nototrochs from segment 7 in small individualsand from segment 8 onwards in large worms,consisting of one row of cilia.

Pygidium white, cup-shaped or disk-like withwide dorsal gap or narrow incision (Figure 2B).

Glandular pouches from segment 7, large untilsegment 12–14 and then gradually diminishing insize.

Gizzard-like structure absent in digestive tract.Hind gut white within 10–20 posteriormost seg-ments in large individuals.

Metanephridial segmental organs from seg-ment 7, opening to exterior laterally on anterior,sterile segments and dorsally on fertile segments;consegmental nephridia opening separatelythroughout.

Infestation characteristics

Prevalence of abalone infestation by worms var-ied substantially among cultivation tanks. In atank with small molluscs, 19–45 mm long(mean ¼ 34 ± 5 mm, n ¼ 124), only 12.1% of allabalone were infested, while in another tank,with larger molluscs, 33–70 mm long (mean ¼48 ± 6 mm, n ¼ 167), 98.8% abalone wereinfested by P. uncinata. Up to 42 worms werefound in one shell, and approximately 2 worms/cm were found on the shell surface. The wormsresided in U-shaped burrows within the shell andoften caused formation of dark brown muddy or

Figure 4. Polydora uncinata. (A) inner surface of abalone shell of a severely infested mollusc, showing blisters caused by worms;

(B) outer surface of abalone shell, showing silty tube extending worm burrow, and characteristic banded palps of a worm protrud-

ing out of the tube; (C–E) fragments of egg capsule strings showing developing larvae and nurse eggs. (C, D) egg capsules with

early stage of larval development, showing few small larvae and numerous nurse eggs; (E) egg capsules with late stage of larval

development, showing few large larvae which have already consumed most of the nurse eggs. Scale bars: (A) – 10 mm; (B) –

5 mm; (C), (E) – 200 lm; (D) – 100 lm.

493

nacreous blisters on the inner shell surface (Fig-ure 4A). Severely infested molluscs had up to50% of the inner shell surface covered by blisters.Worms were mainly aggregated in the apical partof shells, but blisters near the respiratory poresand on the leading edge were also frequent. Thewalls of the burrow were lined with detritus,forming inner detrital tube. The ends of eachburrow were opened to the outside and extendedby two smooth silty tubes, up to 4 mm long. Liveworms could be seen with their palps protrudingout of the tubes (Figure 4B).

ReproductionMature females, egg capsules with various stagesof larval development and recently settled juve-nile individuals were found in abalone shells dur-ing the whole period of study. Males were notrecognized. Females had oocytes in middle seg-ments, from segments 28–34 to 59–75. Egg cap-sules were joined to each other in a string(Figure 4C). Each capsule was attached by twothin stalks to the inner wall of the female burrowand contained up to 39 eggs (mean ¼ 25.2 ± 6.4,n ¼ 92). The total number of capsules producedby one female ranged from 24 to 55(mean ¼ 37.5 ± 8.9, n ¼ 23); the total number ofeggs deposited per brood ranged from 468 to1591 (n ¼ 18). The eggs were oval, 170–175 lmby 133–138 lm in diameter (n ¼ 20) (Figure 4D).Females brooding larvae in capsules had vitello-genic oocytes up to 80 lm in diameter developingin the ovaries.

Larval developmentOne to three eggs in each capsule usually devel-oped into larvae whereas others did not undergocleavage and were later consumed by developinglarvae (Figures 4C–E). Occasionally, all the eggswere nurse in a capsule. Larval development wasentirely lecithotrophic (exolecithotrophic) withlarvae staying inside egg capsules until about 17-segment stage and hatching shortly before meta-morphosis.

The 19–20-segment juveniles were found onshells near adults. They had small glandularpouches in segment 6 and larger pouches fromsegment 7 onwards. One pair of provisionalmajor modified spines, in addition to the typicaladult form of major spines, were present in noto-podia of segment 5.

Discussion

Worms found in abalone from land-based tanksin Coquimbo thoroughly correspond in morphol-ogy to the examined paratypes of P. uncinatafrom Japan. However, the description given inthe present study slightly differs from that pro-vided by Sato-Okoshi (1998) in terms of size ofworms, arrangement of branchiae and heavyrecurved spines in posterior notopodia. The spec-imens from Chile are larger than the specimensfrom Japan (32 mm vs 25 mm long) and at thesame time contain fewer segments (117 vs 160).Difference in length may, however, result frommeasuring procedure, when measurements weredone on live relaxed individuals in Chile and onfixed worms in Japan (material fixed in formalinand preserved in ethanol is usually reduced 10%–20% in length). Chilean specimens might havefewer number of segments because they wereyounger than Japanese ones. Sato-Okoshi (1998)reported that branchiae continue to the posteriorend of the body and co-occur with recurvedspines on posterior segments. No branchiae butslightly enlarged notopodial postchaetal lamellae(similar to the form of branchiae) were found onposterior segments both in Chilean worms andtype specimens from Japan. Thus, notopodialspines in the species start 1–17 segments posteriorto the last branchiate segment and very rarelyco-occur in the last branchiate segment. Remark-ably that females from both regions have similaroocytes of about 170 lm in diameter. Conse-quently, we consider Chilean and Japaneseworms to be conspecific.

Polydora uncinata was only recently describedfrom Japan, thus it is unknown whether thisregion is native for the species. Nevertheless, weassume that its presence in Chile resulted froman accidental transportation namely from Japan.It is not possible, however, to state the exact wayby which such a transportation might happen.Seawater for abalone tanks in Coquimbo is takendirectly from Herradura Bay where the Pacificoyster C. gigas is cultivated. The oysters wereimported from Japan to Chile in 1980s and havebeen successfully naturalized in the bay.Although sanitary certification for all kinds ofimported biological specimens has always beenrequired by the Subsecretarıa de Pesca, polydoridinfestation has never been mentioned among

494

oyster diseases to be certified. The so-called ‘po-lydoriasis’ was determined for the first time by aDecree which was called into operation in Chileonly in 1996 (Exempt Decree No 75/96 of Minis-terio de Economıa, Fomento y Reconstruccion).This Decree requires that only imported abalonemust be certified free of polydorid infestation(although it also requires that oysters and aba-lone should be certified free of ecto- and endo-parasites). Thus, oysters and the first importedabalone, which were transported to Chile beforethis Decree, might have been ‘legally’ infestedwith polychaetes.

Herradura Bay is frequently visited by trans-oceanic Japanese cargo vessels which present apotential vector for Polydora larvae transportedin ballast waters. However, considering shortpelagic life of P. uncinata larvae, this transportmethod appears unlikely. Two oysters from Her-radura Bay were examined but no P. uncinatawas found. Ultimately, accidental transportationwith abalone seems the most likely mechanismfor the infestation of abalone cultured in land-based tanks. Facts of transportation of spionidpolychaetes along with commercially cultivatedmolluscs mentioned in the ‘Introduction’ furthersupport this idea.

Easy transportation of spionid polychaetesalong with molluscs and shrimps for aquaculturehas been already discussed by Bailey-Brock(2000). Reasons underlying this ability include(1) small size of these polychaetes, thus evadingdetection and hitch-hiking in tubes attached tothe shell surface or in burrows perforated inshells, (2) high survivorship of pelagic larvae intransportation water and resistance of adults tostress conditions (most of the introduced spionidsare intertidal species), and (3) utilization of thesame food supplied for the cultivated organisms.

Accidental transportation of P. uncinata toChile is cause for concern. Intensive reproductionof the species in land-based tanks at Coquimboindicates that the living conditions are suitablefor it. Regardless of how the worm was trans-ported to Chile, its release to the natural ecosys-tem may have negative unforeseen impacts onthe native fauna. As such, further studies arerequired to examine cultivated oysters and nativemolluscs in order to determine the extent towhich P. uncinata is established within Chileancoastal waters.

Acknowledgements

Dr Wolfgang Stotz and Dr Carlos Bertran Vivesprovided general support and laboratory facilitiesfor this study. Dr Martin Thiel and Dr Jason D.Williams provided careful editorial assistance andvaluable comments on a draft of this manuscript.Three anonymous reviewers essentially editedand commented on the manuscript after submis-sion. To all these persons we express our sinceregratitude. Financial support was provided by theproject MECESUP AUS 0101 through the Insti-tuto de Zoologia, Universidad Austral de Chile,Valdivia for VIR in the year 2002; the projectFONDEF D99I1099 for CO in the year 2002;and the project 03-3-A-06-125 of the Far EasternBranch of the Russian Academy of Sciences forVIR in the year 2003.

References

Bailey-Brock JH (1987) Phylum Annelida. In: Devaney DM

and Eldredge LG (eds) Reef and shore fauna of Hawaii.

Bishop Museum Special Publication 64 (2 and 3), pp 213–

454. Bishop Museum Press, Honolulu

Bailey-Brock JH (1990) Polydora nuchalis (Polychaeta: Spioni-

dae), a new Hawaiian record from aquaculture ponds.

Pacific Science 44(1): 81–87

Bailey-Brock JH (2000) A new record of the polychaete Boc-

cardia proboscidea (family Spionidae), imported to Hawai’i

with oysters. Pacific Science 54(1): 27–30

Bailey-Brock JH and Ringwood A (1982) Methods for con-

trol of the mud blister worm, Polydora websteri, in Hawai-

ian oyster culture. Sea Grant Quarterly 4(3): 1–6

Basilio CD, Canete JI and Rozbaczylo N (1995) Polydora sp.

(Spionidae), un poliqueto perforador de las valvas del osti-

on Argopecten purpuratus (Bivalvia: Pectinidae) en Bahıa

Tongoy, Chile. Revista de Biologıa Marina, Valparaıso

30(1): 71–77

Blake JA (1983) Polychaetes of the family Spionidae from

South America, Antarctica, and adjacent seas and islands.

Biology of the Antarctic Seas XIV. Antarctic Research Ser-

ies 39(3): 205–288

Blake JA (1996) Family Spionidae Grube, 1850. Including a

review of the genera and species from California and a

revision of the genus Polydora Bosc, 1802. In: Blake JA,

Hilbig B and Scott PH (eds) Taxonomic Atlas of the Ben-

thic Fauna of the Santa Maria Basin and Western Santa

Barbara Channel. Volume 6. The Annelida Part 3 – Poly-

chaeta: Orbiniidae to Cossuridae, pp 81–223. Santa Bar-

bara Museum of Natural History, Santa Barbara, CA

Blake JA and Evans JW (1973) Polydora and related genera

as borers in mollusk shells and other calcareous substrates

(Polychaeta: Spionidae). Veliger 15(3): 235–249

495

Carlton JT (1975) Introduced intertidal invertebrates. In:

Smith RI and Carlton JT (eds) Light’s Manual: Intertidal

Invertebrates of the Central California Coast, pp 17–25.

University of California Press, Berkeley, CA

Carlton JT (1987) Patterns of transoceanic marine biological

invasions in the Pacific Ocean. Bulletin of Marine Science

41: 452–465

Carrasco FD (1974) Spionidae (Polychaeta) provenientes de

la Bahıa de Concepcion y lugares adyacentes. Boletın de la

Sociedad de Biologıa de Concepcion 48: 185–201

Cohen AN and Carlton JT (2001) Accelerating invasion rate

in a highly invaded estuary. Science 279: 555–558

DiSalvo LH and Martınez E (1985) Cultivo de Ostrea chilen-

sis Philippi 1845 en una bahıa de la costa norte-centro de

Chile. Biologıa Pesquera 14: 16–22

Galtsoff PS (1964) The American oyster Crassostrea virginica

Gmelin. Fishery Bulletin of the Fish and Wildlife Service

64: 1–480

Handley SJ (1995) Spionid polychaetes in Pacific oysters,

Crassostrea gigas (Thunberg) from Admiralty Bay, Marl-

borough Sounds, New Zealand. New Zealand Journal of

Marine and Freshwater Research 29(3): 305–309

Handley SJ (1998) Power to the oyster: Do spionid-induced

shell blisters affect condition in subtidal oysters? Journal of

Shellfish Research 17(4): 1093–1099

Handley SJ (2000) Larval development of Boccardia knoxi, a

shell-infesting spionid polychaete. New Zealand Journal of

Marine and Freshwater Research 34(4): 681–687

Handley SJ and Bergquist PR (1997) Spionid polychaete

infestations of intertidal Pacific oysters Crassostrea gigas

(Thunberg), Mahurangi harbour, northern New Zealand.

Aquaculture 153(3–4): 191–205

Hartmann-Schroder G (1962) Zur Kenntnis des Eulitorals der

chilenischen Pazifikkuste und der argentinischen Kuste

Sudpatagoniens unter besonderer Berucksichtigung der

Polychaeten und Ostracoden. Teil II. Die Polychaeten des

Eulitorals. Mitteilungen aus dem hamburgischen zoologis-

chen Museum und Institut 60 (Erg.Bd): 57–167

Haswell WA (1885) On a destructive parasite of the rock oys-

ter. Proceedings of the Linnean Society of New South

Wales 10: 273–275

Hewatt WG and Andrews JD (1954) Oyster mortality studies

in Virginia. Mortalities of oysters in trays at Gloucester

Point, York River. Texas Journal of Sciences 6: 121–133

Kent RML (1979) The influence of heavy infestations of Poly-

dora ciliata on the flesh content of Mytilus edulis. Journal

of the Marine Biological Association of the United King-

dom 59(2): 289–298

Lauckner G (1980) Diseases of Mollusca: Gastropoda. In:

Kinne O (ed) Diseases of Marine Animals. Vol. I, pp 311–

424. Wiley, Chichester, UK

Lauckner G (1983) Diseases of Mollusca: Bivalvia. In: Kinne

O (ed) Diseases of Marine Animals. Vol. II, pp 477–961.

Biologische Anstalt Helgoland, Hamburg, Germany

Lleonart M, Handlinger J and Powell M (2003a) Treatment

of spionid mud worm (Boccardia knoxi Rainer) infestation

of cultured abalone. Aquaculture 217(1–4): 1–10

Lleonart M, Handlinger J and Powell M (2003b) Spionid

mud worm infestation of farmed abalone (Haliotis spp.).

Aquaculture 221(1–4): 85–96

Loosanoff VL and Engle JB (1943) Polydora in oysters sus-

pended in the water. Biological Bulletin of the marine bio-

logical Laboratory Woods Hole 85(1): 69–78

Lunz GR Jr. (1941) Polydora, a pest in South Carolina oys-

ters. Journal of the Elisha Mitchell Scientific Society 57(2):

273–283

Mohammad M-BM (1972) Infestation of the pearl oyster

Pinctada margaritifera (Linne) by a new species of Polydo-

ra in Kuwait, Arabian Gulf. Hydrobiologia 39(4): 463–477

Naylor RL, Williams SL and Strong DR (2001) Aquaculture

– a gateway for exotic species. Science 294: 1655–1656

Owen HM (1957) Etiological studies on oyster mortality. II.

Polydora websteri Hartman (Polychaeta: Spionidae). Bulle-

tin of Marine Science of the Gulf and Caribbean 7(1): 35–

46

Radashevsky VI and Cardenas CA (2004) Morphology and

biology of Polydora rickettsi (Polychaeta: Spionidae) from

Chile. New Zealand Journal of Marine and Freshwater

Research 38(2): 243–254

Rozbaczylo N (1985) Los Anelidos Poliquetos de Chile. In-

dice Sinonımico y distribucion geografica de especies. Mo-

nografıas Biologicas 3: 1–284

Rozbaczylo N, Schmiede P and Sanchez M (1980) Polydora

sp. (Polychaeta, Spionidae) a parasite of the clam Meso-

desma donacium (Mollusca, Mesodesmatidae). Archivos de

Biologıa y Medicina Experimentales 13(1): 105–105

Sato-Okoshi W (1998) Three new species of polydorids (Poly-

chaeta, Spionidae) from Japan. Species Diversity 3: 277–

288

Sato-Okoshi W (1999) Polydorid species (Polychaeta: Spioni-

dae) in Japan, with descriptions of morphology, ecology

and burrow structure. 1. Boring species. Journal of the

Marine Biological Association of the United Kingdom 79:

831–848

Sato-Okoshi W and Takatsuka M (2001) Polydora and

related genera (Polychaeta, Spionidae) around Puerto

Montt and Chiloe Island (Chile), with description of a new

species of Dipolydora. Bulletin of Marine Science 68(3):

485–503

Skeel ME (1979) Shell-boring worms (Spionidae: Polychaeta)

infecting cultivated bivalve molluscs in Australia. Proceed-

ings of the World Mariculture Society 10: 529–533

Wargo RN and Ford SE (1993) The effect of shell infestation

by Polydora sp. and infection by Haplosporidium nelsoni

(MSX) on the tissue condition of oysters, Crassostrea virgi-

nica. Estuaries 16(2): 229–234

Whitlegge T (1890) Report on the worm disease affecting the

oysters on the coast of New South Wales. Memoirs of the

Australian Museum, Sydney 1: 41–53

Williams JD (2001) Polydora and related genera associated

with hermit crabs from the Indo-West Pacific (Polydora:

Spionidae), with descriptions of two new species and a sec-

ond polydorid egg predator of hermit crabs. Pacific Science

55(4): 429–565

496