Polydora uncinata (Polychaeta: Spionidae) in Chile: an accidental transportation across the Pacific

Springer 2005

Biological Invasions (2005) 7: 489–496

Polydora uncinata (Polychaeta: Spionidae) in Chile: an accidental transportation across the Pacific Vasily I. Radashevsky1 & Carolina Olivares2,* 1

Institute of Marine Biology, Russian Academy of Sciences, Vladivostok 690041, Russia; 2Departamento de Biologı´a Marina, Universidad Cato´lica del Norte, Casilla 117, Coquimbo, Chile; *Author for correspondence (e-mail: [email protected])

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 landbased tanks in Coquimbo, Chile. Spionid polychaetes of Polydora and related genera have been reported from Chile but no worms similar to those found in abalone have been described. The abalone pest corresponds in morphology to Polydora uncinata Sato-Okoshi, 1998, a shell-boring species which was originally described from Japan and never reported from outside the country. It is suggested that occurrence of the species in Chile resulted from its accidental transportation from Japan. Adult worms were most likely transported to Coquimbo with imported abalone brood stock. Prevalence of abalone infestation by 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 which covered up to 50% of the inner shell surface. Egg capsules with developing larvae were present in female burrows. 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. Polydora uncinata is redescribed based on individuals from Coquimbo to alert zoologists in case of accidental release of worms into Chilean coastal waters. Regardless of how the species was transported to Chile, its release to the natural ecosystem may have negative unforeseen impacts on the native fauna.

Introduction Since 1987, 11 shipments of adult abalone Haliotis discus hannai Ino, 1953 have been transported to aquaculture facilities in Coquimbo, Chile, from four provinces on the Pacific side of Honshu 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 de Economı´ a, Fomento y Reconstruccio´n). Imported abalone were maintained in a land-based system in Coquimbo and used as brood stock to provide offspring to other land-based centers in the country. Progeny of these abalone were also

used in a pilot experiment aimed at introduction of the molluscs into coastal waters for further commercial cultivation (Resolution No. 220/02 of Ministerio de Economı´ a, Fomento y Reconstruccio´n). Abalone from tanks in Coquimbo were studied by the authors and numerous individuals of a polydorid polychaete were found boring in abalone shells. These worms differed substantially from polydorids so far reported from Chile (Hartmann-Schro¨der 1962; Carrasco 1974; Rozbaczylo et al. 1980; Blake 1983; DiSalvo and Martı´ nez 1985; Rozbaczylo 1985; Basilio et al. 1995; Sato-Okoshi and Takatsuka 2001; Radashevsky and Ca´rdenas 2004) and were identified

490 as Polydora uncinata Sato-Okoshi, 1998. This Polydora species was originally described from the Pacific coast of Honshu Island as a borer of shells of both wild Omphalius rusticus (Gmelin, 1791) and cultivated Pacific oyster Crassostrea gigas (Thunberg, 1793), and has not been reported from outside of Japan (Sato-Okoshi 1998). Commercial oyster industry and aquaculture in general is one of the means by which cultivated and associated species can be dispersed outward from their native regions through human’s activity (Carlton 1975, 1987; Cohen and Carlton 2001; Naylor et al. 2001). Lists of species introduced by these means usually include polychaetes, and spionids are always among them. It is likely that four tube-dwelling spionid species have been introduced to California in entrapped sediment that accompanied adult and seed oysters: Polydora cornuta Bosc, 1802 and Streblospio benedicti Webster, 1879 in association with the American oyster, Crassostrea virginica (Gmelin), transplanted from the Atlantic coast of North America, plus Pseudopolydora kempi (Southern, 1921) and Pseudopolydora paucibranchiata (Okuda, 1937) along with the Pacific oyster, C. gigas, transplanted from Japan (Carlton 1975). A boring spionid Polydora websteri Hartman in Loosanoff and Engle, 1943 was introduced to the Hawaiian Islands along with spat and young oysters purchased from hatcheries on the east and west coasts of North America (Bailey-Brock and Ringwood 1982; Bailey-Brock 1987). Tube-dwelling Polydora nuchalis Woodwick, 1953 was probably introduced to the Hawaiian Islands with shipments of shrimp from western Mexico to stock ponds at one of the aquaculture farms (Bailey-Brock 1990). Boccardia proboscidea Hartman, 1940 was introduced to an oyster culture farm in the Hawaiian Islands with shipments of Ostrea edulis Linnaeus, 1758 from Maine (Bailey-Brock 2000). Three boring spionids, Polydora websteri, Polydora hoplura Clapare`de, 1869 and Boccardia chilensis Blake and Woodwick, 1971 infesting commercial bivalves were possibly introduced to New Zealand (Handley 2000). Similarly, Boccardia berkeleyorum Blake and Woodwick, 1971 known from California and Vancouver Island was recently reported from gastropod shells in the Philippines, likely representing an accidental introduction to the Indo-West Pacific (Williams 2001).

Boring polydorids, also called blisterworms or mudworms are known pests which can cause serious damage to molluscs, both cultivated and living in natural ecosystems (Haswell 1885; Whitlegge 1890; Lunz 1941; Loosanoff and Engle 1943; Hewatt and Andrews 1954; Owen 1957; Galtsoff 1964; Mohammad 1972; Blake and Evans 1973; Kent 1979; Skeel 1979; Lauckner 1980, 1983; Wargo and Ford 1993; Handley 1995, 1998; Blake 1996; Handley and Bergquist 1997; Lleonart et al. 2003a, b). Many of them can rapidly become established and reach epidemic proportion in aquaculture facilities. For example, an infestation of P. websteri in cultured oysters contributed to the collapse of a highly intensive aquaculture industry at Kahuku, Hawaiian Islands (Bailey-Brock and Ringwood 1982; Bailey-Brock 1987). Cumulative mortality levels of 50% or more associated with two spionid mudworms, Boccardia knoxi (Rainer, 1973) and P. hoplura, were reported by various seabased abalone culture facilities within Tasmania during the mid-1990s (Lleonart et al. 2003a, b). The purpose of the present study is to describe the Polydora worms from abalone shells in Coquimbo, compare them with type material of P. uncinata from Japan, report an accidental transportation of P. uncinata to Chile, and alert zoologists to the potential for accidental release of worms into Chilean coastal ecosystems.

Materials and methods Live abalone were collected from land-based cultivation tanks in Coquimbo (2959¢ S, 7122¢ W), Chile monthly from November 2002 through April 2003. Blister coverage was estimated visually. Abalone shells were broken into small fragments with pliers and polychaetes were removed under a stereomicroscope in the laboratory. The worms were relaxed in isotonic magnesium chloride, measured and examined alive with light microscopes. Drawings were made using a camera lucida and images were taken using a digital camera. After examination, a part of adult worms was fixed in 10% formalin solution, rinsed in freshwater and transferred to 70% ethanol. Fixed material was deposited at the Museo Nacional de Historia Natural, Santiago de Chile (MNHN An 2010-2012, 3 specimens) and

491 Senckenberg Museum, Frankfurt am Main, Germany (SMF 13492, 18 specimens). Type material of P. uncinata deposited in the Natural History Museum and Institute, Chiba, Japan (NHMIC CBM-ZW 902, 3 paratypes) was also examined.

Results Systematic account Spionidae Grube, 1850 Polydora Bosc, 1802 Polydora uncinata Sato-Okoshi, 1998 (Figures 1–4) 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 wide on segment 7 for 117 segments. Body pale in life; fixed specimens usually with secretory cells visible as small dark spots scattered on dorsal side of posterior segments. Fine continuous black line usually present on palps along edges of ciliated food groove in small individuals; up to 12 pairs of black bars present on each palp in large individuals; bars arranged regularly on distal 1/2–2/3

of palp (Figure 2A); occasionally, pigmentation on palps absent. Prostomium weakly incised anteriorly, thus incision occasionally seen only in ventral view. Caruncle extending posteriorly until end of segment 2 or middle of segment 3. Short nuchal antenna present on caruncle. Four eyes usually present, including one pair of anterior and one pair of posterior eyes; occasionally eyes absent. Palps extending posteriorly for 10–20 segments; with longitudinal food groove lined with fine frontal cilia; latero-frontal motile compound cilia (cirri) and short papillae with non-motile cirri bordering food groove; papillae with non-motile cirri also scattered on lateral and abfrontal palp surfaces. Segment 1 with small postchaetal lamellae in both rami; notochaetae absent; short capillaries present in neuropodia. Single (occasionally two) recurved heavy spines and 2–6 slender capillaries present in notopodia of posterior postbranchiate segments (Figures 2B and 2C). Spines first appearing in juveniles on segment 18, synchronously with formation of segment, and developing on all following segments; spines lost from anterior notopodia as growth proceeding and starting from more posterior segments in bigger worms (Figure 3). In adults spines usually starting 1–3 (occasionally 4–17) segments after posterior

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

492

Figure 2. Polydora uncinata (SMF 13492): (A) anterior end, dorsal view, left palp omitted; (B) posterior end, dorsal view; (C) posterior 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 segment 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 branchiate segment) and the total number of segments (filled circles), and the arrangement of heavy recurved spines in notopodia (in segment numbers, referring to the first spine-bearing segment) and the total number of segments (empty circles).

branchiate segment; in one individual, spines started on last branchiate segment. Notopodial postchaetal lamellae reduced on branchiate segments but slightly enlarged on posterior, abranchiate segments, thus appearing like branchiae (Figures 2B and 2C). In largest individual with 117 segments, branchiae terminating on segment 102 and recurved spines starting on segment 104. Segment 5 greatly modified, almost twice as large as segments 4 or 6, without postchaetal lamellae, with 3–6 dorsal superior winged capillaries (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 shorter and fewer than those on adjacent segments. Major spines arranged in a slightly curved diagonal row; spines falcate, with large lateral flange (Figure 2F); upper and inner part of the flange thinner than lower and outer one, often broken basally in anterior old spines, thus the whole structure appearing as a large tooth. Hooded hooks in neuropodia from segment 7, up to 12 in a series, not accompanied by capillaries. Hooks bidentate, with shaft slightly curved,

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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 protruding 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.

with weak constriction on shaft in anterior segments (Figure 2G) and greater constriction in posterior segments (Figure 2H). Branchiae from segment 7, full-sized from segment 8–10, gradually diminishing in size along posterior half of body and absent on 5–20 posteriormost segments (Figure 3). Branchiae flattened, with surfaces oriented parallel to body axis, free from notopodial postchaetal lamellae. Nototrochs from segment 7 in small individuals and from segment 8 onwards in large worms, consisting of one row of cilia. Pygidium white, cup-shaped or disk-like with wide dorsal gap or narrow incision (Figure 2B). Glandular pouches from segment 7, large until segment 12–14 and then gradually diminishing in size. Gizzard-like structure absent in digestive tract. Hind gut white within 10–20 posteriormost segments in large individuals.

Metanephridial segmental organs from segment 7, opening to exterior laterally on anterior, sterile segments and dorsally on fertile segments; consegmental nephridia opening separately throughout. Infestation characteristics Prevalence of abalone infestation by worms varied substantially among cultivation tanks. In a tank with small molluscs, 19–45 mm long (mean ¼ 34 ± 5 mm, n ¼ 124), only 12.1% of all abalone were infested, while in another tank, with larger molluscs, 33–70 mm long (mean ¼ 48 ± 6 mm, n ¼ 167), 98.8% abalone were infested by P. uncinata. Up to 42 worms were found in one shell, and approximately 2 worms/ cm were found on the shell surface. The worms resided in U-shaped burrows within the shell and often caused formation of dark brown muddy or

494 nacreous blisters on the inner shell surface (Figure 4A). Severely infested molluscs had up to 50% of the inner shell surface covered by blisters. Worms were mainly aggregated in the apical part of shells, but blisters near the respiratory pores and on the leading edge were also frequent. The walls of the burrow were lined with detritus, forming inner detrital tube. The ends of each burrow were opened to the outside and extended by two smooth silty tubes, up to 4 mm long. Live worms could be seen with their palps protruding out of the tubes (Figure 4B). Reproduction Mature females, egg capsules with various stages of larval development and recently settled juvenile individuals were found in abalone shells during the whole period of study. Males were not recognized. Females had oocytes in middle segments, from segments 28–34 to 59–75. Egg capsules were joined to each other in a string (Figure 4C). Each capsule was attached by two thin stalks to the inner wall of the female burrow and contained up to 39 eggs (mean ¼ 25.2 ± 6.4, n ¼ 92). The total number of capsules produced by one female ranged from 24 to 55 (mean ¼ 37.5 ± 8.9, n ¼ 23); the total number of eggs deposited per brood ranged from 468 to 1591 (n ¼ 18). The eggs were oval, 170–175 lm by 133–138 lm in diameter (n ¼ 20) (Figure 4D). Females brooding larvae in capsules had vitellogenic oocytes up to 80 lm in diameter developing in the ovaries. Larval development One to three eggs in each capsule usually developed into larvae whereas others did not undergo cleavage and were later consumed by developing larvae (Figures 4C–E). Occasionally, all the eggs were nurse in a capsule. Larval development was entirely lecithotrophic (exolecithotrophic) with larvae staying inside egg capsules until about 17segment stage and hatching shortly before metamorphosis. The 19–20-segment juveniles were found on shells near adults. They had small glandular pouches in segment 6 and larger pouches from segment 7 onwards. One pair of provisional major modified spines, in addition to the typical adult form of major spines, were present in notopodia of segment 5.

Discussion Worms found in abalone from land-based tanks in Coquimbo thoroughly correspond in morphology to the examined paratypes of P. uncinata from Japan. However, the description given in the present study slightly differs from that provided by Sato-Okoshi (1998) in terms of size of worms, arrangement of branchiae and heavy recurved spines in posterior notopodia. The specimens from Chile are larger than the specimens from Japan (32 mm vs 25 mm long) and at the same time contain fewer segments (117 vs 160). Difference in length may, however, result from measuring procedure, when measurements were done on live relaxed individuals in Chile and on fixed worms in Japan (material fixed in formalin and preserved in ethanol is usually reduced 10%– 20% in length). Chilean specimens might have fewer number of segments because they were younger than Japanese ones. Sato-Okoshi (1998) reported that branchiae continue to the posterior end of the body and co-occur with recurved spines on posterior segments. No branchiae but slightly enlarged notopodial postchaetal lamellae (similar to the form of branchiae) were found on posterior segments both in Chilean worms and type specimens from Japan. Thus, notopodial spines in the species start 1–17 segments posterior to the last branchiate segment and very rarely co-occur in the last branchiate segment. Remarkably that females from both regions have similar oocytes of about 170 lm in diameter. Consequently, we consider Chilean and Japanese worms to be conspecific. Polydora uncinata was only recently described from Japan, thus it is unknown whether this region is native for the species. Nevertheless, we assume that its presence in Chile resulted from an accidental transportation namely from Japan. It is not possible, however, to state the exact way by which such a transportation might happen. Seawater for abalone tanks in Coquimbo is taken directly from Herradura Bay where the Pacific oyster C. gigas is cultivated. The oysters were imported from Japan to Chile in 1980s and have been successfully naturalized in the bay. Although sanitary certification for all kinds of imported biological specimens has always been required by the Subsecretarı´ a de Pesca, polydorid infestation has never been mentioned among

495 oyster diseases to be certified. The so-called ‘polydoriasis’ was determined for the first time by a Decree which was called into operation in Chile only in 1996 (Exempt Decree No 75/96 of Ministerio de Economı´ a, Fomento y Reconstruccio´n). This Decree requires that only imported abalone must be certified free of polydorid infestation (although it also requires that oysters and abalone should be certified free of ecto- and endoparasites). Thus, oysters and the first imported abalone, which were transported to Chile before this Decree, might have been ‘legally’ infested with polychaetes. Herradura Bay is frequently visited by transoceanic Japanese cargo vessels which present a potential vector for Polydora larvae transported in ballast waters. However, considering short pelagic life of P. uncinata larvae, this transport method appears unlikely. Two oysters from Herradura Bay were examined but no P. uncinata was found. Ultimately, accidental transportation with abalone seems the most likely mechanism for the infestation of abalone cultured in landbased tanks. Facts of transportation of spionid polychaetes along with commercially cultivated molluscs mentioned in the ‘Introduction’ further support this idea. Easy transportation of spionid polychaetes along with molluscs and shrimps for aquaculture has been already discussed by Bailey-Brock (2000). Reasons underlying this ability include (1) small size of these polychaetes, thus evading detection and hitch-hiking in tubes attached to the shell surface or in burrows perforated in shells, (2) high survivorship of pelagic larvae in transportation water and resistance of adults to stress conditions (most of the introduced spionids are intertidal species), and (3) utilization of the same food supplied for the cultivated organisms. Accidental transportation of P. uncinata to Chile is cause for concern. Intensive reproduction of the species in land-based tanks at Coquimbo indicates that the living conditions are suitable for it. Regardless of how the worm was transported to Chile, its release to the natural ecosystem may have negative unforeseen impacts on the native fauna. As such, further studies are required to examine cultivated oysters and native molluscs in order to determine the extent to which P. uncinata is established within Chilean coastal waters.

Acknowledgements Dr Wolfgang Stotz and Dr Carlos Bertra´n Vives provided general support and laboratory facilities for this study. Dr Martin Thiel and Dr Jason D. Williams provided careful editorial assistance and valuable comments on a draft of this manuscript. Three anonymous reviewers essentially edited and commented on the manuscript after submission. To all these persons we express our sincere gratitude. Financial support was provided by the project MECESUP AUS 0101 through the Instituto de Zoologia, Universidad Austral de Chile, Valdivia for VIR in the year 2002; the project FONDEF D99I1099 for CO in the year 2002; and the project 03-3-A-06-125 of the Far Eastern Branch of the Russian Academy of Sciences for VIR in the year 2003.

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