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Hydroides dianthus (Polychaeta: Serpulidae), an alien species introduced into Tokyo Bay, Japan Heike Link*†‡, Ejiroh Nishi∫¤ Katsuhiko Tanaka§, Rolando Bastida-Zavala¶, Elena K. Kupriyanova◊ and Takehisa Yamakita† *Leibniz Institute of Marine Sciences, Duesternbrooker Weg 20, 24105 Kiel, Germany. †Biodiversity and Evolutionary Biology Division, Gaduate School of Science, Chiba University, 1-33 Yayoi, Inage, Chiba 263-8522, Japan. ‡Present address: Institute des Sciences de la Mer, University of Quebec at Rimouski, 310 allée des Ursulines, Rimouski, Quebec G5L 3A1, Canada. ∫Manazuru Marine Laboratory for Science Education,Yokohama National University, Iwa, Manazuru, Kanagawa 259-0202, Japan. §IORGC Institute of Observational Research for Global Change, JAMSTEC Yokosuka Headquarters, 2–15 Natsushima-cho, Yokosuka-city, Kanagawa, 237-0061, Japan. ¶Laboratorio de Sistemática de Invertebrados Marinos, Universidad del Mar, campus Puerto Ángel, Ciudad Universitaria, Apdo. Postal 47, Puerto Ángel, Oaxaca, 70902, México. ◊Faculty of Education and Human Sciences, Yokohama National University, Tokiwadai, Hodogaya, Yokohama 240-8501, Japan. ¤ Corresponding author, e-mail:
[email protected]
Calcareous tube polychaetes (Family Serpulidae) are notorious biofoulers that are easily transported and introduced to allochtonous habitats. Here we report the recent introduction of Hydroides dianthus (Verrill, 1873) to eastern Japan as its first occurrence in east Asia, probably from European or American coasts. Specimens had been found on artificial hard substrata together with congeners H. ezoensis, H. exaltatus and H. fusicolus in Tokyo Bay, Japan in 2006. The origin, vector, source of introduction and possible impact of H. dianthus on Japanese coasts is discussed from a perspective based on worldwide Hydroides transport. Keywords: Tokyo Bay; alien species; invader organisms; Hydroides dianthus; biofouling
INTRODUCTION Calcareous tube worms (Family Serpulidae) are taxonomically and biologically relatively well studied, especially as compared to other families of Polychaeta. Among the many alien species reported world-wide, 18 serpulid species (excluding spirorbins) were reported as invasive or cryptogenic (Nishi & Kato, 2004). Comprising world-wide 89 described species (see ten Hove & Kupriyanova, 2009 for a review) and particularly speciose in the tropics, the largest serpulid genus Hydroides has 16 species recorded from temperate Japan: H. fusicola Mörch, 1863, H. diramphus Mörch, 1863, H. albiceps (Grube, 1870), H. minax (Grube, 1878), H. elegans (Haswell, 1883), H. exaltatus (Marenzeller, 1884), H. multispinosus Marenzeller, 1884, H. novaepommeraniae Augener, 1925, H. ezoensis Okuda, 1934, H. brachyacanthus Rioja, 1941, H. tambalagamensis Pillai, 1961, H. externispina Straughan, 1967, H. fuscus Imajima, 1976a, H. tuberculatus Imajima, 1976a, H. longispinosus Imajima 1976b, H. bisectus Imajima & ten Hove, 1989 (Imajima, 1996). Most species of this list were originally described from the Indian Ocean and Western Pacific; however, H. brachyacanthus is either an alien species (Zibrowius, 1971) or a member of a complex of species (Bastida-Zavala & ten Hove 2003b). Also at least two species, H. diramphus and H. elegans are considered cryptogenic sensu Carlton (1996), that is, are neither clearly native nor introduced. These two species of uncertain origin have been well known as fouling organisms on ship hulls world-wide since the late 19th Century (Zibrowius, 1971). More recently, H. ezoensis was transported to Europe, likely associated with oysters (Zibrowius, 1978, Thorp et al., 1987, Breton & Vincent, 1999) and introduced by shiptransport to Australia, where it became well-established (Hayes & Sliwa, 2003). Although H. ezoensis was originally described by Okuda (1934) from Hokkaido (formerly Ezo), Japan, some specimens of this species were studied by Fauvel in 1927 at Seto, Wakayama, near Osaka, and deposited in Seto Marine Biological Laboratory, Kyoto University (Iwasaki et al., 2004; Nishi & Tanaka, 2008). Being quite common in Japan and east Asia, H. ezoensis, is, however, found predominantly as fouling organisms on mariculture as well as ships and piers in harbours and ports, which is characteristic for invasive species. Consequently, Nishi & Tanaka (2008) tentatively considered it a cryptogenic species whose occurrence in natural habitats outside harbours and ports needs to be confirmed. Many Japanese and Asian species are found to have been introduced into European waters, often developing into harmful pests (e.g. Eno et al., 1997). Japanese coasts also sometimes receive invasive species from Europe and America (Iwasaki et al., 2004, Nabeshima, 2007). Here we report a characteristic example of another common Hydroides species recently introduced into Tokyo Bay, central Japan, imported from either temperate European or American waters.
MATERIALS AND METHODS Polyvynilchloride (PVC) panels (15 cm×15 cm) were immersed at 80 cm depth in Shinhama Lagoon, inner part of Tokyo Bay (35°66.519'N 139°91.764'E), from May until November, 2006. The
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lagoon is a 83 ha wetland park connected to Ichikawa Port by one open and one underground channel. In summer, salinity ranges from 20 to 24‰ (Tanaka et al. 2005) and the water temperature can exceed 25°C.The average water depth here is less than 3 m, and the sea floor consists of sandy silt with clay. Hard substrata found in the muddy tidal flat are oyster reefs and the concrete wall, which surrounds about two thirds of the lagoon. Material was sorted under the stereomicroscope and polychaete species were identified and counted. Although more serpulid species were found (Link, 2007), we only studied the relatively newly recorded H. dianthus in detail. Specimens were fixed using 4% neutralized formaldehyde and preserved in 70% ethanol. An anterior part of one specimen was observed with a JEOL scanning electron microscope. Five specimens were stored in the Universidad del Mar Polychaete Reference Collection (UMAR Poly, Oaxaca, México), and nine more specimens were deposited in Natural History Museum and Institute of Chiba, Japan (CBM), Coastal Branch of Natural History Museum and Institute, Chiba, Katsuura, Chiba, Japan (CMNH), The South Australian Museum, Adelaide, Australia (SAM), The National Museum of Natural History, Smithsonian Institution, Washington DC, USA (USNM), The Senckenberg Museum, Frankfurt, Germany (SMF), The Zoological Museum, University of Copenhagen, Copenhagen, Denmark (ZMUC) and the Natural History Museum, London (NHM). In the diagnosis the notation between parentheses corresponds to the minimum measurement in ‘juveniles’, following Bastida-Zavala & ten Hove (2003a).
RESULTS Genus Hydroides Gunnerus, 1768 Hydroides dianthus (Verrill, 1873). (Figure 1A–G) Material examined Twelve adult and one juvenile specimens. CBM-ZW-1010 (2 specimens), CMNH-ZW-1696 (1 specimen), NHM-ANEA 2009.1 (1 specimen), USNM 1122383 (1 specimen), SAMA-E3716 (1 specimen), UMAR Poly-107 (5 specimens), SMF 17915 (1 specimen), ZMUC-POL-2010 (1 specimen). Ichikawa area, Tokyo Bay, 22 August 2006, collected by H. Link, from PVC panels in 80 cm depth. Specimens with gametes have not been found. Description Tube white, internal diameter 1.3 mm (N=10, r: 0.1–1.3, µ=0.8 ±0.4), external diameter 1.5 mm (N=10, r: 0.1–1.5, µ=1.0 ±0.4); one tube covered by epibionts, all tubes have transversal ridges and lack peristomes; one specimen shows three longitudinal ridges and three none. Body colourless in preserved specimens; total length 10.7 mm (N=11, r: (3.0)4.6–15.7, µ=11.3 ±3.1). Branchial crown with 12 radioles (N=10, r: (8)9.0–20.0, µ=11.6 ±3.0) on each lobe. Peduncle length 3.2 mm (N=8, r: 2.1–3.6, µ=3.0 ±0.4), all specimens show insertion of the peduncle left; constriction ill-defined or lacking (Figure 1G). Pseudoperculum present in all specimens. Operculum length 0.7 mm (N=11, r: (0.2)0.5–1.0, µ=0.8 ±0.2), diameter 0.7 mm (N=5, r: 0.5–0.8, µ=0.7 ±0.1). Funnel with 26 radii (N=11, r: (10)17–33, µ=25.8 ±4.7) with pointed tip (Figure 1A–B, G). Inter-radial grooves ½ of funnel length in all opercula.Verticil with nine yellowish spines (N=11, r:8–10, µ=9.4 ±0.7), all curving more or less in ventral direction (Figures 1A–B, G). Dorsal spines larger than ventral ones, in ‘juvenile’ specimens the dorsal verticil spines are less developed. Tip of spines pointed. Spines with one basal internal spinule, one specimen lack internal spinule; without external and lateral spinules and/or wings.Verticil without central tooth. Collar chaetae bayonet type, with two blunt-rounded teeth, distal blade smooth (Figures 1C–D). Length of thorax 2.5 mm (N=11, r: (0.7)1.0–3.4, µ=2.3 ±0.7), width 1.0 mm (N=11, r: (0.3)0.6–1.0, µ=0.8 ±0.1). Thoracic membranes forming well developed ventral apron. Six chaetigers with hooded (limbate) chaetae of two sizes, saw-shaped uncini with 7 teeth (Figure 1E). Abdomen with 45 (N=10, r: (30)35–48, µ=40.9 ±4.7) chaetigers. JMBA2 - Biodiversity Records Published on-line
Figure 1. (A, B) scanning electron micrographs of Hydroides dianthus operculum; a characteristic basal funnel is crowned with a verticil made of chitinous spines without external spinules; (C) operculum of H. sanctaecrusis; the verticil bears typical external spinules, sp; (D, E) H. dianthus, SEM of collar chaetae;. (F) H. dianthus, anterior abdominal uncini; (G) H. dianthus, thoracic uncini from 4th chaetiger. Scale bars: A, B, 200 μm; D, 20 μm; E, 50 μm; F, G, 10 μm.
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Figure 2. Updated distribution of Hydroides dianthus and H. sanctaecrucis according to Zibrowius (1971), Bastida-Zavala & ten Hove (2003a,b) and Lewis et al. (2006). Question mark on the map indicates the records that have not been confirmed.
Anterior and middle abdominal chaetigers with flat-trumpet chaetae. Posterior chaetigers with ‘capillary’ chaetae. Anterior uncini saw-shaped, with eight teeth (Figure 1F). Habitat The species is found in fouling communities on buoys and piers in embayments, and particularly on artificial substrates such as concrete walls, ropes and PVC plates.The serpulid fouling community at the collection site consisted of 4 species of Hydroides: H. ezoensis, H. fusicola, H. exaltatus and H. dianthus, with addition of some Polydorid species. Distribution: Amphi-Atlantic. East coast of United States, New Jersey to Massachusetts, Gulf of Mexico, Atlantic coasts of France and Spain, Mediterranean Sea,West Africa (Senegal), Japan (Figure 2).
DISCUSSION The morphological characters of the specimens described here fit well the description of BastidaZavala & ten Hove (2003a), although the specimens found in Japan are relatively small compared to those recorded from the western Atlantic. However, the important diagnostic characters, such as the number of opercular radii or spines, fit in the short range (radii: 24–37, spines: 8–13) recorded from the western Atlantic. Hydroides dianthus was originally described (as Serpula dianthus) by Verill (1878) from the coast of New England. It appears to be native at the east coast of North America where it is widely distributed in a variety of ‘natural’ habitats including open coasts as well as in partly brackish waters of bays, lagoons, and ports. In Europe and western Africa, however, its distribution is disjoint, it occurs only in ports and lagoons, leaving out ‘natural’ habitats of full marine salinity, except in areas immediately adjacent to harbours (Zibrowius, 1971; Bastida-Zavala & ten Hove, 2003a). Specimens of Hydroides dianthus have been abundant (along with H. diramphus and H. elegans) as fouling organisms at Naples harbours as early as 1888. But the occurrence of H. dianthus can be traced back to an even earlier date at Izmir (year of publication 1865) and at Trieste (year of collecting 1874) (Zibrowius, 1971, 1973, 1978). Possibly the arrival of H. dianthus via ship hull fouling in the Mediterranean considerably antedates their first records. The species was discovered at Humble Spit in Southampton Water, England, in 1970 (Zibrowius, 1978) but has apparently not spread further (Zibrowius, 1992). It has also been recorded from the Atlantic coast of France and Spain (Zibrowius, 1983, 1991, 1994, Zibrowius & Thorp, 1989). This study is the first well documented record of H. dianthus for Japan and the Asian region in general, although its occurrence has independently been mentioned at a local conference (Otani & Yamanishi, 2007). This was based on the material collected in Osaka by Otani and referred to by Nabeshima (2007). We revised the material and the identification was confirmed by R.B.-Z. Whereas the record from the Osaka Bay is the first for Japan, our record from Tokyo Bay is a range extension to the eastern part of Honshu, central Japan. Serpulid polychaetes, especially of the genus Hydroides, are important fouling organisms on ships and in mariculture and therefore, their taxonomy and biology have been well studied in Japan (e.g. Kajihara, 1964, Imajima, 1976, 1996). Morphologically, H. dianthus is hard to confuse with local JMBA2 - Biodiversity Records Published on-line
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congeners, thus, the lack of previous records of this species in Japan most likely is not a result of misidentification, but rather is an indication of its recent introduction. Hydroides dianthus has been partly confused with and sometimes misidentified as a morphologically similar congener H. sanctaecrucis Krøyer [in] Mörch, 1863 (Lewis et al., 2006). Both species have partly sympatric distribution in the western Atlantic region (Bastida-Zavala & ten Hove, 2003a). H. sanctaecrucis is commonly found along the Caribbean Sea, Suriname and Gulf of Mexico (BastidaZavala & ten Hove, 2003a). It also recently invaded the Pacific Coast of Panama and some localities along the Pacific coast of Mexico (Bastida-Zavala & ten Hove, 2003b), as well as Australia and Singapore (Lewis et al., 2006) (Figure 2). Hydroides sanctaecrucis and H. dianthus are distinguished by the presence of external spinules on the main spines of the verticil: the spinules are present in H. sanctaecrucis and are absent in H. dianthus. (Figure 1C, sp). The Japanese specimens reported here are clearly without external or lateral spinules (Figures 1A, G) and thus belong to H. dianthus. The possible sources of invasion of Hydroides dianthus reported here may include both the American or European coasts. Notably, this species has not been previously reported from the Asian region or the Pacific Ocean; the only record from Socorro Island, Pacific Coast of Mexico by Holguín-Qiñones (1994; as Eupomatus dianthus) is questionable and has not been confirmed yet. Therefore, it most likely has been introduced to Japan from an Atlantic or Mediterranean population. Hydroides dianthus is most likely to be introduced via ship hull-fouling, but its planktonic larvae might also be transported in ballast-water. Non-indigenous species can have serious ecological and environmental impacts on the recipient area where they establish. For example, H. elegans is a notorious pest of fisheries and mariculture in Japan, where it competes with oysters for food and oxygen. An outbreak of this serpulid polychaete in Hiroshima Bay has caused the heavy economic loss to cultured oyster crops through fouling on their shells, estimated at ¥3 billion in 1969 (equivalent to ~¥10 billion today) (Arakawa, 1971). Hydroides dianthus occurs in both temperate and subtropical estuaries and does not appear to have the temperature restrictions of other species of the genus Hydroides (Zibrowius & Thorp, 1989). Its close congeneric H. elegans has a reasonably wide salinity tolerance: although freshwater caused 100% mortality of the tubeless worms in two minutes, 5‰ caused 100% mortality after 9.5 h only (Mak & Huang, 1980). Similarly, maturation of H. dianthus is satisfactory in the salinity range of 25‰ to 35‰ (Leone, 1970). Larvae of Hydroides dianthus are planktonic for up to two weeks (Toonen & Pawlik, 2001) and show a tolerance for low dissolved oxygen (Sagasti et al., 2000). Although H. dianthus larvae preferentially settle on bare space (Dean, 1981) and its recruitment is inhibited by most other sessile species (Dean & Hurd, 1980), their settlement is also markedly gregarious, among conspecific adults (Scheltema et al., 1980, Toonen & Pawlik, 2001). As a result, Hydroides dianthus occurs in tube clusters that provide microhabitats to diverse assemblages of other invertebrates (Haines & Maurer, 1980). In the Mediterranean H. dianthus even builds small (less than 1 m) reefs in the western part of the Lagoon of Orbetello, Italy (Bianchi & Morri, 2001). The species has also been known to smother juvenile oysters by overgrowing them in its native range of North America (Eno et al., 1997). The fact that new settlement of H. dianthus was recorded in Tokyo bay suggests that the species has already established in the habitats studied here. According to its biological traits as discussed above, its introduction into the ecosystems along Japanese coasts may have serious negative effects, such as intensive fouling not only on harbour structures but also on mariculture.Therefore, expansion of this species in Japan has to be carefully monitored and the possibilities of preventing its spread to other areas need to be assessed. The first author thanks Dr Masahiro Nakaoka and his laboratory staff, now at Akkeshi Marine Station, Hokkaido University, Japan, for their assistance in collecting in the field. The field work has been conducted in the frame of the GAME (Global Approach by Modular Experiments) project coordinated by Martin Wahl and Mark Lenz, IFM-Geomar, Kiel, Germany. This work is partly funded by the Kanagawa Academy of Science and Technology (KAST), Kurita Water and Environment Research Fund (KWEF) and Fujiwara Natural History Foundation to E.N. This work was supported by the Grant-in-Aid for Scientific Research (KAKENHI 20008766).
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Numerical analysis of water quality improvement in the enclosed coastal area using Micro Bubble. Annual Journal of Coastal Engineering, 52, 1126–1130. [In Japanese.] Ten Hove, H.A., 1974. Notes on Hydroides elegans (Haswell, 1883) and Mercierella enigmatica Fauvel, 1923, alien serpulid polychaetes introduced into the Netherlands. Bulletin Zoologisch Museum, Universiteit van Amsterdam, 4, 45–51. Thorp, C.H., Pyne, S. & West, S. A., 1987. Hydroides ezoensis Okuda, a fouling serpulid new to British coastal waters. Journal of Natural History, 21, 863–877. Toonen, R.J. & Pawlik, J.R., 1994. Foundations of gregariousness. Nature, London, 370, 511–512. Verrill, A.E., 1873. Results of the recent dredging expeditions on the coast of New England. No. 3. American Journal of Science and Arts, 6, 435–441. Zibrowius, H., 1971. Les espèces Méditerranéennes du genre Hydroides (Polychaeta Serpulidae). Remarques sur le prétendu polymorphisme de Hydroides uncinata. Téthys, 2, 691–746. 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Zibrowius, H., 1978. Introduction du polychète Serpulidae japonais Hydroides ezoensis sur la côte atlantique française et remarques sur la propagation d’autre espèces de Serpulidae. Téthys, 8 (1976), 141–150. Zibrowius, H., 1992. Ongoing modification of the Mediterranean marine fauna and flora by the establishment of exotic species. Mesogee, 51, 83–107. Zibrowius, H., 1994. Introduced invertebrates: examples of success and nuisance in the European Atlantic and Mediterranean. In Introduced species in European Coastal Waters (ed. C.F. Boudouresque et al.) pp.44–49. Luxembourg: European Commission. Submitted 19 September 2008. Accepted 22 December 2008.
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