Hydroides ezoensis -

Hydroides ezoensis is originally found in the northeastern part of the Pacific Ocean, specifically in the Sea of Japan and the East China Sea ^[2,3].

First observation in Belgium

Hydroides ezoensis was first observed in 2021, and possibly even slightly earlier, in the marina of Zeebrugge ^[4]. Due to its very limited and inconspicuous presence among the growth on the marina's pontoons, it is likely that the species was present there before 2021 but went unnoticed. Any potential pre-2021 sightings were not recorded and received insufficient attention due to the assumption that they might be the cosmopolitan Hydroides norvegicus, with which Hydroides ezoensis can be confused ^[5-9].
 

Distribution in Belgium

Outside the marina, the species was also likely found on groynes along the east coast: in 2023 near Zwinbosjes (Knokke) and in 2024 at Duinbergen ^[10]. The validity of these observations will need further investigation.
 

Distribution in neighbouring countries

In several locations along the Atlantic coast of France, large quantities of oyster spat (transported on oyster and large mantle shells) from the Japanese oyster Crassostrea/Magallana gigas were introduced for cultivation starting in 1968, particularly between 1971 and 1973. In 1974, research conducted in the Bay of Bourgneuf and around Le Croisic investigated the epifauna that accompanied this introduction. It was found that Hydroides ezoensis was abundant on the shells serving as substrate ^[11]. In addition to the reportings at several other sites along the French Atlantic coast, it was also suggested that Hydroides ezoensis may have arrived with oyster spat introductions in the early 1970s in various locations in the Channel (North Brittany and Normandy), as well as in the Mediterranean (Sète) ^[2,3]. However, it remained uncertain whether the species had actually established itself along the French coast. Extensive monitoring of harbors and oyster farms along the French Atlantic and Channel coasts in 1986 found no specimens of Hydroides ezoensis ^[2,12]. A new observation in French waters did not occur until 1997, when the crown worm was noted in the port area of Le Havre (Normandy), with the assumption that it had been introduced there in 1996 ^[13].

In England, the crown worm was found in large numbers on stationary tugboats in the docks of Southampton in 1982. Similar growth was reportedly observed on a shipyard in nearby Marchwood in 1980 and 1981. Revisiting material collected in 1979 from two marinas in the Hamble estuary also revealed adult specimens of this worm. In 1977, a small specimen of a calcareous tube worm species was accidentally discovered in the seawater inlet of the Fawley power station, which later turned out to be Hydroides ezoensis. Research in the early 1980s in Southampton Water, the Hamble estuary, the Solent, and adjacent ports in Portsmouth, Langstone, and Chichester revealed numerous sites of the worm in this region. Surveys in other harbors along the English south and west coasts, and one on the east coast, were all negative. The introduction of the species into the marina of Brighton in 1984 via fouling on a ship's hull was unsuccessful, with the population proving non-viable and nearly disappearing by 1986. It is suggested that the colonisation of the Solent and surrounding areas may not have occurred planktonically from temporary (short-lived?) populations along the French Channel coast, but rather through repeated arrivals as fouling or in ballast water from ships from Japan ^[2,12]. In 2003, the presence of Hydroides ezoensis was confirmed in the northeastern part of the English east Channel coast ^[14].

In 2019, Hydroides ezoensis was found on artificial structures in the harbors of Vlissingen and Rotterdam ^[15]. Two years later, several specimens were also discovered at various locations in the western part of the Grevelingenmeer ^[16]. Further afield, Hydroides ezoensis also arrived in Australia in 1996 ^[5,17].

In France, the species was found in the 1970s on shells of Japanese oysters Crassostrea/Magallana gigas imported from Japan. Regarding England, it is considered more likely that the species was introduced through the transport of adult individuals via ships from Japan (ballast water or fouling on hulls), rather than planktonic larvae being naturally transported by currents from France ^[12]. Furthermore, the time gap of several decades between the introductions in France and the Netherlands cannot be easily explained. Both the increase in water temperature (with a gradual northward shift in populations) and incidental further spread via shipping are plausible options ^[15].

The species appears to be tolerant of seawater temperature variations ranging from -1°C (winter) to 32.2°C (summer) ^[18-20], with a minimum and optimal reproductive temperature of 18°C and 24°C, respectively ^[20]. It is believed that the species cannot survive under natural conditions at salinities below 10 psu. The highest survival and metamorphosis rates occur at salinities between 25 and 35 psu, but the species can survive within a salinity range of 20 to 40 psu ^[21].

The worm attaches to almost any submerged structure with a microbial film in the low intertidal zone to shallow subtidal areas (found up to 11.8 meters deep), such as rocks, shells, macroalgae, ship hulls, buoys, marine aquaculture equipment, and docks ^[2,5,17].

With a planktonic larval stage and a sessile adult stage, Hydroides species can be easily transported (whether by human activity or not) and introduced to new locations, where they can rapidly establish large populations under favorable environmental conditions ^[22-24].

The species is known as a fouling organism that forms dense colonies of strongly adhering calcareous tubes on submerged structures such as aquaculture equipment (on nets and also on the shellfish themselves ^[25]), ship hulls, buoys ^[26], and cooling water systems ^[6,12,27]. For instance, in England, the species has caused navigation problems by fouling navigation buoys with tubes up to 30 cm thick, affecting their buoyancy ^[28]. This results in high economic costs for removing the tubes from artificial structures and negatively impacts the market price of affected shellfish for human consumption ^[6]. Efforts to remove Hydroides ezoensis from oyster beds, such as immersion in fresh water, have proven largely ineffective ^[12].

These fouling communities can also negatively impact local marine community structure by altering ecosystem dynamics and species composition through competition for space and resources ^[6]. However, it remains uncertain whether this scenario will occur in the current introduction areas.

Hydroides ezoensis can grow up to 43 mm in length (typically 25-35 mm ^[22]), with a maximum thorax width of 7 mm ^[7,8]. These tube worms filter food particles from the water using a double crown of tentacles at the head, which consists of about 30 bristles and has a diameter of approximately 15 mm. The color of the crowns varies by individual, ranging from inconspicuous (semi-transparent whitish, grayish-white, gray-green with pale brown bands) to brightly colored yellow and blue. When the worms are retracted into their tubes, the tentacle crowns are not visible. They close the opening of their tube with a closing plate (operculum) ^[29]. The branchiae and operculum make up about one-fifth of the total length ^[5,7,8].

The calcareous tubes are white and firmly attached to the substrate, typically stones or shells, or other organisms. They are often coiled in multiple spiral turns but can also be elongated, angular, or curved. A very characteristic feature is the two (sometimes less distinct) ridges on the upper side of the tube. This can cause confusion with the native calcareous tube worm, Spirobranchus triqueter, which has only one clear, sharp keel on the tube, giving it a triangular cross-section ^[29]. Hydroides ezoensis is also closely related to another native calcareous tube worm, Hydroides norvegicus, and could be confused with it, especially when the ridges are less distinct ^[8]. For a detailed description of these species, see the specialised literature ^[5,7-9].

The identification of introduced Hydroides species can be complicated as other species, such as Hydroides elegans, Hydroides dianthus, and others, also appear to spread worldwide through anthropogenic means and might potentially establish here ^[12,30]. Additionally, if there is niche overlap among Hydroides species, leading to sympatric occurrences, it will require extra attention for accurate identification ^[4].

[1]          World Register of Marine Species (WoRMS) (2024). Hydroides ezoensis Okuda, 1934. https://www.marinespecies.org/aphia.php?p=taxdetails&id=131003 (2024-10-18). 

[2]          Thorp, C.H.; Pyne, S.; West, S.A. (1987). Hydroides ezoensis Okuda, a fouling serpulid new to British coastal waters. J. Nat. Hist. 21(4): 863-877. [https://www.vliz.be/nl/imis?module=ref&refid=365433] 

[3]          Zibrowius, H. (1978). Introduction du polychète Serpulidae japonais Hydroides ezoensis sur la côte atlantique française et remarques sur la propagation d’autres espèces de Serpulidae. Téthys 8(2): 141-150. [https://www.vliz.be/en/imis?module=ref&refid=393924] 

[4]          Dumoulin, E. (2024). Persoonlijke mededeling.

[5]          Sun, Y.; Wong, E.; ten Hove, H.A.; Hutchings, P.A.; Williamson, J.E.; Kupriyanova, E.K. (2015). Revision of the genus Hydroides (Annelida: Serpulidae) from Australia. Zootaxa, 4009(1). Magnolia Press: Auckland. ISBN 978-1-77557-779-9. 1-99 pp. [https://www.vliz.be/en/imis?module=ref&refid=393879] 

[6]          Sun, Y. (2017). Taxonomy, barcoding and phylogeny of Hydroides (Serpulidae, Annelida), the largest genus of notorious fouling and invading calcareous tubeworms. PhD Thesis. Macquarie University, Department of Biological Sciences: Sydney. vii, 320 pp. [https://www.vliz.be/en/imis?module=ref&refid=393868] 

[7]          Imajima, M. (1976). Serpulinae (Annelida: Polychaeta) from Japan: I. The genus Hydroides. Bull. Natl. Mus. Nat. Sci., Ser. A 2(4): 229-248. [https://www.vliz.be/en/imis?module=ref&refid=393878]  

[8]          Okuda, S. (1934). Some tubicolous annelids from Hokkaido. Journal Fac. Sci. Hokkaido Un. Zool. 3(4): 233-246. [https://www.vliz.be/en/imis?module=ref&refid=393468]  

[9]          Rzhavsky, A.V.; Kupriyanova, E.K.; Sikorski, A.V.; Dahle, S. (2014). Calcareous tubeworms (Polychaeta, Serpulidae) of the Arctic Ocean. KMK Scientific Press: Moscow. ISBN 978-5-87317-988-6. 191 + plates pp. [https://www.vliz.be/nl/imis?module=ref&refid=245464] 

[10]        waarnemingen.be. Hydroides ezoensis Okuda, 1934. https://waarnemingen.be/species/837209/ (2024-03-05).

[11]        Gruet, Y.; Héral, M.; Robert, J.M. (1976). Premières observations sur l’introduction de la faune associée au naissain d’huîtres japonaises Crassostrea gigas (Thunberg), importé sur la côte atlantique française. Cah. Biol. Mar. 17(2): 173-184. [https://www.vliz.be/nl/imis?module=ref&refid=61523] 

[12]        Zibrowius, H.; Thorp, C.H. (1989). A review of the alien serpulid and spirorbid polychaetes (Polychaeta, Annelida) in the British Isles. Cah. Biol. Mar. 30(3): 271-285. [https://www.vliz.be/nl/imis?module=ref&refid=65077] 

[13]        Breton, G.; Vincent, T. (1999). Invasion du port du Havre (France, Manche) par Hydroides ezoensis (Polychaeta, Serpulidae), espèce d’origine japonaise. Bull. trim. Soc. Géol. Normandie et Amis Muséum du Havre 86(2): 33-43. [https://www.vliz.be/en/imis?module=ref&refid=393922]  

[14]        Dauvin, J.-C.; Dewarumez, J.-M.; Gentil, F. (2003). Liste actualisée des espèces d’Annélides Polychètes présentes en Manche = An up to date list of polychaetous annelids from the English Channel. Cah. Biol. Mar. 44(1): 67-95. [https://www.vliz.be/nl/imis?module=ref&refid=33908] 

[15]        Faasse, M.; ten Hove, H.A.; Paalvast, P. (2020). The Pacific serpulid tube worm Hydroides ezoensis Okuda, 1934 reaches the ports of Rotterdam and Vlissingen (Flushing), the Netherlands (North Sea). Cah. Biol. Mar. 61: 415-421. [https://vliz.be/nl/imis?module=ref&refid=367145] 

[16]        Aleman, A.; Faasse, M. (2021). Gaat de Kroontjesworm Hydroides ezoensis Okuda, 1934 Nederland veroveren? Het Zeepaard 81(5): 249-253. [https://vliz.be/nl/imis?module=ref&refid=350282] 

[17]        Hayes, K.R.; Sliwa, C.; Migus, S.; McEnnulty, F.R.; Dunstan, P. (2004). National priority pests: Part II. Ranking of Australian marine pests. Australian Government Department of the Environment and Heritage: Parkes. ISBN 1 876996 80 3. 98 pp. [https://www.vliz.be/en/imis?module=ref&refid=393921] 

[18]        Ovsyannikova, I.I.; Levenets, I.R. (2003). Macrofouling of the scallop Mizuhopecten yessoensis in the polluted area of Amursky Bay, Sea of Japan. Russ. J. Mar. Biol. 29(6): 395-402. [https://www.vliz.be/en/imis?module=ref&refid=393920] 

[19]        Uchida, T.; Yamada, M.; Iwata, F.; Oguro, C.; Nagao, Z. (1963). The zoological environs of the Akkeshi Marine Biological Station. Publ. Akkeshi Mar. Biol. Stat. 13: 1-36 + 7 text-figures and 4 pls. [https://www.vliz.be/en/imis?module=ref&refid=393919] 

[20]        Cao, S.-M.; Xu, H.; Liu, P.-L.; Li, J.; Sun, W.-S. (2009). Effects of temperatures on growth, development and metamorphosis of Hydroides ezoensis larvae. J. Dalian Fish. Coll. = Dalian Shuichan Xueyuan Xuebao 24(6): 531-535. [https://www.vliz.be/en/imis?module=ref&refid=393887]  

[21]        Cao, S.-M.; Liu, R.-C.; Li, X.-J.; Hao, S.; Xu, H. (2013). Effects of salinity on fertility, hatching rate, survival, and metamorphosis in Hydroides ezoensis larvae. Journal of Dalian Ocean University 28(2): 133-137. [https://www.vliz.be/en/imis?module=ref&refid=393884]  

[22]        Lewis, J.A.; Watson, C.; ten Hove, H.A. (2006). Establishment of the Caribbean serpulid tubeworm Hydroides sanctaecrucis Krøyer [in] Mörch, 1863, in Northern Australia. Biological Invasions 8(4): 665-671. [https://www.vliz.be/en/imis?module=ref&refid=393875] 

[23]        Link, H.; Nishi, E.; Tanaka, K.; Bastida-Zavala, R.; Kupriyanova, E.K.; Yamakita, T. (2009). Hydroides dianthus (Polychaeta: Serpulidae), an alien species introduced into Tokyo Bay, Japan. Marine Biodiversity Records 2: e87. [https://www.vliz.be/en/imis?module=ref&refid=393873] 

[24]        Pettengill, J.B.; Wendt, D.E.; Schug, M.D.; Hadfield, M.G. (2007). Biofouling likely serves as a major mode of dispersal for the polychaete tubeworm Hydroides elegans as inferred from microsatellite loci. Biofouling (Print) 23(3): 161-169. [https://www.vliz.be/en/imis?module=ref&refid=393872] 

[25]        Arakawa, K.Y. (1971). Notes on a serious damage to cultured oyster crops in Hiroshima caused by a unique and unprecedented outbreak of a serpulid worm, Hydroides norvegica (Gunnerus) in 1969 . Venus Jap. J. Malacol. 30(2): 75-82. [https://www.vliz.be/en/imis?module=ref&refid=393871] 

[26]        Wang, J.; Huang, Z. (1993). Fouling polychaetes of Hong Kong and adjacent waters. Asian Mar. Biol. 10: 1-12. [https://www.vliz.be/en/imis?module=ref&refid=393995]  

[27]        Qiu, J.W.; Qian, P.Y. (1997). Combined effects of salinity, temperature and food on early development of the polychaete Hydroides elegans. Mar. Ecol. Prog. Ser. 152: 79-88. [https://www.vliz.be/en/imis?module=ref&refid=393822] 

[28]        Eno, N.C.; Clark, R.A.; Sanderson, W.G. (Ed.) (1997). Non-native marine species in British waters: a review and directory. Joint Nature Conservation Committee: Peterborough. ISBN 1-86107-442-5. 152 pp. [https://www.vliz.be/nl/imis?module=ref&refid=24400] 

[29]        Aleman, A. (2022). Herken de Kroontjesworm, een nieuwe kalkkokerworm. Zoekbeeld: nieuwsbrief van Stichting Anemoon 12(2): 22-23. [https://www.vliz.be/nl/imis?module=ref&refid=365709] 

[30]        ten Hove, H.A. (1974). Notes on Hydroides elegans (Haswell 1883) and Mercierella enigmatica Fauvel 1923, alien serpulid polychaetes introduced into the Netherlands. Bull. Zool. Mus. Univ. Amsterdam 4(6): 45-51. [https://www.vliz.be/nl/imis?module=ref&refid=119065]

VLIZ Alien Species Consortium (2024). Hydroides ezoensis. Introduced alien species of the Belgian part of the North Sea and adjacent estuaries anno 2024. Flanders Marine Institute (VLIZ). 7 pp.