Abe et al. Marine Biodiversity Records (2019) 12:7 https://doi.org/10.1186/s41200-019-0167-4 RESEARCH Open Access Habitat availability determines distribution patterns of spionid polychaetes (Annelida: Spionidae) around Tokyo Bay Hirokazu Abe1,2,3* , Toshimitsu Takeuchi2,4, Masanori Taru3, Waka Sato-Okoshi5 and Kenji Okoshi2,3 Abstract An investigation of the distribution and habitat utilization of spionid polychaetes in Tokyo Bay revealed eight shell- boring and 18 non-boring (interstitial, epifaunal, and infaunal) species, of these 11 species were recorded in the area for the first time. Most of the boring and interstitial species, which are associated with mollusc shells, were mainly distributed in exposed environments favoured by their host species outside Tokyo Bay. Only two boring species, Polydora websteri and Polydora haswelli preferred the enclosed waters of Tokyo Bay. Epifaunal and infaunal species were mainly distributed in the sandy and/or muddy sediment within Tokyo Bay. A widespread or localized distribution pattern within species was observed corresponding to the larval developmental mode. We concluded that habitat availability determines distribution patterns of spionid polychaetes around Tokyo Bay. Novel habitats for Boccardiella hamata, Boccardia proboscidea, Carazziella spongilla,andPolydora cornuta were recorded. Boccardia pseudonatrix, which was recorded for the first time from Japan with clear locality information, is considered to be a potential alien species. Keywords: Polydorids, Habitat type, Host utilization, Distribution trend, Boring, Tokyo Bay Introduction and developmental modes (Blake and Arnofsky 1999) The family Spionidae, one of the largest and most di- are presumed to play an important role in the evolution- verse taxa of polychaetous annelids, is a major compo- ary success of spionids. nent of marine and estuarine benthic communities all Spionid polychaetes, especially in polydorids (the gen- over the world. The spionids are widely distributed from era: Polydora, Dipolydora, Pseudopolydora, Boccardia, deep-sea to freshwaters (e.g. Glasby and Timm 2008; Polydorella, Tripolydora, Boccardiella, Carazziella, and Paterson et al. 2016). The group is well known to utilize Amphipolydora), are well known as invasive polychaetes various substrates such as bottom sediment, sand or worldwide and pose a potential risk of marine biological mud deposits in crevices of stones, rocks, shells, and invasion (Çinar 2013). In most cases, the invasion path- byssus and to associate with other invertebrates. Some way of spionids is considered to be through ship fouling spionids can bore into various hard calcareous substrates or ballast water (Carlton 1985; Çinar 2013). Additionally, (Blake and Evans 1972). Shell boring ability is considered anthropogenic translocation of molluscs for aquaculture to be species specific (Sato-Okoshi 1999, 2000), although is a significant invasive pathway for spionids, which bore there are some exceptions (e.g. Radashevsky and Pan- into, or associate with, commercially important molluscs kova 2013). In addition to the ability to exploit a wide (Simon and Sato-Okoshi 2015). The rapid globalization range of habitats that are not utilized by other inverte- and increasing trends of the living shellfish trade brates (Blake 1996), the great plasticity in feeding worldwide in recent decades have accelerated marine methods (Dauer et al. 1981) and diverse reproduction biological invasions of the boring spionid polychaetes (Radashevsky and Olivares 2005; Sato-Okoshi et al. * Correspondence: [email protected]; [email protected] 2008). Biological invasions are one of the most import- 1Department of Biology, Center for Liberal Arts & Sciences, Iwate Medical University, 2-1-1 Nishitokuta, Yahaba-cho, Shiwa-gun, Iwate 028-3694, Japan ant direct drivers of biodiversity loss and a major pres- 2Department of Environmental Science, Faculty of Science, Toho University, sure on several types of ecosystems (Katsanevakis et al. 2-2-1 Miyama, Funabashi, Chiba 274-8510, Japan 2014). Nevertheless, little attention has been paid to Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Abe et al. Marine Biodiversity Records (2019) 12:7 Page 2 of 12 marine biological invasions, especially in unintentionally Although Tokyo Bay connects to open ocean adjacent to transported species including spionids (Sato-Okoshi et the Sagami Gulf via the Uraga Channel, water exchange al. 2012). An understanding of basic ecology, including is limited by the narrow width (7 km) of the channel environmental preference and habitat utilization (Fig. 1; Sukigara and Saino 2005). Huge environmental patterns of the spionids which pose a potential risk of differences between the inside (north of the boundary marine biological invasion, is useful for the prediction of line from Cape Futtsu on Boso Peninsulato to Cape their expansion and of the potential ecological impacts Kannonzaki on Miura Peninsula, an enclosed bay) and when the species invade a new geographical region. In outside (Uraga Channel and open ocean) of Tokyo Bay particular, such studies in areas which include big inter- allow an evaluation of the environmental preferences of national trading ports and thus susceptible to biological spionid species. invasions would provide valuable information in the In the present study, to reveal the distribution of the context of the real invasion problems. spionid fauna occurring around Tokyo Bay and the detec- Tokyo Bay, which is surrounded by Boso Peninsula tion of potentially invasive alien species, a field survey and Miura Peninsula (Fig. 1), is one of the biggest ‘melt- across a wide variety of habitats was carried out. This was ing pots’ of alien species in Asia as a consequence of the also intended to indicate environmental preferences and presence of Tokyo Port, one of the biggest international habitat utilization patterns of the spionids, as well as the trading ports in Japan (Asakura 1992; Iwasaki 2006). relationships between habitat availability and distribution Extensive loss of tidal flats by reclamation has occurred pattern especially focused on the polydorid spionids. in the twentieth century (Furukawa and Okada 2006). Owing to a large population and intensive industrial Methods activity surrounding the bay, eutrophication often leads Sampling of spionid polychaetes was conducted at 24 to seasonal hypoxia of bottom waters. Wind-driven sites around Tokyo Bay (Fig. 1; outside of the bay: A-I, coastal upwelling of the hypoxic water sometimes causes inside of the bay: J-X) during the period from July 2012 mass mortality of marine organisms (Takeda et al. 1991). to July 2016 (Table 1). Mollusc species (23 gastropods, Fig. 1 Localities of sampling sites around Tokyo Bay, Japan. Sampling sites were as follows: (A) Kominato, (B) Chikura, (C) Okinoshima, (D) Tomiura, (E) Takeoka, (F) Kannonzaki, (G) Ena, (H) Bishamon, and (I) Jogashima outside of Tokyo Bay and (J) Shiomi, (K) Obitsu, (L) Kisarazu, (M) Mitate, (N) Yoro, (O) Chiba, (P) Inage, (Q) Funabashi, (R) Sanbanze, (S) Kasai, (T) Wakasu, (U) Odaiba, (V) Tama, (W) Kanazawa, and (X) Nojima in Tokyo Bay Abe Table 1 List of sampling sites, locality, sampling date, and collected samples in the present study Site Locality Sampling Surveyed Collected samples et al. Marine Biodiversity Records dates environment Gastropoda Bivalvia Other invertebrates Substrates Outside of Tokyo Bay A Kominato Aug 2013, Oct Rocky shore Cellana nigrolineata, Patelloida saccharina lanx, Pinctada martensii Ishnochitonidae sp., 2016, Jul 2017 Lottia dorsuosa, Haliotis diversicolor aquatilis, Liolophura japonica, Haliotis gigantea, Haliotis discus discus, Cryptoplax japonica, Omphalius pfeifferi pfeifferi, Monodonta Hymeniacidon sinapium, confusa, Turbo sazae, Lunella coreensis, Demospongiae sp. Lyncina vitellus, Thais clavigera B Chikura Jul 2012, Mar Fishery habor Batillaria attramentaria Crassostrea gigas, Saccostrea Liolophura japonica, 2013, Jul 2016 kegaki Hymeniacidon sinapium (2019)12:7 C Okinoshima Jul 2013 Rocky shore Patelloida saccharina lanx, Omphalius pfeifferi Crassostrea gigas, Saccostrea Liolophura japonica pfeifferi, Trochus sacellus rota, Monoplex kegaki parthenopeus, Thais clavigera D Tomiura Aug 2013, Fishery habor Cellana nigrolineata, Patelloida saccharina lanx, Hyotissa inermis, Crassostrea Apr 2016 Omphalius pfeifferi pfeifferi, Trochus sacellus rota, gigas, Crossostrea nippona, Turbo stenogyrus, Monoplex parthenopeus, Thais Saccostrea clavigera kegaki E Takeoka Jun 2014 Rocky shore, Chlorostoma lischkei, Omphalius rusticus, Crassostrea gigas, Saccostrea Liolophura japonica Fishery habor Calliostoma unicum, Monoplex parthenopeus, kegaki Monodonta confusa, Thais clavigera F Kannonzaki Jul 2013 Rocky shore Patelloida saccharina lanx, Chlorostoma lischkei, Anomia chinensis, Crassostrea Liolophura japonica Omphalius rusticus, Monodonta confusa, Thais gigas, Saccostrea