Recent discovery of Paranthura japonica Richardson , 1909 ( Crustacea : Isopoda : Paranthuridae ) in European marine waters ( Arcachon Bay , Bay of Biscay )

The Asiatic isopod Paranthura japonica Richardson, 1909 was collected in 2007 in Arcachon Bay (SW France), where the species occurs in a variety of habitats, both in the intertidal and at shallow depths. This species, native to the Sea of Japan, may have been accidentally introduced in Arcachon Bay with oyster transfers or as fouling on ship hulls.


Introduction
Only three Paranthura species (Crustacea: Isopoda: Paranthuridae) are known to occur in coastal Atlantic European waters: P. costana Bate & Westwood, 1866, from the Shetland Islands to Morocco (0-355 m depth), P. nigropunctata (Lucas, 1846), from the English Channel to Mauritania (0-84 m depth) (Junoy and Castelló 2003) and P. santiparrai Frutos, Sorbe & Junoy, 2011 recently described from the 'El Cachucho' Marine Protected Area, southern Bay of Biscay (498-817 m depth).The Asiatic species Paranthura japonica Richardson, 1909 was first described from a single female specimen collected in 1906 by the US steamer Albatross on the shore of Muroran (Hokkaido Island, Japan).At present, its known distribution includes many localities (0-15 m depth) from northern and southern coasts of Japan (Yamada et al. 2007;Nunomura, pers. comm.), eastern Russia (Nunomura 1975(Nunomura , 1977)), and eastern China (Ong Che and Morton 1991;Li 2003;Zhang et al. 2009;Wang et al. 2010).Outside its native area, this species has been recorded in San Francisco Bay in 1993 (Cohen and Carlton 1995) and in Southern California in 2000 (Cohen et al. 2005) and is recognized as an exotic species in California (Ruiz et al. 2011).This paper reports the discovery of P. japonica in European marine waters (Arcachon Bay, SW France).

Study area
Arcachon Bay is a 180-km² macrotidal (maximum tidal range: 4.9 m) coastal lagoon situated on the south-western coast of France (Figure 1).This lagoon connects with the Atlantic Ocean by a narrow channel and receives freshwater inputs in its south-eastern part (Leyre River).It is characterised by large intertidal flats (115 km²), the lower parts of which are used for cupped oyster [Crassostrea gigas (Thunberg, 1793)] farming.Most of the intertidal area (46.2 km²) is covered by seagrass beds, Zostera noltei Hornemann, 1832 (Plus et al. 2010).In the inner lagoon, tidal channels represent an area of 71 km², with 1.02 km² occupied by eelgrass beds, Zostera marina Linnaeus, 1753 (Plus et al. 2010).

Material examined
During surveys carried out between 2007 and 2010, Paranthura japonica was collected in several stations in Arcachon Bay (Figure 1).Bottom sediments were collected using a Van Veen grab in subtidal habitats or a hand-corer in intertidal habitats.These specimens (Figure 2
As reported by Frutos et al. (2011), the specimens (males, females and juveniles) from Arcachon Bay can be easily separated from the European Paranthura species by the mid-dorsal fusion of their pleonites 1-5 (Figure 2B).Moreover, the comparison with specimens of P. japonica from the Sea of Japan revealed similar external morphology, characterized by the following features (and excludes other known Japanese Paranthura species, according to the descriptions by Nunomura (1974Nunomura ( , 1975Nunomura ( , 1977Nunomura ( , 1993))): eyes composed of less than 17 ommatidia that are clumped together; short pleotelson barely exceeding the tip of uropods; pereonite 6 shorter than pereonite 5; and anterolateral angles of cephalon exceeding rostral projection.None of the other known Paranthura species shows such a combination of morphological characters.Therefore, we concluded that the Arcachon specimens were P. japonica.
At first glance, P. japonica could be confused with the cosmopolitan Cyathura carinata (Krøyer, 1847), a well-known littoral Anthuridae from European coasts, and including muddy fine sediments from Arcachon Bay (Salvat 1967).However, this last species can be distinguished by mouth appendages not acutely produced (a major morphological feature at family level), pleonites 1-5 completely fused, appendix masculina of pleopod 2 bearing distally two flat lobes and a stout anchor-shaped seta, and telson with two dorsal statocysts (see full description in Cléret 1960).

Discussion
The vector of introduction of Paranthura japonica in Arcachon Bay is difficult to determine.The natural spread of adult specimens from another location is unlikely for several reasons: (1) the species is known only from its native area (NE Pacific) and California; (2) as a benthic species, it does not seem able to swim over long distances; and (3) the major shipping harbours in SW France are situated far from Arcachon Bay (Bordeaux 200 km, Bayonne 150 km) and separated from the bay by highly dynamic, sandy, shores.Ship's ballast water and fouling have been hypothesized as the way of introduction of P. japonica on the Pacific coast of North America (Cohen and Carlton 1995;Cohen et al. 2005).In our opinion transport in ballast waters may be dismissed because of the direct development and the lack of pelagic larvae in Paranthuridae (Frutos et al. 2011), as well as the absence of large commercial ships in Arcachon Bay.Introduction with colonial organisms (e.g.sponges, hydroids, ascidians or bryozoans) fouling the hulls of sailing ships or pleasure boats is a possible vector for P. japonica's entry in Arcachon Bay and was suggested for other isopods such as Mesanthura sp. in Italian harbours (Lorenti et al. 2009) and Synidotea laevidorsalis (Miers, 1881) on a world-wide scale (Chapman and Carlton 1994).
Accidental introduction with oyster transfers is a likelier hypothesis.Arcachon Bay is one of the major French oyster farming sites with a production of 7,000-8,000 t per year (Scourzic et al. 2011).In the early 1970s, the Portuguese cupped oyster Crassostrea angulata (Lamarck, 1819), which was farmed in the bay since the end of the 19 th century, was decimated by a viral disease (Goulletquer et al. 2002).To sustain the local oyster industry, the exotic Pacific cupped oyster C. gigas was then massively introduced in Arcachon Bay between 1971 and 1975, as spat from Senday Bay, NE Honshu Island, Japan (1,176 t of spat collectors from 1971 to 1975) and as adults from British Columbia, Canada (137.5 t from 1971to 1973) (Grizel and Héral 1991).Intentional oyster transfer is a well-known vector of accidental introduction for many alien species (Gruet et al. 1976;Verlaque et al. 2007), and may have been be responsible for the introduction of P. japonica in Arcachon Bay and was previously documented for other non-native species in this area (Bachelet et al. 2004(Bachelet et al. , 2008)).However, no import of cupped oyster from Japan to Arcachon has been officially reported after the 1970s.This means that P. japonica may have remained unnoticed in Arcachon Bay since that time, either because it was too rare or misidentified.Alternatively, it could have been introduced with an undeclared oyster transfer from Japan or from another area where this anthurid has not been identified so far.
In Japanese waters, P. japonica is associated with subtidal Zostera spp.meadows (Nakaoka et al. 2001;Yamada et al. 2007) or with colonies of brown algae Sargassum spp.(Nunomura 1977).In Arcachon Bay, it seems to be well established in the whole area, including different locations and habitats, but it remains a rare species with low abundances (see Appendix 1).
P. japonica might be present in other European shellfish farming areas.The transfer of C. gigas among regions has caused the introduction and spread of numerous alien species in northern Europe (Goulletquer et al. 2002).The lack of previous records in Europe might be due to the small size of individuals, the low abundance of local populations, or its misidentification (including a possible confusion with Cyathura carinata).

Figure 1 .
Figure 1.Stations where the benthic anthurid isopod Paranthura japonica was collected in Arcachon Bay.
) were compared to P. japonica specimens stored in the Muséum National d'Histoire Naturelle, Paris (Gurjanova leg, 1934, MNHN-IU-2009-45, Petrov Island, Sea of Japan) and in the Toyama Science Museum, Japan (Japanese specimens collected in the Toyama and Mutsu Bays, Honshu; N. Nunomura, Osaka Museum, pers.comm.).All specimens were examined under a Nikon SMZ 1500 stereomicroscope, photographed with a Nikon DS-Fi 2 camera and an image of one specimen drawn with a Wacom Intuos 5 tablet and the Inkscape software.Total length TL was measured with the NIS-Elements Analysis software from the cephalon anterior margin to the telson apex.Five specimens from Arcachon Bay (Station K) were deposited in the Muséum National d'Histoire Naturelle, Paris (MNHN-IU-2012-1359).