The Galeommatoidea is a bivalve superfamily that exhibits high species diversity in shallow waters. Many members of this superfamily are associated commensally with burrowing marine invertebrates in benthic sediments. The genus Borniopsis is known only from eastern Asia and exhibits high host diversity (e.g., mantis shrimps, crabs, holothurians, sipunculans and echiurans). A new species, Borniopsis mortoni sp. n., is described from mud flats at the mouth of the Souzu River, southwestern Shikoku Island, Japan. This species has elongate-ovate shells covered by a tan to dark brown periostracum, and lives attached by both its foot and byssal threads to the body surface of the synaptid sea cucumber Patinapta ooplax. Several individuals of B. mortoni are often found on the same host, but sometimes more than 10 individuals can occur together. Borniopsis mortoni is one of the smallest species in this genus. Probably, its small body size is an adaptation to the mode of life in a narrow host burrow. Until now, only two other Borniopsis species were known to have commensal associations with synaptids. Thus, this is the third example of a synaptid-associated species from this genus. In addition, we briefly review the galeommatoideans commensal with apodid sea cucumbers.

Apodida , Bivalvia , Borniopsis , Byssobornia , commensalism, Galeommatoidea , host shift, Holothuroidea , Pseudopythina , symbiosis, Synaptidae

The Galeommatoidea is a superfamily of small bivalves that exhibits tremendous diversity in the intertidal zone (Bouchet et al. 2002, Paulay 2003, Lützen and Nielsen 2005). Many members of this superfamily are commensals associated in highly specific relationships with benthic invertebrates that burrow in soft sediments (Boss 1965, Morton and Scott 1989, Li et al. 2012, Goto et al. 2012). Most commensal galeommatoideans live attached directly onto the host’s body surface or the walls of its burrow (Boss 1965, Morton and Scott 1989, Goto et al. 2012).

The genus Borniopsis was established for B. tsurumaru Habe, 1959 as the type species with a second species, B. ariakensis Habe, 1959, from Japan (Habe 1959). Morton and Scott (1989) described four Pseudopythina (Borniopsis) species from Hong Kong. After this publication, Borniopsis was frequently synonymized with Pseudopythina (e.g., Lützen et al. 2004, Goto et al. 2012). However, Huber (2015) noticed that these East Asian Pseudopythina species are distinct from the type species P. macandrewi (P. Fischer, 1867), which occurs only in the eastern Atlantic Ocean, in dentition, seminal receptacles, and demibranchs and thus he transferred them to Borniopsis together with some species of Byssobornia, Squillaconcha and Kellia (Huber, 2015), although B. fujitaniana (Yokoyama, 1927) was recently reassigned to the genus Tellimya (Goto et al., 2016). As a result, at least nine species currently belong to this genus – B. tsurumaru, B. ariakensis, B. macrophthalmensis (Morton & Scott, 1989), B. maipoensis (Morton & Scott, 1989), B. nodosa (Morton & Scott, 1989), B. ochetostomae (Morton & Scott, 1989), B. subsinuata (Lischke, 1871), B. yamakawai (Yokoyama, 1922) and B. sagamiensis (Habe, 1961) (Huber 2015). All of these species are known only from eastern Asia. Those Borniopsis species, for which the biology is known, are host-specific commensals associated with burrowing invertebrates (mantis shrimps, crabs, holothurians, sipunculans, echiurans and probably tanaids) (Kuroda 1937, Morton 1972, 1988, Morton and Scott 1989, Goto and Kato 2012, Goto et al. 2012). Host animals are different among the Borniopsis species, except for one species pair (B. tsurumaru and B. ariakensis), suggesting that this group diversified by repeated host shifts among various invertebrates in eastern Asia. This assumption is partially confirmed by molecular phylogeny (Goto et al. 2012).

In this study, we describe a new species of Borniopsis, which was collected from the synaptid sea cucumber Patinapta ooplax (von Marenzeller, 1881) on mud flats at the mouth of Souzu River, southwestern Shikoku Island, Japan. Patinapta ooplax is a small earthworm-like holothurian that burrows in muddy sediments in the intertidal zone. We compared its morphology and host associations with the other Borniopsis species. In addition, we reviewed galeommatoideans associated with apodid sea cucumbers.

An undescribed species of Borniopsis was found attached to the synaptid sea cucumber Patinapta ooplax in the mud flats at the mouth of the Souzu River, Ainan-cho, Ehime Prefecture, southwestern Shikoku Island, Japan (32°57'N, 132°33'E) on 20 May 2000. We collected the specimens of this bivalve species during spring low tides in 2000, 2001, 2003, 2006, 2007, 2009, 2012, and 2013. Seven specimens collected on 11 March 2012 and two specimens collected on 15 March 2013 were preserved in 100% ethanol and brought back to the laboratory and observed under a binocular dissecting microscope for description. One specimen collected on 12 April 2009 was bleached to remove the periostracum for observation of shell surface sculpture. We deposited the holotype and two paratypes in the Museum of Zoology, University of Michigan(UMMZ), and two paratypes in National Museum of Nature and Science, Tokyo (NSMT). We also observed specimens of B. tsurumaru (SBMNH 149526), B. ariakensis (SBMNH35056), B. ochetostomae (SBMNH 149525) and B. maipoensis (SBMNH 35126) loaned from the Santa Barbara Natural History Museum. All the loaned specimens were collected from the mud flats of Hong Kong.

Apodid sea cucumbers, including members of the families Synaptidae and Chiridotidae, are one of the major hosts for galeommatoideans (Boss 1965, Morton and Scott 1989, Kato 1998, Middelfart and Craig 2004) (Table 1). Including B. mortoni, at least 13 species are known to have commensal associations with apodid holothurians (Table 1). They can be separated into the following four groups: the first group includes Anisodevonia, Austrodevonia, Devonia and Entovalva, which have reduced shells covered by well-developed mantle lobes (Kawahara 1942, Kato 1998, Middelfart and Craig 2004); the second group includes Borniopsis covered in this study (Morton 1988, Morton and Scott 1989); the third groups includes Montacuta (Bateson 1923, Fox 1979); and the forth group includes Scintillona (Morton 1957, Ó Foighil and Gibson 1984). All of these four groups live attached to the apodid’s body surface, except for Entovalva, which lives inside the host’s oesophagus (Spärk 1931, Kato 1998). Molecular phylogenies suggested that associations with apodids have evolved repeatedly in the Galeommatoidea (Goto et al. 2012).

Borniopsis mortoni lives commensally with the apodid sea cucumber P. ooplax on the temperate coast of western Shikoku Island. On the other hand, another galeommatoidean species, Anisodevonia ohshimai, lives attached to P. ooplax on the subtropical coast of the Ryukyu Islands, southwestern Japan (Kawahara 1942, Kato 1998). Extensive sampling for A. ohshimai has been undertaken in the Ryukyu Islands (Kawahara 1942, Kato 1998, Kosuge 2001). However, B. mortoni has never been found there. Thus, B. mortoni probably does not occur on the subtropical coast of the Ryukyu Islands and may be restricted to more temperate coasts. An alternative hypothesis is that P. ooplax used by A. ohshimai in the Ryukyu Islands is a different species to that used by B. mortoni in eastern Shikoku Island. The taxonomy of this group of synaptid holothurians remains poorly understood and thus it is highly probable that P. ooplax is a species complex.

A new species of the genus Borniopsis is described herein. This genus is restricted to eastern Asia, and each species apparently utilizes a different invertebrate host (Table 2), suggesting that its diversification was caused by repeated host shifting. The shell size varies among species (Table 2), which is probably a specialization to each particular commensal lifestyle. Borniopsis macrophthalmensis, B. maipoensis and B. mortoni are the three smallest species in this genus (Table 2). Borniopsis macrophthalmensis is attached to the body surface of highly-mobile intertidal crabs only by fine byssal threads (Morton and Scott 1989). If B. macrophthalmensis had a large, heavy shell, it would easily fall off the host crab when it scurries quickly on the surface of the mudflat. Thus, such a small shell is probably an adaptation for life on a highly-mobile crab. Similarly, another galeomatoidean species, Arthritica japonica Lützen & Takahashi, 2003, which is also attached to the body surface of crabs, has very small shells (up to 2.05 mm) (Lützen and Takahashi 2003). This may represent a morphological convergence to a similar commensal lifestyle and supports our hypothesis of reduction in shell size associated with fast-moving hosts mentioned above. On the other hand, the second species B. maipoensis lives commensally with the tanaid Discapseudes sp. (Morton and Scott 1989), whereas the third species B. mortoni lives with the synaptid sea cucumber P. ooplax. The diameter of these host burrows is very small. Thus, the small-sized shells of B. maipoensis and B. mortoni are probably an adaptation to the mode of life in narrow host burrows.

The mudflats of eastern Asia evidently possess one of the richest burrowing invertebrate faunas in the world. However, burrow associates remain poorly understood in many of them. Thus, further investigation in this area could reveal increased diversity of this distinctive bivalve genus Borniopsis.

We wish to express our sincere gratitude to the following people: Y. Hamamura (Hiroshima Prefecture) for providing the information of B. tsurumaru and B. ariakensis and the images on B. mortoni; P. Valentich-Scott (Santa Barbara Natural History Museum) for allowing us to loan the specimens and use of his image on B. maipoensis; D. Ó Foighil (University of Michigan) for hosting RG as a research fellow for this study and permission to use the facilities in the laboratory; L. Taehwan (University of Michigan) for helping RG to set up the laboratory facilities to observe specimens; R. C. Willan (Museum and Art Gallery of the Northern Territory), E. V. Coan (Santa Barbara Natural History Museum) and A. Holmes (National Museum Wales) for comments that greatly improved the manuscript. This study was partially supported by grants to RG from the Japan Society for the Promotion of Science (JSPS) Research Fellowship for Young Scientists and the JSPS Postdoctoral Fellowships for Research Abroad.