Living together in dead coral rocks: macrosymbiotic communities associated with Bonellia echiuran worms (Annelida: Thalassematidae: Bonelliinae), involving new commensal bivalve and amphipod species Author Goto, Ryutaro Seto Marine Biological Laboratory, Field Science Education and Research Center, Kyoto University, 459 Shirahama, Nishimuro, Wakayama 649 - 2211, Japan gotoryutaro@gmail.com Author Hirabayashi, Isao Kushimoto Marine Park Center Ltd, 1157 Arita, Kushimoto, Wakayama 649 - 3514, Japan & Kuroshio Biological Research Foundation, 560 Nishidomari, Otsuki, Kochi 788 - 0333, Japan Author Seike, Koji Geological Survey of Japan, National Institute of Advanced Industrial Science and Technology, 1 - 1 - 1 Highashi, Tsukuba, Ibaraki 305 - 0046, Japan & Department of Natural Environmental Studies, Graduate School of Frontier Sciences, The University of Tokyo, 5 - 1 - 5 Kashiwanoha, Kashiwa, Chiba 277 - 8563, Japan & School of Science, The University of New South Wales, Northcott Drive, Canberra, ACT 2600, Australia Author Yamashita, Momo Geological Survey of Japan, National Institute of Advanced Industrial Science and Technology, 1 - 1 - 1 Highashi, Tsukuba, Ibaraki 305 - 0046, Japan & Center for Collections, National Museum of Nature and Science, 4 - 1 - 1 Amakubo, Tsukuba 305 - 0005, Japan Author Shimomura, Michitaka Seto Marine Biological Laboratory, Field Science Education and Research Center, Kyoto University, 459 Shirahama, Nishimuro, Wakayama 649 - 2211, Japan text Zoological Journal of the Linnean Society 2024 2023-10-11 200 4 915 939 http://dx.doi.org/10.1093/zoolinnean/zlad103 journal article 297169 10.1093/zoolinnean/zlad103 e21d902e-2a58-4d99-aeb2-bad4034444da 0024-4082 11240746 7F78BDE9-9589-4878-94EB-852F88C8B4C9 Basterotia bonelliphila Goto & Hirabayashi , sp. nov. (New Japanese Name: Yokaze-gai) ( Figs 4A, B , 5 , 11–13 ) Zoobank registration: urn:lsid:zoobank.org:act: 9D61F68C-2F66-492C-97F7-B650CB870025 . Material examined: Holotype ( Fig. 11 ): NSMT-Mo 79470 [SL (shell length) 4.0 mm, SH (shell height) 1.6 mm , SW (shell width) 1.7 mm , Sabiura, Kushimoto, Wakayama , Japan , obtained from the burrow of Bo. sp. aff. minor , collected by I. Hirabayashi , 3 June 2020 ] . Paratype ( Fig. 12 ): NSMT-Mo 79471 (SL 2.6 mm , SH 1.3 mm , Sabiura, Kushimoto, Wakayama , Japan , obtained from the burrow of Bo. sp. aff. minor , collected by I. Hirabayashi , 3 June 2020 ) . Other material ( Fig. 13 ): 1 specimen (SL 4.3 mm , Sabiura, Kushimoto, Wakayama , Japan , obtained from the burrow of Bo . sp. aff. minor , collected by I. Hirabayashi , 4 July 2020 ) . Type locality: Sabiura , Kushimoto , Wakayama , Japan ( 33°28’43.61”N , 135°44’45.45”E ; Fig. 1 ) . Description: Shell length up to 4.3 mm , small for genus; shell thin, fragile, equivalve, strongly inequilateral, length/height ratio about 2.3, compressed (width/length ratio 0.43, holotype ). Shell gaping from anteroventral to anterodorsal margins. Shell outline cuneate; anterodorsal margin short, sloping steeply; anterior end rounded; ventral margin straight, nearly parallel with the dorsal margin; posteroventral margin obliquely rounded-subtruncate to a point near base; ventral margin long, nearly straight, slightly curved towards anterior and posterior ends. Beaks low, small, inflexed, prosogyrous, situated at about 17–19% from anterior end. A weak, oblique ridge running from the umbo to the posteroventral corner. Shell externally white with light brown tint; shell sculpture with irregular commarginal growth lines. Hinge ( Figs 11G, H , 12E, F ): A projecting prominent cardinal tooth present both in right and left valves. Cardinal tooth in right valve shorter than that in left valve. Ligament external, short, posterior to umbo (opisthodetic), moderate in size. Prodissoconch II 246 to 248 µm long ( paratype ). Soft tissue ( Fig. 11E, F ): Ctenidia narrow long, composed of outer and inner demibranches. Labial palps small, narrow, present anterior to foot. Mantle without tentacles, thin except for the posterior siphonal regions. Inhalant and exhalant siphons short, located at posterior end. Inhalant siphon muscular, tubular, longer than exhalant siphon ( Fig. 13 ). Evenly separated small papillae present on the base of the inhalant siphon ( Fig. 13D ). Pedal gape situated at the anteroventral position ( Fig. 13C ). Foot white, slender with the tip rounded ( Fig. 13C ). Digestive gland brownish, occupying nearly half of visceral mass ( Fig. 11E, F ). Anterior and posterior adductor muscles ovate in shape, with anterior smaller than posterior ( Fig. 11E, F ). Host: Bonellia sp. aff. minor ( Annelida : Thalassematidae : Bonelliinae ). Host association and biology: This bivalve species lives attached by byssal threads onto the burrow wall of Bo. sp. aff. minor in the dead coral rocks ( Figs 4B , 5 ). The live animals actively crawl away using their foot and extend their inhalant and exhalant siphons from the posterodorsal margin by slightly opening the shells.In the aquaria, the bivalve extends its short inhalant siphon against the host body trunk. Distribution: Only known from the type locality (Sabiura, Wakayama , Japan ). Epifauna: Dorsal marginal surface of the shells was often attached to by entoprocts ( Figs 4B , 11A–D ), whereas the lateral surface of the shells was often attached to by foraminiferans ( Figs 4B , 11D ). Figure 11. Basterotia bonelliphila (holotype NSMT-Mo 79470). A, B, Dorsal and ventral views. Anterior is right. C, D, External view of right and left valves. E, F, Internal view of right and left valves. The tip of the foot was removed for DNA analysis. G, H, Hinge structure of left and right valves. Abbreviations: aa, anterior adductor muscle; ac, anterior cardinal tooth; apa, anterior-venral pedal aperture; d, demibranches; dg, digestive gland; exl, external ligament; f, foot; lp, labial palps; pa, posterior adductor muscle; p2, prodissoconch II; s, exhalant and inhalant siphons. Scale bars = 1 mm (A–F), 100 µm (G, H). Etymology: The new species is named after its commensal association with the spoon worm Bonellia . Remarks: Species of Basterotia are known to inhabit the burrows of the thalassematin echiurans in sediment bottoms ( Anker et al. 2005 , Goto et al. 2011 , 2017 , Goto and Kato 2012 , Goto 2017 ). Basterotia bonelliphila is distinct among the genus with its small, elongate shells and in inhabiting the burrows of Bonellia (Bonelliinae) in the dead coral rocks ( Figs 4A , 5 ). Probably, its small shell size and elongate shell shape are adaptations to the Bonellia ’s narrow burrow. Some congeneric species [e.g. Basterotia sp. from Rodrigues Island in Oliver and Holmes (2004) ] and some species belonging to other basterotiin genera [e.g. Basterotina rectangularis Coan, 1999 and Ensitellops hertleini W.K. Emerson & Puffer, 1957 in Coan and Valentich-Scott (2012) ] have relatively similar elongate, small shells. Although the biology of these species remains unknown, they may also inhabit the narrow burrows of Bonellia or other echiurans in the hard substrata. The shells of Basterotina are different from those of Basterotia in having low, non-projecting hinge teeth ( Coan 1999 ), whereas the shells of Ensitellops are more elongate and possess a usual internal ligament ( Coan and Valentich-Scott 2012 , Huber 2015 ). The outline of this species changes from subtrapezoidal to subelliptical as it grows. Young individuals of Ba. bonelliphila (e.g. paratype , SL ~ 2.6 mm , Fig. 12 ) are relatively similar to the type of Basterotia subalata (Gatliff & Gabriel, 1910) (SL ~ 7.5 mm ) from southern Australia , the type of Basterotia corbuloidea (Dall, 1899) (SL ~ 6.5 mm ) from North Carolina, or Basterotia oblonga E.A. Smith, 1890 (SL ~ 8.5 mm ) from St. Helena in shell shape. However, the large individuals of Ba. bonelliphila are not similar to those species. Figure 12. Basterotia bonelliphila (paratype NSMT-Mo 79471). A, B, External view of right and left valves. C, D, Internal view of right and left valves. E, F, Hinge structure of right and left valves. G, H, Prodissoconch II of right and left valves. Abbreviations: ac, anterior cardinal tooth; exl, external ligament; p2, prodissoconch II. Scale bars = 1 mm (A–D), 100 µm (E–H). The siphons of Basterotia are often surrounded by numerous tentacles ( Goto et al. 2011 , 2017 ). However, Ba. bonelliphila lack such tentacles except for very short papillae ( Fig. 13D ). In Basterotia bivalves, small juveniles often attach to the ventral margin of larger individuals (e.g. Goto et al. 2011 ). However, we did not find such small individuals in this study. Our sampling was limited to early summer (June and July). Thus, the settlement of juveniles of this species may occur in different seasons.