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 10.1093/zoolinnean/zlad103 0024-4082 11240746 7F78BDE9-9589-4878-94EB-852F88C8B4C9 Leucothoe bonelliae Shimomura, Hirabayashi & Goto , sp. nov. (New Japanese Name: Bonelli-no-Maruhasami-Yokoebi) ( Figs 4C, D , 5 , 14–19 ) Zoobank registration: urn:lsid:zoobank.org:act: C7A2CCDE-9864-4CB7-9C03-BBFB0EF1C82D . Material examined: Holotype , male, 5.4 mm ( SMBL-V0661 ), Sabiura, Kushimoto, Wakayama Prefecture , obtained from Bo. sp. aff. minor , collected by I. Hirabayashi , 6 June 2020 . Figure 13. A living individual of Basterotia bonelliphila . A, Dorsal view of an individual opening its valves and extending its inhalant and exhalant siphons from the postero-dorsal margin. Posterior is left. B, Ventral view of an individual extending its inhalant siphon. Posterior is left. C, Ventral view of an individual extending its inhalant siphon and foot. Posterior is right. D, Close-up of the inhalant siphon. Arrowheads indicate the papillae on the base of the siphon. Scale bars = 1 mm. Abbreviations: exs, exhalant siphon; ins, inhalant siphon. Paratypes , 1 ovigerous female, 5.1 mm ( SMBL-V0662 ) , 1 male , 4.5 mm ( SMBL-V0663 ), 1 ovigerous female, 4.1 mm ( SMBL-V0664 ) , 1 male , 5.3 mm ( SMBL-V0665 ), 1 ovigerous female, 4.6 mm ( SMBL-V0666 ) , 1 female , 4.3mm ( SMBL-V0667 ), 1 non-ovigerous female, 4.0 mm ( SMBL-V0668 ) , 1 juvenile (sex unknown), 2.6 mm ( SMBL-V0669 ), collection data as for holotype . Diagnosis: Eyes small, not reaching to anterior end of coxa 1. Article 2 of mandibular palp 2 with 9 setae. Lacinia mobilis of right mandible with dentate surface. Epistome of upper lip with marginal setae. Coxa 1 with 2 setae. Palm of propodus with 3 or 4 distal robust setae. Carpus of gnathopod 2 distally truncate, expanded; propodus mediofacial setal row displaced below midline. Bases of pereopods 5–7 posteriorly tapered. Epimeron 1 without setae. Telson apex moderately blunt, dorsally with 2 pairs of plumose setae. Description of the holotype male: Head ( Fig. 14A ). Anterior margin rounded, anterodistal margin evenly rounded; ventral cephalic keel anterior margin excavate, anteroventral margin subquadrate, ventral margin straight. Eyes ( Fig. 14A ) with more than 30 ommatidia, round. Epimerons 1–3 ( Fig. 14A, B ) bare, posteriorly pointed. Telson ( Fig. 14C, D ) 2.4 times as long as maximum width, with 2 setae subapically; apex moderately blunt. Antenna 1 ( Fig. 14A, E ) 0.2 times as long as body length: flagellum 6-articulate, each with 1 aesthetascs; peduncle article 1 1.8 times as wide as article 2; accessory flagellum absent. Antenna 2 ( Fig. 14A, F ) 0.2 times as long as body length, subequal in length with antenna 1; flagellum 3-articulate. Upper lip ( Fig. 15A ) asymmetrically lobate; anterior margin setose; epistome with marginal setae. Left mandible ( Fig. 15B ) with 18 raker spines: incisor strongly dentate; palp ratio of articles 1–3 1.0: 2.4: 1.0; article 3 with 2 distal setae; lacinia mobilis large, strongly toothed. Right mandible ( Fig. 13C ) with 15 raker spines; incisor strongly dentate; lacinia mobilis small, with dentate surface. Lower lip ( Fig. 15F ) inner lobes fused, with facial setae; outer lobes with moderate gape; anterior margin setose. Maxilla 1 ( Fig. 15D ): palp 2-articulate with 4 distal setae; outer plate with 7 distal robust setae and 4 distal slender setae. Maxilla 2 ( Fig. 15E ): inner plate with 7 robust distal setae and many fine marginal setae; outer plate with 3 robust distal setae, 1 slender distal setae and many fine setae. Figure 14. Leucothoe bonelliae holotype (SMBL-V0661): (A) habitus, lateral; (B) pereonites 5–7, coxal plates 5–7 and pleonites 1–3, lateral; (C) telson, dorsal; (D) apical part of telson, dorsal; (E) left antenna 1, lateral; (F) left antenna 2, lateral. Scale bars = 100 µm. Figure 15. Leucothoe bonelliae holotype (SMBL-V0661): (A) upper lip, dorsal; (B) left mandible, dorsal; (C) right mandible, dorsal; (D) left maxilla 1, ventral; (E) left maxilla 2, ventral; (F) lower lip, dorsal; (G) right maxilliped, dorsal. Scale bar = 100 µm. Figure 16. Leucothoe bonelliae : (A) holotype (SMBL-V0661), (B) paratype (SMBL-V0662), (C) paratype (SMBL-V0663): (A–C) left gnathopod 1, lateral. Scale bar = 100 µm. Figure 17. Leucothoe bonelliae : (A, B) holotype (SMBL-V0661), (C, D) paratype SMBL-V0662: (A) left gnathopod 2, medial; (B) left gnathopod 2, lateral, omitted setae; (C) left gnathopod 2, medial; (D) left gnathopod, 2, lateral, omitted setae. Scale bar = 100 µm. Figure 18. Leucothoe bonelliae holotype (SMBL-V0661): (A) left pereopod 3, lateral; (B) left pereopod 4, lateral; (C) left pereopod 5, lateral; (D) left pereopod 6, lateral; (E) left pereopod 7, lateral. Scale bar = 100 µm. Figure 19. Leucothoe bonelliae holotype (SMBL-V0661): (A) left pleopod 1, dorsal, omitted plumose setae; (B) left pleopod 2, dorsal, omitted plumose setae; (C) left pleopod 3, dorsal, omitted plumose setae; (D) left uropod 1, lateral; (E) left uropod 2, lateral; (F) left uropod 3, lateral. Scale = 100 µm. Maxilliped ( Fig. 15G ): inner plate with 1 long and 1 short robust setae distally; distal margin with v-shaped indentation; inner margin of outer plate smooth, reaching half of palp article 1, distally with 2 short robust setae; article 4 of palp shorter than article 3. Coxae 1–4 ( Fig. 14A ) relative width 1.0: 1.3: 0.9: 1.3. Gnathopod 1 ( Figs 14A , 16A ): coxa smooth, with 2 long, medial facial setae and some tiny marginal setae: anterolateral margin produced, subquadrate; distal margin straight; posterior margin excavate; basis proximally winded; anterior margin with 7 short setae; posterior margin bare; ischium bare; merus with 1 long and 1 short setae distally; carpus linear, 3.3 times as long as wide; proximal margin dentate; distal margin with 3 short setae; propodus straight; palm dentate, with 4 distal robust setae; dactylus smooth, reaching 0.25 of propodus length. Gnathopod 2 ( Figs 14A , 17A, B ): coxa smooth, with some tiny marginal setae, without facial setae, broader than long, subequal to coxa 4, anterodistally rounded; distal margin straight; posterior margin weakly excavate; basis proximally winded, without anterodistal tubercles; anterior margin 9 short and long setae; posterior margin with 1 short distal seta; ischium with 1 anterior, 1 posteriordistal and 2 mediodistal setae; merus with 9 mediodistal setae; carpus half of propodus length, curved, distally with excavation, expanded; anterior margin dentate; propodus with mediofacial setal row displaced below midline; posterior margin smooth; palm convex, with 4 major tubercles; dactylus curved; proximal margin smooth, bare; anterior margin distally, subacute, reaching 0.6 of propodus length. Pereopod 3 ( Figs 14A , 18A ): coxa 1.3 times as long as wide, without facial setae; anterodistal corner overriding distal face of coxa 2, extending below it, smooth, with tiny marginal setae; anterior margin convex; distal margin oblique; posterior margin straight; basis with tiny marginal setae; ischium with 1 posterior distal seta; merus 3.7 times as long as ischium; carpus 0.6 times as long as merus; propodus with 4 robust setae posteriorly; dactylus curved. Pereopod 4 ( Figs 14A , 18B ) without facial setae: coxa with tiny marginal setae; anterior margin produced; distal margin evenly rounded; posterior margin excavate; basis–dactylus similar to ones of pereopod 3 in shape. Pereopods 5–7 ( Figs 14A, B , 18C–E ): coxae without facial setae; bases posteriorly tapered; width length rations 1: 1.2, 1: 1.2, 1: 1.3; posterior margins smooth, setose; bases–dactyli similar in shape. Pleopods 1–3 ( Fig. 19A–C ) relative lengths 1.0: 1.0: 0.9. Pleopods1 and 2 ( Fig.19A,B ) with2 coupling hooks mediodistally, respectively; pleopod 3 ( Fig. 19C ) without coupling hooks. Uropods 1–3 ( Fig. 19D–F ) relative lengths 1.0: 0.8: 0.9. Uropod 1 ( Fig. 19D ): peduncle 1.1 times as long as outer ramus, with 8 robust setae; inner ramus with 3 robust setae; outer ramus with 4 robust setae. Uropod 2 ( Fig. 19E ): peduncle 1.2 times as long as inner ramus, with 2 robust setae; outer ramus 0.8 times as long as inner ramus; inner ramus with 1 robust seta; outer ramus with 2 robust setae. Uropod 3 ( Fig. 19F ): peduncle 1.9 times as long as inner ramus, with 2 robust setae; outer ramus 0.9 times as long as inner ramus; inner and outer rami each with 2 robust setae. Description of the paratype female (SMBL-V0662) Gnathopod 1 ( Fig. 16B ): anterior margin of basis with 5 short seta; distal margin of carpus 3 short setae; palm of propodus with 4 robust setae distally. Gnathopod 2 ( Fig. 17C, D ): anterior margin with 6 short and 3 long setae; distal end of carpus without excavation; palm of propodus with smaller tubercles. Variation: Some variation was recognized in the number of setae on gnathopod 1 ( Fig. 16C ) and telson; palm of propodus of gnathopod 1 with 3 or 4 robust setae distally; apex of telson with 2 or 3 setae. Colour in life: Body has a light brown ‘saddleback’ colour pattern with a deep red dot on coxa 4. Anterior body white. A pair of small orangish dots present laterally on pereon 1, 2 and dorsally on pereon 2, 3, 4. Eyes bright pink. Antenna 1 reddish brown with a distal white band on peduncular article 2. Antenna 2 reddish brown with a distal white band on peduncular article 4, but small specimens lack bands on antenna 2. Etymology: The new species is named after its commensal association with the spoon worm Bonellia . Remarks: Leucothoe bonelliae is close to Leucothoe vulgaris from Okinawa , Amami-Oshima and Yakushima Islands, Japan , with which it shares a setose epistome, an antenna 1 lacking an accessory flagellum, coxae 1–7 without facial setae, a dentate posterior margin of gnathopod 1, 4 tubercles on palm of propodus of gnathopod 2, a dentate surface on right mandible and a body with a ‘saddleback’ colour pattern. Leucothoe bonelliae is distinguished from L. vulgaris by the following features (those of L. vulgaris in parentheses): eyes small, not reaching to anterior margin of coxa 1 (large, reaching to anterior margin of coxa 1); telson dorsally with 2 pairs of plumose setae (without setae); apex of telson moderately blunt (strongly pointed); palm of gnathopod 1 propodus with 3 or 4 distal robust setae (6 setae); article 2 of mandibular palp with 9 setae (15 setae); antennae reddish brown with a distal white band (yellow without band); and a ‘saddleback’ colour pattern to the body of light brown (red); and small orangish dots present on pereon 1–4 present (absent). In our phylogenetic analysis, L. bonelliae is most closely related to L. vermicola ( Fig. 9 ), which was recently described by Kodama et al. (2022) as a new species closely related to L. vulgaris . However, L. bonelliae and L. vermicola are clearly separated both by nuclear and mitochondrial genes (see Results). In addition, L. bonelliae is distinguished from L. vermicola by the following features (those of L. vermicola in parentheses): maxilla 1 palp with two distinct (one article with indistinct transverse line); telson dorsally with 2 pairs of plumose setae (several short simple setae); antennae reddish brown (red); ‘saddleback’ colour pattern of body light brown (reddish purple); and a white snowflake colour pattern covering the body absent (present).