Martynov A et al. (2015), When Ontogeny Matters: A New Japanese Species o...

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PLoS One 2015 Jan 01;1010:e0139463. doi: 10.1371/journal.pone.0139463.

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When Ontogeny Matters: A New Japanese Species of Brittle Star Illustrates the Importance of Considering both Adult and Juvenile Characters in Taxonomic Practice.

Martynov A , Ishida Y , Irimura S , Tajiri R , O'Hara T , Fujita T .

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Current taxonomy offers numerous approaches and methods for species delimitation and description. However, most of them are based on the adult characters and rarely suggest a dynamic representation of developmental transformations of taxonomically important features. Here we show how the underestimation of ontogenetic changes may result in long term lack of recognition of a new species of one of the most common ophiacanthid brittle stars (Echinodermata: Ophiuroidea) from the North Pacific. Based on vast material collected predominantly by various Japanese expeditions in the course of more than 50 years, and thorough study of appropriate type material, we revise the complex of three common species of the ophiuroid genus Ophiacantha which have been persistently confused with each other. The present study thus reveals the previously unrecognized new species Ophiacantha kokusai sp.nov. which is commonly distributed off the Pacific coast of Japan. The new species shows developmental differentiation from the closely related species Ophiacantha rhachophora H. L. Clark, 1911 and retains clearly expressed early juvenile features in the adult morphology. Another species, Ophiacantha clypeata Kyte, 1977, which had been separated from O. rhachophora, is in turn shown to be just a juvenile stage of another North Pacific species, Ophiacantha trachybactra H.L. Clark, 1911. For every species, detailed morphological data from both adult and juvenile specimens based on scanning electron microscopy are presented. A special grinding method showing complex internal features has been utilized for the first time. For all three species in this complex, a clear bathymetric differentiation is revealed: O. rhachophora predominantly inhabits shallow waters, 0-250 m, the new species O. kokusai lives deeper, at 250-600 m, and the third species, O. trachybactra, is found at 500-2,000 m. The present case clearly highlights the importance of considering developmental transformations, not only for a limited number of model organisms, but as part of the taxonomic process.

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Species referenced: Echinodermata
Genes referenced: LOC100887844 LOC105444561 LOC115919910 LOC115925415 LOC579609 LOC763415

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	Fig 1. Ophiacantha kokusai sp.nov., holotype NSMT E–3188 from Owase Trough, Kii Peninsula, 5.1 mm dd, external views. A, dorsal view; B, ventral view; C, proximal arm segments, dorsal view; D, proximal arm segments, ventral view; E, proximal arm segments, lateral view, SEM; F, oral frame, details. ap, adoral shield papilla; as, adoral shields; gs, genital slit; j, jaws; op, oral papillae; os, oral shield. Scale bars, 0.5 mm (E), 1 mm (A, C, D), 0.2 mm (B, F).
	Fig 2. Adult disk spines and oral frames of Ophiacantha kokusai sp.nov. (A–B, holotype), Ophiacantha rhachophora H.L. Clark, 1911 (C–D, NSMT E–1540) and Ophiacantha trachybactra H.L. Clark, 1911 (E–F, NSMT E–7543). SEM of uncoated specimens using Keyence VHX-D510. ap, adoral shield papillae; as, adoral shields; dp, dental plate; gs, genital slit; j, jaws; op, oral papillae; os, oral shield; th, teeth; red asterisks indicate absence of the adoral shield papillae in adult O. rhachophora and O. trachybactra. Scales bars, 0.1 mm.
	Fig 3. Ophiacantha kokusai sp.nov., holotype NSMT E–3188, details, SEM. A–N, proximal segments. A, lateral arm plate; B, same, inside view; C, ventral arm plate; D, dorsal spine; E, arm spine articulations; F, spine, ventral view; G, hollow dorsal spine, transversally sectioned at basal part; H, hollow dorsal spine, mid transverse section; I, ventral spine; J, ventral spine mid-section showing small cavities; K, vertebra, dorsal view; L, same, ventral view; M, same, distal view; N, same, proximal view; O–T, middle segments. O–P, lateral arm plates showing no protuberances; Q, arm spine articulations; R, vertebra, dorsal view; S, same, distal view; T, ventral arm plate. vc, vertebral condyle on proximal vertebrae; red asterisk indicates the absence of vertebral condyle on more distal vertebrae. Scales bars, 0.05 (G, J, Q), 0.1 mm (C, E, F, H, I, M–O, P–T), 0.2 mm (A, B, K, L), 0.5 mm (D).
	Fig 4. Ophiacantha kokusai sp.nov., paratype NSMT E–7638 from Sagami Bay, internal structures of entire specimen uncovered using the grinding method. A,D, dorsalmost sections; B,E, middle sections; C,F, ventralmost sections. dp, dental plate; g, gonads; gp, genital plates; j, jaws; lap, lateral arm plates; op, oral papillae; rs, radial shields; s, spines; vt, vertebrae. Scale bars, 1 mm.
	Fig 5. Ophiacantha kokusai sp.nov., paratype NSMT E–7596 from Sagami Bay, 4.5 mm dd, external views and details, SEM. A, dorsal view; B, ventral view; C,D, thorny adoral shield papilla with central spine and numerous fine thorns; E, dental plates; F, dorsal spine; G, third lateral arm plate (first free proximal segment) closely adjacent to the disk showing striated elevation near articulations; H, arm spine articulations; I, proximal vertebra, dorsal view; J, middle vertebra, dorsal view; K, proximal vertebra, distal view; Scales bars, 0.05 (I), 0.1 mm (C, D, E, F, G, H, J, K), 1 mm (A, B). ap, adoral shield papilla; as, adoral shields; gs, genital slit; op, oral papillae; os, oral shield; vc, vertebral condyle of proximal vertebrae (zygospondylous articulation).
	Fig 6. Comparison of the oral frame patterns in O. rhachophora H.L. Clark 1911 and O. kokusai sp. nov. and (specimen NSMT E–1540 and paratype NSMT E–7638 respectively) using the grinding method technique. A–C, three consecutive sections of the disk of O. rhachophora showing placement of only three oral papillae (including distalmost one) emerging exclusively from the jaws; D–F, three consecutive sections of the disk of O. kokusai sp.nov. showing placement of three oral papillae emerging from jaws and a fourth separate thorny papilla emerging from the adoral shield. ap, adoral shield papillae; as, adoral shields; dp, dental plate; gs, genital slit; j, jaws; op, oral papillae; os, oral shield; th, teeth; red asterisks indicate the absence of the adoral shield papillae in O. rhachophora (A–C). Scale bars, 1 mm.
	Fig 7. (A–D) Mean annual temperatures for the waters off Northern Honshū and Hokkaido (A), central Honshū (B), Southern Honshū and Shikoku (C), Okinawa (D). On each figure the left image represents mean annual temperature values at the depth of 300 m (upper value in each cell; lower value in each cell–number of years with measurements) and the right image represents annual water temperature at different depth horizons for particular locality (corresponding to particular cells in the red frame). (E) Mean annual temperatures for May off the central Honshū. (F) Mean annual temperatures for May off Okinawa.Same figure designations as for (A–D). Data compiled from the Japan Oceanographic Data Center portal (http://www.jodc.go.jp/index.html).

	Fig 9. Ophiacantha rhachophora H.L. Clark, 1911, holotype USNM 25630 from Gotō Islands (ca. 100 km W to Nagasaki Prefecture), 5.6 mm dd, external views. A, dorsal view; B, ventral view; C, proximal arm segments, dorsal view; D, proximal arm segments, ventral view; E, proximal arm segments, lateral view, SEM; F, oral frame, details. as, adoral shields; gs, genital slit; j, jaws; op, oral papillae; os, oral shield; red asterisks indicate the former position of the adoral shield papillae during early ontogeny (i.e. absence of the distalmost oral papillae at the adoral shields in adult state). Scales bars, 1 mm (A–F).
	Fig 10. Ophiacantha rhachophora H.L. Clark, 1911, holotype USNM 25630, 5.6 mm dd, details, SEM. A–L, proximal segments. A, lateral arm plate; B, same, inside view; C, ventral arm plate; D, dorsal spine; E, arm spine articulations; F, spine, ventral view; G, hollow dorsal spine, transversally sectioned at middle part; H, ventral spine; I, vertebra, dorsal view; J, same, ventral view; K, same, distal view; L, same, proximal view; M–R, middle segments. M–N, lateral arm plates showing spine-like protuberance; O, arm spine articulations; P, vertebra, dorsal view; Q, same, distal view; R, ventral arm plate. Red asterisks indicate the absence of the vertebral condyle (streptospondylous articulation) on both proximal and distal vertebrae. Scales bars, 0.05 mm (E, F, Q), 0.1 mm (A–C, G, H, J, K–R), 0.2 mm (D, I).
	Fig 11. Ophiacantha rhachophora H.L. Clark, 1911, NSMT E–7614 from Sagami Bay, 4.5 mm dd, external views and details, SEM. A, dorsal view; B, ventral view; C,D, lobed, not thorny, distalmost oral papilla placed on the jaw instead of adoral shield; E, F, dental plates; G, third lateral arm plate (first free proximal segment) closely adjacent to the disk showing no striated elevation near articulations; H, arm spine articulations; I, proximal vertebra, dorsal view; J, middle vertebra, dorsal view; K, proximal vertebra, distal view. as, adoral shields; op, oral papillae; gs, genital slit; j, jaws; op, oral papillae; os, oral shield; red asterisk indicates the absence of the vertebral condyle (streptospondylous articulation) on proximal vertebrae. Scales bars, 0.1 mm (C, D, G–K); 0.2 mm (E, F), 1 mm (A, B).
	Fig 12. Ophiacantha clypeata Kyte, 1977 (new synonym of O. trachybactra H.L. Clark, 1911), type material, external views. A, holotype USNM 26241 from Bowers Bank, Bering Sea, 5.2 mm dd, dorsal view; B, same, ventral view; C, paratype USNM 26698 from Bowers Bank, Bering Sea, 6.5 mm dd, dorsal view; D, same, ventral view; E, proximal arm segments, lateral view, SEM; F, proximal arm segments, lateral view, details, SEM. ap, adoral shield papillae; as, adoral shields; gs, genital slit; j, jaws; op, oral papillae; os, oral shield; red asterisks indicate the absence of the adoral shield papillae. Scales bars, 0.5 mm (F), 1 mm (A–E).
	Fig 13. Ophiacantha clypeata Kyte, 1977 (new synonym of O. trachybactra H.L. Clark, 1911), details of the paratype USNM 26698, middle segments, SEM. A, lateral arm plate; B, same, inside view; C, ventral arm plate; D, dorsal spine; E, arm spine articulations; F, spine, ventral view; G, dorsal spine, transversely sectioned at the base showing a single large cavity; H, dorsal spine, transversely sectioned in the middle showing several small cavities; I, ventral spine; J, vertebra, dorsal view; K, same, ventral view; L, same, distal view; M, same, proximal view. Red asterisk indicates the absence of vertebral condyle (streptospondylous articulation) throughout the arms. Scales bars, 0.05 mm (G), 0.1 mm (E, F, I–M), 0.2 mm (A–D).
	Fig 14. Ophiacantha trachybactra H.L. Clark, 1911, type material, external views. A, holotype USNM 25649, 12.7 mm dd, off Cape Terpeniya, Sakhalin Id., Okhotsk Sea, dorsal view; B, same, ventral view; C, paratype USNM 25694, Shumagin Bank, Alaska, 7.2 mm dd, dorsal view; D, same, ventral view; E, same, proximal arm segments, dorsal view; F, same, latero-ventral view, SEM. as, adoral shields; gs, genital slit; j, jaws; op, oral papillae; os, oral shield; red asterisks indicate the absence of the adoral shield papillae. Scales bars, 0.5 mm (F), 1 mm (A–E).
	Fig 15. Ophiacantha trachybactra H.L. Clark, 1911, details of the paratype USNM 25694, details, middle segments, SEM. A, lateral arm plate; B, same, inside view; C, ventral arm plate; D, dorsal spine; E, arm spine articulations; F, spine, ventral view; G, dorsal spine, transversely sectioned at the base showing a single large cavity; H, dorsal spine, transversely sectioned in the middle showing several small cavities; I, ventral spine; J, vertebra, dorsal view; K, same, ventral view; L, same, distal view; M, same, proximal view. Red asterisk indicates the absence of the vertebral condyle (streptospondylous articulation) throughout the arms. Scales bars, 0.05 mm (H), 0.1 mm (C, E, F, G, I), 0.2 mm (A, B, D, J–M).
	Fig 16. Ophiacantha trachybactra H.L. Clark, 1911, adult specimen 10.9 mm disk diameter NSMT E–7557, sta. KT-93-15 (M 3), off Sanriku, northern Honshū, external views. A, dorsal view; B, ventral view; C, proximal arm segments, dorsal view; D, proximal arm segments, ventral view; E, proximal arm segments, ventral view, SEM; F, proximal arm segments, ventral view, details, SEM. as, adoral shields; gs, genital slit; j, jaws; op, oral papillae; os, oral shield; red asterisks indicate the absence of the adoral shield papillae. Scales bars, 0.5 mm (F), 1 mm (A–E).
	Fig 17. Ophiacantha trachybactra H.L. Clark, 1911, adult specimen 10.9 mm disk diameter NSMT E–7557, sta. KT-93-15 (M 3), off Sanriku, northern Honshū, details, SEM. A–N, proximal segments. A, lateral arm plate; B, same, inside view; C, ventral arm plate; D, dorsal spine; E, arm spine articulations; F, spine, ventral view; G, dorsal spine, transversely sectioned at the base showing a single large cavity; H, dorsal spine, transversely sectioned in the middle showing several small cavities; I, ventral spine; J, ventral spine sectioned in the middle showing small cavities; K, vertebra, dorsal view; L, same, ventral view; M, same, distal view; N, same, proximal view; O–T, middle segments. O–P, lateral arm plates showing no additional protuberance; Q, arm spine articulations; R, vertebra, dorsal view; S, same, distal view; T, ventral arm plate. Red asterisks indicate the absence of the vertebral condyle (streptospondylous articulation) throughout arms. Scales bars, 0.05 mm (F), 0.1 mm (C, E, G, H, I, J, Q, T), 0.2 mm (A, B, K, L, M, N, O, P, R, S), 0.5 mm (D).
	Fig 18. Ophiacantha trachybactra H.L. Clark, 1911, subadult specimen 6.8 mm disk diameter NSMT E–7557, sta. KT-93-15 (M 3), off Sanriku, northern Honshū, external views. A, dorsal view; B, ventral view; C, proximal arm segments, dorsal view; D, proximal arm segments, ventral view; E, proximal arm segments, ventral view, SEM; F, proximal arm segments, ventral view, details, SEM. as, adoral shields; gs, genital slit; j, jaws; op, oral papillae; os, oral shield; red asterisks indicate the absence of the adoral shield papillae. Scales bars, 0.5 mm (F), 1 mm (A–E).
	Fig 19. Ophiacantha trachybactra H.L. Clark, 1911, subadult specimen 6.8 mm disk diameter NSMT E–7557, sta. KT-93-15 (M 3), off Sanriku, northern Honshū, details, SEM. A–M, proximal segments. A, lateral arm plate; B, same, inside view; C, ventral arm plate; D, dorsal spine; E, arm spine articulations; F, spine, ventral view; G, dorsal spine, transversely sectioned at the base showing a single large cavity; H, dorsal spine, transversely sectioned in the middle showing several small cavities; I, ventral spine; J, vertebra, dorsal view; K, same, ventral view; L, same, distal view; M, same, proximal view; N–T, middle segments. N,O, lateral arm plates showing no additional protuberance; P, arm spine articulations; Q, vertebra, dorsal view; R, same, distal view; S, ventral arm plate. Red asterisks indicate the absence of the vertebral condyle (streptospondylous articulation) throughout the arms. Scales bars, 0.05 mm (F, G, H), 0.1 mm (A, B, C, E, I–S), 0.2 mm (D).
	Fig 20. Main stages of the development of Ophiura leptoctenia H.L. Clark, 1911 (family Ophiuridae), a series from the locality in Okhotsk Sea (sta. 79). A, C, E, development of the dorsal disk characters. A, adult specimen, 10 mm disk diameter, primary plates occupy a restricted area within the disk (ZMMU D–1051); C, juvenile specimen, 2 mm disk diameter, primary plates occupy a considerable area of the disk (ZMMU D–1051), SEM; E, early postlarval specimen, 1 mm disk diameter, primary plates occupy whole dorsal disk area (ZMMU D–1051), SEM; B, D, F, development of the ventral oral characters, SEM. B, adult specimen, 10 mm disk diameter, all oral papillae are spiniform, 2–3 adoral shield papillae; D, juvenile specimen, 2 mm disk diameter, both spiniform and block-shaped oral papillae present, 2 pairs of adoral shield papillae; F, early postlarval specimen, 1 mm disk diameter, only pair of block-shaped oral papillae present, and pair of adoral shield papillae. ap, adoral shield papillae; as, adoral shields; cpp, central primary plate; dp, dental plate; j, jaws; rpp, radial primary plates; op, oral papillae; os, oral shield; th, teeth. Scales bars, 0.1 mm (E, F), 0.3 mm (B, D), 1 mm (C), 5 mm (A).
	Fig 21. Main stages of the development of Amphiodia craterodmeta H.L. Clark, 1911 (family Amphiuridae), a series from the locality in Okhotsk Sea (sta. 37), SEM. A, C, E, development of the dorsal disk characters. A, adult specimen, 5 mm disk diameter, primary plates occupy a restricted area of the disk (ZMMU D–1116); C, juvenile specimen, 2 mm disk diameter, primary plates occupy a considerable area of the disk (ZMMU D–1116); E, early postlarval specimen, 1 mm disk diameter, primary plates occupy major part of the dorsal disk area (ZMMU D–1116); B, D, F, development of the ventral oral characters. B, adult specimen, 5 mm disk diameter, all oral papillae are rounded to pointed, no adoral shield papillae; D, juvenile specimen, 2 mm disk diameter, all oral papillae are rounded to pointed, no adoral shield papillae; F, early postlarval specimen, 1 mm disk diameter, both pointed and block-shaped oral papillae present, pair of adoral shield papillae. ap, adoral shield papillae; as, adoral shields; cpp, central primary plate; dp, dental plate; j, jaws; rpp, radial primary plates; op, oral papillae; os, oral shield; th, teeth; red asterisk on the Fig 20A indicates absence of the definite primary plates rosette, red asterisks on the Fig 20B–20F indicate absence of the adoral shield papllae. Scales bars, 0.1 mm (B, F), 0.3 mm (D, E), 1 mm (A, C).
	Fig 22. Adult and juvenile characters of Ophiacantha rhachophora H.L. Clark, 1911 and Ophiacantha kokusai sp.nov. (family Ophiacanthidae). A, C, E, Ophiacantha rhachophora. A, adult specimen, 4.5 mm disk diameter, dorsal view (NSMT E–7609); C, oral frame of adult specimen 4.6 mm disk diameter, lobed distal oral papilla is completely migrated from the adoral shield to the jaws (NSMT E–875), SEM; E, oral frame of early postlarval specimen, 0.9 mm disk diameter, distal papilla is thorny and attached to the adoral shield (NSMT E–7642), SEM; B, D, F, Ophiacantha kokusai sp. nov. B, adult specimen, 4 mm disk diameter (NSMT E–7641); D, oral frame of adult specimen, 4.2 mm disk diameter, thorny distal “oral” papilla is the adoral shield papilla and is attached to the adoral shield (NSMT E–7589), SEM; F, oral frame of early postlarval specimen, 0.5 mm disk diameter, distal papilla is thorny and attached to the adoral shield (NSMT E–7607), SEM. ap, adoral shield papillae; as, adoral shields; dp, dental plate; j, jaws; op, oral papillae; os, oral shield; th, teeth; red asterisks indicate absence of the adoral shield papillae in adult O. rhachophora. Scales bars, 0.1 mm (F, E), 0.2 mm (D), 0.5 mm (C), 2 mm (A, B).
	Fig 23. Adult and juvenile characters of Ophiacantha trachybactra H.L. Clark, 1911 and Ophiophthalmus normani (Lyman, 1879) (family Ophiacanthidae). A, C, E, Ophiacantha trachybactra. A, adult specimen, 9 mm disk diameter, dorsal view (NSMT E–7557); C, oral frame of adult specimen 9 mm disk diameter, distal oral papilla is completely detached from the adoral shield (NSMT E–7557), SEM; E, oral frame of juvenile specimen, 1.7 mm disk diameter, distal papilla is semi-detached from the adoral shield (NSMT E–7533), SEM; B, D, F, Ophiophthalmus normani. B, adult specimen, 10 mm disk diameter (NSMT E–2610); D, oral frame of the same specimen, distal oral papilla is completely detached from the adoral shield, SEM; F, oral frame of juvenile specimen 2 mm disk diameter, distal papilla is the adoral shield spine (ORI KT 90–08), SEM. ap, adoral shield papillae; as, adoral shields; dp, dental plate; gs, genital slit; j, jaws; op, oral papillae; os, oral shield; th, teeth; red asterisks indicate absence of the adoral shield papillae. Scales bars, 0.1 mm (E, F), 0.5 mm (C, D), 4 mm (A), 5 mm (B).

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