A new species of Fibularia from Japanese waters with a redescription of F. japonica and F. ovulum (Echinodermata: Echinoidea: Clypeasteroida) Author Tanaka, Hayate Author Wakabayashi, Kaori Author Fujita, Toshihiko text Zootaxa 2019 2019-01-07 4543 2 241 260 journal article 27704 10.11646/zootaxa.4543.2.4 c828ed56-5b75-4093-afdf-994576a03ccb 1175-5326 2617781 2A1736C7-FB28-4C8E-9954-B17BA60B6E57 Fibularia coffea sp. nov. [New Japanese name: Kohi-mame-uni] Figs. 3–8 ; Tables 1 , 2 ; Electronic Supplementary Table S1 . Non Fibularia japonica Shigei 1982 : 11 –16, figs. 1–48 (part). Non Fibularia plateia Schultz 2005 : 321 , fig. 603. Fibularia n. sp. “bean” Gomes & Mooi 2015 : poster presentation. Material examined. Holotype : NSMT E-10371, whole, with spines, Ayamaru Cape , Amami-Oshima Island , Kagoshima Prefecture , Japan ( 28°28′26″N , 129°43′09″E ), depth 1 m , snorkeling, coll. H. Tanaka , 23 Mar. 2015 . Paratypes : 1 specimen , NSMT E-10372, whole, denuded, SEM stub, Tsuchi-Hama , Amami-Oshima Island , Kagoshima Prefecture , Japan ( 28°24′36″N , 129°40′47″E ), depth 2 m , snorkeling, coll. H. Tanaka and L. Sakamoto, 20 Mar. 2015 ; 2 specimens , NSMT E-10373, whole, denuded, SEM stub, Kunigami , Nishinoomote city, Tanegashima Island , Kagoshima Prefecture , Japan ( 30°48′19″N , 131°01′24″E ), depth 4–5 m , scuba diving, coll. H. Yamasaki and R. Yoshida, 1 Mar. 2014 ; 1 specimen , NSMT E-10374, whole, denuded, SEM stub, Tateyama Bay , Tateyama city, Chiba Prefecture , Japan ( 34°58′56″N , 139°48′43″E ), depth 6.9–8.1 m , dredging, coll. Y. Yoshida , 14 Jan. 2015 ; 1 specimen , NSMT E-10375, whole, denuded, SEM stub, Tateyama Bay , Tateyama city, Chiba Prefecture , Japan ( 34°59′05″N , 139°48′57″E ), depth 9–12 m , dredging, coll. Y. Yoshida , 12 May. 2014 ; 1 specimen , NSMT E-10376, whole, denuded, SEM stub, Tateyama Bay , Tateyama city, Chiba Prefecture , Japan ( 34°58′40″N , 139°46′05″E ), depth 5 m , scuba diving, coll. K. Kosoba , 30 Aug. 2015 ; 29 specimens , NSMT E-10377, dead tests, Tomioka , Amakusa group, Kumamoto Prefecture , Japan , dredging, coll. H. Tanaka , 21 Mar. 2015 ; 1 specimen , NSMT E-10378, dead test, Ayamaru Cape , Amami-Oshima Island , Kagoshima Prefecture , Japan ( 28°28′30″N , 129°43′05″E ), beachcombing, coll. H. Tanaka , 23 Mar. 2015 ; 7 specimens , NSMT E-10379, dead tests, Ayamaru Cape , Amami-Oshima Island , Kagoshima Prefecture , Japan ( 28°28′30″N , 129°43′05″E ), beachcombing, coll. H. Arima , 11 Dec. 2013 – 27 Mar. 2014 ; 7 specimens , NSMT E-10380, dead tests, Kosyuku , Amami-Oshima Island , Kagoshima Prefecture , Japan ( 28°24′10″N , 129°28′04″E ), beachcombing, coll. H. Arima , 13 Dec. 2013 – 22 Mar. 2015 ; 2 specimens , NSMT E-10381, dead tests, Kosyuku , Amami-Oshima Island , Kagoshima Prefecture , Japan ( 28°24′10″N , 129°28′04″E ), beachcombing, coll. H. Tanaka , 22 Mar. 2015 ; 5 specimens , NSMT E-10382, dead tests, Tsuchi-Hama , Amami-Oshima Island , Kagoshima Prefecture , Japan ( 28°24′39″N , 129°40′37″E ), beachcombing, coll. H. Tanaka , 15 Jul. 2014 ; 3 specimens , NSMT E-10383, dead tests, Tsuyazaki , Fukutsu city, Fukuoka Prefecture , Japan ( 33°45′59″N , 130°23′03″E ), beachcombing, coll. K. Wakabayashi , 17 Jun. 2005 ; 10 specimens , NSMT E-10384, dead test, Wada Beach , Oi county , Fukui Prefecture , Japan ( 35°29′41″N , 135°34′32″E ), beachcombing, coll. H. Tanaka , 3 Jan. 2014 ; 4 specimens , NSMT E-10385, dead tests, Yoan Beach , Amami-Oshima Island , Kagoshima Prefecture , Japan ( 28°24′12″N , 129°38′35″E ), beachcombing, coll. H. Tanaka and L. Sakamoto, 31 Jan. 2016 ; 48 specimens , NSMT E-10386, dead tests, Zushi Beach , Zushi city, Kanagawa Prefecture , Japan ( 35°17′18″N , 139°34′25″E ), beachcombing, coll. H. Tanaka , 21 Jul. 2012 – 2 Feb. 2014 ; 2 specimens , NSMT E-10387, whole, denuded, Tsuchi-Hama , Amami-Oshima Island , Kagoshima Prefecture , Japan ( 28°24′36″N , 129°40′47″E ), intertidal, snorkeling, coll. H. Tanaka and L. Sakamoto, 24 Mar. 2015 ; 1 specimen , NSMT E-10388, whole, denuded, Tsuchi-Hama , Amami-Oshima Island , Kagoshima Prefecture , Japan ( 28°24′36″N , 129°40′47″E ), intertidal, snorkeling, coll. H. Tanaka and L. Sakamoto, 22 Oct. 2016 . One specimen, UMUTZ-Ecn-SG10-17T No. 7 (as a paratype of Fibularia japonica ), dead test, off Misaki Marine Biological Station, Sagami Bay, sublittoral zone, coll. K. Aoki, J. Deguchi, T. Sekimoto, H. Suzuki, and M. Shigei, 1926–1978 . GenBank accession number. LC388935 ( holotype : NSMT E-10371, Amami-Oshima Island , Kagoshima Prefecture , Japan ) , LC388934 ( paratype : NSMT E-10374, Tateyama Bay , Tateyama city, Chiba Prefecture , Japan ) . FIGURE 3. Fibularia coffea , paratype (NSMT E-10372, Amami-Oshima Island, Kagoshima Prefecture). A–C, SEM images of the test; A, aboral view; B, oral view; C, left lateral view; D–F, plate patterns of the test; D, aboral view; E, oral view; F, left lateral view. Pores of each pore pair are linked by fine dotted lines. Interambulacra are shaded. Abbreviations as in Fig. 2. TABLE 1. Allometric regressions of test measurements and test length (TL) analyzed by smatr in Fibularia coffea , F. japonica , and F. ovulum . See Figure 2 for the abbreviations of test measurements.

Parameter
Species	X	Y	intercept	slope	p	R 2	N
F. coffea	TL	TW (mm)	-0.1	1.0	<0.001	0.99	123
TH (mm)	-0.4	1.1	<0.001	0.96	123
PL (mm)	-0.4	1.3	<0.001	0.97	111
PW (mm)	-0.5	1.3	<0.001	0.96	112
SL (mm)	-0.5	0.8	<0.001	0.92	117
SW (mm)	-0.6	0.8	<0.001	0.92	116
S-A (mm)	-1.0	0.9	<0.001	0.79	118
AL (mm)	-0.9	1.0	<0.001	0.94	118
AW (mm)	-0.9	0.9	<0.001	0.94	116
A-Tp (mm)	-1.0	1.3	<0.001	0.94	119
F. japonica	TL	TW (mm)	-0.1	1.0	<0.001	0.97	102
TH (mm)	-0.2	1.0	<0.001	0.84	101
PL (mm)	-0.4	1.1	<0.001	0.84	102
PW (mm)	-0.5	1.1	<0.001	0.86	101
SL (mm)	-0.5	0.7	<0.001	0.83	97
SW (mm)	-0.5	0.7	<0.001	0.81	96
S-A (mm)	-1.0	0.9	<0.001	0.68	97
AL (mm)	-1.0	1.0	<0.001	0.86	97
AW (mm)	-0.8	0.8	<0.001	0.78	97
A-Tp (mm)	-1.0	1.4	<0.001	0.84	101
F. ovulum	TL	TW (mm)	-0.1	1.0	<0.001	0.99	78
TH (mm)	-0.2	1.1	<0.001	0.96	78
PL (mm)	-0.3	1.0	<0.001	0.97	78
PW (mm)	-0.4	1.1	<0.001	0.96	78
SL (mm)	-0.5	0.7	<0.001	0.88	78
SW (mm)	-0.6	0.7	<0.001	0.86	78
S-A (mm)	-1.0	0.9	<0.001	0.89	78
AL (mm)	-1.0	1.1	<0.001	0.92	78
AW (mm)	-0.8	0.9	<0.001	0.91	78
A-Tp (mm)	-1.4	1.7	<0.001	0.71	78

Diagnosis. Test outline elliptical when viewed from above; height low; oral surface slightly depressed toward the peristome. Periproct outline round square shaped. Petaloid region large; number of pores of petal III continues to increase with the test growth, reaching over 20 at TL> 5 mm . Diameter of genital pores equal to or smaller than that of petaloid pores in mature individuals. Two hydropores opening in an irregularly-shaped groove. Black pigments on each aboral perradius, forming symmetric pentaradial in living animals. Description. The test is very small (TL = 1.53–9.73 mm ) ( Fig. 3 ), flattened (TH/TL = 0.38–0.55) ( Fig. 3C ), elliptical when viewed from above (TW/TL = 0.67–0.86), and truncated posteriorly ( Figs. 3A, B ). The test proportion hardly changes with the test growth (slope value is 1.0 between TW and TL, and 1.1 between TH and TL in the allometry regression, Table 1 ). The oral surface is slightly depressed around the peristome. The aboral surface is slightly arched convex. There are no internal buttresses. Food grooves are absent ( Fig. 3B ). The ambulacra are almost the same width as the interambulacra ( Figs. 3 D–F). The height of both ambulacral and interambulacral plates are lower than the width at the ambitus ( Fig. 3F ). The petaloid region is large (PL/TL = 0.46–0.75, PW/TL = 0.33–0.61). The ratio of petaloid region size to test size becomes larger with test growth (slope value is 1.3 between PL and TL, as well as between PW and TL in the allometry regression). Each petal is composed of almost parallel series of pore pairs lying oblique, and crossing the ambulacral plates ( Fig. 3D ). The number of pores of petal III, IV, and V is continuously increasing up to 40, 28 and 36, respectively, with the test growth ( Fig. 4 ). The pores become larger towards the distal tip of the petals. FIGURE 4. Increase of pore number in petal III through growth in F. coffea , F. japonica , and F. ovulum . White circles indicate the specimens collected newly from Japanese waters in this study. Grey circles indicate type specimens ( F. japonica ) and specimens collected from Maldives ( F. ovulum ). Grey stars indicate holotype ( F. coffea and F. japonica ). X-mark in F. japonica indicates the paratype of F. japonica re-identified as F. coffea (UMUTZ-Ecn-SG10-17T No. 7). FIGURE 5. Fibularia coffea , SEM images of paratype (NSMT E-10372, Amami-Oshima Island, Kagoshima Prefecture). A, apical system; B, ambulacrum; C, tubercles; D, tubercles viewed obliquely. Abbreviations: gt = glassy tubercle, mt = miliary tubercle, pt = primary tubercle. Other abbreviations as in Fig. 2. The peristome, situated at the center of the oral side, is small (SL/TL = 0.17–0.34, SW/TW = 0.14–0.30) and slightly elongated antero-posteriorly ( Figs. 3B, E ). The ratio of peristome size to test size becomes smaller with the test grows (slope value is 0.8 between SL and TL, as well as between SW and TL in the allometry regression). The peristomial membrane lacks spine and pedicellariae. Two buccal pores are situated in each ambulacrum at the edge of the peristome. Single sphaeridium is fully enclosed within the test, and in the sphaeridial chamber in each ambulacrum near the peristome. The rounded square shaped periproct is located halfway between the peristome and posterior margin of the test and is smaller than the peristome (AL/TL = 0.08–0.15, AW/TW = 0.08–0.16) ( Figs. 3B, E ) and covered by 4–6 (mainly 5) naked radiating periproctal plates. The ratio of periproct size to test size hardly changes with the test grows (slope value is 1.0 between AL and TL, and 0.9 between AW and TL in the allometry regression). The apical system is situated slightly anterior on the aboral surface ( Figs. 3A, D ). It consists of four genital pores, five ocular pores in small ocular plates, and two hydropores in a deep, irregularly-shaped groove ( Fig. 5A ). The diameter of the genital pores (<150 µm) is equal to or smaller than that of the largest petaloid pore (<ca. 150 µm). There is no obvious dimorphism in gonopore size ( Fig. 6 ). The gonopores open in specimens as small as TL = 1.79 mm . The diameter of the ocular pores (ca. 40 µm) is much larger than that of the accessory pores (ca. 25 µm). Accessory pores are situated in oblique patches in the centers of ambulacral plates ( Fig. 5B ). FIGURE 6. Increase of gonopore diameter (GD) through growth in F. coffea , F. japonica , and F. ovulum . White circles indicate the specimens collected newly from Japanese waters in this study. Grey circles indicate type specimens ( F. japonica ) and specimens collected from Maldives ( F. ovulum ). Grey stars indicate holotype ( F. coffea and F. japonica ). The primary tubercles are hemispherical, crenulate, and perforate ( Figs. 5C, D ). The diameters of oral and aboral primary tubercles are almost equal, ca. 150–200 µm. Their mamelons are constricted at the base ( Fig. 5D ). The miliary tubercles are hemispherical, poorly to non-crenulate, and indistinctly to non-perforate ( Figs. 5C, D ). They scattered around the primary tubercles. The diameters of oral and aboral miliary tubercles are almost equal, ca. 50–60 µm. The glassy tubercles occur between primary and miliary tubercles ( Fig. 5C, D ). The primary spines are ca. 350–450 µm in length ( Fig. 7 Ai). The number of wedges in a primary spine is 8–10, and each wedge has many small granules and a series of distinct denticles ( Figs. 7 Aii, Aiii). The tip of each primary spine is somewhat truncated ( Fig. 7 Aii). The distal end of primary spines around the peristome is slightly curved towards the peristome, and their shafts are somewhat broadened and flattened ( Fig. 7B ). The miliary spines are ca. 250–350 µm in length ( Fig. 7 Ci). Each miliary spine bears a distal crown ( Fig. 7 Cii), and the number of wedges in a miliary spine is six for all examined spines. Each wedge has many small granules along its outer surface ( Fig. 7 Ciii). Two types of pedicellariae, ophicephalous and tridentate, are present ( Figs. 7D, E ). These two types pedicellariae occur on small tubercles similar to those of miliary spines. The ophicephalous pedicellariae ( Fig. 7D ) are numerous and occur over the entire test surface. The head is ca. 80–100 µm in length ( Fig. 7 Dii), and consists of three valves that differ from each other in size and shape. The largest valve has a large, bilaterally symmetric handle. The medium-sized valve has a left-right asymmetric handle. The smallest valve has a small, bilaterally symmetric handle. The left and right ends of each valve have a finger-like structure near the hinge ( Fig. 7 Dvi), making an “intertwined loop” ( Mooi 1990 ). The valves are connected to each other by these intertwined loops ( Figs. 7 Dii, Dv–Dvii). Each valve has 20–25 teeth, and each tooth has 1–2 denticles ( Fig. 7 Div). The proximal end of the handle on the largest valve is inserted into a depression at the distal end of the pedicellarial stalk ( Figs. 7 Di– Diii). The tridentate pedicellariae ( Fig. 7E ) occur only around the peristome and periproct. These pedicellariae consist of a head with three slender valves ( Fig. 7 Ei), short neck, and stem. The valves possess ca. 11–15 teeth on the edge and without denticles ( Figs. 7E ). Some valves have ca. 1–4 teeth in the inner area ( Figs. 7 Ei, Eii, Eiv). The accessory tube feet lack a calcareous disk or spicules. Color. The color is yellow to brown in life ( Figs. 8A, B ) but changes to green when preserved in ethanol. Black pigments are apparent in each ambulacrum along the pore pair columns, forming a pentaradially symmetric pattern on the aboral surface ( Figs. 8A, B ). The black pigments remain even after preservation in ethanol. The denuded test is whitish. Distribution. This species is recorded in Japanese waters from Sagami Bay to the Amami-Oshima Islands; 1– 12 m in depth (present study). Schultz (2005) recorded F. plateia from Queensland , Australia but the figured specimen seems to be F. coffea from the flattened test and the large number of pores of petals (the number of pores of petal III, IV and V are 32, 22 and 32, respectively). In addition, Gomez & Mooi (2015) recorded an unknown species Fibularia n. sp. “bean” from the Philippines and Micronesia that seems to be the same as F. coffea from the flattened test and the large number of pores of petals (the number of pores of petal III, IV and V are 34, 26 and 33, respectively; counted from the sketch image). Therefore, this species is considered to be widely distributed across the Indo-Pacific. Habitat. The micro-habitat of this new species is presumed to thin sand deposits directly on a hard substrate like rock-reefs. No living individual of this species was found in the sandy or muddy substrate around rock-reef although such substrates are inhabited by many species of clypeasteroids ( Mooi 1990 ). At Amami-Oshima Island, six live sea urchins (NSMT E-10371, E-10372, E-10373, and E-10387) were collected from the thinly deposited sand of 1–2 cm thick on a rock-reef ( Figs. 8C, D ). In addition, one live specimen (NSMT E-10388) was found in the thin accumulation of sand of ca. 1 cm in thickness trapped by branched calcareous algae on a vertical surface of a rock-reef. In Tateyama, one live F. coffea (NSMT E-10376) was also collected from a 1–2 cm thin sand layer on a rock-reef. Two sea urchins (NSMT E-10374 and NSMT E-10375) were collected by dredging from sediments containing rubble and stones where rock-reef and sand bottom are interfingering. TABLE 2. Tabular key to the species of Fibularia . See Figure 2C, D for the abbreviations of test measurements.

F. coffea	F. japonica	F. ovulum	F. plateia	F. nutriens	F. cribellum
TH/TL	0.38–0.60	0.49–0.80	0.59–0.84	ca. 0.38*	ca. 0.52*	ca. 0.43*
Dimorphism in GD	absent	present	absent	present	present	present
Total number of pores of petal III	up to 40	up to 14	up to 30	up to 7	petals rudimentary	up to 8
Peristome	slightly depressed	not depressed	not depressed	no data	slightly depressed	slightly depressed
No. of hydropores	2	2	2	1	1	2
Position of hydropores	in groove	in groove	in groove	directly on apical system	directly on apical system	in groove
References	this study	Shigei (1982), this study	A.M. Clark and Rowe (1971), this study	H.L. Clark (1928)	H.L. Clark (1909)	de Meijere (1904)

* These data were calculated by the authors based on the descriptions in each reference. FIGURE 7. Fibularia coffea , SEM images of holotype (NSMT E-10371, Amami-Oshima Island, Kagoshima Prefecture). A, primary spine from marginal of test (i, whole; ii, distal end; iii, proximal end); B, primary spine around peristome (i, whole viewed from peristomial side; ii, whole viewed towards peristome); C, miliary spine from marginal of test (i, whole; ii, distal end; iii, proximal end); D, ophicephalous pedicellariae (i, whole; ii, head; iii, tip of stem; iv, enlarged view of peripheral teeth; v, enlarged view of junction between valves; vi, enlarged view of looped structure near hinge of valves; vii, enlarged view of projection at the junction. White arrow head indicates the opening of the looped structure, black arrow heads indicate the projection); E, tridentate pedicellariae (i, head; ii–vi, internal view of valve). FIGURE 8. Live specimens and underwater photographs of collection sites of Fibularia coffea . A, holotype (NSMT E-10371); B, one of the paratypes (NSMT E-10376); C, collection site of holotype at 1 m depth, Ayamaru Cape, Amami-Oshima Island, Kagoshima Prefecture, Japan; D, collection site of one of the paratypes (NSMT E-10372) at 2 m depth, Tsuchi-Hama, Amami-Oshima Island, Kagoshima Prefecture, Japan. Dotted circles indicate the exact collection points. Etymology. The species name is derived from the Latin “ coffea ”, meaning “coffee”, because the elliptical outline of test and the brownish color of living specimens resemble coffee beans. Remarks. F. coffea can be easily distinguished from all other extant species of Fibularia except F. ovulum by the mode of increase of the number of pores in the petal. The number of pores in the petal III of F. coffea is greater than in F. japonica , F. plateia , F. cribellum , and F. nutriens , reaching 20 in specimens of TL> 5.0 mm and 30 in specimens of TL> 7.5 mm ( Fig. 4 ). On the other hand, the number of pores of petal III is up to 14 for F. japonica even in the specimens of TL> 7.5 mm ( Fig. 4 ), 7 for the holotype of F. plateia (TL = 6.25 mm ) ( H.L. Clark 1928 ), 8 or less for F. cribellum (TL = 6.0– 6.1 mm ) (de Meijere 1903; Schultz 2009 ). Moreover, the number of pores of petal III of F. coffea continues to increase even after TL = 5.0 mm ( Fig. 4 ). In contrast, in F. japonica , F. plateia , F. cribellum and F. nutriens , increase in pore pair number significantly slows down at TL = ca. 3.0 mm and almost stops after TL = ca. 4.0 mm ( Fig. 4 ) ( Gomez & Mooi 2015 ). F. ovulum is the most similar species to F. coffea . The number of pores of petal III of F. ovulum increases like in F. coffea below TL = 5.0 mm. However, in F. ovulum , that increase slows down above 5.0 mm TL, and only a maximum of 30 pores is reached in the largest specimens studied ( 9.45 mm TL). In F. coffea , that increase continues, up to 40 ( Fig. 4 ). F. coffea can be more clearly distinguished from F. ovulum by its lower (TH/TL = 0.38–0.55 in F. coffea vs. 0.59–0.84 in F. ovulum ) and less wide test (TW/TL = 0.67–0.86 in F. coffea vs. 0.77–0.92 in F. ovulum ). The difference in these proportions of the test is consistent throughout their growth (slope value is 1.0 and 1.0 between TW and TL, and 1.1 and 1.1 between TH and TL in the allometry regression for F. coffea and F. ovulum ), so it is more useful for identification between two species. Moreover, F. coffea can be distinguished by the larger peristome (SL/TL = 0.17–0.34 in F. coffea vs. 0.12–0.24 in F. ovulum ; SW/TL = 0.14–0.30 in F. coffea vs. 0.11–0.23 in F. ovulum ). In addition, the area around the peristome is depressed in F. coffea but inflated in F. ovulum . In life, F. coffea can be distinguished from F. ovulum by its coloration: the former has black pigment on the aboral surface ( Fig. 7A, B ), and the latter lacks this pigment and usually has purplish accessory tube feet ( Mortensen 1948 ).