Choerodon margaritiferus Fowler and Bean, 1928

Miyamoto, Kei, Nonaka, Ai & Oka, Shin-Ichiro, 2015, Northernmost record of a poorly known tuskfish, Choerodon margaritiferus (Perciformes: Labridae), from southern Japan, and first description of a female, Zootaxa 4007 (1) : -

Choerodon margaritiferus Fowler and Bean, 1928

English name: Pearly Tuskfish

New standard Japanese name: Yuumodoro-bera Figs. 1 , 2 , 3 ; Table 1

Choerodon margaritiferus Fowler and Bean, 1928: 197 (type locality: Jolo market, Jolo, the Philippines); Parenti and Randall, 2000: 10 ( New Caledonia and the Philippines); Westneat, 2001: 3400 ( Philippines); Allen and Randall, 2002: 113 (the Philippines); Shea and Liu, 2010: Choerodon margaritiferus ( New Caledonia, Chesterfield Islands, and the Philippines); Allen and Erdmann, 2012: 646, unnumbered color photograph (the Philippines and Taiwan); Puckridge et al., 2015: 66 (Tanjung Luar, Lombok, Indonesia).

Choerodon sp. A: White et al., 2013: 266, pl. 89.19 (Tanjung Luar, Lombok, Indonesia).

Material examined. 5 specimens, 94.5–107.0 mm in standard length (SL), all from near Sesoko Island, Okinawa, southern Japan (26º39′N, 127 º51′E), 30 m depth, fishing by Y. Omata: OCF-P 20140825-3, female, 96.4 mm SL, 24 August 2014; OCF-P 20140827-1, male, 107.0 mm SL, 27 August 2014; OCF-P 20140827-2, 20140827-3 and 20140827-4, female, 94.5–103.0 mm SL, 27 August 2014.

Comparative material. Holotype of C. margaritiferus Fowler and Bean, 1928 : USNM 89966, male, 116.0 mm SL, Jolo market, Jolo, the Philippines, 11 February 1908.

Diagnosis. Distinguished from congeners by the following combination of characters: dorsal-fin rays XII, 8; scales between lateral line and 5th dorsal-fin spine 2 ½; lower pectoral-fin rays elongate; male brown or pale orange dorsally, with a blue or white stripe below eye continuing as a line of spots to upper pectoral-fin base, an additional stripe located dorsally on caudal-peduncle and below most of the dorsal-fin base, a white or blue bar on pectoral-fin base, and an eye-sized red blotch on back below base of 9th to 11th dorsal-fin spines (center of the blotch above lateral line); female orange dorsally, with a broad red band on posterior edge of caudal-fin.

Description. Counts and proportional measurements of 5 Okinawan specimens and holotype of C. margaritiferus are displayed in Table 1 . Body moderately slender, elongate, deepest at pectoral-fin base, depth 3.7– 4.0 (3.5) in SL; head large, length 2.6 (2.8) in SL; snout moderately short, slightly pointed, 3.3–3.6 (3.4) in head length (HL); eyes large, round, located along upper portion of anteroposterior axis, diameter 4.5–5.0 (4.9) in HL; mouth large, terminal, and slightly oblique; upper jaw nearly reaching vertical at front edge of orbit, 3.5–3.8 (3.6) in HL; 2 pairs of enlarged canines on front of upper jaw, inner pair projecting forward and curved ventrally, outer pair curved posteriorly; 1–2 (1) enlarged canines on rear portion of upper jaw, at the angle of the mouth, strongly curved anterolaterally; no teeth between front and rear canines of upper jaw; 2 pairs of enlarged canines anteriorly on lower jaw, inner pair projecting forward and slightly smaller than outer pair, outer pair strongly curved posterolaterally; single row of 9–10 (10) small canines aligned along middle of lower jaw; posterior edge of preopercle slightly serrated; membranous edge of opercle produced, tip of membranous edge over pectoral-fin origin; nostrils small, on the line between top of eye and tip of snout, anterior nostril at midpoint on this line and posterior nostril about midway between anterior edge of eye and anterior nostril; posterior nostril ovate without a rim, slightly bigger than anterior nostril.

Scales cycloid; head scales generally smaller than body scales; snout, lower jaw, and interorbital area scaleless; 3 (3) transverse scale rows on rear of cheek, remainder of cheek and suborbital region scaleless; preopercle naked; interopercle mainly naked except for a single row of 6–8 (6) small scales just below lower edge of preopercle; 4–5 (5) transverse scale rows on opercle; membranous edge of opercle and subopercle scaleless; predorsal scales extending anteriorly to level between rear edge of eye and posterior margin of preopercle; scales between lateral line and 5th dorsal-fin spine 2 ½; lateral line not interrupted, abruptly descending under 3rd to 7th soft dorsal-fin rays; last two pored scales of lateral line (posterior to hypural plate) greatly enlarged, the terminal one extending to about middle of caudal-fin; basal sheath of dorsal and anal fins consisting of row of small (compared to adjacent body scales), pointed scales; pectoral fins scaleless; 3–4 elongate scales adjacent to the outer edge of each pelvic fin.

Origin of dorsal fin above 3rd lateral line scale, predorsal-fin length 1.0–1.1 (1.1) in HL; 1st dorsal-fin spine 5.3–5.9 (5.3) in HL; 2nd dorsal-fin spine 4.2–4.6 (4.0) in HL; 5th dorsal-fin spine 3.7–4.1 (3.7) in HL; 5th to 11th dorsal-fin spines about equal in length; membranes of dorsal-fin spines extending slightly above spine tips; 1st soft dorsal-fin ray 3.7–4.0 (3.8) in HL; last soft dorsal-fin ray 4.1–4.8 (4.2) in HL; origin of anal fin about level with 10th dorsal-fin spine, preanal-fin length 1.6 (1.6) in SL; 3rd anal-fin spine longest, 4.3–4.7 (broken in holotype) in HL; 1st soft anal-fin ray 3.8–4.3 (4.0) in HL; last soft anal-fin ray 4.3–4.4 (3.8) in HL; tips of dorsal and anal fin rays falling well short of caudal-fin base; origin of pectoral fins just below origin of dorsal fin; pectoral fins short, upper tip of pectoral fins reaching under 9th or 10th dorsal-fin spine, pectoral fins 1.6–1.7 (1.7) in HL; lower pectoral fin rays elongate, about half the length of longest pectoral-fin ray, 3.3–4.1 (3.7) in HL; origin of pelvic fins about level with 2nd dorsal-fin spine, tip of fins just or not quite reaching anus, their length 1.9–2.0 (1.9) in HL; caudal fin generally truncate with slightly extruded upper and lower fin tips, longest rays 1.8–2.0 (2.0) in HL, middle of posterior edge slightly convex in male (vs. truncate in female).

Color of fresh male ( Fig. 1 A). Generally pale orange dorsally and pearly white ventrally; iris yellow; red lateral stripe from top of preopercle to upper portion of caudal-fin base; notable eye-sized red blotch on back below base of 9th to 11th dorsal-fin spines, center of blotch above lateral line; anterior edge of red blotch slightly bordered with white; blue lateral stripe from snout tip past lower boundary of eye, continued as row of fuzzy light blue spots to below end of dorsal fin; similar stripe from middle of postocular space to below 5th dorsal-fin spine; small blue spot on upper side of postocular; 2 blue lateral stripes on caudal-peduncle along dorsal edge and lateral line; faint whitish bar on pectoral-fin base; dorsal fin mainly yellow, broad blue stripe along outer edge, spines and soft rays slightly reddish; pectoral fins clear and colorless; pelvic-fins mainly bluish white, narrow yellow stripe along 2nd soft ray; anal fin mainly blue, broad yellow stripe across middle of the fin; caudal fin pale orange.

Color of preserved male (10% formalin for 3 months). Generally grayish dorsally and whitish ventrally; head grayish; iris light yellow; red stripe and blotch present in the fresh condition completely lost; blue stripes and spots present in the fresh condition faded to grayish blue; white bar on pectoral-fin base; all fins translucent white.

Color of fresh female ( Fig. 1 B). Generally orange dorsally and white ventrally; iris yellow; around the eye slightly pinkish; red lateral stripe from upper portion of preopercle to upper half of caudal-fin base, its lower border pinkish; dorsal fin mainly yellow, broad mauve stripe across upper half of the fin, spines and soft rays slightly reddish; pectoral fins clear and colorless; pelvic fins mainly bluish white, narrow yellow stripe along second soft ray; anal fin mainly blue, fuzzy yellow stripe across upper half of the fin, lower edge bordered with yellow; caudal fin mainly yellow and small red dots scattered, prominent broad red band on posterior edge of caudal fin.

Color of preserved female (10% formalin for 3 months). Generally light yellow dorsally and whitish ventrally; opercle grayish; iris light yellow; red stripe present in the fresh condition completely lost; all fins generally translucent white; posterior edge of caudal fin sometimes blackish.

Distribution. Choerodon margaritiferus has been collected from Okinawa Island, Japan (in the present study), Taiwan ( Allen & Erdmann 2012), Jolo, the Philippines ( Fowler & Bean 1928) and Lombok, Indonesia ( White et al. 2013; as Choerodon sp. A). Shea & Liu (2010) and Parenti & Randall (2000) included Chesterfield Islands (Coral Sea) and New Caledonia, respectively, in the range of the species. However, they did not show sufficient evidence that the species lives throughout this range, and further research is needed in these areas. In Okinawa, this species was collected from a depth of 30 m over sand-rubble bottom.

Ecological note. Histological observation of the gonads indicates that the specimens were mature, because filled spermatozoa were present in the testes of the male and mature oocytes (vitellogenetic and hydrated stages) were present in the female ( Fig. 2 ). In addition, some immature oocytes (perinucleolar stage) were found in a mature testis ( Fig. 2 A), providing strong evidence of the protogynic hermaphroditism found in most labrids.

Etymology. The English name “Pearly Tuskfish” follows Allen and Erdmann (2012). The word “Yuumodoro” used in the new standard Japanese name means the scene of sunset at Motobu town, near our collecting site, in the Okinawan local song. The red blotch and blue lateral stripe in the male suggest a sunset over the ocean. In addition, the word “Bera” means wrasse fish in standard Japanese.

Identification. Choerodon margaritiferus Fowler and Bean, 1928 was originally described on the basis of 1 specimen (Holotype: USNM 89966) collected from Jolo, the Philippines. Counts and measurements of examined specimens agree closely with those of the holotype (see description and Table 1 ). Although the body color of the holotype has mostly faded, some diagnostic coloration remained in the form of white marks: a lateral stripe under the eye, a row of spots on the mid-lateral part of the body, a lateral stripe on the middle of the caudal peduncle, and a bar on the pectoral-fin base ( Fig. 1 C). These color patterns matched well with those of the examined male specimen (see Figs. 1 A, C). In addition, the coloration of the holotype as described agrees almost exactly with that of the specimen. The only point of difference is that the notable red blotch in our male specimen was not noted in the original description. Fowler and Bean may have not observed it, because this character easily vanishes during preservation.

In the genetic analysis, the partial sequence of COI of examined specimens and 6 comparative species were aligned at 626 sites, 184 of which were polymorphic. The neighbor-joining dendrogram derived from the aligned sequences showed that the described specimens and C. margaritiferus ( KM224711 , from Indonesia, identified by Puckridge et al., 2015) represent the same clade ( Fig. 3 ). No genetic differences were found between the two color types (male and female) of examined specimens. Thus, examined specimens in this study were regarded as the same species. Meanwhile, other comparative species clearly represented separate clades with 78–100% bootstrap probability. This result emphasizes that the specimens collected from Okinawan waters were identified correctly as C. margaritiferus .

Choerodon margaritiferus Pectoral-fin rays 14 14 14 14 14 15 Pelvic-fin rays I, 5 I, 5 I, 5 I, 5 I, 5 I, 5 Principal caudal-fin rays 14 14 14 14 14 14 Upper procurrent caudal rays 7 7 8 7 7 8 ......continued on the next page Holotype Non-type specimens from Okinawan waters

USNM OCF-P OCF-P OCF-P OCF-P OCF-P 89966 20140827-1 20140825-3 20140827-2 20140827-3 20140827- 4 male male Female female female female

Figures

FIGURE 1. Choerodon margaritiferus. A) OCF-P 20140827 - 1, 107.0 mm standard length (SL), male, Okinawa Island, Japan; B) OCF-P 20140825 - 3, 96.4 mm SL, female, Okinawa Island, Japan; C) USNM 89966, holotype of C. margaritiferus, 116.0 mm SL, Jolo, the Philippines. Photographs by K. Miyamoto (A and B) and S. Raredon, National Museum of Natural History (C).

FIGURE 2. Gonadal sections, stained with Mayer’s hematoxylin and eosin, of Choerodon margaritiferus. A) OCF- P 20140827 - 1, 107.0 mm standard length (SL), male. B) OCF-P 20140825 - 3, 96.4 mm SL, female. hyo: hydrated oocyte, pns: perinucleolar stage, sc: spermatocytes, sz: spermatozoa, vs: vitellogenetic stage. Scale bars = 100 µm.

FIGURE 3. Neighbor-joining dendrogram derived from partial sequence of the mitochondrial cytochrome oxidase subunit I of Choerodon margaritiferus and closely related species. Scale bar equals 0.02 Kimura 2 - parameter distance. Numbers at branches indicate bootstrap probabilities in 1,000 bootstrap replications. DDBJ / EMBL / GenBank accession numbers are shown in parentheses.

Tables

TABLE 1. Counts and measurements of Choerodon margaritiferus holotype and additional specimens from Okinawan waters.

	Holotype USNM 89966 male	Non-type specimens from Okinawan waters OCF-P OCF-P OCF-P 20140827-1 20140825-3 20140827-2 male Female female	OCF-P 20140827-3 female	OCF-P 20140827-4 female
Standard length (mm)	116.0	107.0 96.4 103.0	94.5	97.4
Counts Dorsal-fin rays Anal-fin rays	XII, 8 III, 10	XII, 8 XII, 8 XII, 8 III, 10 III, 10 III, 10	XII, 8 III, 10	XII, 8 III, 10