Taxonomic review of the deep water flathead genus Parabembras with description of the new species Parabembras multisquamata from the western Pacific Ocean (Teleostei, Parabembridae)

Abstract Three valid species of Parabembras are recognized: P. curta, P. robinsoni, and the new species P. multisquamata. Parabembras robinsoni from the southwestern Indian Ocean (South Africa to Mozambique) is easily distinguishable from the other species in having eleven spines in the first dorsal fin, a distinct symphyseal knob on the lower jaw, two preocular spines, and a single lachrymal spine. Parabembras multisquamata from the southwestern Pacific (Vanuatu, Papua New Guinea) and the Philippines, and P. curta, known from the northwestern Pacific (southern Japan to South China Sea), are similar in sharing the absence of a symphyseal knob on the lower jaw, the presence of two lachrymal spines, and a single preocular spine, but the former is clearly distinguished from the latter in usually having 10 spines in the first dorsal fin (vs. eight or nine spines in P. curta), 9–11 supraocular spines (vs. 6–8 in P. curta), 40–44 pored lateral line scales (vs. 34–39 in P. curta), and the pectoral fin extending beyond the level of the anus (vs. not reaching to the level of the anus in P. curta).


Introduction
The family Parabembridae, or deep water flatheads, comprises only two species, Parabembras curta (Temminck & Schlegel, 1843) from the northwestern Pacific Ocean, and P. robinsoni Regan, 1921, from the western Indian Ocean (Eschmeyer et al. 2017). The former species was originally placed in the genus Bembras Cuvier, 1829, but assigned by Bleeker (1874) to the then monotypic genus Parabembras. Jordan and Hubbs (1925), established the family as Parabembradidae [currently Parabembradidae (van der Laan et al. 2014)], but several authors synonymized Parabembridae with Bembridae (e.g., Knapp 1986;Nelson et al. 2016). Imamura (1996; recognized Parabembridae as a valid family on the basis of a phylogenetic analysis based on osteological and myological characters. According to Imamura (1996), the family is diagnosed by the presence of spines and absence of tubercles on the dorsal surface of the head; the lower jaw projecting beyond the tip of the upper jaw; the separation of the ascending process and the remaining part of the premaxilla; the absence of free fin rays from the pectoral fin; three spines in the anal fin; about 35-40 scales in the lateral line; and the absence of a swim bladder.
We examined four relatively recently collected  specimens of a species of Parabembras from the waters of Vanuatu, Papua New Guinea, and the Philippines. These specimens differ from the two currently known species of the family by the spines on the head, number of dorsal-fin spines and pored lateral line scales, and several proportional measurements, and are described herein as a new species of Parabembras. In addition, the two congeneric species P. curtus and P. robinsoni are redescribed, and a key to the species of Parabembras is presented.

Materials and methods
Counts and measurements follow Motomura (2004), except where otherwise noted. Body depths 1 and 2 are taken at the anterior insertions of the first and second dorsal fins, respectively; predorsal lengths 1 and 2 from tip the tip of the snout to the anterior insertion of the first and second dorsal fins, respectively; and the body width is measured between the uppermost part of the base of the right and left pectoral fins. Pored lateral line scales were counted from the first pored scale near the gill opening to the pored scale on the posterior margin of the hypural plate. The terminology of head spines follows Knapp et al. (2000). The standard length is abbreviated as SL. Characters given in the diagnosis of the genus were not repeated in the species descriptions. To provide an objectively defined score that summarizes the major components of variable measurements between specimens, a principal component analysis (PCA) was conducted on morphometric characters by using the function prcomp in the software package R 3.3.2. (R Core Team 2016). We removed the effect of changes in size by calculating the residuals from the linear regressions of changes in all variables on changes in SL (Revell et al. 2007). All variables were log-transformed prior to analysis.
The specimens examined in this study are deposited in the fish collections of the Natural History Museum, London (BMNH), Kyoto University, Kyoto and Maizuru (FAKU), Muséum national d'Histoire naturelle, Paris (MNHN), National Museum of Marine Biology and Aquarium, Taiwan (NMMBA), National Museum of Nature and Science, Tsukuba (NSMT), the National Taiwan University Museums, Taipei (NTUM), and the Museum of Comparative Zoology, Harvard University, Cambridge, Massachusetts (MCZ).
Type species. Bembras curtus Temminck & Schlegel, 1843 by monotypy. Diagnosis. Body cylindrical, head somewhat depressed. Dorsal surface of head with spines only, tubercles absent. Ctenoid scales covering nape, postorbital, cheek, and opercular regions. Lower jaw projecting beyond upper jaw; dermal flap on posterior margin of maxillary. Two dorsal fins; first dorsal fin with 9 (rarely 8) to 11 spines; second dorsal fin with one spine and 8 or 9 soft rays. Anal fin with three robust spines and 5 soft rays. Pectoral fin without free rays. Pelvic fin with one spine and 5 soft rays, inserted below base of pectoral fin. Pored lateral line scales 34-44.
Remarks. Imamura (1996) diagnosed the then monotypic family Parabembridae on the basis of dissection of a single species, Parabembras curtus. Because of the rarity of the other species, we could not confirm the status of internal diagnostic characters given by Imamura (1996). Although Nelson et al. (2016) placed Parabembras under family Bembridae with Bembradium Gilbert, 1905: the former is clearly distinguishable from the latter in having three anal-fin spines (vs. anal-fin spines absent). In the phylogenetic analysis, Imamura (2004) recovered a sister relationship between Bembradium and Plectrogenium Gilbert, 1905 Material examined. FAKU 12176, 12280, 12371, 14289, 41439, 41441, 41443, 41445-41447, 106.0-193.1 mm SL (10 specimens), East China Sea, coll. Matsui and Takai, 20 Oct. 1949;FAKU 34911, 145.5 mm SL (1), Yawatahama, Ehime, Japan, Kishida, Mar. 1962;FAKU 35093, 114.8 mm SL (1), Tosa Bay, Kochi, Japan,. K. Amaoka, Mar. 1962;FAKU 37892, 37893, 37897, 143.9-154.1 mm SL (3), Shimonoseki, Yamaguchi, Japan, N. Taniguchi, 10 Jun. 1965 Diagnosis. Parabembras curta is distinguished from P. robinsoni in the absence of a symphyseal knob on the lower jaw (vs. distinct symphyseal knob in P. robinsoni), presence of a single preocular spine (vs. two preocular spines), and presence of two robust lachrymal spines (vs. a single robust lachrymal spine). It is further distinguished from P. multisquamata, in having 6-8 supraocular spines (vs. 9-11 supraocular spines in P. multisquamata); nine (rarely eight) spines in the first dorsal fin (vs. 10 spines); 34-39 pored lateral-line scales (vs. 40-44 pored lateral line scales). Description. Measurements are shown in Table 1. Body cylindrical, posteriorly weakly compressed, completely covered with ctenoid scales. Nasal spine simple, dorsoposteriorly directed. Anterior lachrymal with single robust spine, posterolaterally directed, in some specimens with small additional spine anteriorly; posterior lachrymal with sharp spine, posteroventrally directed. Single preocular spine present. Interorbital region narrow and weekly depressed, with 6-8 supraocular spines. Single postocular spine present, slightly larger than posteriormost supraocular spine. Suborbital ridge strongly or moderately developed, with three robust spines; tip of anteriormost spine below center of eye, second below posterior margin of eye, posteriormost below pterotic spine. Parietal spine robust and sharp, posteriorly directed. Three nuchal spines, one each on supratemporal, posttemporal, and supracleithrum, respectively; posttemporal in some specimens with additional spine. Pterotic with single sharp posteriorly directed spine. Preopercle with single robust posteriorly directed spine, in some specimens with supplementary spine; ventral margin of preopercle smooth. Opercle with upper and lower spines, directed slightly dorsoposteriorly and ventroposteriorly, respectively. Dermal flaps on head absent, except for flap on anterior nostril. Gill rakers blunt, usually four (in some specimens five) on upper limb; 11-13 (modally 12) on lower limb, including single (longest) raker at angle. Lateral line running parallel to dorsal contour of body, extending beyond caudal-fin base; 34-39 (modally 36) pored lateral line scales on body and 2-3 on caudal fin, each with single, robust tube. Mouth large, slightly oblique; maxilla reaching anterior rim of pupil; posterior margin of maxilla with distinct notch. Upper half of maxilla fitting within groove below suborbital ridge. Symphyseal knob absent from lower jaw. Upper and lower jaws with villiform teeth arranged in a band; vomer V-shaped, with villiform teeth; tooth band on palatine narrow. First dorsal fin originating above level of pectoral-fin base, with usually nine spines (rarely eight), gradually increasing in length to fifth spine. First and second dorsal fins well separated. Second dorsal fin with one spine and eight soft rays; first soft ray somewhat longer than spine. Second dorsal and anal fins opposite each other, nearly equal in length and height; origin of latter slightly posterior to that of former. Caudal fin rounded. Pectoral fin rounded, upper half somewhat longer than lower half; its tip not reaching to level of anus, usually with 20-22 rays (modally 21), the lower 3-8 rays unbranched.
Coloration. In fresh condition, head and body reddish orange, white ventrally; faint dark red saddle below first and second dorsal fins, respectively; fins red, interradial membranes pale red; posterior half of caudal fin dark red. In preserved specimens, head and body pale brown; fins pale gray without any markings.
Geographical distribution. Known from the western Pacific Ocean; Wakasa Bay of Sea of Japan and Kumano-nada, Pacific coast of Japan and Korea south to China and Taiwan (East China Sea, Yellow Sea, Bohai, and northern part of South China Sea) (Fig. 3). Benthic, on sandy mud substrate from depths of 60-141 m (Chu and Jin, 1963;Nakabo and Kai, 2013;present study).
Remarks. Parabembras curta was originally described as a member of Bembras by Temminck and Schlegel (1843) on the basis of the specimens collected in Japan 1823-1834 by Philipp von. Siebold and Heinrich Bürger. Boeseman (1947) reviewed the Siebold and Bürger's collection, and designated RMNH-D 682 as the lectotype and RMNH-D 2057 as paralectotype of the species. According to Boeseman (1947), the lectotype has nine spines in the first dorsal fin and the paralectotype has eight spines. The figure of the species given in the original description is characterized as having eight spines in first dorsal fin, one spine and eight rays in the second dorsal fin, a single preocular spine, seven supraorbital spines, and two robust lacrimal spines. The photo of RMNH-D 682 published by Yamaguchi and Machida (2003) indicates clearly the absence of a symphyseal knob on the lower jaw.
The short description of P. curta given by Günther (1860) agrees with the present specimens in the nine spines in the first dorsal fin. Jordan and Hubbs (1925), who established the family Parabembridae (originally as Parabembradidae), described P. curta as having nine spines in the first dorsal fin and two spines and seven rays in the second dorsal fin. Although the count of spines in the second dorsal fin is not usual for any three species recognized here, the counts of pored lateral line scales (37), gill rakers on lower limb (11) and supraocular spines (6) agreed well with the present specimens of P. curta. The descriptions of P. curta from the East China Sea given by Li (1955), Chu and Jin (1963) and Jin (2006) and that from Kochi, Japan by Kamohara (1952) are referable to the species identified here with reference to the counts of dorsal-fin spine (9) and lateral line scales (35-40). Lindberg and Krasyukova (1987) recorded P. curta on the basis of four specimens from Busan (Korea) and the East China Sea. They characterized the species as having nine spines in the first dorsal fin and 36-38 lateral line scales, which agrees with counts in the present specimens of P. curta. Suzuki and Kataoka (1997) characterized P. curta from Mie Prefecture, Japan as having 10 spines in the first dorsal fin. Although the count of dorsal-fin spines was rather similar to Parabembras multisquamata described below, the pectoral fin of their specimen does not reach to anus, matching the condition of the present specimens of P. curta. In addition, the established distributional range of P. curta is close to the locality of Suzuki and Kataoka's (1997) specimen. The short description of P. curta given by Ochiai (1984) apparently includes several species recognized here, because he assumed that P. curta was widely distributed in the Indo-West Pacific, and also presented a wide range in the count of dorsal-fin rays (IX-X-I, 7-9) (which apparently also includes P. multisquamata and P. robinsoni). The photograph provided by Ochiai (1984) agrees with the present specimens of P. curta in the short pectoral fin (not reaching to the anus) and absence of a symphyseal knob. The description of Shen (1993) apparently followed that of Ochiai (1984), but the photograph provided by him is referable to P. curtus recognized by the short pectoral fin (not reaching to the anus) and absence of a symphyseal knob. The keys and short descriptions of P. curtus presented by Nakabo (2000;2002) also apparently followed Ochiai (1984). The images of P. curta and Bembradium roseum Gilbert, 1905 published by Shen and Wu (2011) are here both identified as P. curta in having nine spines in the first dorsal fin and three spines in the anal fin. However, their description of B. roseum does not agree with the specimen shown in their photograph which has 11 anal-fin rays.
The record of P. curta from the eastern Indian Ocean by Lin (1974: 26, western Indonesia) cannot be verified; specimens from these regions are needed to establish their identity. Although Krakstad et al. (2014: 74, 75) listed P. curtus from Myanmar, this record is not based on a species of Parabembras, but of Bembras (Peter Psomadakis, pers. comm.).
Description. Measurements are shown in Table 1. Body cylindrical, posteriorly moderately compressed, completely covered with ctenoid scales. Anterior lachrymal with single robust spine, posterolaterally directed, in some specimens with small additional spine anteriorly; posterior lachrymal without spine. Two preocular spines present. Interorbital region narrow and slightly depressed, with more than 12 small spines, forming a serrated ridge. Single small postocular spine present. Suborbital ridge strongly or moderately developed, with three robust spines, tip of anteriormost spine below center of eye, second below posterior margin of eye; posteriormost below pterotic spine. Parietal spine sharp, posteriorly directed. Three nuchal spines, one each on supratemporal, posttemporal, and supracleithrum, respectively; posttemporal sometimes with additional spine. Pterotic with two sharp spines posteriorly directed. Posterior rim of orbit armed with small spines. Preopercle with single robust spine, posteriorly directed; usually with supplementary spine; ventral margin of preopercle smooth. Opercle with upper and lower spines, slightly directed dorsoposteriorly and posteriorly, respectively. Dermal flaps on head absent, except for flap on anterior nostril. Gill rakers blunt, usually 4-5 on upper limb; 14-16 (modally 15) on lower limb, including single (longest) raker at angle. Lateral line running parallel to dorsal contour of body, extending beyond caudal-fin base; 38-41 (modally 39) pored lateral-line scales on body and 2-3 on caudal fin, each with single, robust tube.
Mouth large, slightly oblique; maxilla reaching level of anterior rim of pupil; posterior margin of maxilla weakly notched. Upper half of maxilla fitting within groove below suborbital ridge. Lower jaw with distinct symphyseal knob. Upper and lower jaws with villiform teeth in a band; vomer V-shaped with villiform teeth; tooth band on palatine narrow. First dorsal fin originating above level of pectoral-fin base, usually with eleven spines (in some specimens ten), gradually increasing in length to fifth spine. Last spine of first dorsal fin separated from penultimate spine without membrane, positioned midway between penultimate spine of first dorsal fin and insertion of second dorsal fin. Second dorsal fin with one spine and 8-9 soft rays; first soft ray slightly longer than spine. Second dorsal and anal fins directly opposite each other, nearly equal in length and height. Caudal fin rounded. Pectoral fin usually with 19-21 rays (modally 20), lower 4-7 rays unbranched; its rounded upper half somewhat longer than lower half, slightly extending beyond level of anus.
Coloration. In fresh condition, head and body reddish orange, white ventrally; fins red, interradial membranes pale red; distal margins of dorsal and anal fins dark red; posterior half of caudal fin dark red [based on pl. E. Afr-97 of Ochiai (1976)]. In preserved condition, head and body dark brown; fins pale gray; distal margin of second dorsal, anal and caudal fins dark brown.
Geographical distribution. Western Indian Ocean, from Durban to at least southern Mozambique, along the east coast of South Africa at depths of 200-600 m (Knapp 1986). According to Everett et al. (2015), the species may be distributed along the East African coast north to Kenya; however, these records need confirmation.
Remarks. Parabembras robinsoni was originally described by Regan (1921), characterized as having 10 spines in the first and one spine and nine soft-rays in the second dorsal fin. However, the last spine of the first dorsal fin, which is positioned between the penultimate ray of the first dorsal fin and the insertion of the second dorsal fin, is present in the holotype (BMNH 1921.3.1.19), which has eleven dorsal-fin spines, a distinct symphyseal knob in the lower jaw and a single lachrymal spine; hence, the present specimens are identified as P. robinsoni. Barnard (1927) and Smith (1949Smith ( , 1961Smith ( , 1985 reported P. robinsoni from off the coast of KwaZulu-Natal, South Africa as having ten or eleven spines in the first dorsal fin. The short description by Knapp (1986) also characterized P. robinsoni as having ten or eleven spines in the first dorsal fin and a symphyseal knob in the lower jaw. These characters agree well with the present specimens of P. robinsoni. In contrast, Gilchrist (1922) described P. curta from South Africa and considered P. robinsoni as a junior synonym of P. curta. However, he described the species as having two preocular spines, agreeing with the present specimens of P. robinsoni, but not with P. curta. Similarly, Ochiai (1976) described P. curta from the east coast of South Africa. His photograph clearly shows P. robinsoni, judging by the presence of a distinct symphyseal knob in the lower jaw. Ochiai assumed that P. curta was widely distributed in the Indo-West Pacific, but apparently he confused P. curta and P. robinsoni. Probably due to this report, some subsequent authors mistakenly reported an occurrence of P. curta in the Indian Ocean (e.g., Nakabo 2000Nakabo , 2002Yamada et al. 2007).  : 26cp4, 23 Nov. 1980;MNHN-IC-2008-2443, 2009  Diagnosis. Parabembras multisquamata is distinguished from P. robinsoni in having two lachrymal spines and no symphyseal knob on the lower jaw. It is most similar to P. curta, but is clearly distinguished from the latter in having usually 10 first dorsal-fin spines (vs. 8 or 9 spines in P. curta), 9-11 supraocular spines (vs. 6-8 in P. curta), and 40-44 pored lateral line scales (vs. 34-39 in P. curta).

Parabembras multisquamata
Description. Measurements are shown in Table 1. Data of the holotype are given first, followed by data of the paratypes, in parentheses, if different from holotype. Body cylindrical, posteriorly weakly compressed, completely covered with ctenoid scales. Nasal spine simple, dorsoposteriorly directed. Anterior lachrymal with single robust spine, posterolaterally directed, with small additional spine anteriorly (without an additional spine in MNHN-IC-1984-0687); posterior lachrymal with sharp spine, directing posteroventrally. Single preocular spine present. Interorbital region narrow and weekly depressed, armed with 11 (9-11) supraocular spines. Single postocular spine present, somewhat larger than posteriormost supraocular spine. Suborbital ridge strongly developed (moderately developed), with three (three or four) robust spines; tip of anteriormost spine below center of eye, second below posterior margin of eye, third below pterotic spine (posteriormost on margin of preopercle). Three nuchal spines; one each on supratemporal, posttemporal, and supracleithrum, respectively. Pterotic with two sharp spines posteriorly directed. Posterior rim of orbit armed with small spines. Preopercle with single robust and several small supplementary spines, posteriorly directed; ventral margin of preopercle with three (0-5) tiny spines. Opercle with upper and lower spines, slightly dorsoposteriorly and ventoposteriorly directed, respectively. Dermal flaps on head absent, except for flap on anterior nostril. Gill rakers blunt, usually 5 (4-5) on upper limb; 14 (12-13) on lower limb, including single (longest) raker at angle. Lateral line running parallel to dorsal contour of body, extending beyond caudal-fin base; 44 (40-44) pored lateral-line scales on body and 2 (2-3) on caudal fin, each with single, robust tube.
Mouth large, slightly oblique; maxilla reaching anterior rim of pupil; posterior margin of maxilla with distinct notch. Upper half of maxilla fitting within groove below suborbital ridge. Symphyseal knob absent from lower jaw. Upper and lower jaws with villiform teeth arranged in a band; vomer V-shaped, with villiform teeth; tooth band on palatine narrow. First dorsal fin originating above level of pectoral-fin base, usually with 10 spines (nine in MNHN-IC-2009-0115), gradually increasing in length to fifth (forth or fifth) spine. First and second dorsal fins well separated. Second dorsal fin with one spine and 8 soft rays; first soft ray somewhat longer than spine. Second dorsal and anal fins opposite each other, nearly equal in length and height; anterior insertion of latter slightly posterior to that of former. Caudal fin rounded. Pectoral fin rounded, upper half somewhat longer than lower half; its tip extending beyond level of anus, with 19 rays (19-21) of which lower 7 (6-7) rays unbranched.
Coloration. In fresh specimens [based on fig. 8 in Fricke (2015), NTUM 10690], head and body red, white ventrally; first dorsal fin dark red margined with black; second dorsal fin red with black marking; posterior half of caudal fin dark red; pectoral fin bright red; pelvic fin pale red. In preserved condition, head and body pale brown; first dorsal fin margined with black; second dorsal fin with dark brown marking.
Geographical distribution. Known from the western Pacific Ocean, off southwestern Luzon, Philippines, Morobe Province of Papua New Guinea, and Espiritu Santo, Vanuatu. The new species was collected at depths of 299-444 m (Fig. 3).
Etymology. The name multisquamata is derived from Latin multus meaning many and squamatus meaning scaled, in reference to the high number of pored lateral line scales. The name is an adjective, its ending following the feminine gender of the generic name Parabembras.
Remarks. Fricke (2015) reported P. multisquamata as P. curtus (non Temminck and Schlegel 1843) from Morobe Province of Papua New Guinea on the basis of a single specimen, NTUM 10690, which is now one of the paratypes of P. multisquamata. Judging from the collection data, the record of P. curta from off southwestern Luzon, Philippines by Fourmanoir (1985: 46, as P. curtus) was based on MNHN-IC-1984-0687, one of the paratypes of P. multisquamata.

Discussion
Parabembras multisquamata is most similar to P. curta in having two lachrymal spines and no symphyseal knob on the lower jaw, but is clearly distinguished as described above. These two species differ further in some morphometric characters, including the preanal length and the first spine of the second dorsal fin (Fig. 4). Furthermore, the pectoral fin of P. multisquamata extends beyond the level of the anus (vs. not reaching to the level of anus in P. curta). The PCA using 20 measurements (eight were eliminated due to the lack of data in some of the specimens) resulted in the rough separation of three species. The first and second principal components accounted for 34.4 % and 18.3 % of the variation. PC1 was heavily loaded on caudal peduncle depth, body depth 2, and length of second anal-fin spine, providing separation between P. robinsoni and the other two species (Fig. 5). PC2 was heavily loaded on length of second anal-fin  spine, body width, and body depth 1, providing separation between P. multisquamata and the other two species. These results also support the existence of three species in Parabembras. The distributional ranges of the three species are not overlapped, suggesting that they speciated allopatrically.