Atopocottus tribranchius Bolin, 1936

Matsunuma, Mizuki, Sato, Mao & Kai, Yoshiaki, 2017, Redescription of Atopocottus tribranchius (Cottidae) from Japan with comments on the generic diagnosis and distribution, Species Diversity 22, pp. 87-97 : 93-96

Atopocottus tribranchius Bolin, 1936

[Japanese name: Kawari-anahaze] ( Figs 1–4 , 8 , Tables 1, 2)

Material examined. 56 specimens (12.0– 27.9 mm SL) from Japan: Tosa Bay (Kochi Prefecture): BSKU 78985 (female), 27.9 mm SL, 33°14′53″N, 133°38′02″E – 33°14′53″N, 133°38′02″E, 200 m, RV Kotaka-maru , 6 July 2006; BSKU 98806 , 13.6 mm SL, 33°14′55″N, 133°38′55″E – 33°13′30″N, 133°38′48″E, 201–207 m, RV Kotaka-maru, otter trawl, 17 June 2009; BSKU 99875 (male), 26.6 mm SL, BSKU 121004 , 13.8 mm SL, BSKU 121005 (male), 25.4 mm SL, BSKU 121006 , 17.3 mm SL, BSKU 121007 (female), 26.3 mm SL, BSKU 121008 , 13.7 mm SL, BSKU 121009 (male), 22.8 mm SL, BSKU 121010 , 19.3 mm SL, BSKU 121011 (male), 16.9 mm SL, BSKU 121012 (male), 24.0 mm SL, BSKU 121013 (male), 18.3 mm SL, BSKU 121014 , 13.3 mm SL, BSKU 121015 (female), 18.5 mm SL, BSKU 121016 (female), 18.2 mm SL, BSKU 121017 (female), 20.6 mm SL, 33°18′18″N, 133°36′22″E, 200 m, RV Kotakamaru, 14 September 2009; BSKU 101389 (male), 25.9 mm SL, 33°12′47″N, 133°35′00″E – 33°11′17″N, 133°32′53″E, 186– 203 m, RV Kotaka-maru, 10 August 2010; BSKU 103020 , 2 specimens (females), 24.1–26.8 mm SL, 200 m, RV Kotakamaru, 8 March 2010; BSKU 118396 , 20.2 mm SL, BSKU 118397 , 17.8 mm SL, BSKU 118398 , 18.1 mm SL, BSKU 118399 , 18.4 mm SL, 33°12′50″N, 133°34′56″E – 33°10′49″N, 133°32′37″E, 203–222 m, RV Kotaka-maru, otter trawl, 15 September 2009; BSKU 118400 , 19.8 mm SL, BSKU 118401 (female), 22.5 mm SL, BSKU 118402 , 16.8 mm SL, BSKU 118403 , 23.0 mm SL, BSKU 118404 (female), 23.4 mm SL, 33°14.81′N, 133°37.95′E – 33°13.33′N, 133°34.98′E, 179– 219 m, RV Kotaka-maru, 16 November 2009; BSKU 118405 , 22.8 mm SL, BSKU 118406 , 21.2 mm SL, BSKU 118407 , 21.4 mm SL, BSKU 118408 (male), 20.9 mm SL, BSKU 118409 (female), 25.1 mm SL, BSKU 118410 , 23.1 mm SL, BSKU 118411 (female), 26.5 mm SL, BSKU 118412 (male), 27.7 mm SL, 33°14′46″N, 133°37′53″E – 33°13′09″N, 133°34′57″E, 186–207 m, RV Kotaka-maru, otter trawl, 5 October 2009; KPM-NI 26830 , 12.0 mm SL, KPM-NI 26831 , 15.4 mm SL, 33°12′33″N, 133°34′34″E – 33°12′20″N, 133°34′27″E, 211–218 m, T . Sato, RV Tansei-maru , dredge, 15 August 2010 . Yamaguchi Prefecture: FAKU 82636 , 25.2 mm SL, off Yamaguchi, 35°28′26″N, 131°16′31″E, 118 m, TV Tanshu-maru , 18 July 1995; SNFR 17688 (female), 27.6 mm SL, 35°30’N, 131°30′E, RV Mizuho-maru, 11 June 2011 . Kyoto Prefecture: FAKU 132665 (female), 25.6 mm SL, off Kanmuri-jima, Maizuru, 150 m, Y . Kai, RV Ryokuyo-maru, 20 July 2010; FAKU 132893 , 5 specimens, 18.9–22.4 mm SL, FAKU 132895 , 3 specimens, 18.5–22.3 mm SL, off Kanmuri-jima, Maizuru , 150 m, Y . Kai, RV Ryokuyo-maru , 21 December 2010 . Niigata Prefecture: FAKU 135499 , 2 specimens (one female and one sex undetermined), 24.3–27.5 mm SL, off Niigata, 38°24′23″N, 139°00′47″E, 140 m, RV Mizuho-maru, 12 May 2013 . East China Sea : KAUM –I . 75280, 20.5 mm SL, southwest of Danjo Islands, 32°09′N, 128°02′E, 147–148 m, bottom trawl, 21 June 2015; SNFR 15014 , 3 specimens, 18.1–19.3 mm SL, southwest of Danjo Islands , 32°45′N, 127°45′E, RV Yokomaru, bottom trawl, 26 August 1998 .

Diagnosis. As for genus.

Description. Meristics and morphometrics shown in Table 2. Body small, posterior portion strongly compressed ( Fig. 1 ). Head and body fleshy, naked except for a row of 3–5 lateral-line scales under skin, restricted to anterodorsal portion of body, each scale with a single canal with anteri- or and posterior openings; pores opening on skin between each lateral-line scale and posterior margin of last scale, 4–6 pores in total [FAKU 135499 (1 of 2, 27.5 mm SL) with separated rows of lateral-line scales on left side of body; anterior canal continued to postorbital canal with 2 pores, posterior canal isolated with 3 pores]. No cirri on head and body. Head moderately large, rounded; eye very large, orbit diameter 34–43% of head length; interorbital space very narrow. Mouth terminal, moderately large; posterior margin of maxilla extending beyond a vertical through mid-orbit. Both jaws with narrow bands of 2 rows of small, slender conical teeth; crescent-shaped row of small conical teeth on prevomer; palatines with short band of small teeth. Gill rakers rudimentary, tubercular, restricted to lower limb; branchiostegal membranes broadly united with each other, free from isthmus. Preopercle with 4 distinct spines; lowermost spine canted anteroventrally; uppermost spine longest with 1–6 branches dorsally (number of branches increasing with growth; Fig. 4 ). No other spines on head. Dorsal fin broadly separated into spinous and soft-rayed portions. Dorsal-fin spines tiny; 3rd spine shorter than both 2nd and 4th spines, forming distinct notch in dorsal contour of fin; length of 3rd spine 58–98% and 57–91% of 2nd and 4th spines length, respectively. Second dorsal fin slightly higher than 1st dorsal fin; all soft rays unbranched. Anal fin origin below 2nd soft ray of 2nd dorsal fin; length of base shorter than that of 2nd dorsal fin; all soft rays unbranched. Pectoral fin relatively large, long; all rays unbranched; tip of longest ray, reaching a vertical through middle of 2nd dorsal-fin base. Pelvic fin slender; all soft rays unbranched; spine tiny, fused with 1st soft ray; 2nd ray longest, its tip not reaching anus. Caudal fin small, truncate, with 8 or 9 branched rays. Caudal peduncle relatively long, low.

Cephalic sensory system shown in Fig. 3A, B . Supraorbital canal with anterior and posterior nasal pores and 4 supraorbital pores; 1st and 2nd supraorbital pores on anterior portion of frontal; 3rd pore (SO3) absent; 4th and 5th supraorbital pores on posterior edge of orbit. Infraorbital canal with 9 posterior pores. Posterior portion of interorbital region with anterior and posterior coronal pores. Postorbital canal with 6 pores. Occipital canal with posterior medial pore, lateral anterior central pore, lateral posterior central pore, lateral anterior pore and lateral posterior pore; anterior medial pore (OCA) absent. Preoperculo-mandibular canal with 10 pores; 1st to 3rd on ventral surface of dentary, 4th on border between dentary and angular, 5th to 9th on preopercle between each preopercular spine and 10th on upper end of thin sensory canal from preopercle.

Fresh coloration. Based on color photograph of 20.5 mm SL-specimen ( Fig. 1 ). Head and body white with numerous small yellowish-green blotches scattered on head and dorsum of body, numerous small blackish blotches scattered on lateral surface of body, except for abdomen; large black blotch dorsally on pectoral-fin base. First dorsal-fin membrane white with black blotch between 4th and 6th spines. Second dorsal-fin membrane semi-translucent, posterodorsal edge tinged with white; posterior rays with blackish tinge. Anal-fin membrane semi-translucent, posteroventral edge broadly tinged with white. Pectoral fin semi-translucent with ca. 4 irregular, narrow yellowish-green bands. Posteriormost portion of caudal peduncle and caudal fin base broadly blackish. Caudal fin semi-translucent.

Preserved coloration. Head and body creamy-white; white and yellowish markings diffused but black markings retained; second dorsal fin broadly blackish in some large specimens.

Distribution. The species has been recorded from the northwestern Pacific Ocean, including the northern East China Sea, off the Japan Sea coast and in Tosa Bay, Kochi and off Ibaraki on the Pacific coast of Japan. The examined specimens were collected in depths of 118–222 m, off Niigata, Kyoto, Yamaguchi, Kochi and in the northern East China Sea ( Fig. 8 ). The species has also been recorded in earlier studies from Yamagata ( Honma 1959, 1960) and Akita ( Komoto and Yamada 2013; Komoto et al. 2015) on the Japan Sea coast and Ibaraki ( Ohashi et al. 2017) on the Pacific coast of central and northern Japan.

Bolin (1936) originally described At. tribranchius on the basis of 11 specimens from Japan, giving the type locality as “Nugatu”. Okada and Matsubara (1938) regarded “Nugatu” as a misspelling of Numazu, a city facing Suruga Bay, Shizuoka Prefecture on the Pacific coast of central Japan. Subsequently, Kuroda (1951) listed At. tribranchius in his checklist of fishes of Suruga Bay and Yabe (2011) also included Suruga Bay in the distributional range of the species. However, because Honma (1960) had noted the type locality as more likely being Niigata on the Japan Sea coast of central Japan, due to the consistency of the geographic coordinates of the type locality given by Bolin (1936) with that location, Nakabo and Kai (2013) omitted Suruga Bay from the distribution of the species.

After the original description, Okada and Matsubara (1938) proposed the Japanese name, Kawari-anahaze, for At. tribranchius . Honma (1959, 1960) subsequently redescribed the species based on specimens from Niigata and Yamagata. Yabe (1984) stated that the species was known only from Niigata and Nishimura (1974) also regarded the species as being endemic to the Japan Sea. However, Yabe (2011) recently included Yamaguchi ( Japan Sea coast), Tosa Bay, Kochi and Suruga Bay (Pacific coast) in the distributional range of the species, although specimen data was not included. More recently, Nakabo and Kai (2013), in the latest edition of “Fishes of Japan with pictorial keys to species”, stated that the species was distributed in Yamagata, Niigata, Kyoto, Yamaguchi and Kochi, Japan, their records from Kyoto being based on specimens (FAKU 131623 and 132168) collected off Tango Peninsula, and those from Yamagata and Niigata, and Yamaguchi and Kochi being referred to Honma (1960) and Yabe (2011), respectively. Additionally, Komoto and Yamada (2013) and Komoto et al. (2015) recorded the species from Akita Prefecture in lists of fishes collected during experimental benthic trawl surveys. Ohashi et al. (2017), recently, recorded the species from off Ibaraki. The present specimens from Kochi, Yamaguchi and the northern East China Sea, therefore, represent the first specimen-based records of the species from those regions. The species seems to have been rarely captured due to its very small size and relatively deep water habitat, most of the present specimens having been collected by small mesh benthic trawl or biological dredge during scientific surveys.

Remarks. The specimens examined here agree with the holotype and the original description, as well as with Honma’s (1959, 1960) redescriptions of At. tribranchius , in overall body appearance, meristic characters, head spination, coloration and the remarkably small mature size. Their identity was also confirmed by keys to the cottid species of the northwestern Pacific Ocean given by Yabe (2011) and Japanese waters given by Nakabo and Kai (2013).

Honma (1960) reported that examples of At. tribranchius <30 mm SL possessed fully matured ovaries. Among the present specimens, several females (22.5–27.6 mm SL) similarly possessed mature ovaries, one 27.6 mm SL-female specimen (SNFR 17688) having developed ova of ca. 1 mm diameter. Although sexual dimorphism and dichromatism in cottid fishes have been recognized in fin shape and coloration ( Nakabo and Kai 2013), no significant morphological differences were recognized between the sexes of At. tribranchius .

A morphological change in the uppermost preopercular spine shape was apparent in the species, the number of branches on the upper margin of the spine tending to increase with growth. Small specimens (between 13.6 and 22.4 mm SL) usually possessed a single branchial spine on the uppermost preopercular spine ( Fig. 4E ), its tip becoming divided into two spinous points with growth ( Fig. 4D ). In contrast, large specimens (between 20.6 and 27.9 mm SL) usually possessed an additional small branch near the preopercular spine tip, some specimens having 3 or more branches ( Fig. 4A–C ). No other significant ontogenetic changes were apparent in the meristic or morphometric characters.

Bolin’s (1936) description of 27–29 minute lateral-line pores along the trunk to the caudal-fin base, following 3–6 lateral-line scales, was followed by Nakabo and Kai (2013), although they did not include pores on the lateral-line scales. However, Honma’s (1959, 1960), redescriptions of the species did not mention such pores. In the present specimens, a row of numerous minute organs along the trunk was recognizable in several specimens in good condition but proved very difficult to distinguish, and therefore uncountable. A similar condition was also reported for An. galatheae by Bolin (1952). Because the organs are most likely epidermal pits containing free neuromasts, they should not be considered as lateral-line pores. The ease with which such organs may be obscured or damaged during capture and preservation, makes future examinations based on fresh specimens highly preferable.

Comparative material examined. Atopocottus tribranchius (holotype): USNM 102105, 26.8 mm SL, off Niigata Prefecture (originally as “Nugatu”), Japan, RV Albatross, station 4817, 38°14′N, 138°52′E, 61 fm (ca. 111.6 m). Stlengis distoechus (5 specimens, 58.7–72.1 mm SL, all from Tosa Bay , Kochi, Japan): BSKU 12978 , 58.7 mm SL; BSKU 12979 , 62.9 mm SL; BSKU 13155 , 72.1 mm SL; BSKU 13157 , 67.1 mm SL; BSKU 41916 , 62.4 mm SL . Stlengis misakia (5 specimens, 61.1–83.6 mm SL): BSKU 29089 , 73.0 mm SL, BSKU 94658 , 63.1 mm SL, BSKU 97678 , 83.6 mm SL, Tosa Bay , Kochi, Japan; BSKU 110030 , 74.9 mm SL, BSKU 110053 , 61.1 mm SL, Suruga Bay, Japan . Stlengis osensis (10 specimens, 32.6–39.4mm SL, all from Tosa Bay , Kochi, Japan): BSKU 107873 , 37.1 mm SL; BSKU 107932 , 9 specimens, 32.6–39.4 mm SL .

Figures

Fig. 1. Fresh specimen of Atopocottus tribranchius, KAUM–I.75280, 20.5mm SL, East China Sea.

Fig. 2. Semi-schematic drawings of lateral-line scales (anterior to left) (A); ventral view of pelvic girdle (B); and lateral view of caudal skeleton (C) of Atopocottus tribranchius. A, BSKU 113020 (1 of 2 specimens), 26.8mm SL; B, C, BSKU 121005, 25.4mm SL. EP, epurals; HP, hypural complex; HS, haemal spine; NS, neural spine; POP, postpelvic process; PV, pelvis; SBP, subpelvic process.Bars indicate 1mm.

Fig. 3. Dorsal (A) and lateral (B) views of cephalic sensory system and dorsal (C) and lateral (D) views of skull of Atopocottus tribranchius. BSKU 121005, 25.4mm SL. CA, anterior coronal pore; CP, posterior coronal pore; F, frontal; IO, infraorbitals; IOP, posterior infraorbital pores; L, lacrimal; LLP, lateral-line pores; OCLA, lateral anterior central pore of occipital canal; OCLP, lateral posterior central pore of occipital canal; OCP, posterior medial pore of occipital canal; OLA, lateral anterior pore of occipital canal; OLP, lateral posterior pore of occipital canal; NA, anterior nasal pore; NP, posterior nasal pore; P, parietal; PM, preoperculo-mandibular pores; SO, supraorbital pore; T, postorbital pores. Shaded areas in C, D indicate cephalic pores.

Fig. 4. Uppermost preopercular spines of Atopocottus tribranchius at different growth stages, showing ontogenetic changes. BSKU 118412, 27.7mm SL (A); BSKU 103020, 26.8mm SL (B); BSKU 121007, 26.3mm SL (C); BSKU 121013, 18.4mm SL (D); BSKU 121008, 13.7mm SL (E). Bars indicate 1mm.

Fig. 8. Distributional map of Atopocottus tribranchius. 1: Akita Prefecture; 2: Yamagata Prefecture; 3: Niigata Prefecture; 4: Kyoto Prefecture; 5: Yamaguchi Prefecture; 6: northern East China Sea; 7: Kochi Prefecture; and 8: Ibaraki Prefecture. Stars indicate localities of present specimens. Akita, Yamagata, and Ibaraki based on literature records.