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Careproctus iacchus, a new variegated snailfish (Liparidae) from the Seas of Japan and Okhotsk

  • Yoshiaki Kai
  • Akira Tohkairin
  • Kunihiro Fujiwara
  • Tomonori Hamatsu
Full Paper

Abstract

A new species of snailfishes, Careproctus iacchus, is described on the basis of three specimens collected from the Seas of Japan and Okhotsk. Among the species of Careproctus, the new species is most similar to Careproctus comus and Careproctus faunus, both known from the Aleutian Islands, in having a variegated body coloration. However, it can be distinguished in having 44–46 dorsal- and 39–40 anal-fin rays (vs. 50–56 and 44–50 in C. comus and 47–51 and 41–45 in C. faunus, respectively), a pectoral fin without a notch (vs. both with a shallow notch), no interradial fenestra between proximal radials two and three in the pectoral girdle (vs. both having a fenestra between proximal radials two and three), a gill slit entirely above the pectoral fin (extending to just above the pectoral fin or to 1–5th ray), a body with many white spots (vs. mottled with red and white), and a large white blotch on cheek (vs. no distinct markings on cheek) when fresh.

Keywords

Careproctus comus Careproctus faunus New species COI Western North Pacific 

Introduction

The snailfish family Liparidae is a species-rich group, comprising over 420 species in about 30 genera (Chernova et al. 2004; Murasaki et al. 2017), and its speciation and phenotypic evolutionary rates are estimated to be fastest in the marine fishes (Rabosky et al. 2013). Many species of snailfish are uncommon or rare and several are only known from holotypes (Sakurai and Shinohara 2008), and large number of new species are still being described (e.g., Stein 2012; Gerringer et al. 2017). In addition, recent molecular studies also recognized many species awaiting to be described (Kai et al. 2011; Orr et al. 2015; Gardner et al. 2016). Careproctus Krøyer 1862 is the most species-rich genus in the family including over 100 species, about 30 of which are known from the North Pacific (Orr 2016). According to Orr and Maslenikov (2007), Careproctus can be diagnosed by the following combination of characters: one pair of nostrils; pseudobranch absent; pelvic disk present; pectoral fins typically with fewer rays than anal fin; body color uniformly dark or light, when light often gradually darkening posteriorly, rarely variegated.

To date, only two species of Careproctus with a variegated coloration have been described: Careproctus comus Orr and Maslenikov 2007 and Careproctus faunus Orr and Maslenikov 2007, both known from the Aleutian Islands. After Orr and Maslenikov (2007), Tohkairin et al. (2015) reported an unidentified specimen of Careproctus with variegated color from the Sea of Okhotsk. Recently, two additional specimens of the same species were collected from the Sea of Japan. These three specimens are clearly different from C. comus and C. faunus and, therefore, described as a new species in this paper.

Materials and methods

Counts, measurements, and descriptive terminology follow Orr and Maslenikov (2007). Counts of median-fin rays and vertebrae were taken from radiographs. The right pectoral girdle of the holotype was dissected and stained by alcian blue and alizarin red following the methods of Kawamura and Hosoya (1991). Standard length was abbreviated as SL. Data of the holotype are given first, followed by data of the paratypes, in parentheses, if different from holotype. The specimens examined in this study are deposited in the fish collections of the Kyoto University, Kyoto and Maizuru, Japan (FAKU), the Hokkaido University Museum, Hakodate, Japan (HUMZ), National Museum of Nature and Science, Tsukuba, Japan (NSMT), the Smithsonian Institution, National Museum of Natural History, Suitland, USA (USNM), and the Burke Museum, University of Washington, Seattle, USA (UW).

For DNA barcoding, total DNA of the holotype and one of the paratypes was extracted from muscle tissue or fin clips preserved in 99.5% ethanol, using the Wizard Genomic DNA Purification Kit (Promega Inc.), according to the manufacturer’s protocols. The partial cytochrome oxidase subunit I (COI) gene was amplified following Gardner et al. (2016). The PCR products were purified with ExoSAP-It (USB Corporation) enzyme. Automated sequencing was performed for both directions, using the BigDye terminator sequencing kit (Applied Biosystems) and analyzed on a model 310 Sequencer (Applied Biosystems). All sequences are available from INSDC (International Nucleotide Sequence Database Collaboration) under accessions LC349295 and LC349296. Sequence similarity searches were performed using DDBJ (DNA Data Bank of Japan) BLASTn (http://ddbj.nig.ac.jp/blast/blastn). The uncorrected p-distance was calculated with MEGA7 (Kumar et al. 2016).

Careproctus iacchus sp. nov.

(New Japanese name: Oboro-bikunin; Figs. 1, 2; Table 1)
Fig. 1

Careproctus iacchus sp. nov. in fresh condition: a holotype, FAKU 145603, 42.6 mm SL; b paratype, FAKU 201379, 39.2 mm SL [modified from Tohkairin et al. (2015) with permission]

Fig. 2

a Cephalic pores and b pectoral girdle of Careproctus iacchus sp. nov., holotype, FAKU 145603, 42.6 mm SL. Shaded area represents cartilage. Bars 5 mm

Table 1

Proportional morphometric characters for individuals of Careproctus iacchus sp. nov.

 

Holotype

Paratypes

FAKU 145603

FAKU 201379

NSMT-P 109786

Standard length (mm)

42.6

39.2

37.2

In % of standard length

 Head length

25.6

25.9

26.8

 Snout length

7.7

7.3

9.1

 Orbit length

6.5

6.9

6.5

 Interorbital width

9.3

10.3

9.2

 Mouth width

12.1

11.0

12.4

 Maxilla length

9.1

9.5

9.4

 Gill slit length

4.6

-

4.0

 Body depth at pelvic disk

19.4

20.0

20.0

 Body depth at anal-fin origin

15.8

14.4

13.8

 Pectoral-fin length

22.2

23.5

20.3

 Predorsal length

28.3

27.9

31.1

 Preanal length

41.5

38.9

37.5

 Pelvic disk length

7.6

7.6

9.0

 Pelvic disk width

6.6

8.6

7.1

 Caudal-fin length

13.0

14.8

15.4

In % of caudal fin

 Dorsal-fin connection to caudal fin

34.2

26.6

22.7

 Anal-fin connection to caudal fin

36.3

38.9

31.4

Careproctus sp.: Tohkairin et al. 2015, 10, pl. VII, fig. 4, Sea of Okhotsk.

Holotype. FAKU 145603, 42.6 mm SL, female, 39°07.94′N, 138°48.59′E–39°08.51′N, 138º47.97′E (Mogami Bank, Sea of Japan), 302–313 m, R/V Mizuho-maru, 20 Jul. 2016, coll. by K. Fujiwara and Y. Yagi (INSDC accession: LC349296).

Paratype. FAKU 201379, 39.2 mm SL, female, 44°21.80′N, 143°55.40′E (off Hokkaido, Sea of Okhotsk), 163 m, R/V Kaiyo-maru No. 5, 19 Apr. 2014, coll. by A. Tohkairin (INSDC accession: LC349295). NSMT-P 109786, 37.2 mm SL, 44°43.63′N, 140°5.65′E–44°43.12′N, 140°5.44′E (Musashi Bank, Sea of Japan), 152–170 m, R/V Tansei-maru, 27 May 2011, coll. by M. Nakae.

Diagnosis. A species of Careproctus with the following combination of characters: vertebrae 49–52; dorsal-fin rays 44–46; anal-fin rays 39–40; pectoral-fin rays 36; pectoral fin without distinct notch; proximal pectoral radials 4 (3 + 1), no interradial fenestra between proximal radials 2 and 3; snout protruding beyond tip of premaxilla; pupil longitudinally oval or reduced to slit; gill slit entirely above pectoral fin; teeth trilobed; body pinkish with many white spots; cheek with white large blotch.

Description. Measurements are shown in Table 1. Paratype data are given in parentheses if different from the holotype.

Body somewhat elongated tapering posteriorly, rounded in cross section anterior to anus, deepest at nape. Skin thin and fragile, prickles absent. Head robust and moderately large, dorsal profile slightly sloping from nape to snout. Snout rounded, protruding beyond tip of premaxilla. Mouth subterminal and small, maxilla extending to posterior margin of pupil, oral cleft extending to anterior point of pupil. Premaxillary teeth trilobed in 5 (4–5) oblique rows; inner teeth larger. Mandibular teeth trilobed in 5 oblique rows; inner teeth larger. Diastema absent at symphysis of upper and lower jaws. Orbit relatively small, pupil longitudinally oval (elliptical or reduced to slit). Nostril single, with short tube at level with upper part of orbit. Pores of cephalic lateralis of large size: nasal pores 2, maxillary pores 6, preoperculomandibular pores 7, suprabranchial pores 2 (damaged in one of paratypes, FAKU 201379); cephalic pore pattern 2-6-7-2 (Fig. 2a). Chin pores paired in separate pits. Interorbital pore absent. Gill slit moderate, upper margin at level of dorsal rim of orbit, entirely above pectoral fin (damaged in one of paratypes, FAKU 201379). Opercular flap angular, pointing posterodorsally.

Vertebrae 50 (49–52), precaudal 10 (9–10) and 40 (40–42) caudal. Dorsal-fin unlobed, rays 46 (44–46). Anteriormost dorsal-fin pterygiophore inserted between neural spines 3 and 4, bearing single ray. Membrane of posterior dorsal-fin rays continuous with caudal fin. Anal-fin rays 39 (39–40). Anal-fin origin below vertebrae 13 (12–13). Membrane of posterior anal-fin rays continuous with caudal fin. Caudal fin truncate. Principal caudal-fin rays 10 (10–11). Hypurals and parhypural fused into single plate. Pleural ribs 2 pairs, on abdominal vertebrae 9 and 10 (8 and 9).

Pectoral fin without distinct notch, with 36 rays, just reaching to (slightly beyond) level of anal-fin origin. Tip of pectoral-fin rays free of membrane, lower rays more strongly exserted. Rays 23–32 (21–32), slightly more widely spaced than other rays. Uppermost pectoral-fin base level with lower part of orbit. Lowermost pectoral-fin base below posterior rim of orbit (pupil). Proximal pectoral radials 4 (Fig. 2b). Third proximal radial weakly notched. Interradial fenestra between scapula and proximal radial 1; no other interradial fenestra. Scapula with strong helve, extending to uppermost proximal radial. Coracoid triangular with lamina (partly damaged in holotype). Distal radials present at base of uppermost to 24th pectoral-fin rays, more ventral radials reduced or absent (status of paratypes unknown). Pelvic disk round, moderate in size, approximately equal to orbital diameter. Anus closer to pelvic disk than to anal-fin origin.

Color when fresh (Fig. 1). Head and body dusky pinkish (yellowish) with white spots, becoming irregular white markings ventrally; cheek with large white marking. Distal margins of posterior dorsal and anal fins somewhat dark. Caudal fin dark with indistinct pale stripes. Pectoral fin white, basal part somewhat reddish. Pelvic disk white. Cephalic pores white. Lower half of eye silvery. Stomach and peritoneum white.

Color in alcohol. Head and body pale; spots and markings when fresh vanished. Distal margins of posterior dorsal and anal fins somewhat dark. Caudal fin dark. Pectoral fin and pelvic disk white. Stomach and peritoneum pale.

Distribution. Known only from the northern Sea of Japan and the southern part of Sea of Okhotsk, off Yubetsu, Hokkaido, Japan at depth of 152–313 m (Fig. 3).
Fig. 3

Distribution of Careproctus iacchus sp. nov. Star indicates the collection site of the holotype; circles indicate those of paratypes

Etymology. Named after the Roman god, Iacchus, the half-brother of Comus and Faunus, because of the close similarity of the new species to Careproctus comus and Careproctus faunus. Iacchus is a child-god who is forever young, also referring to the small size of this species.

Comparison. Among the species of Careproctus from the North Pacific, the new species is most similar to C. comus and C. faunus in having a variegated body coloration. However, it is distinguishable from both in having 44–46 dorsal- and 39–40 anal-fin rays (vs. 50–56 and 44–50 in C. comus and 47–51 and 41–45 in C. faunus, respectively), a pectoral fin without a notch (vs. both with a shallow notch), no interradial fenestra between proximal radials two and three in the pectoral girdle (vs. both having a fenestra between proximal radials two and three), and a gill slit entirely above the pectoral fin (vs. extending to just above the pectoral fin or to 1–5th ray) (Orr and Maslenikov 2007; present study). The new species is further distinguishable from the others in having a body with many white spots [vs. mottled with red, white, and gray; fig. 1 of Orr and Maslenikov (2007)] and a large white marking on the cheek (vs. no distinct markings on cheek). Among morphometric characters, the following are useful to distinguish the new species from C. comus and C. faunus: orbit length shorter (6.5–6.9% SL vs. 8.3–11.9% SL and 8.3–12.5% SL) and pectoral fin longer (20.3–23.5% SL vs. 15.8–22.4% SL and 17.0–22.8% SL) (Orr and Maslenikov 2007; present study). The BLASTn search (accessed on 11-12-2017) also supported the close relationships of the new species with C. comus and C. faunus. The COI sequences (478 bp) of the present new species were most similar to that of C. comus (accession number: KU053756) with high sequence identities (96%). The uncorrected p-distance within the new species was 0.2%, similar to other levels of intraspecific COI variation in Careproctus (see Gardner et al. 2016).

Careproctus nelsoni Orr 2016 and Careproctus staufferi Orr 2016 are also similar to the new species in the mottled red and pale body coloration. However, both C. nelsoni and C. staufferi can be distinguished from the new species in having lower numbers of dorsal- (40–42 and 39–41, respectively) and anal-fin rays (33–37 and 33–35, respectively) (Orr 2016).

Careproctus pycnosoma Gilbert and Burke 1912b is similar to C. iacchus in the counts of dorsal- and anal-fin rays. Although the species was long known only from the holotype, Kido (1985) reported the second specimen collected from the Aleutian Islands and described the species as having 42–45 dorsal- and 36–39 anal-fin rays. Several authors cited Kido’s (1985) record as C. pycnosoma (e.g., Mecklenburg et al. 2002; Murasaki et al. 2017), but Orr and Busby (2006) reidentified Kido’s (1985) specimens as Allocareproctus tanix Orr and Busby 2006. The holotype of C. pycnosoma has 45 dorsal- and 39 anal-fin rays, being similar to the present new species, but distinguishable from the latter in having longer orbit length (8.5% SL vs. 6.5–6.9% SL), slender body (body depth at pelvic disk: 15.3% SL vs. 19.4–20.0% SL), and short pectoral fin (15.4% SL vs. 20.3–23.5% SL).

Careproctus iacchus also shares characters of similar counts of dorsal- and anal-fin rays, trilobed teeth, and a gill slit entirely above the pectoral fin with the following three species known from the North Pacific: Careproctus attenuatus Gilbert and Burke 1912a, Careproctus marginatus Kido 1988, and Careproctus rotundifrons Sakurai and Shinohara 2008. Among these species, C. attenuatus, only known from the holotype, can be immediately distinguished from other species in having the anterior mandibular pores opening into a single pit (vs. opening as separated pores). Careproctus marginatus, known from the Pacific coast of northern Japan and Sea of Okhotsk, has significantly fewer pectoral fins than C. iacchus (25–29 vs. 36) (Kido 1988; this study). It is also distinguishable from the latter in having dorsal and anal fins broadly margined with black (vs. distal margins of posterior dorsal and anal fins somewhat dark). The counts of dorsal-, anal- and pectoral-fin rays of C. iacchus are within or near the lower end of the range of C. rotundifrons, known from the Pacific coast of Japan (off Fukushima southward to Suruga Bay); however, the former differs in having a pectoral fin without a notch (vs. with a distinct notch) and in several morphometric characters, including a longer pectoral fin (20.3–23.5% SL vs. 16.7–21.7% SL) and a larger pelvic disk (7.6–9.0% SL vs. 4.7–7.1% SL) (Sakurai and Shinohara 2008; this study).

Among other snailfishes of the North Pacific, Temnocora candida (Gilbert and Burke 1912a) is also similar to the new species in the mottled red and white body coloration. However, it can be distinguished from the new species in having a lobed dorsal fin, a pectoral fin with a distinct notch, and a small fenestra between proximal radials two and three (Gilbert and Burke 1912a; Orr and Maslenikov 2007).

Comparative materials. Careproctus attenuatus: USNM 74386, 33.6 mm SL, holotype, off Agattu Is., Aleutian Islands, USA. Careproctus comus: FAKU 120223, 84.5 mm SL, 52°10′N, 179°31′E (Aleutian Islands, USA); FAKU 120224, 82.1 mm SL, 52°10′N, 179°35′E (Aleutian Islands, USA); UW 111858, 3 paratypes, 78.1–88.6 mm SL, 52°26′N, 173°13′W (Aleutian Islands, USA). Careproctus faunus: UW 113658, 46.4–70.1 mm SL, 2 of 3 paratypes, 52°49′N, 171°26′W (Aleutian Islands, USA). Careproctus marginatus: HUMZ 72755, holotype, 174.7 mm SL, 41°58.3′N, 143°46.1′E, off Pacific coast of Hokkaido, Japan; FAKU 132187, 132191, 153.9–155.7 mm SL, Pacific coast of Tohoku District, Japan; FAKU 200478, 176.9 mm SL, southern part of Okhotsk Sea, Japan. Careproctus pycnosoma: USNM 73340, holotype, 39.8 mm SL, 46°42′N, 151°45′E (Simushir Island, Russia). Careproctus rotundifrons: NSMT-P 76691, 97.9 mm SL, holotype, 35°13.55′N, 139°22.35′E (Sagami Bay, Japan).

Notes

Acknowledgements

We greatly appreciate the captains and crews of R/V Mizuho-maru, Kaiyo-maru No. 5, and Tansei-maru for the collection of new species. Our appreciation is also extended to G. Shinohara and M. Nakae (NSMT), M. Yabe, H. Imamura, and T. Kawai (HUMZ), J. T. Williams, D.G. Smith, S. Raredon, and K. Murphy (USNM) for access to collections, and K. P. Maslenikov (UW) for the loan of specimens. J. W. Orr (NOAA, Alaska Fisheries Science Center) provided the X-rays of paratypes of C. comus and C. faunus and critically reviewed the manuscript.

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Copyright information

© The Ichthyological Society of Japan 2018

Authors and Affiliations

  1. 1.Maizuru Fisheries Research Station, Field Science Education and Research CenterKyoto UniversityMaizuruJapan
  2. 2.Fisheries Technology DepartmentKyoto Prefectural Agriculture, Forestry and Fisheries Technology CenterMiyazuJapan
  3. 3.Japan Sea National Fisheries Research InstituteJapan Fisheries Research and Education AgencyNiigataJapan
  4. 4.Hokkaido National Fisheries Research InstituteJapan Fisheries Research and Education AgencyKushiroJapan

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