Epinephelus randalli, Hoshino & Senou & Nguyễn, 2024

Hoshino, Kouichi, Senou, Hiroshi & Nguy ễn, Quân Văn, 2024, Taxonomic Status of the Commercially Important Grouper, Epinephelus bruneus and E. moara (Osteichthys: Perciformes: Epinephelidae), with the Redescription of E. bruneus and the Description of a New Species, Species Diversity 29 (2), pp. 389-407 : 399-404

Epinephelus randalli sp. nov.

[English name: Mud Grouper; new standard Japanese name: Minami-kue] ( Figs 4d–f , 5b, f , 7 )

Serranus brunneus (non Bloch): Günther 1859: 107 (description; China); Fowler and Bean 1930: 260–261 (description; Kowloon, China); Fowler 1937: 281 (description; China: Kowloon, Hong Kong).

Epinephelus brunneus (non Bloch): Boulenger 1895: 213– 214 (description; Canton, China); Chan 1968: 24, pl. 4 (description; Hong Kong); Cheng and Zheng 1987: 290 (key); Lee 1993: 683, pl. 72-7 (in part; picture; Taiwan).

Epinephelus moara (non Temminck and Schlegel): Jordan and Seale 1905: 9, pl. 5 (description; Hong Kong); Institute of Zoology Academia Sinica et al. 1962: 32, fig. 250 (description; South China Sea, China); Jin 1985: 19–20, fig. 357 (in part; description; Fujian, China).

Serranus fasciatomaculatus (non Peters): Fowler 1931: 292, fig. 4 (figure; Hong Kong).

Serranus mo-ara (non Temminck and Schlegel): Fowler 1937: 279 (in part; description; China).

Epinephelus bruneus (non Bloch): Lee 1990: 40, fig. 46 (in part; picture, Taiwan); Randall and Heemstra 1991: 108– 111, unnumbered figs (in part; description); Heemstra and Randall 1993: 119–120, unnumbered figs, pl. 9, fig. d (in part; description); Heemstra and Randall 1999: 2490 (in part; description); Guo et al. 2008: 107, fig. 1 (right) (description; China); Craig et al. 2011: 97–98 (in part; description); M. Liu et al. 2013: 1686, 1688–1689, fig. 1, table 1 (diagnosis; China); Nakae 2018: 101, middle fig. (description; Vietnam); Koeda 2019: 620, unnumbered fig. (description; Taiwan).

Specimens examied. Holotype. NSMT-P 66257, 143.3mm SL, fish market, Cat Ba , Hai Phong, Bac Bo Gulf (Gulf of Tonkin), Vietnam, 24 September 2002.

Paratypes. Bac Bo Gulf (Gulf of Tonkin), Vietnam: FRLM 49723, 177.6 mm SL, Ha Long Bay, Bac Bo Gulf , Ha Long Market , Ha Long City , Quang Ninh, 13 December 2014; FRLM 55580 and 55581, 106.7– 124.6 mm SL, Ha Long Bay , Bac Bo Gulf , Ha Long Market , Ha Long City , Quang Ninh, 13 August 2015; NSMT-P 68341, 164.4 mm SL, Long Chau – Cat Ba islands , 22 September 2002; NSMT-P 68411, 334 mm SL, collected with NSMT-P 68341 . Hong Kong: CAS-SU 9278, 110.6 mm SL, 22°13.2 ′ N, 114°10.8 ′ E, date unknown; CAS-SU 30298, 154.7 mm SL, March 1934; CAS-SU 31247, 151.1 mm SL, 4 January 1934 .

Diagnosis. Serrae at angle of preopercle abruptly and remarkably enlarged from dorsal to ventral direction ( Fig. 4d–f ); dorsal-fin soft rays 13–14; scales on lateral body cycloid except ctenoid at pectoral region; back and side with six oblique transversal bars, second bar steeply oblique not becoming nearly horizontal ventral to lateral line, reaching opercular margin dorsal to and ventral to its posterior tip ( Figs 5b , 7 ); third bar on body without an anterior branch ( Figs 5b , 7 ); fourth band on head very narrow, much narrower than diameter of pupil ( Fig. 5f ).

Description. Meristics are in Table 1, and morphometrics are in Table 2. Body elongate, compressed; deepest at (or slightly behind) dorsal-fin origin; dorsal profile gently and evenly arched. Caudal peduncle about 1/3 of body in depth.

Eye moderately large, entirely in front of middle of head. Interorbital space nearly flat, its width smaller than eye diameter. Snout moderately long, pointed, with evenly curved profile, its length longer than eye diameter. Nostrils small, subequal, directly in front of eye; anterior one with a flap posteriorly; posterior one located more dorsally, with a slightly elevated rim or absent.

Mouth oblique, large; upper jaw posteriorly reaching a vertical through rear edge of orbit (or extending beyond it; extending more in larger specimens); lower jaw projecting beyond upper jaw. Teeth on both jaws canine-like or conical, sharply pointed, slightly curved inward. Upper-jaw teeth in two series: teeth in outer series in a row, immovable, anteriormost one enlarged to form a pair of canines; teeth in inner series in a band formed by 2–3 irregular rows, depressible inward, enlarged anteriorly, two (one or two) pairs of which becoming canines, but much smaller posteriorly. Teeth in lower jaws in two series: those in outer series similar to those of upper jaw in shape and arrangement; those in inner series forming a band anteriorly, with two pairs somewhat enlarged, but in a series posteriorly, larger than corresponding teeth of outer series. Vomerine teeth small, conical, sharply pointed, curved inward, in reversed V-shaped band; palatine teeth as vomerine teeth in shape, in a narrow band. Teeth absent on tongue.

Preopercular border rounded, serrated posteriorly; serrae abruptly and remarkably enlarged at angle, 3 (2–4, usually 2–3) in number. Opercle tapering posteriorly, with three spines, middle one longest. Margin of interopercle smooth. Gill rakers pointed, short, much shorter than gill filaments; rudimentary at uppermost and lowermost parts of gill arch.

Dorsal fin originating posterior to upper end of gill opening and anterior to end of opercular flap; base of spiny portion longer than that of soft-ray portion; dorsal-fin spines, with evenly rounded margin, longest at fourth (third to fifth) spine; last spine slightly longer than penultimate; membrane of spinous portion of dorsal fin deeply incised. Anal fin short-based, originating ventral to base of first or second dorsal-fin soft ray; first spine short; second spine slightly shorter than (or subequal to), and somewhat stronger than third; longest soft ray subequal to (or slightly longer than) that of dorsal fin. Caudal fin broadly rounded. Pectoral fin subsymmetrical, rounded posteriorly, extending to vertical through base of eighth to nineth dorsal-fin spine. Pelvic fin short, falling slightly short of (or reaching) vertical through posterior end of pectoral fin when depressed.

Scales small, cycloid on body, head, caudal peduncle, and basal part of each fin, but ctenoid in pectoral region of body; maxillary scaled. Lateral line high, complete, gently curved following dorsal contour, straight in caudal peduncle, ending at base of caudal fin.

Body light brown in the specimens preserved in alcohol (darker in fresh specimens; Koeda 2019; Fig. 7c ), with six broad oblique transverse dark brown bars on back and side, more oblique anteriorly (bars blurred in some paratypes; Fig. 7b, c ); first bar originating slightly posterior to dorsal-fin origin and immediately bending forward; second bar beginning at anterior portion of spiny dorsal fin, gently curved anteriorly and remaining steep, reaching to opercle dorsal to and ventral to its posterior tip, and to pectoral-fin base ( Fig. 5b ); third bar originating at posterior portion of spiny dorsal fin, without an anterior branch ( Fig. 5b ); fourth and fifth bars originating from soft-ray portion of dorsal fin; sixth bar on caudal peduncle distinctly split (margin of bars variably broken into irregular short lines or dots in some paratypes). Whitish spots of variable size scattered in bars.

Four dark brown bands on head radiating from eye: first band from upper margin of eye to nape; second band from snout, through eye, to confluent with first bar of body; third band from posterior margin of eye, bifurcated at posterior margin of preopercle, its upper branch confluent with dorsal part of second bar of body, its lower branch ending at posterior margin of opercle; fourth band much narrower than diameter of pupil, from lower margin of eye and ending at posterior margin of preopercle. No white margin of fins, except caudal fin margin weakly white. No yellowish area of fins in fresh specimens ( Koeda 2019; Fig. 7c ).

Distribution. South China Sea: Vietnamese coast of Bac Bo Gulf (Gulf of Tonkin) ( Nakae 2018; this study); Chinese coast of Bac Bo Gulf (Beihai), Hainan Island (Sanya), Swatow and Jieshi ( Institute of Zoology Academia Sinica et al. 1962); Hong Kong ( Jordan and Seale 1905; Chan 1968; this study); Canton ( Boulenger 1895; Fowler 1937); Fujian ( Cheng 1963; Jin 1985; Guo et al. 2008; M. Liu et al. 2013); Penghu Islands ( Heemstra and Randall 1993), southern part of Taiwan ( Koeda 2019). The northern limit of E. randalli seems, from the records of references identifiable as this species, southern Fujian Province of China (M. Liu et al. 2013) and Penghu Islands of Taiwan ( Heemstra and Randall 1993) ( Fig. 6 ). This species is also recorded from the western coast of Bac Bo Gulf, south to Lang Co of Thua Thien Hue Province ( Nguyen et al. 2021) ( Fig. 6 ). The localities of the type series and those reported in references identifiable as E. randalli are mapped on Fig. 6 . The record from Philippines by Elera (1895) listed as “ Serranus brunneus ” (not accompanied by description and illustration) might represent E. randalli . However, further study is needed to confirm the distribution of E. randalli or E. bruneus in Philippines.

Etymology. The specific name randalli is named in honor of the distinguished ichthyologist late Dr. John E. Randall, who passed away in 2020. In the new standard Japanese name, Minami-kue, “minami” is “south” or “southern” in Japanese, and “kue” is the Japanese name of the longtooth grouper.

Comparison. Epinephelus randalli can be distinguished from all other species of the Epinephelidae other than E. bruneus by the combination of characters used to distinguish the lectotypes of E. bruneus and S. moara and their original illustrations from other epinephelids (see above). Epinephelus randalli and E. bruneus can be distinguished from one another by the following characters: the number of dorsal-fin soft rays (13–14, usually 13 in E. randalli vs. 14–16, usually 15 in E. bruneus ) ( Tables 1, 3), and the size and number of serrae at the preopercular angle (abruptly and remarkably enlarged vs. gradually and slightly enlarged; 2–4, usually 2–3 vs. 2–11, usually 4–7) ( Fig. 4 ; Table 4); these characters were proposed by Guo et al. (2008) and M. Liu et al. (2013) to separate their “ E. bruneus ” from “ E. moara ”. In addition, the two species are distinguished by the following characters: the scales on the side of the body (cycloid except ctenoid in the pectoral region in E. randalli vs. mostly ctenoid in E. bruneus ), the orientation of the second bar on the body ventral to the lateral line (not turned anteriorly, steeply oblique vs. abruptly turned anteriorly becoming nearly horizontal) ( Fig. 5a, b ), position of the second bar reaching the opercle (dorsal and ventral to the posterior tip of the opercle vs. only dorsal to the posterior tip) ( Fig. 5a, b ), the anterior branch of the third bar of the body (absent vs. present) ( Fig. 5a, b ), and the width of the fourth band of the head (narrower than the diameter of pupil vs. as broad as or broader than eye diameter) ( Fig. 5e, f ). The “southern form” (= “ E. bruneus ” of M. Liu et al. 2013) can be identified as E. randalli , because the characters of the former demonstrated by Guo et al. (2008) and M. Liu et al. (2013: fig. 1b, table 1) agree with those of E. randalli .

Additionally, M. Liu et al. (2013) pointed out that the white margins of the vertical and pelvic fins in “ E. moara ” (= E. bruneus ) (n=10), are present irrespective of body size (188–602 mm TL), whereas they were not observed in “ E. bruneus ” (= E. randalli ). However, in the present study, the white margins of the fins in E. bruneus were clear in relatively large specimens (189.2–373 mm SL) but not clear, or absent, in some smaller specimens (62.2–186.3 mm SL; Fig. 1b ). Further, in the holotype and all of the paratypes of E. randalli , the caudal-fin margin was weakly white ( Fig. 7 ). Therefore, E. bruneus specimens at or larger than 188 mm TL (according to M. Liu et al. 2013) may be distinguished from E. randalli specimens by the white margins of the fins, but in smaller specimens the variation in intensity of the white margins, and the weakly white margin of the caudal fin in E. randalli , should be taken into consideration.

M. Liu et al. (2013) also pointed out that the margin of the dorsal fin, and the upper and lower margins of the caudal fin are yellowish (orange or greenish-yellow) in “ E. moara ” (= E. bruneus ), but not in “ E. bruneus ” (= E. randalli ). The yellowish margins of the dorsal and caudal fins were observed in most of the fresh images of the examined specimens of E. bruneus ( Fig. 1a, c ) and were confirmed in some pictures in references (e.g., Okada et al. 1935: pl. 66; Katayama 1984: pl. 117, fig. I; Shen 1984: pl. 40, fig. 289-24; Machida 1985). On the other hand, in the fresh images of E. randalli of a paratype ( Fig. 7c ) and in the literature ( Heemstra and Randall 1993: pl. 9; M. Liu et al. 2013: fig. 1; Nakae 2018: 101; Koeda 2019: 620) (as E. bruneus ), the fin margins are not yellowish. This character is likely to be a useful field identifier in areas where both E. bruneus and E. randalli are distributed (e.g., Fujian, China).

Remarks. In many previous studies, the “southern form” was described and/or illustrated but misidentified as “bruneus ” (often misspelled as “ brunneus ”) or “moara ” (or spelled as “ mo-ara ”) and combined with either Epinephelus or Serranus , as discussed below. The misidentifications may be attributed to the poor condition of the type specimen of E. bruneus , and the “deformed” illustration of the original description ( Bloch 1793) ( Fig. 2a ). It should be emphasized that the description of E. randalli as a new species is due in part to Guo et al. (2008) and M. Liu et al. (2013) who established that there were two species of longtooth grouper, and who documented useful distinguishing characters. The present study is supplementary to these studies, resolving the nomenclatural problems and offering additional diagnostic characters.

The species now identified as E. randalli was first reported by Günther (1859) from China, but it was identified as Serranus brunneus [sic]. His description (ditto: 107) of “Brown with six darker cross-band, inclining forwards as they descend”, “cheeks with oblique darker bands” and the dorsal-fin rays (XI, 13) expresses the characters of E. randalli . He also briefly described “ Serranus moara ” (= E. bruneus ) from Japan, in which the count of dorsal-fin rays was expressed as XI, 15.

Subsequently, Boulenger (1895) described “ E. brunneus ” from Canton. From his description, “D XI 13”, “3 or 4 enlarged serrae at the preopercle”, “Scales mostly cycloid”, “Brown with five or six oblique darker cross-band, which may be broken up into spots below the lateral line”, “Oblique dark streaks from the eye to the cheek and opercle”, the fish can be identified as E. randalli .

Jordan and Seale (1905) described “ E. moara ” from Hong Kong with a fine illustration ( Fig. 8a ). It can be undoubtedly identified as E. randalli from the pattern of the body bars and the head bands in the illustration, and the description “D XI, 13”, “preopercle denticulate with rather strong teeth at angle”, “4–5 dusky vertical bars on posterior of body, more or less broken up and sloping towards head anteriorly”.

Fowler and Bean (1930) described “ S. brunneus ” examining specimens from Kowloon, China (adjacent to Hong Kong). Their description “preopercle edge minutely serrae and three spines at angle”, “D XI 13 or 14”, “six transverse oblique cross band” and “oblique dark streaks from eye over postocular and cheek” indicates that their specimens were E. randalli . Fowler (1937) again described “ S. brunneus ” based on the specimens from Kowloon and Hong Kong, demonstrating essentially the same data as in Fowler and Bean (1930). Fowler (1937) also described “ S. mo-ara ” but without examining any specimens. He cited “ E. moara ” of Jordan and Seale (1905), that can be clearly identified as E. randalli as noted above, in the synonym list and showed the count of dorsal-fin rays as XI, 13 to 15. This indicates that in his description of “ S. mo-ara ”, the data of E. bruneus and E. randalli are combined.

Fowler (1931: fig. 4) illustrated the fish identified as “ S. fasciatomaculatus ( Peters, 1865) ” ( Fig. 8b ). However, the fish can be inconspicuously identified as E. randalli from the body bars, 13 dorsal-fin soft rays and three remarkably enlarged serrae at the preopercular angle.

The illustrations of “ E. moara ” by the Institute of Zoology Academia Sinica et al. (1962: 302, fig. 250), Cheng (1963: 218, fig. 162) and Jin (1985: 20, fig. 357) can be identified as E. randalli from the patterns of body bars and head bands, but the body scales are described as “small ctenoid”, which disagrees with E. randalli (cycloid scales except in the pectoral region). This may represent confusion with data taken from E. bruneus . One of the specimens Cheng (1963) examined (Cat. No. 59s-0285) is likely to represent E. bruneus from its locality, Shanghai, along the coast of East China Sea.

The specimens examined by Randall and Heemstra (1991) identified as E. bruneus apparently include E. randalli , because the range of dorsal-fin soft rays is 13–15 covering the two species, and the scales are described as “on some specimens ctenoid except anterodorsal, on thorax, and abdomen” (representing E. bruneus ) and “on others ctenoid only in pectoral region” (representing E. randalli ). In Heemstra and Randall (1993), the picture of d) in plate ix (437 mm SL, Penghu Islands, Taiwan) identified as E. bruneus apparently represents E. randalli from its remarkably enlarged serrae at the preopercular angle, and the pattern of bars on the body (considerably blurred but the second bar being oblique not becoming horizontal and reaching the opercular margin dorsal to and ventral to its posterior tip). The same picture is demonstrated in Lee (1990: fig. 4b) and Lee (1993: pl. 72-7) although the locality is not given.

Variations of body color are noticed within the type series of E. randalli and the references. The margins of the body bars were variably broken into spots in one paratype (CAS-SU 030298). The body bars with broken margins were described by Boulenger (1895) and illustrated by Jordan and Seale (1905) ( Fig. 8a ). The picture in M. Liu et al. (2013: fig. 1b) of their “ E. bruneus ” also well represents the broken margins of the body bars. The bars were more or less blurred in some paratypes ( Fig. 7b, c ), but the oblique (not horizontal) orientation and relation with the opercular margin (reaching dorsal to and ventral to its posterior tip) of the second bar characteristic of E. randalli are discernible ( Fig. 7b, c ).

The white spots in the body bars are variable in size and number. The holotype of E. randalli (NSMT-P 66257: Fig. 7a ) had relatively large and few spots, but paratypes had smaller and more numerous spots in the bars ( Fig. 7b ). Guo et al. (2008) and M. Liu et al. (2013) pointed out that their “ E. bruneus ” (= E. randalli ) had smaller white spots in the bars compared to “ E. moara ” (= E. bruneus ). The illustration by Fowler (1931) ( Fig. 8b ) well represents the character, which has not been observed in E. bruneus by the present authors. However, it seems difficult to clearly distinguish the two species by this character alone, due to the intraspecific variation in E. randalli .

Notes on fishery, aquaculture, and conservation. The genetics, fishery, and conservation of E. randalli has been studied under the scientific name of E. bruneus (e.g., Guo et al. 2009, 2014; To and Sadovy de Mitchenson 2009; M. Liu et al. 2013; Vo et al. 2013, 2016; To et al. 2018; Nguyen et al. 2019). The artificial production of juvenile E. randalli at commercial levels has not yet been reported. However, we caution against introducing juvenile specimens of E. randalli outside its natural distribution (e.g., Japan), which may result in the introduction of the exotic species and disruption of the local ecosystem. Similarly, the introduction of “real” E. bruneus to the coast of the South China Sea beyond its natural distribution is also cautioned against. E. randalli was once one of the most abundant groupers in Hong Kong in the 1960’s and 1970’s ( Chan 1968; To et al. 2018). Its population data are limited, but in Hong Kong, significant reductions are observed in landings and body size, and the species is assessed as “Vulnerable” in the Red List of IUCN (To et al. 2018) under the name Epinephelus bruneus . The use of correct scientific names is highly recommended for appropriate development of stock management, aquaculture, and conservation of the longtooth and mud groupers.

Figures

Fig. 4. Variation of serrae of the preopercular angle in Epinephelus bruneus (= “northern form”; a–c) and E. randalli sp. nov. (= “southern form”; d–f). a, KPM-NI 26999, 186.3mm SL, Japan; b, KPM-NI 26963, 120.2mm SL, Japan; c, KPM-NI 35270, 769mm SL, Japan; d, NSMT- P 66257, 143.3mm SL, Vietnam, holotype; e, NSMT-P 68341, 164.4mm SL, Vietnam, paratype; f, NSMT-P 68411, 334mm SL, Vietnam, paratype.

Fig. 5. Second and third bars of body (a–d) and fourth bar of head (e–g) of Epinephelus bruneus (= “northern form”) and E. randalli sp. nov.(= “southern form”). a, e, Epinephelus bruneus, KAUM–I. 80316, 224.7mm SL, Japan; b, f, E. randalli sp. nov., NSMT-P 66257, 143.3mm SL, Vietnam, holotype; c, g, original illustration for description of E. bruneus (Bloch 1793); d, original illustration for description of Serranus moara (Temminck and Schlegel 1843). Downward arrow, second bar of body ventral to lateral line; upward arrow, anterior branch of third bar of body; rectangle, fourth bar of head.

Fig. 7. Epinephelus randalli sp. nov. a, NSMT-P 66257, holotype, 143.3mm SL, Hai Phong, Vietnam; b, NSMT-P 68411, paratype, 334mm SL, Long Chau Bay, Vietnam; c, FRLM 49723, paratype, 177.6mm SL, Ha Long, Vietnam. a, b, Images of preserved specimens; c, an image of a fresh specimen.

Fig. 6. Distribution of Epinephelus bruneus and E. randalli sp. nov. Type locality of Serranus moara (= E. bruneus, solid circle); localities of E. bruneus specimens examined in this study (large open circles on magnified map); localities of E. bruneus in references (small open circles on wide area map); type locality of E. randalli sp. nov. (solid square); localities of paratypes of E. randalli sp. nov. (large open squares); localities of E. randalli sp. nov. in references (small open squares).

Fig. 1. Epinephelus bruneus. a, KAUM–I. 80316, 224.7mm SL, Japan; b, KPM-NI 26963, 120.2mm SL, Japan; c, KPM-NI 35270, 769mm SL, Japan.

Fig. 2. Illustrations of Epinephelus bruneus Bloch, 1793 and Serranus moara Temminck and Schlegel, 1843. a, Published illustration in original description of E. bruneus; b, its original illustration deposited in ZMB; c, original illustration for description of S. moara deposited in RMNH.

Fig. 8. Illustrations of Epinephelus randalli sp. nov. that are misidentified in references. a, Illustration in Jordan and Seale (1905: pl. 5) as “Epinephelus moara”; b, illustration in Fowler (1931: fig. 4) as “Serranus fasciatomaculatus”.