Research Article |
Corresponding author: Shaoxiong Ding ( sxding@xmu.edu.cn ) Academic editor: Maria Elina Bichuette
© 2020 Haohao Wu, Meng Qu, Hungdu Lin, Wei Tang, Shaoxiong Ding.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Wu H, Qu M, Lin H, Tang W, Ding S (2020) Epinephelus tankahkeei, a new species of grouper (Teleostei, Perciformes, Epinephelidae) from the South China Sea. ZooKeys 933: 125-137. https://doi.org/10.3897/zookeys.933.46406
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A new species of grouper, Epinephelus tankahkeei sp. nov. is described from the South China Sea based on examination of morphological and molecular characteristics. This new species has been treated as, and is similar to, its congener E. chlorostigma. Epinephelus tankahkeei sp. nov. can be distinguished from E. chlorostigma by the following combination of characters: a convex anal fin; closer dark spots on the body; a lack of dark spots on the abdomen, cheek, and pectoral fin; the absence of a clear posterior white margin on the caudal fin. Molecular analyses of the mitochondrial COI sequence variation, genetic distances, and a phylogeny, all highly support E. tankahkeei sp. nov. as a distinct species. A key to E. tankahkeei sp. nov. and its most closely related species is provided.
Epinephelidae, Epinephelus tankahkeei, groupers, new species, South China Sea
The groupers are an assemblage of reef fishes in the perciform family Epinephelidae (
In recent years, we collected a new form of grouper from the South China Sea that had been previously regarded as Epinephelus chlorostigma. Further investigation based on morphometric and molecular characteristics shows that this new form should be a new species of the genus Epinephelus. Herein, we describe this new species as Epinephelus tankahkeei. In addition, a key to E. tankahkeei sp. nov. and its most closely related species is provided.
Between 2011 and 2019, nine specimens of the new species were collected from fish markets and fishing boats in Xiamen, Shenzhen, Sansha, and Haikou, China. ODV v5.1.5 software was used to generate a collection site map (
The methods of counting and measurement followed Randall and Heemstra (1993) and include: total length; standard length (as SL); head length; snout length; body depth; body width; orbit diameter; interorbital width; preorbital depth; maxilla width; upper jaw length; lower jaw length; length of pelvic-fin and anal-fin spines; lengths of the dorsal, anal, pectoral, pelvic and caudal fins; caudal-peduncle depth; caudal-peduncle length; predorsal length; preanal length; prepelvic length; dorsal-fin base; longest hard dorsal spine; longest soft dorsal ray; anal-fin base; and length of the third anal spine, longest anal soft ray, and pelvic-fin spine. The following counts were made: gill rakers, lateral-line scales, lateral scale series, pectoral-fin rays, anal-fin rays, dorsal-fin rays, pelvic-fin rays, caudal-fin rays, and vertebras.
The procedures for DNA isolation, PCR amplification and sequencing followed
Due to the availability of data for other related species in GenBank, we chose the mitochondrial COI gene sequence to calculate intraspecific and interspecific genetic distances and perform maximum likelihood (ML) and Bayesian analyses in this study. The intraspecific and interspecific genetic distances were generated using the Kimura two-parameter (K2P) distance model with MEGA 7 (
Holotype : ZMUA-eptan06, 244.5 mm SL, Caught in Yongxing Island, Sansha, Hainan, 2 April 2017. Paratypes: ZMUA-eptan01, 111.0 mm SL, China, purchased at a fish market in Xiamen, Fujian, China, 1 September 2011, reported as collected in the south Taiwan Strait; ZMUA-eptan02, 233.2 mm SL, purchased at the Bashi market in Xiamen, Fujian, China, 22 August 2016, reported as collected in the south Taiwan Strait; ZMUA-eptan03, 215.4 mm SL, collected with the ZMUA-eptan02; ZMUA-eptan04, 262.5 mm SL, purchased at a fish market in Shenzhen, Guangdong, China, 15 February 2017, reported as collected in the South China Sea; ZMUA-eptan05, 232.6 mm SL, collected with the holotype; ZMUA-eptan07, 252.9 mm SL, purchased at a fish market in Shenzhen, Guangdong, China, 1 July 2017, reported as collected in the South China Sea; ZMUA-eptan08, 274.2 mm SL, China, purchased at a fish market in Xiamen, Fujian, China, 31 July 2018, reported as collected in the south Taiwan Strait. ZMUA-eptan09, 186.5 mm SL, China, purchased at a fish market in Haikou, Hainan, China, 22 March 2019, reported as captured using a trawl net in Mulan Bay, Wenchang, Hainan.
Epinephelus tankahkeei sp. nov. can be distinguished from all other Indo-Pacific Epinephelus species by the following characteristics: dorsal-fin rays XI, 16–18 (vs. 14–15 in Epinephelus gabriellae); anal-fin rays III, 8; pectoral-fin rays 16 or 17; lateral-line scales 47–51 (vs. 65–72 in Epinephelus polylepis); caudal fin convex (vs. slightly emarginate or truncate caudal fin in E. chlorostigma, Epinephelus areolatus, Epinephelus bleekeri, and Epinephelus geoffroyi) ; anal fin rounded (vs. angular anal fin in E. chlorostigma, and E. geoffroyi); membranes of spinous portion of dorsal fin slightly incised; head (except chest), body (except abdomen), and fins (pectoral fin spotted only basally) with numerous, irregular, close-set, dark brown spots, becoming more widely spaced on the lower part, the ground color forming a pale network (vs. lager spots in Epinephelus miliaris, and E. areolatus); rear margin of the caudal fin without a narrow white line (vs. a clear white margin posteriorly on the caudal fin in E. chlorostigma, and E. areolatus).
Dorsal-fin rays XI, 16 (16–18); anal-fin rays III, 8; pectoral-fin rays 16 (16 or 17); lateral-line scales 51 (47–51); lateral scale series 123 (111–123); gill rakers 10 (10–11) +15 (14–16); vertebra 24; body slightly elongated and body depth less than head length. Body depth contained 3.2 (3.0–3.2) in standard length. Body laterally compressed and body width 2.6 (2.1–2.6) in body depth. Head length 2.7 (2.5–2.7) in SL; orbit diameter 6.1 (4.9–6.8) in head; snout length 3.8 (3.6–4.0) in head. Dorsal profile of head nearly straight except at the snout with a slight notch before eyes. Interorbital region convex, width 6.3 (5.6– 7.2) in head; preorbital depth 7.8 (7.8–11.3) in head; caudal-peduncle length 1.9 (1.8–2.2) in head; caudal-peduncle depth 3.3 (3.2–3.7).
Mouth large and lower jaw slightly projecting and oblique. Lower jaw 3.4 (3.4–3.9) in head length; upper jaw 2.4 (2.3–2.5) in head. Maxilla slightly extending to rear edge of eye and posterior edge of maxilla slightly rounded. Maxilla width 8.1 (7.9–9.2) in head. One or two pairs of canine teeth at anterior part of the upper and lower jaw. Teeth of lower jaw form two rows and expand anteriorly into three rows; teeth in the outer side are larger than the inner side. Villiform teeth present on vomer and palatines. Tongue slender and sharp at tip. Longest gill raker was greater in length than longest gill filament. Nostrils round and posterior nostril larger than anterior nostril. Anterior nostril with a membranous flap.
Three spines on operculum, topmost and undermost small, the middle the largest. Tip of middle spine extending farther towards tail than tip of lower spine. Upper edge of opercular membrane slightly convex coming to a rounded point posteriorly. Preopercle rounded with four to five prominent spines at angle and with numerous fine serrae while increasing in size downward. Lateral line starting from posterior opercle and slightly arched over pectoral region. Scales on head, thorax, abdomen, anterodorsal part of body and fin membranes weakly ctenoid. Auxiliary scales absent. Small scales present on inner margins of dorsal, pectoral, pelvic, and caudal fins and not extending to the rear margin area.
Origin of dorsal fin before pectoral-fin base. Membranes of spinous portion of dorsal fin slightly incised. First dorsal spine contained 1.9 (1.6–2.0) times in second spine; second spine 1.2 (1.2–1.5) times in longest spine (third and fourth spine); longest spine contained 2.6 (2.6–3.1) in head length. Longest soft dorsal ray 2.4 (2.3–2.8) in head. Anal-fin origin below origin of first soft dorsal ray. First anal spine 2.0 (1.9– 2.3) times in second anal spine; second anal spine 1.2 (1.1– 1.4) times in third anal spine; third anal spine longest 3.5 (3.0–4.1) in head. Longest anal-fin rays 2.1 (1.9–2.5) in head. Caudal fin convex, 1.7 (1.6–2.0) in head. Middle pectoral rays longest, 1.8 (1.7–1.9) in head and reaching to base of 9th dorsal spine. Origin of pelvic fin slightly posterior to pectoral-fin base.
Meristics and measurements for type specimens of Epinephelus tankahkeei and E. chlorostigma. The dashes indicate that data were not collected due to specimen damage, which prevented an accurate measurement or count.
Epinephelus tankahkeei | E. chlorostigma | |||
ZMUA-eptan06 (holotype) | Range for all type specimens | ANSP 103722 | ANSP 163245 | |
Standard length (mm) | 244.5 | 111–274.2 | 281 | 398 |
Total length (mm) | 286.2 | 136.5–334.7 | 355 | 503 |
Dorsal-fin ray count | XI, 17 | XI, 16–18 | XI, 16 | XI, 16 |
Anal-fin ray count | III,8 | III,8 | III,8 | III,8 |
Pectoral-fin ray count | 16 | 16–17 | 18 | 17 |
Pelvic-fin ray count | I+5 | I+5 | I+5 | I+5 |
Lateral line scales | 51 | 47–51 | 52 | 58 |
Lateral scale series | 123 | 111–123 | 102 | 106 |
Gill rakers count | 10+15 | 10–11+14–16 | 9+14 | 8+18 |
% of SL | ||||
Body depth | 31.1 | 31.1–33.7 | 34.9 | 35.6 |
Body width | 12.2 | 12.2–15.6 | 16.3 | 18.1 |
Head length | 37.1 | 36.9–39.6 | 38.7 | 39.2 |
Snout length | 9.8 | 9.5–10.9 | 10.0 | 10.1 |
Orbit diameter | 6.1 | 5.7–8 | 7.5 | 6.1 |
Preorbital depth | 4.8 | 3.5–4.8 | 4.7 | 4.5 |
Interorbital width | 5.8 | 5.5–6.7 | 7.2 | 8 |
Maxilla width | 4.6 | 4.1–4.8 | 4.9 | 5.1 |
Upper jaw length | 15.6 | 15.6–17.1 | 18.0 | 17.5 |
Lower jaw length | 11 | 8.6–11.5 | 12.4 | 11.7 |
Caudal peduncle depth | 11.1 | 10.5–12.1 | 11.9 | 10.8 |
Caudal peduncle length | 19.2 | 18–21.1 | 20.0 | 22.7 |
Predorsal length | 34.6 | 32.4–38.8 | 36.4 | 36.5 |
Preanal length | 63.4 | 58.5–69.1 | 68.7 | 73.9 |
Prepelvic length | 36.8 | 34.8–40.8 | 38.8 | 34.7 |
Dorsal-fin base | 53.4 | 53.1–61.4 | 59.4 | 54.8 |
Longest hard dorsal ray | 14.3 | 12.4–14.4 | 15.7 | 14.3 |
Longest soft dorsal ray | 15.2 | 13.4–16.9 | 14.5 | 15.4 |
Anal-fin base | 15 | 14.8–17.3 | 15.4 | 16.2 |
Third anal spine length | 10.7 | 9.3–13.3 | 10.0 | 8.1 |
Longest anal soft ray | 17.3 | 14.9–21.1 | 15.7 | 15 |
Caudal-fin length | 22.1 | 18.7–24.2 | 25.5 | 22.3 |
Pectoral-fin length | 20.1 | 19.6–23.2 | 20.9 | 20.2 |
Pelvic-fin length | 19.5 | 18.1–21.7 | 20.4 | 17.4 |
Pelvic spine length | 11 | 9.7–12.6 | 10.4 | 9.2 |
(based on photographs of the fresh holotype and paratypes). Head (except chest), body (except abdomen), and fins (pectoral fin only basally) with numerous, irregular, close-set, dark brown spots becoming more widely spaced on the lower part and with the ground color forming a pale network (Fig.
Body yellowish-brown to tan with close-set spots remaining prominent or faded (Fig.
Mitochondrial COI gene sequences were obtained from nine specimens of E. tankahkeei. Several sequences of related species were also sequenced in this study or obtained from GenBank. E. tankahkeei has 13 species-specific mutations at nucleotide positions 126, 216, 222, 249, 276, 372, 414, 519, 525, 528, 558, 567, and 576 (Table
The new species was recently observed in the South China Sea and Taiwan Strait. Similar to other congeners, E. tankahkeei is a reef-associated species that feeds on fishes and invertebrates.
Epinephelus tankahkeei is named after Tan Kah Kee (1874–1961), who was a famous overseas Chinese educator, philanthropist, and social activist and the founder of Xiamen University and Jimei School, in honor of his significant contribution to the motherland.
Species-specific mutation sites in the COI gene for Epinephelus tankahkeei.
Nucleotide position (beginning from 5’ end) | |||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|
126 | 216 | 222 | 249 | 276 | 372 | 414 | 519 | 525 | 528 | 558 | 567 | 576 | |
Epinephelus tankahkeei | T | C | C | A | C | G | G | T | G | C | T | G | C |
Other closely related species in this study | C | A, G | T | T, C | A | A | A | A, G | C | G, A | A, G, C | A | A, T |
Analysis of the intraspecific and interspecific (K2P model) distances, interspecific distances (in lower left) and standard errors (in upper right) based on the COI locus between Epinephelus tankahkeei and closely related species; IMD = Intraspecific mean distance; SE = standard error.
Interspecific Mean Distance | |||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|
Group | Species | N | IMD | SE | 1 | 2 | 3 | 4 | 5 | 6 | 7 |
1 | Epinephelus tankahkeei | 9 | 0.0028 | 0.0010 | – | 0.0112 | 0.0100 | 0.0144 | 0.0123 | 0.0141 | 0.0122 |
2 | E. polylepis | 4 | 0.0031 | 0.0015 | 0.0771 | – | 0.0093 | 0.0144 | 0.0127 | 0.0136 | 0.0119 |
3 | E. chlorostigma | 6 | 0.0030 | 0.0013 | 0.0621 | 0.0545 | – | 0.0143 | 0.0110 | 0.0138 | 0.0110 |
4 | E. gabriellae | 2 | 0.0016 | 0.0015 | 0.1263 | 0.1142 | 0.1169 | – | 0.0148 | 0.0066 | 0.0154 |
5 | E. miliaris | 2 | 0.0000 | 0.0000 | 0.0904 | 0.0885 | 0.0730 | 0.1143 | – | 0.0143 | 0.0122 |
6 | E. geoffroyi | 2 | 0.0047 | 0.0026 | 0.1219 | 0.1073 | 0.1107 | 0.0321 | 0.1107 | – | 0.0143 |
7 | E. areolatus | 3 | 0.0031 | 0.0018 | 0.0855 | 0.0831 | 0.0641 | 0.1239 | 0.0918 | 0.1152 | – |
Epinephelus chlorostigma was formerly reported to have a wide distribution range from the Red Sea and the coast of Africa to the western Pacific Ocean. It was considered a species complex (the E. chlorostigma species complex) (
Our molecular analyses also corroborated the morphological results. In E. tankahkeei, 13 species-specific mutations were found in the COI gene fragment (Table
In the China Seas, the first record of E. chlorostigma was Serranus reevesii Richardson, 1846, type locality Canton, China (based on a painting by John Reeves) (
1a | Lateral-line scales 65–72, lateral-scale series 126–137 | E. polylepis |
1b | Lateral-line scales 47–54, lateral-scale series 92–126 | 2 |
2a | Dorsal-fin rays 14 or 15; body depth 3.2 to 3.6 times in standard length [coast of Oman, eastern border of Yemen, Somalia] | E. gabriellae |
2b | Dorsal-fin rays 16 to 18 (rarely 15 in E. areolatus); body depth 2.8 to 3.3 times in standard length | 3 |
3a | Caudal fin rounded or convex | 4 |
3b | Caudal fin slightly emarginate (truncate on some specimens of E. chlorostigma) | 5 |
4a | Body and fins with dark brown to black spots, those spots on fins (except spinous dorsal fin) much larger than those on body; lateral-scale series 92 to 108 [Indo-Pacific but not in Red Sea and Persian Gulf] | E. miliaris |
4b | Body and fins with dark brown spots, becoming more widely spaced on the lower part; lateral-scale series 114 to 123 [South China Sea and Taiwan Strait] | E. tankahkeei |
5a | Dorsal-fin rays 15 to 17; anal fin margin in adults rounded or slightly angular; dark spots on body of adults subequal to pupil [Red Sea to western Pacific] | E. areolatus |
5b | Dorsal-fin rays 16 to 18; anal fin of adults angular; largest dark spots on body of adults distinctly smaller than pupil | 6 |
6a | Posterior margin of caudal fin without a narrow, clear whitish margin; margin of anal fin distinctly angular; gill rakers 25–29 [Red Sea] | E. geoffroyi |
6b | Posterior margin of caudal fin with a narrow, clear whitish margin; margin of anal fin slightly angular; gill rakers 23–26 [Western Indian Ocean to western Pacific] | E. chlorostigma |
Epinephelus areolatus: ANSP 54826, ZMUA-epare01, ZMUA-epare02, and ZMUA-epare03.
Epinephelus chlorostigma: FLMNH_I 2006-0681, FLMNH_I 2007-1089, ANSP 162821, ANSP 163245, and ANSP 103722.
Epinephelus miliaris: FLMNH_I 2006-0784 and FLMNH_I 2006-0728.
Epinephelus polylepis: FLMNH_I 2005-1073.
Epinephelus geoffroyi: ZMUA-epgeo01 and ZMUA-epgeo02.
(See Suppl. material
We would like to thank Dr Matthew T. Craig for providing us with helpful advice on our research. We would also like to thank Dr Xuan Zhuang for giving us her constructive comments. We would like to thank the Florida Museum of Natural History, University of Florida for providing us grouper specimens. We would also like to thank Benjamin W. Frable for checking the specimens from ANSP. We would like to thank Ji Feng, Third Institute of Oceanography, Ministry of Natural Resources, for the assistance with radiographs. We would also like to thank Lei Fan, Haoran Zhang, and Xiang Zhang for assistance in specimen collection. This work was supported by the National Key R & D Program of China (2018YFD0900803) and the National Programme on Global Change and Air-Sea Interaction (GASI-02-SCS-YDsum).
Table S1. Samples information
Data type: samples data