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Ichthyological Research

, Volume 64, Issue 1, pp 104–110 | Cite as

Redescription of Lagocephalus cheesemanii (Clarke 1897), a senior synonym of Lagocephalus gloveri Abe and Tabeta 1983, based on morphological and genetic comparisons (Actinopterygii: Tetraodontiformes: Tetraodontidae)

  • Keiichi Matsuura
  • Takashi P. Satoh
Full Paper

Abstract

Lagocephalus gloveri Abe and Tabeta 1983 is shown to be a junior synonym of Tetrodon cheesemanii Clarke 1897 based on examination of morphological characters and DNA analysis of specimens collected from the western North Pacific, Australia and New Zealand. Lagocephalus cheesemanii is distinguished from other species of Lagocephalus by the following combination of characters: spinules on the back in a rhomboidal patch extending from the region between the nasal organ to the posterior part of the pectoral fin; caudal fin double emarginate with middle rays posteriorly produced; dorsal-fin rays 11–15; anal-fin rays 11–14; pectoral-fin rays 15–18; vertebrae 8+11=19; dorsal half of the body dark brown to brownish black; caudal fin dark brown to black with dorsal and ventral white tips. A neotype of L. cheesemanii is designated.

Keywords

Puffers Distribution Neotype taxonomy 

Introduction

Puffers of the genus Lagocephalus Swainson 1839 are widely distributed in the warm waters of the world (Shipp 1974; Kyushin et al. 1982; Sainsbury et al. 1985; Smith and Heemstra 1986; Mohsin and Ambak 1996; Matsuura 1997, 2001). They are easily distinguished from other tetraodontid genera by the following combination of characters: a wide, silver-white band coursing longitudinally ventral to the eye from the snout to the caudal-fin base; a longitudinal skin fold extending on the ventro-lateral corner of the body from the chin to the ventral part of the caudal peduncle; lateral lines divided into ventral and lateral elements, the ventral element coursing along the skin fold and the lateral element extending along the mid-lateral side of the body from the region dorsal to the gill opening to the caudal-fin base with the anterior extension coursing from ventral to the eye to the snout region; and two openings in the nasal organ (Matsuura 2001).

Although the genus Lagocephalus has been well recognized by many authors (Shipp 1974; Smith and Heemstra 1986; Matsuura 1997, 2001; Yamada 2002), classification at the species level in Lagocephalus has not yet been studied in depth, causing confusion about the status of several species (Matsuura 2010; Matsuura et al. 2011). Examinations of specimens of Lagocephalus collected from the western North Pacific, Australia and New Zealand enable us to conclude that Lagocephalus gloveri Abe and Tabeta 1983 is a junior synonym of Tetrodon cheesemanii Clarke 1897.

Materials and methods

Specimens used in this study are deposited in the following museums and universities: Fish Section, Natural History Museum, London (BMNH); Faculty of Agriculture, Kyoto University, Maizuru (FAKU); Kagoshima University Museum, Kagoshima (KAUM); Kanagawa Prefectural Museum of Natural History, Odawara (KPM); National Museum of New Zealand Te Papa Tongarewa (NMNZ); Department of Zoology, National Museum of Nature and Science, Tsukuba (NSMT); Department of Zoology, University Museum, University of Tokyo, Tokyo (ZUMT). Counts and measurements follow Dekkers (1975). Measurements were made with calipers to the nearest 0.1 mm. Characters shown in Diagnosis are not repeated in Description. The standard length and total length are abbreviated as SL and TL, respectively. Neotype values are presented first, followed by value ranges in other specimens examined where they differ enclosed in parentheses. Radiographs were used to count the number of vertebrae.

DNA extraction, sequencing and editing data. We examined the genetic divergence between species of Lagocephalus using mitochondrial cytochrome oxidase subunit I (COI) barcode sequences. Tissues from Lagocephalus cheesemanii and Lagocephalus guentheri (Miranda Ribeiro 1915) were kindly provided by Mark McGrouther (AMS: AMS-I. 44764-023), Alastair Graham (CSIRO: CSIRO-H 6836-12), Jeff Johnson (QM: QM-I. 38585) and Daniel Golani (Hebrew University: NSMT-DNA 19441), and those of Lagocephalus inermis (Temminck and Schlegel 1850) (NSMT-P 97703), Lagocephalus lagocephalus (Linnaeus 1758) (NSMT-P 103992), Lagocephalus lunaris (Bloch and Schneider 1801) (NSMT-DNA 17833) and Lagocephalus spadiceus (Richardson) (NSMT-P 118417)were excised from fresh specimens of each species and immediately preserved in 99.5 % ethanol. Total genomic DNA was extracted using a Gentra Puregene tissue kit (Qiagen) following the manufacturer’s protocol. PCR was carried out following protocols previously described (Miya and Nishida 1999) using four versatile fish primers: FishF1, FishR1, FishF2, and FishR2 (Ward et al. 2005). The products were purified using an ExoSAP-IT enzyme (Affymetrix) and subsequently sequenced with dye-labelled terminators (BigDye terminator ver. 3.1, Applied Biosystems). The primers used were the same as those for the PCR. Sequencing reactions were conducted following the manufacturer’s instructions, followed by electrophoresis on a 3130xl Genetic Analyzer (Applied Biosystems). Sequence data were edited and analyzed with AutoAssembler ver 2.1 (Applied Biosystems) and DNASIS ver 3.2 (Hitachi Software Engineering). After trimming uncertain bases at both ends, the aligned sequences were 636 bp long. Sequence divergences were quantified using the Kimura 2-parameter (K2P) distance model of nucleotide substitution (Kimura 1980) using PAUP* ver. 4.0b10 (Swofford 2002). All new sequences have been deposited in GenBank under accession numbers LC155433 to LC155442 with the catalog numbers of the voucher specimens.

Lagocephalus cheesemanii (Clarke 1897)

(English name: Cheeseman’s Puffer; Japanese name: Kuro-sabafugu) (Figs. 1–4; Table 1)
Fig. 1

a Neotype of Lagocephalus cheesemanii (Clarke 1897), NMMZ P. 18876, 278 mm SL, New Zealand, North Island, Taranaki, New Plymouth, off White Cliffs (38°52’S, 174°32’E), 1985. b Holotype of Lagocephalus gloveri Abe and Tabeta 1983, ZUMT 54324, 248 mm SL, Japan, Honshu, Sagami Bay, east coast of Izu Peninsula, off Futo

Fig. 2

a Dorsal view of neotype of Lagocephalus cheesemanii (Clarke 1897), NMMZ P. 18876, 278 mm SL, New Zealand, North Island, Taranaki, New Plymouth, off White Cliffs (38°52’S, 174°32’E), 1985. b Dorsal view of holotype of Lagocephalus gloveri Abe and Tabeta 1983, ZUMT 54324, 248 mm SL, Honshu, Sagami Bay, east coast of Izu Peninsula, off Futo

Fig. 3

Lagocephalus cheesemanii. a KAUM-I. 56155, 238 mm SL, Japan, Kyushu, Kagoshima Prefecture, Kagoshima Bay, off Chiringa-jima Island. b NSMT-P 96107, 221 mm SL, southern Vietnam, 65 m north of Nha Trang

Fig. 4

Original illustrations of Tetrodon cheesemanii Clarke 1897

Table 1

Frequency distributions of fin-ray counts of Lagocephalus cheesemanii

Dorsal-fin rays

11

12

13

14

15

1

5

19

19

4*

Anal-fin rays

11

12

13

14

 

3

30

14

1*

 

Pectoral-fin rays

15

16

17

18

 

1

11

32*

4

 

* Neotype

Tetrodon cheesemanii Clarke 1897: 248, pl. 15.

Lagocephalus gloveri Abe and Tabeta 1983: 2, pls. 1–3.

Specimens examined. 49 specimens, 67–309 mm SL. Japan: FAKU 99720 (135 mm SL), Honshu, Wakayama Prefecture, Kii Peninsula, Kushimoto, 14 July 2007; FAKU 75127 (207 mm SL), East China Sea (28°29.7’N, 126°30.5’E-28°30.6’N, 126°32.2’E), 136 m depth, 24 August 1999; HUMZ 105860 (293 mm SL), Honshu, Shizuoka Prefecture, Suruga Bay, off Kunou-zan Mt., 12 November 1985; KAUM-I. 7774 (150 mm SL), 7775 (156 mm SL), Kyuhsu, Kagoshima Prefecture, Osumi Peninsula, Uchinoura Bay (31°17’N, 131°05’E), 40 m depth, 27 July 2006; KAUM-I. 10987 (232 mm SL), collection locality same as the preceding, 20 July 2008; KAUM-I. 15207 (104 mm SL), Ryukyu Islands, Kikai-jima Island, 31 July 1960; KAUM-I. 21935 (181 mm SL), Kyushu, Kagoshima Prefecture, Osumi Peninsula, Ibusuki, off Yamagawa, 30–60 m depth, 27–28 July 2009; KAUM-I. 22418 (190 mm SL), 22419 (200 mm SL), collection locality same as that of KAUM-I. 21935, 40–80 m depth, 25–26 July 2009; KAUM-I. 25549 (163 mm SL), Kyushu, Kagoshima Prefecture, Satsuma Peninsula, Kasasa, off Sakinoyama (31°25.44’N, 130°11.49’E), 27 m depth, 4 February 2010; KAUM-I. 28318 (190 mm SL), Kyushu, Kagoshima Prefecture, Satsuma Peninsula, 1 km southwest off Kawajiri fishing port (31°10’N, 130°32’E), 40 m depth, 7 April 2010; KAUM-I. 55977 (211 mm SL), 55988 (201 mm SL), 55992 (199 mm SL), Kyushu, Kagoshima Prefecture, Kagoshima Bay, 28 August 2013; KAUM-I. 56155 (238 mm SL), 56156 (236 mm SL), Kyushu, Kagoshima Prefecture, Kagoshima Bay, off Chiringa-jima Island (31°16.38’N, 130°40.18’E), 25 m depth, 7 September 2013; KAUM-I. 66491 (283 mm SL), Ryukyu Islands, Tanegashima Island, off Sata Point (30°50’N, 130°45’E), 115–120 m depth, 20 August 2014; KPM-NI 91 (282 mm SL), Honshu, off southeast coast of Miura Peninsula, 11 November 1966; NSMT-P 12531 (218 mm SL), Honshu, Suruga Bay, 11 April 1969; NSMT-P 48612 (3 specimens, 142–173 mm SL), Kyushu, Goto Islands, 5 April 1995; NSMT-P 118418 (129 mm SL), Honshu, Iwate Prefecture, Kamaishi, June 2013; ZUMT 54324 (holotype of L. gloveri, 248 mm SL), 54325 (paratype of L. gloveri, 232 mm SL), Honshu, Sagami Bay, east coast of Izu Peninsula, off Futo, 24 October 1982. Korea: NSMT-P 78307 (205 mm SL), South Korea, around Cheju Island, 20 December 1982. China: NSMT-P 54880 (237 mm SL), Hainan Island, south coast of Hainan Island, 100 km south of Sanya, 23 February 1997. Vietnam: NSMT-P 96107 (221 mm SL), 96108 (250 mm SL), southern Vietnam, 65 km north of Nha Trang, 14 September 2008. Philippines: NSMT-P 92575 (141 mm SL), Visayan Sea, 16 March 2007. Indonesia: BMNH 1987.1.23:6 (164 mm SL), eastern Indian Ocean between Java and Bali (8°26S’, 114°29’E), 21 August 1980; BMNH 1987.1.23.:7–8 (2 specimens, 60.1, 72.0 mm SL), eastern Indian Ocean, south Indonesia. Australia: AMS-IB. 2561 (245 mm SL), New South Wales, 1950; AMS I. 31476-003 (67.0 mm SL), New South Wales, off Murwillumbah (28°20’S, 153°01’E–28°25’S, 153°41’E), 54–58 m depth, 2 May 1990; CSIRO C1787 (2 specimens, 237–240 mm SL), New South Wales, Port Hacking, 25 May 1953; CSIRO H5963-10, (153 mm SL), New South Wales, east of Yamba (29°23’S, 153°23’ E –29°24’S, 153°22’E), 15–16 m depth, 17 April 1966; AMS I. 25665-023 (122 mm SL), Queensland, northeast of Yamba (29°21’S, 153°29’E), 21 March 1985; AMS I. 38088-019 (122 mm SL), Queensland, east of Swain’s Reef (21°50.99’S, 153°40’E), 199 m depth, 10–11 September 1995; AMS I. 40195-008 (101 mm SL), Queensland, east of Swain’s Reef (21°50.99’S, 153°01’E–21°43.23’S, 152°57’E), 198 m depth, 10–11 September 1995; AMS I. 40492-005 (104 mm SL), Queensland, east of Swain’s Reef (22°25’S, 153°20’E–22°11.97’S, 153°12’E), 181 m depth, 9–10 September 1995; QM-I. 38585 (192 mm SL), Queensland, Moreton Island, east of Cape Moreton (27°03’S, 153°33’E), 98 m depth, 19 July 2009; CSIRO H1915-01, 02 (2 specimens, 279–280 mm SL), Western Australia, off Carnarvon (23°59.6’S, 112°47.4’E–24°00.5’S, 112°45.9’E), 16 December 1987. New Zealand: NMNZ P. 297 (201 mm SL), North Island, Taranaki, New Plymouth (39°00’S, 174°00’E), date unknown; NMNZ P. 5099 (250 mm SL), North Island, North Auckland, off Whale Island (37°40’S, 176°25’E), May 1968; NMNZ P. 18876 (neotype, 278 mm SL), North Island, Taranaki, New Plymouth, off White Cliffs (38°52’S, 174°32’E), 29 m depth, 1985; NMNZ P. 36917 (239 mm SL), North Island, North Auckland, south end of Mercury Island (36°37’S, 175°48’E), 30 m depth, 21 May 1999; NMNZ P. 45601 (220 mm SL), North Island, North Auckland, Bay of Islands, Bird Rock (35°10’S, 174°19’E), 20 m depth, 3 April 2009.

Tissue samples for DNA analysis. Australia: AMS-I. 44764-023, New South Wales, Off Coffs Harbour (GenBank Accession No.LC155433); CSIRO-H 6836-12, New South Wales (LC155434); QM-I. 38585, Queensland, Cape Moreton (LC155435). Japan: NSMT-P 100266, Shikoku, Kochi Prefecture, Hata County, Kuroshio Town, Saga fishing port (LC155437). Vietnam: NSMT-P 96108, 65 km North of Nha Trang, Qua Be (LC155436).

Diagnosis. Lagocephalus cheesemanii is distinguished from other species of Lagocephalus by the following combination of characters: spinules on the back in a rhomboidal patch, starting anteriorly between the nasal organ and the eye with the widest expansion dorsal to midway between the eye and the gill opening, tapering posteriorly and ending at the region dorsal to the posterior part of the pectoral fin; caudal fin double emarginate with middle rays posteriorly produced; dorsal half of body dark brown to brownish black; the side of head silver with dark yellowish tinge; the lower side of the body between gill opening and the caudal-fin base silver; dorsal and pectoral fins dark; caudal fin dark brown to black with dorsal and ventral white tips; dorsal-fin rays 15 (11–14); anal-fin rays 14 (11–13); pectoral-fin rays 17 (15–18); vertebrae 8+11=19 (Table 1).

Description. Head length 32.4 % SL (30.0–34.7 % SL), snout length 15.8 % SL (13.9–16.2 % SL), snout to dorsal-fin origin 65.4 % SL (63.0–67.5 % SL), snout to anal-fin origin 67.6 % SL (64.6–70.8 % SL), body width at pectoral-fin base 23.1 % SL (14.0–23.9 % SL), body depth at anal-fin origin 20.5 % SL (17.1–22.1 % SL), depth of caudal peduncle 6.3 % SL (5.3–7.0 % SL), length of caudal peduncle 20.3 % SL (19.7–23.4 % SL), gill opening length 9.2 % SL (7.9–12.3 % SL), eye diameter 7.6 % SL (6.8–8.9 % SL), bony interorbital width 14.2 % SL (10.1–14.4 % SL), snout to anterior edge of nasal organ 10.1% SL (8.2–10.9 % SL), posterior edge of nasal organ to anterior edge of eye 5.0 % SL (3.9–6.2 % SL), length of dorsal-fin base 12.5 % (9.6–15.1 % SL), length of anal-fin base 11.0 % SL (9.6–12.6 % SL), longest dorsal-fin ray 17.8 % SL (16.1–22.5 % SL), longest anal-fin ray 18.3 % SL (16.3–22.0 % SL), longest pectoral-fin ray 19.3 % SL (17.0–20.4 % SL), caudal-fin length 17.9 % SL (17.5–22.3 % SL).

Longitudinal skin fold extending on the ventro-lateral corner of the body from chin to the ventral part of caudal peduncle; the lateral lines divided into ventral and lateral elements, the ventral element coursing along the skin fold and the lateral element extending along the mid-lateral side of the body from the region dorsal to the gill opening to the caudal-fin base with the anterior extension coursing from ventral to the eye to the snout region; two openings in nasal organ wide; the ventral surface of head and belly covered with spinules, extending just posterior to the lower jaw to slightly before anus; dorsal and anal fins slightly pointed; pectoral fin rounded; caudal fin double emarginated, the middle rays slightly produced posteriorly; the dorsal and ventral tips of the caudal fin produced posteriorly.

Color of the neotype in ethanol (Figs. 1, 2). The dorsal side of the body dark brown, a light brown band coursing longitudinally on the side ventral to the level of the eye from the snout to the caudal-fin base; the ventral side of the body white; the dorsal, pectoral and caudal fins dusky. The anal fins pale.

Color of fresh specimens (Fig. 3). The dorsal half of the body dark brown to brownish black; side of head silver with dark yellowish tinge; the lower side of the body between the gill opening and the caudal-fin base silver, edged dorsally with an obscure yellowish stripe; dorsal and pectoral fins dark; anal fin white; caudal fin dark brown to black with dorsal and ventral white tips.

Distribution. Japan, Korea, China, Philippines, Vietnam, Indonesia, Australia and New Zealand.

Neotype designation. Clarke (1897) described Tetrodon cheesemanii as a new species based on a single specimen (11.25 inches TL = 285 mm TL) collected from Moturoa, Taranaki, New Zealand. His description and illustrations of this species are adequate to classify T. cheesemanii to Lagocephalus by showing a longitudinal skin fold extending on the ventro-lateral corner of the body from the chin to the caudal peduncle, two lateral lines on the body, and a wide, silver-white band coursing longitudinally ventral to the eye from snout to the caudal-fin base. His description also distinguishes T. cheesemanii from the other species of Lagocephalus by the following characters: spinules on the back in a rhomboidal patch extending from the region between nasal organ to the region dorsal to the posterior part of pectoral fin, and the dark caudal fin with white margins on the dorsal and ventral lobes (Fig. 4). Upon my request Clive Roberts of the Museum of New Zealand Te Papa Tongarewa kindly searched for Clarke’s specimen, the holotype of T. cheesemanii, but it was not found in the museum. He suggested that the holotype is lost.

Many species of Lagocephalus are similar to one another and difficult to identify. This has led to taxonomic confusion in Lagocephalus (Matsuura 2010; Matsuura et al. 2011) and misidentifications of specimens in museum collections. To remedy the current situation, a neotype of L. cheesemanii is necessary to stabilize its taxonomic status. We hereby designate as neotype the specimen NMNZ P. 18876, which was collected near the type locality.

Remarks. Abe and Tabeta (1983) described Lagocephalus gloveri based on only three specimens collected from Suruga Bay, Japan. They mentioned differences among L. gloveri, Lagocephalus lunaris (Bloch and Schneider 1801) and Lagocephalus spadiceus (Richardson 1845). As they did not mention L. cheesemanii in their paper, it seems clear that they overlooked Clarke’s (1897) paper.

Morphological examination of 49 specimens including the holotype and the paratype of L. gloveri revealed no differences between the specimens from the Northern Hemisphere (previously identified as L. gloveri) and those from the Southern Hemisphere (Australia and New Zealand). We also conducted an examination of COI diversity to compare the genetic divergence of barcode sequences among 10 individuals from seven species of Lagocephalus. As a result, three individuals of L. cheesemanii from the Southern Hemisphere and two individuals from the Northern Hemisphere had identical sequences (636bp), and there was no genetic divergence among them. On the other hand, the K2P distances between other species ranged from 6.3 % (L. guentheri and L. spadiceus) to 18.7 % (L. inermis and L. spadiceus) (Table 2). These values are equivalent to the variation within genera (or within families) in other studies (Ward et al. 2005; Ward 2009; Zhang and Hanner 2012). Therefore, we conclude that L. cheesemanii is a senior synonym of L. gloveri.
Table 2

Interspecific K2P distances for the 636 bp of COI gene in Lagocephalus

 

1

2

3

4

5

6

7

1. L. cheesemanii (NH)

-

      

2. L. cheesemanii (SH)

0.00000

-

     

3. L. spadiceus

0.09527

0.09527

-

    

4. L. guentheri

0.10091

0.10091

0.06324

-

   

5. L. lagocephalus

0.07170

0.07170

0.09493

0.09122

-

  

6. L. inermis

0.17683

0.17683

0.18744

0.17921

0.16775

-

 

7. L. lunaris

0.17967

0.17967

0.16703

0.18160

0.17043

0.16052

-

NH Northern Hemisphere, SH Southern Hemisphere

Lagocephalus cheesemanii has been collected from depths of 0–200 m (this study; Yamada et al. 2007; Ikeda and Nakabo 2015; Stewart and Roberts 2015). In the Northern Hemisphere it is commonly found in many areas in Japan from southern Hokkaido to Kyushu (Matsuura 1997; Yamada 2002; Yamada et al. 2007; Ikeda and Nakabo 2015), Korea (Kim et al. 2005) and China (Su and Li 2002). The specimens examined in this study have revealed that L. cheesemanii is distributed in the Philippines, Vietnam and Indonesia including the equatorial region. In the Southern Hemisphere, it is known from eastern Australia and New Zealand (Stewart and Roberts 2015). Yamada et al. (2007) stated that many specimens of this species were captured by trawl at depths of 90–116 m in the East China Sea. They also reported that this species reached 40 cm in total length.

Notes

Acknowledgments

We are grateful to the following persons and institutions for specimen loan, gifts of tissue samples for DNA analysis, and facilities provided during visits of the first author: Mark McGrouther (AMS), James Maclaine (BMNH); Alastair Graham and John Pogonoski (CSIRO), Yoshiaki Kai and Fumihito Tashiro (FAKU); Daniel Golani (Hebrew University), Toshio Kawai, Hisashi Imamura, and Mamoru Yabe (HUMZ); Hiroyuki Motomura (KAUM); Hiroshi Senou (KPM); Clive Roberts and Carl Struthers (NMNZ); Jeff Johnson (QM); Kazuo Sakamoto (ZUMT). Kaoru Kuriiwa (NSMT) took the photographs of the neotype of L. cheesemanii and the holotype of L. gloveri. Edward O. Murdy provided comments on the manuscript. This study was partially supported by Grant-in-Aids for Scientific Researches (B) (JP24370041) from the Japan Society for the Promotion of Science; Health Labour Sciences Research Grant (FY2015–2017) of the Ministry of Health, Labour and Welfare, Japan; the “Biological Properties of Biodiversity Hotspots in Japan” Project of the National Museum of Nature and Science; and JSPS Asian Core Program “Establishment of Research and Education Network on Coastal Marine Science in Southeast Asia.”

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Copyright information

© The Ichthyological Society of Japan 2016

Authors and Affiliations

  1. 1.National Museum of Nature and ScienceTsukubaJapan
  2. 2.Seto Marine Biological Laboratory, Field Science Education and Research CenterKyoto UniversityNishimuroJapan

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