New Record of the Birdbeak Burrfish Cyclichthys orbicularis (Pisces: Diodontidae), in Korea

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  • ABSTRACT

    A total of six specimens (57.03-100.72 mm in standard length) belonging to the family Diodontidae were collected around Jeju Island, Korea between July and August 2013. On the Basis of morphological and molecular analyses, we identified the specimens as Cyclichthys orbicularis (Bloch, 1785), a new record to the Korean fish fauna. Morphologically, the species is characterized by nine caudal fin rays, immovable spines on the head and body except the caudal peduncle, and small black spots dorsally. Some morphometric characters changed disproportionately with growth, which was a new finding. Caudal peduncle length, body width and preanus length to standard length tend to grow at a rate different from that of overall growth. When the 601 base pairs of mitochondrial DNA cytochrome c oxidase subunit I sequences of our specimens were compared with those of other diodontid fishes, our specimens clustered tightly around C. orbicularis (d = 0.000-0.002) in an NJ tree, with a high bootstrap value (99%). We herein describe the morphological and molecular traits of the specimens, and propose a new Korean name, “gud-ga-si-bok-sok” for the genus Cyclichthys, and “dung-geun-gud-ga-si-bok” for C. orbicularis.


  • KEYWORD

    Cyclichthys orbicularis , Diodontidae , Jeju Island , Korean fish fauna , New record

  • Introduction

    The family Diodontidae of the order Tetraodontiformes comprises 19 species in 6 genera worldwide (Nelson, 2006), with 2 species in 2 genera in Korea (Kim et al., 2005) [Diodon holocanthus Linnaeus, 1958; Chilomnycterus affinis (Linnaeus, 1758)]. Diodontid fishes are commonly known as porcupinefishes, burrfishes, and spiny puffers (Gallo et al., 2009). They are able to inflate the body, an important defense mechanism for such slow moving species (Cavaleri, 2000; Leis, 2006; Gallo et al., 2009). The body is covered with well-developed sharp spines, and species are identified according to whether the spines are movable or immovable (Leis, 1986; Aizawa, 2002; Leis, 2006). Some diodontid fishes are poisonous, having tetradotoxin in their ovaries (females) and liver, and can also cause ciguatera (Allen and Erdmann, 2012; Bandyopadhyay, 2013). Most are generally scarce due to their solitary habits; they are found on soft bottoms, on rocky or coral reefs as well as coastal trawling grounds (Leis, 2001; Allen and Erdmann, 2012). Consequently, diodontid fishes have high bycatch rates by trawling and their recovery capacity is low (Stobutzki, 2001). Although Diodontidae fishes are not usually sold commercially for consumption, they are popular in the marine aquarium trade (Leis, 2001; Ellis, 2006). They are a conspicuous and readily captured species, and have been the focus of interest by naturalists for some time (Leis, 2006). However, in Korea, there have been few studies on diodontid fishes other than the brief description of the two species by Kim et al. (2005).

    During a survey of fish resources around Jeju Island, Korea, a total of six specimens (57.03-100.72 mm SL) were collected, that were identified as Cyclichthys orbicularis, a new record to the Korean fish fauna. We herein provide morphological and molecular traits of the species and suggest a new Korean name.

    Material and Methods

    total of six specimens were collected around Jeju island, Korea between July and August 2013 (Fig. 1). Counts and measurements methods followed Nakabo (2002) with a Vernier caliper to the nearest 0.1 mm. Those specimens are deposited in the ichthyology laboratory in Pukyong National University (PKU), Korea. Genomic DNA was extracted from muscle tissue using Chelex 100 resin (Bio-rad, USA), and then polymerase chain reaction (PCR) was performed using VF2 (5´-TCAACCAACCACAAAGACATTGGCAC-3´) and FishR1 (5´-TACAC TTCTGGGTGGCCAAAGAATCA-3´) primers that amplifies mtDNA COI (Ward et al., 2005; Ivanova et al., 2007). PCR was performed in a total volume of 30 μL which contained DNA template 1 μL, dNTP 2.4 μL, 10X buffer 3 μL, Taq polymerase 0.1 μL, reverse primer 1 μL, forward primer 1 μL, and distilled water, and conducted under the following conditions: initial denaturation was for 3 min at 94°C, followed by 35 cycles of 30 s at 94°C for denaturation, 30 s at 50°C for annealing, and 90 s at 72°C for extension, with a final extension at 72°C for 10 min. The PCR products were purified with DavinchTM PCR Purification Kit (Davinch-K, Seoul, Korea). The DNA was sequenced using an ABI 3730XL sequencer and an ABI PRISMR BigDyeTM Terminator v 3.0 Ready Reaction Cycle Sequencing Kit (Applied Biosystems, USA). The nucleotide sequence was deposited in the DDBJ/EMBL/GenBank databases (accession numbers: KJ626293‒KJ626296). The sequence was aligned with ClustalW (Thompson et al., 1994) in BioEdit version 7 (Hall, 1999). Sequences of four diodontid fishes (Cyclichthys orbicularis, C. spilostylus, Chilomycterus reticulatus, Diodon holocanthus), from the National Center for Biological Information database, were used for the comparison, and Takifugu niphobles was used as an outgroup. The genetic distances were calculated with the Kimura-2-parameter model (Kimura, 1980) in MEGA 5 (Tamura et al., 2011). An neighbor-joining(NJ) tree was constructed in MEGA 5 (Tamura et al., 2011) with 5,000 bootstrap replications.

    Results and Discussion

      >  Cyclichthys Kaup, 1855

    (New Korean genus name: Gud-ga-si-bok-sok)

    Cyclichthys Kaup, 1855: 231, Type by subsequent designation; Bleeker, 1865: 48, Type apparently designated first; Matsuura & Sakai, 1993: 372; Leis, 2001: 3959.

      >  Description

    Spines of body and head with 3 bases, except in C. spilostylus which has some spines on top of head with 4 bases; no spines on caudal peduncle; 9 caudal fin rays; no spots on fins. The most similar genus, Chilomycterus, is distinguishable from Cyclichthys in having a small spine on dorsal side of caudal peduncle, 10 caudal fin rays, and spots on fins (Leis, 1986).

    Cyclichthys orbicularis (Bloch, 1785) (Fig. 2)

    (New Korean species name: Dung-geun-gud-ga-si-bok)

    Diodon orbicularis Bloch 1785: 73 (Type locality: Jamaica); Allen & Swainston, 1988: 156, Australia; Matsuura & Sakai, 1993: 372, Japan; Mishra & Krishnam, 2003: 51, India.

    Chilomycterus parcomaculatus von Bonde, 1923: 38 (Type locality: Union of South Africa).

    Cyclichthys orbicularis: Leis, 1986: 904; Francis, 1993: 168; Matsuura et al., 1993: 372; Leis, 2001: 3962; Aizawa, 2002: 1434; Allen & Adrim, 2003: 65; Adrim et al., 2004: 127; Heemstra & Heemstra, 2004: 455; Allen et al., 2005: 420; Leis, 2006: 82; Allen and Erdmann, 2012: 1098.

      >  Description

    D. 11-12; P. 19-21; A. 10-11; C. 9. Meristic and morphometric characters are shown in Table 1. Body round in cross section and inflatable. Body covered with short spines; spines immovable, fixed by 3-rooted bases. Three spines dorsal to eye, 4 dorsally between pectoral fin bases, 8-9 anterior to dorsal fin base; caudal peduncle without spines. Mouth small, terminal. Posterior margin of lips not reaching to anterior margin of eye. Teeth fused to a strong and beak-like structure. Nostril a short tube with 2 openings. Gill opening a vertical slit immediately before pectoral fin bases. Pectoral fins broad and anterior to the middle of the body. Dorsal and anal fins located posteriorly on body. Pelvic fins absent; caudal fin slightly rounded. All fin rays branched.

    Color when fresh. the body greyish dorsally and white ventrally. Several clusters of black spots on dorsal and lateral sides of body, none ventrally. Black spots either absent from fins or present only faintly. Coloration similar in preservation.

      >  Distribution

    Found in the tropic waters of the Indo-West Pacific (Leis, 2001) and Southeast Atlantic (Leis,1986) Oceans, near reef areas, at depths of 9-170 m (Sommer et al., 1996).

      >  MtDNA COI sequences analysis

    Comparison of the 601 bp of mtDNA COI sequences of four specimens with those of other diodontid fishes revealed that the sequences of the specimens aligned best with that of C. orbicularis (d = 0.000-0.002), but clearly differed from those of C. spilostylus (d = 0.066-0.068), Chilomycterus reticulatus (d = 0.105-0.108), and Diodon holocanthus (d = 0.105-0.107). In an NJ tree, the specimens clustered with C. orbicularis (GU804950), with a high bootstrap value of 99% (Fig. 3).

      >  Remarks

    Our specimens collected around Jeju Island are placed in the genus Cyclichthys because they possess immovable spines with 3-rooted bases, 9 caudal fin rays, no spots on the fins, and no spines on the caudal peduncle (Leis, 1986, 2001). The specimens also matched the original description of C. orbicularis in most meristic counts, the presence of black spots in clusters dorsally and dorsolaterally, and three spines on top of eyes (Bloch, 1785; Leis, 2006; Allen and Erdmann, 2012). Molecular analysis supported the identification as C. orbicularis (d = 0.000-0.002). Cyclichthys orbicularis differs from Chilomycterus reticulatus in the number of caudal fin rays (9 in Cyclichthys orbicularis vs. 10 in Chilomycterus reticulatus), the spine on dorsal surface of caudal peduncle (absent vs. present), and black spots on all fins (absent vs. present) (Leis, 1986; Aizawa, 2002; Kim et al., 2005). Although, according to Matsuura et al. (1993), several measurements of Cyclichthys orbicularis overlap with those of the morphologically similar C. spilostylus, the former is well distinguished from the latter by the number of subdermal roots (all spines with 3 roots in C. orbicularis vs. some spines with 4 roots in C. spilostylus), and clusters of dark spots on ventral side of body (absent vs. present) (Leis, 2001; Aizawa, 2002). Most measurements of the specimens in this study overlapped those of C. orbicularis in Japan, but the specimens showed significant differences in body width, caudal peduncle length, and preanus length (Table 1). Generally, body shape in fishes is associated with a variety of environmental factors, type of food or feeding mode, and sexual differences as well as growth period (Marcil et al., 2006; Frederich et al., 2008; Fruciano et al., 2011; Song et al., 2013). But, when standard length was regressed against the various measurements, caudal peduncle length showed positive correlation (Fig. 4a), whereas body width and preanus length were negatively correlated with standard length (Fig. 4b, 4c). Therefore, our results suggested that body shape changes with growth, not due to regional variation. We propose the new Korean name “gud-ga-si-bok-sok” for the genus Cyclichthys, and “dung-geun-gud-ga-si-bok” for C. orbicularis based on the species’ rounded shape.

  • 1. Adrim M, Chen IS, Chen ZP, Lim KK, Tan HH, Yusof Y, Jaafar Z 2004 Marine fishes recorded from the Anambas and Natuna islands, South China Sea [Ruffles Bull Zool Suppl] Vol.11 P.117-130 google
  • 2. Aizawa M, Nakabo T 2002 Diodontidae P.1632 google
  • 3. Allen GR, Adrim M 2003 Coral reef fishes of Indonesia [Zoological Studies] Vol.42 P.1-72 google
  • 4. Allen GR, Erdmann MV 2012 Diodontidae P.1097-1099 google
  • 5. Allen GR, Steene R, Humann P, DeLoach N 2003 Reef Fish Identification: Tropical Pacific P.457 google
  • 6. Allen GR, Swainston R 1988 The marine fishes of north-western Australia, A field guide for anglers and divers, i?vi + 1?201 google
  • 7. Bleeker P 1869 Atlas ichthyologique des Indes Orientales Neerlandaises, publie sous les auspices du Gouvernement colonial neerlandais P.1-152 google
  • 8. Bloch ME 1785 Naturgeschichte der auslandischen Fische, v. 1: i?viii + 1?136 google
  • 9. Cavalieri K 2000 Diodontidae holocanthus [Topical Biol] Vol.5 P.18-21 google
  • 10. Ellis JR 2006 Occurrence of exotic fishes in east anglian waters: porcupinefish Diodon hystrix and piranha Pygocentrus sp [Suff Nat His] Vol.42 P.39-42 google
  • 11. Follesa MC, Mulas A, Porcu C, Cau A 2009 First record of Chilomycterus reticulatus (Osteichthyes: Diodontidae) in the Mediterranean Sea [J Fish Biol] Vol.74 P.1677-1681 google doi
  • 12. Francis MP 1993 Checklist of the coastal fishes of Lord Howe, Norfolk, and Kermadec Island, southwest Pacific Ocean [Pac Sci] Vol.47 P.136-170 google
  • 13. Frederich B, Pilet A, Parmentier E, Vandewalle P 2008 Comparative trophic morphology in eight species of damselfishes (Pomacentridae) [J Morphol] Vol.269 P.175-188 google doi
  • 14. Fruciano C, Tigano C, Ferrito V 2012 Body shape variation and colour change during growth in a protogynous fish [Environ Biol Fish] Vol.94 P.615-622 google doi
  • 15. Gallo V, Carvalho MSSD, Souto AA 2009 A possible occurrence of Diodontidae (Teleostei, Tetraodontiformes) in the Upper Cretaceous of the Paraiba Basin, northeastern Brazil [Cretaceous Res] Vol.30 P.599-604 google doi
  • 16. Hall TA 1999 BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT [Nucl Acids Symp Ser] Vol.41 P.95-98 google
  • 17. Heemstra PC, Heemstra E 2004 Coastal fishes of southern Africa, i?xxiv + 1?488 google
  • 18. Hubbs CL, Lagler KF 2004 Fishes of the Great Lakes region google
  • 19. Kaup JJ 1855 Uebersicht uber die Species einiger Familien der Sclerodermen [Archiv fur Naturgeschichte] Vol.21 P.215-233 google
  • 20. Kim IS, Choi Y, Lee CL, Lee YJ, Kim BJ, Kim JH 2005 Illustrated Book of Korean fishes google
  • 21. Kimura M 1980 A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences [J Mol Evol] Vol.16 P.111-120 google doi
  • 22. Kuiter RH, Tonozuka T 2001 Pictorial Guide to Indonesian Reef Fishes;Jawfishes - Sunfishes, Opistognathidae - Molidae P.623-893 google
  • 23. Leis JM, Smith MM, Heemstra PC 1986 Family No. 269: Diodontidae P.903-907 google
  • 24. Leis JM 2001 Diodontidae P.3958-3965 google
  • 25. Leis JM 2006 Nomenclature and distribution of the species of the porcupinefish family Diodontidae (Pisces, Teleostei) [Mem MusVictoria] Vol.63 P.77-90 google
  • 26. Lieske E, Myers R 1994 Collins Pocket Guide, Coral reef fishes. Indo-Pacific & Caribbean including the Red Sea P.400 google
  • 27. Linnaeus C 1758 Systema Naturae per Regna Tria Naturae, Secundun Classes, Ordines, Genera, Species, cum Characteribus, Differentiis, Synonymis, Locis google
  • 28. Marcil J, Swain DP, Hutchings JA 2006 Countergradient variation in body shape between two populations of Atlantic cod (Gadus morhua) [Proc Roy Soc B: Biol Sci] Vol.273 P.217-223 google doi
  • 29. Matsuura K, Sakai K, Yoshino T 1993 Records of two diodontid fishes, Cyclichthys orbicularis and C. spilostylus, from Japan [Japan J Ichthyol] Vol.40 P.372-376 google
  • 30. Mishra SS, Krishnan S 2003 Marine fishes of Pondichery and Karaikal Rec Zool Surv India [Miscell Pub, Occa Paper] Vol.216 P.1-53 google
  • 31. Nakabo T 2002 Fishes of Japan with Pictorial Keys to the Species P.1748 google
  • 32. Nelson JS 2006 Fishes of the World P.1-601 google
  • 33. Sommer C, Schneider W, Poutiers JM 1996 FAO Species Identification Field Guide for Fishery Purposes;The living marine resources of Somalia P.376 google
  • 34. Song YS, Kim JK 2013 Ontogenetic color variation of Abudefduf notatus (Pomacentridae: Perciformes) revealed by 16s rRNA Sequences Analysis [Korea J Ichthyol] Vol.25 P.53-58 google
  • 35. Stobutzki I, Miller M, Brewer D 2001 Sustainability of fishery bycatch: a process for assessing highly diverse and numerous bycatch [Environ Conserv] Vol.28 P.167-181 google
  • 36. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S 2011 MEGA5: molecular evolutionary genetics analysis using maximum likelihood evolutionary distance and maximum parsimony methods [Mol Biol Evol] Vol.28 P.2731-2739 google doi
  • 37. von Bonde C 1923 Shallow-water fishes procured by the S. S. “Pickle” [Rep Fish Mar Biol Surv, Union of South Africa Rep] Vol.3 P.1-40 google
  • [Fig. 1.] Sampling area of Cyclichthys orbicularis in the present study.
    Sampling area of Cyclichthys orbicularis in the present study.
  • [Fig. 2.] Cyclichthys orbicularis, PKU 9454, 80.69 mm SL, Jeju Island, Korea. (A) Lateral view, (B) Frontal view.
    Cyclichthys orbicularis, PKU 9454, 80.69 mm SL, Jeju Island, Korea. (A) Lateral view, (B) Frontal view.
  • [Table 1.] Comparison of counts and measurements for Cyclichthys orbicularis and C. spilostylus
    Comparison of counts and measurements for Cyclichthys orbicularis and C. spilostylus
  • [Fig. 3.] Neighbor-joining (NJ) tree for cytochrome oxidase subunit I (COI) gene sequences of 4 diodontid fishes. The NJ tree was constructed under the K2P model using Takifugu niphobles as the outgroup. Superscripts indicate the registration number of voucher specimens.
    Neighbor-joining (NJ) tree for cytochrome oxidase subunit I (COI) gene sequences of 4 diodontid fishes. The NJ tree was constructed under the K2P model using Takifugu niphobles as the outgroup. Superscripts indicate the registration number of voucher specimens.
  • [Fig. 4.] Comparison of relationships between standard length (SL) and proportional measurements of caudal peduncle length (A), body width (B), and preanus length (C) for Cyclichthys orbicularis from Korea (rectangle) and from Japan (diamond).
    Comparison of relationships between standard length (SL) and proportional measurements of caudal peduncle length (A), body width (B), and preanus length (C) for Cyclichthys orbicularis from Korea (rectangle) and from Japan (diamond).