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All issues Volume 31 (2018) Aquat. Living Resour., 31 (2018) 32 Full HTML
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Aquat. Living Resour.
Volume 31, 2018
Article Number 32
Number of page(s) 10
DOI https://doi.org/10.1051/alr/2018015
Published online 29 October 2018

© EDP Sciences 2018

1 Introduction

Flathead fishes of the genus Platycephalus, family Platycephalidae, were widely distributed in the tropical and temperate areas of the Indo-West Pacific and eastern Mediterranean (Hureau, 1986; Shao and Chen, 1987; Imamura, 1996; Knapp, 1999; Qin et al., 2013). These species have a high commercial value in some parts of the Indo-Pacific region. They were among the first fishes to be commercially targeted by the trawling industry, and are prized for their high-quality flesh (Qin et al., 2013). At present, a total of four species have been recorded in northwest Pacific Ocean. These four species were Platycephalus indicus, Platycephalus cultellatus and two valid but undescribed species, Platycephalus sp. 1 and Platycephalus sp. 2, respectively (Kamei and Ishiyama, 1968; Masuda et al., 1991, 1997; Osatomi et al., 2001; Yamada et al., 2007; Nakabo, 2013; Qin et al., 2013). Of them, although P. cultellatus was originally found and named in its type locality, Canton, Guangdong Province, China, after its original discovery, except that Qin et al. in 2013 simply mentioned the literature records of this species, no Chinese taxonomy books or publications have ever recorded or described local P. cultellatus (Zhu et al., 1963; Whitehead, 1970; Chen, 1982; Chen and Zhao, 1986; Kong et al., 1994; Zhang et al., 1994; Jin, 2006; Tang, 2006; Qin et al., 2013; Imamura, 2015a, 2015b). All species introduction of native Platycephalus made by local ichthyologists was confined to P. indicus and Platycephalus sp. 1.  For better Chinese Platycephalus scientific studies and fisheries management, it was necessary to fill the P. cultellatus description gap and give enough additions to this species’ morphological characters.

Our purpose here was first confirming the existence of true P. cultellatus and then providing plentifully morphological characters of this species. Due to the complexities of morphological characters used in traditional taxonomy and taxonomic confusion as well as cryptic species has arisen in Platycephalus concerning the nomenclature (Imamura et al., 2006; Imamura, 2008, 2013a, 2013b, 2013c, 2015a, 2015b by, employing solely morphological means to solve chaotically taxonomic identification was improper sometimes in traditional taxonomy. The mitochondrial cytochrome oxidase I gene (COI) varies noticeably between species and very little between the individuals of a given species (Gross, 2012). Therefore, a fragment of COI gene, as DNA barcoding (Hebert et al., 2003), has proven to be extremely effective at discriminating species (Domingues et al., 2013; Puckridge et al., 2013; Ming et al., 2015), discovering new-recorded and new species (Gao et al., 2011; Qin et al., 2013), uncovering cryptic species (Hajibabaei et al., 2007; Zemlak et al., 2009), identification of ichthyoplankton (Bian et al., 2008; He et al., 2011). In the present study, a mitochondrial DNA barcoding approach was also employed in order to better solve the identification problems of P. cultellatus at genetic level. These results will contribute to Chinese Platycephalus species identification and be helpful to native fishery management, biodiversity conservation, and sustainable exploitation of this species.

2 Materials and methods

2.1 Sampling

A total of 48 individuals were collected from the coastal waters of Zhuhai, Yangjiang, Zhanjiang and Beihai from November 2012 to January 2016. All specimens were identified based on morphological characteristics commonly-used by Imamura (2013c, 2015b). The body color and pigmentation were pictured in fresh fish and all measurements were made on preserved specimens. For genetic study, a piece of muscle tissue was obtained from each individual and preserved in 95% ethanol or directly extracted from frozen samples. All specimens examined were frozen and preserved at the Fishery Ecology Laboratory, Fisheries College, Ocean University of China in Qingdao (Fig. 1).

thumbnail Fig. 1

Sampling location, date, and number of Platycephalus cultellatus individuals in this study. To better show the sample distribution, a smaller scale map was used in the left and its partial enlarged drawing in the right.

2.2 Morphological study

Counts and measurements followed the standard methods given by Imamura (2013c, 2015b). The detailed guidance was listed as follows: gill rakers (GR), defined as depressible bony elements and not including tooth plates, were counted on the right side. Other counts were routinely taken from the left side. Measurements of body lengths were done on a measuring board graduated in 1.0 mm intervals. All other measurements were taken using dial calipers and recorded to the nearest 0.1 mm. Fin rays were counted using a magnifier when specimens were too small. Small isolated anterior and posterior first dorsal-fin spines are given before and after the first dorsal-fin ray count (in Roman numerals), respectively. Orbital diameter (OD) was measured from the anteroventral to posteromedial portions, which was the greatest distance in many species of Platycephalus. Interorbital width (IW) was measured level with the eye center. When two small isolated anterior dorsal-fin spines were present, predorsal length (PDL) was measured from the tip of the snout to the base of the second spine, since the latter was homologous with the single small isolated anterior spine present in many species of Platycephalus (see Imamura, 1996 for homology of such spines). Terminology of head spines follows  and Imamura (2015b). The following abbreviations for counts and measurements were used: first dorsal-fin rays (D1); second dorsal-fin rays (D2); anal-fin rays (A); pectoral-fin rays (P1); branched caudal-fin rays (C); pored lateral line scales (LLS); oblique body scale rows slanting downward and backward above lateral line (OBS); GR; total length (TL); standard length (SL); head length (HL); PDL; length of first dorsal-fin base (LD1B); length of second dorsal-fin base (LD2B); length of anal-fin base (LAB); snout length (SNL); OD; upper-jaw length (UJL); lower-jaw length (LJL); IW; postorbital length (POL); suborbital width (SW); pectoral-fin length (P1L); pelvic-fin length (P2L); and caudal-fin length (CL) (all words above in this paragraph were from Imamura, 2013c, 2015b). Some counts could not be determined because of the poor condition of these samples. In such instances the reported values were taken from the original description or the specimens were discarded from analysis.

2.3 DNA extraction and sequencing

After morphometric measurements, all specimens from Zhuhai and Zhanjiang, four individuals from Beihai and six from Yangjiang were randomly selected for genetic studies. The classical phenol-chloroform technique was used for DNA extraction. Polymerase chain reaction (PCR) was subsequently conducted. primer sequences used for COI amplification were 5′-TCGACTAATCATAAAGATATCGGCAC-3′ and 5′-ACTTCAGGGTGACCGAAGAATCAGAA-3′ (Ivanova et al., 2007), respectively. PCR was carried out in a 25 µL reaction mix containing DNA template (1 µL, 50 ng/uL), forward primer (F, 1 µL, 10 uM/L), reverse primer (R, 1 µL, 10 uM/L), dNTPs (2 µL, 2.5 mM/L each), EasyTaq DNA Polymerase (0.15 µL, 5 U/µl) and 10 × PCR buffer (2.5 µL, 25 uM/L). A Biometra thermal cycler (Göttingen, Germany) with the following given procedure: one initial denaturation (95 °C, 5 min), thirty-five cycles consisting of denaturation (94 °C, 35 s), annealing (54 °C, 35 s) and extension (72 °C, 35 s), and one final extension (72 °C, 10 min), was employed to put PCR amplification into effect. PCR products were sent to Shanghai Majorbio Bio-Pharm Technology Co., Ltd to get original COI sequences.

2.4 COI analysis

All 12 individuals’ original sequences were successfully obtained and revised by DNASTAR software (DNASTAR Inc., Madison, WI, USA). One COI sequence of Cociella crocodila and 23 sequences of Platycephalus were also downloaded from NCBI for phylogenetic study (Tab. 1). These 36 COI sequences were then aligned using the above DNASTAR software. MEGA 5.0 (Tamura et al., 2011) was used to construct neighbor-joining (NJ) tree under the Kimura 2-parameter (K2P) model.

Table 1

GenBank accession numbers of related COI sequences downloaded from NCBI for phylogenetic tree study. No COI sequences of Platycephalus cultellatus were found in NCBI.

3 Results

3.1 Morphological characters

The generally morphological features were shown in Figure 2. Body was elongate and head strongly depressed. Rear edge of maxilla reached to about below middle of eye. Preopercular spines were 2, and the lower was longer than the upper. A trace of an accessory spine usually present on base of upper spine. Supraorbital ridge was pretty smooth. Spines and ridges on top and side of head weakly developed. Preorbital spine was lacking and a single preocular spine obscure in large adults. Suborbital ridge was smooth in adults, bearing a spine below rear of eye in juveniles. Teeth on vomer were in a single transverse band. Upper iris lappet was a simple elongated lobe. Interopercular flap presented, finger-like in shape. Total GR on first gill arch ranged from 7–10 (usually 9 or 10). In addition to 13 (usually) second dorsal-fin rays and 13 anal-fin rays, first dorsal-fin spines and pectoral-fin rays were I-II + VII+0-I (usually II + VII+I) and 17–19, respectively. Oblique body scale rows slanting downward and backward above lateral line ranged from 86 to 120. LLS were usually 65–76. Anterior-most scale usually had a one or two spine or ridge. Scale pores of lateral line had a single opening to the outside.

Besides above description, these specimens were also a species of Platycephalus with the following combination of characters: upper jaw without large caniniform teeth. Teeth absent on dorsal surface of anterolateral edge of upper jaw. Lip margins without papillae. First and second dorsal fin narrowly separated. Head and body covered with small brown flecks, whitish below, several indistinct dark bands crossing back in some; upper surface of eye without papillae; scales covering snout, a small area anteroventral to eye, interorbit, occipital region, nape, postorbital and opercular regions; suborbital region naked; first dorsal fin usually with two single small isolated spine anteriorly; body with two dark brown bands below second dorsal fin; pectoral fins without small dark spots along; caudal fin with 3–6 horizontal dark bars, no prominent yellow blotch near middle of fin when fresh; HL 29.39–32.45% in SL; pectoral fin length 12.4–16.84% SL. Pelvic fin length 16.67–21.35% SL. Caudal fin usually slightly rounded or mostly straight posteriorly, length 13.23–16.38% SL. POL 59.3–66.21% HL; SNL 21.65–25.25% HL; interorbit narrower than OD in smaller specimens, becoming equal to or wider than OD with the development of specimens, width 15.07–18.5% HL; OD 11.56–15.58% HL.

thumbnail Fig. 2

Lateral (upper) and dorsal (lower) views of Platycephalus cultellatus, 347.3 mm SL.

3.2 Sequence analysis of the COI gene

Thirteen sequences (654 bp) of COI gene fragments were obtained. After combined the downloaded COI sequences of Platycephalus, a total of 36 sequences were used for analysis. Table 2 reported the genetic distances between all species. The mean distance among all species was 19.61%. Genetic distance between our 12 specimens was only 0.25%. Net genetic distances between P. cultellatus and other 14 species of the genus Platycephalus ranged from 11.59 to 25.48%, which vastly exceeded the threshold of species delimitation. A NJ phylogenetic tree was constructed using MEGA 5.0 (Fig. 3). C. crocodila was chosen as the out-group to root the tree. All COI sequences of specimens in present study clustered in the same group, and 5 haplotypes were defined. All haplotype sequences were submitted to GenBank with the following accession numbers: KY611406- KY611410. The haplotype 2 (Hap-2) was shared by one specimen from Yangjiang and all individuals form Beihai and Zhanjiang. Similarly, haplotype 5 (Hap-5) were shared by 3 Yangjiang individuals. Remaining haplotypes were unique and each of them was shared by the rest specimens form Yangjiang and Zhuhai. At the same time, a large genetic distance (12.77% and 19.68% respectively) between specimens and Platycephalus sp.1 and P. indicus indicated that these specimens couldn't be the latter two species existed in the coastal waters of China.

Table 2

Net genetic distances (K2P) within (on the diagonal, bold font) and between (below the diagonal, normal font) species.

thumbnail Fig. 3

Phylogenetic tree based on neighbor-joining analysis of COI sequence. Cociella crocodila (JQ349911) was chosen as the out-group to root the tree. Numbers above branches indicate neighbor-joining bootstrap percentages. Only Bootstrap values of >50% are shown in the NJ tree.

4 Discussion

The morphological characters of specimens used in this study were photographed, counted and compared with previously representative records in Table 3. These individuals were characterized by: first dorsal fin usually with two small isolated spine anteriorly; second dorsal-fin and anal-fin usually with 13 soft rays; pectoral fin usually with 17–19 soft rays and without very small dark spots; caudal fin with 3–6 horizontal blackish bands, but without yellow marking on the middle when fresh; GR 7–10 and pored LLS 65–76. These phenotypic traits were consistent with the authoritative descriptions of typical P. cultellatus described by Richardson and Imamura (Richardson, 1846; Imamura et al., 2006; Imamura, 2013c, 2015a, 2015b; Eschmeyer et al., 2018). As for the total four species distributed in northwest Pacific Ocean, all of them were characterized by usually 13 dorsal- and anal-fin rays, caudal fin with several horizontal blackish bands, interorbit and occipital region scaled, large caniniform teeth absent on the upper jaw, a finger-like interopercular flap and so on (Zhu et al., 1963; Chang, 1980; Chen, 1982; Chen and Zhao, 1986; Kong et al., 1994; Zhang et al., 1994; Jin, 2006; Tang, 2006; Imamura, 2013, 2015a, 2015b; Nakabo, 2013; Qin et al., 2013). Besides, by reviewing all known references including our present results, it could be obviously found that P. cultellatus were very similar with other three species in meristic values. Almost all morphological characteristics were overlapped. Such overlaps appeared to be very common among Platycephalus that were either closely related or lived in similar habitats (Imamura, 2015b). The very rare appearance and similar meristic values might be the reason why P. cultellatus distributed in the coastal waters of China did not catch people’s attention permanently and routinely overlapped by native ichthyologists.

Although P. cultellatus was similar with Platycephalus sp. 1, Platycephalus sp. 2 and P. indicus and long-termly lacked rediscovery and correct descriptions, there was still some obvious difference that could separate P. cultellatus from other three Platycephalus species. Among above four species, pectoral fins of both Platycephalus sp. 1 and Platycephalus sp. 2 had very small black spots whereas P. cultellatus didnot have (Fig. 4, the left part of the picture) (Nakabo, 2013). Besides, the light brown spots dorsally and the more GR (11–17, usually 14, see Tab. 3) of Platycephalus sp. 1 could also contribute to the identification of P. cultellatus (body without light brown spots, Figure 4, the middle part of the picture; GR 7–10, usually 9 or 10, Tab. 3). Large scale sampling and literature records revolved that Platycephalus sp. 2 dominatingly existed in the coastal waters of Japan but not in China, which meant that the distribution of Chinese P. cultellatus was not overlapped with Platycephalus sp. 2 and hardly misidentified as it. The blackish body color of Platycephalus sp. 2 could also distinguish P. cultellatus from it (Fig. 4, the middle part of the picture). Besides, P. indicus was the only one species that had the first dorsal fin with a single small isolated spine anteriorly (Tab. 3) and the caudal fin with a yellow marking on the middle when fresh (Fig. 4, the right part of the picture) (Whitehead, 1970; Imamura, 2015a, 2015b). The other three species including P. cultellatus uniformly usually had a caudal fin without yellow color and usually two small isolated spines in front of first dorsal fin (Whitehead, 1970; Imamura, 2013; 2015a, 2015b). Morphological characters of our specimens were clearly consistent with that of P. cultellatus but different from the descriptions of other Platycephalus species including Platycephalus sp. 1, Platycephalus sp. 2 and P. indicus.

COI sequence was recognized as an effective and reliable method for species identification (Masuda and Ozawa, 2000; Hebert et al., 2003; Domingues et al., 2013; Qin et al., 2013). The validity of P. cultellatus has also been demonstrated from genetically reconstructed phylogenetic relationships of Platycephalus, showing that specimens from the coastal waters of South China Sea were included in a same monophyletic clades. As an indicator of speciation, Hebert et al. (2004) proposed the “10 × rule”, whereby barcoded individuals are flagged as possible another species if they diverge by 10 times or more the average intraspecific variability of the group. A different approach was taken by Ward et al. (2009), who analyzed barcode data from about 1000 fish species and showed that at a level of 2% distance or greater, individuals were much more likely to be congeneric than conspecific. We identified that P. cultellatus and other Platycephalus species were distinguished by distance from 11.59 to 25.48%. The mean evolutionary distance within the species P. cultellatus was 0.25%, use of either the 10× or 2% rule suggests that the genetic distance between groups was significantly higher than the average genetic distance within the group, which indicated that the COI gene used as a barcode of P. cultellatus was effective at identifying Platycephalus species. Thus, these reality provided our studies a strongly morphological and genetic level support that the species P. cultellatus collected from Zhuhai, Yangjiang, Zhanjiang and Beihai was correctly identified and described.

It was also reported that Platycephalus were widely distributed in the coastal waters of China (Zhu et al., 1963; Chang, 1980; Chen, 1982; Chen and Zhao, 1986; Kong et al., 1994; Zhang et al., 1994; Jin, 2006; Tang, 2006). But fishermen and researchers could hardly see the occurrence of P. cultellatus apart from the coastal waters of South China Sea. All P. cultellatus collected in the past years came from this small area. The inundant distribution of Platycephalus sp. 1 and infrequent presence of P. cultellatus made a sharp contrast. The distribution of P. indicus suggested this species might prefer warm water and live in lower latitude areas. Further domestic and overseas specimen collection is also indispensable in order to define its geographic limits.

Accurate identification of fish is essential and would assist in fisheries managements for long-term sustainability, and improve ecosystem research and conservation. Complex species identification usually requires careful morphological analysis from expert taxonomists (Ward et al., 2005; Xiao et al., 2016). Mitochondrial sequence divergences are strongly linked to the process of speciation, DNA barcoding and morphological analysis should go hand-in-hand. The data presented here would aid more taxonomy information and correct numerous misidentification and records within genus Platycephalus. We hope this study will not only promote the sustainable exploitation, biodiversity conservation and fisheries management of Platycephalus distributed in China but also contribute to species identification within this genus in the future.

Table 3

Comparative counts of Platycephalus cultellatus, Platycephalus indicus, Platycephalus sp. 1 and Platycephalus sp. 2 from different records.

thumbnail Fig. 4

Distinguishing characteristic among four species distributed in northwest Pacific Ocean.

5 Conclusion

Individuals of P. cultellatus from the coastal waters of South China Sea were identified and described in detail. Conclusive characters of these specimens were consistent with typical P. cultellatus individuals and could thoroughly separate them from other Platycephalus species. The phylogenetic analysis of COI gene similarly supported the validity of P. cultellatus existed in the coastal waters of South China Sea. This study will contribute to species identification within this genus distributed in Chinese seas.

Acknowledgements

This work was supported by the National Natural Science Foundation of China (41776171). There are no conflicts of interest and authors are solely responsible for the contents and writing of the paper.

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Cite this article as: Chen Z, Song N, Zou J, Gao T. 2018. Rediscovery and elaborate description of Platycephalus cultellatus Richardson, 1846 collected from the coastal waters of South China Sea. Aquat. Living Resour. 31: 32

All Tables

Table 1

GenBank accession numbers of related COI sequences downloaded from NCBI for phylogenetic tree study. No COI sequences of Platycephalus cultellatus were found in NCBI.

In the text
Table 2

Net genetic distances (K2P) within (on the diagonal, bold font) and between (below the diagonal, normal font) species.

In the text
Table 3

Comparative counts of Platycephalus cultellatus, Platycephalus indicus, Platycephalus sp. 1 and Platycephalus sp. 2 from different records.

In the text

All Figures

thumbnail Fig. 1

Sampling location, date, and number of Platycephalus cultellatus individuals in this study. To better show the sample distribution, a smaller scale map was used in the left and its partial enlarged drawing in the right.
In the text
thumbnail Fig. 2

Lateral (upper) and dorsal (lower) views of Platycephalus cultellatus, 347.3 mm SL.
In the text
thumbnail Fig. 3

Phylogenetic tree based on neighbor-joining analysis of COI sequence. Cociella crocodila (JQ349911) was chosen as the out-group to root the tree. Numbers above branches indicate neighbor-joining bootstrap percentages. Only Bootstrap values of >50% are shown in the NJ tree.
In the text
thumbnail Fig. 4

Distinguishing characteristic among four species distributed in northwest Pacific Ocean.
In the text

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