Free Access
Issue
Aquat. Living Resour.
Volume 33, 2020
Article Number 5
Number of page(s) 6
DOI https://doi.org/10.1051/alr/2020006
Published online 12 June 2020

© EDP Sciences 2020

1 Introduction

The genus Pampus (Perciformes: Stromateidae) includes important commercial fishes, including six valid species in China (Li et al., 2019b): Pampus minor Liu and Li, 1998, Pampus argenteus (Euphrasen, 1788), Pampus chinensis (Euphrasen, 1788), Pampus cinereus (Bloch, 1795), Pampus punctatissimus (Temminck et Schlegel, 1845) and Pampus echinogaster (Basilewsky, 1855). According to previous reports (Cheng,1962; Nakabo, 2002; Liu and Li, 2002; Yang et al., 2006; Dolganov et al., 2007; Yamada et al., 2009), P. echinogaster, P. punctatissimus and P. chinensis are common species in the coastal waters of Wenzhou. In recent years, a variety of molecular markers have been successfully applied to study the taxonomy and genetic structure of the genus Pampus. In a taxonomic study of Pampus fishes, Divya et al. (2017) utilized the CO1 gene to establish the molecular identity of P. argenteus in Indian waters. Li et al. (2017) used the CO1 gene to correct the morphological redescription and DNA barcoding of P. echinogaster. In the most recent study, Li et al. (2019b) combined the CO1 gene with morphological characteristics to reidentify Pampus species, and preliminarily confirmed the existence of seven valid species. In a study on the genetic structure of Pampus species based on the mitochondrial DNA control region (CR) and microsatellite markers, Li et al. (2018) found that the complex migratory behavior and high dispersal ability of ichthyoplankton may have played important roles in shaping the current genetic structure of P. echinogaster. Meanwhile, in research on P. chinensis, based on the same methods, (Li et al., 2019a)pointed out that the P. chinensis populations in different geographical regions constituted a single panmictic stock with high gene flow.

P. minor was initially reported to be widely distributed in the southern part of the Taiwan Strait and to probably occur in Southeast Asian seas (Liu and Li, 1998). P. minor was once considered the juvenile of P. argenteus and P. cinereus (Liu and Li, 1998). Guo et al. (2010) used DNA barcoding to confirm the differences between P. minor and other species, reducing confusion over its identification. However, in our recent fishery resource survey in Zhejiang Province (Wentai fishing ground) conducted in March 2019, a total of 65 fish species, including 110437 individuals, were caught by bottom trawling, all of which belonged to class Actinopterygii, none of Chondrichthyes fishes, and 26 species of which were in the order Perciformes. In this survey, we collected five samples of P. minor. Although this species is rarely observed, for further studies, it is important to determine whether the species does indeed occur in these offshore waters. To this end, our purpose here was to use traditional taxonomy to accurately identify P. minor and then use DNA barcoding to confirm its occurrence.

DNA barcoding is a taxonomic approach that uses a short genetic marker in an organism's DNA to identify that organism as belonging to a certain species (Hebert et al., 2003a; Hua et al., 2004). This method differs from molecular phylogenetics in that the main goal is not to determine relationships but to identify an unknown sample according to a preexisting classification system (Ali et al., 2014). In this study, to ensure the accuracy of species identification, the distribution range of P. minor was supplemented by combining morphological identification with DNA barcoding.

2 Materials and methods

2.1 Sample collection

In March 2019, five samples of P. minor were collected by bottom trawling in the coastal waters of Wenzhou (121°05.494′E, 27°01.648′N) (Fig. 1). Other P. minor individuals were collected from different geographical locations (Tab. 1), bought at the dock or obtained through fishery resource surveys. In addition, P. argenteus, P. cinereus, and P. echinogaster were collected to construct a phylogenetic tree (Tab. 1). All individuals were identified based on morphological characteristics (Li et al., 2019b), and a piece of muscle tissue was obtained from each individual and preserved in 95% ethanol. All examined specimens were preserved at −20 °C and stored in the Laboratory of Marine Biology and Ecology, Third Institute of Oceanography, Ministry of Natural Resources.

thumbnail Fig. 1

P. minor collected from the coastal waters of Wenzhou, China (standard length: 101 mm).

Table 1

Information on the Pampus samples and sequences in this study.

2.2 Morphological analysis

We measured the morphological characteristics of five individuals of P. minor. Counting and measurement were performed as described by Elliott et al. (1995) and Li et al. (2017). The countable traits included the following: dorsal fin rays, pectoral fin rays, anal fin rays, caudal fin rays, gill rakers on the first gill arch, and vertebrae. The measurable traits included the following: total weight, fork length, standard length, head length, eye diameter, postorbital length, body width, caudle peduncle length, caudal peduncle width, dorsal fin length, anal fin length, pectoral fin length, and tail length. All measurements were performed using calipers to the nearest 0.1 mm. All remaining measurements were obtained using preserved specimens.

2.3 Molecular analyses

Molecular methods were implemented as described by Li et al. (2017). Genomic DNA was isolated from muscle tissue with an Easy Pure® Marine Animal Genomic DNA Kit (Beijing TransGen Biotech). A fragment of CO1 mitochondrial DNA was amplified using the primers F1: 5′-TCAACCAACCACAAAGACATTGGCAC-3′ and R1: 5′-TAGACTTCTGGGTGGCCAAAGAATCA-3′ (Ward et al., 2005). Each polymerase chain reaction (PCR) was performed in a 25 µL reaction mixture containing 17.5 µL of ultrapure water, 2.5 µL of 10× PCR buffer, 2 µL of dNTPs, 1 µL of each primer (5 µmol/L), 0.15 µL of Taq polymerase, and 1 µL of DNA template. PCR amplification was performed in a Biometra thermal cycler under the following conditions: 5 min of initial denaturation at 94 °C; 32 cycles of 30 s at 94 °C for denaturation, 30 s at 52 °C for annealing, and 40 s at 72 °C for extension; and a final extension at 72 °C for 10 min. The PCR products were preserved at 4 °C. After agarose gel electrophoresis, the PCR products were sequenced by Personal Biotechnology Co., Ltd.

To determine the correct DNA barcoding for P. minor, all original sequences were revised by DNASTAR software (DNASTAR, Madison, WI, USA), and some CO1 sequences were downloaded from GenBank for comparative analysis (Tab. 1). All sequences were aligned again using DNASTAR software. A neighbor-joining (NJ) tree was created with all related Pampus species, and the distances between and within groups were calculated using MEGA 5.0 (Tamura et al., 2011) with 1000 bootstrap replicates based on evolutionary distances calculated using the best model, i.e., the Kimura 2-parameter (K2P) model.

3 Results

3.1 Morphological analysis

We accurately identified P. minor on the basis of biometrical characteristics of the studied specimens. Finally, we summarized its major diagnostic morphological characteristics as follows: body oval; dorsal fins VII-IX 34–39, pectoral fins 22–24, anal fins V-VII 35–39, caudal fins 18–20; transverse occipital canals and dorsal branches of the lateral line canal on top of the head with a truncated rear edge; ventral transverse occipital canals sparse and slightly longer than or equal in length to the dorsal branches; gill rakers thin (delicate), sparse, 3–4 + 8–10 = 11–14; and vertebrae 29–31. The detailed counts and measurements of the morphological characteristics of P. minor are provided in Table 2.

According to the data in Table 2, the numbers of caudal fin rays and vertebrae are distinct between P. minor and the other two Pampus species, while the remaining countable characters overlap. The most distinguishable characters of P. minor are the truncated edge of the transverse occipital canal and dorsal branches on the upper back of the head. The transverse occipital canal on the ventral branch is spare and slightly longer than or equal in length to the dorsal branch of the lateral line canal. The composition is similar to that of the intestinal wall, and the main function is to enlarge the absorption surface area, which verifies the identification of this species in the coastal waters of Wenzhou, China.

Table 2

Comparative counts and measurements of P. minor (including the data from Liu and Li (1998) and this study) and other Pampus species from Wenzhou, China.

3.2 Molecular analysis

Thirty-four sequences with a total length of 630 bp were employed in the analysis. The newly obtained CO1 haplotype sequences of P. minor have been submitted to GenBank under accession numbers MT316581-MT316586 (Tab. 1). In total, six variable sites, three parsimony-informative sites, and three singleton sites were identified, and no deletions/insertions were observed. The A+T base content (A: 26.2%; T: 33.1%) was higher than the G+C base content (G: 16.8%; C: 23.9%). The NJ phylogenetic tree is shown in Figure 2. All P. minor individuals clustered into a group, and P. echinogaster, P. argenteus, and P. cinereus clustered individually. Genetic distances between P. minor and the other three species of the genus Pampus ranged from 13.4% to 15.5%. The genetic distance within the P. minor group was only 0.2%, and the interspecific genetic distance was over 10 times greater than the intraspecific genetic distance, which vastly exceeded the threshold for species delimitation (Hebert et al., 2003b). The results of the combined morphological and genetic analyses strongly supported the validity of this new record of P. minor in Wenzhou.

thumbnail Fig. 2

NJ tree constructed using the K2P model for CO1 gene sequences of P. minor. Bootstrap values greater than 50% from 1000 replicates are shown.

4 Discussion

In 1998, Liu and Li first described the morphological characteristics of P. minor and confirmed its taxonomic status as a new species by comparing its morphological characteristics with those of other Pampus species (Liu and Li, 1998). Because of its small size (the adult does not exceed 150 mm in standard length) and the similarity of external characteristics within the genus Pampus, P. minor was regarded as the larva of P. argenteus and P. cinereus until Liu and Li (1998) identified it as a valid species (Li et al., 2019b).

Climate may be a significant factor determining the distribution of biomes (Dulvy et al., 2008; Perry et al., 2005). Climate change can influence the adaptability of different species in a region and the competitiveness of different populations within ecosystems (Vanderwal et al., 2013; Hoffmann and Sgro, 2011). Animals and plants in nature may be displaced because they are unable to adapt to global warming at an adequate speed (Wiens, 2016). Similarly, Chen et al. (2018) found that the observed northward migration of some Platyrhina sinensis individuals in Zhejiang from their southern habitat might be because of global warming. Studies have also shown that the distribution of Larimichthys polyactis in the central and southern waters of the Yellow Sea has shifted offshore in spring and northward in winter during the past 10 years (Shan et al., 2011). Given the adjacent waters, the changes in the distribution of P. minor may be somewhat related to global warming. Temperature is a critical factor for fish physiology (Shan et al., 2011), and an increase in temperature will affect the normal metabolic processes of fish and alter their physiology and life history. P. minor always appears in warm coastal waters (Liu and Li, 1998), and the coastal waters of Wenzhou are influenced by the high temperatures of the Taiwan Warm Current and South China Sea warm current, causing warm-water and warm-temperate species to dominate in these waters (Dong et al., 2017). Therefore, climate change may have shifted the distribution of P. minor northward to Wenzhou, changing its original distribution area.

As an alternative explanation, P. minor may have always been distributed in the coastal waters of Wenzhou, but because of the morphological similarity of Pampus fishes, it may have been misidentified as other Pampus species (Liu and Li, 1998; Li et al., 2019b). For example, for a long time, Periophthalmus magnuspinnatus was misidentified as other species of Gobiidae because of their similar morphological characteristics (Wang and Yang, 2006). Furthermore, it is possible that P. minor is rare in the coastal waters of Wenzhou and was ignored in previous surveys. Wang and Fan (2007) once found just five sharks in the southern area of the East China Sea and identified them as a new record, which was named Megachasma pelagios. The abundance of this species might be very low, but its occurrence in this area over a long period of time cannot be denied.

5 Conclusions

In this study, we used a combination of biometrical identification and molecular biological methods to identify P. minor. Our findings provide the first record of this species from the coastal waters of Wenzhou and revise the distribution range of this species. The species is mainly distributed in the southern part of the Taiwan Strait and the northern part of the South China Sea and Beibu Gulf, with its northernmost distribution reaching the coastal waters of Wenzhou, China. The reason for the observed northward migration of some P. minor individuals might be global warming. In summary, this study lays a solid foundation for the in-depth study of P. minor and provides evidence that global warming leads to the northward movement of species.

Acknowledgments

This research was funded by the National Key Research and Development Program of China (2018YFC1406302), the Natural Science Foundation of Fujian Province of China (2019J05146), the National Programme on Global Change and Air-Sea Interaction (GASI-02-SCS-YDsum/spr/aut), and the Bilateral Cooperation of Maritime Affairs (2200207). We also thank the anonymous reviewers for their helpful comments. The authors declare no conflicts of interest, and the authors alone are responsible for the content and writing of the paper.

References

  • Ali MA, Gyulai G, Hidvegi N, Kerti B, Hemaid FMAA, Pandey AK, Lee J. 2014. The changing epitome of species identification-DNA barcoding. Saudi J Biol Sci 21: 204–231. [CrossRef] [PubMed] [Google Scholar]
  • Cheng QT. 1962. Fishes of South China Sea. Beijing: China Ocean Press, pp. 759–766. [Google Scholar]
  • Chen Z, Wang XY, Zhang J, Li Y, Gao TX, Lin LS. 2018. First record of the Chinese fanray, Platyrhina sinensis (Elasmobranchii: Myliobatiformes: Platyrhinidae), in the seawaters of Zhujiajian, Zhoushan, China. Acta Ichthyol Piscatoria 48: 409–414. [CrossRef] [Google Scholar]
  • Divya PR, Mohitha C, Rahul GK, Shanis CPR, Basheer VS, Gopalakrishnan A. 2017. Molecular based phylogenetic species recognition in the genus Pampus (Perciformes: Stromateidae) reveals hidden diversity in the Indian Ocean. Mol Phylogenet Evol 109: 240–245. [Google Scholar]
  • Dolganov VN, Kharin VE, Zemnukhov VV. 2007. Species composition and distribution of butterfishes (Stromateidae) in waters of Russia. J Ichthyol 47: 579–584. [CrossRef] [Google Scholar]
  • Dong JR, Hu CY, Shui YY, Tian K. 2017. Fish community structure and its relationships with environmental factors in the southern inshore waters of Wenzhou. J Fish Sci China 24: 209–219. [Google Scholar]
  • Dulvy NK, Rogers SI, Jennings S, Stelzenmüller V, Dye SR, Skjoldal HR. 2008. Climate change and deepening of the North Sea fish assemblage: a biotic indicator of warming seas. J Appl Ecol 45: 1029–1039. [Google Scholar]
  • Elliott NG, Haskard K, Koslow JA. 1995. Morphometric analysis of orange roughy (Hoplostethus atlanticus) off the continental slope of southern Australia. J Fish Biol 46: 202 –220. [Google Scholar]
  • Guo EM, Liu Y, Liu J, Cui CX. 2010. DNA barcoding discriminates Pampus minor (Liu, et al., 1998) from Pampus species. Chin J Oceanol Limnol 28: 1266–1274. [Google Scholar]
  • Hebert PDN, Cywinska A, Ball SL, Dewaard JR. 2003a. Biological identifications through DNA barcodes. Proc R Soc London Ser B 270: 313–321. [CrossRef] [PubMed] [Google Scholar]
  • Hebert PDN, Ratnasingham S, Dewaard JR. 2003b. Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc R Soc London Ser B 270(Suppl_1), S96–S99. [Google Scholar]
  • Hoffmann AA, Sgro CM. 2011. Climate change and evolutionary adaptation. Nature 470: 479–485. [PubMed] [Google Scholar]
  • Hua XJ, Hui X, Wei HD. 2004. DNA barcoding: new approach of biological taxonomy. Acta Zool Sin 50: 852–855. [Google Scholar]
  • Li Y, Gao TX, Zhou YD, Lin LS. 2019a. Spatial genetic subdivision among populations of Pampus chinensis between China and Pakistan: testing the barrier effect of the Malay Peninsula. Aquat Living Resour 32: 8. [CrossRef] [EDP Sciences] [Google Scholar]
  • Li Y, Lin LS, Song N, Zhang Y, Gao TX. 2018. Population genetics of Pampus echinogaster along the Pacific coastline of China: insights from the mitochondrial DNA control region and microsatellite molecular markers. Mar Freshwater Res 69: 971–981. [CrossRef] [MathSciNet] [Google Scholar]
  • Li Y, Zhang Y, Gao TX, Han ZQ, Lin LS, Zhang XM. 2017. Morphological characteristics and DNA barcoding of Pampus echinogaster (basilewsky, 1855). Acta Oceanol Sin 36: 18–23. [CrossRef] [Google Scholar]
  • Li Y, Zhou YD, Li PF, Gao TX, Lin LS. 2019b. Species identification and cryptic diversity in Pampus species as inferred from morphological and molecular characteristics. Mar Biodivers 49: 2521–2534. [Google Scholar]
  • Liu J, Li CS. 1998. A new pomfret species, Pampus minor sp. nov. (Stromateidae) from Chinese waters. Chin J Oceanol Limnol 16: 280–285. [Google Scholar]
  • Liu J, Li CS. 2002. Phylogeny and biogeography of Chinese pomfret fishes (Pisces: Stromateidae). Stud Mar Sin 44: 235–239. [Google Scholar]
  • Nakabo T. 2002. Fishes of Japan: With Pictorial Keys to the Species. Tokyo: Tokai University Press. [Google Scholar]
  • Perry AL, Low PJ, Ellis JR, Reynolds JD. 2005. Climate change and distribution shifts in marine fishes. Science 308: 1912–1915. [Google Scholar]
  • Shan XJ, Li ZL, Dai FQ, Jin XS. 2011. Seasonal and annual variations in biological characteristics of small yellow croaker Larimichthys polyactis in the central and southern Yellow Sea. Prog Fish Sci 32: 7–16. [Google Scholar]
  • 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 28: 2731–2739. [CrossRef] [PubMed] [Google Scholar]
  • Vanderwal J, Murphy HT, Kutt AS, Perkins GC, Bateman BL, Perry JJ, Reside AE. 2013. Focus on poleward shifts in species' distribution underestimates the fingerprint of climate change. Nat Clim Change 3: 239–243. [CrossRef] [Google Scholar]
  • Wang HG, Fan ZY. 2007. New record species of shark from seacoast of china mainland. Acta Zootaxonomica Sin 32: 490–491. [Google Scholar]
  • Wang ZQ, Yang JQ. 2006. A long-term misidentified new record species of gobiidae from china- Periopaus magnuspinnatus . Acta Zootaxonomica Sin 31: 906–910. [Google Scholar]
  • Ward RD, Zemlak TS, Innes BH, Last PR, Hebert PDN. 2005. DNA barcoding Australia's fish species. Philos Trans R Soc B 360: 1847–1857. [CrossRef] [PubMed] [Google Scholar]
  • Wiens JJ. 2016. Climate-related local extinctions are already widespread among plant and animal species. PLoS Biol 14(12). [PubMed] [Google Scholar]
  • Yamada U, Tokimura M, Hoshino K, Deng SM, Zheng YJ, Li SF, Kim YS, Kim JK. 2009. Names and Illustrations of Fishes from the East China Sea and the Yellow Sea-Japanese/Chinese/Korean. Over seas Fishery Cooperation Foundation of Japan. Tokyo, pp. 525–528. [Google Scholar]
  • Yang WT, Jian LI, Yue GH. 2006 Multiplex genotyping of novel microsatellites from silver pomfret (Pampus argenteus) and cross-amplification in other pomfret species. Mol Ecol Resour 6: 1073–1075. [Google Scholar]

Cite this article as: Liu C, Yang Z, Liu P, Ye S, Siyal FK, Zhu G, Lin L, Li Y. 2020. First record of Pampus minor (Actinopterygii: Perciformes: Stromateidae) from the coastal waters of Wenzhou, China. Aquat. Living Resour. 33: 5

All Tables

Table 1

Information on the Pampus samples and sequences in this study.

Table 2

Comparative counts and measurements of P. minor (including the data from Liu and Li (1998) and this study) and other Pampus species from Wenzhou, China.

All Figures

thumbnail Fig. 1

P. minor collected from the coastal waters of Wenzhou, China (standard length: 101 mm).

In the text
thumbnail Fig. 2

NJ tree constructed using the K2P model for CO1 gene sequences of P. minor. Bootstrap values greater than 50% from 1000 replicates are shown.

In the text

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