This study constitutes the first record of the Por’s goatfish, Upeneus pori Ben-Tuvia et Golani, 1989, from the South China Sea. This fish had formerly only been reported in the western Indian Ocean. Six specimens of U. pori collected from the South China Sea were identified through comparisons of morphology and molecular analysis. Upeneus pori and Upeneus tragula Richardson, 1846 are very similar. The difference is that the former has seven spines in the first dorsal fin, lacks any spots or blotches on its body, and exhibits white or creamy white barbels. The latter has eight spines in the first dorsal fin, exhibits black spots on its body, and displays orange-colored barbels, along with different caudal fin patterns. Pairwise genetic distance computation demonstrated that U. pori exhibits a very low genetic distance from sequences of the other three recorded U. pori species found in the type locality of Israel, Red Sea, as documented in GenBank. These findings provide compelling evidence of the Por’s goatfish’s presence in the South China Sea.

COI, morphometry, novel distribution, south coast of China, taxonomy

The family Mullidae is composed of 100 species and six genera (Fricke et al. 2023) that are distributed in the Atlantic, Indian, and Pacific oceans and rarely found in brackish waters (Uiblein and Gouws 2014; Chen and Zhang 2015; Nelson et al. 2016). The mullids are otherwise known as goatfishes and have two independently moving hyoid barbels that contain chemical receptors used for detecting sand or holes in the reef to search for bottom-dwelling invertebrates. Until recently, the family Mullidae had been affiliated with the order Perciformes. Since 2022 it has been placed in Syngnathiformes (see Nash et al. 2022), which is accepted by (Fricke et al. 2023). A total of twenty-eight species of goatfishes, representing three genera (Mulloidichthys, Parupeneus, and Upeneus), have been recorded in China (Cheng et al. 1962; Shen 1993; Randall 2001). With the highly exhibited diversity of the goatfishes, the genus Upeneus Cuvier 1829 was revised by Lachner (1954), but only ten species were known at that time. Subsequently, Uiblein and Heemstra (2010) studied and verified the morphological characteristics of 26 species of Upeneus and summarized the taxonomy of this genus. They pointed out that 25 of the 26 species could be separated into four taxonomic groups (japonicus group, tragula group, moluccensis group, and vittatus group). Later, an increasing number of new species of Upeneus were described and new records of known species were reported worldwide using alpha taxonomy alone or in combination with barcoding approaches. To date, the number of valid species of the genus Upeneus has reached 47 species (Fricke et al. 2023) and there are seven taxonomic groups (japonicus group, tragula group, moluccensis group, stenopsis group, margarethae group, suahelicus group, pori group) (Uiblein and Maclaine 2021). The majority of these discoveries were concentrated in the Indian and Atlantic oceans (Yamashita et al. 2011; Nicolaidou et al. 2012; Uiblein and Lisher 2013; Bos 2014; Uiblein and White 2015; Uiblein et al. 2016, 2017, 2019, 2020; Deidun et al. 2018; Uiblein and Motomura 2021).

Since the discovery of Upeneus quadrilineatus Cheng et Wang, 1963, from the East China Sea, neither new species nor new records of Upeneus have been reported from this body of water. As recently as 2019, a new species Upeneus heterospinus Uiblein et Pavlov, 2019 was described, based on the material collected from the South China Sea (Uiblein et al. 2019). Thus, the following nine goatfishes of the genus Upeneus have been recorded in China: Upeneus tragula Richardson, 1846; Upeneus vittatus (Forsskål, 1775); Upeneus subvittatus (Temminck et Schlegel, 1843); Upeneus sulphureus Cuvier, 1829; Upeneus moluccensis (Bleeker, 1855); Upeneus japonicus (Houttuyn, 1782); Upeneus luzonius Jordan et Seale, 1907; U. quadrilineatus; and U. heterospinus. According to research related to the diversity and distribution of goatfishes in the western Pacific by Jiao and Chen (2000), the biodiversity of goatfish plummets from southern to northern waters in the China Sea. These authors also considered that the destruction of coral reefs has led to a sharp decline in fish production and some common species are difficult to find.

Materials and methods

Six specimens of fishes visually representing a species of the genus Upeneus were collected from the local fish markets in coastal cities near the northwestern South China Sea (Fig. 1). All specimens were caught by bottom trawling. Detailed collection information is given in Table 1. According to the key morphological characteristics provided by Ben-Tuvia and Golani (1989), these specimens were examined, identified, and deposited in the College of Fisheries, Guangdong Ocean University. We performed a morphometric examination on six samples according to the measurement and counting method by Uiblein and Heemstra (2010) and compared them with paratypes from the Red Sea described by Ben-Tuvia and Golani (1989). Standard length (SL) and other measurements were made with dial calipers from Shanghai Shenhan Measuring Tools Co., Ltd. with an accuracy of 0.1 mm.

Figure 1. 

Distribution records for Upeneus pori in the world’s oceans. The triangles indicate records added in this study and the circles denote historical records.

Table 1.

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Information on the COI sequences and collection in this study.

Species	Specimen No.	Sampling location	Coordinates	Accession No.	Source
U. pori	GOU103674	South China Sea, China	18.238°N, 109.509°E	GAF
	GOU103676	South China Sea, China	18.238°N, 109.509°E	MW922385	This study
	GOU103678	South China Sea, China	18.238°N, 109.509°E	MW922386	This study
	GOU104100	South China Sea, China	21.572°N, 111.832°E	MW922387	This study
	GOU104101	South China Sea, China	21.572°N, 111.832°E	GAF
	GOU104102	South China Sea, China	21.572°N, 111.832°E	MW922388	This study
	UpPo14A	Israel		KM538630	GenBank
	Upor	Egypt		LC572156	GenBank
	1059	Turkey		KY176690	GenBank
	P. 14829	Israel	31.799°N, 34.608°E	KF564319	GenBank
U. sulphureus	FSCS045-06	Guangdong, China	20.42°N, 109.84°E	EF607609	GenBank
	BW-A11206	Indonesia	8.80°S, 116.48°E	JN313348	GenBank
U. subvittatus	NS587	Nansha Island, China	5.317°N, 111.667°E	KY372338	GenBank
	NS586	Nansha Island, China	5.317°N, 111.667°E	KY372339	GenBank
U. quadrilineatus	BW-A6880	Jawa Timur, Indonesia	8.21667°S, 111.067°E	GU674207	GenBank
	BW-A6879	Indonesia	8.21667°S, 111.067°E	GU674208	GenBank
U. moluccensis	TR1879EK	Turkey	8.81°N, 78.14°E	KC501840	GenBank
	CIFE:FGB UM-01	India	8.81°N, 78.14°E	KJ920110	GenBank
U. japonicus	ASIZP0078749	Taiwan		KT718279	GenBank
	HMJ6	Shizuoka Japan	34.667°N, 138.333°E	JF952884	GenBank
U. tragula	GBMIN131725-17	Phu Quoc, Vietnam		KX887496	GenBank
	FSCS209-06	Guangdong, China	20.92°N, 110.54°E	EF607611	GenBank
Mullus argentinae	HRCB:53038	Sao Paulo, Brazil	26.352°S, 45.139°W	JQ365451	GenBank
Parupeneus multifasciatus	IRD BMF-162.2	Maluku, Indonesia	3.6876°S, 128.183°E	MN870495	GenBank

GAF = COI gene amplification failure.

Muscle tissues (50 mg) were stored in a 95% alcohol solution and in a –20°C freezer for later study. DNA was extracted by a Rapid Animal Genomic DNA Isolation Kit (Sangon Biotech, Inc., Shanghai, China). Using the universal primers FishF1 and FishR1, the COI gene was amplified (Ward et al. 2005). PCR was carried out in a 25 μL reaction mixture containing 12.5 μL of Taq PCR Master Mix (Sangon Biotech, Inc., Shanghai, China), 2 μL of MgCl₂, 5 μL of DNA template, 1 μL of forward, and reverse primer and 3.5 μL of ultrapure water. The thermal regime consisted of denaturation for three min at 95°C, followed by 33 cycles of 45 s at 92°C, 45 s at 50°C and one minute at 72°C, with post-extension at 72°C for ten min. Then, the temperature was maintained at 4°C. The PCR products were sequenced by Sangon Biotech Co., Ltd. (Shanghai) using an ABI PRISM 3730 DNA sequencer (Applied Biosystems, Foster City, CA, USA) with the BigDye Terminator kit (Applied Biosystems).

Sequence alignment and manual editing were performed using Sequencher 5.4.5 software. Four sequences were obtained and utilized to search for homologous sequences using BLAST on the NCBI website (Altschul et al. 1990) and then deposited in GenBank under accession numbers MW922385 to MW922388. The Maximum Likelihood (ML) method tree of 22 sequences was performed by the software PhyloSuite v.1.2.2 (Zhang et al. 2020), of which two sequences were downloaded from GenBank as out-group sequences: Parupeneus multifasciatus (Quoy et Gaimard, 1825), MN870495 and Mullus argentinae Hubbs et Marini, 1933, JQ365451. The HKY+G4+F model was selected for the best-fit model using the BIC criterion by ModelFinder (Kalyaanamoorthy et al. 2017). Maximum Likelihood phylogenies were inferred using IQ-TREE (Nguyen et al. 2015) with the HKY+G4+F model for 5000 ultrafast (Minh et al. 2013) bootstraps, as well as the Shimodaira–Hasegawa-like approximate likelihood-ratio test (SH-aLRT) (Guindon et al. 2010). The Kimura two-parameter model (K2P) model was used to calculate intra- and interspecific genetic distances of the genus Upeneus. Information on the COI sequences of Upeneus is provided in Table 1.

The collected specimens represented a single species, Upeneus pori, which was confirmed using morphological methods as well as DNA barcoding.

Taxonomy

Family Mullidae Rafinesque, 1815

Genus Upeneus Cuvier, 1829

 Upeneus pori Ben-Tuvia et Golani, 1989

(Figs 2 and 3; Table 2)

Morphological characteristics

The morphometric measurements are shown in Table 2. Head medium, obtuse, and conical; body laterally compressed and elongated; maxilla slightly longer than the mandible; cordiform teeth present in both jaws, palatine, and vomer; single complete lateral-line on each body side; snout slightly inferior; body with rhomboidal ctenoid scales; two separate dorsal-fins; two barbels on the chin; upper lobe of the caudal fin larger than the lower lobe.

Table 2.

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Presently reported (n = 6) morphometric measurements of Upeneus pori compared with the data of the paratypes in Ben-Tuvia and Golani (1989) (n = 22).

Character	Upeneus pori
	Presently reported study		Ben-Tuvia and Golani 1989
	Range	Mean	Range	Mean
SL [mm]	101.1–114.1	105	74–125
	In % SL
Body depth	24.4–26.4	25.2	21.8–25.9	23.9
Body width	14.3–17.2	15.8
Head length	23.7–27.1	25.8	25.8–29.2	27.8
Snout length	7.4–10.0	8.3	9.7–12.1	10.9
Orbit diameter	5.4–6.7	6.3	6.4–8.5	7.2
Interorbital width	7.6–8.0	7.8	6.6–8.1	7.4
Upper jaw length	6.0–10.7	8.6
Lower jaw length	5.4–9.1	7.6
Predorsal length	29.8–35.2	32.6	32.0–38.2	35.6
Prepelvic length	27.7–29.3	28.8
Preanal length	63.3–65.4	64.6
Prepectoral length	25.9–29.9	27.5
First dorsal-fin height	17.7–20.5	19.4	17.1–20.1	18.6
Second dorsal-fin height	13.5–16.8	15.1	13.0–16.9	15.1
Pectoral fin length	16.8–21.1	20.0	18.3–21.3	19.6
Pelvic fin length	13.8–18.2	17.4	16.5–20.5	18.3
Anal fin height	13.7–16.5	15.5	12.7–15.6	13.8
Caudal peduncle depth	9.9–10.9	10.2	9.4–11.1	10.0
Caudal peduncle length	21.0–25.2	23.1	21.9–27.8	25.6
Barbels length	16.7–18.1	17.2	15.3–20.1	17.1
Meristic counts
Dorsal fin rays	VII, 9		VII, 9
Anal fin rays	I-6–7		I-7
Pectoral fin rays	14		14–15
Lateral line scales	29–31		29–30
Scales above lateral line	2
Scales below lateral line	4–5
Total developed gill rakers	3–5 + 13–14
Total gill rakers	6–7 + 17–19		6–8 + 18–20

SL = standard length.

Color

Mainly based on recently deceased specimens (Fig. 2A). Dorsally darkened, head and sides reddish-brown, belly whitish; mid-lateral body with faint brownish-red bar running from snout to base of caudal fin in fresh fish; barbels white or creamy white; first and second dorsal-fins with 3–4 sets of reddish-brown spots running horizontally; pectoral fins cream-colored to transparent; pelvic fins creamy-white and base of fins with several yellow marks; anal fin rays whitish with transparent membranes; upper lobe of caudal fin with 4–5 oblique reddish-brown stripes intersecting rays; middle part of lower lobe of caudal fin with wide reddish-brown band extending from base of caudal fin to tip of lower lobe; 3–4 red-brown stripes above wide band; 6–7 stripes with same color below wide band and all stripes approximately perpendicular to wide band; fluorescent yellow spots between stripes on both lobes of caudal fin, sometimes vague (Figs 2C and 2D). The preserved specimens are dorsally dark-brown; all fins retain original spots, bars, or stripes; mid-lateral sides with faint dark grey bar (Fig. 2B).

Figure 2. 

Upeneus pori, 106 mm SL, GOU104100, (A) fresh specimen; (B) preserved specimen; (C) caudal-fin characteristics; (D) drawing of caudal-fin patterns.

Sequence analysis of the COI gene

The mean sequence of some mitochondrial cytochrome C oxidase (COI) genes, collected from fish specimens examined in the presently reported study, was 690 nucleotide sites. The base frequencies of A, C, T, and G of twenty COI sequences were 22.2%, 29.4%, 29.4%, and 19.0%, respectively and the A + T content (51.6%) was greater than the C + G content (48.4%). The intraspecific genetic distance ranged from 0% to 1.58% and the interspecific genetic distance ranged from 8.87% to 19.36% (Table 3). The interspecific genetic distance was much greater than the intraspecific genetic distance. According to the results of the maximum likelihood tree (Fig. 4), Upeneus sulphureus, U. subvittatus, U. quadrilineatus, U. moluccensis, U. japonicus, and U. tragula clustered and separated from U. pori with high bootstrap values and SH-aLRT values, respectively, indicating significant differentiation amongst them, of which the sequences in this study (GOU103676, GOU103678, GOU104100, and GOU104102) were clustered with the sequences (KM538630, LC572156, KY176690, and KF564319) distinguished as U. pori in the Red Sea area from GenBank with high SH-aLRT and ultrafast bootstrap values (97/99). The genetic distance (Table 4) shows that the U. pori collected in the South China Sea and the U. pori from the Red Sea belong to the species range.

Table 3.

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Interspecific (bottom half of matrix) and intraspecific (bold diagonal) sequence divergences of 7 species of Upeneus, corrected using the Kimura two-parameter (K2P) model.

	U. japonicus	U. pori	U. tragula	U. sulphureus	U. subvittatus	U. quadrilineatus	U. moluccensis
U. japonicus	0.0039
U. pori	0.1328	0.0000
U. tragula	0.1089	0.0950	0.0000
U. sulphureus	0.1821	0.1751	0.1600	0.0098
U. subvittatus	0.1936	0.1759	0.1686	0.1250	0.0019
U. quadrilineatus	0.1645	0.1705	0.1555	0.1048	0.1072	0.0000
U. moluccensis	0.1930	0.1675	0.1679	0.1285	0.0887	0.1012	0.0158

Table 4.

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Pairwise genetic distance calculated using the K2P model between the COI gene sequences of Upeneus pori from the South China Sea (this study) and the 12 sequences of different species of Upeneus from GenBank.

Group	Sequence	Group
		1	2	3	4	5	6	7	8	9	10	11	12	13	14	15	16	17	18	19
1	GOU103676_U. pori_SCS
2	GOU103678_U. pori_SCS	0.0000
3	GOU104100_U. pori_SCS	0.0000	0.0000
4	GOU104102_U. pori_SCS	0.0000	0.0000	0.0000
5	KM538630_U. pori_RS	0.0000	0.0000	0.0000	0.0000
6	LC572156_U. pori_RS	0.0000	0.0000	0.0000	0.0000	0.0000
7	KY176690_U. pori_RS	0.0000	0.0000	0.0000	0.0000	0.0000	0.0000
8	KF564319_U. pori_RS	0.0000	0.0000	0.0000	0.0000	0.0000	0.0000	0.0000
9	EF607609_U. sulphureus_SCS	0.1751	0.1751	0.1751	0.1751	0.1751	0.1751	0.1751	0.1751
10	JN313348_U. sulphureus_IDOW	0.1751	0.1751	0.1751	0.1751	0.1751	0.1751	0.1751	0.1751	0.0098
11	KY372338_U. subvittatus_SCS	0.1746	0.1746	0.1746	0.1746	0.1746	0.1746	0.1746	0.1746	0.1274	0.1250
12	KY372339_U. subvittatus_SCS	0.1772	0.1772	0.1772	0.1772	0.1772	0.1772	0.1772	0.1772	0.1250	0.1226	0.0019
13	GU674207_U. quadrilineatus_ IDOW	0.1705	0.1705	0.1705	0.1705	0.1705	0.1705	0.1705	0.1705	0.1037	0.1060	0.1084	0.1060
14	GU674208_U. quadrilineatus_ IDOW	0.1705	0.1705	0.1705	0.1705	0.1705	0.1705	0.1705	0.1705	0.1037	0.1060	0.1084	0.1060	0.0000
15	KC501840_U. moluccensis_IDAW	0.1699	0.1699	0.1699	0.1699	0.1699	0.1699	0.1699	0.1699	0.1344	0.1222	0.0897	0.0920	0.1010	0.1010
16	KT718279_U. moluccensis_SCS	0.1651	0.1651	0.1651	0.1651	0.1651	0.1651	0.1651	0.1651	0.1348	0.1226	0.0854	0.0876	0.1013	0.1013	0.0158
17	KJ920110_U. japonicus_SCS	0.1303	0.1303	0.1303	0.1303	0.1303	0.1303	0.1303	0.1303	0.1742	0.1847	0.1922	0.1896	0.1620	0.1620	0.1927	0.1878
18	JF952884_U. japonicus_JAW	0.1353	0.1353	0.1353	0.1353	0.1353	0.1353	0.1353	0.1353	0.1794	0.1900	0.1976	0.1949	0.1671	0.1671	0.1981	0.1932	0.0039
19	KX887496_U. tragula_SCS	0.0951	0.0951	0.0951	0.0951	0.0951	0.0951	0.0951	0.0951	0.1625	0.1574	0.1699	0.1673	0.1555	0.1555	0.1677	0.1065	0.1682	0.1113
20	EF607611_U. tragula_SCS	0.0951	0.0951	0.0951	0.0951	0.0951	0.0951	0.0951	0.0951	0.1625	0.1574	0.1699	0.1673	0.1555	0.1555	0.1677	0.1065	0.1682	0.1113	0.0000

SCS = South China Sea, RS = Red Sea, IDOW = Indonesian waters, IDAW = Indian waters, JAW = Japanese waters.

Upeneus pori was first reported in the Mediterranean by Kosswig (1950) as U. tragula. Then, Ben-Tuvia and Golani (1989) re-examined the specimens and suggested there was a new species of the genus Upeneus in the Red Sea and named the new one Upeneus pori in recognition of Professor Francis Dov Por’s contribution to the field of the Lessepsian migration of organisms. Before this time, many scholars misidentified U. pori for other species of Upeneus (see Ben-Tuvia 1953, 1966; George and Athanassiou 1966, 1967). Although few resources of U. pori were investigated in the Chinese waters, we observed U. pori was often mingled with U. tragula for sale in the local fish markets. The reason for the above is that there is still a lack of systematic classification of Upeneus species in China. At the same time, some Upeneus species exhibit a similar body color after death (Figs 3C and 3D), which can lead observers to believe it is the same fish. In addition, due to the lack of resources, it is highly likely to be ignored as another species and considered to be U. tragula. Here are different diagnoses between U. pori and U. tragula (Figs 2A, 2C, and 2D; Figs 3A and 3B; Table 5):

Figure 3. 

Comparison between Upeneus pori and Upeneus tragula. (A) Upeneus pori, fresh, 114 mm SL; (B) Upeneus tragula, fresh, 216 mm SL, (C) Upeneus pori, dead, 102 mm SL, GOU103678, this study; (D) Upeneus tragula, dead, 145.4 mm SL. Photos A and B by Randall JE (1997). Randall’s tank photos. Collection of 10,000 large-format photos (slides) of dead fishes. Published in Froese and Pauly (2023). Photo D by Sahat Ratmuangkhwang; published in Froese and Pauly (2023).

Figure 4. 

Maximum Likelihood phylogenetic tree of Upeneus pori, based on DNA sequences of the mitochondrial COI gene (bold fonts for sequences of this study, not bold for previous research). Numbers on the branches indicate the Shimodaira–Hasegawa-like approximate likelihood ratio test (SH-aLRT) and ultrafast bootstrap support (only values above 70% are displayed).

• barbels color: white or creamy-white vs. yellow barbels, but may be pale brown or orange in fresh fish;
• body pattern: without any spots or blotches vs. slightly darker above the lateral line, with irregular red, brown, or black spots and/or blotches;
• first dorsal-fin: seven spines, without blotch around tip, vs. eight spines, with a large blotch around tip;
• caudal-fin: different pattern shown in Uiblein and Heemstra (2010).

Uiblein and Heemstra (2010) established four taxonomic groups for separating morphologically similar species within the same group. They included 25 of the 26 species recorded in China, being separated in japonicus group, tragula group, moluccensis group, and vittatus group, which were distinguished by the differences in the number of spines in the first dorsal-fin, gill rakers, pectoral-fin rays, and stripes of the caudal-fin. Upeneus pori belonged to the japonicus group, as suggested by Uiblein and Heemstra (2010). New species and new records were gradually recorded, resulting in the taxonomic status of Upeneus being altered. The vittatus group was divided into the stenopsis group (Uiblein and Causse 2013) and the suahelicus group (Uiblein and Gouws 2015), causing U. vittatus to be ungrouped and the vittatus group to be cancelled. Uiblein et al. (2019) reported that Upeneus margarethae Uiblein et Heemstra, 2010; Upeneus mouthami Randall et Kulbicki, 2006; and Upeneus randalli Uiblein et Heemstra, 2011 differed from other tragula group species in the first dorsal-fin tip without dark pigmentation, total gill rakers 21–25 and 28–30 lateral-line scales so a new taxonomic group was proposed—the margarethae group. Uiblein and Maclaine (2021) proposed reclassifying U. pori, originally part of the japonicus group, into the newly established pori group. This reclassification is based on the limited distribution range exhibited by members of the pori group, as well as their shared coloration and morphological characteristics. These features distinguish them from other members of the japonicus group. As for Chinese records, they include the margarethae group (U. heterospinus), japonicus group (U. japonicus), moluccensis group (U. moluccensis, U. quadrilineatus, and U. sulphureus), stenopsis group (U. subvittatus), tragula group (Upeneus sundaicus (Bleeker, 1855), U. luzonius, and U. tragula), and ungrouped (U. vittatus). In this study, we have identified U. pori, a member of the pori group, which is recorded in China for the first time.

This study has a certain reference value for the taxonomy of the genus Upeneus in the coastal areas of China. For further research and an in-depth understanding of the taxonomy and phylogeny of Upeneus within China’s regional distribution, it is necessary to collect sufficient samples in various Chinese waters and provide detailed morphological characteristics. Apart from morphology, molecular analysis enables us to collect more knowledge about the taxonomy and phylogeny of Upeneus, which also contributes to coastal ecosystem management measures and provides the basis for the protection of local species diversity.

The presently reported study confirms a new record of Upeneus pori from the South China Sea, based on morphological characteristics and DNA barcodes and this record expands the distributional range of U. pori in the world’s oceans and enriches the species composition and biodiversity of the South China Sea. This study also emphasizes that it is essential to increase taxonomic studies to survey the South China Sea with its high species diversity to better protect species diversity and monitor marine fisheries in the South China Sea.

We gratefully acknowledge the funding support under the Guangdong Basic and Applied Basic Research Foundation, Grant/Award Number: [2019B1515120064]; Southern Marine Science and Engineering Guangdong Laboratory (Zhanjiang), Grant /Award Number: [ZJW-2019-08]; Science and Technology Plan Projects of Guangdong Province, China, Grant/Award Number: [2018B030320006].