Larval Spatiotemporal Distribution of Six Fish Species: Implications for Sustainable Fisheries Management in the East China Sea

: The larval distributions of the small-sized fishes Omobranchus elegans , Erisphex pottii , Benthosema pterotum , Acropoma japonicum , Upeneus bensasi , and Apogonichthys lineatus in the East China Sea ecosystem are important due to their ecological and economic benefits. To date, however, there have been few studies describing their population distributions and dynamics. In the current study, ichthyoplankton surveys were carried out from April to July 2018 to analyze variations in the larval abundance, distribution, and development stages of these species. In addition, the spatiotemporal larval distribution was investigated in terms of measured environmental variables. It was found that larvae were mainly distributed at depths of 5.00–66.00 m, in areas with sea surface temperature of 4.40–29.60 ◦ C, sea surface salinity of 16.54–34.60 psu, pH of 7.00–9.00, and dissolved oxygen concentration of 2.54–8.70 mg/L. Benthosema pterotum and A. lineatus migrated from 30.00–31.00 ◦ N 123.17–123.50 ◦ E in June to 30.00–32.50 ◦ N 122.22–123.50 ◦ E in July. The results of this study can help to preserve spawning and nursery grounds and contribute to sustainable coastal fisheries management.


Introduction
The East China Sea is one of the most productive and warming marginal seas in the world, which has also been over-exploited since the late 1980s by large fisheries [1]. The area is connected to terrestrial water, the Pacific Ocean, the Sea of Japan, and the Yellow Sea by a very complex ocean system, including both deep and shallow sea features [2]. Several water masses in this area are described as Changjiang river diluted water (CRDW), with low temperature and salinity, Taiwan Warm Current (TWC), with high temperature and salinity, Yellow Sea cold water mass, with low temperature and high salinity, and Subei coastal current, with high temperature and low salinity. Kuroshio current flows from eastern Taiwan, enters into the East China Sea region, and then flows along the continental shelf. The Taiwan warm current extends northward and outward from the central Zhejiang coast to the southern Changjiang estuary. The distribution characteristics of the ichthyoplankton assemblages in this area are very complex. Many factors, such as type of water mass, might influence the larval distribution in shelf waters.
Understanding the larval distributions of the fishes Omobranchus elegans, Erisphex pottii, Benthosema pterotum, Acropoma japonicum, Upeneus bensasi, and Apogonichthys lineatus is crucial for the maintenance and sustainable development of the East China Sea

Materials and Methods
The study area covered the southern Yellow Sea and the northern East China Sea. The average depth of the southern Yellow Sea is 45.00 m. The study area included the Yellow Sea warm current and the Yellow Sea cold water mass [22]. As one of the largest marginal semi-enclosed sea areas in the western Pacific Ocean, the northern East China Sea is characterized by oceanic water with high salinity and diluted coastal water with low salinity [23]. Kuroshio current flows from eastern Taiwan, enters into the East China Sea region, and then flows along the continental shelf [24]. The Taiwan warm current extends northward and outward from the central Zhejiang coast to the southern Changjiang estuary. Larvae of O. elegans, E. pottii, B. pterotum, A. japonicum, U. bensasi, and A. lineatus were collected in situ, on a monthly basis, as part of cruises over the continental shelf area (24.26-33.00 • N 118.55-123.50 • E; 133 sampling stations) from April to July 2018. The cruises were within the closed area for marine trawl fisheries in the southern Yellow Sea and the northern East China Sea and were carried out on fishing vessels (#Lanhai 201 and #Zhongkeyu 211) (Figure 1). The survey transects were perpendicular to the coastline of China, with a sampling grid of approximately 0.50 • N latitude (0.25 • latitude in a range of 30. 50-31.50 • N) and separated by a distance of 0.167 • E longitude, moving progressively from west to east.
The average depth of the southern Yellow Sea is 45.00 m. The study area included the Yellow Sea warm current and the Yellow Sea cold water mass [22]. As one of the largest marginal semi-enclosed sea areas in the western Pacific Ocean, the northern East China Sea is characterized by oceanic water with high salinity and diluted coastal water with low salinity [23]. Kuroshio current flows from eastern Taiwan, enters into the East China Sea region, and then flows along the continental shelf [24]. The Taiwan warm current extends northward and outward from the central Zhejiang coast to the southern Changjiang estuary.
Larvae of O. elegans, E. pottii, B. pterotum, A. japonicum, U. bensasi, and A. lineatus were collected in situ, on a monthly basis, as part of cruises over the continental shelf area (24.26-33.00° N 118.55-123.50° E; 133 sampling stations) from April to July 2018. The cruises were within the closed area for marine trawl fisheries in the southern Yellow Sea and the northern East China Sea and were carried out on fishing vessels (#Lanhai 201 and #Zhongkeyu 211) ( Figure 1). The survey transects were perpendicular to the coastline of China, with a sampling grid of approximately 0.50° N latitude (0.25° latitude in a range of 30.50-31.50° N) and separated by a distance of 0.167°E longitude, moving progressively from west to east. For sample collection, the engine of the survey vessel was stopped, and cone-shaped ichthyoplankton nets (130 cm diameter, 600 cm length, and 0.50 mm mesh size) were cast into the sea, equipped with a calibrated flowmeter mounted in the center of net mouth to measure flow rate. Near-surface discrete sampling was carried out with the top of the net ring just below the air-water interface for 10 min ("horizontal haul"). Near-bottom discrete sampling was carried out by towing the net from the near bottom to the near surface For sample collection, the engine of the survey vessel was stopped, and cone-shaped ichthyoplankton nets (130 cm diameter, 600 cm length, and 0.50 mm mesh size) were cast into the sea, equipped with a calibrated flowmeter mounted in the center of net mouth to measure flow rate. Near-surface discrete sampling was carried out with the top of the net ring just below the air-water interface for 10 min ("horizontal haul"). Near-bottom discrete sampling was carried out by towing the net from the near bottom to the near surface for 10 min, using a buoy line to adjust the desired depth ("oblique haul"). We used a SeaBird SBE−19 CTD at each site to record hydrographic parameters such as depth, water temperature, salinity, pH, and dissolved oxygen concentration. After the hauls, ichthyoplankton samples containing O. elegans, E. pottii, B. pterotum, A. japonicum, U. bensasi, and A. lineatus larvae were immediately washed into a stainless end collection cup with flowing seawater. The samples were preserved in situ in 5% buffered formaldehyde prepared in seawater for further analysis. Larvae from the samples were identified using morphological classification and enumerated in the laboratory using a stereomicroscope (ZEISS, Stemi 2000, Oberkochen, Germany). The developmental stages were divided into yolk-sac, preflexion, flexion, postflexion, and juvenile stages. The density of larvae in We calculated the habitat suitability index (HSI) to investigate fish larval number distribution patterns of B. pterotum and A. lineatus in relation to selected measured hydrographic parameters, including depth (m), sea surface temperature ( • C), sea bottom temperature ( • C), sea surface salinity (psu), and sea bottom salinity (psu) in June and July 2018. HSI was obtained by comprehensive calculations of many number-based suitability index (SI) values [25]. Each SI was estimated as a value between 0.0 and 1.0. The SIs were estimated as follows: where Y is larvae number after smoothed regression and Y max and Y min are maximum and minimum predicted values. A SI value is closer to 1.0 means a higher suitability index, and a SI value closer to 0.0 means a lower suitability index. SI values between 0.7 and 1.0 correspond to environmental factors that are regarded as the most suitable environment range [26].
We calculated HSI values using the equation given below: where HSI is habitat suitability index, SI i is the SI value of the environmental variable, i and w i are the weight of the environmental variable, and i, and n are the number of environmental factors [27]. Finally, a hydrodynamic numerical model was applied to simulate salinity and sea temperature structures. Based on the original estuarine, coastal and ocean models [28], the State Key Laboratory of Estuarine and Coastal Research, East China Normal University developed and improved the model [29]. A third-order HSIMT advection scheme was used to solve the tracer advection terms [29]. The model domain covered the entire Yellow Sea, East China Sea, and Bohai Sea, as well as part of the Pacific Ocean and the Japan Sea. The mesh grid with a resolution of~1 km or higher was refined to 367 × 319 based on previous studies inside the Changjiang River Estuary and 2-4 km east and south of the Changjiang River mouth [30]. The model previously was validated comprehensively and performed in reproducing multi-scale salinity, temperature, and current distribution structures reasonably [31][32][33][34][35][36].

Positive Sampling Stations and Larval Number
The positive sampling stations number range of O. elegans, E. pottii, B. pterotum, A. japonicum, U. bensasi, and A. lineatus were 2-24, 1-11, 1-51, and 11 only in July, and 3-6 and 1-40 thereafter. The stations of O. elegans, E. pottii, and A. lineatus were recorded at 24, 11, and 40 in June, respectively, making June the month with the highest number of records. In the other sampling months, E. pottii was only recorded at 1-2 sampling stations. Omobranchus elegans and A. lineatus were recorded at the second highest number of sampling stations in July, being present at 15 and 29 stations, respectively. Apogonichthys japonicum was recorded at 11 sampling stations in July, and U. bensasi was recorded at 3-6 sampling stations from April to July. Benthosema pterotum was recorded at the highest number of sampling stations (51) in July, followed by 32 sampling stations in June, with the lowest number of records (1 and 3 sampling stations) from April to May (Table 1).
Benthosema pterotum Acropoma japonicum In terms of larval number, only 52 A. japonicum individuals were collected in July during the oblique haul. For B. pterotum, 1 and 3 individuals were collected from April to May. However, 5303 and 8527 individuals were collected in the horizontal and oblique hauls in July, respectively. The number of B. pterotum larvae collected by oblique hauls in June and July was higher than the number collected in horizontal hauls. The number of U. bensasi larvae was recorded as 3-34 and 2-29 individuals (ind), respectively, in horizontal and oblique hauls. The abundance of E. pottii larvae was highest in June, and very few individuals were collected in the other months. The abundance of O. elegans larvae in the horizontal hauls was higher than the number in oblique hauls, particularly in May (120 versus 7 individuals) and July (101 versus 10 individuals). A low abundance (1-3 individuals) of A. lineatus was recorded in samples from April to May, with highest abundance (174-364 individuals) recorded from June to July (Table 1).

Apogonichthys lineatus
The larvae of O. elegans collected in horizontal hauls were predominantly in the preflexion stage from May (114 individuals) to June (42 individuals), while the postflexion stage was dominant in July (63 individuals). The larvae of E. pottii were predominantly in the preflexion stage in June. The majority of B. pterotum larvae were in the flexion stage in June and postflexion and juvenile stages in July. Acropoma japonicum larvae were recorded from the yolk-sac to the postflexion stage, with the preflexion stage being dominant in July. The larvae of U. bensasi ranged from the preflexion to juvenile stages from April to June, and the majority were at the juvenile stage in July. The larvae of A. lineatus, collected in horizontal hauls in June, were mainly in the flexion stage (245 individuals), while those collected in oblique hauls were in the preflexion to postflexion stages (Table 1).

Spatiotemporal Abundance Distributions
The spatial distribution range of O. elegans in June mainly included the coastal area of the Zhejiang coastline and outside the Yangtze Estuary, at latitudes ranging from 26.00 • N to 32. (Figures 1 and 3 and Table 2). Compared with the distribution range of B. pterotum, the spatial distribution of A. lineatus was closer to the Yangtze River estuary in July (Figure 3). The habitat-area range of these two species roughly overlapped.

Variations in Measured Environmental Variables
The six species were distributed from shallow waters (5.00 m deep) to deeper waters (66.00 m deep). The sea surface temperature (SST) range of the six species was 4.40-29.60 • C.
Omobranchus elegans had the widest temperature range, from 4.40-28.73 • C. The lower SST limit of E. pottii, U. bensasi, and A. lineatus were similar (18.69 to 18.89 • C), and the upper range limits for these species were 25.20, 28.07, and 29.60 • C, respectively. The highest SST values for B. pterotum and A. japonicum were 29.60 • C, but the lower SST limit of B. pterotum was far lower than that of A. japonicum ( N (Figure 3).     (Table 3).

Discussion
Benthosema pterotum larvae were recorded almost all year round in the East China Sea, with the highest abundance from July to August [17]. In the Indian Ocean, Benthosema pterotum spawning takes place throughout the year with peaks from March to June and September to November, which corresponds to the transition period between monsoon seasons [37]. In the Oman Sea, the breeding season is from May to September [18]. In the current study, B. pterotum larvae were most abundant in July. This indicated that the spawning period in the East China Sea is much shorter than that in the Indian Ocean.
In terms of habitat, adult B. pterotum are reported to be distributed in the area of north of 30.00 • N [38]. They migrate a short distance in the northern East China Sea, from the southwest in winter to the northeast in spring, and then from the northeast in summer to the southwest in autumn. The population distribution in spring and summer is a little more east than that in autumn and winter [38].  suggested that adults are mainly distributed in  Sassa et al. (2015) also observed that the high abundance of the larvae occurred in the area of 30.00-30.50 • N 124.50-126.00 • E [39]. That is to say, the spawning grounds might be in the intersecting waters between the Changjiang diluted water and Kuroshio branch current. The shelf-break salinity front might act as a barrier restricting the offshore dispersion of the larvae, enabling them to recruit into the area of adult habitat. In addition, cold water in Northern Taiwan resulting from the impingement of the Kuroshio Current onto the continental shelf causes upwelling, creating good spawning and nursery grounds for B. pterotum [40].
The current study also identified the larvae of B. pterotum migrating to the nearshore. The density of the adult population was reported to be higher in the nearshore waters than offshore areas [38], suggesting that larger individuals of this species preferred to inhabit coastal waters. Some juveniles moved to the south of the Changjiang River estuary. We suggest that the reason they migrate to the inshore area is due to high productivity and low transparency. High concentrations of B. pterotum were observed in the highly productive areas [41]. It has been reported that increases in primary production occur with greater river discharge from nearshore waters to offshore waters in the East China Sea [42]. Regarding the low transparency, highly turbid waters in the bottom layer are found at 30.00-32.00 • N over the mud shelf region [43]. Suspended particulate matter discharged into the ocean along with river water produced highly turbid waters. The dim light conditions enable the mesopelagic B. pterotum to live in such a shallow area. In addition, the larvae are less likely to be preyed upon when water turbidity increases and light decreases [44].
In the current study, the larvae of B. pterotum were mainly in the flexion stage in June and the postflexion stage in July. Owing to a very short egg hatching period (12 h at 21 • C) [45], the distribution of larvae at the preflexion to flexion stages represented the approximate location of the spawning grounds. After complete formation of the caudal fin base, postflexion larvae have sufficient swimming ability. It was reported that the preflexion and flexion larvae were mainly observed in the waters of the south and central shelf region, and postflexion larvae and juveniles were abundant in the waters of the north and peripheral shelf region of the East China Sea [46]. In terms of larval abundance, the mean abundance of the larvae in this study was 0.06-5993.68 ind/100 m 3  In terms of measured hydrographic characteristics (such as DO, water temperature, and salinity) affecting the distribution of the larvae, the largest DO range in the current study was recorded for B. pterotum (4.80 to 8.50 mg/L). CCA ordination analysis showed that the larvae were most influenced by high DO concentrations [47]. High DO concentrations in the coastal waters, caused by upwelling, attracted larvae to move inshore [48]. In the Indian Ocean, spawning is expected to occur in waters of~21.00-28.00 • C [45]. The optimal water temperature for the larvae in the current study was 18.00-20.00 • C with a range of 13.97-29.60 • C, suggesting an optimum temperature >24.00 • C for larvae [49]. Larvae in the preflexion and flexion stages inhabit optimum temperatures ranging from 28.20 to 28.80 • C at 25.00−29.00 • N 121.00−125.00 • E [46]. The sea surface temperature isotherm produced by the Kuroshio front might be a key oceanographic structure defining larval distribution dynamics. Sassa et al. (2014) suggested that salinity affected the distribution of the larvae [50]. In the Arabian Sea, the salinity of the larvae ranged from 35.00 to 37.00 psu [51]. On the shelf of the East China Sea, the salinity was much lower than that of the Arabian Sea with a range of 33.50-33.90 psu [52]. Sassa et al. (2014) suggested two distinct distribution patterns of larvae: the area of <33.70 psu and near the 33.70 psu isohaline [50]. Our study suggested the bottom salinity isohaline of 32.00-34.00 psu for larvae distribution. Conclusively, the East China Sea is one of the most rapidly warming large marine ecosystems, and its SST increased by 1.22 • C between 1982 and 2006 [54]. SST showed a significant warming trend in the waters of China, and its increasing rate is far higher than the global average [55,56]. Wang et al. (2020) reported that the SST in the waters of northeastern Taiwan in winter increased between 1985 and 2015 [45]. In July and August 2017, extreme warm SST anomalies (SSTAs) were observed in the northern Yellow Sea, which lasted for 60 days with a maximum daily SST of 2.93 • C on the date of the peak. High water temperature was considered as one of the most important factors leading to the mass emaciation and mortality of scallops on Zhangzi Island [57,58]. Larval assemblies are more easily to be affected by extra climate and increasing water temperature. Thus, it is important to perform continuous large-scale ichthyoplankton surveys in the East China Sea to understand the spatiotemporal variations of eggs and larvae of important fish species in the context of increasing temperatures.

Summary
The descriptions on the larval distribution of the small-sized fishes Omobranchus elegans, Erisphex pottii, Benthosema pterotum, Acropoma japonicum, Upeneus bensasi, and Apogonichthys lineatus in the East China Sea ecosystem remain scant. The current study contributed to the knowledge of the spatiotemporal distributions and dynamics of the early life history of these species. Especially, we found B. pterotum and A. lineatus migrated from 30.00-31.00 • N 123.17-123.50 • E in June to 30.00-32.50 • N 122.22-123.50 • E in July. Our findings contribute to the maintenance of ocean biodiversity and promote sustainable fisheries managements.
Author Contributions: M.X., L.Y., Z.L., Y.W. and J.C. contributed to the development, planning, data collection; Y.J., X.Y., H.Z., X.S. and T.O. contributed to data analysis and interpretation. All authors contributed to the writing of the manuscript. All authors have read and agreed to the published version of the manuscript.