Seasonal and Spatial Distribution Characteristics of Sepia esculenta in the East China Sea Region: Transfer of the Central Distribution from 29° N to 28° N

Simple Summary Since the 1990s, the golden cuttlefish (Sepia esculenta) has become the dominant cuttlefish fisheries target in the seas around China. In this paper, we aim to determine the current resource status and spatio-seasonal variation in the population in the East China Sea region. We found more juveniles at latitudes of 27.50–28.00° N and 29.00° N and more subadult individuals at 28.50° N in autumn, exhibiting different growth rates and resource densities. In addition, we found the majority of the catches were composed of parent groups in spring, while in autumn, the majority of the catches were composed of juvenile groups. We concluded that the subadult groups might have dispersed widely for feeding and growth along the latitude of 30.00° N and to the south in summer, and the southern area of the Yangtze River extending north was the spawning ground in spring. The groups of S. esculenta preferred to stay in areas with a stable water temperature of ~20.00 °C, and many S. esculenta juveniles might have adapted to endure the negative influence of the low oxygen content in summer. The depth range of the S. esculenta population was 10.00–133.00 m from spring to autumn, but this shrank to 66.00–107.00 m in winter. Abstract The golden cuttlefish (Sepia esculenta) is an important cephalopod species with a lifespan of approximately one year. The species plays a crucial role in marine ecological support services and is commercially valuable in fisheries. In the seas around China, this species has emerged as the main target for cuttlefish fisheries, replacing Sepiella maindroni since the 1990s. Variations in oceanographic conditions associated with global warming could significantly impact the temporal-spatial distribution of the species. In this study, we performed bottom trawling surveys with four cruises during 2018–2019 in the East China Sea region to determine the current resource status and seasonal-spatial variations in S. esculenta. We found that the average individual weight (AIW) values were 4.87 and 519.00 g/ind at stations located at 30.50° N, 124.00° E and 30.50° N, 124.50° E, respectively, with the aggregation of larvae and parent groups in spring. The species was not distributed north of 32.00° N in summer. The catch per unit effort by weight (CPUEw) value decreased in the order of 2772.50→2575.20→503.29→124.36 g/h, corresponding to latitudes of 34.50° N→34.00° N→33.50° N→32.50° N 121.50° E in autumn. The most suitable fishing areas were the south of the East China Sea region in spring; the south of the East China Sea region extending to the center and outer parts of the East China Sea region in summer; the south of the Yellow Sea close to the Haizhou Bay fishing ground and the forbidden fishing line region of the Lusi and Dasha fishing grounds in autumn; and the south and center of the East China Sea region in winter. The most suitable sea bottom temperature (SBT) values from spring to winter were 14.76–20.53 °C, 19.54–22.98 °C, 11.79–17.64 °C, and 16.94–20.36 °C, respectively. The most suitable sea bottom salinity (SBS) values were 31.53–34.80‰ in spring, 32.95–34.68‰ in summer, 31.51–34.77‰ in autumn, and 33.82–34.51‰ in winter. We concluded the following: (1) the southern and northern areas of the East China Sea region are spawning and nursery grounds, respectively, in spring; (2) the central distribution is located at a latitude of 28.00° N in autumn and winter; and (3) the southern area of the Yangtze River to the north is a spawning ground in spring, and the areas located at 29.00–34.50° N, 124.00–124.50° E, and 28.00–30.50° N, 125.50–126.50° E are nursery grounds. The results of this study provide useful guidance for appropriate fisheries management, thereby avoiding a collapse in the S. esculenta population, which has been experienced in other species in this area.


Introduction
Cephalopods, including squids, cuttlefish, and octopus, are important providers of marine ecological support services and commodities in commercial fisheries [1].They are the main prey items for many seabirds, larger fishes, and marine mammals [2].Their marine catch has been increasing globally at unprecedented rates in recent decades [3], although some of their stocks have been overexploited [4].In China, coastal cephalopods are a vital component of the local fisheries catch [5], with a noticeable and substantial increase in the total biomass in recent decades [6].Their production fluctuations are likely to be largely driven by environmental variations [7].Variations in oceanographic conditions associated with global warming variations could significantly influence the temporal-spatial distribution of cephalopods [8].In the seas around China, the golden cuttlefish (Sepia esculenta) has become the dominant cuttlefish fisheries target, replacing Sepiella maindroni since the 1990s [9].Yan et al. (2007) reported that the population of S. esculenta was highest in autumn and lowest in summer, and it was the dominant cephalopod species in the East China Sea from 2008 to 2009 [10].
Sepia esculenta, commonly known as 'moyu' in Chinese slang, belongs to the phylum Mollusca (Cephalopoda, Sepioidea, Sepiidae, Sepia), and is the most important commercial coastal cepholopod species in Japan, Korea, and China [10].The species inhabits warmtemperate shallow coastal sea at depths of ~10-100 m, e.g., the Russian far east region, the waters west and south of the Korean Peninsula, coastal sea areas of south Japan, the seas around China, and the Philippine islands in the Northwestern Pacific [11].Their traditional main fishing grounds include Hinoshino Beach and Seto Inland Sea of Japan, Lanshantou, Qingdao, the central and northern part of the Yellow Sea in China, and Jeju Island in Korea [12].The species has a short lifespan of one year or less and conducts batch spawning (egg maturation in batches) with a trophic level of 2.86 [13].The adult carcass length can be ~20 cm [14].They are a nektobenthic migratory species and are the main target of cage fishing and a bycatch target of trawling and fixed net fishing [11].The female groups prefer to lay individual egg capsules, each laying one egg capsule on the branches of macroalgae or the sea floor and producing 23-65 egg capsules during a single egg-laying period [15].Newly hatched juveniles are miniature adults that already have schooling and nektobenthic tendencies [16] and usually prefer to remain on the sea bottom [17].Their spawning sites and distribution are usually influenced by prey availability and macroalgae attachments during the migration [18].Li (1963) argued that grouping time has a close relationship with the population number along the Zhejiang coast [19].As a carnivorous species, they prey on a variety of fish and crustacean species, such as the fish Engraulis japonius, Setipinna taty, and Collichthys lucidus, and crustaceans of the Xanthidae, including Squilla oratoria, Trachypenaeus curvirostris, and Acetes, as well as other S. esculenta individuals [20][21][22].Dong et al. (1991) [12] and Zheng et al. (2003) [23] identified 50.0%crustaceans, 25.0% fish, and 25.0% S. esculenta in the diet of S. esculenta in the Yellow Sea.Natsukari and Tashiro (1991) concluded that the diet consisted of 45.7% fish, 39.5% crustaceans in Order Decapoda, 8.0% Stomatopoda and Cephalopoda, and 0.7% Mysidacea [24].Robinson et al. (2013) found that the population of S. esculenta tended to be distributed in cold areas and preferred a relatively low optimal water temperature in the Japan Sea and Korean waters [25].Warmer water might negatively affect the growth and development of the species [25].Negative correlations between catches and the increasing sea surface temperature (SST) were observed in autumn and winter [26].Belkin (2009) observed an increase of 1.22 • C in the SST in the East China Sea from1982 to 2006, which was potentially associated with global warming [27][28][29].The winter SST in the East China Sea has tended to increase since the late 1980s, which might significantly accelerate the somatic growth rate and cause advanced maturation at small sizes and younger ages [30][31][32].Pang et al. (2018) explored the impacts of environmental changes on Chinese coastal cephalopods in the seas around China and concluded that fluctuations in coastal productions were mainly driven by large-scale environmental variations associated with climate change and/or marine ecosystem regime shifts [26].The S. esculenta migrated to the overwintering ground in China's Yellow Sea, where the water temperature was gradually decreasing [26].Crozier and Hutchings et al. (2014) found that when there was a higher water temperature in the overwintering area, the overwintering period was shortened [33].This induced the early onset of spawning migration, resulting in a relatively poor reproductive condition, high marine mortality, and subsequently weak recruitment [33].It is, therefore, necessary to understand the resource status and spatio-temporal variation characteristics of S. esculenta in recent years.
The aim of this study was to determine the current resource status and spatio-seasonal variations in the S. esculenta population with a detailed investigation in the East China Sea region.We also compared our data with historical distribution records to obtain a clear picture of the movement of the resource center under the warming of the East China Sea region.We also attempted to identify the location of the spawning and nursery grounds, the most suitable range area, and the impact of environmental factors on the population.The results will enable the impacts of environmental variations on population fluctuations to be determined.They will also provide useful guidance for appropriate fisheries management, thereby avoiding a collapse in the S. esculenta population, which has been experienced in other species in this area.

Materials and Methods
We conducted four consecutive bottom trawling surveys with the survey vessels (#Zhongkeyu 211 and 212) in cruises during 2018-2019 in the East China Sea region, which covered the southern Yellow Sea and the East China Sea (autumn: 2-11 November 2018; winter: 4-27 January 2019; spring: 22 April to 10 May 2019; summer: 13 August to 27 September 2019) (Table 1).The trawling net had a mouth size of 102 mesh with a height of 10-15 m.The headline was 72.24 m long, and the bottom line was 82.44 m long.The net had a mesh size of 20.00 mm.Within the survey area (26 • 30 ′ -35 • 00 ′ N, 120 • 00 ′ -127 • 00 ′ E), survey stations were determined using a sampling grid with dimensions of 30 min of latitude and 30 min of longitude (30 ′ × 30 ′ ).The in situ survey in all seasons is performed by adopting a snake-like pattern along the route.In the southern area below 30 • 00 ′ N latitude, the survey was performed from north to south.In the northern area above 30 • 00 ′ N latitude, the survey was conducted from south to north.Following the surveys, fish, crustaceans, and other organisms, including S. esculenta, were identified to the lowest possible taxonomic level, counted, and weighed to the nearest 0.1 g of wet weight in the laboratory.The biomass index representing catch density per unit of time is measured using two components: biomass density (unit: g•h −1 ) and individual density (unit: ind•h −1 ).An SBE-19 conductivity-temperature-depth (CTD) instrument (SeaBird-Scientific, Bellevue, WA, USA) was used at each site to record hydrographic parameters, such as depth, water temperature, salinity, and the dissolved oxygen (DO) concentration.Among the parameters measured, SST, sea surface salinity (SSS), and sea surface dissolved oxygen (SSDO) were selected to define the mean temperature, salinity, and DO of the water layer within 3 m of the surface, and sea bottom temperature (SBT), sea bottom salinity (SBS), and sea bottom dissolved oxygen (SBDO) were selected to define the mean temperature, salinity, and DO of the water layer within 2 m of the bottom for depths < 50 m, or the water layer within 2−4 m of the bottom for depths > 50 m.
The formula for calculating catch per unit effort (CPUE) was as follows: where N i is the catch in number (ind) at i station; W i is the catch in weight (g) at i station; and t i is the trawling time (h) at i station.Additionally, we defined the average individual weight (AIW) as the ratio of the CPUE by weight (CPUE w ) against CPUE by number (CPUE n ) at a station.The suitability index (SI) was used to assess the habitat suitability of S. esculenta according to the functional relationships between environmental factors and resource abundance.The biomass data of this species varied across the different seasons due to the variations in the proportions of the population in the different stages of their life histories.There can be large differences in size among these individuals, and therefore, we used the number of individuals caught per unit to construct the SI.The relationships between environmental variables (depth, SST, SBT, SSS, SBS, SSDO, and SBDO) and SI were fitted using a smooth function with a range of 0.0-1.0.An SI value closer to 1.0 means a higher suitability index, and an SI value closer to 0.0 means a lower suitability index.SI values between 0.7 and 1.0 corresponded to environmental factors that were considered the most suitable environmental range.An SI value of 0.7-1.0 was most suitable, with relative suitability at values of 0.4-0.7 and instability at values of 0.0-0.4[34].
The SI was calculated as shown below: where Ŷ is the catch in number per unit area after a smoothed regression, and Ŷmax and Ŷmin are the maximum and minimum predicted values, respectively.
The HSI model was composed of the SI index for all the environmental variables.The model used a boosted regression tree (BRT) and the total variance contribution rate approach to calculate the weight of environmental factors.We calculated HSI values by an arithmetic mean model (AMM) using the equation below [35]: where HSI is the habitat suitability index, SI i is the SI value of the environmental variable I, ω i is the weight of the environmental variable i, and n is the number of environmental factors.

Seasonal Characteristics of the Distribution, CPUE w, and AIW
The whole survey area could be divided into two regions in spring: region I 32.50-34.50E, which was the northernmost survey station and was located adjacent to the Korean Peninsula, had a CPUE w of 250.62 g/h and AIW of 200.50 g/ind under conditions with an SBT of 9.60 • C and SBS of 32.76‰ in spring (Figure 1a,e).In region I, the regional average CPUE w and AIW were 1125.08 g/h and 500.24g/ind, respectively.In region II, the regional average CPUE w and AIW were 561.47 g/h and 262.14 g/ind, respectively, i.e., less than half that of region I.The average CPUE w (1931.90g/h) at the stations at 34.00

The Population Numbers and Areas Most Suitable for Fishing
Group sizes of 0-100 g/ind were most commonly observed (24 stations) in summer and were least frequent (2-4 stations) in the other three seasons.Group sizes of 100-200 g/ind were only observed at two stations in spring and winter and 12-15 stations in summer and autumn.The frequency of observed group sizes of 200-300 g/ind followed the order of autumn and spring (10-11 stations) > summer (6 stations) > winter (2 stations).Group sizes of 300-400 and 400-500 g/ind were observed at one and zero stations, respectively, in summer, and 4-6 and 1-2 stations, respectively, in the other three seasons.Group sizes of >500 g/ind were only found at four stations in spring (see Table 2).
The most suitable areas for fishing in spring were the south of the East China Sea region ( 26 2 and Figure 3).

The Population Numbers and Areas Most Suitable for Fishing
Group sizes of 0-100 g/ind were most commonly observed (24 stations) in summer and were least frequent (2-4 stations) in the other three seasons.Group sizes of 100-200 g/ind were only observed at two stations in spring and winter and 12-15 stations in summer and autumn.The frequency of observed group sizes of 200-300 g/ind followed the order of autumn and spring (10-11 stations) > summer (6 stations) > winter (2 stations).Group sizes of 300-400 and 400-500 g/ind were observed at one and zero stations, respectively, in summer, and 4-6 and 1-2 stations, respectively, in the other three seasons.Group sizes of >500 g/ind were only found at four stations in spring (see Table 2).
The most suitable areas for fishing in spring were the south of the East China Sea region ( 26 2 and Figure 3).The most suitable areas for fishing in autumn were the south of the Yellow Sea close to the Haizhou Bay fishing ground and the forbidden fishing line parts of the Lusi and Dasha fishing grounds (33.00-34.50°N 121.50−122.00°E) (Table 2 and Figure 3).The most suitable areas for fishing in winter were the south and center of the East China Sea  2 and Figure 3).

The Environmental Factors Supporting S. esculenta Populations
The depth range of the S. esculenta population was 10.00-133.00m from spring to autumn, but this shrank to 66.00-107.00m in winter (Table 3).The most suitable depth with an SI > 0.7 was 140.00 m in spring, 65.00-96.00m in summer, 14.00-21.00m in autumn, and 77.00-122.00m in winter (Figure 4).The range of SSTs (13.17-25.78• C in spring; 16.91-25.16• C in autumn) and SBTs (9.60-20.53• C in spring; 10.08-22.83• C in autumn) were similar in spring and autumn, respectively, and SSTs were 3.00-6.00• C higher than SBTs (Table 3).The range of SBTs was larger than that of SSTs in summer (SST 26.20-29.61• C; SBT 13.09-28.25• C), and the upper limits of SST and SBT were close in summer (29.61 • C vs. 28.25 • C) (Table 3).The lower limit of SBT in winter was higher than in spring and autumn (15.93 vs. 9.60-10.08• C), and the upper limit of SBT (19.76  4).The second most suitable SBT ranges for fishing (SI = 0.4−0.7)were 25.99-28.50• C in summer and 19.33-22.20 • C in autumn (Figure 4).The ranges of SSS and SBS were 31.00-35.00‰ in spring and autumn, which demonstrated the influence of dilution with water from the Changjiang River on bottom salinity.The SBS range was 32.95-34.68‰,revealing an influence from the East China Sea warm current in summer and winter (Table 3).The SSS range of 27.69-34.23‰in summer was clearly higher than in spring and autumn, and the upper limit of SSS (34.23‰) in summer was close to that of spring (34.52‰) and autumn (34.45‰).The overwintering group preferred a high SSS value of 33.68-34.39‰ in winter (Table 3).The most suitable SBS values were 31.53-34.80‰ in spring, 32.95-34.68‰ in summer, 31.51-34.77‰ in autumn, and 33.82-34.51‰ in winter (Figure 4).The SBT and SBS ranges were 18.87-28.19• C and 33.43-34.59‰ in summer when the CPUE n was 11.00-171.00ind/h (Figure 2), which represented a wide range of water temperatures and a narrow range of salinities.In the group where the CPUE n was 15.85-29.00ind/h, the SBS range was wider (31.73-34.63‰),and the SBT range was narrower (16.79-21.36• C) from summer to autumn (Figure 2).The surface and bottom DO values were lowest in summer, with higher values at the sea surface (4.77-6.43mg/L) than at the bottom (2.51-6.65 mg/L) (Table 3).The sea surface DO concentrations were similar in spring (7.94-8.56mg/L) and winter (7.40-8.00mg/L) (Table 3).
Table 3.The measured in situ value range of environmental factors in spring to winter: depth (m), sea surface temperature SST ( • C), sea bottom temperature SBT ( • C), sea surface salinity SSS (‰), sea bottom salinity (‰), sea surface dissolved oxygen SSDO (mg/L), and sea bottom dissolved oxygen SBDO (mg/L).The superscript of the values is the proportional deviation calculated by the HSI model, and the proportional deviation of depth, SST, SBT, SSS, and SBS sum up to 100.00%.A higher proportional deviation means a higher impact of environmental factors on the distribution of the species.

Spring Summer Autumn Winter
Depth 13.00-120.00Table 3.The measured in situ value range of environmental factors in spring to winter: depth (m), sea surface temperature SST (°C), sea bottom temperature SBT (°C), sea surface salinity SSS (‰), sea bottom salinity (‰), sea surface dissolved oxygen SSDO (mg/L), and sea bottom dissolved oxygen SBDO (mg/L).The superscript of the values is the proportional deviation calculated by the HSI model, and the proportional deviation of depth, SST, SBT, SSS, and SBS sum up to 100.00%.A higher proportional deviation means a higher impact of environmental factors on the distribution of the species.

Discussion
The life history characteristics of S. esculenta indicate a lifespan of approximately one year, as determined by Sun (1993) [36], who summarized the relationship between carcass length and day age.It has been reported that parent groups form groups for spawning in coastal areas from May to July, with the larvae born in June to August, and the juveniles grow and develop in the offshore area from July to October [37].Through observations made in indoor rearing experiments, Wei et al. (1964) also confirmed that the parents died in July [38].The duration of grouping and the time that grouping began for this species were different in the areas surveyed in the present study.For example, the grouping period in the south coastal areas of Zhejiang is April to May [39], but it is May to June in

Discussion
The life history characteristics of S. esculenta indicate a lifespan of approximately one year, as determined by Sun (1993) [36], who summarized the relationship between carcass length and day age.It has been reported that parent groups form groups for spawning in coastal areas from May to July, with the larvae born in June to August, and the juveniles grow and develop in the offshore area from July to October [37].Through observations made in indoor rearing experiments, Wei et al. (1964) also confirmed that the parents died in July [38].The duration of grouping and the time that grouping began for this species were different in the areas surveyed in the present study.For example, the grouping period in the south coastal areas of Zhejiang is April to May [39], but it is May to June in Zhoushan and the Shengsi Islands in northern Zhejiang [40].The grouping time is mid-April to the end of May in the offshore area of Rizhao; early May to mid-July in the coastal areas of Qingdao [19,23]; early March to mid-June in Tokyo Bay [41]; the end of March to early July in Mikawa Bay, Japan [42]; mid-April to the end of May and the end of May to early June, respectively, along the south and west coasts of Korea, respectively, [43]; early May to early June in the East China Sea; and June to July in the Yellow Sea, China [44].Generally, the grouping time is gradually delayed from south to north in the seas around China [45].Our surveys were conducted from April to May, which was the grouping time for parent groups; August to September, which had a large abundance of newly released juveniles; November, when larger juveniles were present; and January, during the growth and development of subadults (e.g., we found the weights to be 200-400 g/ind in most stations at this time) based on an analysis of individual weights (unit: g/ind) in the East China Sea region (Figure 1h).
The groups contained juveniles that exhibited different growth rates, resulting in different resource densities.For example, the individuals at 29.00 • N (164.53-210.17g/ind at 29.00 • N, 125.00-126.50• E) were larger than the individuals at 29.50 • N (68.14-118.10g/ind at 29.50 • N, 124.50-126.00• E) from August to September (Figure 1f).Based on the mixed distributions of individuals with weights ranging from 100-200 to 300-400 g/ind in summer, we concluded that there was a mixed distribution of juveniles and subadult groups.Wang et al. (2019) concluded that the differences in the duration of the larvae hatching stage can lead to differences in the growth of the species [18].Li et al. (1963) suggested that differences in the time of arrival for grouping in the coastal areas in each year might also cause differences in growth [19].Li (1963) confirmed that a mixed distribution of subadults and adults was found in the overwintering ground of the Yellow Sea [19].Our study found more juveniles at latitudes of 27.50-28.00• N and 29.00 • N and more subadult individuals at 28.50 • N in autumn.
The seasonal distribution characteristics could be explained by groups of S. esculenta making a planned migration from the coastal areas to the offshore areas.Li et al. (2010) observed clear seasonal variations in biomass and abundance in Jiaozhou Bay, with higher resource densities in summer and autumn than in the other two seasons [46].Niu et al. (2017) found that the areas with a higher resource density gradually moved from Linshan Bay to the offshore area southwest of the Linshan Islands due to the growth of juveniles, with a tendency for the area with a high CPUE w to move to the south and east of Linshan Bay [47].Our study found more juveniles in coastal shallow areas and larger individuals in offshore sea areas in spring.We found more larger individuals in the northern areas than in the southern areas of the East China Sea region.In spring, the individual weight of the species decreased from 253.00 to 89.20 g/ind at 28.50 • →26.50 • N, 123.00 • E, and the individual weight decreased from 541.00 to 109.85 g/ind at 34.00 • →27.00 • N, 122.00 • E (Figure 1e).We, therefore, concluded that the southern and northern areas of the East China Sea region were spawning and nursery grounds, respectively, in spring.
In terms of the seasonal variations in CPUE w , although the average CPUE w values were similar in spring and autumn, there were differences in the composition of the catches.In spring, the majority of the catches were composed of parent groups, while in autumn, the majority of the catches were composed of juvenile groups.For the areas of 32.50-35.00• N and 121.50-123.00• E in autumn, the CPUE w value decreased from the north to south: 1338.00-1631.17g/h at 34.00-35.00• N to 124.36-428.145g/h at 32.50-33.50• N (Figure 1c).Yan et al. (2007) concluded that the location of the central distribution of this species in the East China Sea region (in the period of [2000][2001] was the area of 124.00 • E to the east and both sides of 29.00 • N, 124.00-125.00• E in spring, autumn, and winter [10].However, our study suggested that the location of the central distribution was the latitude line of 28.00 • N in autumn and winter.For example, larger individuals (300-400 g/ind) were found on both sides of 28.00 • N in autumn (Figure 1c).The CPUE w in autumn was highest at 28.00 • N and decreased on both sides of the 28.00 • N line, including the areas of 30.50 • →28.00 • N and 28.00 • →27.00 • N (Figure 1c).We found individuals with a weight of < 100 g/ind at 31.00 • N, 125.00 • E in autumn (Figure 1c), indicating the possibility of juveniles migrating from the open sea to this location, as well as the presence of larvae in the open sea in the East China Sea region.We found 100-200 g/ind at 27.00-31.001c), indicating a mixed distribution of juveniles and subadults.The individual weight increased from 2.70 to 44.97 g/ind at 28.00 • N 125.00 • E→30.50 • N 125.50 • E in winter (Figure 1h).We found larger individuals in the area south of 30.00  1f).We concluded that the subadult groups might have dispersed widely for feeding and growth along the latitude of 30.00 • N and to the south in summer.
We concluded that the southern area of the Yangtze River extending north was the spawning ground in spring, including the area at 29.00-34.50• N, 124.00-124.50• E, because of the similar distributions of larvae and parent groups and the occurrence of a large number of larvae at 28.00-30.00• N, 123.00-126.00• E (Figure 1e).Additionally, we concluded that the area of 28.00-30.50• N, 125.50-126.50• E was the nursery ground due to the presence of larvae with a weight of 5.23 g/ind at 30.00 • N, 126.00 • E in summer (Figure 1f).The CPUE w values were 2873.01 and 6678.00 g/h at 30.50  1b,f).The individual weight was 22.40 g/ind at the neighboring station at 34.00 • N, 122.00 • E in autumn (Figure 1f).Juveniles with weights of 2.70 and 44.97 g/ind were found at 28.00 • N, 125.00 • E and 30.50 • N, 125.50 • E, respectively, indicating that these two stations were influenced by the warmer bottom water in winter (Figure 1g).According to Zhang et al. (2019), the offspring groups begin their overwinter migration to the central and southern areas of the Yellow Sea in November with the decreasing water temperature (~15.00 • C SST in the Qingdao area) [37].They overwinter with a mixed distribution in the central and southern parts of the Yellow Sea, north of Taiwan, and southwest of Tsushima Island in winter.They then migrate radially from the overwintering grounds to the spawning grounds in the near shore area after four months of growth.Zhang et al. (2019) and the present study found that their spawning grounds included the area north of the mouth of the Yalu River and the southern part of the Zhoushan coastal waters, but they did not extend beyond the southern boundary of the Zhoushan coastal waters [37].The spawning grounds became nursery grounds when the parent groups finished spawning.Zheng et al. (2003) concluded that their overwintering grounds included the southwestern part of Tsushima Island, central parts of the Yellow Sea (approximately 38.00-33.00• N, 122.50-123.83• E), and the area north of Taiwan [23].Individual weights of 5.23 and 33.4 g/ind were recorded at 30.00 • N, 126.00 • E and 30.00 • N, 124.50 • E, respectively, indicating the mixed distribution of larvae and juveniles in summer (Figure 1f).Individual weights of 96.30 to 75.67 g/ind and CPUE w values of 5200.20 to 1180.40 g/h were found in the area of 30.00 • N 124.00 • →127.00 • E in summer, indicating the presence of many larger individuals in the coastal areas (Figure 1f).An individual weight of 58.38 g/ind and CPUE w of 3794.70 g/h were observed at 29.00 • N, 123.50 • E in summer, highlighting the importance of coastal areas as nursery grounds (Figure 1b,f).Li (1963) found that the groups of S. esculenta exhibited a preference for water depths of ~70.00 m during the overwintering period, but in the coastal areas, they were present at depths of ~5.00-10.00m for long periods of time [19].We found that the deepest distribution of S. esculenta in winter was 66.00 m, and there was a large depth range in spring, summer, and autumn.Zhejiang Aquatic Products Bureau (1956) showed that the most suitable water temperature for fishing was in the range of 16.00-32.00• C in Hainan Island and Beibu Gulf of China, 10.00-24.00• C in Kyushu of Japan and the south bank of the Korean Peninsula, and 11.00-23.00• C in Jiaozhou Bay of China [39].Li (1963) argued that the hatching rate of eggs could exceed 70% when the water temperature exceeded 6.00 • C, and the incubation time was 20-21 d under conditions with a salinity of 30.00 ppt and water temperature of 22.00-24.00• C [19].There was a large difference in the surface and bottom water temperatures in summer and a surface salinity range of 27.69-34.23‰(Table 3), indicating substantial variability in the water conditions.In particular, some of the S. esculenta inhabited areas with low SSS, suggesting that their potential distribution areas might be influenced by water from the Changjiang River in summer.The range of SSTs was 16.11-20.12• C (Table 3).The water temperature ranges in surface and bottom water were similar (SST 16.11-20.12• C vs. SBT 15.93-19.76• C) in winter (Table 3).Furthermore, there was a difference of 4.00 • C between the upper limit of the SBT (19.76 • C) and the lower limit of the SST (15.93 • C).The lower limit range of water temperature values (both SST and SBT) during winter was 15.93 • C to 16.11 • C, indicating relatively consistent minimum temperatures in both surface and bottom waters (Table 3).Thus, we concluded that the overwintering ground might be influenced by the Kuroshio warm current, and the groups of S. esculenta preferred to stay in areas with a stable water temperature of ~20.00 • C.
The most suitable sea bottom salinity for fishing was similar in spring and autumn, but the difference in the CPUE w between these two seasons was large.The upper limit of sea surface salinity was similar (34.23-34.52‰)throughout the year (Table 3), indicating that some groups preferred to stay in areas with a high surface salinity.We found that the most suitable salinity for this species was 31.50-34.50‰(Figure 4).Tian et al. (2008) concluded that the fishery production of S. esculenta substantially decreased in the late 1980s in Korea due to the increase in winter SSTs in the Yellow Sea [48].Uda (1931) found that the population of S. esculenta preferred to remain in an 8-9 • narrow and long isothermal area that began from the 36.00• N latitude line and extended northwestward to the south bank of the Shandong Peninsula and extended southeastward to the south bank of the Korean Peninsula [49].Wang et al. (2019) suggested that larvae could actively avoid the negative influences of high water temperatures in the coastal waters in later periods, and recently hatched larvae might have a longer favorable growing period [18].
The role of the seasons for S. esculenta was identified as overwintering in winter to spring and spawning and nurseries in summer to autumn, with the spawning and nursery grounds located in the same sea area.This suggests that S. esculenta utilizes different seasonal periods for specific stages of its life history.Additionally, there was a large sea bottom area with a low DO content (minimum of 2.51 mg/L) in summer (Table 3), and many S. esculenta juveniles might have adapted to endure the negative influence of the low oxygen content.Water depth had an important impact on this species over the one year of its life history, and large groups of S. esculenta were found in the coastal area in autumn and in deeper offshore areas in winter.We proposed the following fisheries management strategies.(1) Species-specific management measures should be enforced to manage the populations of Chinese coastal cephalopods in overexploited and degraded ecosystems, with a particular focus on the monitoring of recruitment groups.(2) It is important to monitor the water temperature from May to August over the long term.(3) It is important to monitor the relationship between the populations of coastal cephalopods and other fish species.Long-term fishing pressure has reduced the population of many fish species, with cephalopods, including S. esculenta, using vacant ecological niches to increase their population [7].(4) It is important to delineate the management units and perform the necessary actions, including stock releases (usually in late July).The released groups will grow quickly in the coastal area and form a large recruitment population.The remaining groups will become a reproductive population after migrating over winter and will then supplement the natural population.

Conclusions
The main conclusions of this study were as follows: (1) The location of the central distribution of the groups of S. esculenta from 2018 to 2019 was the latitude line of 28.00 • N, which was more northerly than reported by Yan et al. (2007) [10].We propose that a gradient of rising water temperature could potentially force a northward shift in the location of its central distribution.In the future, in addition to monitoring water temperature, it will also be important to monitor environmental factors such as SSS, wind direction, seabed topography, and the presence of prey organisms.It is necessary to create a database and conduct population classifications, including gene communication and genetic exchange of different groups in geographical areas.The useful information obtained in this study will offer insights into how to fine-tune conservation and fishery management measures for this species and the wider resource in the future.
• N, 122.00 • E and 33.50 • N, 122.00 • E was 1176.40 g/h higher than the average value (735.02g/h) at the stations at 33.00 • N, 123.50 • E and 32.50 • N 123.50 • E (Figure 1a), but the average AIW (415.35 g/ind) was lower at the longitude of 122.00 • E at 33.50-34.00• N than the average value (735.02g/ind) at 123.50 • E in 32.50-33.00• N (Figure 1e).The AIW values were 4.87 and 519.00 g/ind in the stations at 30.50 • N, 124.00 • E and 30.50 • N, 124.50 • E, respectively, which was due to the group aggregation of larvae at an SBT of 16.81 • C and SBS of 33.00‰, and parent groups at an SBT of 13.67 • C and SBS of 33.41‰ (Figure 1e).The CPUE w and AIW ranged from 802.80-812.90g/h and 89.20-109.85g/ind over the spatial range of 26.50-27.00• N, 122.00-123.00• E, with an SBT of 18.60−20.53• C and SBS of 34.40-34.52‰.The CPUE w ranged from 201.94 to 2184.70 g/h, and AIW ranged from 188.85to 414.89 g/ind in the range of 28.00-30.00• N, 123.00-126.50• E with an SBT of 14.27-19.93• C and SBS of 33.61-34.77‰.The AIW value varied from 414.89 to 273.09 g/ind over the spatial range of 30.00 • N→29.00 • N, 124.50 • E (Figure 1e), and the CPUE w value was 2184.70 g/h at 29.00 • N, 124.50 • E with an SBT of 18.13 • C and SBS of 34.77‰ (Figure 1a).

Figure 3 .
Figure 3.The bottom horizontal distributions of the habitat suitability index (HSI) of the golden cuttlefish (Sepia esculenta) during the various surveys.The black dots indicate sampling stations.

Figure 3 .
Figure 3.The bottom horizontal distributions of the habitat suitability index (HSI) of the golden cuttlefish (Sepia esculenta) during the various surveys.The black dots indicate sampling stations.

Table 1 .
Details of the cruise number and season with survey time and total sampling stations.

Table 2 .
The value and value range of average catch per unit effort by weight (CPUE w ) at all stations (unit: g/h), average CPUE w at collection stations (unit: g/h), value range of CPUE w (unit: g/h), average CPUE n at all stations (unit: ind/h), average CPUE n at collection stations (unit: ind/h), the value range of CPUE n (unit: ind/h), average AIW (unit: g/ind), value range of AIW (unit: g/ind), most suitable distribution area, and the statistical details of station number classified by AIW (0-100, 100-200, 200-300, 300-400, 400-500, >500; unit: g/ind) in spring to winter.