Xin’an Wang, Aijun Ma, Zhifeng Liu, Zhibin Sun, Liguang Zhu, Haowen Chang. Genetic parameters estimation for growth traits in cultured tiger pufferfish (fugu), Takifugu rubripes[J]. Acta Oceanologica Sinica, 2022, 41(12): 73-79. doi: 10.1007/s13131-022-2058-5
Citation: Xin’an Wang, Aijun Ma, Zhifeng Liu, Zhibin Sun, Liguang Zhu, Haowen Chang. Genetic parameters estimation for growth traits in cultured tiger pufferfish (fugu), Takifugu rubripes[J]. Acta Oceanologica Sinica, 2022, 41(12): 73-79. doi: 10.1007/s13131-022-2058-5

Genetic parameters estimation for growth traits in cultured tiger pufferfish (fugu), Takifugu rubripes

doi: 10.1007/s13131-022-2058-5
Funds:  The National Key R&D Program of China under contract No. 2018YFD0900102; the Key Research and Development Plan of Nation under contract No. 2018YFD0900301; the AoShan Talents Cultivation Program Supported by Pilot National Laboratory for Marine Science and Technology (Qingdao) under contract No. 2017ASTCP-OS04; the Earmarked Fund for the Modern AgroIndustry Technology Research System under contract No. CARS-47-G01; the Central Public-interest Scientific Institution Basal Research Fund under contract No. 2020TD25.
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  • Corresponding author: E-mail: maaj@ysfri.ac.cn
  • Received Date: 2022-01-26
  • Accepted Date: 2022-06-24
  • Available Online: 2022-09-02
  • Publish Date: 2022-12-30
  • The aim of this study was to evaluate the genetic parameters of the growth performance of Takifugu rubripes. Heritabilities and genetic correlations were estimated for body weight (BW), body length (BL), total length (TL), chest measurement (CM) and trunk length (TKL) of T. rubripes from measurements of progeny at 6 months and 12 months. The results showed that the heritability was 0.37 for BW6, 0.19 for BL6, 0.35 for TL6, 0.29 for CM6, 0.26 for TKL6, 0.36 for BW12, 0.26 for BL12, 0.25 for TL12, 0.31 for CM12 and 0.15 for TKL12. The range of genetic correlations estimated at 6 months was 0.025–0.725 and −0.002–0.706 at 12 months. The results indicated that genetic improvement for faster growth rate or increased body weight in cultured T. rubripes was effective. Based on selection theory, the selection strategy for traits with medium heritability is flexible. Considering that these growth traits do not reach the high level of heritability, family selection should be expected. Given positive genetic correlations among BW, BL, TL, CM, and TKL at 6 months, the five traits could be improved simultaneously through selective breeding. As there was high genetic correlation only between BW12, BL12 and TL12, and negative correlations between TKL12 and BL12 as well as between CM12 and TL12, and only BW, BL and TL at 12 months could be improved simultaneously.
  • Takifugu rubripes is a demersal species mainly distributed in Japan, the Korean Peninsula and the coastal areas of China in the western part of the North Pacific Ocean. Takifugu rubripes has high commercial value because its meat has a good flavor and is tender (Cui et al., 2006; Lin et al., 2020). Research on the breeding and cultivation of T. rubripes in China began in the early 1980s. Along with the technological breakthrough in the artificial breeding of this fish, by the mid-1990s, T. rubripes was beginning to be cultured on a large scale, and gradually became one of the main breeding species in the coastal areas of northern China. With the rapid development of the T. rubripes breeding industry, some problems impacting the development of the industry have emerged, including the lack of effective parent fish management and a reasonable breeding scheme. Declines in hatching rate, survival rate, growth rate and stress resistance pose serious problems for the industry (Ma et al., 2016). In order to ensure the healthy, stable and sustainable development of the T. rubripes culture industry, it is important to find effective methods to systematically select and breed new varieties with high quality, high yield and stress resistance (Li et al., 2013).

    In order to carry out the genetic improvement of target traits, it is necessary to obtain accurate and reliable genetic parameters, which is the premise and foundation of breeding planning (Taylor et al., 2009; Fu et al., 2015; Sun et al., 2015; Liu et al., 2016; Ma et al., 2018; Wang and Ma, 2019; Wang et al., 2019). Heritability and genetic correlation are two of the most important genetic parameters in quantitative genetics (Ma et al., 2018; Wang et al., 2021). Heritability is a key quantitative index used to study the genetic essence of traits based on phenotypic variation. It plays an important role in the formulation of selection indices, prediction of selection response, comparison of selection methods and breeding planning decisions (Sun et al., 2015; Ma et al., 2018; Wang and Ma, 2019). Genetic correlation is another important basic genetic parameter, which can be used to describe the degree of correlation between different traits due to various genetic reasons. It plays an important role in determining the basis of indirect selection and predicting the response of indirect selection, comparing the selection effect under different environmental conditions, and formulating a comprehensive selection index (Sun et al., 2015; Ma et al., 2018; Wang and Ma, 2019).

    In the current study, we used 2 400 and 2 011 individuals from 48 full-sib groups to evaluate the genetic parameters of body weight (BW), body length (BL), total length (TL), chest measurement (CM) and trunk length (TKL) at the age of 6 and 12 months. The purpose of this study is to estimate the genetic parameters of growth traits of T. rubripes, and discuss their potential impacts on the breeding planning of T. rubripes, so as to provide the basic parameters for formulating and optimizing the breeding planning of T. rubripes.

    Takifugu rubripes used as broodstock were collected from three different cultured populations (China Dalian Tianzheng Industrial Company Limited cultured population, a population introduced from Japan in 2010 and a wild population caught in the Yellow Sea in 2009), and brought to China Yantai Tianyuan Aquatic Limited Corporation. The genetic background of the three populations can be found in the literature (Ma et al., 2016). In April 2012, individuals with mature gonads were selected from these three populations as parent fish. The selected parent fish reached sexual maturity at the same time after artificial cultivation and reproductive regulation. The broodstock of T. rubripes was induced by injection of luteinizing hormone releasing hormone A3 (LRH-A3) 250–300 g/kg + human chorionic gonadotrophin (hCG) 500 IU/kg (Ningbo hormone factory, Ningbo, China). The gonadal maturation of the broodstock was examined 24–48 h after induction. The abdomen of mature brood fish was obviously swollen. The female’s genital pore is filled with blood and slightly valgus, while milky semen flows out of the male fish when their abdomen is squeezed slightly. After gonadal maturation, the abdomen of female fish was squeezed to collect mature eggs in a dry white porcelain basin. The abdomen of the male was then squeezed to collect mature sperm. The sperm and eggs were then mixed. The sperm was activated by adding an appropriate amount of seawater, and the eggs were washed after standing for 5 min, until the fertilized eggs no longer adhered to the basin wall. The fertilized eggs were incubated in a 60 mesh sieve silk cone hatching net with a diameter of 80 cm. All the cone hatching nets were placed in a 40 m3 pond, with aeration and micro flow incubation. The incubation temperature was 18–19℃. Families were produced according to a nested mating design with two females nested within a male among 24 males and 48 females (8 males and 16 females in each population). First, eggs were obtained from two females and stored in two different beakers. Subsequently, the male fish were stripped and the milt was divided in two. Each portion was used to fertilize one of the two females. In total, 48 full-sib families (24 half-sib families) were obtained through artificial insemination.

    The larvae were fed with enriched rotifers on the 4th day after hatching (DAH), and enriched rotifers and Artemia nauplii on the 15th DAH. Larvae were fed a small amount of surimi on the 28th DAH, and only surimi was fed on the 45th DAH. On the 60th DAH the families were transferred to a sea cage for cultivation. In the early stages of family cultivation, individuals were too small to carry out tagging identification and polyculture, so each family had to be cultivated in a separate pond. So the families were inevitably affected by environmental factors. In order to reduce the differences in environmental effects among different families, environmental condition standardization and quantity standardization methods were used during breeding. In order to eliminate the effect of stocking density on each family at different stages of development, four levels of standardized treatment were carried out in combination with the ecological habits and culture modes of T. rubripes. According to the specifications of the breeding pool and sea net cage in the seedling workshop of the experimental site, quantity standardization was as follows: In the first level of quantity standardization, the larvae were cultured in a 5 m3 round cultivation tank. On the 15th DAH, 15 000 larvae were retained for further cultivation, and the surplus larvae were transferred to production for cultivation. For the second level of quantity standardization, on the 30th DAH, 8 000 juveniles with fast growth and good vitality were selected and cultured in a 36 m3 cement pond (6 m×6 m×l m). In the third level quantity standardization, on the 60th DAH, 5 000 juveniles with fast growth and good vitality were selected and placed in a 125 m3 cage (5 m×5 m×5 m) for intermediate cultivation. The fourth level of quantity standardization involved 2 000 juveniles with fast growth and good vitality being selected and placed in a 125 m3 cage (5 m×5 m×5 m) for intermediate cultivation on the 120th DAH. Intermediate cultivation lasted for 60 days. When the fish were 6 months old, 50 individuals from each family were randomly selected and individually tagged with passive integrated transponders (for distinguishing families and individuals). Individuals tagged with passive integrated transponders were transferred to a 400 m3 concrete tank (20 m×20 m×l m) for polyculture, for another 6 months. Any dead individuals were removed from the tank once a day. The breeding conditions of each family were consistently maintained from the hatching of fertilized eggs to larval rearing and tagging polyculture. According to different developmental stages, the families were placed in the same workshop for unified breeding management. During the larval-culture period, water temperature, salinity, illumination intensity, pH, ammonia nitrogen, nitrite-nitrogen, and dissolved oxygen were maintained at 15℃ to 22℃, 25 to 32, 500 lx to 1000 lx, 7.8 to 8.3, ≤1 mg/L, ≤0.4 mg/L, and 5 mg/L to 10 mg/L, respectively. During the juvenile- and adolescent-culture period, the above seven indices were 22℃ to 24℃, 15 to 32, 500 lx to 1000 lx, 7.8 to 8.3, ≤1 mg/L, ≤0.4 mg/L, and ≥6 mg/L, respectively (Li et al., 2013). During the larval- and adolescent-culture period, the bait is minced trash fish and pellet feed, and the feeding amount is 0.7%–1.5% of the total weight of the fish. It is fed once or twice a day. The nutritional components of pellet feed include protein, lipids, vitamins, minerals and carbohydrates.

    Five growth traits, BW, BL, TL, CM, and TKL (Fig. 1), were evaluated at two growth stages. BL, TL and TKL of each T. rubripes were directly measured using Vernier calipers. With the help of the thin line, CM was indirectly measured using Vernier calipers. BW was obtained by weighing using a digital balance. Measurements were taken at 6 and 12 months. A total of 50 individuals were randomly sampled and measured in all 48 full-sib families at 6 months, and all individuals retained in the 48 families (some individuals died or escaped) were measured at 12 months. Prior to measurements, all individuals were anaesthetized with 100 μL/L MS222 (tricaine methane sulfonate) (Maya Reagent, Jiaxing, China).

    Figure  1.  Morphometric measurements of Takifugu rubripes. BL: body length; CM: chest measurement; TKL: trunk length; TL: total length.

    The genetic parameters for BW, BL, TL, CM, and TKL were estimated using an animal model. The model can be written as

    $$ y_{ij}=\mu+a_i+f_j+e_{ij}, $$ (1)

    where μ is the mean value of population; yij is the observation of each trait (BW, BL, TL, CM, and TKL); ai is the random additive effect of individual i and is distributed ~N (0, A$ {\sigma }_{{\rm{a}}}^{2} $), where A is the numerator relationship matrix; fj is the full-sib family j as a random effect and eij is the random residual error of individual i. Heritability and genetic correlations were estimated using univariate animal model and bivariate animal model, respectively.

    The narrow sense heritability was calculated as the proportion of additive genetic variance to total variance as follows:

    $$ h^2= {\sigma }_{{\rm{a}}}^{2}/({\sigma }_{{\rm{a}}}^{2} +{\sigma }_{{\rm{f}}}^{2} + {\sigma }_{{\rm{e}}}^{2} ) , $$ (2)

    where ${\sigma }_{{\rm{a}}}^{2}$, ${\sigma }_{{\rm{f}}}^{2}$ and ${\sigma }_{{\rm{e}}}^{2}$ are additive variance components, the full-sib family variance component, and the residual variance component, respectively.

    The phenotypic correlation and genetic correlation between the five growth traits were calculated based on phenotype value and breeding value.

    Phenotypic correlation (rp) can be written:

    $$ r_{\rm{p}}= {\rm{cov}}(p_x, p_y)/\sqrt{{\sigma }_{{p}_{x}}^{2}{\cdot \sigma }_{{p}_{y}}^{2}} . $$ (3)

    Genetic correlation (rg) can be written:

    $$ r_{\rm{g}}= {\rm{cov}}( a_x, a_y)/\sqrt{{\sigma }_{{a}_{x}}^{2}{\cdot\sigma }_{{a}_{y}}^{2}} , $$ (4)

    where, px and py are the measurement results of x- and y- growth traits and cov(px, py) is covariance of px and py; ax, ay are additive genetic effects of x- and y- growth traits, and cov(ax, ay) is covariance of ax and ay.

    Heritability could be classified as low (0.05–0.15), medium (0.20–0.40), high (0.45–0.60) and very high (>0.65) levels. Correlations could be classified as low (0–0.40), medium (0.45–0.55) and high (0.60–1), independent of the sign (Cardellino and Rovira, 1987). When p<0.05 or p<0.01, the correlation reached significant or highly significant level.

    Variance components, heritabilities and genetic correlations for BW, BL, TL, CM, and TKL were estimated using derivative-free restricted maximum likelihood estimation as implemented in the MTDFREML package (Boldman et al., 1995). The phenotypic correlations among BW, BL, TL, CM, and TKL were estimated as Pearson’s correlations using the SPSS 13.0 software package (Norušis, 2005). The t test was used to test the significance level of each correlation coefficient from zero. Before analysis, all data were checked for outliers using box plots.

    Five growth traits at two growth stages were included in these analyses: 6-month body weight (BW6), 6-month body length (BL6), 6-month total length (TL6), 6-month chest measurement (CM6), 6-month trunk length (TKL6), 12-month body weight (BW12), 12-month body length (BL12), 12-month total length (TL12), 12-month chest measurement (CM12) and 12-month trunk length (TKL12). The growth trait distributions are shown in Table 1. The coefficient of variation (CV) of the four growth traits was generally high at over 10%, with up to 19.238% and 17.649% for BW6 and BW12, respectively. The genetic diversity of BW was the highest. CV decreased gradually with the growth of juveniles. On the whole, the growth tendency of the 48 full-sib families remained the same at the 6-month and the 12-month stages (Figs 26).

    Table  1.  Descriptive statistics for all the variables included in the analysis
    TraitNumber of
    Takifugu rubripes
    Mean trait
    value
    Standard
    deviation
    Coefficient of
    variation/%
    Minimum
    trait value
    Maximum
    trait value
    BW62 400167.474 g32.220 g19.23893.500 g216.700 g
    BL62 40016.069 cm1.144 cm8.98614.600 cm19.200 cm
    TL62 40019.925 cm1.176 cm5.90217.000 cm21.300 cm
    CM62 40014.481 cm1.408 cm9.72311.000 cm16.200 cm
    TKL62 4005.908 cm0.772 cm13.0675.000 cm7.000 cm
    BW122 011353.379 g62.369 g17.649176.000 g513.700 g
    BL122 01120.625 cm1.235 cm5.98717.900 cm24.300 cm
    TL122 01123.957 cm1.354 cm5.65119.600 cm27.000 cm
    CM122 01119.479 cm1.554 cm7.97718.000 cm22.600 cm
    TKL122 0117.002 cm0.783 cm11.1826.000 cm8.800 cm
    Note: BW, body weight; BL, body length; TL, total length; CM, chest measurement; TKL, trunk length.
     | Show Table
    DownLoad: CSV
    Figure  2.  Forty eight full-sib families’ growth tendency in terms of body weight (BW) in the 0−12-month stage.
    Figure  3.  Forty eight full-sib families’ growth tendency in terms of body length (BL) in the 0−12-month stage.
    Figure  4.  Forty eight full-sib families’ growth tendency in terms of total length (TL) in the 0−12-month stage.
    Figure  5.  Forty eight full-sib families’ growth tendency in terms of chest measurement (CM) in the 0−12-month stage.
    Figure  6.  Forty eight full-sib families’ growth tendency in terms of trunk length (TKL) in the 0−12-month stage.

    Estimates of the variance component and the heritability of five growth traits are presented in Table 2. It was found that heritability was 0.37 for BW6, 0.19 for BL6, 0.35 for TL6, 0.29 for CM6, 0.26 for TKL6, 0.36 for BW12, 0.26 for BL12, 0.25 for TL12, 0.31 for CM12 and 0.15 for TKL12. The heritabilities of the other traits were moderate, except for BL6 and TKL12.

    Table  2.  Variance components and heritability (h2) of five growth traits in Takifugu rubripes
    Growth traitsVariance components
    $ {{\sigma }}_{\mathrm{a}}^{2} $${\sigma }_{{\rm{f}}}^{2}$${\sigma }_{{\rm{e}}}^{2}$h2
    BW6265.967 9 g360.891 0 g95.155 0 g0.37±0.040
    BL60.102 2 cm0.265 6 cm0.172 8 cm0.19±0.023
    TL60.580 6 cm0.820 8 cm0.274 0 cm0.35±0.037
    CM60.288 1 cm0.487 0 cm0.216 9 cm0.29±0.032
    TKL60.092 0 cm0.170 5 cm0.092 1 cm0.26±0.026
    BW12345.567 4 g524.396 0 g96.666 0 g0.36±0.041
    BL120.413 9 cm0.824 89 cm0.341 9 cm0.26±0.031
    TL120.485 7 cm0.959 3 cm0.535 0 cm0.25±0.025
    CM120.519 0 cm0.869 2 cm0.311 0 cm0.31±0.034
    TKL120.093 1 cm0.305 8 cm0.242 8 cm0.15±0.020
    Note: BW6, 6-month body weight; BL6, 6-month body length; TL6, 6-month total length; CM6, 6-month chest measurement; TKL6, 6-month trunk length; BW12, 12-month body weight; BL12, 12-month body length; TL12, 12-month total length; CM12, 12-month chest measurement; TKL12, 12-month trunk length; ${\sigma }_{{\rm{a}}}^{2}$, additive genetic variance; ${\sigma }_{{\rm{f}}}^{2}$, full-sib variance; ${\sigma }_{{\rm{e}}}^{2}$, residual variance; h2, heritability.
     | Show Table
    DownLoad: CSV

    Phenotypic and genetic correlations for all growth traits of 6- and 12- month old T. rubripes are shown in Tables 3 and 4. The ranges of phenotypic and genetic correlations estimated for the traits at 6 months were 0.010–0.727 and 0.025–0.725, respectively. The phenotypic correlation between BW6 and BL6 (0.727), and the genetic correlation between BW6 and BL6 (0.725) were the strongest. The ranges of phenotypic and genetic correlations estimated for traits at 12 months were 0.001–0.697 and −0.002–0.706, respectively. The phenotypic correlation between BW12 and TKL12 (0.697) as well as the genetic correlation between BW12 and TKL12 (0.706) were the strongest.

    Table  3.  Phenotypic (rp) (above the diagonal) and genetic (under the diagonal) correlations (rg) of growth traits in 6-month-old Takifugu rubripes
    TraitBW6BL6TL6CM6TKL6
    BW60.727**0.727**0.580**0.155**
    BL60.725**0.454**0.461**0.010
    TL60.721**0.445**0.438**0.105**
    CM60.578**0.464**0.420**0.344**
    TKL60.146**0.0250.074**0.357**
    Note: BW6, 6-month body weight; BL6, 6-month body length; TL6, 6-month total length; CM6, 6-month chest measurement; TKL6, 6-month trunk length. ** Correlation is significant at the 0.01 level (2-tailed).
     | Show Table
    DownLoad: CSV
    Table  4.  Phenotypic (rp) (above the diagonal) and genetic (under the diagonal) correlations (rg) of growth traits in 12-month-old Takifugu rubripes
    TraitBW12BL12TL12CM12TKL12
    BW120.145**0.482**0.581**0.697**
    BL120.146**0.462**0.075**0.001
    TL120.495**0.466**0.0260.453**
    CM120.547**0.072**−0.0200.376**
    TKL120.706**−0.0020.453**0.373**
    Note: BW12, 12-month body weight; BL12, 12-month body length; TL12, 12-month total length; CM12, 12-month chest measurement; TKL12, 12-month trunk length. ** Correlation is significant at the 0.01 level (2-tailed).
     | Show Table
    DownLoad: CSV

    In recent years, the genetic improvement of the main economic traits of T. rubripes in China has led to the estimation of genetic parameters of breeding traits of T. rubripes being estimated using AI-REML (Liu et al., 2014, 2017) and ANOVA (Yu et al., 2016). The results showed that the heritability of 6-month old individuals was 0.54 for BW, 0.38 for BL, and 0.52 for TL. The heritability of 12-month old fish was 0.46 for BW, 0.37 for BL, and 0.44 for TL (Yu et al., 2016). There was a genetic correlation of 0.99 between BW and BL, 0.99 between BW and TL, and 0.98 between BL and TL at 6 months of age. In 12-month old fish, the genetic correlation was found to be 0.97 between BW and BL, 0.97 between BW and TL, and 0.96 between BL and TL (Yu et al., 2016). Heritabilities of BW and BL of T. rubripes have been estimated using AI-REML with three different animal models (in model 1 the additive genetic effect, the maternal genetic effect and the family effect were considered; in model 2 the additive genetic effect and the maternal genetic effect were included; and in model 3 the additive genetic effect and the family effect were analyzed). The results showed that the estimated heritabilities for BW and the BL at 200 days were 0.16 and 0.14, respectively (Liu et al., 2014). Heritabilities of BW and BL of T. rubripes have been estimated using a marker-based pedigree animal model. The results showed that the estimated heritabilities for BW and the BL at 150 days were 0.17 and 0.15, respectively, and 0.21 and 0.18 at 240 days (Liu et al., 2017).

    In present study, heritabilities of BW, BL, TL, CM, and TKL in 6- and 12-month old T. rubripes, as well as the genetic correlations among them were estimated using the derivative-free restricted maximum likelihood method applied to an animal model. The estimated heritabilities for growth traits of T. rubripes in the present study were lower than those reported by Yu et al. (2016), but higher than those reported by Liu et al. (2014, 2017). In addition, the estimated genetic correlation of growth traits was also lower than that estimated by Yu et al. (2016). In addition to the different analysis methods used, these differences were also attributed to the intraspecific differences, sample size, number of families and sample time. Heritability is one of the main bases to determine the selection method of traits. It is widely accepted that a trait with medium and high heritability (h2>0.2) is suitable for individual or group phenotypic selection, whereas a trait with low heritability (h2<0.2) is suitable for family selection or within-family selection (Sun et al., 2015). In the present study, the heritabilities of the other traits were moderate, except for BL6 and CM12. Therefore, the method of genetic improvement for these growth traits is flexible. In selective breeding, some traits can obtain satisfactory breeding results through direct selection, while it is difficult to obtain ideal breeding results for some traits through direct selection. Then, indirect selection will be used through the selection of traits with higher correlations with these traits (Sun et al., 2015). Heritable traits usually include morphological, behavioral, physiological and life-history traits. For most morphological/production traits, genetic correlations tend to be highly positive (Perry et al., 2005). In fact, in the field of aquatic animals, there are many reports of positive genetic correlation between economic traits of different species (Liu et al., 2011; Wang et al., 2011; Fu et al., 2015; Sun et al., 2015; Yu et al., 2016; Ma et al., 2018; Srimai et al., 2019; Wang and Ma, 2020). At 6 and 12 months, with the exception of two negative genetic correlations between TKL12 and BL12 as well as between CM12 and TL12, the phenotypic correlations and genetic correlations among the other traits were positive. The results of the current study are consistent with this conclusion.

    In conclusion, the results of this study indicate that genetic improvement is effective in improving the growth rate or weight gain of T. rubripes, as can be expected from moderate heritabilities. The selection strategy for the traits with medium heritability is flexible. However, these growth traits have not yet reached high heritability level. Based on this consideration, family selection should be an ideal method. At 6 and 12 months, with the exception of two negative genetic correlations between TKL12 and BL12 as well as between CM12 and TL12, the phenotypic correlations and genetic correlations among the other traits were positive. There were positive genetic correlations among BW, BL, TL, CM, and TKL at 6 months, which indicated that collecting data on one trait could promote the evaluation of other traits. Therefore, the five traits can be improved simultaneously by selective breeding. However, at 12 months, only BW12, BL12 and TL12 could be improved simultaneously because of the negative correlations between TKL12 and BL12 as well as between CM12 and TL12.

    Acknowledgements: We thank Ning Wang from Class 2018, Environmental Art Design, College of Art, Northeast Petroleum University for drawing Fig. 1. We are grateful to the staffs of Tianyuan Aquatic Limited Corporation in Yantai for their assistance and support in sampling.
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