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Stable isotope analysis has been widely used and proven to be a powerful and flexible tool to study food web structures and energy flows in aquatic ecosystems (Cabana & Rasmussen 1996, Post 2002, Boecklen et al. 2011). Stable carbon isotopes can be used to analyze the food sources of consumers because they enrich very tiny by approximately 0.1[per thousand]-0.4[per thousand] across functional groups along the food chain in an ecosystem (Simenstad & Wissmar 1985, Hanson et al. 2010). By contrast, stable nitrogen is usually used to estimate the trophic positions of species in the food chain because it enriches more from food to consumer (Pinnegar et al. 2002). With the application and development of isotope technology, stable nitrogen and carbon isotopes have been widely used in diverse studies, such as reconstruction of energy flow (Parnell et al. 2010), estimation of trophic niches (Jaeger et al. 2010), and quantification of marine ecological food webs (Davenport & Bax 2002), as well as migration tracing of animals (Hobson 1999).

Diverse nutrients and organic compounds from the base of ecosystem food webs can influence the isotope composition of organisms at different trophic levels (Hsieh et al. 2000) and spatiotemporal differences in stable isotopic patterns in individuals and communities (Cabana & Rasmussen 1996, Post 2002). Thus, a reference indicator (baseline) is necessary for the studies of trophic relationship between species and comparative studies of multiple ecosystems because isotopic baseline indicators are references for determining the trophic positions in food web studies (Cabana & Rasmussen 1996). Choosing a right baseline reference is the basis for quantitative assessment and accurate analysis of ecosystem structure and function. Researchers have found that sedentary primary consumers with long life spans and low tissue turnover rates can absorb these variations, and trace the trophic organism transfer at the base of food webs, offering a reasonable reference from that can be used to allocate primary sources and determine trophic positions of supporting consumers (Post 2002, Boecklen et al. 2011). As sedentary suspension feeders, bivalves can indicate the spatial differentiation of their food sources better than other consumers and are widely used as isotopic baseline indicators in aquatic ecosystems (Jorgensen 1996, Raikow & Hamilton 2001, Howard et al. 2005, Xu et al. 2011, Gong et al. 2017).

The Asian moon scallop (Amusium pleuronectes) is a common bivalve that inhabits the coastal areas of the South China Sea (Fu et al. 2012, Guo et al. 2012, Yang et al. 2013, Wang et al. 2016). The scallop muscle tissue has been used as a baseline indicator to calculate the trophic level of fish (Yan et al. 2013), and the shell used to trace metal elements in the marine environment (Siriprom & Limsuwan 2009). Aspects of resource distribution (Fu et al. 2012), growth, recruitment, mortality and reproduction (Norte 1988), artificial cultivation and feeding (Belda & Norte 1988, Wang et al. 2009), mitochondrial DNA diversity (Mahidol et al. 2007), and nutritional components (Zhu et al. 2011) of A. pleuronectes have been studied in the past; however, no research reports on the feeding habits and stable isotopes of A. pleuronectes in the Beibu Gulf have been published. In the current study, with the specimens of A. pleuronectes collected from the Beibu Gulf, South China Sea, at a seasonal interval, feeding habit and characteristics of carbon and nitrogen isotopes were studied. Furthermore, a baseline isotopic signature is provided to determine the trophic levels of consumers in the South China Sea.


Sample Collection

The study was carried out seasonally by the "Beiyu 60011" bottom-trawl vessel in the Beibu Gulf in October 2014 (autumn), January 2015 (winter), April 2015 (spring), and July 2015 (summer). Sampling was conducted during the daytime using a trawl net with a cod end, with a 40-mm stretched mesh size at a speed of about 3.0 knot for 2 h at each site. A total of 160 specimens (Table 1) were collected from 9 of the 17 sampling sites (18[degrees] 30'-22[degrees] 00' N, 106[degrees] 30'-110[degrees] 00' E, Fig. 1) and immediately placed on ice and subsequently frozen to deliver to the laboratory for later experiments. The depth of sampling water ranges from 10 to 70 m.

Laboratory Experiment

Biological experiments were performed in the laboratory. Specimens were measured for shell length (SL) to the nearest 0.01 mm with a Vernier caliper and weighed for total weight with a digital balance to an accuracy of 0.01 g.

The internal tissues were washed with distilled water to be sure no other confusing items were present after removal of the dorsal shell. Then, stomachs were removed and conserved in the concentration of 10% formalin for later analysis. Adductor muscles were cut from Amusium pleuronectes for stable isotope analysis.

Stomach Content Analyses

To analyze the stomach contents, stomachs were removed from formalin and put on the filter paper to absorb the formalin thoroughly. The stomach contents were transferred to a petri dish containing 2 mL distilled water completely with tweezers after the stomach was cut with scissors and stirred them to mix well with distilled water. Then, 0.1-mL solution containing the food items was removed to a plankton-counting chamber (10 X 10) and dyed with Lugol's iodine. Identification and frequency calculation of the stomach contents were performed under a binocular microscope (Leica DME, German). Food items were identified at the genus level based on the morphological characteristics of objects and the relevant literature (Lotsy 1896, Allen 1914, Jin 1965, Shumway et al. 1987, Guo 2004).

Stable Isotope Analysis

Three samples were selected randomly from each group and 88 samples were taken for isotope analysis based on the SL group, season, and sampling site. All the specimen will be selected when the number of sample in some groups is smaller than three (the number of sample in some groups is smaller than three). After the adductor muscles had been cleaned with distilled water, they would be placed in a freezer dryer (Lyophilization machines ALPHA1-2LD plus) for dehydration treatment at a temperature of -48[degrees]C for 48 h. Then, the dried muscles were ground into fine powder for stable isotope measurements using a mortar and pestle.

Stable carbon and nitrogen isotopes were measured with an elemental analyzer (Carlo Erba NC 2500) and a continuousflow isotope ratio mass spectrometer (Finnegan Mat Delta Plus CF-IRMS). The stable carbon ([delta][.sup.13]C) and nitrogen ([delta][.sup.15]N) isotope values of the specimens were expressed as parts per thousand ([per thousand]) deviation from the standard isotope ratio using the following equation (Xu et al. 2011):

[delta]X([per thousand]) = [([R.sub.sample]/[R.sub.standard]) - 1] x 1000

where x is [.sup.13]C or [.sup.15]N, and R is [delta][.sup.13]C or [delta][.sup.15]N. Vienna Pee Dee Belemnite limestone carbonate and atmospheric [N.sub.2] were used as standards for [delta][.sup.13]C and [delta][.sup.15]N, respectively. More than 15% of the samples were analyzed more than three times to make sure the accuracy of the results. The SD for the replicate analyses was smaller than 0.3% for both [delta][.sup.13]C and [delta][.sup.15]N.

Data Analysis

One-way analyses of variance (ANOVA) were used to test the differences in the [delta][.sup.13]C and [delta][.sup.15]N values in different SL groups, seasons, sites, and depths.


Stomach Content Analysis

Stomach contents of Amusium pleuronectes were identified using binocular microscopy in the laboratory. All food items comprised eight phyla, 47 genera, and other unknown meromelia, including 31 genera of Bacillariophyta, four genera of Pyrrophyta, three genera of Cyanophyta, four genera of Chlorophyta, and two genera each of Euglenophyta, Chrysophyta, Arthropoda, and Protozoa (Table 2).

The dominant genera were Diploneis, Cyclotella, Navicula, Leptocylindrus, Pinnularia, Pleurosigma, Chlorella, and Coscinodiscus. Seasonal food composition was identified in the food items, with two phyla and 13 genera in spring, four phyla and 25 genera in summer, five phyla and 35 genera in autumn, six phyla and 29 genera in winter.

Stable Isotope Changes with Shell Length

One-way ANOVA was used to evaluate the [delta][.sup.15]N and [delta][.sup.13]C values among the different shell-length groups. The [delta][.sup.15]N values did not show significant differences, whereas significant changes in the [delta][.sup.13]C values were seen among shell-length groups (df = 4, F = 4, P < 0.01). The variations of [delta][.sup.13]C and [delta][.sup.15]C values displayed the same tendencies with the increasing of SL, and the [delta][.sup.13]C values maintained an approximately consistent increase, whereas the [delta][.sup.15]N values showed a rapid increase after a small decrease (Fig. 2).

Temporal Variability of [delta][.sup.13]C and [delta][.sup.15]N

The [delta][.sup.13]C and [delta][.sup.15]N values of adductor muscles ranged from -21.45[per thousand] to -17.56[per thousand] (average -19.54[per thousand]) and 6.41[per thousand]-12.80[per thousand] (average 8.89[per thousand]) from spring to winter, respectively (Table 3). The seasonal fluctuations of the [delta][.sup.13]C and [delta][.sup.15]C values of adductor muscles are shown in Figure 3. Adductor tissue of Amusium pleuronectes from the Beibu Gulf displayed significant seasonal variability in [delta][.sup.13]C (ANOVA, df = 3, F= 36, P<0.01) and [delta][.sup.15]C (ANOVA, df = 3, F = 10, P < 0.01) isotopic composition. The [delta][.sup.15]C and [delta][.sup.15]N values presented similar seasonal downtrend from spring to winter.

Spatial Distribution

Significant differences in [delta][.sup.15]C (ANOVA, df = 9, F = 9, P < 0.01) and [delta][.sup.15]C (ANOVA, df = 9, F = 10, P < 0.01) values were found among sites. It is obvious that the [delta][.sup.15]C or [delta][.sup.15]C values at the sites close to the shore were higher than those far from the shore (Fig. 4).

Specimens were collected from a depth range of 10-70 m. The [delta][.sup.13]C and [delta][.sup.15]C values showed significant differences (ANOVA, df = 5, F = 24, P < 0.01; df = 5, F = 10,P< 0.01) between depth groups. The average [delta][.sup.13]C and [delta][.sup.15]N values declined with depth from 10 to 70 m (Table 4).


Feeding Habit

The feeding habit of bivalves has been extensively studied for the past century. A point of disagreement that the main food source for suspension-feeding bivalves was reported in the literature. Some researchers claimed that detritus were the main food source base on gut content analyses of multiple bivalve species (Petersen 1908, Petersen & Jensen 1911, Blegvad 1914), and Allen (1914) even found a little higher proportion of animal food in the freshwater mussels, whereas subsequent and more researchers found that bivalve molluscs feed mainly on phytoplankton and detrital particles, particularly diatoms (Lotsy 1896, Field 1911, Martin 1925, Galtsoff 1964, Rosa et al. 2018). As in most prior studies on food items for the bivalve species, Amusium pleuronectes feeded on diatom groups as the primary food items, while ingesting a small amount of animal food and detrital particles in this study. Diatom groups were also observed to dominate in the food content of Amusiumjaponicum in the Beibu Gulf (Ye & Liang 1990). This may be related to the feeding selectivity of bivalves or to the availability of particular species seasonally as most scallops are opportunistic feeders that prey on available seston and their feeding contents can be influenced by the particle species composition and distribution in particular water (Shumway et al. 1985, Ward & Shumway 2004, Rosa et al. 2018). Gao et al. (2001) identified 382 species of phytoplankton, belonging to Bacillariophyta (contributed 67%), Pyrrophyta, Cyanophyta, and Chrysophyta, in the Beibu Gulf and found that the lowest and highest diversity indices displayed in spring and autumn, respectively; that is, species consumed are reflected in the species available. And the result that the diatom groups played a dominant role in the food composition of A. pleuronectes in each season in this study seems to be consistent with this. Moreover, particle capture is an important step in the feeding process of bivalve molluscs, and the capture efficiency has been attributed solely to particle size. Shumway et al. (1985) demonstrated that European oyster (Ostrea edulis) preferentially captured the dinoflagellate over a similarly sized diatom and flagellate. The current study seems to show the similar results with the diatoms and dinoflagellate preferentially captured by A. pleuronectes.

Variations of Stable Isotopes

Previous researches had reported that the stable carbon and nitrogen values of mussels exhibit substantial changes at different sites, indicating the spatial heterogeneity of baseline stable carbon and nitrogen values in coastal waters (Hsieh et al. 2000, Mckinney et al. 2001). In the current study, variations were found in the stable carbon and nitrogen values among sites. The [delta][.sup.15]C and [delta][.sup.15]C values at sites 1, 3, 5, 6, and 7 (the northern Beibu Gulf) were higher than those at the other stations. These variations may be related to the trophic difference in the gulf and the human activities around. First, as an important spawning ground and feeding ground for many economically valuable fishes (Zuo-zhi & Yong-song 2005, Wang et al. 2010), the northern Beibu Gulf (sites 1, 3, 5, 6, and 7) has higher productivity than the southern Beibu Gulf. And the phytoplankton in the north of the gulf were reported to be richer too (Gao et al. 2001). This is why the [delta][.sup.13]C values were higher here because the stable carbon isotope of organisms in a marine trophic system could be influenced by the phytoplankton growth rate (Laws et al. 1995), the occurrence of phytoplankton blooms (Gervais & Riebesell 2001, Nakatsuka et al. 1992), primary productivity (Laws et al. 1995, Schell 2000), and CO2 concentration (Burkhardt et al. 1999, Tortell et al. 2000). Second, organisms from fish farms are enriched in [delta][.sup.15]N compared with those from unaffected offshore reference waters (Dolenec et al. 2007). Mckinney et al. (2001) reported a large variation in the [delta][.sup.15]N values of ribbed mussels in coastal salt marshes and noted that the [delta][.sup.15]N values of the mussels were influenced by nitrogen derived from human activities in the adjoining marsh watershed. Fukumori et al. (2008) even found that the relatively higher [delta][.sup.15]N values of oysters at some stations may be partly due to the effects of fish farming. Therefore, the higher [delta][.sup.13]C and [delta][.sup.15]N values in sites 1, 3, 5, 6, and 7 may be not only due to higher productivity but also due to to the human activities as these sites were near the coastal fish farms of Weizhou Island and can receive more carbon and nitrogen supplements.

A Baseline Indicator Recommendation

Stable isotope analysis has been widely used to provide longterm information on feeding relationships and energy flow in an aquatic ecosystem (Kling et al. 1992, Peterson & Fry 1987, Xu et al. 2013). An isotopic baseline signature is essential for calculating the diets or trophic positions of marine organisms and comparing the food web structure among and within ecosystems using stable isotopic data (Jun et al. 2010, Xu et al. 2011). An accurate analysis of stable isotopic studies relies on an appropriate baseline (Fukumori et al. 2008). Although the particulate organic matter and the initial consumers of zooplankton and benthos are usually selected as isotopic baseline indicators to study the feeding ecology of aquatic ecosystems (Zanden et al. 2003), bivalve molluscs are the most common baseline organisms, especially in freshwater and marine ecosystems (Mckinney et al. 1999, Fukumori et al. 2008).

The isotopic baseline organisms used in previous studies are diverse. There is still not a universal standard baseline in marine ecosystem research. One of the aims of this study was to investigate the possible use of the carbon and nitrogen isotopic values of Amusium pleuronectes as a baseline indicator for the Beibu Gulf or even for the whole South China Sea. Results of the present study provide several reasons to support this prospect. First, the mean stable nitrogen isotope value of A. pleuronectes (8.82[per thousand]) in the Beibu Gulf was lower than that of fish (14.38[per thousand]), cephalopods (13.23[per thousand]), crabs (12.48[per thousand]), and shrimp (12.28[per thousand]) in Liusha Bay (Yang et al. 2015), and fish, cephalopods, and shrimp (8.92[per thousand]-17.63[per thousand]) in the whole Beibu Gulf (Yan 2014). Second, studies have confirmed that suspension-feeding bivalve molluscs are suitable baselines to determine the isotopic values when studying marine systems (Cabana & Rasmussen 1996, Mckinney et al. 2001, Fukumori et al. 2008) because of their stable feeding habits, longevity, and ease of sampling. That A. pleuronectes mainly feeds on plankton and organic detritus has been reported by Guo et al. (2012) and confirmed again in the current study. Norte (1988) also found that the life span of A. pleuronectes was approximately 2 y. Third, Mackey (2015) suggested that "bivalves with high abundances and wide distributions can be used to compare baselines [delta][.sup.15]N over large spatial scales and offer a reliable indicator of baseline [delta][.sup.15]N in the coastal waters." The Asian moon scallop just meets this condition as it is a common bivalve that widely inhabits the coastal waters of the north South China Sea (Yang et al. 2013) and Beibu Gulf (Fu et al. 2012, Wang et al. 2016).

In conclusion, this study indicated that Amusium pleuronectes is a good indicator of isotopic baselines in the marine ecosystems of the Beibu Gulf. It is recommended that the [delta][.sup.15]N values of A. pleuronectes can be used as isotopic baselines throughout the year in the Beibu Gulf. Although the [delta][.sup.15]N values of A. pleuronectes in the Beibu Gulf showed significant differences among seasons and sites, the spatial and temporal heterogeneity of the baseline organisms can be decreased by increasing the sampling density.


We thank Xin Su, Rongjie Zhang, Jinlong Li, and Weisheng Liao for their help with sampling work and the reviewers for their helpful advices. This research was funded by the National Key R&D Program of China (2018YFD0900905), Science and Technology Plan Projects of Guangdong Province, China (2018B030320006), and the National Natural Science Foundation of China (41376158, 41476149).


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(1) Fisheries College, Guangdong Ocean University, No. 1, Haida Road, Mazhang Block, Zhanjiang, Guangdong 524088, China; (2) Fisheries College, Jimei University, No. 43, Yindou Road, Jimei Block, Xiamen, Fujian 361021, China; (3) Center of Marine Fisheries Information and Technology, Shenzhen Institute of Guangdong Ocean University, No. 3, BinHai 2nd Road, Dapeng New District, Shenzhen 518120, China; (4) Fisheries College, Ocean University of China, No. 5, Yushan Road, Qingdao 266003, China

*Corresponding authors. E-mails: tunajs@, or

DOI: 10.2983/035.038.0204
Sample information of Amusium pleuronectes in different times.

Time       N      Range        [+ or -] SE          Range

Spring      9  69.32-86.87  79.20 [+ or -] 1.76  10.35-43.40
Summer     16  76.66-93.01  85.07 [+ or -] 1.45  26.33-59.14
Autumn    104  50.59-86.78  63.41 [+ or -] 0.61   6.91-45.54
Winter     31  57.60-86.09  73.92 [+ or -] 0.99  15.39-42.46
All year  160  50.59-93.01  68.44 [+ or -] 0.75   6.91-59.14

Time          [+ or -] SE

Spring    26.83 [+ or -] 3.19
Summer    41.89 [+ or -] 2.86
Autumn    15.56 [+ or -] 0.61
Winter    29.50 [+ or -] 1.18
All year  21.45 [+ or -] 0.89

N, number of specimens.

Occurrence frequency of Amusium pleuronectes food items in the Beibu

    Phylum           Genus          Spring  Summer  Autumn  Winter

Bacillariophyta  Coscinodiscus       6.00    6.50   3.47    7.69
                 Cyclotella          -      12.65   3.29    3.90
                 Thalassionema       2.00    3.20   3.10    1.50
                 Leptocylindrus      2.00    9.25   2.56    2.86
                 Pleurosigma        12.43   15.20   2.46    4.31
                 Diploneis          13.86   18.81   2.37    3.39
                 Podocystis          -       -      2.00    -
                 Synedra             2.00   11.25   1.97    3.50
                 Actinocyclus        1.75    8.00   1.96    3.00
                 Navicula            1.00    7.00   1.78    2.70
                 Chaetoceros         -       -      1.67    -
                 Surirella           2.60    7.86   1.58    3.07
                 Cocconeis           -       3.00   1.53    3.72
                 Thalassiosira       -       -      1.38    -
                 Nitzschia           1.00    4.50   1.36    3.44
                 Pinnularia         14.14    6.25   1.22    2.10
                 Actinoptychus       1.00    3.67   1.10    4.00
                 Gyrosigma           -       7.75   1.00    2.42
                 Planktoniella       -       1.00   1.00    -
                 Triceratium         -       -      1.00    1.50
                 Trachyneis          -       -      1.00    0.50
                 Skeletonema         -       -      1.00    -
                 Asterionella        -       -      1.00    -
                 Thalassiothrix      -       -      0.50    3.75
                 Bacteriastrum       -       -      0.50    -
                 Hyalodiscus         -       -      0.50    -
                 Synedra             -       2.50   -       -
                 Melosira            -       0.50   -       2.00
                 Grammatophora       -       -      -       0.50
                 Hemidiscus          -       -      -       0.50
                 Biddulphia          -       -      -       0.50
Pyrrophyta       Gonyaulax           -       1.50    1.53   -
                 Lingulodinium       -       -       1.23   -
                 Prorocentrum        -       -       1.00   -
                 Ornithocercus       -       -              1.50
Cyanophyta       Oscillatoria        -       -      7.00
                 Anabeana            -       0.75   1.00    0.50
                 Nostoc              -       1.00   0.50
Chlorophyta      Pandorina           -       3.50   1.67    3.75
                 Chlorella          16.00    5.79   1.40    1.83
                 Planktosphaeria     -       2.50   -       2.20
                 Closterium          -       1.75   -       -
Euglenophyta     Trachelomonas       -       -      1.00    -
                 Phacus              -       -      -       1.50
Chrysophyta      Dictyocha           -       -      -       0.50
Protozoa         Arcella discoides   -       -      1.33    -
Arthropoda       Copepoda            -       -      1.17    1.00
Unknown          Unknown 1           -       -      1.38
                 Unknown 2           -       1.00   -       -
                 Unknown 3           -       1.00   -       -

Stable carbon and nitrogen isotope of Amusium pleuronectes at different

                  [delta][.sup.13]C([per thousand])
Time      N        Range        Average [+ or -] SE

Spring     9  -19.27 to -17.58  -18.25 [+ or -] 0.16
Summer    16  -20.22 to -17.79  -18.43 [+ or -] 0.14
Autumn    32  -21.45 to -17.56  -20.06 [+ or -] 0.15
Winter    31  -20.91 to -18.84  -19.94 [+ or -] 0.09
All year  88  -21.45 to -17.56  -19.54 [+ or -] 0.11

            [delta][.sup.13]C([per thousand])
Time        Range     Average [+ or -] SE

Spring    8.82-10.11  9.53 [+ or -] 0.13
Summer    8.72-11.27  9.80 [+ or -] 0.16
Autumn    7.24-11.14  8.79 [+ or -] 0.17
Winter    6.41-12.80  8.34 [+ or -] 0.21
All year  6.41-12.80  8.89 [+ or -] 0.12

N, number of specimens.

Stable carhop and nitrogen isotope of Amusium pleuronectes at different

                  [delta][.sup.13]C([per thousand])
Depth (m)  N         Range       Average [+ or -] SE

20.1-30.0   4  -19.69 to -17.56  -18.18 [+ or -] 0.51
30.1-40.0   7  -20.31 to -18.90  -19.48 [+ or -] 0.25
40.1-50.0  31  -20.91 to -17.58  -18.91 [+ or -] 0.15
50.1-60.0  36  -21.45 to -18.99  -20.15 [+ or -] 0.07
60.1-70.0  10  -20.72 to -20.01  -20.43 [+ or -] 0.07

            [delta][.sup.13]C([per thousand])
Depth (m)    Range     Average [+ or -] SE

20.1-30.0  8.54-11.14  10.36 [+ or -] 0.61
30.1-40.0  7.69-9.37    8.75 [+ or -] 0.26
40.1-50.0  7.47-11.27   9.22 [+ or -] 0.14
50.1-60.0  6.41-12.80   8.39 [+ or -] 0.15
60.1-70.0  6.42-7.43    6.68 [+ or -] 0.12

N, number of specimens.
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Article Details
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Author:He, Xiongbo; Zhu, Dewen; Zhao, Chunxu; Yan, Yunrong; Kang, Bin
Publication:Journal of Shellfish Research
Geographic Code:9CHIN
Date:Aug 1, 2019

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