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Article

Feeding Selectivity of Ruditapes philippinarum on Phytoplankton

by
Yin Liu
1,†,
Lun Song
2,*,†,
Guangjun Song
2,
Jinhao Wu
2,
Kun Wang
2,
Zhaohui Wang
2 and
Suxuan Liu
3
1
College of Fisheries and Life Science, Dalian Ocean University, Dalian 116023, China
2
Key Laboratory of Marine Biological Resources and Ecology, Liaoning Ocean and Fisheries Science Research Institute, Dalian 116023, China
3
College of Marine Sciences and Technology and Environment, Dalian Ocean University, Dalian 116023, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Fishes 2022, 7(5), 222; https://doi.org/10.3390/fishes7050222
Submission received: 25 July 2022 / Revised: 10 August 2022 / Accepted: 24 August 2022 / Published: 26 August 2022
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Abstract

:
A monthly survey of the feeding selectivity of Ruditapes philippinarum in the Yalu River Estuary in 2020–2021 was conducted using high-throughput sequencing identification and visual grading technology. The results showed that the most-dominant species in the water of the shellfish culture area and in the stomachs of R. philippinarum was Karlodinium veneficum in those years. The selectivity index (E) indicated that R. philippinarum avoided consuming Bacillariophyta, Chrysophyta and Cryptophyta throughout the year and preferentially consumed Dinophyta and Chlorophyta. In 2020, the annual average biomass of Dinophyta, Bacillariophyta, Chlorophyta, Dictyochophyta, Cryptophyta and Chrysophyta in the stomach contents of R. philippinarum was 54:14:16:1:10:4; it was 41:12:28:0:1:17 in 2021. The annual average biomass ratio of picophytoplankton, nanophytoplankton and microphytoplankton in the stomachs of R. philippinarum was 13:48:39 in 2020; it was 14:66:20 in 2021. R. philippinarum actively fed on nanophytoplankton and avoided picophytoplankton. Among the phytoplankton of different sizes and groups that R. philippinarum prefer to feed, chemical oxygen demand (COD) and organic phosphorus (DOP) have a significant negative effect on the nanophytoplankton community, pH has a positive effect on the Dictyochophyta community and COD and the inorganic nitrogen to phosphorus ratio (DI-N/P) have a significant positive effect on the Chlorophyta community.

1. Introduction

Aquaculture, which is one of the fastest-growing food-producing sectors in the world, will play a critical role in narrowing the gap between rising consumer demand for seafood and declines in the supply of wild-caught seafood products. Many countries have thus made the development of aquaculture a national priority. Filter-feeding shellfish have become increasingly common in China’s coastal waters because of the continual increase in the scale of filter-feeding shellfish culture. Unlike farmed fish that can be fed diverse feeds, the main food source for filter-feeding shellfish culture is natural phytoplankton [1,2]; however, filter-feeding shellfish are selective feeders [3,4]. Large phytoplankton tend to be selectively ingested via the ctenoid gills of filter-feeding shellfish; after entering the intestinal tract, phytoplankton are assimilated selectively through the cilia. Unassimilated phytoplankton are embedded in the mucus and excreted as feces. Both of these selection mechanisms are affected by various properties of phytoplankton, including their size, shape, mobility, viscosity, toxicity and nutrient composition [4,5,6,7,8,9,10,11]. The selective feeding mechanism of shellfish is complex, and phytoplankton retention rates and preferences vary among regions, seasons and environments [2].
Ruditapes philippinarum, Mollusca, Bivalvia, Veneroida, Veneridae, Ruditapes, is dioecious. It is one of the four major shellfish species cultured in China, and it is widely distributed along the coast of China. Its rapid growth and short culture period, coupled with its high adaptability, make it an excellent species for artificial high-density culture. It has great commercial value and has been introduced all over the world. The Yalu River Estuary of Dandong City, Liaoning Province, China, is one of the main regions for R. philippinarum culture, and it accounts for 18% of China’s total output of R. philippinarum. However, R. philippinarum yields have decreased steadily in recent years because of slowing growth rates, reductions in meat quality, and increases in mortality, and this poses a major threat to the sustainable and healthy development of the shellfish aquaculture industry. Previous studies have found that the phytoplankton in the Yalu River Estuary has small particle size components and weak nutrient supply capacity, which may affect the nutritional reserve and healthy growth of R. philippinarum. The aim of this study was to evaluate the feeding preferences of R. philippinarum for phytoplankton of different sizes and from different groups during different periods to evaluate whether nanophytoplankton and Dinophyta have contributed to the decline in R. philippinarum yields.
Phytoplankton are typically identified by observing morphological characters with the aid of a microscope. Given the limitations in the resolution of traditional microscopes, many small phytoplankton, especially picophytoplankton, have not been detected in previous studies, and thus are understudied. Here, high-throughput sequencing identification and visual grading technology were used to characterize the monthly feeding preferences of R. philippinarum for different types and sizes of phytoplankton in the Yalu River Estuary in 2020 and 2021. Our results provide new insights that could be used to identify possible approaches for ensuring the sustainable development of R. philippinarum culture in the Yalu River Estuary.

2. Materials and Methods

2.1. Sample Collection

Samples of R. philippinarum and phytoplankton were collected from the fixed stations in March–December 2020 and March–October and December 2021 (in November 2021, due to epidemic, we could not go out to sea for sampling, so there are no data) in the Yalu River Estuary, which is located in the northern part of the Yellow Sea (Figure 1). In 2020, it was only sampled at Station 1, and in 2021 at Station 1 and Station 2. Because the average water depth of our sampling site was approximately 5 m, environmental DNA samples of phytoplankton were only collected from the surface of the seawater at a depth of 0.5 m. Using a 5 L card cover type water collector to collect seawater about 0.5 m below the water surface, at least 1 L of seawater was vacuum-filtered through 0.22-μm cellulose acetate membranes and subsequently folded and flash-frozen at –80 °C until further processing in the laboratory. At the same time, 1 kg of R. philippinarum was collected from each station, and 30 stomach contents of R. philippinarum, about 0.5 g, were collected from each station every month for high-throughput molecular sequencing.
The pretreatment, preservation, detection and quality control methods for the environmental samples were implemented with reference to “Marine Survey Specifications” (GB/T12763-2007) and “Marine Monitoring Specifications” (GB17378-2007). The measured parameters were seawater depth (Dep), water temperature (T), salinity (SST), pH, dissolved oxygen (DO), chemical oxygen demand (COD), total nitrogen (TN), total phosphorus (TP), silicate (SiO3), dissolved inorganic nutrients (nitrite (NO2), nitrate (NO3), ammonia nitrogen (NH4), inorganic phosphorus (DIP), and inorganic nitrogen (DIN)), the inorganic nitrogen-to-phosphorus ratio (DI-N/P), organic nitrogen (DON), organic phosphorus (DOP) and the organic nitrogen-to-phosphorus ratio (DO-N/P).

2.2. Genomic DNA Extraction

The metagenome of the eukaryotic phytoplankton was extracted using the cetyltrimethylammonium bromide (CTAB) method. The filter membrane and visceral mass of R. philippinarum were cut into small pieces and placed in a 1.5-mL centrifuge tube; 500 μL of CTAB lysate (2% CTAB; 100 mmol/L Tris-Cl, pH 8.0; 1.4 mmol/LNaCl; and 10 mmol/L EDTA), 1 μL of β-mercaptoethanol and 5–10 μL of protease were added and left at 55 °C for 1–1.5 h. Following centrifugation, the liquid was removed and placed in a new centrifuge tube; the supernatant was then extracted twice using the phenol-chloroform method. The supernatant was collected, and twice the volume of pre-cooled absolute ethanol was added and left to precipitate for 2–3 h. After collecting the precipitate, it was washed with 75% ethanol to obtain phytoplankton genomic DNA. The concentration and purity of DNA were determined using 1% agarose gel electrophoresis and an ultraviolet spectrophotometer (Unico Instrument Co., Ltd, Shanghai, China); the samples were stored in a refrigerator at –20 °C for subsequent use.

2.3. PCR Amplification of the 18S rDNA V4 Variable Region

Total genomic DNA from the seawater samples was extracted using the CTAB/SDS method. The primers used in this study were V4(F/R), which are self-developed primers for amplification of the 18S rDNA V4 region of eukaryotic phytoplankton. The upstream primer was V4-F (5ʹ-GCGGTAATTCCAGCTCCAATA-3ʹ), and the downstream primer was V4-R (5ʹ-GATCCCHWACTTTCGTTCTTGA-3ʹ) [12]. The primers were designed with different labels and sent to Shanghai Shenggong Biological Company for synthesis. The PCR reaction system was 50 μL, including 5 μL of PCR buffer, 8 μL of dNTP mixture and 2 μL of downstream primers (10 μmol/L) each, 2 μL of template DNA, 2.5 U Taq DNA polymerase and sterile water. The amplification reactions were conducted on a PE 9700 PCR instrument (Perkin Elmer, Waltham, MA, USA). The thermal cycling conditions were as follows: pre-denaturation at 94 °C for 3 min; 33 cycles of denaturation at 94 °C for 30 s, annealing at 58 °C for 45 s, elongation at 72 °C for 45 s and a final extension at 72 °C for 5 min. PCR products were detected by 1% agarose gel electrophoresis. Sequencing libraries were generated using the NEB Next® Ultra™ DNA Library Prep Kit for Illumina (NEB, San Diego, CA, USA) per the manufacturer’s instructions; index codes were subsequently added. Library quality was assessed on a Qubit@ 2.0 Fluorometer (Thermo Scientific, Waltham, MA, USA) and an Agilent Bioanalyzer 2100 system. The library was sequenced on an Illumina HiSeq 2500 platform, and 250-bp and 300-bp paired-end reads were generated. The experimental reagents were all from Tianjin Kemiou Chemical Reagent Co., Ltd, Tianjin, China.

2.4. Data Analysis

2.4.1. Quality Control and Analysis of Sequencing Data

The raw data obtained were spliced using FLASH software. Quality control of the spliced sequences was carried out in QIIME software to obtain high-quality data. To ensure the accuracy of our sequencing analysis, more than 90% of our dataset comprised high-quality data. Sequence analyses were performed using Uparse software (Uparse v7.0.1001, http://drive5.com/uparse/, accessed on 22 February 2021, Independent Investigator, Edgar, R.C., Tiburon, CA, USA). Sequences with ≥97% similarity with a given operational taxonomic unit (OTU) were assigned to that OTU [13]. The representative sequence for each OTU was screened for further annotation. The Silva Database (http://www.arb-silva.de/, accessed on 2 November 2021) was used to annotate taxonomic information with the RDP classifier algorithm (v2.2, http://sourceforge.net/projects/rdp-classifier/, accessed on 11 April 2022, Microbial Genomics and Bioinformatics Research Group and Ribocon GmbH, Bremen, Germany). Non-algal OTUs were removed given that we were exclusively interested in the abundance and richness of eukaryotic phytoplankton.

2.4.2. Dominance

Previous studies have shown that the relative proportion of eukaryotic phytoplankton sequences is closely related to the biomass ratio of phytoplankton populations [14,15,16,17]; thus, the proportion of each eukaryotic phytoplankton sequence can be used as an indicator of the biomass ratio. Dominant species were identified according to the equivalent spherical diameter [14,15,16,18,19,20,21], and species with a phytoplankton dominance over 0.1% in each sample were considered dominant. The sum of the eukaryotic phytoplankton sequences with an equivalent spherical diameter greater than 20 μm was used as the microphytoplankton centralized statistic; the sum of the eukaryotic phytoplankton sequences with an equivalent spherical diameter of 3–20 μm was used as the nanophytoplankton centralized statistics; and the sum of the eukaryotic phytoplankton sequence with an equivalent spherical diameter of less than 3 μm was used as a centralized statistic for picophytoplankton. The proportions of the different size-fractionated phytoplankton were determined according to the numbers of sequences derived from each phytoplankton population.
The dominance index Y represents the distribution of biological individuals within a community and is also used as an indicator of biodiversity (Equation (1)):
Y = n x N f x
where nx is the sum of the sequences of x algae in all samples; N is the sum of all algae sequences; and fx is the occurrence frequency of x algae in all samples. Species with a dominance greater than 0.1% at each station were considered overall dominant species according to the cell-size biomass ratio.
Ivlev’s selection index E was used to analyze the feeding selectivity of R. philippinarum in the Yalu River Estuary.
E = ri − p i r i + p i
where ri represents the percentage of phytoplankton i in the stomachs of R. philippinarum, and pi represents the biomass percentage of phytoplankton i in the water. The range of E is [−1,1]. When E is −1, R. philippinarum avoids consuming phytoplankton i; when E is 1, R. philippinarum preferentially consumes phytoplankton i; and when E is close to 0, R. philippinarum neither avoids nor preferentially consumes phytoplankton i.

2.5. Statistical Analysis

The sampling method of environmental parameters refers to the Chinese National Standard: Ocean Survey Specification (GB/T 12763.4-2007), and the measurement method refers to the Chinese National Standard: Ocean Monitoring Specification (GB 17378-2007), as shown in Table 1. The dominance of the dominant phytoplankton species was represented by boxplots; the significant difference between environmental factors and particle size groups was analyzed by the Pearson statistical test; and the statistical results were represented by heatmaps. The formula calculation, data analysis and distribution map were all completed by WPS Office and Origin 2021 software.

3. Results

3.1. Phytoplankton Community Structure in the Stomachs of Shellfish and Seawater

3.1.1. Dominant Species

From 2020 to 2021, the top five dominant species and those with dominance in the stomachs of R. philippinarum and the water of the Yalu River Estuary are shown in Figure 2. Among them, Karlodinium veneficum had the highest average dominance in the two years, and it was the first dominant species in the water and stomachs in 2020 and stomachs in 2021, with an annual dominance of 0.12, 0.21 and 0.36, respectively. In 2021, the first dominant species in the water was Akashiwo sanguinea, with an annual dominance of 0.09, of which the highest dominance in autumn was 0.33, and the annual dominance of K. veneficum was 0.03. Chattonella subsalsa was the second dominant species in the stomachs in 2021, with an annual dominance of 0.18, of which the highest dominance, 0.47, was in summer. Teleaulax amphioxeia was the third dominant species in the water in 2021, with the highest dominance in spring at 0.12, followed by Micromonas pusilla as the fourth dominant species, with the highest dominance in summer, which was 0.10. According to the two-year investigation results, among the top five dominant species, the average dominance of K. veneficum and C. subsalsa in the water was lower than that in the stomachs, while the other three dominant species were higher than that in the stomachs.

3.1.2. Phytoplankton Groups

The dominant species (Y > 0.02) of phytoplankton in various groups in the stomachs of R. philippinarum and the water in the Yalu River Estuary in 2020 and 2021 are shown in Table 2. In 2020, the most-dominant species of Bacillariophyta in the stomachs of R. philippinarum was Guinardia striata (its dominance peaked in October at 0.72); the dominance in the water was 0.001, where it had not reached dominance. The most-dominant species of Bacillariophyta in the water was Thalassiosira nordenskioeldii (its dominance peaked in May at 0.28); the dominance in the stomachs was 0.002, where it had not reached dominance. In 2021, the most-dominant species of Bacillariophyta in the stomachs of R. philippinarum was Bacillariophyta sp. GSL077 (its dominance peaked in December at 0.29), and it was not a dominant species in water. The most-dominant species of Bacillariophyta in water was Chaetoceros sp. NIES-3971 (its dominance peaked in March at 0.66); the dominance in the stomachs was 0.01.
In 2020, the most-dominant species of Dinophyta in the stomachs of R. philippinarum was K. veneficum (its dominance peaked in April at 0.73), and the most-dominant species in water was also K. veneficum (its dominance peaked in August at 0.60). In 2021, the most-dominant species of Dinophyta in the stomachs of R. philippinarum was K. veneficum (its dominance peaked in May at 0.69), while the dominance in water was 0.03. The most-dominant species of Dinophyta in water was A. sanguinea (its dominance peaked in September at 0.54), and it was not a dominant species in the stomachs.
In 2020, the most-dominant species of Chlorophyta in the stomachs of R. philippinarum was Picochlorum sp. (its dominance peaked in June at 0.46); the dominance in the water was 0.002, where it had not reached dominance. The most-dominant species of Chlorophyta in water was Ostreococcus tauri (its dominance peaked in July at 0.84); the dominance in the stomachs was 0.01, where it had not reached dominance. In 2021, the most-dominant species of Chlorophyta in the stomachs of R. philippinarum was Pterosperma cristatum (its dominance peaked in March at 0.39); the dominance in the water was 0.003, where it had not reached dominance. The most-dominant species of Chlorophyta in water was M. pusilla (its dominance peaked in August at 0.16), and it was not a dominant species in the stomachs.
In 2020, the most-dominant species of Cryptophyta in the stomachs of R. philippinarum was T. amphioxeia (its dominance peaked in September at 0.07), and its dominance in water was 0.02. The most-dominant species of Cryptophyta in water was Cryptomonadales sp. (its dominance peaked in November at 0.23), and its dominance in the stomachs was only 0.02. In 2021, the most-dominant species of Cryptophyta in the stomachs was T. amphioxeia (its dominance peaked in May at 0.28); however, no Chlorophyta in the stomach contents reached dominance.
Overall, the biomass ratio of Dinophyta, Bacillariophyta, Chlorophyta, Dictyochophyta, Cryptophyta, Chrysophyta and unknown algae in the stomachs was 54:14:16:1:10:4:1 and 41:12:28:0:1:17:1 in 2020 and 2021, respectively. Chlorophyta accounted for the highest proportion in June; Bacillariophyta accounted for the highest proportion in November; and Dinophyta accounted for the highest proportion in other months. In 2021, only March, May, June and October had the highest proportion of Dinophyta. The proportion of biomass in water was 41:26:17:1:11:2:2 and 25:44:12:1:15:2:1, respectively, in 2020 and 2021. In 2020, the proportion of Dinophyta was the highest in March, August, September and December; in 2021, only June and September had the highest proportion of Dinophyta (Figure 3).

3.1.3. Phytoplankton Sizes

The dominant species (Y > 0.02) of phytoplankton of different sizes in the stomachs of R. philippinarum and the water in the Yalu River Estuary in 2020 and 2021 are shown in Table 3. In 2020, the most-dominant picophytoplankton species in the stomachs of R. philippinarum was Picochlorum sp.; the most-dominant picophytoplankton species in water was O. tauri. In 2021, the most-dominant picophytoplankton species in the stomachs of R. philippinarum was Bacillariophyta sp. GSL077; the most-dominant picophytoplankton species in water was M. pusilla.
In 2020, the most-dominant nanophytoplankton species in the stomach of R. philippinarum and the water was K. veneficum. In 2021, the most-dominant nanophytoplankton species in water was also K. veneficum, and the most-dominant nanophytoplankton species in water was Chaetoceros sp. NIES-3971.
In 2020, the most-dominant microphytoplankton species in the stomach of R. philippinarum was G. striata; the most-dominant microphytoplankton species in the water was Dissodinium pseudolunula (its abundance peaked in March at 0.57), and the dominance in the stomachs was 0.003, where it had not reached dominance. In 2021, the most-dominant microphytoplankton species in the stomachs of R. philippinarum was P. cristatum; the most-dominant microphytoplankton species in water was A. sanguinea.
Overall, the biomass ratio of picophytoplankton, nanophytoplankton and microphytoplankton in the stomachs of R. philippinarum was 13:48:39 and 14:66:20 in 2020 and 2021, respectively. In 2020, picophytoplankton accounted for the highest proportion in June, microphytoplankton accounted for the highest proportion in March, September and October, and nanophytoplankton accounted for the highest proportion in other months. In 2021, only March had the highest proportion of microphytoplankton, and nanophytoplankton accounted for the highest proportion in other months. The proportion of biomass in water was 19:44:37 and 22:39:39 in 2020 and 2021, respectively. In 2020, the proportion of nanophytoplankton was the highest in April, May, August, November and December. In 2021, only March, May and July had the highest proportion of nanophytoplankton (Figure 4).

3.2. Selectivity Index (E) Value

3.2.1. Selectivity for Phytoplankton Groups

The selectivity index of R. philippinarum to various groups of phytoplankton in the water in the Yalu River Estuary was shown in Figure 5, and the situation of E values greater than 0 is shown in Figure 6. Judging from the proportion of E values greater than 0 in the whole year, R. philippinarum preferred to feed on Dinophyta and Chlorophyta; Bacillariophyta, Chrysophyta, Cryptophyta and Dictyochophyta were negative. Among Bacillariophyta, the proportion of E values greater than 0 in winter in 2020 and 2021 was higher than 0.5, so R. philippinarum may prefer to eat on Bacillariophyta in winter. Among Dictyochophyta, the proportion of E values greater than 0 in spring and autumn of 2020 was higher than 0.5, so R. philippinarum may like eating Dictyochophyta better than others in spring and autumn. Among Cryptophyta, the proportion of E values greater than 0 in winter in 2020 was higher than 0.5, so R. philippinarum may prefer to feed on Cryptophyta in winter. Among Chrysophyta, the proportion of E values greater than 0 in spring of 2020 and spring and summer of 2021 was higher than 0.5, so R. philippinarum may prefer to feed on Chrysophyta in spring and summer.

3.2.2. Selectivity for Phytoplankton of Different Sizes

Judging from the proportion of E values greater than 0 in the whole year, R. philippinarum preferred to feed on nanophytoplankton; picophytoplankton and microphytoplankton were negative. In the picophytoplankton community, the proportion of E values greater than 0 in autumn and winter of 2020 and winter of 2021 was higher than 0.5, so R. philippinarum may like consuming picophytoplankton better than others in autumn and winter. In the spring of 2021, the proportion of E values of microphytoplankton larger than 0 was higher than 0.5, so R. philippinarum may prefer to eat on microphytoplankton in spring (Figure 5 and Figure 6).

3.3. Relationship between the Environmental Factors and Feeding Selectivity

The average values of environmental parameters for each season in 2020 and 2021 are shown in Table 4. NO3, NH4, DIN, TN, and TP gradually increase with the change in seasons, while DON and DOP had little change throughout the year. DI-N/P, COD and T were the highest in summer, followed by spring and autumn, and lowest in winter.
The relationship between the phytoplankton dominance and environmental factors in the water at Station 1 in 2020 and Station 1 and Station 2 in 2021 is shown in Figure 7. Among them, DO, SST and DO-N/P had positive effects on the nanophytoplankton community, but none of them reached significance, while COD and DOP had significant negative effects on the nanophytoplankton community. pH, SST and DON had positive effects on Dinophyta community, and pH had a significant effect on Dinophyta. NO3, DIN and DI-N/P had negative effects on the Dinophyta community, but none of them reached significance. COD and DI-N/P had significant positive effects on the Chlorophyta community, while NH4, DO and DIP had negative effects on the Chlorophyta community, but none of them reached significance.

4. Discussion

The proportion of Dinophyta biomass in the water was higher than that of Bacillariophyta in 2020, and the proportion of Bacillariophyta was higher than that of Dinophyta in 2021, while the proportion of Dinophyta biomass in the stomachs of R. philippinarum was far higher than that of Bacillariophyta in 2020 and 2021. At the same time, from the ratio of E values greater than 0, it can be found that the R. philippinarum avoided consuming most Bacillariophyta, Chrysophyta, Dictyochophyta and Cryptophyta and preferred consuming Dinophyta, and Chlorophyta throughout the year in the shellfish culture area of the Yalu River Estuary. This is consistent with the feeding habits of wild shellfish in that area as observed by Pan [22], in which feeding selectivity was higher for Dinophyta and Chrysophyta than for Bacillariophyta and Chlorophyta. In this study, R. philippinarum avoided feeding on Bacillariophyta in spring. Lavaud et al. stated that Pecten maximus cease consuming Bacillariophyta when their density in water is high [23]. Bougrier et al. indicated that Ostrea chilensis avoids consuming small Bacillariophyta [24]. The second most-dominant species observed in spring was T. nordenskioeldii, and the first dominant species observed was Chaetoceros sp. NIES-3971 in the water, which had high cell density in the water and they belong to Bacillariophyta with a relatively small particle size, so R. philippinarum chose to avoid eating. In addition, there were great differences between the different Bacillariophyta entering the digestive glands of shellfish [22], which may lead to R. philippinarum avoiding Bacillariophyta in Yalu River Estuary.
Langdon and Waldock [25] believed that filter-feeding shellfish ingested less or no toxin-producing phytoplankton, while Jiang et al. stated that shellfish are insensitive to most toxic phytoplankton and can ingest and accumulate toxins without affecting their feeding selectivity [26]. Different species of bivalve mollusks have relatively different feeding choices to toxic phytoplankton. Mytilus edulis rarely have negative responses when ingesting paralytic shellfish poisoning (PSP) toxin-producing phytoplankton (Alexandrium sp.), but scallops, oysters and clams decrease in different degrees, which may be related to the difference in sensitivity of shellfish neuron cells to PSP [27,28,29]. In this study, it was found that the first predominant species of K. veneficum in the water in the shellfish culture area of the Yalu River Estuary had hemolysin toxin, and was the first dominant species in the stomachs of R. philippinarum. A. sanguinea with hemolytic toxin was also the dominant species in the water and stomachs. Therefore, the negative response of R. philippinarum to toxic algae may not be great.
This study found that DI-N/P had a positive effect on Chlorophyta, while NH4 had a negative effect on Chlorophyta. In spring and summer, DI-N/P was significantly higher than that in autumn and winter, and the NH4 content was significantly lower than that in autumn and winter, so the content of Chlorophyta in water was higher. Langdon and Waldock indicated that filter-feeding juvenile oysters eat phytoplankton containing specific fatty acids [25]. Navarro et al. also found that Dinophyta had a higher fatty acid content than Bacillariophyta, and high fatty acid can promote Argopecten purpuratus to feed [30]. Ding et al. also indicated that unsaturated fatty acid was an important factor for the growth of many bivalves [31]. Sun et al. found that Picochlorum sp. contains higher unsaturated fatty acids, and this study found that Picochlorum sp. was the dominant species in the stomachs of R. philippinarum in 2020 and 2021 [32]. All these reasons may make R. philippinarum prefer to eat Dinophyta and Chlorophyta.
Molina et al. showed that Limnoperna fortunei does not feed on Cryptophyta [33], and Loret et al. found that Pecten maximus selectively feeds on Cryptophyta [34]. In our study, R. philippinarum avoided consuming Cryptophyta in spring, summer and autumn, but preferentially consumed Cryptophyta in winter. This finding might be explained by differences in the properties of shellfish species. Alternatively, this could be caused by the failure to detect the cells of Cryptophyta in the stomachs of mussels given that their fragile cell walls can be easily broken during digestion [35]. Shumway et al. also indicated that Cryptophyta cells may be completely digested and absorbed by bivalve mollusks during their passage through the intestinal tract [3]. In this study, it was found that the proportion of Cryptophyta in winter was relatively higher compared with other seasons, and the water temperature in winter was low. It is possible that Cryptophyta can stay in the stomach of R. philippinarum for a long time, so the detected proportion was higher in winter than other seasons. Therefore, although some fragile Cryptophyta may not be capable of being detected in the stomachs of bivalve mollusks through microscopy, they appear to be an important food source for natural populations of bivalves [3,34,35,36].
The biomass ratio of picophytoplankton, nanophytoplankton and microphytoplankton in the stomachs of R. philippinarum in the shellfish culture area of the Yalu River Estuary was 13:48:39 and 14:66:20 in 2020 and 2021, respectively, which indicated that R. philippinarum preferred consuming nanophytoplankton. Cranford et al. found that bivalve mollusks could easily feed on nanophytoplankton and that the retention rate of 2–8 μm phytoplankton was high [1]. Strohmeier et al. found that the retention rate of phytoplankton by Mytilus edulis gradually increased with the size of phytoplankton, and the maximum retention rate was observed for 7–35 μm phytoplankton [37]. Rosa et al. found that M. edulis preferred algae that were greater than 4 μm in size [38]. Dunphy et al. showed that O. chilensis retains 6 μm phytoplankton less efficiently than the 15 μm phytoplankton, which is consistent with the findings of our study [39]. Møhlenberg et al. showed that the retention rate of phytoplankton by M. edulis decreased rapidly for phytoplankton less than 4 μm in size [40]. Tammes et al. indicated that M. edulis could not effectively retain phytoplankton smaller than 2.5 μm [41]. Zhang measured the rejection rate of 2 μm phytoplankton in M. edulis, Crassostrea gigas and Azumapecten farreri by simulating on-site running water, which was 19%, 17% and 8%, respectively, and the rejection rate of particles below 2 μm was even lower [2]. These findings are consistent with the observation that R. philippinarum avoided consuming picophytoplankton in the shellfish culture area of the Yalu River Estuary.
The consumption of bivalve shellfish is determined by the filtration rate and particle-retention efficiency of the gills, which is the main organ for the transportation of seawater and the retention of particles. The feeding of shellfish is closely related to the structure of the gills and the movement of cilia on the gill filaments [42,43]. Jørgensen and Ward et al. found that the retention rate of phytoplankton was severely reduced when the anterior cilia of M. edulis were inactivated, which indicates that the anterior cilia are critically important for shellfish feeding [44,45]. Riisgård measured the retention rate of phytoplankton by six filter-feeding shellfish and found that the retention rate of phytoplankton larger than 4 μm in shellfish with larger anterior cilia, such as Geukensia demissa, Spisula solidissima, Brachidontes exustus and Mercenaria mercenaria, was 100%; by contrast, the retention rate of phytoplankton larger than 4 μm in shellfish with small anterior cilia or no anterior cilia, such as Crassostrea virginica and Argopecten irradians, was 75%–85% [43].
R. philippinarum possesses large anterior cilia; consequently, it preferred consuming large phytoplankton (nanophytoplankton and microphytoplankton). Among the six filter-feeding shellfish species studied by Riisgård [43], only G. demissa could significantly retain 0.2–2 μm phytoplankton, which may stem from the greater compactness of the cilia of G. demissa compared with the other five species examined. Wang found that the distance between the lateral cilia of R. philippinarum, Argopecten irradians, A. farreri and C. gigas was less than 1 μm, which is consistent with the proportion of picophytoplankton detected in the stomachs of R. philippinarum in our study (18%) [42]. Some researchers have suggested that filter-feeding shellfish prefer phytoplankton with greater concentrations of organic nutrients, and phytoplankton with low concentrations of organic nutrients are excreted as feces; picophytoplankton are typically not consumed by bivalves because of their small size and low nutritional quality [46,47].
This study found that the retention rate of picophytoplankton by R. philippinarum in the Yalu River Estuary was greater in autumn and winter than in summer and R. philippinarum preferred feeding on Chaetoceros calcitrans and Syndiniales sp. among picophytoplankton. Wei argued that C. calcitrans was an ideal opening food source for bivalves [48], and Lora-Vilchis also found that C. calcitrans was rich in some specific fatty acids; it also has a better effect as an initial feed for the larvae of Pinna rudis Linnaeus [49], which indicates that the picophytoplankton C. calcitrans can be ingested by juveniles. Ward et al. showed that slender or tri-radial phytoplankton may be more easily trapped by bivalves than spherical phytoplankton of the same volume [4,50]. C. calcitrans is mostly chain-like in water and is more likely to be trapped and fed; these considerations might explain why R. philippinarum preferentially consumed picophytoplankton in the Yalu River Estuary in autumn and winter [51,52,53,54,55].
The research area in the study was the main breeding area for R. philippinarum, in recent years, slow growth, decreased meat quality, and increased mortality have generally occurred, but no diseases, pollution, or red tides have been found in this sea area.The results showed that R. philippinarum avoided feeding on picophytoplankton, and the nanophytoplankton that actively fed was K. veneficum with low nutrition and toxicity in the study. Due to the quantitative selectivity strategy of R. philippinarum on feed microalgae, it filtered and fed on the dominant K. veneficum as much as possible in the case of low effective feed concentration. In addition, the increasing density of R. philippinarum culture resulted in the slow growth of R. philippinarum and increased mortality in the region. Therefore, it is recommended that the cultivation density should be reasonably controlled within the range of cultivation capacity in this region to maintain the healthy and sustainable cultivation of R. philippinarum.

5. Conclusions

In the Yalu River Estuary, R. philippinarum avoided consuming most Bacillariophyta, Chrysophyta, Dictyochophyta and Cryptophyta and preferentially fed on Dinophyta and Chlorophyta. R. philippinarum had a particularly strong preference for consuming K. veneficum, which was the most-dominant species in the water.
The annual average biomass ratio of picophytoplankton, nanophytoplankton and microphytoplankton in the stomachs of R. philippinarum was 13:48:39 in 2020 and 14:66:20 in 2021. R. philippinarum actively fed on nanophytoplankton and avoided picophytoplankton.
Among the phytoplankton of different grain sizes and groups that R. philippinarum prefer to feed, COD and DOP have a significant negative effect on the nanophytoplankton community, pH has a positive effect on the Dictyochophyta community, and COD and DI-N/P have a significant positive effect on the Chlorophyta community.

Author Contributions

Conceptualization, Y.L.; data curation, G.S.; formal analysis, K.W. and S.L.; investigation, G.S.; project administration, J.W.; software, Y.L.; supervision, Z.W.; validation, L.S.; writing—original draft, Y.L.; writing—review and editing, L.S. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Liaoning revitalization talents program (XLYC1907109); outstanding young scientific and technological personnel of Dalian (2019RJ09); Modern Agro-industry Technology Research System (CARS-49); and key research and development project of Liaoning Province, China (2018228004).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

We thank our colleagues for their assistance in collecting samples and Liwen Bianji for editing the language of a draft of this manuscript.

Conflicts of Interest

The authors declare that they have no known competing financial interest or personal relationships that could have appeared to influence the work reported in this paper.

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Fishes 07 00222 g001 550
Figure 1. Sampling sites in Yalu River Estuary, China.
Figure 1. Sampling sites in Yalu River Estuary, China.
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Figure 2. The top five dominant species and dominance in the stomachs of R. philippinarum in the water of the Yalu River Estuary. Vertical bars are the mean ± SE. Kar van: Karlodinium veneficum; Cha sub: Chattonella subsalsa; Mic pus: Micromonas pusilla; Tel amp: Teleaulax amphioxeia; Aka san: Akashiwo sanguinea.
Figure 2. The top five dominant species and dominance in the stomachs of R. philippinarum in the water of the Yalu River Estuary. Vertical bars are the mean ± SE. Kar van: Karlodinium veneficum; Cha sub: Chattonella subsalsa; Mic pus: Micromonas pusilla; Tel amp: Teleaulax amphioxeia; Aka san: Akashiwo sanguinea.
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Figure 3. The biomass proportion of various groups of phytoplankton in 2020 and 2021: (A) monthly in the stomachs; (B) monthly in the water; (C) seasonal in the stomachs; (D) seasonal in the water.
Figure 3. The biomass proportion of various groups of phytoplankton in 2020 and 2021: (A) monthly in the stomachs; (B) monthly in the water; (C) seasonal in the stomachs; (D) seasonal in the water.
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Figure 4. The biomass proportion of phytoplankton of different sizes in 2020 and 2021: (A) monthly in the stomachs; (B) monthly in the water; (C) seasonal in the stomachs; (D) seasonal in the water.
Figure 4. The biomass proportion of phytoplankton of different sizes in 2020 and 2021: (A) monthly in the stomachs; (B) monthly in the water; (C) seasonal in the stomachs; (D) seasonal in the water.
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Figure 5. Selectivity index of R. philippinarum for phytoplankton in the Yalu River Estuary in 2020–2021: (A) various groups; (B) various sizes.
Figure 5. Selectivity index of R. philippinarum for phytoplankton in the Yalu River Estuary in 2020–2021: (A) various groups; (B) various sizes.
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Figure 6. Frequency distribution of the situation of E values greater than 0: (A) various groups; (B) various sizes.
Figure 6. Frequency distribution of the situation of E values greater than 0: (A) various groups; (B) various sizes.
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Figure 7. The relationship between the phytoplankton dominance and environmental factors in water.
Figure 7. The relationship between the phytoplankton dominance and environmental factors in water.
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Table
Table 1. Sampling methods to measure the environmental parameters.
Table 1. Sampling methods to measure the environmental parameters.
Test itemsDetection MethodAccording to Standards
Silicate (SiO3)Silicon content-Molybdenum blue spectrophotometric methodGB17378.4-2007/17.2
Water temperature (T)Surface water thermometerGB17378.4-2007/25.1
pHpH meter methodGB17378.4-2007/26
Salinity (SST)CTD methodGB17378.4-2007/29.2
Dissolved oxygen (DO)IodometryGB17378.4-2007/31
Ammonia nitrogen (NH4)Hypobromite oxidation methodGB17378.4-2007/36.2
Nitrite (NO2)Naphthalene ethylenediamine spectrophotometryGB17378.4-2007/37
Nitrate (NO3)Zn-Cd reduction methodGB17378.4-2007/38.2
Inorganic phosphorus (DIP)Phosphorus molybdenum blue spectrophotometryGB17378.4-2007/39.1
Total phosphorus (TP)Potassium persulfate oxidation methodGB17378.4-2007/40
Total nitrogen (TN)Potassium persulfate oxidation methodGB17378.4-2007/41
Chemical oxygen demand (COD)Alkaline potassium permanganate methodGB17378.4-2007/32
Table
Table 2. Dominant species of various groups of phytoplankton in the stomach contents of R. philippinarum and water of the Yalu River Estuary in 2020–2021.
Table 2. Dominant species of various groups of phytoplankton in the stomach contents of R. philippinarum and water of the Yalu River Estuary in 2020–2021.
GroupSpecies Name (Stomach Contents)YSpecies Name (in Seawater)Y
BacillariophytaGuinardia striata *0.11Chaetoceros sp. NIES-3971 **0.08
Rhizosolenia setigera *0.05Thalassiosira nordenskioeldii *0.05
Bacillariophyta sp. GSL077 **0.04Rhizosolenia setigera **0.04
Skeletonema menzellii **0.04
Brockmanniella brockmannii *0.03
Thalassiosira curviseriata *0.03
Chaetoceros calcitrans **0.03
Thalassiosira pseudonana **0.03
Cyclotella choctawhatcheeana **0.03
Thalassiosira concaviuscula *0.02
Arcocellulus cornucervis **0.02
DinophytaKarlodinium veneficum0.21 */0.34 **Karlodinium veneficum0.12 */0.03 **
Polykrikos kofoidii *0.07Akashiwo sanguinea **0.09
Ansanella granifera *0.05Dissodinium pseudolunula *0.06
Islandinium minutum **0.03Spiniferites belerius *0.05
Akashiwo sanguinea *0.02Ansanella granifera *0.04
Alexandrium affine *0.02Alexandrium hiranoi **0.03
Proterythropsis sp. *0.02Gyrodinium dominans *0.02
Alexandrium leei *0.02Alexandrium affine *0.02
ChlorophytaPicochlorum sp.0.09 */0.04 **Ostreococcus tauri *0.1
Pterosperma cristatum **0.08Micromonas pusilla0.05 */0.06 **
Tetradesmus obliquus **0.03Mamiella gilva **0.05
Chlamydomonas raudensis **0.03
CryptophytaCryptomonadales sp.*0.02Cryptomonadales sp.*0.07 */0.03 **
Teleaulax amphioxeia*0.02Teleaulax amphioxeia **0.06
Cryptomonadales environmental sample **0.03
ChrysophytaChattonella subsalsa**0.18Fibrocapsa japonica *0.01#
Chrysosphaerella sp.*0.02
DictyochophytaPhaeocystis globosa*0.02Phaeocystis globose *0.003 #
* Dominant species of various groups of phytoplankton in the stomachs and water in 2020; ** Dominant species of various groups of phytoplankton in the stomachs and water in 2021; # The dominance of this group of phytoplankton in water did not reach 0.02.
Table
Table 3. Dominant species of phytoplankton of different sizes in the stomach contents of R. philippinarum and water of the Yalu River Estuary in 2020–2021.
Table 3. Dominant species of phytoplankton of different sizes in the stomach contents of R. philippinarum and water of the Yalu River Estuary in 2020–2021.
SizeSpecies Name (Stomach Contents)YSpecies Name (in Seawater)Y
picophytoplanktonPicochlorum sp.0.09 */0.04 **Ostreococcus tauri *0.1
Bacillariophyta sp. GSL077 **0.05Micromonas pusilla0.05 */0.06 **
Mamiella gilva **0.05
Chaetoceros calcitrans **0.03
Cryptomonadales environmental sample**0.03
Cryptomonadales sp. **0.03
nanophytoplanktonKarlodinium veneficum0.21 */0.36 **Karlodinium veneficum0.12 */0.03 **
Chattonella subsalsa **0.18Chaetoceros sp. NIES-3971 **0.08
Ansanella granifera *0.05Cryptomonadales sp. *0.07
Chlamydomonas raudensis **0.03Teleaulax amphioxeia0.02 */0.06 **
Proterythropsis sp. *0.02Thalassiosira nordenskioeldii *0.05
Teleaulax amphioxeia*0.02Ansanella granifera *0.04
Phaeocystis globose *0.02Skeletonema menzellii **0.04
Cryptomonadales sp. *0.02Brockmanniella brockmannii *0.03
Chrysosphaerella sp. *0.02Cyclotella choctawhatcheeana **0.03
Telonema subtile *0.02
Arcocellulus cornucervis **0.02
microphytoplanktonGuinardia striata *0.11Akashiwo sanguinea0.02 */0.09 **
Pterosperma cristatum **0.08Dissodinium pseudolunula *0.06
Polykrikos kofoidii *0.07Spiniferites belerius *0.05
Rhizosolenia setigera *0.05Rhizosolenia setigera0.04
Tetradesmus obliquus **0.02 */0.03 **Thalassiosira curviseriata *0.03
Islandinium minutum **0.03Thalassiosira pseudonana **0.03
Akashiwo sanguinea *0.02Alexandrium hiranoi **0.03
Alexandrium affine *0.02Gyrodinium dominans *0.02
Alexandrium leei *0.02Thalassiosira concaviuscula *0.02
Navicula sp. 39 **0.02Thalassiosira nodulolineata *0.02
Alexandrium affine *0.02
* Dominant species of phytoplankton of different sizes in the stomachs and water in 2020; ** Dominant species of phytoplankton of different sizes in the stomachs and water in 2021.
Table
Table 4. The average values of environmental parameters for each season in 2020 and 2021.
Table 4. The average values of environmental parameters for each season in 2020 and 2021.
Environmental FactorsSpringSummerAutumnWinter
T8.6324.2719.964.57
SST27.5626.2124.8426.56
pH7.998.017.937.86
DO10.948.018.9010.85
TN0.3000.4400.5730.570
TP0.0090.0130.0270.025
COD1.201.701.631.15
DIP0.0030.0050.0200.019
SiO30.1780.9301.0890.868
NO20.0070.0090.0370.019
NO30.1520.2400.3040.320
NH40.0390.0360.0820.108
DIN0.1980.2860.4220.446
DI-N/P245.49351.7476.3151.08
DON0.1010.1540.1510.124
DOP0.0060.0090.0060.006
DO-N/P38.5651.7864.7248.32
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Liu, Y.; Song, L.; Song, G.; Wu, J.; Wang, K.; Wang, Z.; Liu, S. Feeding Selectivity of Ruditapes philippinarum on Phytoplankton. Fishes 2022, 7, 222. https://doi.org/10.3390/fishes7050222

AMA Style

Liu Y, Song L, Song G, Wu J, Wang K, Wang Z, Liu S. Feeding Selectivity of Ruditapes philippinarum on Phytoplankton. Fishes. 2022; 7(5):222. https://doi.org/10.3390/fishes7050222

Chicago/Turabian Style

Liu, Yin, Lun Song, Guangjun Song, Jinhao Wu, Kun Wang, Zhaohui Wang, and Suxuan Liu. 2022. "Feeding Selectivity of Ruditapes philippinarum on Phytoplankton" Fishes 7, no. 5: 222. https://doi.org/10.3390/fishes7050222

APA Style

Liu, Y., Song, L., Song, G., Wu, J., Wang, K., Wang, Z., & Liu, S. (2022). Feeding Selectivity of Ruditapes philippinarum on Phytoplankton. Fishes, 7(5), 222. https://doi.org/10.3390/fishes7050222

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