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Article

Evaluate the Biomass of Fenneropenaeus chinensis from the Southern Coast of Shandong Peninsula Using eDNA

1
Key Laboratory of Sustainable Development of Marine Fisheries, Ministry of Agriculture and Rural Affairs, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, China
2
Function Laboratory for Marine Fisheries Science and Food Production Processes, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao 266237, China
*
Author to whom correspondence should be addressed.
These authors contributed equally to this work.
Water 2023, 15(2), 342; https://doi.org/10.3390/w15020342
Submission received: 10 December 2022 / Revised: 9 January 2023 / Accepted: 11 January 2023 / Published: 13 January 2023
(This article belongs to the Section Biodiversity and Functionality of Aquatic Ecosystems)

Abstract

:
Fenneropenaeus chinensis is an important economic species in the north of China, and plays an important role in both marine fishing and aquaculture. Long-term overfishing has led to the rapid decline of wild F. chinensis resources. The traditional trawl survey could not meet the demands of the F. chinensis resource survey. In this study, environmental DNA (eDNA) technology was used to evaluate the biomass of F. chinensis in the traditional Qinghai (Qingdao Haiyang) fishing ground in the southern sea area of the Shandong Peninsula, with the purpose of verifying whether eDNA technology can provide a new resource assessment method for fisheries resource species such as F. chinensis. The eDNA quantitative results of the Qingdao water samples ranged from 1972 copies/L to 6937 copies/L, with an average of 4366 ±1691 copies/L. Those in Haiyang water samples ranged from 4795 copies/L to 8715 copies/L, with an average of 6737 ± 1348 copies/L. The concentration of eDNA in shrimp culture ponds ranged from 1.14 × 106 copies/L to 7.61 × 106 copies/L, with an average of 3.33 × 106 ± 2.28 × 106 copies/L. The amount of eDNA released by each gram of F. chinensis per 24 h was about 2.91 × 106 copies. According to this calculation, it was estimated that the distribution of F. chinensis was about one shrimp in every 300 m2 sea area. Similarly, it is estimated that one shrimp is distributed every 240 m2 in the Haiyang sea area. The result of this study confirms the feasibility of using eDNA to evaluate the biomass of shrimps.

1. Introduction

Fenneropenaeus chinensis is an important economic species in the north of China, and plays an important role in both marine fishing and aquaculture. Long-term overfishing has led to the rapid decline of F. chinensis resources, and annual landings dropped from 40,000 t in history (autumn shrimp-fishing) to about 3000–5000 t now. The spring shrimp fishing caused by the breeding migration of shrimp has disappeared since early 1990. At present, the biomass of F. chinensis in the Yellow and Bohai Sea mainly relies on artificial propagation and release, and the released shrimp has contributed more than 95% of the autumn yield. The annual migratory gravid female was an important object to evaluate the supplement of resources by propagation and release, which was related to the ecological security of the F. chinensis population. At present, due to disorderly fishing, most gravid female shrimp have been caught in the Yellow Sea off the southeast coast of the Shandong Peninsula, and few of them can enter the traditional spawning grounds along the Bohai Sea (Laizhou Bay, Bohai Bay, and Liaodong Bay). Based on traditional bottom trawl survey methods, gravid female shrimp has not been found in these three spawning grounds for many years. In recent years, the newly emerging environmental DNA (eDNA) technology was expected to effectively remedy the defects of trawl survey. eDNA technology refers to a new technology that analyzes the DNA fragments released into the environment through feces, mucus, blood, skin, decaying tissues, or molting, to determine whether certain organisms exist in a certain environment and their abundance. The most important advantage of this technology in comparison with the traditional methods, is that it can realize the assessment of the existence or even abundance of target species without monitoring live organisms. In aquatic environment ecology, eDNA technology was first used in the monitoring of bullfrogs [1]. After that eDNA technology has also been widely used in invasive species monitoring [2,3], biodiversity, fish diversity, and fishery resources assessment [4,5,6,7], population genetic diversity assessment and conservation genetics [8,9], including activity distribution monitoring of large marine mammals and large fish, and population size assessment [10,11,12]. The eDNA abundance can also be used to predict and evaluate biomass. Baldigo [13] used eDNA technology to evaluate the population density and biomass of Brook trout (Salvelinus fontinalis) in streams. The results showed that eDNA could explain the changes of 44% and 24% of the population density and biomass respectively. Stoeckle [5] research found that the seasonal abundance of up to 70% of the catch was highly consistent both in trawling and eDNA. In view of the fact that the number of gravid female shrimp in spawning grounds in the Yellow and Bohai Seas was becoming less and less, and the traditional trawl survey was weak, and the traditional trawl survey was weak, this study used eDNA technology to evaluate the biomass of F. shrimp in the traditional Qinghai (Qingdao Haiyang) fishing ground in the southern sea area of Shandong Peninsula, with the purpose of verifying whether eDNA technology can provide a new resource assessment method for species such as F. chinensis.

2. Materials and Methods

2.1. Materials

The gravid female F. chinensis in Qinghai fishery ground, belonging to the southern coast of the Shandong Peninsula were collected at two time points. Shrimps in Qingdao waters were collected from Qingdao National Central Fishing Port on 15 April 2022 and those in Haiyang were collected from Haiyang Fishing Port on 30 April 2022. All the samples were gravid females with already-developed gonads. After sampling, shrimps were maintained alive till their transport to the laboratory, where they got weighed.
Corresponding to live sample collection, water sample collection was completed in the corresponding time and corresponding sea area. Specifically, water samples from Qingdao were collected from 6 locations on April 17, and those from Haiyang were collected from 5 locations on April 30 (Figure 1).
In addition to the field experiments, water samples were collected from 8 indoor gravid female F. chinensis culture ponds (Tianjin Shentang Aquatic Breeding & Culturing Co., LTD., Tianjin, China) during the 20–25th of April. eDNA quantitative analysis was also carried out. The water volume of each shrimp pond was 15 m3, with 200 shrimp being raised in each of them. The water was changed 100% every day and replenished to the original water level.

2.2. Methods

A 2 L water intake device was used to collect seawater samples. In each sampling site, the bottom seawater was collected and it was repeated three times according to the depth of the sampling point. Additionally, the water of the surface, middle, and bottom layers of each sampling location were collected respectively, and filtered by means of a 0.45 μm glass fiber filter membrane (Xingya, Shanghai). The eDNA-enriched filter membranes were folded and stored at −20 ℃ for later analysis.
Water samples from the indoor aquaculture ponds were collected both in the middle and around the pond on a daily scale, just before changing the water. The same methods and sampling volume were used as in the wild. Ten individuals were randomly selected from each pond for weight measurement.
Based on the eDNA concentrations, the numbers, and the average body weights of shrimp in culture ponds, the eDNA amount released by shrimp per unit body weight (g) was estimated. Based on this standard and the eDNA concentration of the natural seawater, the biomass of gravid female F. chinensis in the sampling sea area was estimated. Since the eDNA in natural waters was constantly in the process of accumulation and degradation, the eDNA measured in the experiment included both the current release and the accumulation and degradation of eDNA in a certain period of time before. In the present study, the average temperature of seawater was about 10 ℃ during sampling. According to the results of our team’s previous research, the degradation cycle of eDNA in seawater of F. chinensis was about 10 days under this water temperature [14]. The following model was used to correct the concentration of eDNA in seawater [14]:
N = 0 240   680.71 × e 0.0116 x d x   0 24   680.71 × e 0.0116 x   d x
N is the concentration multiple of eDNA accumulated in water compared with that at the time of water sample collection; x is the complete degradation time (hour) of eDNA in water, and the maximum value of x is set as 240 h in this experiment.
The eDNA was extracted using a DNeasy Blood and Tissue kit (Qiagen, Germany). The mitochondrial COI gene was the target fragment of eDNA quantification in each water sample, and the quantitative analysis was conducted by absolute quantitative PCR using the probe method. The primer sequence, probe sequence, standard preparation, and quantitative PCR amplification experiments were all based on the technical system previously established in our laboratory [15].

3. Results

3.1. eDNA Concentration of F. chinensis in Water

A total of 158 and 75 gravid female F. chinensis were collected from Qingdao and Haiyang waters, respectively. The body weights of the samples from Qingdao ranged from 46.6 g to 104.4 g, with an average of 74.22 ± 10.23 g. Those from Haiyang ranged from 56.6 g to 134.1 g, with an average of 99.54 ± 16.98 g. The interval between the two samples was half a month, and the average body weight of Haiyang was significantly higher than that of Qingdao (p < 0.01). The body weight of F. chinensis samples in culture ponds ranged from 55.5 g to 120.3 g, with an average of 85.23 ± 8.17 g.
A total of 9 and 11 samples from different water layers were collected from Qingdao and Haiyang waters, respectively. The eDNA quantitative results of the Qingdao water samples ranged from 1972 copies/L to 6937 copies/L, with an average of 4366 ±1691 copies/L (Table 1). Those in Haiyang water samples ranged from 4795 copies/L to 8715 copies/L, with an average of 6737 ± 1348 copies/L (Table 1). The average eDNA concentration of F. chinensis in Haiyang waters was significantly higher than that in Qingdao (p < 0.01).
The concentration of eDNA in shrimp culture ponds ranged from 1.14 × 106 copies/L to 7.61 × 106 copies/L, with an average of 3.33 × 106 ± 2.28 × 106 copies/L (Table 2). According to this calculation, the amount of eDNA released by each gram of F. chinensis per 24 h was about 2.91 × 106 copies.

3.2. Estimation of the Biomass of F. chinensis in Natural Waters

The eDNA concentration in Qingdao waters was 4.3 × 106 copies/m3, and the average body weight of shrimp samples was 74.22 ± 10.23 g. Therefore, the eDNA concentration per cubic meter of water in Qingdao waters was equivalent to 1.477 g of body weight of shrimp. Equivalently about one F. chinensis is distributed in every 50 m3 of natural water. Since the natural seawater eDNA would have different degradation cycles according to the ambient temperature after being released into the water [14]. The seawater temperature during sampling was about 10 °C, and the degradation cycle was about 10 days [14]. According to Model (1), the accumulated eDNA concentration in water was estimated to be 6 times the concentration of eDNA in the water at the time of sampling. After data correction, it was estimated that the distribution of F. chinensis was about one shrimp in every 300 m3 of water. For the convenience of data comparison, it was roughly converted to one shrimp in every 300 m2 of water.
Similarly, according to the eDNA concentration of 6.7 × 106 copy/m3 and the average weight of 99.54 ± 16.98 g in Haiyang, and the biomass density was about one shrimp in every 240 m3 of water. As above, it is estimated that one shrimp was distributed every 240 m2. Compared with Qingdao waters, the distribution density increased slightly.

4. Discussion

Compared to nuclear genes, mitochondrial DNA has far more copies than nuclear DNA in cells and sequence is more conserved, which makes it easy to detect. Therefore, the mitochondrial COI gene was adapted in eDNA research. A variety of factors, including different species, physiological status, growth rate, feeding, and nutritional status, could affect the amount of eDNA released by organisms into the environment [16,17,18]. It was found that during the molting period, F. chinensis would release 40–200 times more eDNA than the normal state (to be published). In this study, the sampling time of water and shrimp was spring, and the F. chinensis had already mated and completed winter migration. They would not molt before spawning. Therefore, at this stage, the main physiological activities of the shrimp were feeding and supplementing the body nutrients to prepare for spawning, for the concrete manifestation of gonads developing rapidly and body weight increasing significantly. Excluding the slight difference in sea temperature between the two sampling time points, it was speculated that the eDNA of F. chinensis in the water in this study was mainly from the physiological process of defecation. In this study, the time interval of sampling in Qingdao and Haiyang was only half a month, and the average body weight showed a significant increase (p < 0.01). Meanwhile, the eDNA concentration of F. chinensis in the two sampling areas also showed a significant difference (p < 0.01), indicating that with the increase of body weight of F. chinensis, the amount of eDNA released into the water also increased. From Qingdao to Haiyang offshore, which was called Qinghai fishing ground, a certain amount of F. chinensis migrate and enter Jiaozhou Bay and Dingzi Bay to spawn from March to May every year. Since the two sampling areas are adjacent and both belong to Qinghai fishing grounds, there will be no significant difference in population density between the two sampling times. If the average body weights combined with the distribution densities of the two samples (Section 3.2) were converted into the biomass of F. chinensis per 100 m2, the effect of biomass on eDNA concentration can be described more objectively. The biomass of F. chinensis was 30.93 g per 100 m2 in Qingdao and 33.17 g per 100 m2 in Haiyang, which indicated that the increment of eDNA should be significantly correlated with the biomass. The increase in biomass is considered to be an important factor leading to the increase in eDNA release, which has been demonstrated in some freshwater and seawater fish with a linear correlation [18,19]. The positive correlation between biomass and eDNA concentration was not only confirmed by eDNA detection in some single species [7], but also in multi-species high-throughput sequencing of some marine bony fish: the reads sequence abundance of specific fish was also highly positively correlated with the corresponding catch abundance, and this positive correlation was reflected in multiple fishing seasons [5]. Water temperature, water layer, ocean current or tide, physiological state and development stage of animals, etc., all have different degrees of influence on eDNA release and its concentration. With the gradual deepening of the research on these factors, the accuracy of eDNA estimation of biomass can be more accurately improved. However, the positive correlation between eDNA concentration and biomass was not changed.
In this study, the amount of eDNA released in 24 h per gram body weight was calculated by using the concentration of in culture ponds. Combined with the detected concentration of eDNA in Qingdao and Haiyang waters, and the degradation rate of eDNA under the current water temperature, the distribution densities of F. chinensis in Qingdao and Haiyang waters during two sampling points were estimated to be about one per 300 m2 and one per 240 m2, respectively. Historically, the amount of gravid female F. chinensis is quite abundant, and a significant spring shrimp-fishing season of F. chinensis is formed every year. Due to the disordered increase in fishing intensity, the capturing yield in spring declined sharply after the 1980s, and by 1990, the spring shrimp-fishing season disappeared completely [20]. Since then, there was no fishing boat to conduct the exclusive fishing of F. chinensis in spring, and it has become the concurrent fishing object in the fishing operation. This is also the reason why live and water samples in this study were not obtained in the same sampling area. In fact, due to its scarcity, there have been few reports on the biomass of gravid female F. chinensis in its traditional spawning grounds of the Yellow Sea and Bohai Sea in the past 30 years. The most recent correlational research showed that the density of gravid female F. chinensis in Yanwei (Yantai Weihai) fishery ground in late April ranged from 0.31 to 6.50 shrimp/net×hour Between 1989 and 1994 [21], and the average value was calculated as 2.665 shrimp/net×hour. Considering the general single trawl mouth is 10 m wide, and the trawl speed is 2 knots (about 3.70 km/h), the sweep area per hour is about 37,000 m2 [22]. Besides, the escape index of F. chinensis during the trawling process is about 0.7 [22]. Based on the above information, the actual number of gravid female F. chinensis within a 37,000 m2 area is about 8.85, which is equivalent to 0.07 shrimp per 300 m2. It’s important to note that this result is based on the survey from 1989–1994 [21], during which the resources of F. chinensis declined sharply. Although the autumn landings had a small peak in 1990 (13,000 tons), in the same year the spring landings plummeted from 764 t the previous year to zero. In the following years, the autumn landings of F. chinensis also sharply decreased, and it plummeted to 500 t in 1998 [23]). In the past 10 years, with the continuous propagation and release of F. chinensis, the autumn yield in the Yellow Sea and Bohai Sea has recovered to about 4000 t per year. Although it has not reached the historical peak, it has increased by about 8 times compared with the lowest year of 500 t. Assuming that the number of gravid female shrimp also increases in equal proportion, during the breeding migration every spring, the density of gravid female shrimp in Yanwei fishery ground should be restored to about 0.56 shrimp /300 m2, which is very close to the results estimated in this study (1 shrimp /300 m2 and 1 shrimp /240 m2 in Qingdao and Haiyang, respectively). Prediction and assessment of fishery biomass using eDNA have become an interesting topic in the field of fishery resources research. In both relatively closed freshwater streams and open marine environments, eDNA has been used to reveal the biomass and its temporal and spatial changes to varying degrees [19,24,25]. In this study, due to the scarcity of gravid female F. chinensis in natural waters, simultaneous location and time sampling of live and water samples are not possible, which is one of the directions for improving the accuracy of eDNA assessment results in the future. As mentioned above, eDNA concentration is significantly affected by water temperature, ocean current, physiological state, etc. This is an important cause of uncertainty in the assessment of biomass using eDNA. Meanwhile, it should be noted that eDNA in water is always in a dynamic process of continuous accumulation and degradation, which needs to be taken into account. Compared with previous similar studies, the current study incorporated this dynamic process in analysis produced more credible results.

Author Contributions

Conceptualization, W.W.; methodology, S.S.; formal analysis, S.S. and W.W.; resources, D.L. and T.Q.; data curation, W.W.; writing—original draft preparation, W.W.; writing—review and editing, D.L. and S.S.; visualization, S.S.; supervision, W.W. and X.S.; project administration, X.S.; funding acquisition, W.W. All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by the Central Public-Interest Scientific Institution Basal Research Fund, YSFRI, CAFS (No. 20603022021002), and the Marine S&T Fund of Shandong Province for Pilot National Laboratory for Marine Science and Technology (Qingdao) (No.2021QNLM050103-3).

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Sampling location distribution in the Qingdao sea area and Haiyang sea area of the South coast of the Shandong Peninsula. ABCDEF indicate each location respectively in the Qingdao sea area and Haiyang sea area.
Figure 1. Sampling location distribution in the Qingdao sea area and Haiyang sea area of the South coast of the Shandong Peninsula. ABCDEF indicate each location respectively in the Qingdao sea area and Haiyang sea area.
Water 15 00342 g001
Table 1. The eDNA concentration in the Qingdao sea area and Haiyang sea area.
Table 1. The eDNA concentration in the Qingdao sea area and Haiyang sea area.
Locations in the Qingdao Sea AreaeDNA Concentration (Copies/L)Locations in
Haiyang Sea Area
eDNA
Concentration (Copies/L)
Surface layer of A2510.34Surface layer of A4795.98
Bottom layer of A5966.94Surface layer of B4908.12
Bottom layer of B1972.32Middle layer of B6297.90
Bottom layer of C2756.46Bottom layer of B5707.80
Surface layer of D6215.58Surface layer of C8715.00
Bottom layer of D4512.48Middle layer of C5672.94
Surface layer of E6937.56Bottom layer of C6105.12
Bottom layer of E5029.92Surface layer of D8687.28
Bottom layer of F3400.32Middle layer of D7574.38
Surface layer of E7672.14
Middle layer of E8324.40
Bottom layer of E6384.42
Mean4366 ± 1691Mean6737 ± 1348
Table 2. The eDNA concentration in culture ponds.
Table 2. The eDNA concentration in culture ponds.
Number of Culture PondseDNA Concentration (Copies/L)
13,487,183
24,021,327
37,605,872
46,015,915
51,227,555
61,656,314
71,138,116
81,474,368
Mean3.33 × 106 ± 2.28 × 106
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Sun, S.; Lyu, D.; Qian, T.; Shan, X.; Wang, W. Evaluate the Biomass of Fenneropenaeus chinensis from the Southern Coast of Shandong Peninsula Using eDNA. Water 2023, 15, 342. https://doi.org/10.3390/w15020342

AMA Style

Sun S, Lyu D, Qian T, Shan X, Wang W. Evaluate the Biomass of Fenneropenaeus chinensis from the Southern Coast of Shandong Peninsula Using eDNA. Water. 2023; 15(2):342. https://doi.org/10.3390/w15020342

Chicago/Turabian Style

Sun, Song, Ding Lyu, Tangyi Qian, Xiujuan Shan, and Weiji Wang. 2023. "Evaluate the Biomass of Fenneropenaeus chinensis from the Southern Coast of Shandong Peninsula Using eDNA" Water 15, no. 2: 342. https://doi.org/10.3390/w15020342

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