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Research in migration route of hatchery released Chinese shrimp (Fenneropenaeus chinensis) in the Bohai Bay using method of SSR marker
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Weiji Wang1, 2, †, Ding Lyu1, 2, †, Mosang Wang1, 2, Kefeng Liu3, Jie Kong1, 2, Xiujuan Shan1, 2, Xianshi Jin1, 2, *
Acta Oceanologica Sinica | 2020, 39(12) : 76 - 81
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Acta Oceanologica Sinica | 2020, 39(12): 76-81
• Marine Biology •
Research in migration route of hatchery released Chinese shrimp (Fenneropenaeus chinensis) in the Bohai Bay using method of SSR marker
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Weiji Wang1, 2, †, Ding Lyu1, 2, †, Mosang Wang1, 2, Kefeng Liu3, Jie Kong1, 2, Xiujuan Shan1, 2, Xianshi Jin1, 2, *
Affiliations
  • 1 Key Laboratory of Sustainable Development of Marine Fisheries of Ministry of Agriculture, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, China
  • 2 Laboratory for Marine Fisheries Science and Food Production Processes, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao 266237, China
  • 3 Bohai Fisheries Research Institute of Tianjin, Tianjin 300457, China
Published: 2020-12-25 doi: 10.1007/s13131-020-1688-8
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This study provides new insights for the hatchery released Chinese shrimp (Fenneropenaeus chinensis), including proportion, dynamic migration route, after they were released into nature for stock enhancement using a new strategy quite different than ever. Chinese shrimp were sampled at 22 survey stations during two investigation voyages acrossing 74 survey stations in the Bohai Sea from July 16 to August 9 in 2015. Among 289 sampled individuals during the second voyage, totally 155 shrimps were identified as hatchery shrimp released into the Laizhou Bay at mid-May in 2015 based on finger-print of eight SSR (simple sequence repeats) markers, and the proportion of hatchery released shrimp in recapture samples were from 41.30%–85.71% in each station with an average value 53.63%, which verified a previous view point that up to 90% of autumn season Chinese shrimp landing in the Bohai Sea were composed of hatchery released. Meanwhile, the dynamic migration route of hatchery released shrimp revealed that part of released shrimp migrated heading northwest along the west coast of the Bohai Sea up to the Bohai Bay but just remained at the Laizhou Bay until over-wintering migration at mid-October when they initiate over-wintering migration. Present unnatural spring season shrimp fishing model cut the throat of spawner shrimp chance to swim back to their respective spawning plants at each spring, it still no chance to clarify whether the hatchery released shrimp could replenish to the reproduce population and complete a whole life cycle as same as their natural relatives.

Fenneropenaeus chinensis  /  migration route  /  hatchery release  /  stock enhancement  /  SSR marker
Weiji Wang, Ding Lyu, Mosang Wang, Kefeng Liu, Jie Kong, Xiujuan Shan, Xianshi Jin. Research in migration route of hatchery released Chinese shrimp (Fenneropenaeus chinensis) in the Bohai Bay using method of SSR marker[J]. Acta Oceanologica Sinica, 2020 , 39 (12) : 76 -81 . DOI: 10.1007/s13131-020-1688-8
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1 Introduction
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As one of the most important native marine shrimp species in China, with smaller population was also found along the coast of the Korean Peninsula, the Chinese shrimp (Fenneropenaeus chinensis) has played an indispensable role in China fisheries (Deng et al., 1990; Deng, 1998; Liu et al., 2004). However, since the 1980s, once plentiful spring and autumn season landings of Chinese shrimp in the Yellow Sea and Bohai Sea declined. This decline has been mainly attributed to an increase in fishing, pollution and natural habitat destruction. Additionally, the traditional spring shrimp-fishing season disappeared approximately since 1986 (Deng et al., 1990; Deng, 1998). Meanwhile, suffering from the disease (white spot syndrome virus, WSSV) outbreak in shrimp farming, the total annual production of Chinese shrimp dramatically decreased from approximately 200 000 t in the late 1980s to 20 000–40 000 t in the 2000s (Ye et al., 2005). After several decades of continuous practice, hatchery release enhancement was proven to be a useful strategy for natural population recovery of Chinese shrimp, and the fishery was also gradually benefiting from the strategy (Wang et al., 2006). Meanwhile, different methods were developed to assess the recapture rate, a very important index in assessing whether an enhancement program is successful. These methods include marker-recapture methods with physical markers such as eye tags, visible implant elastomers (http://www.nmt.us), code wire tags (http://www.nmt.us) and radio frequency identification (http://www.biomark.com), as the most commonly used (Klima, 1965; Marullo et al., 1976; Luo et al., 2008; Liu et al., 2013; Xu et al., 2017). Considering the huge number of hatchery and the small size of released shrimp, obtaining precise recapture rates for assessing the effect of the enhancement impractical by injecting physical markers is impractical. Therefore, it was necessary to develop a new type of “marker” for “released shrimp tagging”, and further to produce precise recapture rate assessment. Wang et al. (2014) provided a new distinguishable from previous physical tagging methods, which was based on individual identification and pedigree tracing using simple sequence repeat (SSR) markers and was successfully applied in recapture rates estimation in the Jiaozhou Bay and Bohai Bay in China in 2012. Regarding to the limited number of family individuals (named as molecular marker-tagging individuals compared to traditional physical-tagging individuals), including both hatchery released and detected from recaptured shrimp samples, however, previous research only provided limited data that not strong enough to support an overall assessment of shrimp released enhancement activity. Chinese shrimp was with significant migratory habitat. In its whole life cycle, there were three kinds of significant migration (over-wintering, spawning and feeding migration, respectively) that correlated closely with sea water temperature, bait, physiologic phase and hydrography. In addition to assess the enhancement effect, released shrimp identification and migration route tracing are also meaningful to clarify these following two puzzles: (1) Considering the biological behavior, whether the released hatchery shrimp stock is still consistent with their wild counterparts as well? In two fish species Mulloway (Argyrosomus japonicus) and Largemouth Bass (Micropterus salmoides), in which, higher levels of movement activity of hatchery-reared were discovered to be one of the key biological differences from natural stock, but lower survival probability of hatchery-reared was also found in semi-natural environments (Garlock et al., 2014; Taylor et al., 2017). (2) Could the released hatchery-reared shrimp have chance to develop spawner and further back to spawning plant after over-wintering as same as their wild counterparts at the next spring? Since besides to enhance the shrimp production, another important goal of hatchery release is to maintain self-sustainable wild stock (Araki and Schmid, 2010). It was widely believed that up to 80% or more of Chinese shrimp autumn landing were from hatchery-released (Wang et al., 2006; Li et al., 2019); and it is different from coastal invertebrate species, whose sessile or sedentary behaviors can be helpful for them to form self-replenishing population (Bell et al., 2005), Chinese shrimp need migrate to coastal area, especially estuary, to finish spawning just in part of life time. Hence whether the hatchery-released Chinese shrimp could finish a whole migration cycle is a signal of population self-replenishment and spawning plant improvement. Due to released individuals were too small to injected with physical marks, there were few studies focused on the pattern of feeding, overwintering, and spawning migrations of released Chinese shrimp. These questions were just speculated by the migration patterns of wild Chinese shrimp. Using microsatellite markers, we have an opportunity to do a realistic tracking description of them, which is of great significance for scientific evaluation of the ecological values of enhancement and releasing of Chinese shrimp. In this study, single-parent parentage identification in Chinese shrimp based on 8 SSR loci was used to trace the hatchery released shrimp in the Laizhou Bay in Shandong Peninsula in 2015, subsequently, the dynamic migration route and corresponding quantity changing of hatchery-released shrimp in the Bohai Sea were investigated and outlined. This research would be useful in enhancement effect and natural shrimp resource assessment, autumn fishing season landing amount anticipation, and even the dispute resolution of shrimp-fishing in the Bohai Sea.
2 Materials and methods
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2.1 Materials
2.1.1 Shrimp spawner sampling
By the end of June 2015, all of 1016 shrimp spawner were collected from Haifeng Aquatic Ltd., Changyi, Shandong Province, China after they finished larvae produce for shrimp hatchery release mission of the Laizhou Bay (lies in southern coast of the Bohai Sea), Haifeng was the only assigned Chinese shrimp seed producer for hatchery release in the Laizhou Bay in 2015. All samples were transferred with carbon dioxide ice to laboratory in the Yellow Sea Fisheries Research Institute, Qingdao, China and maintained in a –75°C super-cold refrigerator for the following DNA isolation.
2.1.2 Hatchery released shrimp recapture
All hatchery released shrimps, about 0.2–0.3 billion according to a private communication, were released around the estuary of Weihe River that lies in the southern coast of the Laizhou Bay in mid-May, 2015. Two months after the shrimp larvae were released, they were recaptured for the first time across three sea areas in the Bohai Sea by using traditional trawling net, including the Liaodong Bay sea area, the Bohai Bay sea area and Laizhou Bay sea area from July 16 to 18, respectively. In the Liaodong Bay sea area, there were 20 survey stations covered from 40°00′N to 40°45′ N, 120°10′E to 121°45′E; in the Bohai Bay sea area, totally 25 survey stations distributed, from 38°15′N to 39°00′N, 117°45′E to 119°00′E; and in the Laizhou Bay sea area, totally 21 sampling survey stations covered from 37°11′N to 38°00′N, 119°05′E to 120°30′E. From August 6 to 9, released shrimps were recapture for the second time at the other 8 survey stations that covered from 37°25′N to 38°44′N, 118°16′E to 119°45′E. All the recaptured shrimp samples were preserved in refrigerator aboard, then were transferred with ice to laboratory and maintained in a –75°C super-cold refrigerator for DNA isolation.
2.2 Methods
Protocol described by Wang (2008) was used to isolate genomic DNA from the swimming apparatus that dissected from each Chinese shrimp sample. Genomic DNA was dissolved in 0.1 mol/L TE (Tris-EDTA) (pH 8.0), and according to the OD260/280 value that measured using GeneQuant (Amersham Biosciences) and 0.7% agarose electrophoresis, the genomic DNA was adjusted to 50 ng/µL and stored at –20°C for subsequent SSR genotyping. One set of a quadruple-fold fluorescent-labeled SSR-PCR system for F. chinensis and other four single fold fluorescent-labeled SSR-PCR systems were used for total 8 SSR loci genotyping (Table 1), and the PCR reaction components and procedures were adopted following to the description of Li et al. (2012) and Wang et al. (2016) with slight adjustment. An ABI 3130 autosequencer (Applied Biosystmes) was used to separate the PCR amplification products, and the alleles of each SSR loci were sized with a GeneScanTM-500 LIZ Size DNA Standard (Applied Biosystems). A computer software for assignment of parents to their offspring based on genetic markers, Cervus 3.0 software, (http://www.fieldgenetics.com) was used to identify the released shrimp and trace to their parents. An authentic single-parent parentage relationship was declared only if all the alleles between recaptured sample and spawner were consistent and with an LOD score larger than 3.0.
3 Results
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3.1 Shrimp recapture results
During the two hatchery released shrimp recapture voyages, totally 74 survey stations were investigated by using trawling net across the whole Bohai Sea from July 16 to August 9, and the first and second voyages covered 66 and 8 survey stations, respectively. Chinese shrimp samples were captured at total 14 survey stations during the first voyage, the sampled shrimp number were from 1 to 9 per site with a total number of 37. By the second voyage, Chinese shrimp samples were found at all of 8 survey stations, the samples number were from 2 to 76 at each sea site with a total number of 289 (Table 2).
3.2 SSR genotyping results
Genomic DNA for SSR genotyping were isolated successfully from 1 016 shrimp spawner and 289 recaptured shrimp samples in the second voyage (the qualified genomic DNA could not be isolated successfully from all of 37 recaptured shrimp samples in the first voyage due to the poor preserved condition aboard). The total detected number of the alleles on 8 SSR loci after scanned 1 016 shrimp spawner and 289 recaptured shrimp samples were 254 and 238, respectively. The allele numbers at each SSR loci were from 8 to 63 with an average 31.75 and from 6 to 60 with an average 29.75 in spawner and recaptured stocks, respectively. The polymorphic information content (PIC) values of each SSR loci were from 0.780 to 0.952 across both spawner and recaptured stocks, which produced a cumulative probability of exclusion more than 0.999 with only one parent known (Table 3). In a view of genetic polymorphism, moreover, there was no obvious difference was detected between the spawner and recaptured stocks.
3.3 Hatchery released shrimp identification and single-parent parentage confirmation
Shrimps that were artificial released into the Laizhou Bay and were identified from all captured shrimps at 8 survey stations in the second voyage (Fig. 1), the number were from 1 to 37 per site with total number 155, and the proportion of released shrimp were from 41.30%–85.71% at each investigation site with an average value 53.63% (Table 4). All of these hatchery released shrimp could be traced to 135 female from 1 016 spawners that used in hatchery released shrimp larvae produced at the Laizhou Bay in 2015, most of spawners (116) have only 1 filial shrimp were detected, eighteen have 2 filial shrimp and there was also one have 3 filial shrimp were detected. According to the distribution of hatchery released shrimps after they were released into the Laizhou Bay, it was suggested that at least part of the hatchery released shrimps migrated heading northwest along the west coast of the Bohai Sea and even up to the Bohai Bay, which was against that the larvae would just remained at the Laizhou Bay until over-wintering migration around late October as thought before (Fig. 1), and the estimated swimming distance of part of hatchery released shrimp could be up to 100 km or more during two and a half months after they were released.
4 Discussion
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4.1 More precise recapture ratio assessment could be expected
As one of the focus topics, recapture rate assessments have been highlighted since the first hatchery released enhancement of Chinese shrimp at Bohai Sea 30 years ago (Deng, 1983). Many methods, most of them were physical-tagging techniques, have been reported before (Klima, 1965; Marullo et al., 1976; Luo et al., 2008), however, these methods either were only suitable in large sized shrimp. For example, the visible implant elastomer was only suitable for 3 cm or above size shrimp, or the numbers of tagging shrimp were very limited. Besides, physical-tagging was harmful to the tagged individual and the tagging process was labor intensive. Previously, the largest numbers of physical-tagging shrimps were 46 679 and 95 272 in the Bohai Bay and Liaodong Bay in 1986, respectively (Deng et al., 1990). Wang et al. (2014) developed “molecular marker-tagging” technique for recaptured rate estimation of Chinese shrimp, and the numbers of molecular marker-tagging were 204 000 and 300 000 in the Bohai Bay and Jiaozhou Bay, respectively. However, just in the Laizhou Bay, the number of released shrimps was more than 0.2 billion each year, and it could increase to 1.5–2.0 billion in the whole Bohai Sea. Hence, the numbers of either physical-tagging or “molecular-marker tagging” were too small to produce an unbiased recapture rate estimate for enhancement effect assessment (Bravington and Ward, 2004). With the accuracy of SSR on single-parent parentage confirmation in Chinese shrimp was verified in a previous study (Zhang et al., 2014), we introduced single-parent parentage identification using SSR marker in present study. Considering that all of the spawners used in the Laizhou Bay were sampled, theoretically, it is equal to that all of the released filial shrimp were “molecular-marker tagged”, and could be identified and traced to their maternities. In fact, totally 155 released shrimp were identified directly from 289 recaptured samples, and considering the number of identified hatchery released shrimp and its proportion in the whole recaptured samples, combing with an accuracy resource estimate, it was very hopeful to produce an authentic recapture rate estimate. Moreover, the chance to further understanding the survival rate, genetic variability and some other interested topics between hatchery released and wild populations was good as well, which was incomparable the previous physical-tagging release could be. A previous generally accepted view point considering that more than 90% part of Chinese shrimp landing in autumn fishing season each year in the Bohai Sea were hatchery released since the hatchery enhancement initiated 30 a ago, present results suggested that 41.30%–85.71% of recaptured shrimp at eight survey stations were composed of hatchery shrimp that released from the Laizhou Bay, which supported this view point again. Since the Laizhou Bay was not the only hatchery release site in the Bohai Bay, Hebei Province and Tianjin City along west coast of the Bohai Sea are both mainly responsible for at least one third of Chinese shrimp hatchery release in the Bohai Sea, and several survey stations in present study were more close to Hebei Procince or Tianjin City than to the Laizhou Bay (Gu et al., 2014). So, the most of left part in recaptured shrimp samples were from other Chinese shrimp hatchery released stations was also good. Considering there were more than 35 a since the first large-scale Chinese shrimp hatchery release initiated in Bohai Sea in 1984 (Wang et al., 2006), and to keep sustainable development of Chinese shrimp stock enhancement in the future, we are also supposed to pay more attention to the genetic differentiation between hatchery-released stock and wild population in the Bohai Sea areas , since negative effect (genome-wide introgressive hybridization) in wild Atlantic salmon influenced by hatchery released stock has been observed (Ozerov et al., 2016). At present, we still could not discriminate the wild shrimp from recaptured samples, partly because not all of the spawners for hatchery release along coast of the Bohai Sea areas could be sampled, so we still need a more detailed-designed program in future.
4.2 Migration route of released shrimp
Chinese shrimp has long-distance migratory behaviors, the female migratory distance could reach more than 1 000 km during a whole life span. Its life cycle could be divided into three obvious phases: feeding, over-wintering and spawning migration, but only the female individuals can complete the late two phases (in natural, male individuals died gradually after finishing copulation during the over-wintering migration in the late autumn). According to the geographic distribution of spawning plants, the natural Chinese shrimp population was suggested to be composed of the Bohai Bay population, the Laizhou Bay population, the Liaodong Bay population, the west coast of the Korean Peninsula and the other small, or unreported formally population (Zhuang et al., 2001; Liu et al., 2004), and it was generally accepted that although all the populations shared the same over-wintering ground, the shrimps within each population would follow a relatively settled route of feeding, over-wintering and spawning migration. In another word, with respect to population or gene-flow exchange, different geographic populations might share little, or at least there was still lack of strong evidence to support such an exchange.
Today, with continuous implement of hatchery enhancement of Chinese shrimp for 30 a ago, the old problem has been mentioned again: How about the migration routine of hatchery enhancement shrimp after they were released? If the released shrimps have chance escaping from high-intensity shrimp-fishing, could they migrate back to the original released stations to carry out reproduction and accomplish a whole migration cycle with their wild relatives at the next spring? This has puzzled academic fields since the hatchery enhancement was initiated. The reason why these puzzles emerged was mainly because human intervened the natural migration pattern. According to the official regulations of Chinese shrimp enhancement, spawners collection, larvae production and hatchery larvae release must be carried out in-situ, namely the hatchery released shrimp larvae must be produced by the spawners that captured just in the domestic spawning plants and the hatchery larvae must be released at the same site. However, due to the dramatically decreasing natural resource, especial the disappearing of shrimp spring fishing season, most of spawners were captured just around the over-wintering site located at the west coast of the Korea Peninsula before they migrate to their respective spawning plants, at least half of which lie in the coast along the Bohai Sea. Then, all of spawner shrimps for hatchery enhancement were transported alive by fishing vessel and sold to different shrimp larvae production plants along coast of the Bohai Sea in place of spawning migration at their last critical life phase, and that how much it would influence the released shrimp swimming ability or migratory habit is still needed to be clarified and paid more attention in the future. It was reported that two kinds of hatchery released fishes showed higher swimming ability but went with reduced survival rate in one kind than wild populations (Garlock et al., 2014; Taylor et al., 2017). Although present study did not prove hatchery released shrimp displayed higher swimming ability than its wild relative, it was a novel finding that the hatchery shrimp released in the Laizhou Bay did not just concentrate there but part of them could migrate northwest up along the west coast of the Bohai Sea, and based on history survey, some of them even swim up to the Bohai Bay until October when all of shrimp populations in the Bohai Sea initiate over-wintering migration (Wang et al., 2014). Due to the absent of samples captured from over-wintering plants and spawning plants, we still have no chance to clarify whether the released shrimps could complete a whole life cycle composed of three migrations as same as their wild relatives, which has been focused on as one of the next research items. Only if the released individuals were detected to swim back to their spawning plants, then whether the hatchery released shrimp accomplish a whole migration cycle and form replenishment population should be clarified. Hence, it is strongly suggested that the spawners should be only collected at their respective spawning plants.
Since hatchery release of Chinese shrimp were carried out in provinces along coast of the Bohai Seas, including Shandong, Hebei, Liaoning Provinces and Tianjin City in the spring of each year, shrimp-fishing was considered as a main source of revenue in autumn fishing season. However, no special shrimp-landing quota was distributed to fishing vessel, and the fishing disputes were inevitable. If the dynamic migration and distribution of hatchery released shrimp could be clarified, it would help to settle down the shrimp-fishing disputes.
Funding
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  • The National Key R&D Program of China under contract No. 2017YFE0104400; the National Basic Research Program (973 Program) of China under contract No. 2015CB453303.
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Appendix
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Year 2020 volume 39 Issue 12
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doi: 10.1007/s13131-020-1688-8
  • Receive Date：2019-10-16
  • Online Date：2026-03-31
  • Published：2020-12-25
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  • Received：2019-10-16
  • Accepted：2019-12-16
Funding
The National Key R&D Program of China under contract No. 2017YFE0104400; the National Basic Research Program (973 Program) of China under contract No. 2015CB453303.
Affiliations
    1 Key Laboratory of Sustainable Development of Marine Fisheries of Ministry of Agriculture, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, China
    2 Laboratory for Marine Fisheries Science and Food Production Processes, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao 266237, China
    3 Bohai Fisheries Research Institute of Tianjin, Tianjin 300457, China

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表12种不同金属材料的力学参数
科
Family		 属数
Number of
genus		 种数
Number of
species		 占总种数比例
Percentage of
total species (%)		 属
Genus		 种数
Number of
species		 占总种数比例
Percentage of total
species (%)
鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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