Genetic pattern fluctuations in wild swimming crab populations, under the influence of continuous mass stock enhancement
Introduction
Efforts to increase marine fishery production usually depend upon aquaculture, stock restorations, sea ranching and stock enhancements (Grant et al., 2017). Stock enhancements refer to the release of aquaculture-produced animals, commonly of commercial species, into the wild (Loneragan et al., 2019). Such practices have been widely applied to address the degradation of overexploited fishery resources, restore threatened and endangered marine species and improve wild recruitment of recreational or commercially important species (Morvezen et al., 2016; Katalinas et al., 2018). Stock enhancement programs have increased dramatically in the past two decades, mainly because fishery catch output cannot satisfy the demand for seafood, due to overfishing or depletion of habitats (Jackson et al., 2001; Garibaldi, 2012). Indeed, stock enhancement is a complex activity that has shown various levels of success around the world (Kitada, 2020). Katalinas et al. (2018) summarized unsuccessful stock enhancement as (a) exhibiting inadequate research of the life history of the enhancement species; (b) lacking effective monitoring methods for classification of hatchery-produced and wild individuals; and (c) providing insufficient evaluations of ecological and genetic effects of stock enhancement programs on the wild population. The stock enhancement activities in Japan revealed that success can only be achieved with the integration of habitat recovery (i.e., enhancement of seaweed communities) and a reduction in fishing pressure (Kitada et al., 2019). Although there is controversy over whether stock enhancements can really augment wild populations and maintain the genetic diversity of marine species over a long historical period, the effects of such enhancements can be observed over a short time period (Kitada, 2020; Lin et al., 2021). Recently, more than 26 billion hatchery-reared seeds of 180 marine species, across more than 20 countries and regions, have been released into the wild each year (Kitada, 2018). This is considered to be a viable, immediate option to deal with stock decline. The stock enhancement process is rapidly growing in China and other countries around the world. In excess of 94 billion juveniles were released between 2004 and 2013 along the coastal regions of China (Luo and Zhang, 2014) and a considerable proportion of these activities were large-scale stock enhancements. In Japan, around 1.5 billion chum salmon (Oncorhynchus keta) were stocked in 2018 (North Pacific Anadromous Fish Commission, 2019). Although mass-release of hatchery-reared seeds has achieved popularity in many countries for economic benefit, and many efforts have been made to improve aquaculture technologies, the potential temporal influences on local wild populations have seldom been comprehensively addressed. Assessment of the effects on wild populations is required to achieve a successful enhancement program.
The evaluation of stock enhancement activities in salmonids and other fish or crustaceans has indicated that the introduction of enhanced individuals may bring ecological and genetic impacts to wild populations (Araki and Schmid, 2010; Lorenzen et al., 2010). The ecological effects can be evaluated by the consideration of population abundance, age, fecundity and reproductive success (Hilborn et al., 2014; Shelton et al., 2015). These are relatively apparent and easily recognized in fishery monitoring investigations (Grant et al., 2017). However, compared with the evaluation of ecological effects, the genetic influences of stock enhancement on wild populations are invisible and relatively difficult to describe quantitatively. Hatchery-produced individuals usually have a high survival rate in their hatchery period and come from a small number of broodstock populations (Christie et al., 2012). Their parents have a limited gene pool when compared to wild species. Thus, a relatively small effective population size or genetic diversity is often observed in these hatchery-produced individuals, when compared with their natural counterparts (Willoughby and Christie, 2019). Artificial stock supplementation may result in the hatchery-reared and wild individuals mating, which could adversely impact local wild populations (Kitada et al., 2009; Satake et al., 2012). The subsequent genetic effects can be substantial and can alter the genetic profile of wild populations, interrupt microevolution, reduce the population fitness and affect the survival of a species (Hendry et al., 2011). If large-scale hatchery-produced individuals survive in the wild and contribute to future generations, the wild populations may be replaced, rather than supplemented (Laikre et al., 2010).
The swimming crab, Portunus trituberculatus, is one of the most important commercial fishery species and has a wide distribution, from the coastal area of Southeast Asia to the Indian Ocean (Dai et al., 1986). It is regarded as the main marine capture crustacean in China, Korea and Japan, and has a high commercial value (Liu et al., 2018). The swimming crab can live for up to two to three years, but large numbers of individuals are generally reported to live for around one year under high catch pressure in Liaoning (Iwai and Hayashi, 1990; Wang et al., 2020). This species displays both breeding migration and overwintering migration. In the Bohai Sea, individuals usually migrate to shallow waters of two to three meters for spawning, every April, and forage in the coastal areas until November, depending on the local water temperature (Cui, 2013). They are reported to move to the deep waters of the Bohai Sea (ten – thirty meters) for overwintering and conceal themselves in the soft mud or sands (Xue et al., 1997). The overwintering period is generally from early December to the end of March and the overwintering field covers almost the entire central Bohai Sea (Xue et al., 1997). The large-scale release of hatchery-reared juveniles began in 2012 in Liaoning province, which has a 2110 km coastline and is located between the Bohai Sea and the Northern area of the Yellow Sea (Liu et al., 2018). From 2012–2019, in excess of 1.8 billion hatchery-produced juveniles were released into the coastal waters of Liaoning province and more than 21.8 million US dollars (12.1 million US dollars per billion seeds) were spent on the purchase of seeds (Fig. 1). We have reported the process in our previous study (Liu et al., 2018). In short, all fertilized female P. trituberculatus (usually with a body weight from 250 to 500 g) were caught from the wild in April every year (based on the water temperature), and then used to hatch and produce F1 seeds. The female broodstock is renewed every year. The F1 crabs are cultured until they are at the second crab stage (C2), with a carapace width ≥6 mm, and then released during stock enhancement programs. Despite the high intensities of stock supplementation, each year, along the wide coastal waters of China, the genetic assessment of the swimming crab has been inadequate. During enhancement programs, female crabs, who usually weigh 200–300 g, can spawn 400,000–500,000 eggs, which makes the whole crab population vulnerable to recruitment sweepstakes after juvenile release (Hedgecock, 1994; Sun and Hedgecock, 2017). To date, we have only found one reference, Shan et al. (2018), based on an analysis of mitochondrial segments, that shows that relatively long-term hatchery release programs have not affected the genetic structure of local wild swimming crab populations in Shandong province, located between the Bohai Sea and the southern area of the Yellow Sea. No effort has been made to evaluate the temporal genetic effects of stocked swimming crabs on the wild populations in Liaoning province. The term “wild” refers to crabs caught in their local natural habitats, regardless of whether this includes hatchery individuals. This is because the hatchery-produced individuals cannot be directly identified due to the absence of a morphological difference (Liu et al., 2018).
Here, we used eighteen highly polymorphic microsatellite markers to monitor the two main natural habitats (Panjin and Yingkou) of the swimming crab in the long-term. These areas belong to the crab enhancement zones. We aimed to evaluate the temporal genetic variability and differences in local wild swimming crab populations, from 2014 to 2019. This is classed as a relatively long time period, during which mass release of hatchery-produced offspring occurred. Our results provide basic information that can be used to achieve a successful resource restoration for the swimming crab in the future.
Section snippets
Ethics statement
This study was approved by the Care and Use of Laboratory Animals in the Fishery Resources Enhancement Laboratory of Dalian Ocean University (2014−0610). All animal treatment protocols complied with Chinese laws, regulations and ethics.
Sampling, genotyping and quality control
A total of 465 swimming crabs were sampled from the Panjin and Yingkou inshore area, using crab cage nets. The Panjin samples comprised 279 individuals from three different years; 2015 (abbreviated to PJ2015), 2016 (PJ2016) and 2019 (PJ2019). The sampling
Genetic diversity
The Na per stock ranged from 23.722 (YK2015) to 31.667 (PJ2016). The average PIC values ranged from 0.878 (PJ2015) to 0.908 (PJ2016) (Table 1). Our results showed that the loci we used were highly polymorphic. Out of 108 single-locus tests, there were no loci that were Null > 0.2 in any stock and only three cases in which Null was slightly larger than 0.2 (pot44, ptri9 and pot25) (Table S2-S7). Hence, we did not remove these loci from subsequent analyses. The allelic frequency of all loci is
Discussion
The world’s fisheries are now either at capacity or overexploited. In 2018, the total global capture fisheries production reached the highest record of 96.4 million tonnes, with a total first sale value estimated at USD 151 billion (FAO, 2020). Scientific technologies have quickly developed to give us a better understanding of the functioning of aquatic ecosystems. The importance of responsible resource management, utilization and restoration of fishery resources is now widely recognized and
Conclusions
In general, we used genetic monitoring methods to quantify the temporal genetic variance and the level of genetic differentiation among local wild populations within their habitats, over a number of years. Genetic diversity indices were not stable, with clear fluctuations in genetic diversity, especially in the Panjin population. Genetic differentiation was low but small fluctuations or differences exhibited in the genetic architecture may reflect the interactions between the crab life cycle
CRediT authorship contribution statement
Binwei Liu: Formal analysis, Writing - original draft. Xi Zhang: Supervision, Writing - review & editing. Ziwei Wang: Formal analysis, Data curation. Weiyuan Li: Formal analysis, Data curation. Qi Zhang: Formal analysis, Data curation. Qi Liu: Writing - review & editing, Project administration. Wenlei Liu: Formal analysis. Lei Zhang: Data curation. Ying Liu: Project administration. Chenqi Wang: Formal analysis.
Declaration of Competing Interest
The authors report no declarations of interest.
Acknowledgments
This study was supported by the National Key R&D Program of China (2019YFD0900503), R&D Program of Liaoning Province (2019JH2/10200015), Scientific, Technological and Innovation Program of Dalian (2018J12SN069), General Project of Education Department of Liaoning Province (JL201904), the Projects for Dalian Youth Star of Science and Technology (2019RQ130), and Innovation and entrepreneurship training plan for college students in 2020 (B202010158039).
References (82)
- et al.
Is hatchery stocking a help or harm? Evidence, limitations and future directions in ecological and genetic surveys
Aquaculture
(2010) - et al.
Genetics in conservation management: revised recommendations for the 50/500 rules, red list criteria and population viability analyses
Biol. Conserv.
(2014) The FAO global capture production database: a six-decade effort to catch the trend
Mar. Policy
(2012)- et al.
Genetic effects of long-term stock enhancement programs
Aquaculture
(2009) - et al.
Compromising genetic diversity in the wild: unmonitored large-scale release of plants and animals
Trends Ecol. Evol. (Amst.)
(2010) - et al.
Stock enhancement of Culter mongolicus: assessment of growth, recapture and release size in the Yangtze lakes
Fish. Res.
(2021) - et al.
Genetic diversity of swimming crab (Portunus trituberculatus) populations from Shandong peninsula as assessed by microsatellite markers
Biochem. Syst. Ecol.
(2012) - et al.
Using of microsatellite DNA profiling to identify hatchery-reared seed and assess potential genetic risks associated with large-scale release of swimming crab Portunus trituberculatus in Panjin, China
Fish. Res.
(2018) - et al.
Changing phylogeographic pattern of Fenneropenaeus chinensis in the Yellow Sea and Bohai Sea inferred from microsatellite DNA: implications for genetic management
Fish. Res.
(2018) - et al.
Multi-scale interaction processes modulate the population response of a benthic species to global warming
Ecol Model.
(2020)
The importance of identifying spatial population structure in restocking and stock enhancement programmes
Fish. Res.
Effects of climate-induced water temperature changes on the life history of brachyuran crabs
Rev. Aquacult.
Restocking, stock enhancement, and sea ranching: arenas of progress
Rev. Fish. Sci. Aquac.
A responsible approach to marine stock enhancement
Am. Fish. Soc. Symp.
Stocked fish introgression into wild brook trout populations depends on habitat
T. Am. Fish. Soc.
Impacts of and adaptation to inter-decadal marine climate change in coastal China seas
Int. J. Climatol.
Preliminary assessment of stock enhancement in swimming crab (Portunus trituberculatus) based on molecular markers
Pak. J. Zool.
Potentials and limitations of stock enhancement in marine recreational fisheries systems: an integrative review of Florida’s red Drum enhancement
Rev. Fish. Sci. Aquac.
Raising the water temperature: consequences in behavior and biochemical biomarkers of the freshwater crab Aegla longirostri (Crustacea, Anomura)
Environ. Sci. Pollut. Res.
A unified approach to study hypervariable polymorphisms: statistical considerations of determining relatedness and population distances
Effective size of a wild salmonid population is greatly reduced by hatchery supplementation
Heredity
How much does inbreeding contribute to the reduced fitness of captive-born individuals in the wild?
J. Hered.
A single generation of domestication heritably alters the expression of hundreds of genes
Nat. Commun.
Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data
Genet. Soc. Am. Peer-reviewed Educ. Portal
Molecular Genetics and Breeding of Swimming Crab
Marine Crabs in China Sea
NeEstimator v2: reimplementation of software for the estimation of contemporary effective population size (Ne) from genetic data
Mol. Ecol. Resour.
Effects of elevated water temperature and food availability on the reproductive performance of a coral reef fish
Mar. Ecol. Prog. Ser.
STRUCTURE HARVESTER: a web-site and program for visualizing STRUCTURE output and implementing the Evanno method
Conserv. Genet. Resour.
Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study
Mol. Ecol.
Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows
Mol. Ecol. Resour.
A new viewpoint on genetic diversity in prestice black-pied pig: did the breed suffer from a bottleneck?
Acta. Univ. Agric. Silvic. Mendelianae. Brun.
Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies
Genetics
The State of world fisheries and aquaculture
Sustainability in action. Rome
Patterns of epigenetic diversity in two sympatric fish species: genetic vs. Environmental determinants
Genes
Holm-Bonferroni Sequential Correction: an Excel Calculator (v. 1.3) Microsoft Excel Workbook
Responsible genetic approach to stock restoration, sea ranching and stock enhancement of marine fishes and invertebrates
Rev. Fish. Biol. Fisher.
Conserving biodiversity under climate change: the rear edge matters
Ecol. let.
Does variance in reproductive success limit effective population sizes of marine organisms?
Fish Conservation: a Guide to Understanding and Restoring Global Aquatic Biodiversity and Fishery Resources
Evolutionary principles and their practical application
Evol. Appl.
Cited by (7)
Serotonin and dopamine regulate the aggressiveness of swimming crabs (Portunus trituberculatus) in different ways
2023, Physiology and BehaviorGenetic identification of Chinese shrimp Fenneropenaeus chinensis post-release in Jinzhou Bay: Implications for management of stock enhancement
2022, Regional Studies in Marine Science
- 1
These authors contributed equally to this work.