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All issues Volume 33 (2020) Aquat. Living Resour., 33 (2020) 24 Full HTML
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Issue
Aquat. Living Resour.
Volume 33, 2020
Article Number 24
Number of page(s) 8
DOI https://doi.org/10.1051/alr/2020025
Published online 15 December 2020

© EDP Sciences 2020

1 Introduction

Substantial reduction of global fishery resources has been documented over the past half century with over 90% of the world's fisheries fully exploited or overfished. This includes 53% that have been fully exploited and 32% that have been overexploited, depleted, or are recovering from depletion (FAO, 2010). 29% of fish and shellfish species have declined by as much as up to 90% (Worm et al., 2006). Several fish species have already been listed as extinct or endangered. Only 1% of the world's fish stocks are currently recovering from depletion (FAO, 2010).

China is the largest country for fishery production, export and consumption (Sun and Han, 2017; Sun and Li, 2018). It is responsible for most of the growth in fish availability, particularly from aquaculture, which accounts for more than 60% of global aquaculture production by weight (about 49.2 million tons of food-grade fish and 14.4 million tons of aquatic algae) in 2016 (FAO, 2018). However, the natural fishery resources, especially in the coastal and marine areas, have been declining rapidly. For instance, 36–53% of commercial species in 55–66% of exclusive economic zones were likely to be overfished from 1950 to 2004 (Srinivasan et al., 2010). A considerable amount of natural fishery resources has become extinct and many, including the large yellow croaker Larimichthys crocea (Richardson), are endangered.

The species is one of the most economically important marine fish in China. Its natural distribution spans the northern region of the South China Sea, the southern Yellow Sea, and the East China Sea. In the 1970s, wild catch of large yellow croaker in China is more than 1 × 105 tons per year, and reach 1.97 × 105 tons in 1974 (Xu and Liu, 2007; Zhang et al., 2017). In the Fujian sea area, the species migrates to Guanjingyang during mid-May to the end of June every year, which set the basis for the summer fishing seasons established before the 1960s. However, catch intensity increased substantially from the 1960s to 1980s, which led directly to its depletion (Zhang et al., 2017). The current market value of wild caught croaker ranges from $57.37 per kg for individuals weighing about 150 g to $286.85 per kg for those weighing over 1.5 kg. Due to the high economic value and severe depletion, its restoration is both economically and ecologically important. The recovery of China's fishery resources requires cooperation within the country between local governments, relevant enterprises, fishermen and researchers. Marine ranching projects have been introduced as an important development component in the upgrading of the traditional fishing and aquaculture industries (Yang, 2016). Key restoration efforts, which include genetic research, marine protected area management, and release of larvae have increased substantially over the past 30 years. Restoration of the wild large yellow croaker population is important, with continuing work on ecosystem-based management efforts, local community involvement, monitoring of larvae release activities, investigation of life history traits, and construction of a germplasm repository.

The restoration of large yellow croaker in China is mainly led by the government, with the establishment of protected areas, no-fishing period, juvenile releasing, which has certain effects, but it is unknown if and when the wild population can be restored (Zhang et al., 2010, Ye, 2012, Zhang and Hong, 2015), many international restoration progresses of fishery resources are also difficult to evaluate (Neubauer et al., 2013). Thus in order to better assess the potential resilience of the species, we established an integrated assessment method grounded on an ecosystem-based approach. We applied our method on the designated “national aquatic germplasm resource protected area” of the large yellow croaker in Guanjingyang, Fujian, China, which could help us understand the possibility of increasing the natural stock back to recovery, and to provide a scientific basis for these recovery efforts. The assessment is based on available data from 1987 to 2015.

2 Materials and methods

2.1 Study area

The 87 km2 Guanjingyang National Aquatic Germplasm Resource protected area (Fig. 1), formally established in 2007, is located at the southeastern part of Sansha Bay, Fujian Province. As the natural spawning ground of the large yellow croaker, it is also the first and only national aquatic germplasm resource protected area for the large yellow croaker. This region was earlier in 1985 designated as a protected area for large yellow croaker and restoration efforts were put into effect since then in response to depleting fisheries resources recent years (Fig. 2). To date, millions of dollars have been invested for the restoration of the natural population. Evaluating the effectiveness of restoration efforts made here could provide useful information for a wider management application to prevent depletion of large yellow croaker wild populations in China.

thumbnail Fig. 1

Study area, the location of Guanjingyang.
thumbnail Fig. 2

Annual production of the large yellow croaker from 1956 to 2015 in Guanjingyang, China.

2.2 Integrated assessment index

From the perspective of ecosystem-based approach (Pikitch et al., 2004), the restoration potential of large yellow croaker are determined not only by its own population, but also by the habitat as well as the social interventions. Thus to assess the restoration capacity of natural fishery resources, we developed an integrated index system (Tab. 1) which includes three key components: (1) habitat suitability (HS), which is the condition of a specific marine habitat where the croaker spends most of its life cycle; (2) natural population status (PS), which is the natural population size and genetic diversity; (3) government & social interventions (GSI), which includes the key restoration efforts carried out by the government and community.

We call it the Restoration Capacity Index (RCI). Original data are transformed by extreme standardization, which is a linear method that puts all values in a range of 0–1. In order to combine all the indicators together and show the overall restoration capacity trend, the entropy weighting method based on the variation of data is employed to calculate the weights of each indicator (Fagbote et al., 2014; Delgado and Romero, 2016; Zhao et al., 2018). Calculated weights of all indicators are listed in Table 1.

Weighting calculate:

(1) Data matrix:

(2) Standardized data matrix:

Positive indicator:(1)

Negative indicator:(2)

(3) Calculate the entropy:(3) (4) (5)

(4) Calculate the weight:(6)

The RCI is calculated by the three-dimensional state-space model (Mao et al., 2001; Wei et al., 2014; Jiang et al., 2017). Thus, the capacity index can be considered the modulus of a three-dimensional space vector, which reflects the habitat development, population and interventions. The status of the RCI can be effectively depicted by calculating the modulus and the curvature:(7) where Cj is the evaluation index, j represents different years, wi is the calculated weight by entropy method, xi indicates the standardized results, and i represents the indicator types.

Evaluation of results is restricted to the values between 0 and 1, where 0 means the worst and 1 presents the best. We further define different levels for the final results in this study: 0–0.29 is the lowest level, 0.3–0.69 indicates the medium level, 0.7–1.0 represents highest level.

Table 1

Large yellow croaker evaluation index system and weight.

3 Results

3.1 Habitat suitability (HS)

The HS evaluation indicates that Guanjingyang habitat conditions stayed stable from 1987 to 2011, decreased in 2012 to 2015 (Fig. 3). Changes to the protected area are considered to be the most fluctuating component among all the indicators of HS, while water conditions and biodiversity changed little in the past decades.

None of the key physical and chemical factors for both living and reproduction fell outside of the survival ranges, and the key factors of water temperature, DO, and pH mostly were within the optimal ranges. These indicators suggest no severe changes to the water environment, considered stable for the croaker in Guanjingyang.

thumbnail Fig. 3

The Restoration Capacity Index (RCI) of the restoration potential of wild large yellow croaker in Guanjingyang and the performance of Habitat Suitability (HS), Population Status (PS) and Government Social Interventions (GSI) from 1987 to 2015.

3.2 Natural population status (PS)

The PS evaluation (Fig. 3) indicates relatively decrease from 2004 to 2015, in which get the lowest score at 2007. Specifically, population size has not increased, while population genetic diversity has fluctuated with time.

3.3 Government and social Interventions (GSI)

The GSI grew significantly in the Guanjingyang protected area (Fig. 3). It scored low in previous years from 1987 to 2008, but increased quickly in the following years, arriving at its highest point in 2015. From 2010 to 2015, the scores fluctuated sharply. Specifically, research inputs and rehabilitation efforts in GSI rose dramatically from 2009, which became the key indicators.

3.4 Integrated evaluation results

The integrated results generally show an increase trend of the restoration capacity from medium level to the highest level (from 0.38 to 0.74) of large yellow croaker in Guanjingyang (Fig. 3). From 1987 to 2009, the values were lower than 0.5 due to overfishing and weak restoration efforts. The highest value was reached in 2010 and 2015 due to the increased number of large yellow croaker juveniles released in Guanjingyang and the growth of research input. This upward trend shows the government's commitment to the restoration of large yellow croaker resource since 2004. A sharp drop in 2013 is noted, which is likely due to the decrease of research input and juveniles released. However, the values increased sharply from 2014 to 2015, related directly to an increase in released juveniles to reach the highest restoration capacity level in 2015.

The restoration capacity performance of HS, PS and GSI vary in scores and development trends (Fig. 3). The scores of HS and PS are more stable than GSI. While values of GSI show generally increasing trends overall, the scores of PS and HS have the opposite tendency. The integrated results are influenced mainly by HS (from 1987 to 2008), which is changed to GSI after 2009. While the integrated results increase these years the annual production still remains low. These results indicate that the habitat environment has not improved substantially and that the population and diversity of the large yellow croaker only changed slightly, despite the local government pouring a large amount of resources into restoration.

4 Discussion

The marine protected area in Guanjingyang was 329.5 km2 when established in 1985. It was reduced to 314.7 km2 in 1997 because of the construction of a new port and further reduced to 190 km2 in 2012 due to the overall development of tourism, ports, and military purposes. The shrinkage of the area by 42.33% is considered as having a negative impact on the fish restoration efforts (Zhu, 2011).

Adult yellow croakers typically live in the mid-water zone of the near-shore area (depth less than 60 m). The species is a warm-temperature migratory cluster fish in the North Pacific, with a water temperature range of 10–32 °C and an optimum range of 18–25 °C. Water temperatures below 18 °C or above 25 °C are not suitable for the reproduction of large yellow croakers, hatching of fertilized eggs, or growth of juveniles. Additionally, the adaptation salinity range is 24.8–34.5‰ while the optimum range is 30.5–32.5‰. Low salinity will affect cluster movements of the species. The suitable pH is 7.85–8.35, and the dissolved oxygen suitable for its survival is generally above 4 mg/L (Science and Technology Department of Fujian Province, 2004; Liu, 2013).

The recorded data for wild yellow croaker production in Guanjingyang goes back to 1956 (Fig. 2). The annual production underwent three major fluctuations since records began. In the late 1950s, because of large-scale “boat-knocking” fishing activities (hitting interior of boat hull with a club sending sound waves through water to stun fish), fish production was reduced substantially in 1963, less than 6% of that in 1956. With the ban on boat-knocking, the population recovered naturally in the following 5–10 years. In the late 1960s, annual production increased to more than 1600 tons. However, it decreased again after 1970 due to the dramatic increase in fishing effort in the region. Since 1979, the natural production became severely depleted due to overfishing.

Genetic diversity is an important basis for evaluating the status of species resources, and is an important genetic indicator for measuring the evolutionary potential of a species' ability to withstand various survival stresses in nature. Many genetic diversity studies have shown that wild large yellow croaker populations have a relatively higher level of genetic diversity compared to cultured croakers (Wang et al., 2002; Li, 2009; Liu et al., 2015; Lou et al., 2015). By comparing the AFLP data of large yellow croaker with other known fish in Tables 2 and 3, it may be noted that the value of large yellow croaker is higher than that of most economically importance fish species in China. This parameter indicates that although the status of genetic resources of large yellow croaker has deteriorated sharply due to various reasons such as overfishing, genetic drift and artificial breeding, the current wild resource has a good evolutionary potential. This means that the large yellow croaker has the breeding potential for population recovery.

Since the 1950s, Chinese scholars have studied the diet, reproduction, population, ecology, nutritional and medicinal value along with the ethnic issue related to the large yellow croaker resource. The main results published before the late 1980s include: preliminary research on the ethnicity, sexual maturity characteristics, geographical structure variation and individual fertility of large yellow croaker, research on morphological characteristics of larvae and juveniles (Zhang et al., 2009; Jiang et al., 2014; Eero et al., 2012; Garcia and Rosenberg, 2010; Rosenberg et al., 2006; Worm and Zeller, 2009; Wu et al., 2014). These basic scientific works have actively promoted the progress of research, providing a scientific basis for the rational management and protection of the species.

Since the late 1980s, research on wild large yellow croaker resources has focused on molecular biology, including the genome sequence and immune system(Costello and Lester, 2012; Wu et al., 2014). Han et al. (2015) analyzed the karyotype of Guanjingyang large yellow croaker. Wang et al. (2002) used isozyme, RAPD, AFLP and other analytical techniques to detect the genetic diversity of Guanjingyang wild large yellow croaker. Research on the genetic diversity and frozen semen preservation technology laid a solid scientific foundation for the restoration and preservation of wild large yellow croaker germplasm resources. In addition, the National 863 Project “Cultivation of High Quality and Stress Resistant Varieties of Large Yellow Croaker” was successfully completed in October 2010. The cultivation of excellent strains and the successful research on all-female egg production techniques have greatly alleviated the lack of breeding information related to the large yellow croaker. At the same time, the “National Large Yellow Croaker Genetic Breeding Center” was established in 2016 as the first national large yellow croaker genetic breeding center in China.

At present, Ningde City does not have a complete public participation system for the establishment and planning of protected areas and the protection of fishery resources. The Ningde City Ocean and Fisheries Bureau implemented government information disclosure on the Internet in May 2008, including institutional setup, administrative regulations, marine and fishery economic planning, basic statistical information on marine and fishery development, approval and implementation of major construction projects, etc. During 2008–2015, the Ningde government held annual notices or publicity activities on large yellow croaker protection, and actively cooperated with the restoration of the Guanjingyang large yellow croaker breeding reserve.

In addition, the Ningde Large Yellow Croaker Association was established in 2003. It is an industrial social group composed of the city's large yellow croaker industry and related units, community organizations and individual volunteers. However, the level of public participation in the protection of wild croaker resources is low, the government's advertising is weak, and local fishermen have little awareness of the recovery of wild large yellow croaker resources (Ningde Large Yellow Croaker Association, http://www.gjyfish.com/).

In order to strengthen the breeding and protection for the Guanjingyang large yellow croaker, Ningde City implemented navigational restrictions on the Guanjingyang large yellow croaker breeding protection zone during the migratory spawning period. Access is restricted 24 h a day specifically, from June 5th to 9th and June 19th to 23rd. During these periods, fry (more than 5 cm length) are released in the Guanjingyang breeding reserve (Fig. 4). From 2011 to 2015, the number of fry released was 4, 3.701, 2.245, 13.615, and 210.54 million, respectively. In 2016, 3.561 million fries of the species, cultivated by the national-level Guanjingyang large yellow croaker breeding center, were returned to the Guanjingyang large yellow croaker breeding protection zone. In the spring of 2019, the alliance of LYS seedling producers in Jiaocheng District of ningde city moved 1/3 (more than 1 billion) of LYC seedlings into Guanjingyang and Sandao sea area. In addition to human efforts such as proliferation and release, natural incidental factors may also affect the recovery of large yellow croaker. For example, Typhoon Saomai destroyed nearly 70 000 cages in Fuding, Fujian at the summer of 2006; the juvenile that escaped into natural sea may help the restoration of wild stock.

However, many of the fish release have been caught before they have grown into adults and bred, which form an important cause of the fish stock cannot be restored. Prohibiting fishing for consecutive years (at least for several consecutive generations) may be an effective way to restore the natural population of large yellow croaker, as a result of the large yellow croaker in natural sea areas, artificial release and escape from the cage can grow into adults and breed offspring.

According to Ling et al. (2006) large yellow croaker resources in the East China Sea have been severely declining with no signs of recovery. Other fish such as the beltfish (Trichiurus haumela) and Chub mackerel (Scomber japonicus) are already in a state of decline with a possibility of extinction if left unprotected. The fishery resources in the Xiamen sea area and the Minjiang Estuary have also declined significantly, where the primary catch consists of young fish of low trophic levels (Huang et al., 2010a,b). Although the proliferation and release measures have achieved good results with high economic benefits in various places (Shen and Zhou, 2007; Zhang et al., 2009), unreasonable proliferation and release may bring various ecological risks to the natural resources and water ecosystems (Jiang et al., 2014). The impact on the local ecology from the proliferation and release of juveniles should therefore be taken into consideration, so that restoration of the large yellow croaker is effective.

In short, the limiting factor for the recovery of the large yellow croaker populations is overfishing. The uncontrolled knocking operations used by the fishermen in the 1960s devastated the large yellow croaker population in the study region. The intensity of fishing in the 1980s depleted large yellow croaker stock. In general, to obtain better recoveries, a breakthrough in capture yield must be achieved.

Table 2

Genetic diversity evaluation results of Large Yellow Croaker (LYC) in different geographical groups by using AFLP.

Table 3

Some known commercial fishes' AFLP genetic diversity.

thumbnail Fig. 4

Release of the large yellow croaker juvenile from 1987 to 2015 in Guanjingyang, China.

5 Conclusions

Comparing the existing assessments of fishery recovery potential (Kapetsky, 2000; Davies and Jonsen, 2011; Isomaa et al., 2013), this study is the first known attempt to synthesize three key dimensions to evaluate the restoration capacity of marine fish resources. This assessment not only considers attributes of the natural population of the fish species, but also the habitat quality as well as the related government and social interventions. We highlight that the restoration efforts put by the government, scientists and local society are the key drivers for endangered species recovery (Zheng et al., 2013; Hildebrandt et al., 2018), which have only been suggested by other studies.

In Guanjingyang's case, restoration efforts have increased greatly since 2007, including the increase of research inputs, rehabilitation efforts and public awareness, all of which could have positive effects on promoting the recovery of large yellow croaker resource (Xu, 2009; Ma, 2016), but at this point still have had no significant influence for its natural stock recovery. Similarly, a reserve area was designated in 1987 as a result of the severe depletion. Even with the conservation efforts, which have been in effect for almost 30 years, the natural population remained near extinction in 2015. Although the genetic diversity of the species in Guanjingyang was a little higher than other areas, for example, Ningde, Lianjiang (Tab. 2), and may indicate better potential recovery (Neel, 2008; Shao et al., 2009), the integrated evaluation results pointed to a low possibility of natural stock recovery. The main hindrance for the recovery of the large yellow croaker may be related to the low proliferation capacity due to near extinction of the species (Zhang et al., 2017). However, some researchers indicate that extensive studies on genes, species, population, community and ecosystem combined with the efforts on natural habitat restoration may facilitate the restoration of the large yellow croaker wild fisheries in the future (Yan, 2019). China is currently vigorously promoting the development of marine ranching to ensure food safety and improve human health. These efforts also provide opportunities for the restoration of wild fishery stocks, with so far 110 national marine ranches built and distributed along the coast of the Bohai Sea, the Yellow Sea, the East China Sea and the South China Sea. Although fishery restoration efforts have reached unprecedented levels, the evidence suggests that after the depletion of resources, it could be extremely difficult to restore its natural stock. This study highlights that conservation is much more important than restoration for the sustainability of marine biological resources.

Acknowledgements

This research was supported by science and technology project of Zhejiang Province (2017C25004) from Zhejiang Province, China, Key Projects of Philosophy and Social Sciences Research, Ministry of Education (18JZD059) and Ministry of Science and Technology (2019YFD0901305). The data was supported by Fujian Provincial Department of Ocean and Fisheries, China. and thanks to the Observation and Research Station of Marine Ecosystem in the Yangtze River Delta, Ministry of Natural Resources.

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Cite this article as: Ye G, Lin Y, Feng C, Chou LM, Jiang Q, Ma P, Yang S, Shi X, Chen M, Yang X, Sanders C. 2020. Could the wild population of Large Yellow Croaker Larimichthys crocea (Richardson) in China be restored? A case study in Guanjingyang, Fujian, China. Aquat. Living Resour. 33: 24

All Tables

Table 1

Large yellow croaker evaluation index system and weight.

In the text
Table 2

Genetic diversity evaluation results of Large Yellow Croaker (LYC) in different geographical groups by using AFLP.

In the text
Table 3

Some known commercial fishes' AFLP genetic diversity.

In the text

All Figures

thumbnail Fig. 1

Study area, the location of Guanjingyang.
In the text
thumbnail Fig. 2

Annual production of the large yellow croaker from 1956 to 2015 in Guanjingyang, China.
In the text
thumbnail Fig. 3

The Restoration Capacity Index (RCI) of the restoration potential of wild large yellow croaker in Guanjingyang and the performance of Habitat Suitability (HS), Population Status (PS) and Government Social Interventions (GSI) from 1987 to 2015.
In the text
thumbnail Fig. 4

Release of the large yellow croaker juvenile from 1987 to 2015 in Guanjingyang, China.
In the text

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