Fishery Status and Rebuilding of Major Economic Fishes in the Largest Freshwater Lake in China Based on Limited Data

: Poyang Lake, the largest freshwater lake in China, possesses abundant ﬁshery resources, but its ﬁsh stock status is still unclear. In this work, the stock status of and ﬁshing efforts of nine major economic ﬁshes in the Poyang Lake were estimated from 2000 to 2019 with a catch-based maximum sustainable yield (CMSY) model based on catch and resilience data. It was further predicted whether the biomass of those ﬁshes could be restored to support maximum sustainable yield ( B msy ) under the policy of “Ten years ﬁshing moratorium in the Yangtze River”. The results showed that goldﬁsh Carassius auratus , grass carp Ctenopharyngodon idella , and black carp Mylopharyngodon piceus suffered from higher ﬁshing efforts and low biomass in the past 20 years; bighead carp Hypophthalmichthys nobilis , yellow catﬁsh Tachysurus fulvidraco , and common carp Cyprinus carpio responded differently to their ﬁshing efforts; silver carp Hypophthalmichthys molitrix , Amur catﬁsh Silurus asotus , and mandarin ﬁsh Siniperca chuatsi were underexploited. Six species were overﬁshed in 2019, and their biomass would be expected to recover for sustainable exploitation during the ﬁshing moratorium, except for M. piceus . This study provided a case study of feasible freshwater ﬁshery evaluation in limnetic ecosystems.


Introduction
Inland fisheries are characterized by multi-drivers and multi-species [1], providing food and livelihoods for millions of people [2], especially in developing countries. The area of lakes, reservoirs, and wetlands worldwide exceeds more than 12 million km 2 altogether [3], of which lakes contribute a significant proportion to inland fisheries [4,5]. For example, in China, there are more than 2000 natural lakes with an average surface area of more than 1 km 2 and a total area of approximately 80,000 km 2 [6]. The domestic lake fishery experienced three developmental phases: the traditional wild fishery before the 1960s, the rapid growth of fishery production from the 1960s to the mid-1980s, and the fast growth of aquaculture since the mid-1980s [7]. The fishery production increased by 11 times from 75,100 tons in 1979 to 862,300 tons in 2019, with a peak in 2015 at 1,647,800 tons in terms of aquaculture [8,9].
Previous studies on fishery status were mainly based on biological parameters of the targeted fishes, fishing effort, or ecosystem features [10][11][12][13]. Different modeling frameworks require diverse fishery parameters, such as catch and abundance data, CPUE or other fishing effort parameters, and length-based or age-based data [14][15][16][17]. Limited by incomplete data records, selective data collection, and governmental policy prohibition [18], available fishery information might not enable more traditional approaches for estimating stock status in inland waters. Fortunately, the catch-based maximum sustainable yield (CMSY) model, based on fewer fisheries parameters such as catch and resilience of species, was firstly proposed by Martell and Froese [19]. Subsequently, this model was supplemented by Froese et al. [15]. The CMSY model performs well in quantifying maximum sustainable yield (MSY), biomass (B), and other related fishery reference points and have been widely applied to assess stock status [20][21][22][23].
As the biggest inland freshwater lake in China, Poyang Lake, embedded in the middle and lower reaches of the Yangtze River, covers a surface area of more than 3000 km 2 in the wet season [24]. It possessed an affluent fishery with an average catch production of 42,600 tons in the 1990s [25] which then decreased significantly (by as much as half) under multiple stresses [26,27] in the last decade [28]. In addition, some species showed fisheries-induced evolution, characterized primarily by miniaturization and lower age in this lake [29], causing undesirable consequences in fishery resources [30]. The Poyang Lake has significant ecological and socio-economic value [31], thus evaluating the fishery status of the lake becomes imperative for sustainable utilization and management. However, fishery assessment in the Poyang Lake was scarce during the past decades because of limited data availability and the lack of applicable methods. To prevent further depletion of fishery resources, a systematic conservation plan in the Yangtze River was enacted in 2019, which mandated a fishing moratorium in the basin and its major tributaries over the next 10 years [32]. Jiangxi Province, which governs the Poyang Lake, responded to this fishing moratorium law on 21 August 2019, and legitimated that local fishing boats should be banned in the lake area since 2020. Therefore, the questions of interest both for the government and local fishery industry are whether and when local fisheries in the lake can be rebuilt to a sustainable status.
In this study, based on the catch data collected from 2000 to 2019 in the Poyang Lake, we assessed the fishery status of main economic fishes with the CMSY model, aiming to evaluate the historical and current exploitation status of the dominant fishes. We expected different levels of stock status for these fishes and predicted whether over-exploited fishes would respond to the fishing moratorium law and when the biomass of these species could be restored. This work is beneficial in comprehending dynamic variations of fishery resources in Poyang Lake and predicting the efficiency of inland fishing moratorium law on stock recovery.

Study Area
Poyang Lake is located from 28 • 24 to 29 • 46 N and 115 • 49 to 116 • 46 E ( Figure 1) with an average water depth of 7.38 m and mean annual water level of 12.86 m [33]. Both the surface area and the water storage vary seasonally. During the wet season, when the water level of the hydrological station at Hukou is 22.59 m, the floodplains are inundated with a surface area of 4500 km 2 and a storage capacity of 340 × 10 8 m 3 . These metrics dropped to 146 km 2 and 4.5 × 10 8 m 3 in the dry season when the water level at Hukou is 5.9 m [34]. Runoffs attributed to the Yangtze River and upstream tributaries are from the Ganjiang River, Fuhe River, Xiuhe River, Xinjiang River, and Raohe River. The lake's outlet flows into the downstream Yangtze River with an annual runoff of 152.5 km 3 [33]. The climate is a typical subtropical monsoon with an annual precipitation of more than 1000 mm [35].
Poyang Lake provides abundant ecosystem services, such as supplying water and food, offering recreation, and playing important roles in the socio-economic and ecological fields [31,36]. With the economic development, the domestic sewage and industrial wastewater from the upstream rivers flowed into the lake. The numerous heavy metals and nutrition with nitrogen and phosphorus degraded water quality and led to fishery collapse in Poyang Lake [31,37]. In addition, some anthropogenic activities such as dam construction and navigation have also disturbed the growth of aquatic organisms [35]. such as cages and gill nets [40] also accounted for the decrease of fish resources. To alleviate these pressures, a series of fishing regulations were implemented before the ten years fishing moratorium. For example, a few legal fishing tools were allowed, such as angling for recreation and entertainment; fishing nets with meshes smaller than the specified minimum size, e.g., the mesh size of the dragging gillnet should be greater than 100 mm [41].

Fish Data
Catch data were provided by the Jiangxi Fisheries Research Institute and extracted from other published literature, including Qian et al. [25] and Huang and Gong [26]. Twenty years of catch records from 2000 to 2019 were compiled. Nine fishes were selected for assessment based on their economic importance, including goldfish Carassius auratus, grass carp Ctenopharyngodon idella, common carp Cyprinus carpio, silver carp Hypophthalmichthys molitrix, bighead carp Hypophthalmichthys nobilis, black carp Mylopharyngodon piceus, Amur catfish Silurus asotus, Mandarin fish Siniperca chuatsi, and There was a maximum of 136 fishes according to an investigation of Poyang Lake in the last century [38], whereas only 89 fishes were discovered in 2013, and these species were characterized primarily by miniaturization and lower age [29]. Most of them were cyprinid fishes, contributing to 52.2% and 53.9% of total species, respectively. High fishing pressure was the main factor that caused the decline of fish diversity and resources. The average number of fishermen engaged in the fishing industry was 55,000, and the number of vessels was about 20,000 from 2000 to 2019 [39]. Development of various fishing tools such as cages and gill nets [40] also accounted for the decrease of fish resources. To alleviate these pressures, a series of fishing regulations were implemented before the ten years fishing moratorium. For example, a few legal fishing tools were allowed, such as angling for recreation and entertainment; fishing nets with meshes smaller than the specified minimum size, e.g., the mesh size of the dragging gillnet should be greater than 100 mm [41].

Fish Data
Catch data were provided by the Jiangxi Fisheries Research Institute and extracted from other published literature, including Qian et al. [25] and Huang and Gong [26]. Twenty years of catch records from 2000 to 2019 were compiled. Nine fishes were selected for assessment based on their economic importance, including goldfish Carassius auratus, grass carp Ctenopharyngodon idella, common carp Cyprinus carpio, silver carp Hypophthalmichthys molitrix, bighead carp Hypophthalmichthys nobilis, black carp Mylopharyngodon piceus, Amur catfish Silurus asotus, Mandarin fish Siniperca chuatsi, and yellow catfish Tachysurus fulvidraco. These nine fishes contributed 64.7% to 89.9% to the total catch production annually in the Poyang Lake during the recent two decades. Among them, the species C. carpio contributes the highest to the total annual catch, reaching 36.78% on average, followed by S. asotus and C. auratus which contributes 13.61% and 10.68%, respectively. The average contributions of other species are all lower than 10%. They are T. fulvidraco  Table S1, including the age of first sexual maturity, the life-history strategies, and the environmental adaptability.

CMSY Model
Theoretically, temporal fishery catch is highly correlated to yield, biomass, and productivity. The CMSY method uses the catch production and resilience of stocks to assess biomass based on the following equation: where B t and B t+1 are the biomass in t year and t+1 year, respectively, C t is the catch in t year, parameter r is the maximum intrinsic rate of population growth, and k indicates carrying capacity or unexploited stock size. Relationships between different biomass in two successive years, population growth rate, carrying capacity, and catch are reconstructed by the k assumes a linear recruitment decline below half of the B msy [15]. Furthermore, we assume that the largest catch of each stock in a time series should be lower than the unexploited stock size k to make the prior range of k more reasonable.
Biological parameters of fishery resources play critical roles in assessing population status and different degrees of fishing mortality [42]. We used 20 years of catch data per species and combined prior ranges for the r, k, and the relative biomass (B/k) at the beginning and the end year to output reference points and further evaluate stock status. The equation r ≈ 3K was used to determine the ultimate parameter r, where K is the parameter of the Von Bertalanffy somatic growth equation, combined with prior r ranges based on different resilience of species, i.e., High (0.6-1.5), Medium (0.2-0.8), Low (0.05-0.5) and Very low (0.015-0.1) [15,43]. The prior range of k for assessed stocks with low prior biomass in the end year can be determined with the equations: k low = max(C) where k low and k high are the lower and upper bounds of the prior range of k respectively, max(C) is the maximum catch in the time series, r low and r high are the lower and upper bounds of the prior range of r respectively. In addition, the equations: k low = 2max(C) r high and k high = 12max(C) r low , were used to acquire the prior range of k for assessed stocks with high prior biomass. For realistic outputs from the CMSY model, probability distributions of parameters r and k were estimated by JAGS software [44]. Due to the lack of research data on the historical exploitation status of fishes in Poyang Lake, the prior range of relative biomass B/k at the beginning and the end year depended on the ratio of catch per species relative to its maximum catch in a time series [19,45]. Although this process can result in slight bias, it is still a reasonable method when these parameters are limited. A detailed description of R code, equations, and theoretical backgrounds for the CMSY model was given by Froese et al. [15].
Based on the above-mentioned biological parameters, available indices B/B msy (the ratio of observed biomass to biomass compatible with MSY) and F/F msy (the ratio of fishing mortality to fishing mortality compatible with MSY) were estimated. A value of F/F msy greater or lower than 1 indicates a high and low fishing pressure, respectively. According to the values of B/B msy , a detailed standard was applied to categorize the stock status: B/B msy > 1.0, healthy; 0.8 < B/B msy ≤ 1.0, slightly overfished; 0.5 < B/B msy ≤ 0.8, overfished; 0.2 < B/B msy ≤ 0.5, severely overfished; 0 < B/B msy ≤ 0.2, collapsed [46].

Fisheries Rebuilding
Based on fishery reference points B/B msy and F/F msy , the biomass of nine fish under two exploitation scenarios was predicted to determine future stock status. Under the scenario of a fishing moratorium for ten years, fishing mortality was assumed to approximate to 0 (i.e., minimal F allowed for scientific research or something similar), and values of F/F msy are also 0, which was considered as non-fishing pressure (NFP) scenario. Rebuilding of a stock will be complete when its biomass recovers to its B msy in the NFP scenario by the where ∆t is the time in years to reach B msy , B is the biomass in the last year, and other parameters are defined above. Assuming the same fishing pressure in 2019 during the next ten years, which was considered as the current fishing pressure (CFP) scenario, the effects of current fishing efforts on stock status were predicted. Population biomass and stock status in the next year are thus evaluated by the following equations [47]: where B t and B t+1 are the biomass in t year and t+1 year, respectively; F t is fishing mortality in t year. B msy was assumed to be constant during the process of rebuilding.

Exploitation Status of Main Economic Fishes
The dynamic catch production of nine fishes and their MSY estimates during the past 20 years are shown in Figure  scenario of a fishing moratorium for ten years, fishing mortality was assumed to approximate to 0 (i.e., minimal F allowed for scientific research or something similar), and values of F/Fmsy are also 0, which was considered as non-fishing pressure (NFP) scenario. Rebuilding of a stock will be complete when its biomass recovers to its Bmsy in the NFP scenario by the equation , where Δt is the time in years to reach Bmsy, B is the biomass in the last year, and other parameters are defined above. Assuming the same fishing pressure in 2019 during the next ten years, which was considered as the current fishing pressure (CFP) scenario, the effects of current fishing efforts on stock status were predicted. Population biomass and stock status in the next year are thus evaluated by the following equations [47]: < 0.5 where Bt and Bt+1 are the biomass in t year and t+1 year, respectively; Ft is fishing mortality in t year. Bmsy was assumed to be constant during the process of rebuilding.

Exploitation Status of Main Economic Fishes
The dynamic catch production of nine fishes and their MSY estimates during the past 20 years are shown in Figure   Estimated biological parameters and reference points for these nine fishes are listed in Table 1. Exploitation levels for species C. auratus (F/Fmsy = 0.94), C. carpio (F/Fmsy = 0.80), Estimated biological parameters and reference points for these nine fishes are listed in Table 1  fishing pressure in different years; group 4, including species H. molitrix, S. asotus, and S. chuatsi, showing higher biomass (B/B msy > 1) but low fishing pressure (F/F msy < 1) in most years.

Fisheries Rebuilding
Predictions of exploitation status in 2030 are shown in Table 2. Under the NFP scenario during the fishing moratorium, the biomass of all fishes would increase rapidly

Fisheries Rebuilding
Predictions of exploitation status in 2030 are shown in Table 2. Under the NFP scenario during the fishing moratorium, the biomass of all fishes would increase rapidly by 2030. The five over-exploited fishes would recover in different years (B/B msy > 1), such as S. asotus in 2021, H. nobilis in 2022, T. fulvidraco in 2023, C. auratus in 2023, and C. idella in 2026. However, the biomass of M. piceus could not recover its B msy by the end of 2030. Under the CFP scenario in 2030, C. auratus and M. piceus would be healthier than in 2019, C. carpio, S. chuatsi, and T. fulvidraco would remain stable, and the levels of the remaining species would become worse or even collapse ( Table 2). Note: "NA" shows the status of species is healthy in 2019 without recovery.

Historical Status of Main Economic Fishes
Fishing effort is one of the determining factors that affect the fishery resources of the lake [1,[48][49][50]. Under high fishing pressure, stock assessment and managements are in difficulty due to abuse of fishing gears and fishing methods in developing countries or other impoverished regions [51]. Based on habitat conditions and biological characteristics of different fishes, people invented various fishing tools and techniques. Previous studies indicated the use of more than 40 fishing tools in Poyang Lake, such as fish spears, gill nets and trawl nets [38]. Fishing pressure on different fish resources was divergent because of varying fishing gears and efforts, thus the status of these nine fishes in Poyang Lake was classified into four groups. Group 1, including species C. auratus, C. idella, and M. piceus, suffered from high fishing pressure (F/F msy > 1) and dropped in biomass (B/B msy < 1) in the past years. These three fishes were also subject to the high fishing pressure in the inland waters of Asia based on the catch data from the FAO [52]. The biomass of the last two species has been declining for at least two decades. They show low r [43] and late age of maturation [53], which limited their ability to recover to a sustainable level. C. auratus has a low growth rate and fecundity [53,54], causing difficulty with recovery. Particularly, the species C. auratus, one of the primary fishing target species in Poyang Lake, has high catch production and nutritional value [40,55], which have accelerated the overexploitation of this species and led to an unhealthy status.
Group 2, including species H. nobilis and T. fulvidraco, suffered from low to high fishing pressure, accompanied by healthy to poor stock status. The biomass of these two species was high in the initial years. The species H. nobilis has a high intrinsic rate of population increase (r = 0.64), which is beneficial to the resistance of species to overexploitation [43] and recovery of biomass after destroying the population resources. The species T. fulvidraco is an equilibrium strategist with parental care, enhancing the survival rate of the offspring [54]. This species exhibits multiple-batch spawning and has strong adaptability [56] to accelerate population recruitment. However, their biomass also declined in Poyang Lake under intensive fishing pressure in the subsequent years. The species H. nobilis and T. fulvidraco with high edibleness are easily subjected to higher fishing pressure because of increased demand for aquatic products, causing the catch production to be higher than the population recruitment.
The species C. carpio was classified in group 3 and went through healthy-bad-healthy status in the past. The catch production was the highest in Poyang Lake, ranging from 25.6% to 42% during the recent two decades. Though it was exposed to high fishing pressure, its potential high biomass may make this species resistant the risk from overexploitation. In addition, its relatively high r (r = 0.59), low late age of maturation, and strong adaptability to environmental stress may account for the healthy status in several years [53]. Moreover, the wide feeding habits of C. carpio could help it maintain a higher survival rate than species with simple food sources when the food resources are reduced due to water pollution.
Group 4, including species H. molitrix, S. asotus, and S. chuatsi, was subject to low fishing pressure (F/F msy < 1) but had high biomass (B/B msy > 1). Despite the fact the last two species have the high trophic level, their stock status was only slightly influenced by fishing activities. Both these two species are demersal fish, but they prefer rocky habitats, which suggest they are difficult to capture by fishing practices such as bottom trawling [57,58]. In addition, multiple spawning in a year [59,60] helps their population growth. Since 2007, a protection plan for S. chuatsi in Poyang Lake was issued [61], further stifling the resource decline. The species H. molitrix has lower economic value and less palatability compared to the other four major domestic carps, and therefore is a less desirable catch. Meanwhile, the highest population growth rate (r = 0.67) among these nine fishes supported its strongest resilience and resistance to similar fishing pressures. Since 2002, a series of measures were executed in Poyang Lake to slow down the reduction of the fisheries, including the policy of a closed fishing season in the spring and artificial reproduction and releasing [27]. These measures allowed this species enough time to recover the biomass in the early stage, thus the rate of population recruitment exceeded the fishing mortality resulting from human fishing activities.
Even if some measures were applied to recover poor fishery resources, it is also challenging to bring them back to a healthy status, indicating the impact of potential threats other than overfishing on fishery production [62]. For example, dam construction on the rivers upstream of Poyang Lake has significantly disturbed fish growth, including destroying the spawning grounds of migratory fishes and impeding their migration channels. In another instance, reclaiming land from the lake has resulted in a decline of large areas of aquatic vegetation [63,64], reducing the food resources for herbivorous fish such as the species C. idella, and disturbing the spawning substrates of species like C. auratus and C. carpio that lay sticky eggs, leading to little population recruitment for these fishes. Other factors, such as water pollution [36] and sand excavation [65], were possibly associated with natural fish mortality by altering the habitat environment and irregular catch activities in the lake. Therefore, policymakers need to manage these human activities and protect the habitat environment as crucial as reducing human fishing efforts with relevant measures.

Rebuilding of Fish Stocks
Rebuilding activities of global fisheries have mainly concentrated on marine fisheries [66,67], whereas little efforts are devoted to inland freshwater systems. Predictions under the NFP scenario suggested that stocks of those over-exploited species in 2019 would recover their levels of B msy except the species M. piceus if the fishing moratorium law is followed, indicating that main fisheries in Poyang Lake could be recoverable with proper Under the NFP scenario, five fishes that have poor stock status would recover to a biomass level that produces the maximum sustainable yield, including the species S. asotus, H. nobilis, C. auratus, T. fulvidraco, and C. idella. The results suggest that the recovery rates of different species were mainly dependent on their biological characteristics and stock status in 2019. The species H. nobilis, characterized by periodic strategy, large-bodied size, and high r [54], showed the highest recovery rate and healthy status in 2022. The status of both species C. auratus and T. fulvidraco will be healthy in 2023, but the former has a higher recovery rate (former: 13.65%; latter: 12.91%). Human activities, such as hydraulic engineering and sand excavation, influenced the hydrologic conditions and water qualities of Poyang Lake in the past [27]. In turbulent habitats, C. auratus inhabiting frequently disturbed environments [54] showed rapid recovery from severely overfished to a healthy status, while T. fulvidraco, sensitive to changeable currents [43], was slower in its resource recovery. The stock status of C. idella was outside of safe biological limits (B/B msy < 0.5) in 2019, forcing it to require more time to recover its population resources. Compared with the other fishes, the status of S. asotus with strong environmental adaptability [70] was slightly overfished in 2019 and can recover to healthy status quickly under fishing closure. The biomass of these fishes can recover to a healthy status, which should help facilitate fishery activity in Poyang Lake and generate more economic value.
The results show that the status of four species would be worse under the CFP scenario, even going from healthy to overfished status in the case of species like H. molitrix. This is because the F/F msy value of these fish is greater than 1 in 2019, and their biomass will decline if fishing efforts are kept at the same exploitation levels during the next ten years. In contrast, the fishing pressure of both species C. auratus and M. piceus were low in 2019, and their stock status in 2030 will be healthier than that in 2019. Therefore, under sustainable exploitation levels (F < F msy ) rather than high fishing pressure, the stocks are expected to be rebuilt if the fishing moratorium could be extended. This suggests that it may provide an opportunity for scientific research with suitable fishing efforts in the next few years, without prominently affecting fishery resources in Poyang Lake.

Conclusions
This study quantifies the stock status of the nine dominant economic fishes in the Poyang Lake using the CMSY model based on limited data. Almost half of them experienced high fishing pressure (F > F msy ) in the past two decades, and two-thirds of stocks were in different levels of overfished in 2019, indicating the primary fish resources in the Poyang Lake might be declining. However, the biomass of five overfished fishes would likely recover to a healthy status (B > B msy ) under the policy of ten years fishing moratorium in the Yangtze River, suggesting reasonable management measures would benefit the sustainable development of fisheries. In the future, more fishery organisms, relevant biological parameters, and assessed models should be combined to assess the lake fisheries comprehensively.
Supplementary Materials: The following are available online at https://www.mdpi.com/article/10.3 390/fishes7010047/s1, Table S1: The biological information of nine fishes in the Poyang Lake [71][72][73].  Institutional Review Board Statement: The data of this research was extracted from the literature and the official statistics.

Data Availability Statement:
The data that support the findings of this study are available with permission from the authors.