Sea of Japan large marine ecosystems

Author’s Accepted Manuscript Exploitable carrying capacity and potential biomass yield of sectors in the East China Sea, Yellow Sea, and East Sea/Sea of Japan large marine ecosystems Chang-Ik Zhang, Young-Il Seo, Hee-Joong Kang, Jung-Hyun Lim www.elsevier.com/locate/dsr2

PII: DOI: Reference:

S0967-0645(18)30067-5 https://doi.org/10.1016/j.dsr2.2018.11.016 DSRII4533

To appear in: Deep-Sea Research Part II Received date: 6 April 2018 Revised date: 19 November 2018 Accepted date: 19 November 2018 Cite this article as: Chang-Ik Zhang, Young-Il Seo, Hee-Joong Kang and JungHyun Lim, Exploitable carrying capacity and potential biomass yield of sectors in the East China Sea, Yellow Sea, and East Sea/Sea of Japan large marine e c o s y s t e m s , Deep-Sea Research Part II, https://doi.org/10.1016/j.dsr2.2018.11.016 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting galley proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

Exploitable carrying capacity and potential biomass yield of sectors in the East China Sea, Yellow Sea, and East Sea/Sea of Japan large marine ecosystems Chang-Ik Zhanga, Young-Il Seob, Hee-Joong Kangb, Jung-Hyun Lima,* a

Department of Marine Production System Management, Pukyong National University, Busan 48513, Republic of Korea

b

Fisheries Resources Management Division, National Institute of Fisheries Science, Busan 46083, Republic of Korea

* Corresponding author. Tel.: +82-51-629-5892; fax: +82-51-629-5886. E-mail address: [email protected] (J.H. Lim)

ABSTRACT Many fisheries resources in large marine ecosystems (LMEs) of Northeast Asia have become depleted due to overfishing, marine environmental degradation, and other unknown factors. In addition, the quality of coastal ecosystems has been degraded. Although a variety of approaches has been applied to improve the management of fisheries and to facilitate the recovery of depleted fisheries resources in Korea, they have not been wholly successful due to a lack of information on the history of fishing, exploitable biomass, and the current state of fisheries, compared to reference points, such as exploitable carrying capacity (ECC) and potential biomass yield (PBY). In this study, we reviewed the ECC and PBY of sectors in the East China Sea, Yellow Sea, and East Sea/Sea of Japan LMEs using the ecosystem modeling method (EMM) and holistic production method (HPM). EMM uses a mass-balanced ecosystem model, Ecopath with Ecosim, together with fishery catch and ecological data for each species group. HPM utilizes time-series catch and fishing effort data for all species combined. Estimates of the ECC for sectors in the East China Sea, Yellow Sea, and East Sea/Sea of Japan LMEs from these two approaches were similar with values 5.49–6.42 million metric tons (mmt), 1.35–1.36 mmt, and 1.42– 1.81 mmt, respectively. Estimates of PBY were also similar for the two approaches with values 1.02–1.03 mmt for the East China Sea, 0.18–0.26 mmt for the Yellow Sea, and 0.27–0.34 mmt for the East Sea/Sea of Japan. The exploitable biomass began to decline from the early 1970s in the Yellow Sea and the mid-1970s in the East Sea/Sea of Japan and East China Sea, when over-fishing commenced. The current exploitable biomass for the LMEs are about 30-40% of those of the late 1960s. The ecosystem risk index (ERI) was highest for the Yellow Sea at 2.17, while the ERI was 1.95 for the East China Sea and 1.87 for the East Sea/Sea of Japan. Finally, we introduce a practical approach to achieve sustainable ecosystem-based fisheries assessment and management in 1

LMEs, since most commercially important fisheries include species that migrate seasonally across the national boundaries of Korea, Japan, and China.

Keywords: Exploitable carrying capacity; Potential biomass yield; Exploitable biomass; Ecosystem-based fisheries assessment and management; Large marine ecosystems

1. Introduction Large marine ecosystems (LMEs) in Northeast Asia are highly biologically productive areas, and comprise important spawning grounds for demersal and pelagic fishes, regions of aquaculture production, areas of threatened marine mammals, and many other biological resources that need protection (Huh et al., 1992). However, the fishing industry in this area has always been highly competitive. The market demand for fishery products is constantly increasing with the increase in human population, and the most important commercial fish stocks are depleted to some degree due to increasingly intensive fishing. Furthermore, fish has always been an important source of human food around coastal areas. Marine capture fisheries play a substantial role in the total global fishery output and the number of people employed in the fishing industry. LMEs in Northeast Asia are located less than 400 nautical miles from Korea, China, and Japan. Most commercially important fishery resources in waters adjacent to Korea include species that migrate seasonally across national boundaries and are shared by Korea, Japan, and China. Competition between these countries has resulted in heavy exploitation of most economically valuable species. Therefore, negotiation of fishing ground boundaries between these countries was inevitable based on the United Nations Convention on the Law of the Sea (UNCLOS). However, there are only bilateral agreements among each of the three countries in managing fisheries and their resources. Most of the highly exploitable species (about 30% of total catch) have been over-fished over the last four decades (Zhang, 2014). The advancement of fishing technology and the development of large vessels led to overfishing of fisheries resources and degradation of environmental condition. As a result, the catch of coastal fisheries is gradually decreasing and the ecosystem is deteriorated in the East China Sea, Yellow Sea, and East Sea/Sea of Japan. To effectively manage fisheries resources, it is necessary to understand the exploitable carrying capacity (ECC) and potential biomass yield (PBY) of LMEs to clarify available resources in the future. The ECC and PBY are also essential criteria for establishing reference points for ecosystem-based resource assessments (Zhang et al., 2009). However, there have been few studies of ECC and PBY in these LMEs.

2

In general, the carrying capacity (CC) of an environment indicates the maximum equilibrium population biomass to which the population will approach in the absence of interference (Gulland, 1983). Odum (1997) also defined CC as the maximum group size that could be sustained indefinitely without reduction of productivity or sustainability within the ecosystem. Recently, Zhang et al. (2017) defined ECC as the portion of CC that is exploitable by fishing. Conversely, maximum sustainable yield (MSY), which is conveniently referred as the potential yield (PY), estimates how much could be extracted annually (Gulland, 1983), and provides the greatest theoretical yield of a marine ecosystem. Hilborn and Walters (1992) defined MSY as the highest equilibrium catch that can be continuously taken from a stock. MSY is also defined as the acceptable biological limit of fisheries resources currently being used or that will become available from living organisms in a unit of sea area (Shin, 2009). Kim (2016) defined PY as the annual maximum sustainable yield from ECC biomass. In this study, the term PBY is used instead, and is defined as the maximum biomass of sustainably exploitable species or species group in a marine ecosystem prior to the exploited state. There are two approaches for estimating ECC: ecosystem dynamics analysis and production-based analysis. Ecosystem dynamics analysis uses the Ecopath with Ecosim (EwE) model, which is a mass-balanced model that uses the prey-predator relationship to estimate the ECC of an ecosystem. The ECC is the biomass when total respiration is equal to the sum of primary production and detritus inflow (Christensen and Pauly, 1998). Vasconcellos and Gasalla (2001) estimated the ECC of marine ecosystems in southern Brazil, and more recently Lee (2014) estimated the ECC for the Korean sector of the Yellow Sea LME. In production-based analysis, ECC is estimated using time-series catch and fishing effort data by applying surplus production models. Pyo (2006) conducted a comparative analysis of production-based methods to estimate the ECC of anchovy stock in Korean waters. Approaches for estimating PBY can be also divided into two groups like those for ECC. There are two methods for estimating PBY in ecosystem dynamics analysis. The first utilizes information on primary production, the number of trophic levels, and the ecological efficiency of ocean provinces to estimate potential yield (Ryther, 1969), based on the assumptions that PBY is affected by the energy transfer efficiency and length of the food chain, and that a complex food web could be represented by a simple chain with certain length. However, since PBY is very sensitive to violations of these assumptions, it potentially includes a large amount of uncertainty (Alverson et al., 1970). In particular, the estimates for transfer efficiency tend to vary spatially and ecologically (Libralato et al., 2008) and could change with ecological exploitation (Coll et al., 2009a, b). The second method is ecosystem dynamics modeling, which estimates PBY by analyzing the variation in 3

organisms over time using a mass-balanced model. For example, PBY has been estimated by evaluating the ecological interactions with major components of the ecosystem (Christensen and Waters, 2004; Lee, 2014). Production-based analysis to estimate PBY can be divided into two methods. The first method estimates the PBY by extrapolating from the catch trend or by extrapolating catch per unit area; however, it does not estimate PBY for unused or unknown resources (Gulland, 1971). Garcia and Newton (1997) estimated PBY (MSY) for selected species in world capture fisheries, using a simple surplus production model (Fox model; Fox, 1974) with a nonlinear relationship. Kim (2016) estimated PBY in the Korean sector of the Yellow Sea using production-based analysis. The second method uses life history characteristics of ecosystems and fisheries when there is insufficient data to estimate PBY; however, it carries a greater risk of error by using multiple assumptions to estimate PBY (Beddington and Kirkwood, 2005). The objectives of this study are to describe the characteristics of fisheries, their productivity, and the status of exploitable biomass of sectors in the East China Sea, Yellow Sea, and East Sea/Sea of Japan LMEs, to review ECC and PBY of three LMEs, and to suggest an ecosystem-based fisheries assessment approach for recovering depleted fish stocks and managing sustainable fisheries in the LMEs.

2. Characteristics of three LMEs LMEs in the East China Sea, Yellow Sea, and East Sea/Sea of Japan are dominated by the Tsushima Warm Current, which is a branch of the Kuroshio Current (Fig. 1a) that brings warm water into the area (Kim and Kang, 1998). Although LMEs should be distinguished by factors such as oceanographic features, ecological factors, exclusive economic zones (EEZ), and fishery management districts, in practice it is difficult to set clear boundary points (Seo, 2011). Until now, there has been no objectively established boundaries between the Korean LMEs in the East China Sea, Yellow Sea, and East Sea/Sea of Japan. In this study, the boundaries of the three LMEs were based on the fisheries management districts, ecological characteristics, and fisheries data availability (Fig. 1b), since it would be useful to utilize established bio-statistical data more effectively in fisheries assessment and management. The East China Sea is a shelf area in the west near the continent, however, it also has the Okinawa Trough, which is greater than 2,000 m deep at its southern section and less than 1,000 m at its northeastern section (Fig. 1a) (PICES, 2004). The East China Sea is affected by the main Kuroshio Current and short- and long-term changes in the circulation are anticipated (PICES, 2004). Surface circulation in the East China Sea mainly consists of the Kuroshio and Tsushima Warm Currents. The Kuroshio Current enters the East China Sea and 4

flows northeastward along the shelf slope and branches into the Tsushima Strait. The East China Sea is very productive and borders the Korean peninsula and Japan, with several demersal species seasonally migrating between the East China Sea and Yellow Sea (Kim, 2003). Two types of fishery targeting pelagic species operate in the East China Sea. One is the large, powered, purse-seine fishery that catches mostly chub mackerel (Scomber japonicus), and the other is a drag-net fishery that only targets anchovy (Engraulis japonicus). These two fisheries accounted for more than 40% of the total catch in this LME from 2012–2016. Another important fishery was the large, powered otter trawl, which accounted for a further 10% of total catch. The fishery production of the East China Sea was the highest, accounting for about 70% of the total catch of the three LMEs (Table 1a). Catch per unit area (3.65 mt/km2) was also the highest in the East China Sea. Anchovy was the most important species in this LME, followed by chub mackerel, common squid (Todarodes pacificus), hairtail (Trichiurus lepturus), Spanish mackerel (Scomberomorus niphonius), yellow croaker (Larimichthys polyactis), and horse mackerel (Trachurus japonicus), which accounted for about 70% of the total catch of the Korean sector in the East China Sea (Table 1b). In the East China Sea, fisheries resources are heavily exploited, with about 200 species of fishes and invertebrates being exploited commercially (Liang et al., 2018). The Yellow Sea is a semi-enclosed sea surrounded by China and Korea and has a shallow shelf with an average depth of 44 m (Fig. 1a). The Yellow Sea has turbid water, low salinity, and strong tidal interactions (Kim and Khang, 2000). The main current driving regional circulation is the Kuroshio, although the Tsushima Warm Current is still dominant (PICES, 2004). The jagged coastlines and multiple islands of this sea harbor diverse habitats. The Yellow Sea has several types of tidal mudflats that provide important food and ecological environments for a diverse array of organisms. Thus, this sea has high productivity and biodiversity. About 200 fishes are found in the Yellow Sea, including warm-water (45%), warm-temperate (46%), and cold- temperate species (9%) (Zhang et al., 1988). The fish populations include resident species near coastal waters and migratory species that have distinct seasonal movements (Sherman and Tang, 1999). The Yellow Sea is a typical warm temperate zone and its species composition shows obvious seasonal variation (Liang et al., 2018). The Yellow Sea ebbs and flows according to local geographical characteristics. A variety of fisheries using stationary fishing gears have been developed in this LME. The main fishery is the offshore stow-net fishery, which accounts for approximately 25% of the total catch in the area, followed by the coastal gill-net fishery (11%), coastal pot fishery (10%), and coastal stow-net fishery (9%). The average catch from 2012–2016 was the 5

lowest among the three Korean LMEs at 0.12 mmt (Table 1a). Major fishery species in the Yellow Sea over the last 5 years included anchovy, blue crab (Portunus trituberculatus), oysters (Ostreidae spp.), and Japanese littleneck (Tapes philippinarum) (Table 1b). The average catch of the top 10 species accounted for about 70% of the total Korean catch in the Yellow Sea. The East Sea/Sea of Japan is also a semi-enclosed sea surrounded by Korea, the coast of Russia, and Japan (Fig. 1a). This sea is connected to the East China Sea, the North Pacific Ocean, and the Sea of Okhotsk via the Korea Strait, Tsugaru Strait, and Soya Strait, respectively, and has an average depth of 1,500 m. The East Sea Proper Water has a depth of 300 m or less, a temperature of 0–1 °C, and salinity of 33.96–34.14‰, and constitutes about 80% of the total volume of the East Sea/Sea of Japan (Yasui et al., 1967). The boundary of the East Sea/Sea of Japan is where the Tsushima Current meets the North Korea Cold Current, and productivity is high where the clear warm water meets the nutrient-rich cold water (Raymont, 1980). Hence, both cold and warm water species occur, resulting in a wide variety of fishes. In the northern part of the East Sea/Sea of Japan, there are many cold-water demersal fishes, while in the southern part there are many warm-water pelagic fishes, and most live and seasonally migrate between the coast and the continental slope. In the East Sea/Sea of Japan, the average catches from 2012–2016 were 22% for the offshore pot fishery, 19% for the eastern sea trawl fishery, 16% for the offshore angling fishery, and 11% for the coastal gill-net fishery, which together accounted for approximately 80% of the total Korean catch. In particular, catches by offshore pot and angling fisheries, that mainly target dominant species, such as red snow crab (Chionoecetes japonicus) and common squid, were high. The average catch from 2012–2016 was small at 0.18 mmt (17%); however, catch per unit area was the lowest of the three LMEs at 1.13 mt/km2 (Table 1a). As shown in Table 1b, major fishery species in the East Sea/Sea of Japan included common squid, red snow crab, Pacific herring (Clupea pallasii), and sandfish (Arctoscopus japonicus). The average catch of the top 10 species accounted for about 85% of the total catch in the East Sea/Sea of Japan, while the average catch of common squid accounted for about 40%.

3. Exploitable Carrying Capacity (ECC) 3.1 Methods for estimating the ECC Two approaches were used to estimate ECC of Korean sectors in the East China Sea, Yellow Sea, and East Sea/Sea of Japan LMEs. The first analyzed ecosystem dynamics using the ecosystem modeling method (EMM). The second used the holistic production method (HPM). The EMM uses a mass-balanced ecosystem model, EwE, with fishery catch and a variety of ecological data for each species group. The basic equation of the mass6

balanced model for EwE is as follows: 𝑛

𝐵𝑖 (𝑃/𝐵)𝑖 = 𝑌𝑖 + ∑ 𝐵𝑗 (𝑄/𝐵)𝑗 𝐷𝐶𝑗𝑖 + 𝑀0 𝐵𝑖 𝑗=1

where, 𝐵𝑖 is the biomass of species or species group 𝑖 for a specific period; (𝑃/𝐵)𝑖 is the production/biomass ratio of 𝑖, which is equal to instantaneous total mortality (𝑍𝑖 ) at equilibrium (Allen, 1971); 𝑌𝑖 is the catch of 𝑖; 𝐵𝑗 is the biomass of the consumer or predator; (𝑄/𝐵)𝑗 is the consumption per unit biomass of predator 𝑗; and 𝐷𝐶𝑗𝑖 is the portion of 𝑖 as prey of predator 𝑗. Therefore, the total consumption (𝑄𝑗𝑖 ) consumed by predator 𝑗 during a specific period can be expressed as 𝑄𝑗𝑖 = 𝐵𝑗 (𝑄/𝐵)𝑗 𝐷𝐶𝑗𝑖 . 𝑀0 is a mortality coefficient, except for death due to fishing or feeding. In this analysis, the converged value of the Ecosim simulation from setting fishing mortality (F) to zero was regarded as the ECC of each group. The HPM utilizes time-series catch and fishing effort data from 1966–2016 for all species combined. Based on Garcia and Newton (1997), a surplus production approach for combined species using the maximum entropy (ME) model (Golan et al., 1996) was used to estimate the ECCs for the three LMEs. The basic equation for the ME model is as follows: 𝐶𝑡 = 𝑞𝐸𝑡 𝐵𝑡 𝑒𝑥𝑝(𝜀𝑡 ) 𝐵𝑡+1 = [𝐵𝑡 + 𝑟𝐵𝑡 (1 −

𝐵𝑡 ) − 𝐶𝑡 ] 𝑒𝑥𝑝⁡(𝜇𝑡 ) 𝐾

where, 𝐶𝑡 is total catch in year 𝑡; 𝑞 is catchability; 𝐸𝑡 is fishing effort in year 𝑡; 𝐵𝑡 is biomass in year 𝑡; 𝑟 is intrinsic rate of natural increase; 𝐾 is ECC; 𝑟𝐵𝑡 (1 − 𝐵𝑡 /𝐾) is natural increment; 𝜀𝑡 is observation error for catch in year 𝑡; and 𝜇𝑡 is process error for biomass in year 𝑡. ECC can be estimated using the following equation: 𝐸𝐶𝐶 = 𝑝1𝐸𝐶𝐶 ∙ 0 + 𝑝2𝐸𝐶𝐶 ∙ ℎ/2 + 𝑝3𝐸𝐶𝐶 ∙ ℎ⁡ where, ℎ represents the maximum range of probability 𝑝 of each parameter to be estimated. Detailed estimation methods of the ECC, including setting the initial values, are described in Zhang et al. (2017) and Lim (2018). BPBY is biomass needed to achieve the PBY level and is estimated as 𝐵𝑡 when the term 𝑟𝐵𝑡 (1 − 𝐵𝑡 /𝐾), related to surplus production, is maximized in the equation representing the annual biomass above. 3.2 ECC of three LMEs 3.2.1 East China Sea LME The ECC of the Korean sector in the East China Sea LME was 5.49 mmt using EMM and 6.42 mmt using HPM (Table 2 and Fig. 2a). Ecologically and commercially important species, such as anchovy, chub mackerel, 7

common squid, hairtail, and Spanish mackerel, were listed separately as independent groups. Demersal fish represented the most abundant group with more than 2.3 mmt, followed by predator pelagic fish, cephalopods, small pelagic fish, and epifauna (Table 2). Hairtail was the most important species and croakers and flounders were also important in this demersal fish group. ECC of predator pelagic fish was the highest at more than 1 mmt, and chub mackerel and Spanish mackerel were the dominant species in the predator pelagic group. Common squid was also an abundant species with more than 0.5 mmt of ECC. Anchovy was the dominant small pelagic species, accounting for about 75% of the estimated ECC. Annual biomass decreased continuously after a peak of 4.33 mmt in 1973, and began to decline below BPBY (3.21 mmt) as fishing intensity increased in the early 1980s (HPM analysis) (Fig. 2a). Consequently, fish stocks in the East China Sea LME have been overfished since 1981. The current biomass is at a low level of 1.67 mmt, which is about half of the biomass required to achieve PBY (BPBY) level. 3.2.2 Yellow Sea LME ECC of the Korean sector in the Yellow Sea LME estimated using EMM was 1.35 mmt, which was very similar to the 1.36 mmt estimated using HPM (Table 2 and Fig. 2b). In the Yellow Sea LME, ecologically and commercially important species were listed independently from those in the East China Sea LME. Anchovy, chub mackerel, common squid, Pacific cod, and blue crab were included in this group. Demersal fish were the most abundant, followed by infauna and epifauna, which reflected the nature of the wide tidal flats with abundant benthos, such as clams and oysters (Table 2). Rays were distinctly abundant with an ECC of 0.14 mmt. As shown in Fig. 2b, the annual biomass decreased continuously after a peak of 1.20 mmt in 1967. Biomass has continuously decreased below BPBY (0.68 mmt) since the late 1980s. Accordingly, fish stocks have been overfished since 1988. Biomass is currently 0.38 mmt, which is about 56% of BPBY. 3.2.3 East Sea/Sea of Japan LME The estimated ECC of the Korean sector in the East Sea/Sea of Japan LME was 1.81 mmt using EMM and 1.42 mmt using HPM (Table 2 and Fig. 2c). Anchovy, chub mackerel, red snow crab, pacific herring, and sandfish were listed as independent groups. Demersal fish were the most abundant group, followed by cephalopods, small pelagic fish, and red snow crab (Table 2). Common squid was dominant in terms of abundance, which accounted for about 33% of the estimated ECC. Red snow crab and Pacific herring were also dominant species. The annual biomass estimated using HPM showed some fluctuations in the 1970s and then abruptly decreased, reaching its lowest value of 0.3 mmt in the late 1980s (Fig. 2c). As shown in Fig. 2c, fish stocks in the East Sea/Sea of Japan LME have been over-fished since 1981, and are currently below the BPBY 8

level. Biomass has remained at a low level since then and current biomass is at 0.38 mmt, which is about 54% of the required biomass for PBY (BPBY) (0.71 mmt) level.

4. Potential Biomass Yield (PBY) 4.1 Methods for estimating PBY The LMEs for estimating PBYs were the same as those for the ECCs. Two approaches were used to estimate PBY of Korean sectors in the East China Sea, Yellow Sea, and East Sea/Sea of Japan LMEs: the ecosystem modeling method (EMM) and the holistic production method (HPM). Gulland’s (1971) formula was used to estimate PBY in EMM as follows: 𝑃𝐵𝑌 = 0.5 · 𝑀𝑖 ∙ 𝐸𝐶𝐶𝑖 where, 𝑀𝑖 is the natural mortality of representative species by group 𝑖, which was weighted by catch; and 𝐸𝐶𝐶𝑖 is the estimate from the Ecosim simulation of the EMM. In HPM, PBY was estimated using the parameter 𝑟 and ECC estimated from the ME model: 𝑟 = 𝑝1𝑟 ∙ 0 + 𝑝2𝑟 ∙ 0.375 + 𝑝3𝑟 ∙ 0.75 𝐸𝐶𝐶 = 𝑝1𝐸𝐶𝐶 ∙ 0 + 𝑝2𝐸𝐶𝐶 ∙ ℎ/2 + 𝑝3𝐸𝐶𝐶 ∙ ℎ 𝑃𝐵𝑌 =

𝑟 ∙ 𝐸𝐶𝐶 4

where, 𝑟 is the intrinsic rate of natural increase. Details of estimation methods for PBY, including the setting of initial values, are explained in Lim (2018). To examine the status of stocks, acceptable biological catch (ABC) was estimated using the 5-tier ABC estimation system (Zhang and Lee, 2001). Since time-series catch and effort data were used to estimate PBY, the tier-4 was used to estimate the ABC of the three LMEs as follows, with α set to 0.05: (a) Stock status: B/BPBY > 1: ABC=PBY (b) Stock status: α< B/BPBY ≤ 1: ABC= PBY x (B/BPBY – α)/(1- α) (c) Stock status: B/BPBY ≤ α: ABC =0 4.2 PBY of three LMEs 4.2.1 East China Sea LME The estimate of PBY of the Korean sector in the East China Sea LME was 1.02 mmt using the EMM, which was similar to the 1.03 mmt estimated using the HPM (Table 3 and Fig. 3a). Species groups for PBY (Table 3) were the same as those for ECCs shown in Table 2. PBY for chub mackerel was the highest at 0.13 mmt, 9

followed by anchovy at 0.11 mm, hairtail at 0.09 mmt, and common squid at 0.09 mmt (Table 3). Annual catches in the East China Sea LME were lower than the ABC in the 1970s (Fig. 3a). However, since the mid1980s, catches have exceeded ABC, which caused a decline in biomass. Accordingly, the East China Sea LME has been over-fished since the mid-1980s. Since the early 2000s, the total allowable catch (TAC) system has been implemented in Korean fisheries, which could have the potential to reduce the gap between catch and ABC after fisheries resources have recovered. 4.2.2 Yellow Sea LME The estimated PBY of the Korean sector in the Yellow Sea LME was 0.26 mmt using EMM, but only 0.18 mmt using HPM (Table 3 and Fig. 3b). PBY of demersal fish was the highest at 0.1 mmt, followed by infauna and epifauna (Table 3). Rays and blue crabs had also relatively high PBYs at around 0.02 mmt. Fig. 3b shows that annual catches in the Yellow Sea LME have increased continuously since the late 1960s, and exceeded ABC since the mid-1970s, which caused a continuous decline in biomass. Therefore, the Yellow Sea has been over-fished since the mid-1970s. 4.2.3 East Sea/Sea of Japan LME Estimated PBY of the Korean sector in the East Sea/Sea of Japan LME was 0.34 mmt using EMM and 0.27 mmt using HPM (Table 3 and Fig. 3c). As shown in Table 3, common squid had the highest PBY at 0.08 mmt, accounting for 25% of the total estimated PBY. The PBY of red snow crab, one of the dominant species, was quite high at 0.03 mmt, followed by Pacific herring at 0.01 mmt (Table 3). Annual catches in the East Sea/Sea of Japan LME were lower than the ABC in the 1970s (Fig. 3c). However, since the early 1980s, catches have exceeded ABC, which caused a decline in biomass until the early 1990s. This indicated that the East Sea/Sea of Japan LME has been over-fished since the early 1980s. Thereafter, annual catches showed some fluctuations at a higher level than ABC. 4.3 Biological and fishery productivity ECC and PBY per unit area (mt/km2) were estimated to understand biological and fishery productivity in the three LMEs. In the East China Sea LME, ECC per unit area was 31.85 (mt/km2) and PBY per unit area was 5.12 (mt/km2) (Table 4). Both ECC and PBY were the highest in the East China Sea LME. The ECC per unit area was 3.5 times higher in the East China Sea LME than in the East Sea/Sea of Japan LME, and the PBY per unit area was almost 3 times higher in the East China Sea LME than in the East Sea/Sea of Japan LME. This indicates that the East China Sea LME is much more productive than the other two LMEs. For the sustainable management of fisheries resources, it is necessary to understand the mechanism of fluctuations in fisheries 10

resources. As shown in Fig. 2, BPBY (3.21 mmt) was twice as high as the current biomass (1.67 mmt in 2016) and the PBY level (1.03 mmt) was about 1.6 times the current catch level (0.64 mmt in 2016). If an appropriate management plan was implemented and biomass recovered to the required BPBY level, a 1.6 times increase in future catch could be expected from the current level to PBY level (Fig. 4a). As shown in Table 4, ECC per unit area was calculated as 18.22 (mt/km2) and PBY per unit area was 2.40 (mt/km2) in the Yellow Sea LME. Both ECC and PBY were comparatively lower in the Yellow Sea LME than in the East China Sea LME, but higher than in the East Sea/Sea of Japan LME. Fig. 2 shows that BPBY (3.21 mmt) was about 1.8 times the current biomass (0.38 mmt in 2016) and PBY level (0.18 mmt) was about 1.5 times the current catch level (0.12 mmt in 2016). As described above, if biomass recovered to the BPBY level (0.68 mmt), a future catch at the PBY level (0.18 mmt) would be possible in the Yellow Sea LME (Fig. 4b). ECC per unit area in the East Sea/Sea of Japan LME was the lowest at 9.08 mt/km2. PBY per unit area of 1.70 mt/km2 was also the lowest in the East Sea/Sea of Japan LME (Table 4), which indicated that this LME had relatively low productivity, compared to the other two ecosystems. In fact, the East Sea/Sea of Japan LME has a narrow continental shelf and a deep-water continental slope. Thus, exploitable fish resources and available fishing areas are limited, which might explain why it had the lowest ECC and PBY per unit area of the three LMEs. Again, if biomass could be rebuilt up to the BPBY level (0.71 mmt) from the current biomass level in 2016 (0.38 mmt), catches could increase from the current level of 0.17 mmt to the PBY level of 0.27 mmt in the East Sea/Sea of Japan LME (Fig. 4c).

5. Ecosystem-based fisheries assessment and management Conventional tools to assess and manage fisheries resources, which mainly focus on the sustainability of target species, have thus far not been effective. Although a variety of approaches have been applied to improve the management of fishery resources and facilitate the recovery of depleted fisheries resources, they have not been fully successful. In fact, the current exploitable biomasses for the Korean sectors in the three LMEs investigated still remain at about 30–40% of those of the late 1960s. Therefore, an ecosystem-based fisheries assessment (EBFA) approach has been developed to assess fisheries resources in Korean waters, based originally on three management objectives: sustainability, biodiversity, and habitat quality (Zhang et al., 2009). A socio-economic component was added as another management objective of the approach, and further studies have revised the indicators and the relevant reference points (Kim and Zhang, 2011; Kruse et al., 2009; Seung and Zhang, 2011), including an alternative method for scoring risk (Park et al., 2013). Also, the Integrated 11

Fisheries Risk Analysis Method for Ecosystems (IFRAME) was developed based on the EBFA (Zhang et al., 2011) to assess the impacts of climate change on fisheries, and has been positively reviewed (Hollowed et al., 2013). 5.1 Ecosystem-based fisheries assessment (EBFA) In this study, the EBFA was used to assess the fisheries of Korean sectors in three LMEs. We adopted indicators and reference points from previous studies (Zhang et al., 2009, 2010), and modified several indicators. A total of 14 indicators were used, including four for sustainability, four for biodiversity, three for habitat quality, and three for socio-economic benefits (Table 5). Nested risk indices, including an objective risk index (ORI), species risk index (SRI), fishery risk index (FRI), and ecosystem risk index (ERI), were estimated to assess ecosystem status at the management levels of species, fisheries, and ecosystems. Detailed equations are described in Zhang et al. (2009, 2010) and Kang et al. (2018). 5.2 Risk indices of EBFA To assess the status of fisheries resources and their ecosystems based on the EBFA, we estimated FRI and ERI of Korean sectors in the East China Sea, Yellow Sea, and East Sea/Sea of Japan LMEs (Figs. 5 and 6). FRI and ERI were used to assess the ecosystem status at the management levels of fisheries and ecosystems, respectively (Zhang et al., 2009, 2010). Ecosystem risk indices (ERIs) for the East China Sea, Yellow Sea, and East Sea/Sea of Japan LMEs were 1.87, 2.17, and 1.95, respectively, and was highest for the Yellow Sea LME (Fig. 5). FRI was higher than corresponding ERI for two fisheries in the Yellow Sea LME, four fisheries in the East Sea/Sea of Japan LME, and eight fisheries in the East China Sea LME (Fig. 6). To identify the variables that contributed towards a high risk index, we traced an example through the nested risk system. When appropriate management strategies are identified, necessary corrective actions and enforcement measures are suggested. To identify which fisheries contributed the most towards the ERI, we estimated the relative contributions of each fishery by weighting FRI by their percentages. The results showed that the offshore stow-net fishery (62.5%) contributed the highest risk in the Yellow Sea LME, while the large purse-seine fishery (28.6%) and the offshore trap fishery (30.7%) contributed towards the highest ERIs in the East China Sea and the East Sea/Sea of Japan LMEs, respectively. We also estimated the relative contributions of each species to FRI by weighting SRI by their percentages in the top three high risk fisheries, which were offshore stow-net fishery, offshore gill-net fishery, and diving fishery in the Yellow Sea LME. Anchovy (52.3%) contributed the highest risk for offshore stow-net fishery,

12

while blue crab (58.4%) and pen shell (100%) contributed the highest risks for offshore gill-net fishery and diving fishery, respectively. 5.3 Ecosystem-based fisheries management (EBFM) Current fisheries management utilizes various measures and tools for different species and fisheries. However, current management tools do not include the concept of the EBFM. Managing fisheries at the ecosystem level can prevent significant and potentially irreversible changes in LMEs. The results of our risk analyses could serve as a useful basis in establishing strategies and tactics for environmentally-sound and sustainable fisheries, based on specific evaluations of high risk indicators shown in Table 6. The EBFM can identify appropriate management strategies for implementation, and can be used to trace specific cases via the nested system to identify the subject or subjects that contribute towards high risk scores and indices. This process can identify necessary corrective actions or enforcement measures for implementation. The final step is to develop procedures to evaluate the effectiveness of management strategies or tactics and revise the management system as needed. In each step, the involvement of stakeholders to achieve consensus is desirable (Zhang, 2014).

6. Discussion The decrease in coastal productivity and deterioration in the quality of ecosystems that results from overfishing and environmental pollution in the East China Sea, Yellow Sea, and East Sea/Sea of Japan LMEs presents a serious problem. To manage fisheries effectively, it is necessary to determine the ECC and PBY to understand available resources in these LMEs. However, few studies have estimated the ECC and PBY in these seas. The ECC and PBY are also essential criteria for establishing goals and reference points for ecosystembased fisheries assessment and management in these LMEs. Although many ecosystem models have been proposed to analyze the trophic relationships in marine ecosystems, the EwE model practically describes the structure and function of a marine ecosystem (Pauly et al., 2000). In ecosystem dynamics analysis, EMM can utilize EBFM to estimate the interaction between ecosystem components, food chain structure, and biomass of ecosystems at a specific point in time, and predict whole ecosystem change. However, the EwE model has some limitations as it has multiple input parameters, including biomass (B), ratio of production to biomass (P/B), ratio of consumption to biomass (Q/B), and diet composition (DC). In practice, it is not easy to obtain timely data to accurately estimate these parameters. Therefore, it is often assumed that P/B can be indirectly estimated from the instantaneous total mortality rate (Z) at the time of 13

analysis, and Q/B and DC are often obtained from the literature, which sometimes causes uncertainty over the results. The HPM, which estimates ECC using surplus production models with time-series catch and fishing effort data, is simple and easy to apply, and requires much less data. A further advantage is that the non-equilibrium surplus production model’s fit is reasonably good and the reliability of estimated parameters is relatively high compared with the EMM approach, since the parameters are usually estimated from a theoretically optimal range (Golan et al., 1996). This is the reason why many studies have used this approach (Garcia and Newton, 1997; Kim, 2016). Therefore, the ECC and PBY estimates in this study should be considered as still preliminary, as there were uncertainties associated with some input data. The ERIs for three Korean sectors in the East China Sea, Yellow Sea, and East Sea/Sea of Japan LMEs were estimated as 1.87, 2.17, and 1.95, respectively. ERI for the Yellow Sea LME was the highest, which indicated that this ecosystem was the most degraded in terms of stock sustainability, biodiversity, habitat quality, and socio-economic benefits. To improve ecosystem status and reduce ERI, appropriate measures should be identified to manage fisheries, species, and indicators that contribute towards a high ERI. For example, in the Yellow Sea LME, BPBY was about 1.8 times the current biomass and PBY level was about 1.5 times the current catch level (Fig. 4b). Therefore, if biomass is rebuilt to the BPBY level, it would be possible to achieve future catches at the level of PBY in the Yellow Sea LME. Since this is the goal for the EBFM, detailed strategies and tactics should be implemented to achieve this goal (Table 6). The offshore stow-net fishery and anchovy species, which were the highest contributors to the ERI and FRI, respectively, can be considered as priorities for management. Management tools to reduce the risk associated with “age at first capture” might include “controlling mesh size” or “prohibiting capture size, season, and area” as these are the indicators that showed the greatest effects on anchovy caught using offshore stow-nets. The management status index enables a comparison of the status of species, fisheries, or ecosystems relative to several management objectives, both spatially and temporally (Zhang et al., 2009). Korean fisheries have been regulated by a variety of management tools, such as TAC, technical measures, management of threatened protected species and communities, habitat management, resource enhancement activities, marine ranching programs, marine forest enhancement programs, and self-management. However, these management tools have not been proposed and implemented through a single integrated assessment system, but using different assessment approaches. The EBFM requires a deep understanding of the ecological interactions of major species and their relationships with predators, competitors, and prey species, the effects of 14

climate on fish ecology, the complex interactions between fishes and their habitats, and the effects of fishing on fish stocks and their ecosystems (Zhang, 2014). The EBFM approach to sustainable development of LMEs should consider all possible methods, including complex interactions between fishes and their habitats, and the effects of fishing on fisheries and habitats. Also, to effectively manage fisheries in the LMEs around Korea, an organization is needed to regulate the fisheries of the nations that share the same seas, namely Korea, China, and Japan. In other words, efficient management and conservation of fisheries within a joint IFRAME approach is desirable. Ecosystem-based fisheries management can significantly improve current resources management. The UN 2030 Agenda for Sustainable Development and the Sustainable Development Goal 14 (SDG-14) also stressed the importance of not only the protection of marine ecosystems but also the EBFM to ensure food security (Zhang and Kang, 2018). The effect of fishing on ecosystems and the effect of ecosystem changes on fisheries resources

need to be better understood to more effectively apply living marine resources management.

Acknowledgements This work was supported by the National Institute of Fisheries Science [grant number R2018024].

References

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(a) Current system

(b) Map of study area

Fig. 1. Current system (modified from McFarlane et al. (2009)) and map showing the study area including sectors in the (A) East China Sea, (B) Yellow Sea, (C) East Sea/Sea of Japan LMEs. KC: Kuroshio Current; TWC: Tsushima Warm Current; YSWC: Yellow Sea Warm Current; EKWC: East Korea Warm Current; NKCC: North Korea Coastal Current; and LC: Liman Current.

19

(a) East China Sea

(b) Yellow Sea

(c) East Sea/Sea of Japan

Fig. 2. Estimates of exploitable carrying capacity (ECC) by HPM and variations in annual exploitable biomass (EB) of Korean sectors in the East China Sea, Yellow Sea, and East Sea/Sea of Japan LMEs. 20

(a) East China Sea

(b) Yellow Sea

(c) East Sea/Sea of Japan

Fig. 3. Estimates of potential biomass yield (PBY) by HPM and variations in annual catch (AC) of Korean sectors in the East China Sea, Yellow Sea, and East Sea/Sea of Japan LMEs. Solid lines indicate annual acceptable biological catch (ABC). 21

(a) East China Sea

(b) Yellow Sea

(c) East Sea/Sea of Japan

Fig. 4. Goals for rebuilding fisheries resources and recovering fishery yields in terms of target biomass and potential biomass yield (PBY) of Korean sectors in the East China Sea, Yellow Sea, and East Sea/Sea of Japan LMEs. 22

Fig. 5. Ecosystem risk index (ERI) for the Korean sectors in the East China Sea (ECS), Yellow Sea (YS) and East Sea/Sea of Japan (ES/SOJ) LMEs.

23

Fig. 6. Ecosystem risk index (ERI) and fishery risk index (FRI) of Korean sectors in the East China Sea, Yellow Sea, and East Sea/Sea of Japan LMEs. ERIs for the East China Sea, Yellow Sea and East Sea/Sea of Japan LMEs were 1.87, 2.17 and 1.95 respectively.

24

Table 1. Average catch, area, catch per unit area, and average catch of major species in the recent 5 years (2012~2016) of Korean sectors in the East China Sea, Yellow Sea, and East Sea/Sea of Japan LMEs (a) Catch and catch per unit area East Sea/Sea of Japan East China Sea LME

Yellow Sea LME LME

Area (km2)

201,618 (47%)

74,479 (17%)

155,853 (36%)

Average catch (mt) and catch ratio (%)

735,799 (71%)

124,812 (12%)

175,996 (17%)

3.65

1.68

1.13

Catch per unit area (mt/km2)

(b) Catch by major species East China Sea LME Major species

Yellow Sea LME

Average

Average Major species

(Scientific name)

catch (mt) Anchovy

catch (mt) Common squid

177,646 (24.1%) (Engraulis japonicus)

Average Major species

catch (mt)

Anchovy

East Sea/Sea of Japan LME

23,773 (19.0%)

69,026 (39.2%)

(Engraulis japonicus)

(Todarodes pacificus)

Blue crab

Red snow crab

Chub mackerel 121,570 (16.5%)

20,116 (16.1%)

(Portunus

(Chionoecetes

38,136 (21.7%)

(Scomber japonicus) trituberculatus)

Common squid

japonicus)

Oysters

Pacific herring

84,374 (11.5%)

9,453 (7.6%)

(Todarodes pacificus)

(Ostreidae spp.)

Hairtail

Japanese littleneck

17,887 (10.2%) (Clupea pallasii)

Sandfish 38,293 (5.2%) (Trichiurus lepturus)

7,933 (6.4%)

(Arctoscopus

5,579 (3.2%)

(Tapes phillipinarum) japonicus)

Spanish mackerel

Pacific cod

Flounders

30,945 (4.2%) (Scomberomorus niphonius)

4,226 (3.4%) (Gadus macrocephalus)

Yellow croaker

Common penshell 28,089 (3.8%)

5,132 (2.9%) (Paralichthyidae spp.)

Octopus 4,112 (3.3%)

(Larimichthys polyactis)

(Atrina pectinata)

Horse mackerel

Paste shrimp

3,940 (2.2%) (Octopodidae spp.)

Yellowtail 25,553 (3.5%) (Trachurus japonicus)

3,986 (3.2%)

(Seriola

2,823 (1.6%)

(Acetes chinensis) quinqueradiata)

Paste shrimp

13,355 (1.8%)

Sea snails

3,279 (2.6%)

25

Chinese puffer

2,082 (1.2%)

(Acetes chinensis)

(Gastropoda spp.)

Common conger

Goosefish

(Takifugu chinensis)

Spanish mackerel 12,866 (1.7%) (Conger myriaster)

2,853 (2.3%)

(Scomberomorus

2,045 (1.2%)

(Lophius litulon) niphonius)

Pacific herring

Halibut

Horse mackerel

11,647 (1.6%) (Clupea pallasii)

2,515 (2.0%) (Paralichthys olivaceus)

2,039 (1.2%) (Trachurus japonicus)

Others

191,461 (26.0%)

Others

42,566 (34.1%)

Others

27,307 (15.5%)

Total

735,799 (100%)

Total

124,812 (100%)

Total

175,996 (100%)

Table 2. Exploitable carrying capacity (ECC) by species group estimated from the EMM of Korean sectors in the East China Sea, Yellow Sea, and East Sea/Sea of Japan LMEs East China Sea LME Species group Chondrichthyes

ECC (mt) 98,909

Yellow Sea LME Species group

52,031

Rays

Rays

46,878

Sharks

Predator pelagic fish

1,014,820

ECC (mt) 147,553

Chondrichthyes

Sharks

East Sea/Sea of Japan LME

142,864 4,689

Predator pelagic fish

39,242

Species group Chondrichthyes

ECC (mt) 22,326

Rays

19,305

Sharks

3,021

Predator pelagic fish

49,163

Chub mackerel

540,059

Chub mackerel

15,554

Chub mackerel

11,971

Spanish mackerel

158,225

Others

23,688

Others

37,192

Others

316,536

Small pelagic fish

91,535

Small pelagic fish

282,129

712,148

Anchovy

43,661

Pacific herring

61,479

Anchovy

531,805

Others

47,874

Anchovy

44,762

Others

180,343

Demersal fish

534,987

Others

175,888

2,343,920

Flounders

156,941

Demersal fish

729,671

Hairtail

484,085

Croakers

130,294

Flounders

36,231

Croakers

320,999

Pacific cod

24,682

Sandfish

24,927

Flounders

150,170

Others

223,070

Others

668,513

Small pelagic fish

Demersal fish

Others

1,388,666

106,797

Cephalopods

26

Cephalopods

563,731

713,509

Common squid

29,848

Common squid

537,017

Common squid

552,670

Others

76,949

Others

26,714

Others

160,839

Blue crab

22,720

Red snow crab

91,620

Epifauna

487,602

Epifauna

186,011

Epifauna

62,000

Infauna

116,700

Infauna

220,020

Infauna

10,765

Cephalopods

Total

5,487,608

Total

1,348,866

Total

1,811,405

Table 3. Potential biomass yield (PBY) by species group estimated from the EMM of Korean sectors in the East China Sea, Yellow Sea, and East Sea/Sea of Japan LMEs East China Sea LME Species group Chondrichthyes

PBY (mt) 15,331

Yellow Sea LME Species group

8,065

Rays

Rays

7,266

Sharks

Predator pelagic fish

216,814

PBY (mt) 22,871

Chondrichthyes

Sharks

East Sea/Sea of Japan LME

22,144 727

Predator pelagic fish

7,719

Species group Chondrichthyes Rays Sharks Predator pelagic fish

PBY (mt) 3,460 2,992 468 9,070

Chub mackerel

132,314

Chub mackerel

3,811

Chub mackerel

2,933

Spanish mackerel

32,272

Others

3,908

Others

6,137

Others

52,228

Small pelagic fish

18,568

Small pelagic fish

59,159

144,462

Anchovy

8,857

Pacific herring

14,399

Anchovy

107,879

Others

9,711

Anchovy

9,080

Others

36,583

Demersal fish

97,592

Others

35,680

433,507

Croakers

29,968

Demersal fish

138,491

Hairtail

87,912

Flounders

22,090

Sandfish

6,564

Croakers

73,830

Pacific cod

4,683

Flounders

5,100

Flounders

21,136

Others

40,851

Others

Others

250,629

Small pelagic fish

Demersal fish

Cephalopods Common squid

16,553

Cephalopods

Cephalopods

126,827 87,379

110,594

Common squid

4,626

Common squid

83,238

85,664

Others

11,927

Others

4,141

27

Others

24,930

Blue crab

17,835

Red snow crab

32,983

Epifauna

78,748

Epifauna

30,041

Epifauna

10,013

Infauna

23,340

Infauna

44,004

Infauna

2,153

Total

1,022,797

Total

255,182

Total

342,707

Table 4. Exploitable carrying capacity (ECC) per unit area and potential biomass yield (PBY) per unit area of Korean sectors in the East China Sea, Yellow Sea, and East Sea/Sea of Japan LMEs East Sea/Sea of Japan East China Sea LME

Yellow Sea LME LME

ECC (mt/km2)

31.85

18.22

9.08

PBY (mt/km2)

5.12

2.40

1.70

Table 5. Indicators and their reference points used in the EBFA approach. The number of asterisks (*) reflects the subjective relative importance of the indicator, and is used to calculate objective risk indices. Objectives Sustainability

Biodiversity

Habitat

Attribute Biomass

No. S-1

Indicator

Weight

Biomass (B)

***

or Catch per unit effort (CPUE)

**

Fishing intensity

S-2

Fishing mortality (F) or catch (C)

**

Size at first capture

S-3

Age (or length) at first capture (tc or Lopt)

**

Reproductive potential

S-4

Rate of mature fish (MR)

*

Total bycatch

B-1

Bycatch rate (BC/C)

**

Total discards

B-2

Discards rate (D/C)

**

System trophic level

B-3

Mean trophic level of the community (TLc)

*

Diversity

B-4

Diversity index (DI)

*

Habitat damage

H-1

Critical habitat damage rate (DH/H)

**

H-2

Lost fishing gear (FR)

*

28

Discarded wastes

H-3

Discarded wastes (DW)

*

Socio-

Income

E-1

Income per person employed (IPPE)

*

economic

Profitability

E-2

Ratio of profit to sales (RPS)

*

benefit

Employment

E-3

Employment rate (ER)

*

Table 6. Management objectives, strategies, and tactics for fisheries Objectives Sustainability

Strategies

Tactics

- Increase biomass

- Adjust TAC

- Reduce fishing capacity

- Reduce the number of licenses or permits

- Prevent catches of immature fish

- Limit the number of trips and/or fishing days - Control mesh size - Prohibit capture size, season and area

Biodiversity

- Prevent incidental catches

- Adopt a bycatch reduction device

- Preserve diversity and trophic

- Control illegal fishery

level

- Enhance monitoring system

- Maintain community structure

- Use on-board observer system

Habitat

- Prevent habitat damage

- Establish marine protected area (MPA)

quality

- Restrict discarded wastes

- Adopt biodegradable fishing gears - Restrict the use of harmful fishing gears - Adopt temporary fishing recession

Socio-

- Increase revenues

- Enhance community-based management

economy

- Maintain viable production

- Increase government support towards shifted

- Support employment

fisheries - Predict supply and demand - Predict employment

29