Effect of Ocean Climate Changes on the Korean Stock of Pacific Saury, Cololabis saira (BREVOORT)

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1 Journal of Oceanography, Vol. 61, pp. 313 to 325, 2005 Effect of Ocean Climate Changes on the Korean Stock of Pacific Saury, Cololabis saira (BREVOORT) CHANG IK ZHANG 1 * and YEONG GONG 2 1 Pukyong National University, Busan , Korea 2 Korea Fisheries Association, Seoul , Korea (Received 31 January 2004; in revised form 9 June 2004; accepted 9 June 2004) Atmospheric, hydrographic and fishery biological factors indicated that the abnormal northward shift in the distribution of Pacific saury might be the result of a strong flux of warm water into the Japan/East Sea in the late 1970s. Recruitment failure of saury in the late 1970s was attributed to the limitation of the productive area for primary production caused by oligotrophic warm water, and to mismatch of the time of the spring outburst with the earlier arrival of saury to the feeding ground. Comparison of monthly upper mixed layer depth (MLD) and critical depth supported the possibility of the mismatch phenomenon. However, an appropriate management scheme should be implemented to prevent recruitment overfishing for the stock when any sign of ocean climate changes is detected. Keywords: Pacific saury, climate changes, recruitment, primary production, mixed layer depth, critical depth, Korea, Japan Sea. 1. Introduction The annual average catch of Pacific saury in Korean waters amounted to 25,000 metric tonnes (mt), varying between 11,000 mt and 40,000 mt in the 1960s and early 1970s. But the catches started to decline from the late 1970s and dropped to less than 5,000 tonnes in the late 1980s. Since then, the annual catches have fluctuated from 2,000 mt to 18,000 mt (Fig. 1). The Korean stock of Pacific saury migrates from the Japan/East Sea to the eastern part of the East China Sea in late autumn, where they spend winter, and return to the Japan/East Sea in spring summer to spawn and feed. The migration circuit of the saury stock has been contained within the Tsushima Warm Current system. Pacific saury spawn in the northeastern East China Sea in winter and in the southern Japan/East Sea in spring, northward shifting of spawning sites with the shifts of subarctic (or polar) front in early summer (Hatanaka and Sekino, 1956; Kotova, 1958; Fukataki, 1959; Shuntov, 1967; Lim et al., 1970; Jo, 1977). The saury in the Tsushima Warm Current region are composed of two spawning cohorts, that is, spring spawning and autumn spawning cohorts of which the former with 2.5 years of lifespan is major com- * Corresponding author. cizhang@pknu.ac.kr The Editor-in-Chief does not recommend the usage of the term East Sea in place of Japan Sea. Copyright The Oceanographic Society of Japan. ponent (Fukataki, 1963). However, Pacific saury in the North Pacific is known to have a short lifespan of 1.5 years in recent studies (Suyama et al., 1996). Adult saury larger than 20 cm in body length consume large species of zooplankton and juveniles consume small zooplankton. Although the feeding of the saury is active on the flotsam along the frontal zone during the spawning season, the main feeding ground is known to be the northern Japan/East Sea (Fig. 2). High concentrations of saury usually occur in the areas with a temperature ranging from 13 to 18 C and with a salinity ranging from 33.6 to 34.4 (Gong et al., 1985). Few adult saury are found in the low haline surface water in the west of the Tsushima Warm Current front in winter and in the south of the subarctic front in summer (Fig. 2). The pattern of the seasonal migration of saury varies considerably year after year, depending upon oceanic conditions in the stock area (Gong et al., 1983, 1985). It was pointed out that the unfavorable oceanic conditions (e.g. warm in 1976 and cold in 1977) in relation to the availability have to be taken into consideration on the cause of the decline in catches and abundance of Pacific saury in the Japan/East Sea (Gong, 1984). There are several hypotheses of the impact of large-scale climate changes which began in the late 1970s on the marine ecosystem in the North Pacific (Kawasaki, 1994; Trenberth and Hurrell, 1994; Polovina et al., 1995; Mantua et al., 1997; Miller and Schneider, 1998; Klyashtorin, 1998; Sugimoto and Tadokoro, 1999). The sharp decline in abundance of Pacific saury in the late 1970s has been attrib- 313

2 40 Catch in 1,000mt Fig. 1. Annual catches of Pacific saury in Korean waters, 1920~2000. Data source: Statistical Yearbook of Maritime Affairs and Fisheries, 1920~2000. uted to the effect of simultaneous climate changes on the stock (Zhang et al., 2000). The dependence of the marine ecosystem, in particular fish stocks, on climate changes has not been fully understood. Recognition of the 1976~1977 regime shift in the North Pacific Ocean has cast the question of whether that event affects the generation of recruitment and changes in abundance of fish stocks. The objective of this study is to evaluate the impact of ocean climate events on the initiation of primary production, seasonal movements of the saury, fishing conditions and changes in abundance of the saury stock in the Japan/East Sea and the East China Sea. Fig. 2. Distribution ranges of wintering, spawning and feeding areas of Pacific saury in the Tsushima Warm Current system. 2. Data and Methods The volume transport of the Kuroshio Current in the East China Sea (PN line, N, E~30 00 N, E) was standardized during the year of 1955~1993 using data from Fujiwara (1981), Inoue (1981) and Nagasaki Marine Meteorological Laboratory (1996). To determine annual and seasonal variations in sea surface temperature (SST) of the fishing grounds for Pacific saury, monthly SST anomalies and their standardized fluctuation indices (FI) were estimated, based on 10- day mean water temperatures in 1957~1981 at 17 stations in the southern Japan/East Sea (Gong et al., 1983). Wind stress index was estimated based on the daily wind data at Ulreungdo Island (37 29 N, E). Daily means of wind direction and force were divided into southerly (135 ~225 ) and northerly (315 ~45 ) components and summed for each month. These sums were divided by the number of days concerned, and finally multiplied by 100 (Gong et al., 1985). The depth of transparency (TD), measured with a Secchi disc by National Fisheries Research and Development Institute (NFRDI) in the south-western Japan/East Sea (35 N~38 30 N, west of 134 E) for 40 years (1958~1997), was converted into a measure of chlorophyll-a concentration using the relationship of Chl-a = 157.3TD 1.99 (Park, 1996). The critical depth (Dcr) was estimated using the method of Sverdrup (1953). Photosynthetically active radiation (PAR) was estimated from the monthly solar radiation corrected for cloud cover and reflection (Maizuru Marine Observatory, 1972). Two extinction coefficients were selected: high value (k = 0.14 m 1, TD 12 m) for the coastal region and low value (k = 0.10 m 1, TD 17 m) for the offshore region. The extinction coefficient (k) was obtained from the formula: k 1.7/TD, where TD is the depth of transparency (Parsons and LeBrasseur, 1968). Three different charts of monthly mixed layer depth (MLD) were available for the Japan/ East Sea, that is, MLD (1) by Robinson (1976), MLD (2) by Gong and Oh (1977) and MLD (3) by Bathen (1972). The mesh size of the gillnet ranged from 31.9 mm to 36.6 mm with a mean of 33.6 mm and the length (40~50 m) and depth (2.5~3.0 m) of the one unit net (pok) was the same throughout the study period. Monthly fork length frequency data were derived from the study of Gong et al. (1983) that fork length frequencies of Pacific saury taken by Korean gillnets were classified into four size 314 C. I. Zhang and Y. Gong

3 2 Standardized index Fig. 3. Standardized anomaly index of the volume transport of the Kuroshio Current into the East China Sea. Data source; Nagasaki Marine Meteorological Observatory PN line (from N, E to N, E). Fig. 5. Chlorophyll-a concentration (mg m 3 ) in the southern Japan/East Sea, derived from Secchi depth data. A: Monthly mean ( X ) and X ± SD, B: Interannual trend of April and October, Fig. 4. Monthly changes of fluctuation indices (FI) of sea surface temperatures for the 1957~1981 period at the 17 selected stations in the Japan/East Sea off Korea. FI represents the percentage of deviations from mean ( X ) to standard deviation (σ) (FI = (X X )/σ 100) (after Gong et al., 1983). groups: small (<24.9 cm), medium (25.0~27.9 cm), large (28.0~31.9 cm) and extra large size group (>32.0 cm). Abnormal oceanic conditions were identified based on changes in the volume transport in the East China Sea, SST anomaly, thermal structure and position of the polar front in the Japan/East Sea. Monthly critical depths (Dcr) and mixed layer depths (MLD) were compared to identify the changing patterns in the time of onset of production caused by the changes in MLD through the ocean climatic event. The movement and migration patterns of saury were analyzed on the basis of body length compositions of saury taken by gillnet fishing in relation to the SST anomaly. The time of the initiation of the spring phytoplankton outburst and the arrival of saury to the spawning and feeding grounds were compared (match/ mismatch) to detect any effect of oceanic conditions on the failure of the recruitment of saury, based on the match/ mismatch theory. The intensity of the saury fishing in the 1970s was examined based on the fishing effort and abundance index for the Korean gillnet fishing. Finally a hypothesis on the processes of collapse of the fishery was established on the basis of match/mismatch theory in relation to the climate-driven regime shift in the mid 1970s. 3. Results The volume transport of the Kuroshio Current in the East China Sea showed an interdecadal variation, being on average lower (20 sv) before 1975 and higher (25 sv) afterward (Fig. 3). The SST anomaly in the southern Japan/East Sea in winter 1962/1963, 1976/1977 and 1979/ 1980 were sharply shifted from the positive values to the negative (Fig. 4). The monthly average chlorophyll-a concentrations converted from the transparency depth (TD) showed high values in spring (April and May) and in autumn (November and December) in the southern Japan/ East Sea (34 30 N~38 30 N, west of 132 E) (Fig. 5). The chlorophyll-a concentrations in April and October 1962, 1968, 1970, 1976, 1977, 1980 and 1981 were lower than the average value during 1958~1997, and the concentrations in October showed an increasing trend from the mid 1970s. In principle when the critical depth (Dcr) exceeds the depth of mixing (MLD), a net increase in production can take place (Sverdrup, 1953). Table 1 shows the esti- Effect of Ocean Climate Changes on the Korean Stock of Pacific Saury, Cololabis saira (BREVOORT) 315

4 Table 1. Ratio of critical depth (Dcr) to mixed layer depth (MLD) in the Japan/East Sea. St. Oct. Nov. Dec. Jan. Feb. Mar. Apr. May 1 37 N Dcr(2)/MLD(1) E Dcr(2)/MLD(2) N Dcr(3)/MLD(1) E Dcr(3)/MLD(2) N Dcr(3)/MLD(1) E 4 38 N Dcr(3)/MLD(1) E 5 39 N Dcr(3)/MLD(1) E 6 40 N Dcr(3)/MLD(1) E Dcr(3)/MLD(3) N Dcr(3)/MLD(1) E Dcr(3)/MLD(3) N Dcr(3)/MLD(1) E Dcr(2); k = 0.14 m 1 (TD 12 m), Dcr(3); k = 0.10 m 1 (TD 17 m). MLD(1); Robinson (1976), MLD(2); Gong and Oh (1977), MLD(3); Bathen (1972). Data for MLD and light intensity for critical depth (Dcr) are monthly average over 10 years. mated monthly ratios of Dcr to MLD at selected eight stations in the Japan/East Sea. The critical depth (Dcr) exceeded the MLD in the western central region (Sts. 1, 2 and 3: 37 N, west of 131 E) throughout the winter and spring months. However, the Dcr hardly exceeded the MLD (Dcr/MLD < 1.0) in the winter months in the southeastern (St. 4: 38 N, 134 E, St. 5: 39 N, 138 E), northern (St. 6: 40 N, 130 E) and north-eastern region (St. 7: 41 N, 134 E and St. 8: 43 N, 138 E). In May 1975, the area with a strong thermocline at depth was fairly large, but in May 1976 it was small because of the strong shift of warm water to the coast (Fig. 6). The vertical sections of temperature along the 104 line (parallel with Lat N from east coast of Korea to Long E) showed the low temperature in the anomalously deep MLD (200~250 m) in April 1977 (Fig. 6). During the later southward migration season (e.g., February 1970) the large size group (mode 31 cm) and extra large size group (mode 32 cm) of saury in the catches disappeared from the southern Japan/East Sea because of the earlier movement to the East China Sea in relation to the abnormally cold sea conditions (1969/1970). Another group (mode 27 or 28 cm) under the process of transition from the medium to the large size group appeared throughout the season (1969/1970). In the following northward migration season, the large size group (mode 30~31 cm) appeared there later (May~July 1970) than normal (April~May) (Fig. 7). During the anomalous warm winter (1975/1976) the transition group (mode 27~28 cm) appeared later (Jan.~Feb.) than normal (Nov.~Dec.). The large size group (mode 30 cm) was continuously observed in the southern Japan/East Sea in winter 1975 and spring During the later northward migration season (June 1976) the large size group disappeared earlier than normal, indicating that they had already moved to the north of N (northern boundary of fishing) in relation to the abnormally warm sea conditions in winter 1975 and spring 1976 (Fig. 7). In the southward migration season of 1976/1977 the length composition had two modes: one in the large size group (mode 30 cm) and the other in the smaller medium size group (mode 26 cm). The large size group did not appear in January The transition group (mode 27 or 28 cm), which usually appeared in winter months, did not appear in winter 1976/1977. During the northward migration period (March~July) in 1977 the smaller medium size group (mode 25~26 cm) of saury was dominant, while the large size group (mode 29~31 cm) did not appear. It was noticed that the absence of the large size group was connected to the absence of the transition group (mode 27~28 cm) during the former southward migration season (autumn~winter 1976/1977), indicating that the climate driven oceanic changes had already disturbed the ecosystem in the stock area of Pacific saury within the Tsushima Current system. In the 23 years from 1957 to 1981 in which data were available the average composition ratio of large and extra large size groups combined in the northward migration season (March~July) was 67.6%, while the ratio of 1977 was 316 C. I. Zhang and Y. Gong

5 ing ground, it is postulated that the speed of the southward migration of Pacific saury in autumn~early winter was faster than the northward migration in spring~early summer in the Japan/East Sea (Fig. 9). Annual average fishing effort in tonnage of fishing boat and in gillnets per day have increased sharply since the early 1970s (Fig. 10). The fishing area has expanded from the south-western region (34 30 N~38 30 N, west of E) to the central Japan/East Sea since the mid 1970s (see Fig. 9). The annual mean saury catch in the northward migration season (March~July) in 1959~1976 amounted to 20,000 mt and the catch in the southward migration season (October~February) in 1965~1978 to 10,000 mt (Fig. 11). The annual total catches have declined sharply to less than 10,000 mt since 1977 (Fig. 11). During 11 years (1965~1975) the saury catches were at a relatively high level with the increased fishing effort. The catch per unit effort and the abundance index in the saury gillnet fishery steadily declined in the late 1970s and 1980s. Fig. 6. Vertical thermal structure along the 106 line ( N) in mid-may 1975 (A) and 1976 (B). Shaded portions indicate the stable thermocline where primary production gain can be expected in the winter because the critical depth (Dcr) exceeds the mixed layer depth (MLD) (upper panel). Vertical section of temperatures along the 104 line (parallel with Lat N from coast to Long E) showing anomalously deep mixed layer in April 1977 (lower panel). 9.6% (Fig. 8). The rates of large size groups were at the average level in 1978 and 1979, but they declined significantly again in the early 1980s. The rates showed the same annual variations during the main fishing season (April to June). The distribution of monthly mean catches by statistical block (30 30 ) in 1959~1982 showed seasonal shifts and dispersions of fishing grounds of Pacific saury (Fig. 9). The northward migration of Pacific saury in spring~summer and southward migration in autumn~winter were apparent with the shifting of fishing grounds. The highest catches occurred from April to June with a peak in May and fish shoals continuously recruited to the fishing grounds from the south until May, and then the main groups moved to the north of the N in June (northern limit restricted from fishing by military reason). Based on the shifts in positions of the fish- 4. Discussion An increment in the intensity of the subarctic low (and the subtropical high) produced lower temperatures in the cyclonic subarctic low and higher temperatures in the anticyclone, an increase in the depth of the north Pacific thermocline and an increase in advection in the western boundary current area (Hanawa, 1993, 1995). Therefore, the volume transport of the Kuroshio into the East China Sea increased sharply from the mid 1970s (Fig. 3). The volume transport of the Kuroshio across the PN line evaluated by Kawabe (1995) and the Sverdrup transport at 38 N, 130 E by Yasuda and Hanawa (1997) also indicated the increase in warm water in the mid-1970s. The increased advection of warm water by the Kuroshio from lower latitudes to the south of Japan, from which the Tsushima Warm Current originates, has a strong connection with the subtropical gyre in the mid-1970s (Yasuda and Hanawa, 1997). The SST in winter 1975/1976 and spring 1976 in the south-western Japan/East Sea was higher than normal (Fig. 4) (Gong et al., 1983, 1985; Gong and Kang, 1986). The polar front separating cold, low salinity north Korean water from the warmer and more haline Tsushima Warm Current in the Japan/East Sea was shifted further to north than normal in spring summer 1976 (Gong and Son, 1982; Gong and Lie, 1984; Gong et al., 1985). Abnormally warm water was shifted to the north-western Japan/East Sea in winter spring 1975/1976 and 1978/ 1979 (Lee, 1986; Choe, 1986). The sudden shifting of SST anomaly from positive phase in winter 1975/1976 to the negative in winter 1976/ 1977 (Fig. 4) may be related to the winter cooling as shown by wind stress indices (see figure 2 of Gong, 1984). Effect of Ocean Climate Changes on the Korean Stock of Pacific Saury, Cololabis saira (BREVOORT) 317

6 Fig. 7. Monthly length (folk) frequency distribution of saury taken by gillnets in the Japan/East Sea during the southward migration season in 1969/70 (cold winter), 1975/76 (warm winter), 1976/77 (cold winter), 1977/78 (normal winter), and northward migration season in 1970 (cold spring), 1976 (warm spring), 1977 (cold spring) and 1981 (cold spring). The dark shading represents the small and medium sized groups. Gong et al. (1985) reported that the northerly wind at Ulreungdo was abnormally low and SST was high in the south-western Japan/East Sea in winter spring of 1959/ 1960, 1960/1961, 1975/1976, 1978/1979 and 1979/1980. However, it was suggested that SST fields in the spring around the Tsushima Current regions mainly depend on the winter cooling and the effect continues at least to April (Hirai, 1994). The sea level along the coast of the Korea 318 C. I. Zhang and Y. Gong

7 Strait (Pusan and Izuhara) was higher than normal level in the mid 1970s. The precipitation in the southern Japan/East Sea showed the decadal climatic event which increased in the mid 1970s and declined by 1988 (Zhang et al., 2000). The thermal regime in the upper layer showed a high amplitude oscillation in the mid 1970s, and it became the decadal quasi-steady state of low tem- Composition rates (%) Fig. 8. Composition rates (%) of large (28.0~31.9 cm) and extra-large (>32.0 cm) combined size groups of Pacific saury taken by Korean gillnetters in March through July, 1957~1981. peratures thereafter in the central and southern Japan/East Sea, suggesting the initiation of disturbance in the production system related with the intensification of the Aleutian Low and covaried Asian Monsoon (NFRDA, ; Kim and Isoda, 1998; Minami et al., 1999; Chiba and Saino, 2002). Prior to the influx of the warm and low haline surface water to the Japan/East Sea in late spring through the Korea Strait, saury in the southern Japan/East Sea and East China Sea could easily move to the northern Japan/ East Sea with the spreading of high haline water as the winter wind stress relaxed in early spring. It is postulated that the saury which over-wintered in the southern Japan/East Sea started to migrate earlier than normal due to the increased volume of Kuroshio/Tsushima waters and the weak wind stress in winter spring 1975/1976. Shuntov (1967) mentioned that the record for saury early reaching the East Korea Bay (39 N~40 N) was the 17th of March 1960, based on a north Korean researcher s data. Transparency may be a useful index of the long-term trends of phytoplankton biomass in the Japan/East Sea (Nagata et al., 1996). The year to year variations in chlorophyll-a concentrations converted from transparency depth (Fig. 5) and the integrated chlorophyll-a in the up- Fig. 9. Monthly catches of Pacific saury by sea block (30 30 ) for the Korean gillnet fishery in the Japan/East Sea, 1959~1982. Data source: Statistical Yearbook of Maritime Affairs and Fisheries, 1959~1982. Effect of Ocean Climate Changes on the Korean Stock of Pacific Saury, Cololabis saira (BREVOORT) 319

8 Fig. 10. Annual average tonnage of fishing boat (crosses), number of days per cruise (dots) and fishing effort per boat per day (sets; pok) (open circle) for saury gill-net fishing in the southern Japan/East Sea (34 30 N~40 00 N, west of 136 E), 1959~1982. Fig. 11. Catches of Pacific saury in the northward migration season (Mar July) (dark circle) and southward migration season (Oct. Feb.) (open circle). per 30 m water column (Nagata, 1994) revealed the same trend. The chlorophyll-a concentrations in the early spring (April) and autumn (October) in 1968~1970, 1976~1977, 1980~1981 were lower than the 40 year average. This could be due to the clear oligotrophic Tsushima Warm Current originating from the intensified Kuroshio and the subsequent increased MLD, which delayed the onset of the spring outburst of phytoplankton. However, the chlorophyll-a concentration showed higher (1.0) than normal value (0.8) in June 1976 which means the delay of the initiation of spring bloom in the Japan/East Sea (Fig. 5). In general, the average upper mixed layer depth (MLD) is deeper to the north of lat. 40 N and shallower to the south of lat. 36 N, and also the MLD is shallower in the western central region of the Japan/East Sea in winter and early spring (Radzikhovskaya, 1961; Bathen, 1972; Robinson, 1976; Gong and Oh, 1977). It is noticed that the values of MLD in the southern Japan/East Sea range from 30 m in the ridge along the coast to 150 m in the trough along the axis of East Korea Warm Current (130 E~ E) because of tilting of boundary layer along the coast in winter (Gong and Oh, 1977). The mixed layer here should reflect the effects of the variable bathymetry, with shallowing depths (e.g. the ridge) tending to decrease the MLD. The maximum MLD in the Tsushima Current region develops in February and the MLD along the polar front is shallower than that in its south and northern areas (Kim and Isoda, 1998). The MLD in the East Korea Warm Current region was anomalously deep (200~250 m) in April 1977 (Fig. 6). The winter (February) MLD was deeper than normal in the early 1970s and 1977 in the eastern central Japan/East Sea. The variations of MLD may be largely influenced by the interannual extension of the warm Tsushima Current or the disposition of the local warm eddies (Kim and Isoda, 1998). It was suggested that the MLD hardly exceeded the critical depth (Dcr) throughout the winter months in the central south-eastern region of the Japan/East Sea (Nishimura, 1969). However, the MLD could exceed the Dcr (Dcr/MLD < 1.0) in winter months in the south-eastern (Sts. 4 and 5), north and northeastern Japan/East Sea (Sts. 6, 7 and 8) in winter months (Table 1). On the contrary the MLD did not exceed the Dcr (Dcr/MLD > 1.0) throughout the winter months in the central western region (Sts. 1, 2 and 3) because of the shallow MLD (Table 1) and favorable solar radiation during normal climatic conditions (Maizuru Marine Observatory, 1972). The monthly distribution of transparency depth (Nagata et al., 1996) reveals that the chlorophyll-a concentrations are higher in the central western region (off the Korean peninsula) than in the south-eastern Japan/East Sea in spring and autumn. However, the regions with low ratio (Dcr/MLD) in winter and spring months can easily be less than 1 depending upon slight changes in MLD through ocean climate events. Percent changes in mean winter and spring MLD from 1977~1988 and relative to 1960~1976 levels were extremely high (25~30%) in the western Japan/East Sea (Polovina et al., 1995). Abnormally deep MLD and low chlorophyll-a concentrations around Ulneung Is. in 1977~1978 were reported (Kim et al., 1998). In the Japan/East Sea during 1976~1978 MLD deepened by up to 38%, resulting in a decrease of the ratio (Dcr/MLD) in winter and early spring. It was suggested that the higher than normal temperature at 50 m layer in the waters off East Korea Bay in winter (Lee, 1986), larger than normal warm water thickness in the north-western Japan/East Sea (Choe, 1986) in the mid 1970s and the abnormal northward shifting of polar front in 1976 are related to the deeper than normal MLD in the Japan/East Sea during the 1976/1977 regime shift. The chlorophyll-a concentrations were lower than normal in this period (Fig. 5). 320 C. I. Zhang and Y. Gong

9 In fact the vertical temperature section along the NFRDA oceanographic line 106 ( N) in mid May 1975 and 1976 showed a prominent W-E gradient of the frontal layer under the upper mixed layer (Fig. 6). There might be two primary ecosystems in the Japan/East Sea because of the influx of warm Tsushima Current originating in the oligotrophic Kuroshio over the fertilized cold water as suggested by Cushing (1989). The phytoplankton blooms in the central Japan/East Sea from February to April and the heterotrophic phase follows in June (Sorokin, 1974). Therefore, the seasonal succession of the production process in the region might take place in May. However, any changes in the thermal structure in the water column by climatic disturbances will result in a change of the timing. It is easily postulated that the reduced stratified area (nutrients unlimited coastal zone) with the shallow mixed layer in May 1976 and April 1977 resulted in a spring bloom which covered a smaller area compared with the stratified area in May 1975 (Fig. 6). It is noteworthy that the changed primary ecosystem may have contributed to the decline in spring production and to increased autumn production since the mid 1970s (Fig. 5). Abrupt changes in temperature and biomasses of phytoplankton and zooplankton along the PM line in late 1970s are noteworthy in relation to the climatic regime shift in the northern hemisphere (Minami et al., 1999; Chiba and Saino, 2002). It was suggested that changes in stratifications in relation to the Asian Monsoon covaried with the Aleutian Low are responsible for the decline of the phytoplankton biomass in the Japan/East Sea in 1980s (Chiba and Saino, 2002). The oceanographic factors described so far suggest that the abnormal oceanic changes started from winter 1975/1976 and 1977 in Korean waters in relation to the climate event in the North Pacific in the mid 1970s (Polovina et al., 1995; Deser et al., 1996). Comparing the critical depth (Dcr) and increased MLD with the abnormal oceanic changes it was supposed that there could be no net increase in primary production in the coastal waters off Korea, and the initiation of the production could be delayed at least one month in the spawning grounds of saury in the south of polar front and feeding grounds in the north of polar front in the Japan/East Sea in spring 1976 and 1977 because of deeper MLD. When the sea conditions are warmer than normal, the large size group of Pacific saury spend winter in the southern Japan/East Sea (Fig. 2). In particular, Pacific saury in the southern Japan/East Sea in winter 1976 started to migrate earlier (March) than normal (April) to the spawning and feeding grounds along the polar front where the initiation of the spring bloom was delayed by oceanic changes. It is noticed that there must be a failure of saury recruitment because of the mismatch between the time of onset of the spring outburst of phytoplankton and that of earlier than normal arrival of saury in the spawning ground. Distribution of habitat area at early life stages and comparison of catches of Pacific saury from the Kuroshio Current region and the Tsushima Current region suggest that there is no clear stock boundary between the stocks from two regions (Fukataki, 1959; Novikov, 1972, 1979; Watanabe and Lo, 1989). However, catches of Pacific saury inhabiting the Tsushima Current region account for about 10~20% of those in the northwest Pacific (Gong, 1984). The high density of saury by size group along the frontal zone off Korea during at least April, May and June is due to a northward migration by many adults from southern Japan/East Sea and northern East China Sea. Sea surface temperatures and the position of warm-cold fronts strongly influence migration patterns and rates of movement of saury in the Japan/East Sea off Korea (Gong et al., 1983, 1985). The wintering and spawning grounds and fishing grounds by catch and abundance indices are largely shifted north and south depending on the oceanic conditions. Therefore, the anomalous changes in oceanic conditions can be detrimental not only to the early life stages but also to the adult stages of saury through mismatch of prey and predator (saury). Pacific saury that are ready to spawn actively seek flotsam (floating algae and debris) along the watermass boundary, and the most favorable time of spawning in the Japan/East Sea seems to be from April to June (spring spawning) (Kotova, 1958; Shuntov, 1967; Lim et al., 1970; Jo, 1977). After feeding in the northern region, the saury return to the southern Japan/East Sea and East China Sea in autumn and winter. In winter (January March) adult saury spawn in the East China Sea (autumn spawning group). The eggs and larvae of saury were sampled in the Japan/East Sea and East China Sea including southwestern waters of Korea (Fukataki, 1959, 1963; Shuntov, 1967; Lim et al., 1970; Jo, 1977). However, adult saury are found only in the eastern East China Sea and Japan/ East Sea (Gong, 1984), indicating that they had adapted in order to inhabit the haline Tsushima Warm Current system. The density of saury migrating north and south along the western (Korean) side of the Japan/East Sea is higher than that along the eastern (Japanese) side (Fukataki, 1966; Han and Gong, 1970). It is clear that the migration of saury is very diffused, extending over a wide area, but as a whole gradually moving toward the north-western region of the Japan/East Sea in spring and summer (Rumjantsev, 1947; Apanovich, 1962; Fukataki, 1966; Nishimura, 1969; Gong, 1984) from which the centers of occurrence could be obtained. The stock level of the spring spawning group was higher than that of autumn spawning group in the 1960s and early 1970s (Fukataki, 1963; Kim and Park, 1981), and the large Effect of Ocean Climate Changes on the Korean Stock of Pacific Saury, Cololabis saira (BREVOORT) 321

10 than the normal body length (29 30 cm) (Baytalyuk, 2000). Therefore, the absence of the large size group of Pacific saury in the mid 1970s and 1980s was a stockarea-wide event. In fact, the saury catch ratio in the northward migration season decreased more than that of the southward migration season in 1977 and in the early 1980s (Fig. 11) (Gong, 1984). The saury catch and abundance index showed a sharp decrease in 1977 (Fig. 1) (Gong, 1984). The disappearance of large saury in 1977 and the decline of catch and abundance indices since 1977 indicate that there was a mass mortality of early stage and adult stage of the group. In conclusion, the failure of the Korean saury fishery is attributed to the ocean climate change in relation to the climate event which occurred in the mid 1970s. Even if recruitment overfishing does not seem to be the main cause of the decline in saury abundance, it should not be excluded from one of the reasons. The process of environmental influences on the failure of saury fishery in the Japan/East Sea is briefly explained in the diagram (Fig. 12). Fig. 12. Schematically hypothesized diagram showing the effect of climate-driven regime shift on Pacific saury in the Japan/East Sea in mid-1970s. size group of saury occurring in the central Japan/East Sea in spring summer was thought to be originated from the spring spawning group. However, it is not clear whether the large size groups are originated from the spring cohort under the hypothesis of the short lifespan (1.5 years). The transition size group (mode 27 or 28 cm) did not appear in the body length composition in winter 1976/ 1977, resulting in unusual absence of the large size group (mode 30 or 31 cm) in the northward migration season in 1977 (Fig. 8). Dominant mode in the length composition of Pacific saury taken by Japanese gillnet fell in the unusual medium size group (mode 25, 26 cm) and no large size group appeared in the waters off Hokkaido in the northward migration period of 1977 (Wakoh, 1978). In the northwestern region (off Russia) the rates of the large size group (greater than 28 cm in mode) ranged from 5 to 12% during spring and summer (March to October) in , expecting the smaller mean body length (24 26 cm) rather 5. Conclusion The increase of the difference in the sea level led to the intense oceanic circulation in the North Pacific during the climate-driven regime shift in the mid 1970s and 1980s. The increased volume transport of Kuroshio in the East China Sea resulted in a strong influx of the warm Tsushima/East Korea Current into the Korea Strait and Japan/East Sea. Heavy rain, higher SST, unusual northward shifting of the polar front and increased thickness of warm water in the north resulted in the northward shifting of the over-wintering ground of saury and the earlier than normal migration of saury to the spawning and feeding area in the south and north of the polar front in spring (Fig. 12). The area of stable thermocline in the coastal zone (nutrients unlimited zone) was reduced because of unusual westward and northward shifting of the polar front which resulted in the reduction of primary production. The critical depth hardly exceeded the deeper than normal MLD in winter and early spring in the saury spawning and feeding grounds during the early phase of the regime shift (1975~1977). Therefore, the delayed onset of the spring bloom of plankton (prey) and the earlier than normal arrival of spawning groups of saury resulted in the mismatch of prey and predator (larvae and adult) in the spawning and feeding grounds. It is postulated that the disturbance of the production system in the Tsushima Warm Current region was one of the decadal scale events manifested by the abrupt changes in thermal regime in 1976/77, thereafter a quasi-steady state intensified the stratification in 1980s, causing changes in the composi- 322 C. I. Zhang and Y. Gong

11 tion and biomass of dominant phytoplankton species and biomass of zooplankton. This event eventually led to the decrease of the mean body length and the abundance of saury. The dramatic decrease in the ratio of the large size group of saury resulted from the changes in stock structure and the abrupt drop of abundance and catch could be caused by heavy fishing under the destructive recruitment failure and mass mortality of saury in the mid 1970s. The economic consequences of the collapsed gillnet fishery have been considerable for the coastal fishermen off the east coast of the Korean peninsular. Therefore, an appropriate management scheme should be implemented to prevent recruitment overfishing for the stock when any indicator of ocean climate changes is detected. For this purpose, there is a need for sustained fisheries oceanographic monitoring and research on the process of environmental influences on these fisheries resources are necessary. Eventually, the total allowable catch (TAC)-based management system for the saury stock should be developed, based upon the estimates of acceptable biological catch which could be obtained from scientifically sound analyses such as, the relationships between recruitment of fish and the ocean environmental factors (Zhang and Lee, 2001). Acknowledgements This study was funded by the Research Project of of the Korea Science and Engineering Foundation (KOSEF). References Apanovich, S. I. (1962): New objects in saury fisheries. Ryb. Khoz, 38(1), 9 13 (in Russian). Bathen, K. H. (1972): On the seasonal changes in the depth of the mixed layer in the North Pacific Ocean. J. Geophys. Res., 77(36), Baytalyuk, A. (2000): Distribution and stock of saury (Colorabis saira) in the northwestern part of the Japan Sea. p In Extended abstract. Science Board Symposium, 9th PICES Annual Meeting, Hakodate, Japan. Chiba, S. and T. Saino (2002): Interdecadal changes in the upper water column environment and spring diatom community structure in the Japan Sea: an early summer hypothesis. Mar. Ecol. Prog. Ser., 231, Choe, C. Y. (1986): Effects of oceanographic conditions in spring summer on the fishing ground formation of trout and sardine in the northern East Sea. East Sea Fish. Res. Inst., Bull. Fish. Sci. and Tech., 1, 3 17 (in Korean). Cushing, D. H. (1989): A difference in structure between ecosystem in strongly stratified waters and in those that are only weakly stratified. J. Plankton Res., 11, Deser, C., M. A. Alexander and M. S. Timlin (1996): Upper ocean thermal variations in the North Pacific during 1970~1991. J. Climate, 9, Fujiwara, I. (1981): Oceanographic conditions in the East China Sea. Marine Science Monthly, 13(4), (in Japanese). Fukataki, H. (1959): Occurrence and distribution of eggs and larvae of the saury in the Tsushima Current region. Bull. Jpn. Sea Reg. Fish. Res. Lab., 7, (in Japanese). Fukataki, H. (1963): The growth stage and racial problem of the saury occurring in the Japan Sea. Reports of the Cooperative Investigations on the Saury in the Japan Sea for 1962, (in Japanese). Fukataki, H. (1966): Distribution, migration and population density of the saury occurring in the Japan Sea. Reports of the Cooperative Investigations on the Saury in the Japan Sea for 1963 and 1964, (in Japanese). Gong, Y. (1984): Distribution and movements of Pacific saury, Cololabis saira (Brevoort), in relation to oceanographic conditions in waters off Korea. Bull. Fish. Res. Dev. Agency, 33, Gong, Y. and Y. Q. Kang (1986): Sea surface temperature anomalies off the southeastern coast of Korea. Bull. Fish. Res. Dev. Agency, 37, 1 9. Gong, Y. and H. J. Lie (1984): Distribution of thermal fronts in the South-East Sea of Korea (Southern Japan Sea). Min. Sci. and Tech. Korea, BSPE B, 215 pp. (in Korean). Gong, Y. and M. Y. Oh (1977): Oceanographic Environments and Fisheries Resources off the East Coast of Korea. National Federation of Fisheries Cooperatives, 633 pp. Gong, Y. and S. J. Son (1982): A study of oceanic thermal fronts in the southwestern Japan Sea. Bull. Fish. Res. Dev. Agency, 28, (in Korean). Gong, Y., T. Hirano and C. I. Zhang (1983): On the migration of Pacific saury in relation to oceanographic conditions off Korean. Bull. Japan. Soc. Fish. Oceanogr., 44, Gong, Y., T. Hirano and C. I. Zhang (1985): A study on environmental conditions for Pacific saury in Korean waters. Bull. Japan. Soc. Fish. Oceanogr., 47 48, Han, H. S. and Y. Gong (1970): Relation between oceanographical conditions and catch of saury in the Eastern Sea of Korea. p In The Kuroshio. A Symposium on the Japan Current, ed. by J. C. Marr, East-West Center Press, Honolulu. Hanawa, K. (1993): Long-term variation of the oceanic condition and its relation to the atmospheric general circulation. Umi to Sora, 68, Hanawa, K. (1995): Southward penetration of the Oyashio water system and the wintertime condition of midlatitude westerlies over the North Pacific. Bull. Hokkaido Natl. Fish. Res. Inst., 59, Hatanaka, M. and K. Sekino (1956): Spawning ground of the saury, Colorabis saira (Brevoort) in the Japan Sea. Tohoku Jour. Agr. Res., 7, Hirai, M. (1994): Evaluation of the effects of winter cooling on sea surface temperature in the spring around Tsushima Current regions. Bull. Japan Sea Natl. Fish. Inst., 44, 1 17 (in Japanese). Inoue, N. (1981): Progress review on the hydrographic conditions in the East China Sea and Tsushima Warm Current area. Organisms of Koto Is., Comparison Iki Is. with Tsushima. Biol. Soc. Nagasaki, (in Japanese). Jo, M. K. (1977): A study on the distribution of eggs and larvae of saury in the Korean waters. Bull. Fish. Res. Dev. Agency, Effect of Ocean Climate Changes on the Korean Stock of Pacific Saury, Cololabis saira (BREVOORT) 323

12 16, (in Korean). Kawabe, M. (1995): Variations of current path, velocity, and volume transport of the Kuroshio in relation with the large meander. J. Phys. Oceanogr., 25, Kawasaki, T. (1994): A decade of the regime shift of small pelagics from the FAO expert Consultation (1983) to the PICES (1994). Bull. Japan. Soc. Fish. Oceanogr., 58, (in Japanese). Kim, S. W. and Y. Isoda (1998): Interannual variations of the surface mixed layer in the Tsushima Current Region. Umi to Sora, 74, (in Japanese). Kim, S., S. Kang and D. Kang (1998): Effects of climate change in Korean waters. p In Proc. 1st Workshop on Climate Changes and Fisheries Resources, ed. by C. I. Zhang, S. Kim and J. O. Oh (in Korean). Kim, Y. M. and Y. J. Park (1981): A study on the growth of saury, Cololabis saira (BREVOORT), based on the length composition in the Korean waters. Bull. Fish. Res. Dev. Agency, 27, (in Korean). Klyashtorin, L. B. 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(1947): Saury of the Sea of Japan. Izvestiya, TINRO, 25, (in Russian). Shuntov, V. P. (1967): Saury of the Sea of Japan. Izvestiya, TINRO, 56, (in Russian). Sorokin, Yu. I. (1974): Vertical structure and production of a microplankton community in the Sea of Japan in summer. Oceanology, 14, Sugimoto, T. and K. Tadokoro (1999): Delayed response of oceanic and biological conditions in the western Pacific to climate regime shifts (abstract). Paper submitted to the 8th Meeting of PICES, Vladivostok, 8 17 Oct Suyama, S., Y. Sakurai and K. Shimazaki (1996): Age and growth of Pacific saury Colorabis saira (Brevoort) in the western North Pacific estimated from daily otolith growth increments. Fisheries Science, 62, 1 7. Sverdrup, H. U. (1953): On conditions for the vernal blooming of phytoplankton. J. Cons. Int. Explor. Mer., 18, Trenberth, K. E. and J. W. Hurrell (1994): Decadal atmosphereocean variations in the Pacific. Clim. Dyn., 9, Wakoh, M. 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13 ern Pacific Ocean. Fish. Bull., 87, Yasuda, T. and K. Hanawa (1997): Decadal changes in the mode waters in the mid-latitude North Pacific. J. Phys. Oceanogr., 27, Zhang, C. I. and J. B. Lee (2001): Stock assessment and management implications of horse mackerel (Trachurus japonicus) in Korean waters, based on the relationships between recruitment and the ocean environment. Prog. Oceanogr., 49, Zhang, C. I., J. B. Lee, S. Kim and J. H. Oh (2000): Climate regime shifts and their impacts on marine ecosystem and fisheries resources in Korean waters. Prog. Oceanogr., 47, Effect of Ocean Climate Changes on the Korean Stock of Pacific Saury, Cololabis saira (BREVOORT) 325

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