Rising Sea Temperatures Are Forcing Japan's Key Fish Species to Adapt

Authors: (1) Tomoya Aono, Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Chiba, Japan and National Institute of Technology, Ibaraki College, Hitachinaka, Ibaraki, Japan; (2) Tatsuya Sakamoto, Fisheries Resources Institute, Japan Fisheries Research and Education Agency, Nagasaki, Japan (3) Toyoho Ishimura, National Institute of Technology, Ibaraki College, Hitachinaka, Ibaraki, Japan and Graduate School of Human and Environmental Studies, Kyoto University, Kyoto, Japan; (4) Motomitsu Takahashi, Fisheries Resources Institute, Japan Fisheries Research and Education Agency, Nagasaki, Japan; (5) Tohya Yasuda, Fisheries Resources Institute, Japan Fisheries Research and Education Agency, Yokohama, Kanagawa, Japan; (6) Satoshi Kitajima, Fisheries Resources Institute, Japan Fisheries Research and Education Agency, Nagasaki, Japan; (7) Kozue Nishida, National Institute of Technology, Ibaraki College, Hitachinaka, Ibaraki, Japan and Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki, Japan; (8) Takayoshi Matsuura, National Institute of Technology, Ibaraki College, Hitachinaka, Ibaraki, Japan (9) Akito Ikari, National Institute of Technology, Ibaraki College, Hitachinaka, Ibaraki, Japan; (10) Shin-ichi Ito, Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Chiba, Japan. Table of Links Abstract and 1 Introduction 2 Materials & Methods 3 Results 4 Discussion Conflict of Interest, Author Contributions, Funding, Acknowledgments, Data Availability Reference 5 Supplementary Tables and Figures Abstract The Japanese sardine (Sardinops melanostictus) is a small pelagic fish found in the Sea of Japan, the marginal sea of the western North Pacific. It is an important species for regional fisheries, but their transportation and migration patterns during early life stages remain unclear. In this study, we analyzed the stable oxygen isotope ratios of otoliths of young-of-the-year (age 0) Japanese sardines collected from the northern offshore and southern coastal areas of the Sea of Japan in 2015 and 2016. The ontogenetic shifts of the geographic distribution were estimated by comparing the profiles of life-long isotope ratios and temporally varying isoscape, which was calculated using the temperature and salinity fields produced by an ocean data assimilation model. Individuals that were collected in the northern and southern areas hatched and stayed in the southern areas (west offshore of Kyushu) until late June, and thereafter, they can be distinguished into two groups: one that migrated northward at shallow layer and one that stayed around the southern area in the deep layer. A comparison of somatic growth trajectories of the two groups, which was reconstructed based on otolith microstructure analysis, suggested that individuals that migrated northward had significantly larger body lengths in late June than those that stayed in the southern area. These results indicate that young-of-the-year Japanese sardines that hatched in the southern area may have been forced to choose one of two strategies to avoid extremely high water temperatures within seasonal and geographical limits. These include migrating northward or moving to deeper layers. Our results indicate that the environmental variabilities in the southern area could critically impact sardine population dynamics in the Sea of Japan. 1 Introduction The Japanese sardine (Sardinops melanostictus) is a species with large biomass fluctuations. The abundance of Japanese sardines showed substantial fluctuations of several orders of magnitude during the last 3000 years (Kuwae et al., 2017), and fluctuations have also been reported regarding the associated fisheries catch in recent centuries (Yasuda et al., 2019). These fluctuations are considered to be driven by environmental variabilities, which are often represented by the Pacific Decadal Oscillation (e.g., Chavez et al., 2003). Clarification of the mechanistic links between climate and marine environments and population fluctuation is necessary for the accurate prediction of resource abundance and fisheries management. Variations in survival rates during the post-hatching larval and juvenile stages are hypothesized to be of great importance for population fluctuations (e.g., Hjort, 1914). Therefore, the knowledge of the geographical distributions and environment of Japanese sardines during its critical life stages are essential for revealing the impact of climate and marine environment changes on population fluctuations. Current fisheries management of the Japanese sardine assumes two management units or stocks— the Pacific stock (distributed in the western North Pacific) and the Tsushima Warm Current Stock (distributed in the Sea of Japan), both of which show large fluctuations in abundance at similar time scales. While the patterns of transport and migration during the early life stages have been reported for the Pacific stock (e.g., Okunishi et al., 2009; Sakamoto et al., 2019), such knowledge for the Tsushima Warm Current Stock is insufficient. Spawning of the Tsushima Warm Current Stock occurs in coastal areas from west Kyushu to the Noto Peninsula from winter to early summer (January–June, Fig. 1). The main spawning ground changes depending on the sea surface temperature and spawning stock biomass (Furuichi et al., 2020). The young-of-the-year Japanese sardine is widely found from the off Noto Peninsula to the west coast of Kyushu in late summer (Ito, 1961; Yasuda et al., 2021). A recent study showed that the environment of the northern offshore area of the Sea of Japan with larger and lipid-rich prey zooplankton is suitable for the energy acquisition of sardine juveniles (Yasuda et al., 2021). In addition, the distribution of the stock is known to expand and shrink in response to population fluctuations; during periods of increased biomass, the distribution of the stock area expands to the northern offshore area of the Sea of Japan (Muko et al., 2018). These observations lead to the hypothesis that the successive and successful transportation (or migration) of juveniles to the northern offshore area might be the driver of the increase in stock (Muko et al., 2018; Yasuda et al., 2021). However, the origin, transportation, and migration routes of the individuals that reach the northern offshore area of the Sea of Japan have not yet been clarified. Understanding the movement patterns and their variety, and mechanisms that create the variety may, therefore, provide insights into energy acquisition strategies, population dynamics, and ultimately management of sardines in the region. 2 Materials & Methods 2.1 Fish sampling and Otolith δ 18 O analysis The young-of-the-years of Japanese sardines were collected for otolith analyses in three sampling areas (off Noto Peninsula, Tsushima Strait, and off Goto Islands) in the Sea of Japan from August to September in 2015 and 2016 by the R/V Yoko-maru, Japan Fisheries Research and Education Agency (Fig. 1; Table 1). Fish were frozen immediately after capture and preserved in -80 or -20 °C. Thereafter, the specimens were thawed in a laboratory on land and their scaled body length (BL) and body weight were measured. Sagittal otoliths were extracted, cleaned using a brush, rinsed with ethanol and distilled water, and dried at room temperature for several hours. The dried otoliths were embedded in epoxy resin (p-resin, Nichika Inc.) on a glass slide, and then placed in a dryer at 40 °C for at least a day to fix the otoliths. Thereafter, the embedded otoliths were polished with sandpaper (No. 1000, 2000) until the otolith core was exposed from the epoxy resin, and then the entire otolith was polished with alumina suspension (BAIKOWSKI International Corporation) to ensure that the daily rings could be easily observed under a microscope. The number of daily rings of the otolith and otolith daily increment widths were measured using an otolith measurement system (RATOC System Engineering Co. Ltd.). The otoliths of 154 individuals from 18 stations were used for daily ring measurements (Table 1). 2.3 Estimation of migration history To validate the estimated results, the estimated distribution area on the date closest to the sampling date for each individual was compared with the actual sampling area. In addition, the estimated distribution area on the date closest to the hatch date was compared with the results of a monthly egg and larval survey conducted at prefectural fisheries field stations (Oozeki et al., 2007; Furuichi et al., 2020). 2.4 Statistical analysis To examine the differences in biological characteristics between potentially different migratory types, namely the northward migration group (off Noto Peninsula individuals) and resident group (Tsushima Strait and off Goto Islands individuals; see Results and Discussion), we compared somatic growth trajectories between these groups. The Mann-Whitney U test for comparisons of hatching date and BL at the time of sampling was conducted between groups. We also compared the BL before sampling. BL before the time of sampling was calculated using the biological intercept method, assuming a linear relationship between the otolith radius and BL with fixed 5.9 mm of BL at the deposition of the first increment of the otolith, following Takahashi et al. (2008). To test for differences in the daily growth rates among the groups, anomalies of the 3-day running-mean otolith increment width normalized by standard deviation were compared among the three sampling areas using the Kruskal-Wallis test. The anomalies were calculated in two ways: for each day age of the fish and for each calendar day (days from January 1st each year). When a significant difference was detected, a post-hoc Steel-Dwass test was performed to identify areas with significant differences. 3 Results 3.4 Comparison of hatching dates, BL and daily growth rate differences There was a significant difference in the hatching dates between the northward migration group (63 ± 32 days from January 1st; mean ± 1SD) and the resident group (43 ± 30 days from January 1st) (Table 2, p < 0.02, Mann-Whitney U test). The mean BL of the northward group was 136.7 ± 6.4 mm and that of the resident group was 118.9 ± 9.4 mm. The BL of the northward group was significantly larger than that of the resident group (Table 2, p < 0.001, Mann-Whitney U test). In spring (March-May), the mean back-calculated BL of the resident group was larger than that of the northward migration group (Fig. 6). However, from June, the mean back-calculated BL of the northward migration group was higher than that of the resident group. The mean BL at July 1st, which roughly corresponds to the timing when migration patterns started to diverge, was significantly larger in the northward migration group (northward migration: 104.8 ± 14.4 mm, resident: 95.1 ± 14.8 mm, Mann-Whitney U test, p < 0.01, Table 2). When compared by daily age, the normalized deviation of daily growth rate among the three sampling areas was significantly different during 56–147 (with exception for 69, 76-78, and 140) daily age (p < 0.05, Kruskal-Wallis test). Between the off Noto Peninsula and off Goto Islands individuals, the post-hoc Steel-Dwass test showed that the normalized deviation of daily growth rate was significantly different during 56–103 (with exception for 69, 76-78, 89, and 97-98) daily age (Fig. 7, p < 0.05). Between the off Noto Peninsula and Tsushima Strait individuals, the deviation was significantly different between 71––75, 79–86, 88–139, and 141–147 daily age (Fig. 7, p < 0.05) , if the periods that showed significance more than 5 sequential days. When compared by calendar days, there was a significant difference among groups during 113–206 (with exception for 120, 152–157, 170 and 192–193) days from January 1st (late April to late July) (p < 0.05, Kruskal-Wallis test). The post-hoc Steel-Dwass test results showed that the normalized deviation of daily growth rate of the Tsushima Strait and off Goto Islands individuals were significantly different from those of the off Noto Peninsula individuals during 114–118 days (late April) and 185–191 (early July) and 194–206 days (middle July to late July) (Fig. 7, p < 0.05), respectively, if the periods that showed significance more than 5 sequential days. 4 Discussion The northward migration and the resident groups showed significant differences in growth trajectories. The mean BL in spring (March-May) was larger in the resident group (Fig. 6). This was likely because the mean hatch date of the resident group was earlier than that of the northward migration group (Table 2). No difference in the growth rate was observed between the resident group and the northward migration group up to 50 days after hatching (Fig. 7). However, the northward migration group grew faster 50 days after hatching than the resident group, and they became larger in June, despite their smaller size in spring (March-May). This suggests that individuals that grow relatively well during late spring and early summer within the population migrated northward. A migration pattern that includes both migratory and resident individuals is called partial migration, which is observed in various animals, including fish (Chapman et al., 2011, 2012). There are three types of seasonal partial migration of fish species (Chapman et al., 2012). The first is non-breeding partial migration, in which migrants and residents breed sympatrically, but spend non-breeding seasons separately. The second type is partial breeding migration, in which migrants and residents share a nonbreeding habitat but breed separately. The third is skipped breeding partial migration, in which migrants and residents share a non-breeding habitat, and individuals migrate to breed, but not every year, leading to partial migration. In addition to the above three types of partial migration, a shorter spatio-temporal partial migration is identified: partial diel vertical migration, in which migrants move vertically during the day or night while residents remain at the same depth (more details see Chapman et al., 2012). In the family of Japanese sardine, Clupea harengus shows the characteristic of the breeding partial migrants—they share a common feeding ground but migrate to different areas to spawn in the North Sea (Ruzzante et al., 2006). The Celtic Sea populations of C. harengus migrate into the Irish Sea for spawning; these migrants grow more slowly than residents and are therefore recruited later to the adult population (Burke et al., 2008). It is often observed that the body sizes of migrants and residents differ in animals who undergo partial migration (e.g., Kerr et al., 2009). Various hypotheses have been proposed regarding the factors that contribute to size differences (Chapman et al., 2011). The traditional “body size” hypothesis states that a larger body size is advantageous for residents because of their high physiological tolerance to adverse winter conditions (Ketterson and Nolan, 1976). However, exceptions to this hypothesis include birds, in which partial migrations have been well studied. Larger individuals of the male great bustard Otis tarda have been shown to migrate during the hot summer months; this has been attributed to the low tolerance for higher temperatures of the larger individuals compared to the smaller ones (Alonso et al., 2009). Additionally, larger individuals of tropical kingbirds, which have high energy requirements, tend to migrate (Jahn et al., 2010). Within skipjack tuna (Katsuwonus pelamis) tagged and released from the same location in the western North Pacific, higher percentages of larger (46 cm or larger) individuals were collected at higher latitudes than smaller (44 cm or smaller) individuals (Nihira, 1996). In addition, northwardmigrated skipjack tuna had higher energy consumption than those at lower latitudes (Aoki et al., 2017). These findings suggest that the higher energy requirements of larger individuals promote migration, even for fish species. Similarly, in the case of the Japanese sardine in the Sea of Japan, larger individuals might migrate to acquire more energy due to the increase in sea surface temperature around Kyushu. The water temperatures at depths of 10 m and 30 m on the west offshore of Kyushu were almost the same from February to June (Fig. 8). After June, however, the increase in water temperature at 10 m depth accelerated, and there was a difference between the water temperature at the depths of 10 m and 30 m due to the development of stratification. Excessive higher temperatures result in higher energy dissipation and demand substantial energy intake by consumption (Rudstam, 1988; Ito et al., 2013). The Japanese sardine might have avoided this by selecting one of the following two strategies: horizontally migrating northward at shallower depths or having deeper habitat depths and staying in the same area. Individuals with better growth and larger body size would have higher energy demands (Noguchi et al., 1990). Meanwhile, the abundance of zooplankton in the western Sea of Japan gradually decreases from spring to summer (Hirakawa et al., 1995); and zooplankton abundance and energy content in the northern Sea of Japan are higher than those in the western Sea of Japan during the summer months (Yasuda et al., 2021). The Japanese sardine in the northern offshore area had larger sizes and higher lipid contents (Yasuda et al., 2021). The Japanese sardines that were able to successfully reach the northern offshore area were rewarded with a better prey field. Thus, larger individuals that required more food may have migrated northward to remain in the optimal water temperature range and seek places where food is abundant. As partial migration was accompanied by habitat depth differences, this case may be considered a combination of non-breeding partial migration and partial vertical migration with larger migrants. In conclusion, we revealed migrations in the early life stages of the young-of-the-year Japanese sardine in the Sea of Japan in 2015 and 2016. They all hatched and grew west offshore of Kyushu until late June, and may have chosen one of the two strategies to avoid high temperatures within seasonal and geographical limits: migrating northward or moving deeper. Relatively well-grown individuals in summer were more likely to migrate northward to better feeding grounds, thereby suggesting that the environmental conditions in spawning and nursery grounds west offshore of Kyushu may be important for total energy acquisition during the first year of life. In future, it will be necessary to elucidate the factors that control the growth of individuals west of Kyushu. In addition, further analysis of the population structure is necessary to examine the contribution of individuals from spawning grounds in the Sea of Japan to the Tsushima Warm Current Stock. Conflict of Interest All the authors have no conflict of interest. Author Contributions Funding This study was partly supported by grants from the Fisheries Agency of Japan, Kurita Water and Environment Foundation, and JSPS KAKENHI (16H02944, 18H04921, 19H04247, 21H04735, 21K18653, and 22H05030). Acknowledgments This is a preprint to be submitted to a journal. 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Fisheries Agency of Japan and Japan Fisheries and Education Agency. (in Japanese). Retrieved from http://abchan.fra.go.jp/digests2018/details/201802.pdf Yatsu, A., Watanabe, T., Ishida, M., Sugisaki, H., & Jacobson, L. D. (2005). Environmental effects on recruitment and productivity of Japanese sardine Sardinops melanostictus and chub mackerel Scomber japonicus with recommendations for management. Fisheries Oceanography, 14(4), 263– 278. https://doi.org/10.1111/j.1365-2419.2005.00335.x Tables Supplementary Material 5 Supplementary Tables and Figures 5.1 Supplementary Tables TABLE S1. Summary of analytical results for all individuals analyzed for stable isotope analysis. The data will be available from doi: 10.6084/m9.figshare.25241842 after this manuscript is accepted. 5.2 Supplementary Figures Supplementary video 1. An example of otolith milling process in a one-year-old Japanese sardine collected in the Sea of Japan. The distance from the core to the edge of this otolith was 1428 μm. This is not the sample used in this study, but is shown here as an example. Double-click on the image to play it. This paper is available on arxiv under CC BY 4.0 DEED license. Authors: (1) Tomoya Aono, Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Chiba, Japan and National Institute of Technology, Ibaraki College, Hitachinaka, Ibaraki, Japan; (2) Tatsuya Sakamoto, Fisheries Resources Institute, Japan Fisheries Research and Education Agency, Nagasaki, Japan (3) Toyoho Ishimura, National Institute of Technology, Ibaraki College, Hitachinaka, Ibaraki, Japan and Graduate School of Human and Environmental Studies, Kyoto University, Kyoto, Japan; (4) Motomitsu Takahashi, Fisheries Resources Institute, Japan Fisheries Research and Education Agency, Nagasaki, Japan; (5) Tohya Yasuda, Fisheries Resources Institute, Japan Fisheries Research and Education Agency, Yokohama, Kanagawa, Japan; (6) Satoshi Kitajima, Fisheries Resources Institute, Japan Fisheries Research and Education Agency, Nagasaki, Japan; (7) Kozue Nishida, National Institute of Technology, Ibaraki College, Hitachinaka, Ibaraki, Japan and Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki, Japan; (8) Takayoshi Matsuura, National Institute of Technology, Ibaraki College, Hitachinaka, Ibaraki, Japan (9) Akito Ikari, National Institute of Technology, Ibaraki College, Hitachinaka, Ibaraki, Japan; (10) Shin-ichi Ito, Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Chiba, Japan. Authors: Authors: (1) Tomoya Aono, Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Chiba, Japan and National Institute of Technology, Ibaraki College, Hitachinaka, Ibaraki, Japan; (2) Tatsuya Sakamoto, Fisheries Resources Institute, Japan Fisheries Research and Education Agency, Nagasaki, Japan (3) Toyoho Ishimura, National Institute of Technology, Ibaraki College, Hitachinaka, Ibaraki, Japan and Graduate School of Human and Environmental Studies, Kyoto University, Kyoto, Japan; (4) Motomitsu Takahashi, Fisheries Resources Institute, Japan Fisheries Research and Education Agency, Nagasaki, Japan; (5) Tohya Yasuda, Fisheries Resources Institute, Japan Fisheries Research and Education Agency, Yokohama, Kanagawa, Japan; (6) Satoshi Kitajima, Fisheries Resources Institute, Japan Fisheries Research and Education Agency, Nagasaki, Japan; (7) Kozue Nishida, National Institute of Technology, Ibaraki College, Hitachinaka, Ibaraki, Japan and Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki, Japan; (8) Takayoshi Matsuura, National Institute of Technology, Ibaraki College, Hitachinaka, Ibaraki, Japan (9) Akito Ikari, National Institute of Technology, Ibaraki College, Hitachinaka, Ibaraki, Japan; (10) Shin-ichi Ito, Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Chiba, Japan. Table of Links Abstract and 1 Introduction 2 Materials & Methods 3 Results 4 Discussion Conflict of Interest, Author Contributions, Funding, Acknowledgments, Data Availability Reference 5 Supplementary Tables and Figures Abstract and 1 Introduction 2 Materials & Methods 3 Results 4 Discussion Conflict of Interest, Author Contributions, Funding, Acknowledgments, Data Availability Reference 5 Supplementary Tables and Figures Abstract The Japanese sardine ( Sardinops melanostictus ) is a small pelagic fish found in the Sea of Japan, the marginal sea of the western North Pacific. It is an important species for regional fisheries, but their transportation and migration patterns during early life stages remain unclear. In this study, we analyzed the stable oxygen isotope ratios of otoliths of young-of-the-year (age 0) Japanese sardines collected from the northern offshore and southern coastal areas of the Sea of Japan in 2015 and 2016. The ontogenetic shifts of the geographic distribution were estimated by comparing the profiles of life-long isotope ratios and temporally varying isoscape, which was calculated using the temperature and salinity fields produced by an ocean data assimilation model. Individuals that were collected in the northern and southern areas hatched and stayed in the southern areas (west offshore of Kyushu) until late June, and thereafter, they can be distinguished into two groups: one that migrated northward at shallow layer and one that stayed around the southern area in the deep layer. A comparison of somatic growth trajectories of the two groups, which was reconstructed based on otolith microstructure analysis, suggested that individuals that migrated northward had significantly larger body lengths in late June than those that stayed in the southern area. These results indicate that young-of-the-year Japanese sardines that hatched in the southern area may have been forced to choose one of two strategies to avoid extremely high water temperatures within seasonal and geographical limits. These include migrating northward or moving to deeper layers. Our results indicate that the environmental variabilities in the southern area could critically impact sardine population dynamics in the Sea of Japan. Sardinops melanostictus 1 Introduction The Japanese sardine ( Sardinops melanostictus ) is a species with large biomass fluctuations. The abundance of Japanese sardines showed substantial fluctuations of several orders of magnitude during the last 3000 years (Kuwae et al., 2017), and fluctuations have also been reported regarding the associated fisheries catch in recent centuries (Yasuda et al., 2019). These fluctuations are considered to be driven by environmental variabilities, which are often represented by the Pacific Decadal Oscillation (e.g., Chavez et al., 2003). Clarification of the mechanistic links between climate and marine environments and population fluctuation is necessary for the accurate prediction of resource abundance and fisheries management. Variations in survival rates during the post-hatching larval and juvenile stages are hypothesized to be of great importance for population fluctuations (e.g., Hjort, 1914). Therefore, the knowledge of the geographical distributions and environment of Japanese sardines during its critical life stages are essential for revealing the impact of climate and marine environment changes on population fluctuations. Sardinops melanostictus Current fisheries management of the Japanese sardine assumes two management units or stocks— the Pacific stock (distributed in the western North Pacific) and the Tsushima Warm Current Stock (distributed in the Sea of Japan), both of which show large fluctuations in abundance at similar time scales. While the patterns of transport and migration during the early life stages have been reported for the Pacific stock (e.g., Okunishi et al., 2009; Sakamoto et al., 2019), such knowledge for the Tsushima Warm Current Stock is insufficient. Spawning of the Tsushima Warm Current Stock occurs in coastal areas from west Kyushu to the Noto Peninsula from winter to early summer (January–June, Fig. 1). The main spawning ground changes depending on the sea surface temperature and spawning stock biomass (Furuichi et al., 2020). The young-of-the-year Japanese sardine is widely found from the off Noto Peninsula to the west coast of Kyushu in late summer (Ito, 1961; Yasuda et al., 2021). A recent study showed that the environment of the northern offshore area of the Sea of Japan with larger and lipid-rich prey zooplankton is suitable for the energy acquisition of sardine juveniles (Yasuda et al., 2021). In addition, the distribution of the stock is known to expand and shrink in response to population fluctuations; during periods of increased biomass, the distribution of the stock area expands to the northern offshore area of the Sea of Japan (Muko et al., 2018). These observations lead to the hypothesis that the successive and successful transportation (or migration) of juveniles to the northern offshore area might be the driver of the increase in stock (Muko et al., 2018; Yasuda et al., 2021). However, the origin, transportation, and migration routes of the individuals that reach the northern offshore area of the Sea of Japan have not yet been clarified. Understanding the movement patterns and their variety, and mechanisms that create the variety may, therefore, provide insights into energy acquisition strategies, population dynamics, and ultimately management of sardines in the region. 2 Materials & Methods 2.1 Fish sampling and Otolith δ 18 O analysis The young-of-the-years of Japanese sardines were collected for otolith analyses in three sampling areas (off Noto Peninsula, Tsushima Strait, and off Goto Islands) in the Sea of Japan from August to September in 2015 and 2016 by the R/V Yoko-maru, Japan Fisheries Research and Education Agency (Fig. 1; Table 1). Fish were frozen immediately after capture and preserved in -80 or -20 °C. Thereafter, the specimens were thawed in a laboratory on land and their scaled body length (BL) and body weight were measured. Sagittal otoliths were extracted, cleaned using a brush, rinsed with ethanol and distilled water, and dried at room temperature for several hours. The dried otoliths were embedded in epoxy resin (p-resin, Nichika Inc.) on a glass slide, and then placed in a dryer at 40 °C for at least a day to fix the otoliths. Thereafter, the embedded otoliths were polished with sandpaper (No. 1000, 2000) until the otolith core was exposed from the epoxy resin, and then the entire otolith was polished with alumina suspension (BAIKOWSKI International Corporation) to ensure that the daily rings could be easily observed under a microscope. The number of daily rings of the otolith and otolith daily increment widths were measured using an otolith measurement system (RATOC System Engineering Co. Ltd.). The otoliths of 154 individuals from 18 stations were used for daily ring measurements (Table 1). 2.3 Estimation of migration history To validate the estimated results, the estimated distribution area on the date closest to the sampling date for each individual was compared with the actual sampling area. In addition, the estimated distribution area on the date closest to the hatch date was compared with the results of a monthly egg and larval survey conducted at prefectural fisheries field stations (Oozeki et al., 2007; Furuichi et al., 2020). 2.4 Statistical analysis To examine the differences in biological characteristics between potentially different migratory types, namely the northward migration group (off Noto Peninsula individuals) and resident group (Tsushima Strait and off Goto Islands individuals; see Results and Discussion), we compared somatic growth trajectories between these groups. The Mann-Whitney U test for comparisons of hatching date and BL at the time of sampling was conducted between groups. We also compared the BL before sampling. BL before the time of sampling was calculated using the biological intercept method, assuming a linear relationship between the otolith radius and BL with fixed 5.9 mm of BL at the deposition of the first increment of the otolith, following Takahashi et al. (2008). To test for differences in the daily growth rates among the groups, anomalies of the 3-day running-mean otolith increment width normalized by standard deviation were compared among the three sampling areas using the Kruskal-Wallis test. The anomalies were calculated in two ways: for each day age of the fish and for each calendar day (days from January 1st each year). When a significant difference was detected, a post-hoc Steel-Dwass test was performed to identify areas with significant differences. 3 Results 3.4 Comparison of hatching dates, BL and daily growth rate differences There was a significant difference in the hatching dates between the northward migration group (63 ± 32 days from January 1st; mean ± 1SD) and the resident group (43 ± 30 days from January 1st) (Table 2, p < 0.02, Mann-Whitney U test). The mean BL of the northward group was 136.7 ± 6.4 mm and that of the resident group was 118.9 ± 9.4 mm. The BL of the northward group was significantly larger than that of the resident group (Table 2, p < 0.001, Mann-Whitney U test). In spring (March-May), the mean back-calculated BL of the resident group was larger than that of the northward migration group (Fig. 6). However, from June, the mean back-calculated BL of the northward migration group was higher than that of the resident group. The mean BL at July 1st, which roughly corresponds to the timing when migration patterns started to diverge, was significantly larger in the northward migration group (northward migration: 104.8 ± 14.4 mm, resident: 95.1 ± 14.8 mm, Mann-Whitney U test, p < 0.01, Table 2). When compared by daily age, the normalized deviation of daily growth rate among the three sampling areas was significantly different during 56–147 (with exception for 69, 76-78, and 140) daily age (p < 0.05, Kruskal-Wallis test). Between the off Noto Peninsula and off Goto Islands individuals, the post-hoc Steel-Dwass test showed that the normalized deviation of daily growth rate was significantly different during 56–103 (with exception for 69, 76-78, 89, and 97-98) daily age (Fig. 7, p < 0.05). Between the off Noto Peninsula and Tsushima Strait individuals, the deviation was significantly different between 71––75, 79–86, 88–139, and 141–147 daily age (Fig. 7, p < 0.05) , if the periods that showed significance more than 5 sequential days. When compared by calendar days, there was a significant difference among groups during 113–206 (with exception for 120, 152–157, 170 and 192–193) days from January 1st (late April to late July) (p < 0.05, Kruskal-Wallis test). The post-hoc Steel-Dwass test results showed that the normalized deviation of daily growth rate of the Tsushima Strait and off Goto Islands individuals were significantly different from those of the off Noto Peninsula individuals during 114–118 days (late April) and 185–191 (early July) and 194–206 days (middle July to late July) (Fig. 7, p < 0.05), respectively, if the periods that showed significance more than 5 sequential days. 4 Discussion The northward migration and the resident groups showed significant differences in growth trajectories. The mean BL in spring (March-May) was larger in the resident group (Fig. 6). This was likely because the mean hatch date of the resident group was earlier than that of the northward migration group (Table 2). No difference in the growth rate was observed between the resident group and the northward migration group up to 50 days after hatching (Fig. 7). However, the northward migration group grew faster 50 days after hatching than the resident group, and they became larger in June, despite their smaller size in spring (March-May). This suggests that individuals that grow relatively well during late spring and early summer within the population migrated northward. A migration pattern that includes both migratory and resident individuals is called partial migration, which is observed in various animals, including fish (Chapman et al., 2011, 2012). There are three types of seasonal partial migration of fish species (Chapman et al., 2012). The first is non-breeding partial migration, in which migrants and residents breed sympatrically, but spend non-breeding seasons separately. The second type is partial breeding migration, in which migrants and residents share a nonbreeding habitat but breed separately. The third is skipped breeding partial migration, in which migrants and residents share a non-breeding habitat, and individuals migrate to breed, but not every year, leading to partial migration. In addition to the above three types of partial migration, a shorter spatio-temporal partial migration is identified: partial diel vertical migration, in which migrants move vertically during the day or night while residents remain at the same depth (more details see Chapman et al., 2012). In the family of Japanese sardine, Clupea harengus shows the characteristic of the breeding partial migrants—they share a common feeding ground but migrate to different areas to spawn in the North Sea (Ruzzante et al., 2006). The Celtic Sea populations of C. harengus migrate into the Irish Sea for spawning; these migrants grow more slowly than residents and are therefore recruited later to the adult population (Burke et al., 2008). It is often observed that the body sizes of migrants and residents differ in animals who undergo partial migration (e.g., Kerr et al., 2009). Various hypotheses have been proposed regarding the factors that contribute to size differences (Chapman et al., 2011). The traditional “body size” hypothesis states that a larger body size is advantageous for residents because of their high physiological tolerance to adverse winter conditions (Ketterson and Nolan, 1976). However, exceptions to this hypothesis include birds, in which partial migrations have been well studied. Larger individuals of the male great bustard Otis tarda have been shown to migrate during the hot summer months; this has been attributed to the low tolerance for higher temperatures of the larger individuals compared to the smaller ones (Alonso et al., 2009). Additionally, larger individuals of tropical kingbirds, which have high energy requirements, tend to migrate (Jahn et al., 2010). Within skipjack tuna (Katsuwonus pelamis) tagged and released from the same location in the western North Pacific, higher percentages of larger (46 cm or larger) individuals were collected at higher latitudes than smaller (44 cm or smaller) individuals (Nihira, 1996). In addition, northwardmigrated skipjack tuna had higher energy consumption than those at lower latitudes (Aoki et al., 2017). These findings suggest that the higher energy requirements of larger individuals promote migration, even for fish species. Similarly, in the case of the Japanese sardine in the Sea of Japan, larger individuals might migrate to acquire more energy due to the increase in sea surface temperature around Kyushu. The water temperatures at depths of 10 m and 30 m on the west offshore of Kyushu were almost the same from February to June (Fig. 8). After June, however, the increase in water temperature at 10 m depth accelerated, and there was a difference between the water temperature at the depths of 10 m and 30 m due to the development of stratification. Excessive higher temperatures result in higher energy dissipation and demand substantial energy intake by consumption (Rudstam, 1988; Ito et al., 2013). The Japanese sardine might have avoided this by selecting one of the following two strategies: horizontally migrating northward at shallower depths or having deeper habitat depths and staying in the same area. Individuals with better growth and larger body size would have higher energy demands (Noguchi et al., 1990). Meanwhile, the abundance of zooplankton in the western Sea of Japan gradually decreases from spring to summer (Hirakawa et al., 1995); and zooplankton abundance and energy content in the northern Sea of Japan are higher than those in the western Sea of Japan during the summer months (Yasuda et al., 2021). The Japanese sardine in the northern offshore area had larger sizes and higher lipid contents (Yasuda et al., 2021). The Japanese sardines that were able to successfully reach the northern offshore area were rewarded with a better prey field. Thus, larger individuals that required more food may have migrated northward to remain in the optimal water temperature range and seek places where food is abundant. As partial migration was accompanied by habitat depth differences, this case may be considered a combination of non-breeding partial migration and partial vertical migration with larger migrants. In conclusion, we revealed migrations in the early life stages of the young-of-the-year Japanese sardine in the Sea of Japan in 2015 and 2016. They all hatched and grew west offshore of Kyushu until late June, and may have chosen one of the two strategies to avoid high temperatures within seasonal and geographical limits: migrating northward or moving deeper. Relatively well-grown individuals in summer were more likely to migrate northward to better feeding grounds, thereby suggesting that the environmental conditions in spawning and nursery grounds west offshore of Kyushu may be important for total energy acquisition during the first year of life. In future, it will be necessary to elucidate the factors that control the growth of individuals west of Kyushu. In addition, further analysis of the population structure is necessary to examine the contribution of individuals from spawning grounds in the Sea of Japan to the Tsushima Warm Current Stock. Conflict of Interest All the authors have no conflict of interest. Author Contributions Funding This study was partly supported by grants from the Fisheries Agency of Japan, Kurita Water and Environment Foundation, and JSPS KAKENHI (16H02944, 18H04921, 19H04247, 21H04735, 21K18653, and 22H05030). Acknowledgments This is a preprint to be submitted to a journal. 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An example of otolith milling process in a one-year-old Japanese sardine collected in the Sea of Japan. The distance from the core to the edge of this otolith was 1428 μm. This is not the sample used in this study, but is shown here as an example. Double-click on the image to play it. This paper is available on arxiv under CC BY 4.0 DEED license. This paper is available on arxiv under CC BY 4.0 DEED license. available on arxiv