1 INTRODUCTION

The Japanese Spanish mackerel Scomberomorus niphonius is a pelagic, neritic species that occurs widely throughout northwestern Pacific Ocean subtropical and temperate waters (Zhang et al., 2016; Kitada et al., 2017; Jiang et al., 2020). This species is one of the most valuable of commercial fishes in China, with an annual catch exceeding 300 000 t since the late 1990s (Ministry of Agriculture and Rural Affairs of the People's Republic of China, 2020; Wan et al., 2020). However, long-term fishing pressure and environmental change caused apparent changes in population traits of S. niphonius, including lower age structure (Chiba et al., 2008), miniaturized body size (Mu et al., 2018), earlier sexual maturation (Qiu and Ye, 1996), prolonged reproductive period (Yuan et al., 2009), a northward-shifting distribution (Zhang et al., 2013), and an accelerated early growth rate (Zhu et al., 2020).

In particular, the timing of spawning is crucial to recruitment success and associated largely with water temperature. While for species such as sole (Solea solea), low temperature can delay spawning (Fincham et al., 2013), in others such as capelin (Mallotus villosus), warmer temperatures can advance spawning (Carscadden et al., 1997). Different spawning times may lead to differences in growth and development, leading to a match-mismatch between larval and juvenile presence and the resources they require for growth (Houde, 2008). Changes in temperature dramatically affect mortality and recruitment by altering growth rate and extending or reducing developmental duration (Takasuka et al., 2008). For S. niphonius, egg abundance is related to sea surface temperature (SST) (Song et al., 2016), embryological development is closely related to temperature (Jiang et al., 2016), and the timing of its spawning (crucial to recruitment success) is also largely associated with water temperature. However, it is unknown if recent changes in environmental temperature have influenced the timing of spawning of S. niphonius.

Otolith microstructure commonly used to determine the age and growth patterns in fish (Campana and Neilson, 1985; Clark Barkalow et al., 2020). This technique provides key information on growth variation and life history events (Hall et al., 2019) such as hatching, feeding, metamorphosis, migration, and sudden changes in the environment (Campana and Neilson, 1985; Kupchik and Shaw, 2016). Rings on the otoliths of S. niphonius are deposited daily (Shoji et al., 1999), which, through back-calculation, enables reconstruction of spawning periods, and facilitates understanding how environmental factors may influence the spawning period.

We systematically retrospect the spawning period of S. niphonius through otolith microstructure analysis of samples collected over three years from the main spawning grounds of this species in the northern Yellow Sea (NYS). We build a linear regression model to identify the effect water temperature has on the spawning period. Our objectives are to (1) explore temporal variation in the spawning period of S. niphonius; (2) study the relationships between spawning in S. niphonius and water temperature; and (3) advance understanding of S. niphonius spawning and early life history.

2 MATERIAL AND METHOD 2.1 Study area and sample collection

A total of 145 young-of-the-year (YoY) S. niphonius were collected during trawl surveys in coastal waters of the NYS (Fig. 1) in August or September of 2017, 2018, and 2020 (Table 1). All samples were ice-frozen and transported to laboratory for analysis. Fork length (FL, to nearest 1 mm) and body weight (W, to nearest 0.1 g) of each individual were measured, and the sagittal otoliths were extracted.

2.2 Otolith microstructure analysis

The right otolith of each individual was embedded in epoxy resin, and transverse sections (approximately 550 μm thick) were obtained by cutting the otolith core using a Buehler IsoMet saw. Sections were mounted on glass microscope slide using thermoplastic glue (Crystal Bond 502), then ground with waterproof abrasive paper (240–4 000 grit) until thin sections with clear increment sequences along the ventral axis could be counted. Microstructure images were captured at ×400 using an Olympus microscope coupled with an optical camera system.

Daily age was determined by counting the number of opaque zones, read with ImageJ software along a consistent axis of count on the ventral lobe (Fig. 2). Each sample was counted three times independently by the same observer, and counted independently every other month to ensure reading accuracy (Campana, 1984). If a reading error exceeded 10%, a sample was removed. Shoji et al. (2001) studied S. niphonius through artificial fertilization, and found that starts feeding commences after 5 d, and a feeding ring develops after 5 d (Shoji and Tanaka, 2005; Kono et al., 2014). Therefore, the spawning date can be back-calculated from the fishing date by subtracting age (d) determined from the otolith opaque ring count, and adding 5.

2.3 Water temperature data and trend analysis

SST is considered as an important environmental factor influences pelagic fish spawning (Munk, 2007; Takasuka et al., 2007; Murphy et al., 2013). Daily SST data for the NYS (37°00′N–39°00′N, 120°30′E–123°30′E) with 0.05°×0.05° horizontal grid resolution were obtained in situ and using infrared and microwave radiometer satellite data from the Copernicus Marine Environment Monitoring Service website (https://resources.marine.copernicus.eu/products). Data were analyzed by univariate statistics to identify significant temporal differences in SST, with SST set as a dependent variable, years as fixed factors, and date as a covariable. We set 2018 SST data as a standard, and subtracted 2018 SST data records from those for 2017 and 2020 to identify change.

2.4 Spawning date estimation

The spawning dates of S. niphonius were estimated by back-calculation of the daily ages and caputure dates, the distribution of spawning period was determined accordingly. To explore variation in the timing of spawning between years, we calculated the proportion of spawning individuals on each day of each year from the spawning period to the total number, i.e., the spawning frequency, then the cumulative spawning frequency of each day is used to represent the spawning trend for subsequent analysis. The time integral of daily temperature measured from the beginning to the end of the spawning period is expressed as the growing degree-day (GDD, ℃·day) (cumulative SST), which we use to analyze the relationship between cumulative spawning frequency and temperature (Neuheimer and Taggart, 2007). A linear regression between the cumulative spawning frequency (dependent variable) and GDD (independent variables) was prepared. To identify significant temporal differences in the variation trend of spawning with temperature, we used cumulative spawning frequency as a dependent variable, years as fixed factors, and GDD as covariables in an analysis of covariance (ANCOVA), using SPSS. The slope and intercept of the linear regression were analyzed and tested by ANCOVA. The linear regression equation is:

where y is the proportion of S. niphonius in every day i that are in cumulative spawning frequency, x_i is the GDD, and b₀ the intercept and b₁ the slope.

3 RESULT 3.1 Trends in water temperature

Average daily SST increased gradually each year during the spawning period (April–June) (Fig. 3a). The SST in 2017 on April 19 first reached 10 ℃, and was the highest overall temperature in the three years (Fig. 3a–b). The analysis of covariance (ANCOVA) reveals a significant difference between years (P < 0.05) (Fig. 3a–b), with significant differences between 2017 and 2020 (P=0.00), and between 2018 and 2020 (P=0.01). Three years of temperature show a similar but lower increasing warming trend in 2018 than in 2017, although in 2020 the increase in water temperature was slowest in May, and the lowest temperature for the three years (Fig. 3b).

3.2 Spawning period

By back-calculation we determined the spawning dates of S. niphonius to extend from April to June each year (Fig. 4). Spawning period in 2017 was early and extended from April 23 to June 1 (Fig. 4a), whereas that in 2018 extended from May 7 to June 29 (Fig. 4b), and that for 2020 from May 6 to June 22 (Fig. 4c). The spawning peak differed each year, occurring late, from late May to mid-June, in 2020, from early May in 2017, and from mid-to-late May to early June in 2018.

3.3 Relationships between SST and spawning trends

The relationship between GDD and cumulative spawning frequency is linear, and the influence of GDD on cumulative spawning frequency is statistically significant (2017, y=0.2632x+4.9602, R²=0.982, P < 0.001; 2018, y=0.2068x–1.3924, R²=0.997, P < 0.001; 2020, y=0.2408x+3.4856, R²=0.974, P < 0.001, Table 2, Fig. 5). Temperature explains most variation in cumulative spawning frequency, but significant differences exist between 2017 and 2020 (ANCOVA: different slopes, P < 0.05; different intercepts, P=0.00), and between 2018 and 2020 (ANCOVA: different slopes, P=0.00; different intercepts, P= 0.00). Differences between 2017 and 2018 were significant (ANCOVA: different slopes, P=0.00; different intercepts, P=0.00). The slope in 2017 was the highest, and the spawning period was completed at a GDD of 383 ℃·day. The slope was lowest in 2018, with the GDD reaching 506 ℃·day before spawning ended. Although the spawning frequency was initially low in 2020, it increased rapidly, and spawning period ended earlier than in 2018 at a GDD of 448 ℃·day. Although overall GDD varied greatly over time, the initial spawning temperature ranged 10.46–12.00 ℃ (Fig. 5).

4 DISCUSSION

We report interannual variation in the timing and duration of spawning of S. niphonius in the NYS using otolith microstructure analysis. Linear regressions confirm the significant effect of water temperature on spawning period of S. niphonius, a spawning water temperature adaptation, and improve our understanding of the spawning dynamics of this species.

In this study, the otolith daily increment of 145 YoY S. niphonius was back-calculated to determine the spawning periods, to obtain the initial condition of fish life history more accurately and systematically. S. niphonius is a multiple reproductive fish that typically spawns 2 or 3 times during a spawning season (Nakajima et al., 2013; Zhang et al., 2013), which was previously confirmed based on histological analysis gonad tissues and changes in egg diameter (Li et al., 1990; Qiu and Ye, 1994). Spawning of S. niphonius in the Yellow-Bohai seas between 1960 to 1993 extended from May to July (Qiu and Ye, 1996), and in 2016 and 2017 extended from April to June (Mu et al., 2018). We report the spawning period in the NYS to extend from mid-April to late June in 2017, 2018, and 2020, but to differ considerably between years. This suggests that a shift in the spawning period of S. niphonius in this region has occurred since data were first collected (Yuan et al., 2009; Mu et al., 2018). As previous studies suggested that the prolonged spawning period could be a function of lowered age structure because of overfishing (Wei, 1980; Qiu and Ye, 1994). With prolonged fishing pressure, earlier maturing fishes (mostly age 1 individuals) might need more time to acquire energy reserves to reach spawning condition. Therefore, advanced gonad maturation might extend the spawning period of S. niphonius (Qiu and Ye, 1996; Wan et al., 2020). According to the results of our three-year study, which also confirmed the conclusion of previous studies, the spawning period of the S. niphonius appeared earlier and longer.

For many fish species, the spawning period is sensitive to environmental factors that regulate or trigger it (Moltó et al., 2020; Fujita et al., 2021). We report significant temporal differences in spawning dates of S. niphonius, but the temperature at which spawning commenced was maintained in 10–12 ℃. This result is consistent with expectation because of the high temperature sensitivity of S. niphonius. The 10 ℃ isotherm determines whether S. niphonius enters fishing grounds or not during its spawning migration (Wei, 1980). We confirm that water temperature is a determinant of the spawning migration and spawning process of S. niphonius. With development of marine environment monitoring techniques, the recognition of this close relationship between temperature and spawning in this species will enable more efficient population management. Although the spawning period varied between years, the temperature at which spawning occurred remained relatively stable. Because average spring (March 1–May 31) water temperatures in the Yellow Sea have increased in recent years (Park et al., 2015), spawning of S. niphonius may well have advanced also. Water temperature in Yellow Sea is influenced by multiple factors including Cold Water Mass and Warm Current (Oh et al., 2013; Yu et al., 2022), coastal currents, Kuroshio Current and monsoon (Naimie et al., 2001), showing a large interannual-decadal variability. Particularly, SSTs during spring to early summer generally show rapid increase with large variability. In the three years of this study, 2017 was a warm year and 2020 was a cold year compared to 2018. However, the summer of 2020 showed a rapid warming (Fig. 3). The reason for the different annual variation in SST is not clear at this moment, but the interannual variation in SST, particularly the large difference in the seasonal variation may have a significant effect on spawning duration.

Temperature affects when spawning commences, the duration of spawning, and when peaks in spawning occur. The linear relationship between GDD and cumulative spawning frequency largely explains the relationship between water temperature and spawning period. The highest temperatures in 2017 correspond to early start and end spawning dates, and the GDD was lower, supporting the hypothesis that warming of the NYS is related to the advanced spawning of S. niphonius. The lowest rate of warming in 2018 corresponds to an extended spawning period and high GDD. After May 2020, temperatures rose faster and spawning frequency is relatively high, and the GDD required for spawning is lower than in 2018. Accordingly, we conclude that spawning in S. niphonius is affected by increasing temperature, suggesting also that the spawning dynamics of reproductive populations are adapted to temperature.

5 CONCLUSION

Analysis of otolith microstructure reveals the spawning period of S. niphonius in the NYS in 2017, 2018, and 2020, which occurs from late April to late June (spring to early summer) on different starting and ending days. Water temperature was the main factor on the spawning duration and fluctuation. Accordingly, variations in water temperature might be resulted from climate or regional oceanic change, which could affect the spawning dynamics of this species and recruitment, providing information for the management of this fishery resource. For the future perspectives, as long as this study focuses on the microstructure of otoliths, it has not carried out the analysis of otolith microchemistry, the stock structure and migration of this species are not determined. Furthermore, whether the change of spawning will affect the later growth of adult fishes needs to be discussed in combination with the daily increment.

6 DATA AVAILABILITY STATEMENT

Data generated or analyzed in this study are available from the corresponding author on reasonable request.

7 ACKNOWLEDGMENT

We thank the investigators who participated in the seasonal trawl survey.