Study on Trace Element Characteristics in Otoliths of Pacific Saury (Cololabis saira) in Northwest Pacific Ocean

Abstract

The Pacific saury (Cololabis saira), widely distributed in the North Pacific Ocean, is a significant pelagic fishery species in China and has been designated as a priority management species by the North Pacific Fisheries Commission (NPFC). This study examined the trace element characteristics of Pacific saury otoliths and the migration patterns of this species. Based on samples collected from the high seas of the Northwest Pacific Ocean, we estimated their daily age, measured the trace element contents of the otoliths at various life history stages, and analyzed the Sr/Ca, Ba/Ca, Mg/Ca, and Na/Ca values in the otoliths and their relationship with sea surface temperature (SST) changes. The main findings were as follows: (1) Cluster analysis showed significant differences (p < 0.05) in the Sr/Ca, Ba/Ca, Mg/Ca, and Na/Ca values in the core regions of otoliths among the clusters. (2) An analysis of the elemental characteristics across life history stages showed significant differences (p < 0.05) in the Sr/Ca values prior to the juvenile stage (31~90 d) and following the young stage (91~180 d). Significant variations (p < 0.05) in the Ba/Ca values during the juvenile and immature stages imply vertical migration behavior. Additionally, the Mg/Ca and Na/Ca values in adult stages showed significant differences (p < 0.05) to those in early life history stages. (3) GAM fitting and cross-correlation function tests demonstrated a statistically significant (p < 0.05) nonlinear lagged relationship between the otolith Sr/Ca values and SST.

1. Introduction

The Pacific saury (Cololabis saira), a cold-water pelagic migratory species, is widely distributed across the northern Pacific Ocean in waters ranging from subtropical to temperate [1]. Its optimal temperature range is 10~24 °C, with its primary fishing grounds mainly located in areas where the water temperature ranges from 11 to 15 °C [2,3]. Its distribution spans from subtropical regions through the complex Kuroshio–Oyashio Mixed Water region to subarctic zones [4]. Typically, the Pacific saury inhabits the sea surface layer, although its eggs have occasionally been found at depths of up to 30 m [5]. Once established in 2015, the North Pacific Fisheries Commission (NPFC) designated the Pacific saury as a priority species for fishery management [6]. Consequently, research on the resource status and habitat distribution of the Pacific saury has attracted considerable attention [7].

In the early 20th century, ex situ marking techniques were applied to the study of migrations in aquatic organisms [8]. From the 1950s onwards, advances in electronic tagging technology improved the accuracy of migration path monitoring [8]. However, the mark–recapture method is difficult to apply to small pelagic species such as the Pacific saury. Since the 21st century, advancements in computer models, satellite remote sensing data analysis, and methodologies involving trace element and stable isotope analyses have significantly expanded research on the migratory patterns of aquatic organisms such as the Pacific saury [8,9,10]. A recent study indicates that the Pacific saury exhibits a seasonal migration pattern, moving northward during the spring and summer and southward during the autumn and winter [11]. The spawning grounds for the Pacific saury are primarily located in the western North Pacific’s subtropical and mixed-water zones, specifically within the Kuroshio and Kuroshio Extension regions, and are inhabited from early autumn to late spring in the following year [12]. As Pacific saury reach the juvenile or young stages, they begin migrating northward independently, reaching near-subarctic regions by the end of the summer [13]. Upon reaching maturity, they migrate southward again, arriving in the subtropical Kuroshio waters or Kuroshio–Oyashio transition zone to spawn during winter [14]. Thereafter, they may continue their migration further south and west towards coastal regions west of 155 °E [14,15]. However, owing to our inability to accurately estimate the age of Pacific saury, precise differentiation among distinct spawning groups cannot be achieved based on biological traits such as their daily age or body length. Additionally, the precise prediction of the start of migration dates is complicated by annual variations in the marine environmental conditions and fluctuations in the fish abundance across different sea areas. Therefore, investigating the use of otolith trace element characteristics to study the Pacific saury’s migratory patterns in the high seas is of great importance.

The elements deposited in otoliths record rich environmental information throughout the life histories of individual fish, serving as an ideal natural marker [16]. Otolith microchemistry can be utilized to investigate fish life histories, such as by reconstructing habitat experiences and migration pathways [17]. The strontium (Sr) content in otoliths can indicate changes in the environmental temperature, and the relationship between otolith Sr/calcium (Ca) values and the water temperature can be used to determine the environmental conditions during specific life history stages [18,19,20] as well as the patterns of migration between freshwater and marine environments [19,20,21,22]. The barium (Ba) content in otoliths is closely related to oceanic upwelling. Otolith Ba/Ca values are widely used to study the patterns of fish migration among offshore, coastal, and estuarine habitats [23,24]. Vertical migrations across water layers can also be inferred from the relationship between the Ba/Ca values and water depth [25]. In addition, the magnesium (Mg) and sodium (Na) concentrations in otoliths reflect fish growth and physiological characteristics and are frequently used to differentiate fish populations and habitats [26,27,28]. Trace elements in the otolith core reflect the environmental conditions at the time of hatching [29,30], while those at the otolith edge reflect the environmental conditions at the time of capture [31]. By analyzing the trace element content from the core to the edge and the corresponding environmental factors affecting growth, differences in the hatching locations and capture sites can be identified, and the migration routes and environmental changes experienced by individual fish over time and space can be reconstructed [32].

In summary, to analyze the microchemical characteristics of otoliths across the major life history stages of Pacific saury, this study estimated the daily age of Pacific saury samples using their otoliths (left sagittae) and measured the Sr, Ba, Mg, Na, and Ca content at different life history stages using laser ablation–inductively coupled plasma mass spectrometry (LA-ICP-MS). This investigation explored the relationships between the otolith Sr/Ca, Ba/Ca, Mg/Ca, and Na/Ca values and life history stages as well as the sea surface temperature (SST), analyzed the environmental characteristics experienced during different life stages, and provided preliminary inferences on the migratory patterns of Pacific saury throughout their life history. This research aims to provide a foundational reference for understanding the migratory distribution of Pacific saury as well as forecasting fishing seasons and managing resources for this species.

2. Materials and Methods

2.1. Sample Collection

The Pacific saury samples used in this study were collected from the high seas of the North Pacific using the fishing vessels “Guo Ji 908”, “Lupeng Yuanyu 029”, and “Lupeng Yuanyu 078”. The fishing operation method was stick-held dip net (a type of lift net operated from the vessel’s side) fishing. Sampling occurred during June to September in 2023 and 2024. The sampling areas were located at 41°55′~48°22′ N, 151°14′~167°08′ E; 43°52′~49°16′ N, 156°28′~167°25′ E; and 43°50′–48°19′ N, 157°04′–168°00′ E (Figure 1). A total of 72 Pacific saury samples were initially selected for microchemical otolith analysis. However, due to the small size and structural fragility of Pacific saury otoliths, substantial sample attrition occurred during the analytical procedures, particularly during precision grinding and laser ablation preparation. Following strict quality control protocols that excluded specimens with (1) physical damage, (2) ambiguous laser ablation signals, and (3) potential contamination, 34 samples met the quality criteria for further analysis.

2.2. Environmental Data

The sea surface temperature (SST) data for the entire period from 2022 to 2024 were sourced from the National Oceanic and Atmospheric Administration (NOAA; ftp.nodc.noaa.gov, accessed on 13 June 2025). The spatial resolution was 0.01° × 0.01°, with a temporal resolution of one day.

2.3. Sample Analysis

2.3.1. Basic Biological Measurements

Basic biological parameters such as the sex, body length, and body weight of the samples were measured. The measurement process was conducted in accordance with the “GB/T Oceanographic Survey Standards—Part 6: Marine Biological Investigations”.

2.3.2. Daily Age Determination

Place the otolith horizontally in a rectangular plastic mold and embed it with prepared cold-mounting resin. Then grind the mold along the long axis of the otolith using 80-grit, 1200-grit, and 2000-grit waterproof, wear-resistant abrasive paper. Finally, polish the otolith with 2500-grit polishing paper until its core is clearly visible, resulting in prepared otolith sections.

Under an Olympus optical microscope (10× eyepiece, 40× objective, EVIDENT CORPORATION NAGANO 399-0495, Japan), otolith sections were imaged using the built-in FCSnap 2003–2022 software, then stitched together using Adobe Photoshop 2023. Have three independent readers count the otolith increments. If the difference between each reader’s count and the mean is less than 5%, the count is considered accurate. Otherwise, recount until the desired accuracy is achieved. Each increment (daily ring) represents one day of growth (daily age) in Pacific saury. The final daily age of the otolith is represented by the average of the three counts [18,34].

2.3.3. Otolith Trace Element Measurement

In this study, sample points were selected at 100 µm [18] intervals along the polished side of the otolith section from the core to the edge. If the remaining distance to the edge was short, additional sampling points were added closer to the edge (Figure 2). A laser ablation–inductively coupled plasma mass spectrometer (LA-ICP-MS) [35] was used to measure the trace element content of Ca, Sr, Ba, Mg, and Na in the otoliths, and the values of Sr/Ca, Ba/Ca, Mg/Ca, and Na/Ca were calculated. The laser ablation spot diameter was 50 µm, with a frequency of 10 Hz, an ablation time of 40 s, an ablation depth of 1 µm, and a laser energy density of 7 J/cm². Calibration was performed using four reference materials: NIST610, MACS-3, BHVO-2G, and BIR-1G. During the analysis, two reference standards (NIST610 and MACS-3) were used every ten samples. Given that the content of Ca was much higher than that of the other elements in the otolith, the element ratios were standardized according to international conventions as “(X content/Ca content) × 10³” (referred to as the X/Ca value, where X represents each measured element; unit: mmol/mol) [22,36].

2.4. Data Preprocessing

2.4.1. Classification of Different Life History Stages by Daily Age

The life history of the Pacific saury can generally be divided into six stages: eggs (0 d), the larval stage (1~30 d), the juvenile stage (31~90 d), the young stage (91~180 d), the immature stage (181~270 d), and the adult stage (>270 d) [5,37]. According to its daily age corresponding to each sampling point, each sampled point along the otolith of an individual fish was assigned to its respective life history stage.

2.4.2. Back-Calculation of Dates

Given the capture date of a sample, the hatching date was back-calculated based on the otolith’s daily age [38,39]. Accordingly, this study estimated the approximate dates when each Pacific saury sample reached the sampling points during its growth cycle by estimating the growth ages on the otoliths, thus determining the time periods corresponding to each growth stage of each sample. Formula (1) shows the method for estimating the dates corresponding to each point on the otoliths:

$$\mathrm{D}\mathrm{a}\mathrm{t}\mathrm{e} \mathrm{o}\mathrm{f} \mathrm{p}\mathrm{o}\mathrm{i}\mathrm{n}\mathrm{t} \mathrm{X} \mathrm{g}\mathrm{r}\mathrm{o}\mathrm{w}\mathrm{t}\mathrm{h}=\mathrm{C}\mathrm{a}\mathrm{p}\mathrm{t}\mathrm{u}\mathrm{r}\mathrm{e} \mathrm{d}\mathrm{a}\mathrm{t}\mathrm{e}-\mathrm{D}\mathrm{a}\mathrm{i}\mathrm{l}\mathrm{y} \mathrm{a}\mathrm{g}\mathrm{e} \mathrm{a}\mathrm{t} \mathrm{p}\mathrm{o}\mathrm{i}\mathrm{n}\mathrm{t} \mathrm{X}$$

(1)

where “X” represents the otolith sampling points of the Pacific saury samples, the “Capture date” refers to the exact date when the fish was caught, and the “Daily age at point X” represents the number of daily rings at that particular otolith sampling location.

2.5. Analytical Methods

2.5.1. Differential Analysis

To investigate whether there are differences in the otolith trace element content between male and female Pacific saury samples, KW-H (Kruskal–Wallis H) tests were conducted on the Sr/Ca, Ba/Ca, Mg/Ca, and Na/Ca values in the core region of otoliths, as well as on the overall Sr/Ca, Ba/Ca, Mg/Ca, and Na/Ca values of the otoliths (calculated as the average of all sampling points within an individual otolith) for both sexes. To assess the potential variability in the hatching locations of the sampled Pacific saury, a hierarchical cluster analysis was performed on the Sr/Ca, Ba/Ca, Mg/Ca, and Na/Ca values for the otolith core (Point 1), followed by KW-H tests for clustering results. To evaluate any potential significant differences in water temperature during their life history, MW-U (Mann–Whitney U) tests were performed on the Sr/Ca values at distinct life history stages. To examine the potential of vertical migration through the water layers during the life history of Pacific saury, MW-U tests were applied to the Ba/Ca values at distinct life history stages.

2.5.2. Correlation Analysis

To explore the horizontal spatial migration patterns of the Pacific saury samples and the timing of their migration initiation, we used daily SST data for the entire study area collected from 2022 to 2024. Using a time-series approach, a generalized additive model (GAM) was applied to fit the relationship between the otolith Sr/Ca values and SST, as well as the time (segmented into six-month intervals). The trends were analyzed using the pygam package (Python 3.11) to construct the GAM, along with the following formula:

$$y= \beta +s\left(x\right)+ \epsilon$$

(2)

where y is the response variable (Sr/Ca value), β is the intercept term, x represents the explanatory variables (SST or time), and ε is the residual error.

To assess the lagged correlations between the otolith Sr/Ca values and the SST, a cross-correlation function (CCF) test was conducted. Spearman’s rank correlation test was then performed on the results to evaluate the significance of the relationship.

3. Results

3.1. Trace Element Characteristics of Otoliths

The otolith trace element characteristics were analyzed for a total of 34 Pacific saury individuals, including 18 females and 16 males. The collected samples were primarily in the young (2), immature (12) and adult (20) stages. Their body lengths ranged from 238 to 305 mm (277 ± 13 mm), and their daily ages ranged from 102 to 438 days (287 ± 74 d). Their Sr/Ca values (based on individual measurements from each sampling point) ranged from 3.90 to 12.21 (7.36 ± 1.26 mmol/mol), their Ba/Ca values from 0.001 to 0.200 (0.015 ± 0.029 mmol/mol), their Mg/Ca values from 0.02 to 1.00 (0.10 ± 0.11 mmol/mol), and their Na/Ca values from 5.21 to 9.81 (7.40 ± 0.79 mmol/mol). The samples mainly hatched in the autumn (

Table 1. Trace element characteristics of Pacific saury sample otoliths.

Sampling Month		June	July	August	September
Body length/mm		238~287	266~288	268~305	259~303
Daily age/d		145~428	102~438	197~374	199~381
Sr/Ca, mmol·mol−1		7.72 ± 1.41	7.50 ± 1.30	7.18 ± 1.03	7.11 ± 1.20
Ba/Ca, mmol·mol−1		0.012 ± 0.017	0.007 ± 0.008	0.013 ± 0.023	0.026 ± 0.043
Mg/Ca, mmol·mol−1		0.10 ± 0.15	0.10 ± 0.03	0.09 ± 0.03	0.12 ± 0.13
Na/Ca, mmol·mol−1		7.39 ± 0.90	7.68 ± 0.44	7.38 ± 0.56	7.25 ± 0.99
Sample size		9	7	8	10
Breeding season	Spring	3	1	2	2
	Summer	4	3	5	5
	Autumn	1	1	1	2
	Winter	6	1	5	6
Sex	Female	3	6	3	4
	Male	3	1	2	2

).

3.2. Distribution of Characteristics Between Sexes

The KW-H test results for the otolith Sr/Ca and Ba/Ca values (

Table 2. KW-H results for differences in otolith Sr/Ca, Ba/Ca, Mg/Ca, and Na/Ca values between male and female samples.

Area	Sr/Ca		Ba/Ca		Mg/Ca		Na/Ca
	H	p	H	p	H	p	H	p
Core area	0.019	0.890	0.744	0.388	0.686	0.408	0.744	0.388
Entire area	2.018	0.155	0.723	0.395	0.340	0.560	0.046	0.830

) show that there were no significant differences (p > 0.05) in the Sr/Ca, Ba/Ca, Mg/Ca, and Na/Ca values in either the core region or the whole otolith between the male and female Pacific saury samples.

3.3. Distribution Characteristics of Otolith Core Regions

The hierarchical clustering analysis of the Sr/Ca values in the otolith core regions of the Pacific saury samples (Figure 3a) classified samples with values of less than 6.00 mmol/mol as Group 3, those with Sr/Ca values between 6.00 and 7.50 mmol/mol as Group 1, those with values between 7.50 and 10.00 mmol/mol as Group 2, and those with values greater than 10.00 mmol/mol as Group 4. The KW-H test indicated significant differences (p < 0.05) in the core Sr/Ca values among Groups 1, 2, 3, and 4, confirming the statistical validity of the grouping.

Regarding the Ba/Ca values in the otolith core region (Figure 3b), samples with Ba/Ca values less than 0.01 mmol/mol were classified as Group 2, those with values between 0.01 and 0.05 mmol/mol were classified as Group 1, and those with values greater than 0.05 mmol/mol were classified as Group 3. The KW-H test indicated significant differences (p < 0.05) in the core Ba/Ca values among Groups 1, 2, and 3, confirming statistically meaningful grouping.

The clustering of the Mg/Ca values in the otolith cores region (Figure 3c) classified samples with Mg/Ca values of less than 0.13 mmol/mol as Group 2, those with values between 0.13 and 0.65 mmol/mol as Group 1, and those with values above 0.65 mmol/mol as Group 3. The KW-H test indicated significant differences (p < 0.05) in the core Mg/Ca value among Groups 1, 2, and 3, supporting the reliability of the classification.

Regarding the Na/Ca values in the otolith core region (Figure 3d), samples with Na/Ca values of below 6.50 mmol/mol were assigned to Group 1, those with values between 6.50 and 7.50 mmol/mol were assigned to Group 2, and those with values exceeding 7.50 mmol/mol were assigned to Group 3. The KW-H test indicated significant differences (p < 0.05) among these groups, demonstrating that the grouping was statistically valid.

3.4. Distribution of Characteristics Across Life History Stages

The MW-U test results for the Sr/Ca values across the life history stages (Figure 4a) show that there were significant differences (p < 0.05) between the otolith Sr/Ca values during the egg, larval, and juvenile stages and those during the young, immature, and adult stages. Regarding the Ba/Ca values (Figure 4b), significant differences (p < 0.05) were found between the larval stage and all the other life history stages, as well as between the immature stage and all the other stages. Regarding the Mg/Ca values (Figure 4c), the otolith Mg/Ca values in both the immature and adult stages were significantly (p < 0.05) different from those in all the other life history stages. The Na/Ca values (Figure 4d) in the adult stage showed significant differences (p < 0.05) from those in all the other life history stages.

3.5. Relationship Between Otolith Sr/Ca Values and SST

A correlation analysis of the otolith Sr/Ca values and the annual SST across the entire study area showed that, under the time series framework, a generalized additive model (GAM) could be successfully fitted between the otolith Sr/Ca values and the SST (p < 0.05). We divided the timeline into six-month intervals (Periods I–V), and the GAM fitting results for each period are shown in Figure 5. In Period I (March to August 2022), the otolith Sr/Ca values initially decreased and then increased with a rising SST, reaching a minimum around June 2022. In Period II (September 2022 to February 2023), the Sr/Ca values generally decreased as the SST declined. In Period III (March to August 2023), the Sr/Ca values first increased and then decreased with a rising SST, peaking around July 2023 before gradually declining. In Period IV (September 2023 to February 2024), the Sr/Ca values first decreased and then increased with a falling SST, reaching a minimum around October 2023. In Period V (March 2024 to August 2024), the Sr/Ca values first decreased and then increased with a rising SST, reaching a minimum around June 2024.

A cross-correlation function (CCF) analysis of the otolith Sr/Ca values and SST (Figure 6) revealed that the maximum correlation coefficient corresponded to a lag of 44 days (p < 0.05). Spearman’s rank correlation test indicated a significant negative correlation between the otolith Sr/Ca values and the SST at this 44-day lag (r = −0.172, p < 0.05).

4. Discussion

4.1. Relationship Between Otolith Core Sr/Ca, Ba/Ca, Mg/Ca, and Na/Ca Values and Hatching Characteristics

It is known that the elemental content of an otolith core reflects the water environment during an individual fish’s hatching stage [29,30]. To investigate whether there were differences in the hatching locations of Pacific saury samples from the same fishing ground, we conducted a clustering analysis of the otolith Sr/Ca values. From the results shown in Figure 3a, it can be seen that the samples belonged to four different clusters. This suggests that they may have hatched in different marine environments, indicating potentially different hatching locations or times. For example, although samples 9 and 25 both hatched during autumn 2022 and were collected from the same fishing location, they belonged to different clusters, suggesting that they likely originated from different hatching sites. Previous studies have shown that differences in otolith core Mg/Ca and Na/Ca values can be used to distinguish between different populations within the same species [28]. According to the clustering results shown in Figure 3c,d, samples 29 and 32 belonged to the same cluster, indicating that they may have belonged to the same geographic population. These results, in combination with those shown in Figure 3a, show that although samples 29 and 32 were caught at different locations and hatched in different seasons, they still clustered together, leading us to speculate that they may have come from the same hatching site. Therefore, it can be inferred that while Pacific saury samples collected from the same fishing ground may have originated from different hatching sites, those from different fishing grounds could have come from the same hatching area. This indicates potential mixing among different geographical populations throughout the life history of Pacific saury.

The Ba/Ca value in the otolith core may reflect the depth of the water during hatching. Pacific saury typically spawn near the sea surface, although their eggs have also been found at depths of around 30 m [5,40]. Based on the results of the otolith Ba/Ca value clustering analysis (Figure 3b), the samples were divided into three different clusters. Among them, 25 samples (74%) belonged to the same cluster. It was speculated that most of the samples hatched within the same water layer, probably the surface layer. Additionally, sample 23 showed clear inter-cluster differences from the other samples, possibly because it hatched at a deeper water level. This finding aligns with previous research, providing insights into the variability in the water depth at which Pacific saury samples hatch.

4.2. Relationship Between Otolith Trace Element Values and Life History

According to the Chinese national standard “GB/T 8588-2024 Fundamental terms of fishery resource sciences,” [41] the life history cycle of fish is divided into five stages: the egg, larval, juvenile, young, and adult stages. Considering that the Pacific saury has a short life cycle (2 years) [42], to comprehensively explore its life history, this study divided it into six stages based on previous research: the egg (0 d), larval (1~30 d), juvenile (31~90 d), young (91~180 d), immature (181~270 d), and adult stages (>270 d) [5,37]. This division enabled the more accurate inference of the life history stage at which the Pacific saury begins independent migration.

Previous studies have used the relationship between the otolith Sr/Ca values and the temperature to determine the water environment characteristics during specific life history stages, thereby inferring migration patterns [23,24,25,26,27]. In this study, significant differences (p < 0.05) in the otolith Sr/Ca values prior to the juvenile stage and following the young stage indicated habitat changes in habitat environments around the young stage. It was speculated that these differences may have been because the Pacific saury begins independently selecting suitable habitats from the young stage onward (91~180 d), indicating the onset of migration. This finding aligns with previous suggestions that the swimming abilities of Pacific saury develop following the young stage [43], thus providing an approximate timeframe in which migration commences. Additionally, there were no significant differences in the otolith Sr/Ca values before the juvenile stage (p > 0.05), suggesting limited passive dispersal during early life stages. In contrast, significant differences existed in the otolith Sr/Ca values following the young stage (p < 0.05), indicating extensive and prolonged active migration, likely across thermally varying environments. Given that otolith Sr/Ca values are also influenced by the physiological development of Pacific saury, the conclusions drawn in this study may not fully capture all the influencing factors.

According to research by Lian Shulin et al. [25] regarding fish habitats, fluctuations in the otolith Ba content can be analyzed to reveal vertical migration behaviors during the life history of fish. According to the otolith Ba/Ca values shown in Figure 4b, there were no significant differences in the otolith Ba/Ca values across most of the life history stages of the Pacific saury. Significant differences (p < 0.05) were observed between the values observed during the juvenile and immature stages and those in the other life history stages. This difference may have been caused by the growth and development of the Pacific saury [44] or the upwelling or deep-water migration of individual samples [45]. However, due to the uneven distribution of the otolith samples, this result may have certain limitations. Future studies should focus on improving sample collection to enable a more comprehensive investigation into the vertical migration patterns of Pacific saury throughout their entire life history.

Caccavo et al. [26,28] found significant differences in the otolith Mg/Ca and Na/Ca values across life history stages. As shown in Figure 4c,d, significant differences (p < 0.05) existed in the otolith Mg/Ca and Na/Ca values between the adult and other life history stages. Considering that the Pacific saury begins spawning during the adult stage, it was speculated that these differences may be due to growth and developmental behaviors. This aligns with previous findings that the otolith core Mg/Ca values are significantly higher than those at the edge due to the influence of yolk nutrients during the embryonic development stage [27]. Given that the Pacific saury experiences various marine environments throughout its life history, the differences in its otolith Mg/Ca and Na/Ca values during certain life history stages may be attributed to ocean currents or migration behaviors. Future research should further investigate the relationship between trace elements in the otolith and the habitat environment of the Pacific saury.

4.3. Relationship Between Otolith Trace Element Values and Migration Patterns

Morales-Nin et al. [46] inferred the seasonal migration pattern of the Atlantic white croaker (Argyrosomus regius) from estuaries to coastal waters during autumn and winter based on changes in Sr/Ca values throughout its life history. To explore the horizontal spatial migration patterns of the Pacific saury samples, this study adopted a similar methodology. A significant nonlinear lagged negative correlation was found between the otolith Sr/Ca values and the SST at corresponding growth stages (p < 0.05). Inflection points in the Sr/Ca values were observed around June, July, and October (Figure 5). Combined with an optimal lag time of 44 days between the Sr/Ca values and the SST (Figure 6), these results suggest that the Pacific saury’s migration behavior shows clear seasonal variation in response to SST changes. This, combined with the inferred environmental changes experienced by Pacific saury prior to the juvenile stage and after reaching the young stage, further verifies that Pacific saury migrate in different north–south directions. Prior to the juvenile stage, Pacific saury prefer warmer and relatively stable waters, while after reaching the subadult stage, influenced by their feeding behaviors, they gradually migrate towards colder waters. This aligns with previous research findings showing that as water temperatures gradually increase, Pacific saury begin their feeding migration from the juvenile stage, crossing the complex habitat environment formed by the convergence of the Kuroshio and Oyashio currents into the Oyashio waters [47]. Thus, this confirms that the water temperature is a primary driving force for Pacific saury migration. Additionally, by considering the timing of the SST changes, the approximate point of migration onset in the life history of Pacific saury can be inferred.

Considering the differences in the otolith Ba/Ca values across different life history stages, it was speculated that some individuals may undertake vertical migrations due to their physiological development or oceanographic influences. They may remain in the same area or migrate to other regions, following the ocean currents, and thereby separate from their current migratory group. They might then continue to migrate with subsequently encountered groups arriving in the same region, following changes in the SST. This further confirms the phenomenon of mixed-size-class aggregations in Pacific saury populations [48], which also explains why the overall Sr/Ca trends in this study exhibited an S-shaped pattern in Sr/Ca variation with SST, indicating asynchronous migration across individuals. Additionally, due to factors such as feeding and spawning behaviors, individual saury may move back and forth between cold- and warm-water regions. The varying developmental stages of individuals within the same time period may also contribute to the interannual differences in the Sr/Ca value trends.

These results highlight the high adaptability of Pacific saury to changes in the water temperature, reflecting strategic migration patterns, enabling adaptation to environmental changes during their life history. Moreover, this seasonal migration pattern also demonstrates how Pacific saury enhance their utilization of food resources in different marine areas to meet their growth and development needs, thereby promoting feeding and spawning migrations.

5. Conclusions

This study analyzed the microchemical otolith characteristics of Pacific saury at different life history stages to explore their hatching origins, habitat transitions throughout their life history, and migration patterns. The main conclusions are as follows:

(1)

There were no significant differences (p > 0.05) in the otolith Sr/Ca, Ba/Ca, Mg/Ca, and Na/Ca values between male and female Pacific saury, but there were significant differences (p < 0.05) across different life history stages. These results suggest that Pacific saury in the same area may originate from multiple spawning grounds, while individuals from different fishing locations may share common spawning areas. This confirms the phenomenon of mixed populations among different geographic groups of Pacific saury.

(2)

The young stage (91~180 d) marks the beginning of independent migration for Pacific saury. Significant changes in the otolith Sr/Ca values before and after this life history stage reflect the environmental changes experienced by Pacific saury around this time. Additionally, significant changes in the Mg/Ca and Na/Ca values during the adult stage may reflect physiological behaviors such as feeding, spawning, and reproduction.

(3)

A significant nonlinear lagged negative correlation was found between the otolith Sr/Ca values and SST (p < 0.05, r < 0), speculating that the migration pattern of Pacific saury exhibits seasonal variation. The timing of migration may approximately correspond to SST inflection points. Some individuals may also undergo vertical migration across water layers during specific life stages. The maximum cross-correlation lag between the Sr/Ca values and the SST was 44 days, suggesting that SST changes precede otolith Sr/Ca variations by about 44 days. This implies that environmental changes may drive Sr/Ca fluctuations in otoliths after a deposition delay, confirming that the water temperature is a key environmental factor in studying Pacific saury migrations.

In summary, studying the otolith Sr/Ca, Ba/Ca, Mg/Ca, and Na/Ca values of Pacific saury offers critical insights into their hatching origins, life history characteristics, and migration patterns. This study provides new insights into the migration behavior of Pacific saury by modeling their relationship over time and conducting cross-correlation function (CCF) analysis. Future research should incorporate a more comprehensive range of samples and environmental data to further validate the ecological effects between trace elements in the otolith and environmental factors.