The early life stages (ELS), encompassing embryonic, larval, and juvenile phases, are pivotal periods in the life cycle of fish, marked by notably high mortality rates (Houde, 1997). Connectivity among these ELS acts as a vital link, bridging spatially segregated life history stages and profoundly influencing the population structure, dynamics, and evolution of fish species (Cowen and Sponaugle, 2009; Kool et al., 2013; Ovenden, 2013). For numerous marine species, dispersal occurs during the ELS, which is crucial for population connectivity and recruitment success (Ospina-Alvarez et al., 2015; Cabral et al., 2021). For example, the Pacific salmon undergoes a remarkable journey from freshwater spawning grounds to the ocean, navigating through various habitats during its ELS, which greatly influences its population dynamics and survival (Arbeider et al., 2024). The challenges encountered during ELS, especially among marine fish, include their limited swimming capabilities and the complexities of their vast environment (Cowen and Sponaugle, 2009), underscoring the significant roles played by abiotic factors, such as temperature, currents, and dissolved oxygen (Bailey et al., 2008; Molina-Valdivia et al., 2021); biotic factors, including prey density, predators, and competition (Saito et al., 2009; Fennie et al., 2020); and anthropogenic pressures, such as fishing activity (Cartwright, 2009); all of which directly or indirectly influence migration, growth, and recruitment patterns. Based on the critical importance of early life history (ELH) information, especially for migratory and overexploited fish species, there is a growing consensus within the fisheries management community to prioritize robust research in this area (Tulp et al., 2013; Jiang et al., 2022). Understanding ELS not only contributes to effective fisheries management, but also informs broader conservation efforts and ecosystem management strategies, ensuring the sustainability of marine ecosystems and the livelihoods of coastal communities.

There are formidable challenges associated with identifying and delineating the ELH traits of migratory fishes, particularly for the vast and intricate environment of the open ocean (Cowen and Sponaugle, 2009). The microchemistry of otoliths has proven an unrivaled tool for exploring the ELH traits of numerous fishes (Elsdon and Gillanders, 2003; Ruttenberg et al., 2008; Starrs et al., 2014). Two key assumptions underlie the use of otolith microchemistry as environmental tracers and proxies to reconstruct habitat histories. First, otolith chemistry is believed to reflect the chemical composition of the surrounding water (Elsdon and Gillanders, 2004; Izzo et al., 2015). Second, variations in otolith chemistry are influenced by ambient environmental conditions, such as salinity and temperature (Dorval et al., 2011; Morrissey et al., 2020). Among the various elements found in otoliths, strontium (Sr) has attracted particular attention due to its unique properties and potential applications for studying environmental histories of fish (Macdonald and Crook, 2010). The concentration of Sr relative to calcium (Ca) within otoliths has shown relative stability across different aquatic habitats, with significant variations observed among habitats (Elsdon and Gillanders, 2006; Yang et al., 2011; Xiong et al., 2021). This stability, along with Sr’s passive transport across membrane barriers and its incorporation into otolith mineral precipitation, renders it a promising candidate for environmental tracing in fish (Campana, 1999; Hüssy et al., 2020). Moreover, previous studies have demonstrated correlations between water Sr/Ca ratios and salinity (Yang et al., 2011), providing a basis for reconstructing salinity histories experienced by fish with various migratory patterns (Santana et al., 2018). However, it is essential to recognize that otolith microchemistry is influenced not only by environmental factors, but also by physiological factors and feeding habits (Sturrock et al., 2015; Izzo et al., 2018; Tran et al., 2019; Hüssy et al., 2020). However, the effects of these factors are often minimal, especially for diadromous migration between freshwater and marine environments, where the substantial differences in habitats offset these minor influences (Hüssy et al., 2020). In contrast, for oceanodromy exclusively within marine environments, where the salinity of the habitats is relatively stable, the relative importance of physiological factors increases (Sturrock et al., 2012). Relying solely on otolith microchemistry to reconstruct fish life histories may not be entirely reliable, particularly during periods of rapid growth and development during the ELS of fish (Brown and Severin, 2009; Sturrock et al., 2012).

Larimichthys polyactis, a typically oceanodromous species that inhabits the East China, Yellow, and Bohai Seas, holds significant ecological and commercial importance in East Asian nations (Ying et al., 2011; Choi and Kim, 2020; Song et al., 2022a). Studies that focused on the otolith microchemistry of L. polyactis predominantly centered around otolith Sr/Ca analysis, constituting approximately 73% of the relevant literature (based on searches conducted on 19 March 2024 via the Web of Science and China National Knowledge Infrastructure databases, with search criteria including (L. polyactis) and (otolith)). However, a substantial disparity exists between the findings of these studies (Xiong et al., 2017; Song et al., 2022b) and field monitoring observations for the eggs and larvae of L. polyactis (Lin et al., 2018; Xu et al., 2023) regarding ELH traits. In numerous investigations, the otolith Sr/Ca profiles of L. polyactis exhibited two notable characteristics: (i) markedly elevated Sr/Ca values in the otolith core zone, and (ii) a gradual decline in otolith Sr/Ca during ELH (Xiong et al., 2017; Song et al., 2022b; Xiong et al., 2021). Consequently, it is hypothesized that the ELH involves migration from offshore with high-salinity waters (salinity: 25–34 PSU) to nearshore areas with relatively lower salinity (salinity: 5–25 PSU) (Xiong et al., 2017). Conversely, field monitoring surveys of L. polyactis have indicated that the eggs predominantly occur in offshore waters exceeding 30 m in depth (salinity of 28–34 PSU), while larvae are mainly distributed in nearshore waters (salinity of 25–32 PSU), and juveniles tend to migrate to open ocean waters (Lin et al., 2018; Xu et al., 2023). The most significant difference between the otolith Sr/Ca profile interpretation and the field monitoring surveys lies in the salinity of the nursery habitats. Otolith microchemistry suggests that L. polyactis prefers lower salinity estuarine waters (5–25 PSU) as nursery grounds, while field surveys indicate a scarcity of L. polyactis in these estuarine, low-salinity areas (Xu et al., 2023). According to the field surveys, it is theoretically anticipated that the otolith Sr/Ca during the ELH of L. polyactis should exhibit a trend of an initial decrease followed by an increase in later stages.

In the present study, we aimed to explore the drivers of otolith Sr/Ca during the ELS, focusing on L. polyactis, a species subject to overexploitation and migratory patterns. The schematic representation of the study’s fundamental framework is depicted in Figure 1 , which consists of four parts ( Figure 1a, b ). Figure 1a illustrates the basic procedure for extracting otoliths from the brain of L. polyactis for Sr/Ca analysis, while the subsequent figures detail other key processes in the study. Previous investigations into the otolith Sr/Ca of L. polyactis have revealed two common characteristics ( Figure 1b ). Drawing from the correlations between water Sr/Ca ratios and salinity, it is inferred that their ELH involves incubation in offshore waters with high salinity (25–34 PSU), followed by feeding and nursery phases in nearshore waters with relatively lower salinity (5–25 PSU). However, this inference contradicts findings from field monitoring surveys of L. polyactis eggs and larvae (Lin et al., 2018; Xu et al., 2023). Therefore, experiments A and B were conducted to explore the potential factors that contributed to the observed common characteristics of otolith Sr/Ca. Experiment A was designed to investigate whether the Sr/Ca ratio patterns observed in wild L. polyactis could be attributed to specific environmental factors, such as temperature and salinity. This experiment did not aim to directly compare wild and cultured samples but rather to use the cultured samples to validate the Sr/Ca patterns observed in the wild. The cultured fish were reared under stable and controlled environmental conditions (i.e., constant temperature and salinity), where significant fluctuations in otolith Sr/Ca ratios would not be expected. The wild samples, in contrast, were exposed to natural environmental variations. This setup allows us to determine whether the Sr/Ca changes observed in the wild are primarily driven by these environmental factors. Thus, the purpose of Experiment A was not to compare the two groups directly but to use the cultured group to explore the potential role of environmental conditions in the observed Sr/Ca patterns in the wild ( Figure 1b ). Experiment B focused on comparing the Sr/Ca ratios in the core and edge regions of otoliths from adult L. polyactis (wild and cultured), specifically targeting individuals at gonadal development stages V (spawning period) and VI (spent period) (Lim et al., 2010). The otolith core reflects the environmental conditions experienced during the early life stage (i.e., hatching), whereas the edge corresponds to conditions experienced during the adult stage (i.e., after spawning). By comparing these two regions, we aimed to assess whether maternal influence affected the Sr/Ca deposition in the otolith. If the Sr/Ca ratios in the core and edge are similar, it would suggest a maternal effect on Sr/Ca deposition. Conversely, if significant differences exist between the two regions, it would imply that environmental or physiological factors played a more prominent role in shaping the otolith’s Sr/Ca profile (Hegg et al., 2018). This comparison allows us to explore the potential influences of maternal inheritance versus environmental conditions ( Figure 1b ).

During the ELS, the otolith Sr/Ca ratios in both cultured and wild L. polyactis exhibited a descending trend ( Figure 5 ), consistent with previous findings (Xiong et al., 2017; Song et al., 2022b). Notably, there was no significant difference between the Sr/Ca ratios at stages L and M ( Figure 6 ). If not for the comparison with cultured samples, based solely on the variations in SST and SSS of the habitat of wild samples ( Figure 4 ), it would be highly plausible to attribute the pattern of otolith Sr/Ca in the wild samples to the changes in SST. Indeed, some experimental studies have shown a negative correlation between otolith Sr/Ca and temperature, such as for Gadus macrocephalus (DiMaria et al., 2010) and Perca flavescens (Collingsworth et al., 2010). Generally, in regions with cold water, the solubility of strontium (Sr²⁺) and barium (Ba²⁺) ions tends to be higher, leading to elevated concentrations (Corrège, 2006; Saenger et al., 2008). Consequently, fish inhabiting such environments incorporate more of these ions into their otoliths during formation, resulting in higher Sr/Ca or Ba/Ca ratios (Mondal et al., 2022). Conversely, in warmer regions, the solubilities of Sr²⁺ and Ba²⁺ ions are lower, resulting in lower concentrations in water (Corrège, 2006; Saenger et al., 2008). As a result, fish forming otoliths in warmer water absorb fewer Sr²⁺ and Ba²⁺ ions, leading to lower Sr/Ca and Ba/Ca ratios (DiMaria et al., 2010; Mondal et al., 2022). In aquaculture environments with relatively stable water temperatures, the otolith Sr/Ca ratios of cultured L. polyactis also gradually declined, suggesting that water temperature may not be the primary factor influencing the deposition of Sr/Ca in L. polyactis otoliths. Previous studies have conducted meta-analyses focusing on Sr and Ba in otolith chemistry literature, that considered various species, life histories, and environmental conditions, to explore the relationship between ambient salinity and otolith Sr/Ca ratios (Campana, 1999; Izzo et al., 2018). The synthesis of data from these studies indicates a significant positive relationship between ambient salinity and otolith Sr/Ca (Arai, 2010; Hicks et al., 2010; Panfili et al., 2015). Moreover, extensive monitoring data revealed that river and lake environments exhibit a wider range of Sr/Ca levels than marine environments (Brown and Severin, 2009). The median river (2.39) and lake (1.92) Sr/Ca levels are substantially lower than those in the sea (8.61), with Sr/Ca levels ranging from 0.27 to 19.18 in rivers, 0.20 to 5.02 in lakes, and 8.17 to 8.87 in marine water (Yang et al., 2011). The otolith Sr and Sr/Ca ratios are significantly related to salinity for all species, but their predictive resolution is only sufficient to discriminate among fresh water, brackish water, and saltwater residency (Zimmerman, 2005). The salinity of both wild and cultured L. polyactis’s habitat waters remained relatively stable without significant fluctuations, indicating salinity was unlikely to have been the primary determinant of the observed decrease in otolith Sr/Ca ratios. The black line in the Figure 5 represents the Sr/Ca trend in the wild L. polyactis samples. As observed, the Sr/Ca ratios in the wild samples exhibit more pronounced fluctuations and a steeper decline during the ELS. After ruling out temperature and salinity as the primary influencing factors, it is hypothesized that this trend may relate to the physiological growth and development of the fish (Pontual et al., 2003; Peek and Clementz, 2012). During ELS, rapid protein synthesis is essential for growth, particularly in the formation of skeletal structures. This increased demand for calcium in protein synthesis may result in lower calcium availability for otolith formation. As a consequence, the calcium content in the otolith crystal structure decreases, potentially causing other elements related to calcium, such as strontium (Sr), to increase in concentration. Mohan et al. (2022) suggested that the combination of heightened protein concentrations and lower calcium levels could lead to elevated concentrations of other elements, including Sr. In this scenario, Sr may replace Ca in the otolith’s calcium carbonate matrix, contributing to the observed higher Sr/Ca ratios in the core zone of the otolith during early life stages (Courtemanche et al., 2006; Doubleday et al., 2014). This substitution mechanism could explain the significant differences in Sr/Ca ratios among ELS, particularly during the initial stages of development, when the demand for calcium in biological processes is higher. Considering the temperature and salinity environments of their respective habitats, it is plausible this phenomenon related to an additive effect of temperature, salinity, and internal physiological factors (Mazloumi et al., 2017; Tian et al., 2021).

For the adult otolith, If the Sr/Ca ratios in the core and on the edges differ significantly, it could indicate that environmental factors (such as temperature and salinity) and internal physiological factors (such as individual growth and development), rather than maternal effects, are the dominant influences on otolith composition. Notably, the otolith Sr/Ca ratios within the core zone, relating to the incubation period, for both wild and cultured specimens markedly exceeded those manifesting within their respective edge zones, relating to the spawning period, as depicted in Figure 7 . Given the myriad and efficacious applications of otolith Sr/Ca in diadromous fishes, it is widely acknowledged that otolith Sr/Ca exhibits a robust correlation with ambient water salinity (Lin et al., 2007; Walsh and Gillanders, 2018; Islam et al., 2019). Consequently, previous investigations utilizing otolith Sr/Ca consistently postulated that L. polyactis eggs are incubated in offshore waters with elevated ambient water salinity, thereafter migrating to nearshore waters with lower salinity for feeding and growth (Xiong et al., 2017; Song et al., 2022b). However, this assertion appears to falter under scrutiny when considering the relatively stable ambient water salinity experienced by the cultured L. polyactis, which exhibited a similar otolith Sr/Ca trend. Other oceanodromous fish species, such as Collichthys lucidus (Liu et al., 2015) and Miichthys miiuy (Xiong et al., 2015a), also exhibit declining otolith Sr/Ca during their ELH. Furthermore, Xiong et al. (2021) identified a striking resemblance in the otolith Sr/Ca trends of L. polyactis collected a decade apart in 2003 and 2013. Additionally, Song et al. (2022b) compared the otolith Sr/Ca trends of L. polyactis that originated from Lvsi fishing ground, Haizhou Bay fishing ground, and waters off the western coast of the Korean Peninsula, uncovering notable similarities. Consistent decreasing otolith Sr/Ca trends in L. polyactis during ELS, irrespective of spatial or temporal variations in samples, suggests that it is unlikely to be solely driven by external environmental factors, such as salinity and temperature (Tomás et al., 2006; Albuquerque et al., 2012). Therefore, the results of experiment a suggesting that temperature and salinity may not be the primary drivers of otolith Sr/Ca ratios during early development.

The descending Sr/Ca ratios observed during ELH likely originated from three principal factors. First, during ELH, individuals undergo substantial changes in their morphology, physiology, and feeding behavior (Li et al., 2013; Xiong et al., 2015b; Zhan et al., 2016; Wei et al., 2018). In the initial stages, individuals rely on internal yolk sacs for nourishment (Zhan et al., 2016). As development progresses, individuals transition to external feeding, shifting from initially consuming phytoplankton to more complex food sources, such as small zooplankton (Wei et al., 2018). Concurrently, there are significant morphological changes, with the skeletal structure, fin rays, and scales of the fish gradually developing (Li et al., 2013; Zhan et al., 2016). Yatsu et al. (1998) reported differential impacts of Sr and Ca concentrations in the otolith cores of Ommastrephes bartramii during embryonic stages compared with the subsequent ontogenetic phases. In the case of L. polyactis, the complete absorption of the yolk sac within six days post-hatching, followed by reliance on exogenous nutrition with constrained feeding capacities, was a likely contributor (Zhan et al., 2016). Second, significant protein levels are likely necessary in L. polyactis during otolith core zone calcification, as suggested by Murayama et al. (2004) and Svedäng et al. (2020). Moreover, studies propose lower Ca concentrations in the otolith core zone compared with the other zones (Dove et al., 1996). The combination of heightened protein concentrations and reduced Ca levels could lead to elevated concentrations of other Ca-related elements (Mohan et al., 2022). Elements such as Sr replacing Ca as the primary inclusion mechanism in otolith calcium carbonate matrices, may contribute to the higher Sr/Ca ratios in the core zone (Courtemanche et al., 2006; Doubleday et al., 2014). The third factor is centered around the appearance of L. polyactis’ first feeding ring on the fourth increment, approximately 20.67 ± 2.28 μm away from the core zone, indicating prior reliance on yolk sac nutrients for sustenance (Zhan et al., 2016; Song et al., 2022b). Sagittal otoliths in teleost fish form during the embryonic period (Marannu et al., 2017); hence, maternal contributions to progeny otoliths are inevitable (Hegg et al., 2018; Janak et al., 2021). This is supported by evidence of maternal influences in various fishes, such as Morone Saxatilis (Elking, 2014), Mallotus villosus (Loeppky et al., 2018), and Oncorhynchus nerka (Janak et al., 2021). It is suggested that embryonic otolith chemistry may not reflect environmental conditions, such as water chemistry and temperature during egg incubation; rather, it may reflect maternally derived trace elements in the yolk (Volk et al., 2000; Zimmerman and Reeves, 2002) or be influenced by genetically controlled uptake dynamics (Chittaro et al., 2006). Although the results of experiment b suggest that maternal influences may not be the primary cause of elevated Sr/Ca ratios in the otolith core, they remain an essential factor in studying the early life history of fish. Collectively, otolith Sr/Ca ratios during ELS in L. polyactis are more affected by the ontogenetic developmental stage than by environmental factors such as temperature, salinity, or maternal effects.

Given the limitations of current experimental conditions, the Sr/Ca ratios analysis of otoliths has been confined to their growth stages for L. polyactis. Our research will benefit from combining daily environmental data with daily incremental analysis, which may lead to more accurate results. Furthermore, this underscores the necessity for a more detailed interpretation of Sr/Ca ratios. When investigating the life history of oceanodromous fish using Sr/Ca ratios or other elemental analyses, controlled culture experiments should be conducted to mitigate the influence of physiological factors and other variables.

This study explored the dynamics of otolith Sr/Ca ratios in Larimichthys polyactis during early life stages (ELS), examining both wild and cultured populations. Through Experiment A, we identified a consistent decline in Sr/Ca ratios across developmental stages (E, L, M, and J), suggesting that factors beyond simple environmental conditions, such as temperature and salinity, influence otolith chemistry. Experiment B further demonstrated significant differences in Sr/Ca ratios between the otolith core and edge zones, indicating the potential role of early developmental processes in shaping otolith composition. These findings challenge the prevailing notion that Sr/Ca ratios are solely driven by external environmental factors. Instead, our results suggest that internal biological processes, e.g. ontogenetic changes, play a more critical role in determining Sr/Ca deposition patterns. The similar trends observed in both wild and cultured fish reinforce this conclusion, as environmental stability in aquaculture did not prevent the progressive decline in Sr/Ca ratios. While this study provides valuable insights, it also raises new questions. Future research should investigate the precise biological mechanisms behind these Sr/Ca dynamics, including the potential interaction of other environmental factors such as food availability and water chemistry. Additionally, employing advanced statistical models like generalized linear models (GLM) may offer further clarity on the interplay between various influences. The study also offers valuable insights into novel culture experiments that investigate early life history through the analysis of chemical elements at the edge of otoliths, utilizing continuous sampling in conjunction with daily increments. Overall, this study enhances our understanding of otolith chemistry in larval fish and underscores the importance of considering multiple factors when interpreting Sr/Ca data, particularly in tracking early life histories.