Conspicuous changes in geochemical chronologies were present for PBT during the first year of life, and changepoint analysis served as a novel approach to identifying divergences along otolith-based life history profiles. Abrupt shifts in otolith element:Ca ratios are often associated with movements between water masses with different physicochemical properties31–32. Given that physicochemical conditions such as salinity and temperature as well as metal loads in coastal waters (marginal seas) are often distinct relative to offshore waters of the WNPO and associated Kuroshio Current33–34, divergences observed along element:Ca profiles likely predict the timing of egress or ontogenetic changes linked to the movement by young PBT from inshore nurseries to offshore waters.
Observed patterns of decreasing otolith Mg:Ca and Mn:Ca ratios present for PBT during the first year of life are in accord with expected timing of migrations from coastal nurseries to offshore waters of the Pacific Ocean17. Ambient concentrations of Mg and Mn in coastal waters or areas influenced by riverine inputs are often higher relative to offshore waters because metals derived from anthropogenic and lithophilic sources decrease precipitously as the distance from the coastline increases35–36. In the WNPO, surface waters are impacted by the western boundary current (Kuroshio Current) and mesoscale features that are reduced in metals37, further supporting this aforementioned inshore-offshore depletion gradient of both markers. Conspicuous declines in both otolith Mg:Ca and Mn:Ca ratios during the age-0 period of PBT are in agreement with the presumed inshore-offshore transition. Still, it is important to note that otolith geochemistry cannot always be consistently linked to ambient Mg:Ca and Mn:Ca in seawater38–39. Apart from ambient seawater chemistry, salinity and temperature may play a role in observed shifts in otolith Mg:Ca and Mn:Ca, but salient shifts in these markers appear to be driven primarily by changes in somatic growth rather than salinity and/or temperature40–41. While the contribution of each driver to observed patterns in otolith Mg:Ca and Mn:Ca is unresolved and may be partially linked to other factors associated with the inshore-offshore transition (e.g., metabolism, diet, growth), observed divergences in geochemical profiles and the timing of such changes align well with the expected migrations of young PBT from coastal nurseries to foraging areas in offshore waters.
In contrast to otolith Mg:Ca and Mn:Ca, a pronounced increase in otolith Sr:Ca occurred during the age-0 period. Positive relationships between otolith Sr:Ca and salinity have been reported for a wide range of species, with otolith Sr:Ca commonly occurring at proportions relative to ambient levels 41–42. This element:Ca ratio has proven useful for documenting shifts—both ingress and egress—between waters masses with distinct salinity values 40,43. Although Sr and Ca in seawater are conserved at higher salinity, resulting in less Sr: Ca variation in water across marine salinity gradients44–45, this marker has been used to effectively delineate inshore-offshore transitions for several species46–48. Observed Sr:Ca profiles for PBT during the first year of life displayed marked increases in otolith Sr:Ca later during the age-0 period. This finding is in agreement with anticipated egress of young PBT from inshore to offshore waters of the WNPO, which are characterized by higher salinity relative to coastal waters in the East China Sea or Sea of Japan. Physiological influences on otolith composition are particularly evident for certain element:Ca ratios (Sr:Ca) 45,48−49, and physiological changes associated with inshore-offshore ontogenetic transitions of young PBT may have contributed to observed shifts in otolith Sr:Ca. Moreover, physiological controls may be moderated by changes in ambient water temperature also occurring during the transition, which can also have a positive influence on otolith Sr:Ca50–51 and movement into the warmer, oligotrophic waters in the Kuroshio Current52 or farther offshore into the WNPO may also be responsible for pronounced increases in otolith Sr:Ca often observed occurring after the first 6–8 months of life.
The timing (age) of geochemical changepoints used to predict departures of age-0 PBT from coastal nurseries often varied among markers (Mg:Ca, Mn:Ca, and Sr:Ca) for individual PBT. Disparities in mean ages associated with shifts in element:Ca profiles were evident with geochemical changepoints presumably linked to egress detected about three months earlier with otolith Mg:Ca relative to Sr:Ca, with Mn:Ca being intermediate to the these two markers. Despite the disparity of presumed egress ages, the earliest estimated departure times were generally greater than 90 dph for all three markers, suggesting that most recruits remain in coastal nurseries for at least the first three to four months of life. Given that otolith Mg:Ca, Mn:Ca, and Sr:Ca ratios may reflect and/or respond (i.e., lag effect) to changing environmental or physiological conditions differently38,45, combining multiple markers often leads to more robust estimates of age-specific egress or ingress22. Changepoints derived from all three of these markers integrate sensitivities of each and were used to produce a more robust indicator of presumed egress or geochemical shifts by PBT. Using this approach, the majority of geochemical changepoints were detected at 150–200 dph, suggesting that age-0 PBT in our sample inhabited coastal waters throughout the summer and into the fall, taking advantage of elevated primary productivity found here relative to more depleted conditions in offshore waters of the Kuroshio Current53. Our findings are in accord with an archival tagging study that also observed young PBT inhabiting coastal waters inshore of the Kuroshio Current during the summer and fall17. Changepoints in element:Ca profiles for nearly a quarter of the PBT in our sample did not occur until after 200 dph, suggesting these individuals may overwinter in coastal nurseries before moving offshore in the early spring. Overwintering behavior by age-0 PBT from both the East China Sea and Sea of Japan is known to occur in the East China Sea54–55 supporting our finding of a delayed geochemical shift or late egress for some individuals.
Observed variability in the age-at-egress among individual PBT in our sample using average estimates from Mg:Ca, Mn:Ca, and Sr:Ca (93 to 281 dph) is not entirely unexpected given that the birth year (age-0 period) of individuals in our samples spanned many years (Table S1; using age-length relationship derived from previous study56). Interannual variation in coastal and oceanographic conditions are common in the WNPO and strongly influenced by the dynamics of the Kuroshio Current52. The path and coastal intrusion of the Kuroshio Current varies seasonally and annually in the Ryukyu Archipelago and off the east coast of Japan34. Inshore-offshore fluctuations in the Kuroshio Current and associated mesoscale features (e.g., large meander) commonly occur and are known to influence the spatial distribution of prey57–58. Moreover, the position of the Kuroshio Current relative the coastline also influences the habitat use and movement of age-0 PBT between inshore and offshore waters17,55,59. More specifically, advection of waters away from the coast due to the current and associated eddies, often in the winter and spring, results in a wider distribution of age-0 PBT and may facilitate fish moving to offshore waters in the Kuroshio-Oyashi Transition Zone (KOTZ)17. Interannual variation in the pathway and westward penetration of the Kuroshio Current and it subsequent influence on habitat use (inshore vs. offshore water) by young PBT combined with the fact that birth years of adult PBT in our sample spanned more than five years contributed to observed variation in the timing of predicted egress using geochemical changepoints.
Otolith Ba:Ca profiles of PBT were relatively consistent during the first year of life, and changepoints for individuals in our sample were often not detected until that age-1 period. This geochemical marker was presumably uninformative for detecting inshore-offshore transitions by age-0 PBT; nevertheless, conspicuous shifts were detected in the late age-0 to early age-1 period for PBT in our sample, and these geochemical divergences may be related to a different life history transition. Because Ba:Ca in seawater is enriched at depth, upwelling elevates Ba:Ca ratios in surface waters59, which in turn is often reflected in elevated otolith Ba:Ca22,31. As a result, this marker shows promise for signifying entry into upwelling zones by PBT22 and other taxa (e.g., sharks60). Highly productive waters of both the KOTZ in the WNPO and the California Current Large Marine Ecosystem (CCLME) in the eastern North Pacific Ocean represent two areas with strong upwelling and subsequently elevated seawater Ba:Ca61. Elevated primary and secondary productivity occurs along frontal boundaries of both features, which represent critical foraging habitat of young PBT 16,18. As a result, entry into associated upwelling zones of the KOTZ or CCLME by PBT is expected to result in conspicuous increases in otolith Ba:Ca. The majority (70%) of changepoints detected in otolith Ba:Ca profiles of individual PBT were between 10 to 18 months (mean: 344 dph). Interestingly, archival tagging showed that the timing of departures by juveniles from the WNPO in the vicinity of the KOTZ begins at around 12 months with average transit times about 2.5 months15. Therefore, elevated otolith Ba:Ca first observed during the late age-0 or early age-1 period may be linked to their occurrence in highly productive waters of the KOTZ or associated upwelling areas along the margin of the Kuroshio Current62 while elevated values and resulting changepoints detected later in the age-1 period (~ 14–18 months) may signify movement into the highly productive waters of the CCLME22.
Element:Ca signatures in the otoliths of age-0 PBT in our 2011–2012 sample from East China Sea and Sea of Japan were significantly different. Influential element:Ca ratios in otoliths for discriminating young PBT from both regions (Mg:Ca, Mn:Ca, Li:Ca) were consistent with earlier studies21,29, suggesting that long-term differences in physicochemical conditions likely persist between both spawning areas. While age-classed matching with our baseline was limited, predictions of natal origin observed here shed important light on the origin of adult PBT collected in the East China Sea. Our finding of adults from Taiwan fisheries caught off the Ryukyu Islands being predominantly sourced to the East China Sea spawning area (~ 2/3) is suggestive of site fidelity to this region. However, the presence of adult PBT with core signatures matching the Sea of Japan were also observed in our sample, implying that waters in the Ryukyu Archipelago also represent a potential mixing zone for individuals produced from both spawning areas63. Daily geolocation estimates from electronic tags have shown individual tracks of PBT moving between the East China Sea and Sea of Japan64, suggesting that the Ryukyu Archipelago may be an important foraging area that results in a mixing zone for migrants from both spawning areas.
Changepoint analysis of geochemical profiles represents a promising methodology for elucidating habitat shifts or movements of juvenile PBT, including coastal-offshore transitions that occur during the first year of life. An improved understanding of the spatial distribution, dispersal, and inshore-offshore exchange rates of age-0 PBT in the WNPO is important for stock assessments, particularly in light of the fact that increased catches of juveniles in recent years have led to concerns about the sustainability of the population65. Our investigation sheds important light on age-specific migrations of juvenile PBT between coastal and offshore waters, and this work suggests that changepoint analysis of element:Ca chronologies may prove useful for detecting habitat transitions by older, larger PBT as well as other species. A distinct advantage of this approach over other widely used techniques to investigate animal movements (e.g., acoustic and satellite telemetry) is that it allows for retrospective determination of natal origin as well as age-specific estimate of movement by coupling highly resolved (interval ~ daily) otolith microstructure and geochemical data. Moving forward, synthesis of data from multiple techniques, including otolith geochemical chronologies, will be required to fully understand the complex nature of migrations by PBT.