Neon flying squid (Ommastrephes bartramii) is a pelagic squid species extensively distributed in subtropical and temperate oceans. The North Pacific population of O. bartramii comprises two seasonal spawning cohorts (the winter-spring cohort and the autumn cohort) (Bower and Ichii, 2005). Both cohorts undergo meridional migrations between their spawning ground (subtropical frontal zone: 20–30°N) and feeding ground (Kuroshio–Oyashio transition and subarctic frontal zone: 30–50°N) within their 1-year lifespan (Murata, 1993). The importance of this species is underlined by its ecological significance as a structuring role to link different trophic levels (Watanabe et al., 2004), as well as its high commercial value to support international distant-water fisheries (Chen et al., 2008a). It is largely exploited by China (including Chinese Taipei), Japan, and Korea in the Northwest Pacific Ocean. Chinese squid-jigging fishing vessels mainly harvest the western stock of the winter-spring cohort of O. bartramii from July through November in the area bounded by 36°-48°N and 150°-165°E.

The subtropical and subpolar Northwest Pacific Ocean is dominated by two western boundary currents, the Kuroshio Current characterized as a warm and nutrient-poor current and the Oyashio Current characterized as a cold and nutrient-rich current. The Kuroshio-Oyashio transition zone with high biological productivity is an important feeding ground for many commercially important marine species including O. bartramii (Watanabe et al., 2008; Ohshimo et al., 2018; Ishak et al., 2020). Previous studies have suggested that the variability of the Kuroshio path can affect the abundance and distribution of O. bartramii (Shao et al., 2005; Chen et al., 2010a; Chen et al., 2012). The warm, northward-flowing waters of the Kuroshio Current separate from the Japanese coast to flow eastward into the North Pacific Ocean as a free jet-the Kuroshio Extension (KE) Current (Jayne et al., 2009). Based on the satellite altimeter measurement over the past decades, the interannual shifts of the KE path between a stable and an unstable dynamic state has been revealed (Qiu and Chen, 2005; Qiu and Chen, 2010). The impacts of this interannual variability of KE on eddy changes and marine primary production in the North Pacific Ocean have been emphasized by many studies (Lin et al., 2014; Yang et al., 2018). In addition, the impacts of the KE Current-related eddy changes on swordfish, a marine top predator, in the Northwest Pacific Ocean were pointed out by a recent study (Gómez et al., 2020).

Mesoscale eddies are ubiquitous in global oceans, ranging in size from tens to hundreds of kilometers with high energy (Chelton et al., 2011a). Eddies can be categorized as being either cyclonic eddies (cold-core; CE) or anticyclonic eddies (warm-core; AE), which rotate counterclockwise and clockwise in the northern hemisphere, respectively. Eddies modulate regional primary production through a variety of mechanisms, including vertical or horizontal advection of nutrients/phytoplankton, and regulation of light availability by changing ocean stratification (Gaube et al., 2014; McGillicuddy, 2016). Many studies have suggested that mesoscale eddies can attract a variety of marine organisms by providing foraging opportunities (Godø et al., 2012; Schmid et al., 2020) and favorable physical conditions (Gaube et al., 2018; Braun et al., 2019). CEs and AEs are known to have different effects on local marine ecosystems due to the opposite rotating direction and the accompanying opposite vertical movement pattern of water mass (Chelton et al., 2011b; Gaube et al., 2014). Typically, for most surface-intensified eddies, CE causes a vertical upward flow of seawater (upwelling) at its core and outward advection (divergence) at the surface. In contrast, AE causes downwelling at its core and convergent flow at the surface. Thus, CEs are generally considered to be productive due to the upwelling inside them, while AEs are considered to be unproductive ocean “deserts” (Gaube et al., 2014). The differences in the influence of CEs and AEs on biological communities, from plankton to predators, have been explored in numerous studies and have obtained diverse results (Gaube et al., 2014; Hsu et al., 2015; Gaube et al., 2018; Waite et al., 2019).

The KE Current is one of the most dynamic regions in the world’s oceans and contains highly energetic eddies that provide potential habitats for pelagic species (Polovina et al., 2006; Zainuddin et al., 2006). As for O. bartramii, it is believed that the existence of eddies is conducive to the formation of good fishing grounds (Chen, 1995). Sea surface height (SSH) and eddy kinetic energy (EKE), as two variables used to indicate ocean mesoscale dynamics, were widely applied to the evaluation of habitat patterns for O. bartramii (Chen et al., 2011; Yu et al., 2015; Yu et al., 2016). However, the variability and potentially different ecological roles of CEs and AEs cannot be comprehensively revealed by the two variables. A recent study using eddy identification methods suggested that the monthly squid habitat hotspots are likely associated with transient oceanic eddies, especially warm-core eddies (Alabia et al., 2015). The close association between the squid habitat and the eddies has not been confirmed, and the study region was limited to the central North Pacific.

Current knowledge of how the transient eddies affect O. bartramii stock in the Northwest Pacific Ocean is quite scattered. A comprehensive insight into the different roles of CEs and AEs in affecting the abundance and distribution of O. bartramii is still lacking. Based on a weighted-based habitat suitability index (HSI) model and data from 10-year long-term squid fisheries, eddies tracking, and high-resolution ocean reanalysis, this study evaluated the impacts of mesoscale eddies-induced changes in environmental conditions on the abundance and distribution of O. bartramii in the Northwest Pacific Ocean. The distinction between the impacts of cyclonic and anticyclonic eddies on an environment-sensitive squid species was emphasized.

In this study, the impacts of mesoscale eddies on the abundance and distribution of O. bartramii were evaluated in the Northwest Pacific Ocean. Cold-core CEs and warm-core AEs were found to have different impacts on O. bartramii population. A significantly higher abundance of O. bartramii was found in AEs than in CEs during KE unstable years, with a much higher catch and 70% higher CPUE ( Figure 3 ). Based on a weighted AMM based HSI model with crucial ecological factors considered, the eddy-induced O. bartramii habitat distribution patterns were shown ( Figure 6 ). The pattern of habitat explained the variation of O. bartramii distribution in and around the eddies.

Eddies have long been recognized as important oceanic features forming good fishing grounds of O. bartramii. In previous studies, the main mechanisms by which the eddy activities influence the O. bartramii distribution were generally considered to be related to the foraging conditions. The enhanced primary production stimulated by nutrient supply from upwelling occurring at the center of CEs and the edge of AEs (Chen et al., 2010b; Yu et al., 2016), and the aggregation of prey induced by the convergent flow at the center of AEs (Alabia et al., 2015), were believed to be the main reasons that the eddy activities attracted O. bartramii. However, little attention has been paid to the effects of eddies on the thermal adaptation of O. bartramii, especially based on the general understanding that warm-core AEs are oligotrophic (Gaube et al., 2014). And although seawater temperature, either at the surface or subsurface, has been recognized as a crucial factor affecting the distribution of O. bartramii, the link between this factor and the mesoscale eddies has been neglected. In this study, specific distribution patterns of biophysical factors indicating the thermal and nutrient conditions and their corresponding SIs in and around the eddies were shown ( Figures 4 and 5 ). The effects of the factors were found of varying importance, with T_50m being considered the most important. It is suggested that the elevated T_50m in AEs producing an expanded suitable SI range was the main cause of the high O. bartramii abundance in the warm-core AEs. As for CEs, though the observed high Chl-a indicates high productivity conditions, the unfavorable thermal conditions prevented them from being very suitable habitats for O. bartramii.

O. bartramii is a pelagic warm water species. SST has long been considered as a crucial or dominant factor affecting the distribution of O. bartramii (Tian et al., 2009; Yu et al., 2019), in addition, increasing attention has also been paid to the role of the subsurface temperature (Alabia et al., 2016; Wang et al., 2022). In this study, T_50m was selected to characterize subsurface temperature. O. bartramii performs a typical diel vertical migration pattern (Murata and Nakamura, 1998), and they are fished by consistent specific squid jigging operation at about 50-m depth when floating to forage at nighttime. Previous studies have highlighted the role of the temperature vertical structure from the surface to 50-m depth in forming fishing grounds for O. bartramii (Chen et al., 2014). A recent study investigated the effects of subsurface temperature on O. bartramii in the Northwest Pacific Ocean and found that O. bartramii prefer relatively warm water at 30-m depth ranging from 11 – 18°C(Wang et al., 2022). The preference of O. bartramii to subsurface warm water at such depth is probably because it can meet the thermal needs of this ectothermic species during predation.

The HSI model has been widely used in fisheries, ecological impact assessments, and ecological restoration studies. It has been successfully applied to the evaluation and prediction of habitat changes of O. bartramii (Igarashi et al., 2018; Yu et al., 2020). A reliable proxy of species abundance and distribution is crucial to the model. Previous studies concluded that using a CPUE-based HSI model might overestimate the favorable habitat ranges and underestimate the variations in habitat spatial distribution (Tian et al., 2009). In this study, both abundance and presence indicators were taken into consideration in the model development by combining catch and fishing efforts into the aggregation of the HSI model. Three biophysical factors proven to have significant impacts on the O. bartramii habitat, SST, T_50m, and Chl-a, were considered in the model. In addition to the temperature variables mentioned above, Chl-a is another factor often used in the habitat assessment of O. bartramii, which indicated the primary production and food availability (Yu et al., 2019). As O. bartramii does not feed on phytoplankton directly, the effect of Chl-a on O. bartramii population should be indirect, yet a significant association between Chl-a and squid distribution existed ( Table S2 ). By comparing the performance of the weighted AMM-based HSI model under different empirical weighting scenarios ( Table S1 ), the varying importance of factors was shown, and the optimal weight combination was considered to be 0.25, 0.5, and 0.25 for SST, T_50m, and Chl-a, respectively ( Table S3 ). Finally, the model showed excellent prediction performance ( Figure S4 ).

Since the HSI model was built using all the fisheries data in this study, it is based on the assumption that the response of O. bartramii to the biophysical factors was spatially consistent. This means that for each environmental factor included in the model, we assumed that its effect was the same whether it was inside or outside the eddies. The distribution of these variables in the ocean is not completely independent of each other while is appeared to show specific combinations in different regions, and these variables affected the distribution of O. bartramii together. As for two types of eddies, it is generally a combination of low T_50m and high Chl-a in CEs while a combination of high T_50m and low Chl-a in AEs ( Figure 4 ). Although sometimes the effects of mixing in AEs may cause an increase in Chl-a, a low Chl characteristic was still evident from the long-term average. The especially high O. bartramii abundance found in AEs indicated its preference for high T_50m and a relatively suitable Chl-a range or some other properties associated with such conditions. Using an abundance proxy based on the frequency of fishing effort and catch as well as integrating each individual SI in model construction, the preference of O. bartramii for such a combination was evaluated.

An interannual variation of O. bartramii abundance inside warm-core AEs possibly related to the KE dynamic states was found. During the stable KE state, the abundance of O. bartramii was also higher in AEs than CEs. The total catch in AEs was several times that of CEs, while the difference in CPUE was smaller compared to the unstable KE state ( Figure S6 ). Revealing the mechanisms of this interannual variation was beyond the scope of this paper, but some speculations have been proposed. Previous studies have observed increasing regional chlorophyll concentration in the Northwest Pacific during the unstable KE years (Lin et al., 2014). The distribution of fishing effort in AEs and the spatial patterns of Chl-a in AEs in the region with dense effort distribution were shown during the two KE dynamic states ( Figure 7 ). Higher Chl-a in AEs were observed during the unstable KE years, which might be attributed to changes in the chlorophyll background field due to specific ocean circulation associated with an unstable KE. The combination of the suitable subsurface warm water and the favorable nutrient conditions in the unstable KE background could be the main drivers for yielding particularly high O. bartramii abundance in the warm eddies.

In summary, warm-core AEs were found to yield high O. bartramii abundance mainly because of the favorable subsurface thermal condition. The impacts of the eddies on the O. bartramii population, especially of AEs, might change with the interannual KE variability, although its mechanism has not been clearly revealed yet. Other interannual or decadal climate changes, such as the El Niño Southern Oscillation, which significantly affected the biophysical environments in the Northwest Pacific Ocean, may also play a role in influencing the eddy variations, and as a result, affecting squid species, necessitating further research.

The original contributions presented in the study are included in the article/ Supplementary Material . Further inquiries can be directed to the corresponding author.

WY, YZ, and XC conceptualized the study. WY, YZ and MZ designed the methodology and provided the software analyzed the data for the study. YZ and WY wrote the original draft. WY, XC and CZ involved in the funding acquisition. All authors contributed to the article and approved the submitted version. All authors have given approval to the final version of the manuscript.

This study was financially supported by the National Natural Science Foundation of China (41906073, 42106090), the project of Shanghai talent development funding (2021078), the National Key R&D Program of China (2019YFD0901405), the Natural Science Foundation of Shanghai (19ZR1423000), and the open fund of State Key Laboratory of Satellite Ocean Environment Dynamics, Second Institute of Oceanography (QNHX2232).

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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