Understanding the reproductive biology of fish species is prioritized to provide basic knowledge to establish resource conservation plans and regulatory strategies for fishery production and for broodstock management, such as determining the spawning period and planning detailed breeding schemes in aquaculture (Grandcourt et al., 2009; Kujawa et al., 2019; Kucharczyk et al., 2023). The success of commercial-scale fish aquaculture predominantly depends on sufficient production of high-quality larvae from broodstock (Kujawa et al., 2019). Therefore, numerous studies have been conducted to identify the reproductive cycles of various fish species, including flatfish (Paralichthys dentatus, Pleuronectes americanus, and Tanakius kitaharai) (Morse, 1981; Harmin et al., 1995; Narimatsu et al., 2007), greater amberjack (Seriola dumerilii) (Micale et al., 1999), groupers (Epinephelus coioides, Epinephelus ongus, and Epinephelus marginatus) (Chai et al., 2013; Ohta and Ebisawa, 2015; Rodrigues-Filho et al., 2023), sea breams (Dentex tumifrons) (Tominaga et al., 2005), and tunas (Thunnus thynnus and Thunnus orientalis) (Medina, 2020; Park et al., 2023), during their early developmental stages of aquaculture. The reproductive cycle and gonadal development of fish are altered by the neuroendocrine reproductive axis, which is influenced by various internal (age and size) and external (temperature, photoperiod, and other physico-chemical parameters of water) factors (Taranger et al., 2010; Servili et al., 2020; Kumar et al., 2023). Hence, the ongoing and rapid alterations of marine environments caused by global warming and climate change further emphasize the importance of obtaining reliable data on the reproductive characteristics of fish under changing conditions (Servili et al., 2020). Understanding the effect of environmental shifts, particularly temperature variations, on the reproductive cycle and spawning timing is crucial for aquaculture systems. Therefore, clarifying the reproductive cycle of target fish species while accounting for the latest environmental conditions of a location is essential for managing successful spawning strategies.

Chub mackerel (Scomber japonicus), a migratory fish species widely distributed in the subtropical and temperate waters of the Pacific Ocean, is an economically important fishery resource in China, Japan, and the Republic of Korea (hereafter Korea). It is divided into two stocks, the Tsushima warm current (TWC) stock mainly fished by China and Korea (Wang et al., 2022) and the Pacific stock. Since 1996, during which the highest annual fishery production of chub mackerel in Korea reached approximately 400,000 metric tons, the production has fluctuated, reaching approximately 120,000 metric tons in 2023 (KOSIS, 2024). Liang et al. (2020) and Hong et al. (2022) assessed the status of chub mackerel resources caught in the Northwest Pacific Ocean and reported a pessimistic decline in recent years. To preserve chub mackerel resources, a Total Allowable Catch was established and implemented in Japan and Korea from 1997 and 1999, respectively. To meet the significant consumer demand, approximately 51,000 metric tons of Atlantic mackerel (Scomber scombrus), comprising 42% of the domestic fishery production of chub mackerel, have been imported from Norway to Korea in 2023 (KMI, 2024).

Chub mackerel aquaculture can be a suitable solution to ensure a stable supply for consumer demand while also contributing to fishery resource conservation. Over the last few decades, extensive research on this species in Japan has been conducted in various fields including ecology (Yukami et al., 2009; Wang et al., 2022), endocrinology (Matsuyama et al., 2005; Nyuji et al., 2012a; Selvaraj et al., 2015), ethology (Tsuda et al., 2013), and biology (Kobayashi et al., 2011; Shiraishi et al., 2005, 2008). Particularly, Shiraishi et al. (2008) monitored the seasonal changes in the gonadosomatic index (GSI) and ovarian stages of TWC stock in the waters off northern Kyushu and northern East China Sea and concluded that the TWC stock spawning season in this region extended from March to mid-May. Yukami et al. (2009) reported that the GSI of chub mackerel at 50% sexual maturity was 2.5% and identified sea surface temperatures of 15–22°C as suitable spawning conditions. These studies have provided significant insights into reproductive biology and sexual maturation; however, basic knowledge regarding the reproductive biology of chub mackerel under aquaculture conditions remains incomplete.

Previous studies have demonstrated significant variations in the reproductive season of chub mackerel depending on ocean geographical locations. For instance, the reproductive season of chub mackerel in the southern East China Sea typically begins approximately two months earlier than that in the northern East China Sea and four months earlier than that in the East Sea (Sea of Japan) (Yukami et al., 2009). Kim et al. (2020) reported that the reproductive season of wild chub mackerel in Korean coastal waters extended from March to June and peaked in May, based on the GSI and ovarian stages of fish. However, the findings of Kim et al. (2020) were obtained without considering environmental factors, and the reproductive characteristics between wild fish and captive fish could differ (Zupa et al., 2017). In Korea, chub mackerel has primarily been farmed along the southeastern coast and off the waters of Jeju Island since 2010; however, most farming still relied on feeding wild-caught juveniles. The waters surrounding Jeju Island are a major spawning ground for the TWC stock (Kim et al., 2020). Jeju Island boasts well-developed land-based aquaculture facilities and a sufficient supply of underground seawater, offering great potential for regulating environmental conditions throughout the year (Kim, 2022). These advantages provide desirable aquaculture conditions for stable growth and reproduction in this species. Identifying the reproductive characteristics of chub mackerel broodstock in land-based aquaculture systems in Jeju Island may provide foundational information for juvenile production and further spawning regulation.

Therefore, we hypothesized that differences could exist in the reproductive cycle of farmed fish in an aquaculture facility compared to wild chub mackerel, as observed in previous studies. The objective of this study was to identify the reproductive cycle of chub mackerel in an indoor land-based tank on Jeju Island. To the best of our knowledge, this is the first study to examine monthly changes in biological indices, histological gonadal development observations, plasma sex steroid hormone levels, and reproduction-related gene expression in captive male and female chub mackerel throughout the year. The results derived from this study provide crucial insights into the reproductive physiology of chub mackerel, focusing on gonadal development, hormone dynamics, and biological indices. This knowledge is essential for understanding the transition of chub mackerel from wild-caught to cultured species and will serve as a foundation for optimizing breeding schemes and achieving large-scale seed production in land-based tanks.

This study determined the reproductive characteristics of chub mackerel cultured in an indoor land-based tank on Jeju Island based on its biological, histological, endocrinological, and genetic evidence. In this study, one-year-old fish were used, indicating it is first spawning for them. Even if Yoneda et al. (2022) emphasized that 2- or 3-year-old chub mackerel (repeat spawners) could produce a greater number of more nutrient-rich eggs compared to one-year-old fish (first-time spawners), several studies have reported no significant differences in the timing of gonadal development between first-time spawners and repeat spawners (Nyuji et al., 2012a, 2012, 2014). Therefore, comparing the gonadal development of fish in this study and with that of wild fish in past studies seemed to be feasible. In addition, although it is difficult to determine the maturity rates of fish and their participation in spawning from the data obtained in this study, considering that the 50% total length and GSI for mature female chub mackerel were calculated to be 31.4 cm and 2.5%, respectively (Yukami et al., 2009; Kim et al., 2020), and that the total length and GSI of females in May and June ranged from 29.0–30.9 cm and exceeded 4%, respectively, it can be inferred that most individuals likely participated in maturation and spawning. On the basis of the presence of post-ovulatory follicles observed in the histological analysis, spawning event occurrence, and GSI variation, we ascertained that the species spawning period extended from end-May to mid-July and occurred primarily in June. The findings partially align with those of Murata et al. (2005), who reported that captive chub mackerel reared in land-based tanks in Shirahama spawned between May and June at water temperatures of 20.8–24.2°C. However, in contrast to these results, previous studies have documented spawning-capable chub mackerel from March to June in northern Kyushu, the northeastern East China Sea (Shiraishi et al., 2008; Yukami et al., 2009), and the coastal waters of Korea (Kim et al., 2020). These comparisons suggest that chub mackerel reared in indoor land-based tanks on Jeju Island exhibit a spawning period that begins approximately 2 months later than that of their wild counterparts in regions of comparable latitude. This delay highlights the potential influence of controlled rearing conditions on the timing of spawning events. Specifically, potential factors such as stress from confinement, differences in diet, altered photoperiod and temperature regimes, and limited environmental stimuli compared to wild habitats are likely contributors to delayed spawning. In particular, chronic stress has been extensively documented to cause reproductive delays in fish (Campbell et al., 1994; Pankhurst, 2016). Additionally, aquaculture conditions, wherein complex environmental cues are lacking, might affect hormone regulation involved in reproductive readiness, thereby influencing the timing of spawning events (Okuzawa and Gen, 2013; Zupa et al., 2017).

The relatively higher HSI levels (1.62–1.73%) observed in females from January to June compared with those in other months (0.81–1.35%) may be indicative of physiological processes associated with reproduction, though the exact mechanisms remain unclear, as vitellogenin analysis was not carried out in this study. However, the relatively low plasma E2 levels observed in females from January to May do not strongly support the occurrence of active vitellogenesis during this period. Notably, previous studies have shown that both HSI and GSI in fish tend to increase prior to the spawning period and decrease after spawning (Lim et al., 2010; Hismayasari et al., 2015). In this study, the highest plasma levels of E2 and T in June were consistent with histological observations of fully vitellogenic oocytes and post-ovulatory follicles. These findings suggest that vitellogenesis predominantly occurred in June, coinciding with the observed peak in HSI and GSI. This delay in vitellogenesis likely influenced the spawning period, as supported by GSI trends and histological observations (Shiraishi et al., 2008; Mañanós et al., 2009; Kim et al., 2020).

Rearing fish in captivity often causes reproductive dysfunction, particularly in females, characterized by lower GSI levels due to incomplete vitellogenesis. Though reproductive dysfunctions in males are less severe, they often fail to produce a sufficient amount of high-quality sperm despite completing spermatogenesis and spermiation. Lower GSI levels have often been observed in migratory fish, such as the Pacific bluefin tuna (Thunnus orientalis), Atlantic bluefin tuna (Thunnus thynnus), and greater amberjack in captivity (Chen et al., 2006; Corriero et al., 2007; Masuma et al., 2011; Zupa et al., 2017). Lower GSI levels and the presence of fewer vitellogenic oocytes strongly indicate that rearing fish in captivity can negatively affect vitellogenesis (Corriero et al., 2007; Pousis et al., 2011). In this study, the GSI levels of both males (5.59–6.94%) and females (4.29–7.06%) during the observed spawning period were comparable to those of wild fish (6.63–8.33% and 4.70–7.74%, respectively) (Shiraishi et al., 2008; Kim et al., 2020). Conversely, we observed relatively delayed gonadal development in females and a later spawning period compared with the results of previous studies (Shiraishi et al., 2008; Yukami et al., 2009; Kim et al., 2020). It is difficult to clearly explain specific factors causing delayed gonadal development, but a possible hypothesis is that undesirable conditions of rearing in land-based tanks may have caused significant stress to the chub mackerel, which could have delayed fish spawning. Accordingly, Pankhurst (2016) reviewed the consistent inhibitory effect of artificial stress (capture, confinement, and husbandry) on the reproductive performance of fish. Similarly, delayed ovulation, reduced egg weight, and egg production were observed in rainbow trout (Oncorhynchus mykiss) exposed to disturbance stress over nine months (Campbell et al., 1992). Significantly elevated plasma cortisol levels but reduced plasma T and E2 levels were observed in rainbow trout exposed to chronic confinement stress for two weeks (Campbell et al., 1994). The effects of stress hormones on the reproductive performance of chub mackerel should be investigated in future studies.

The higher levels of T and 11-KT observed in plasma indicated that male germ cells underwent active spermatogenesis and spermiation (Weltzien et al., 2002; Lintelmann et al., 2003). Sundaray et al. (2021) reported that the pre-spawning peak of T stimulated gonadal growth, increased pituitary gonadotropin hormone levels, and was a precursor of 11-KT. In this study, significantly higher levels of plasma T and 11-KT were observed in males in February; these increases were associated with strong spermatogenesis in the testes. A distinct peak of plasma T was observed in June. Both T and 11-KT are major androgens that play crucial roles in male reproductive performance, of which 11-KT is recognized as the most effective stimulator of spermatogenesis (Cavaco et al., 2001), whereas T also plays a significant role by stimulating hypothalamic and pituitary actions that regulate the testes (Montero et al., 1995). Therefore, the secondary peak of plasma T levels in June could be associated with sexual behavior regulation during the spawning season. Similar to the results of this study, multiple peaks in plasma T levels have been observed during the reproductive cycle in several male fish species (Barannikova et al., 2004; Gerriero et al., 2005). Both T and E2 are produced in teleost fish ovaries. In addition to serving as a precursor for E2, T can enhance oocyte growth by initiating germinal vesicle breakdown during final oocyte maturation (Sang et al., 2019). E2 is secreted by the ovarian follicle and acts on the liver to produce vitellogenin. The highest levels of plasma T and E2 in females in June indicate that the ovaries underwent vitellogenesis and attained maturity. Similar trends have been observed in E2 levels in other fish species, where they remained high in females during the late vitellogenesis stage and rapidly decreased in the post-spawning stage (Mylonas et al., 1998; Kumar et al., 2015).

Gonadotropin-releasing hormone stimulates the pituitary gland to produce and secrete the gonadotropic hormones, follicle-stimulating and luteinizing hormones (Pierce and Parsons, 1981). Follicle-stimulating hormone is involved in initiating gametogenesis and regulating gonadal growth, whereas luteinizing hormone mainly regulates gonadal maturation and spermiation/ovulation by stimulating sex steroid hormone release (Schulz et al., 2001; Mateos et al., 2002). In this study, we found that monthly trends of relative expression levels of pituitary fshβ and lhβ in both males and females had positive correlations with their gonadal developmental stages and plasma sex steroid levels. Supporting this result, Nyuji et al. (2012a) reported that the relative expression level of pituitary fshβ in female chub mackerel gradually increased during ovarian development and peaked during the late vitellogenesis stage. The relative expression level of lhβ in the late vitellogenesis stage was remarkably higher than those in immature and early vitellogenesis stages and that of fshβ and lhβ sharply decreased in the post-spawning stage. Compared with the relative pituitary expression levels of fshβ and lhβ in males from a previous study (Nyuji et al., 2012b), a distinct peak was found in the pituitary fshβ level in the immature stage of males in this study. The significant increase in the pituitary fshβ level in February directly stimulated the testes to upregulate the release of T and 11-KT, causing a transition from the immature stage to the spermatogenesis stage.

In this study, the observed spawning period of chub mackerel extended until mid-July, with plasma sex steroid hormones (T, 11-KT, and E2) and reproduction-related gene expression levels (gnrh1, fshβ, and lhβ) significantly decreasing in July. While a rapid increase in water temperature above 25°C occurred from June to September, coinciding with the observed end of the spawning period, it is important to note that a relationship between high water temperatures and the termination of spawning was not established in this study. Previous research has suggested that water temperature and photoperiod are critical regulators of the reproductive cycle in fish, with moderate increases in temperature generally enhancing reproductive processes within an optimal range (Taranger et al., 2010; Wang et al., 2010). However, exposure to abnormally high temperatures has been associated with gonadal regression and reduced reproductive function, as confirmed in red sea bream (Pagrus major) at 24°C, where suppression of gnrh1, fshβ, and lhβ expression, along with lower serum E2 levels, was reported (Okuzawa and Gen, 2013). While wild chub mackerel typically avoid water temperatures exceeding 25°C (Yasuda et al., 2018, 2023), the specific thermal range for optimal reproductive performance in this species remains unclear. Given these findings, it is plausible that chronic exposure to temperatures above 25°C could negatively impact reproductive function, potentially contributing to the cessation of spawning. However, further studies are needed to confirm the precise thermal thresholds and mechanisms involved.

Based on GSI and gonad histology, we observed fully developed testes and ovaries from April to June and from May to June, respectively. The spawning was extended from end-May to mid-July. We confirmed that gonadal developments were likely mediated by sex steroid hormones, which were regulated by gonadotropic hormones such as follicle-stimulating and luteinizing hormones. The findings of this study provide a better understanding of the reproductive characteristics of chub mackerel in a land-based aquaculture system in Jeju Island and offer useful data for establishing detailed breeding schemes for aquaculture purposes.