Fish Sci (2013) 79:251–258 DOI 10.1007/s12562-013-0599-4
ORIGINAL ARTICLE
Biology
GnRHa-induced spawning of wild-caught jack mackerel Trachurus japonicus Mitsuo Nyuji • Kazuki Fujisawa • Yui Imanaga Hajime Kitano • Akihiko Yamaguchi • Michiya Matsuyama
•
Received: 16 August 2012 / Accepted: 17 January 2013 / Published online: 12 February 2013 Ó The Japanese Society of Fisheries Science 2013
Abstract The jack mackerel Trachurus japonicus is a key commercially exploited fish species in Japan. The rearing experiment often provides information that is useful for understanding the reproductive characteristics of wild stocks; however, there has been no study on spawning in captive T. japonicus. In the study reported here, we induced spawning in T. japonicus caught in the wild by hook and line. Females with fully vitellogenic oocytes and males during spermiation were selected by gonadal biopsy and injected with gonadotropin-releasing hormone analog (GnRHa) mixed in molten coconut butter. This treatment was performed four times in different groups of four females and five to eight males, and each group was maintained in a 3-m3 concrete tank. We observed the first spawning at 1 or 2 days post-injection and collected between 41,690 and 149,450 eggs. Spawning was recorded on 18 consecutive days in one experiment and for 3 days continuously in the other experiments. In the former, spawning ended when the water temperature reached 23 °C and occurred mainly between 2100 and 2400 hours. These results indicate that GnRHa-induced spawning may be useful for evaluating the reproductive characteristics of T. japonicus and obtaining fertilized eggs to conduct larval experiments. Keywords GnRHa Multiple spawning Rearing experiment Spawning time Trachurus japonicus
M. Nyuji K. Fujisawa Y. Imanaga H. Kitano A. Yamaguchi M. Matsuyama (&) Laboratory of Marine Biology, Faculty of Agriculture, Kyushu University, Fukuoka 812-8581, Japan e-mail:
[email protected]
Introduction The jack mackerel Trachurus japonicus is a key commercially exploited species of pelagic fish in Japan. They are mainly caught by purse seine in the East China Sea, along the coast of the Japan Sea, and off the Pacific Coast of southern Japan [1]. Since 1997, the Japanese T. japonicus fishery has been managed through a total allowable catch system, which is determined by estimating the allowable biological catch; Japanese sardine Sardinops melanostictus and chub mackerel Scomber japonicus are managed similarly [2, 3]. The reproductive characteristics of adult fish are required for accurate stock assessment and fishery management. T. japonicus spawns between January and May in the offshore waters of the southern East China Sea, which is this species largest spawning ground [1]. In this species, size and age at first maturity are assumed to be a fork length (FL) of[190 mm and 1–3 years, respectively [4–6]. However, population data are insufficient, necessitating a field investigation to understand the distribution and migration, age, and growth of the T. japonicus stock. Little information is also available on the reproductive characteristics of T. japonicus. For example, there is growing interest in the application of stock reproductive potential (SRP) to better understand stock–recruitment relationships. The SRP is a measure of the annual variation in a stock’s ability to produce eggs and larvae [7, 8]. Although several SRP measures have been proposed, total egg production (TEP) is considered one of the better indices for estimating the SRP [9]. The TEP index is estimated on the basis of realized fecundity using batch fecundity and spawning frequency [10]. Batch fecundity and spawning frequency of T. japonicus have been reported for fish caught in the southern East China Sea [6, 11], but no other studies have
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been published. The spawning time of T. japonicus has been predicted to be before dawn [6] but has not been clarified. Captive experiments often provide useful information for understanding the reproductive characteristics of fishes. For example, in the Tsushima Current population of chub mackerel, spawning frequency was estimated by comparing the degenerative stage of the postovulatory follicles (POFs) to those of reared fish, with the morphological characteristics of the POFs classified in accordance with the length of time after the induction of ovulation in females with fully vitellogenic oocytes using human chorionic gonadotropin (hCG) injection [12]. One of the advantages of captive experiments for examining reproductive characteristics is the ability to obtain information under a particular rearing condition with high reproducibility. In addition to the spawning characteristics of adult fish, larval growth and survival are important factors affecting pelagic fish recruitment [13], but few rearing experiments on T. japonicus have been conducted [14]. To study these aspects, it is necessary to develop a method to successfully obtain fertilized eggs from captive adult T. japonicus. Therefore, we designed an experiment on captive T. japonicus to study its reproductive characteristics and to determine a suitable method for producing fertilized eggs. Many cultured fish complete vitellogenesis (females) or spermatogenesis (males), although they usually do not spawn spontaneously in captivity because females fail to undergo final oocyte maturation (FOM) and ovulation [15]. Hormonal manipulation techniques have therefore been developed to induce FOM, ovulation, and spawning using pituitary extracts containing gonadotropins (GtHs), hCG, and gonadotropin-releasing hormone analog (GnRHa) which stimulates the release of luteinizing hormone (LH) [15]. In our previous study, we found that in adult T. japonicus reared for over 1 year in concrete tanks, females failed to undergo vitellogenesis and the testes of males during spermiation were much smaller than those in wild fishes, even though they were of reproductive age and had reached a mature size and body condition [16]. A similar dysfunction of vitellogenesis has been observed in the Mediterranean greater amberjack Seriola dumerili [17, 18]. Therefore, for an FOM/spawning-induction method with hormonal manipulation to be established in T. japonicus, it is necessary to produce or obtain adult fish that can complete vitellogenesis and spermatogenesis. Here, we report on GnRHa-induced spawning in T. japonicus. The results of our study provide new information for use in elucidating the reproductive characteristics of this species. Because captive-reared T. japonicus were not suitable for induced spawning, we used wild T. japonicus captured using a low-stress fishing method.
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Materials and methods The adult T. japonicus used in this study were commercially caught by hook and line from the Chikuzen Sea and transferred to 3-m3 outdoor concrete tanks at the Fishery Research Laboratory of Kyushu University, Fukuoka Prefecture, Japan (Fig. 1). The following day, the fish were anaesthetized with 2-phenoxyethanol (200 ppm) and a gonadal biopsy was taken using a plastic catheter to collect gonadal tissues. A portion of ovarian tissues was immersed in Ringer’s solution (135 mM NaCl, 2.4 mM KCl, 1.5 mM CaCl2, 1 mM MgCl2, 1 mM NaHCO3, 0.5 mM NaH2PO4), and the diameters of 10–20 oocytes (mostly advanced) were measured to determine oocyte development. Another portion of ovarian tissues was immersed in Sera solution (ethanol:formalin:acetic acid, 6:3:1, v/v/v) to clear the cytoplasm, and then the presence of a nucleus (germinal vesicle, GV) was confirmed (Fig. 2). If a GV was not seen, indicating oocyte regression, the fish was not suitable for induced spawning [19, 20]. Females possessing ovulated eggs were also removed because fertilization is inhibited by overripe eggs [21]. Consequently, females with normal oocytes (diameter [500 lm) were selected to receive the spawning induction treatment, with males during spermiation. The hormonal treatment was performed at around 1400 hours according to the method described by Scott et al. [22]. In brief, GnRHa (des Gly10-D-[Ala6] LHRH ethylamide; Sigma-Aldrich, St. Louis, MO) dissolved in 50 % ethanol was mixed with molten coconut butter. While
Fig. 1 Location of the spawning grounds of the jack mackerel Trachurus japonicus around Japan, including the capture and laboratory locations. Shaded area Spawning grounds (Kanaji et al. [44]). Area enclosed by gray box is enlarged in the lower right corner of the figure. Arrow Capture location, arrowhead location of the Fishery Research Laboratory of Kyushu University
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Fig. 2 Stereomicroscopic photographs of whole oocytes of jack mackerel T. japonicus. An oocyte immersed in Ringer’s solution (a), and normal vitellogenic (b) and atretic (c) oocytes cleared by Sera solution. GV Germinal vesicle
under anesthesia, fish of both sexes were injected intramuscularly with GnRHa mixed in coconut butter at a dose of 400 lg/kg. Four females and five to eight males were reared in a 3-m3 outdoor concrete tank under natural conditions with circulating seawater and fed frozen-thawed krill Euphausia superba every day. Released eggs were collected in a 300-lm net, which was checked every 2 h during each spawning night. For each spawning, the timing of intense spawning, number of eggs spawned, and fertilization rate [buoyant eggs/(buoyant eggs ? sunken eggs) 9 100] were recorded. The timing for intense spawning was defined as the time period during which [70 % released eggs were collected for each spawning night. The GnRHa treatment was performed four times in total—on 1 June 2009 (experiment 1) and on 26 May and 1 and 15 June 2011 (experiments 2, 3, and 4, respectively). In experiment 1, about 100 fertilized eggs were incubated until hatching, and the hatching rate (hatched eggs/fertilized eggs 9 100) was recorded. Non-treated and/or sham control groups were not set up for each experiment since the number of fish available was small, and eggs were not released when the fish were caught and maintained in a similar manner for about 3–4 days (unpublished). In each experiment, fish were killed at 7–8 days after the last spawning under the guidelines for animal experiments at the Faculty of Agriculture and Graduate Course of Kyushu University, and in accordance with the laws (No. 105) and declaration (No. 6) of the Japanese government. The FL and body weight (BW) of fish are shown in Table 1.
Results The mean FL of female T. japonicus in experiment 1 and experiments 2–4 were [300 and \300 mm, respectively (Table 1). The mean BW of females in experiment 1 and experiments 2–4 were approximately 400 and \300 g, respectively (Table 1). Gonadal biopsy revealed that \50 % of females in experiments 1–3 had ovulated eggs, whereas the majority of females ([60 %) in experiment 4 had ovulated eggs. The first spawning of a group of T. japonicus was observed 2 days after the GnRHa treatment in experiments 1–3, whereas it occurred 1 day after the GnRHa treatment in experiment 4. Fish ate krill in experiment 1, but not in the other experiments. Data recorded for the first and third spawning events of each experiment are shown in Table 2. During experiment 1, spawning was recorded for 18 consecutive days, from June 3 to 20 (Fig. 3). During this period, one female died on June 13 and 15, respectively. The mean water temperature was 20 °C at the first spawning on June 3 and exceeded 23 °C when continuous spawning stopped on June 21 (Fig. 3). Spawning was observed again on June 23 when the water temperature dropped to \23 °C, but it ended when the water temperature once again reached 23 °C. We collected 144,470 eggs on the first night of spawning, 92,040 on the second night, and 1,600–33,000 on the other nights (Fig. 3; Table 2). The mean fertilization and hatching rates were 35.9 ± 4.2 % [mean ± standard error of the mean (SEM); minimum 1.3 %, maximum 82.6 %] and 86.1 ± 1.7 % (mean ± SEM; minimum 67.6 %, maximum 95.3 %), respectively
Table 1 Fork length and body weight of female and male Trachurus japonicus used in the study Females
Fork length (mm) Body weight (g)
Males
Experiment 1
Experiment 2
Experiment 3
Experiment 4
Experiment 1
Experiments 2–4
308.5 ± 8.2 407.6 ± 12.6
268.8 ± 3.4 266.2 ± 12.4
282.5 ± 11.8 293.7 ± 31.0
272.3 ± 4.9 268.7 ± 15.0
275.7 ± 2.2 296.4 ± 9.0
271.2 ± 14.9 333.0 ± 24.0
Data are presented as the mean ± standard error of the mean
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15.6
220 4,540
69.1 74.1
10,800
74.0
74.4
12,070
56.5
78.9
9,140
56.0 27.9
107,680 11,440
82.6
58.6
38,090 24,350 Sunken eggs (n)
Fertilization rate (%)
41.7
10,350
24,330
4,220
40
260 14,690
10,150 30,890
41,690 16,450
12,230
46,370
34,300
115,340
91,010 13,410
23,760 20,800
11,660 41,770
149,450 19,630
Buoyant eggs (n)
8,190 53,950
144,470
120,120
Total number of eggs (n)
92,040
20.3 20.3
2100–2400 1900–0200
20.4 20.3
2100–0200
19.7
2000–2400
19.0
2100–2400
17.8
2000–2300
17.9
2000–2400 2000–2400
17.9 20.1
2100–2300 2000–2400 Timing of intense spawning (h)
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20.1 20.3 Water temperature (°C)
1900–0200
17 June 2 16 June 1 3 June 1 28 May 1 3 June 1 Date: Number of spawnings:
4 June 2 2009 Years:
5 June 3
2011
29 May 2
30 May 3
5 June 3
2011 2011
4 June 2
4 3 2 1 Experiment:
Table 2 Water temperature, timing of intense spawning, total number of eggs, and hatching rate recorded between first and third spawnings in experiments 1–4
2100–2400
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18 June 3
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(Fig. 3). The highest fertilization rate was recorded at the first spawning (June 3), whereas the highest hatching rate was found at the 16th spawning (June 18). During the monitoring period, sunrise and sunset were at about 0510 and 1930 hours, respectively. Eggs were found in the net between 1900 and 0200 hours, but primarily between 2100 and 2400 hours, with the exceptions of June 6, 15, and 23, when eggs were collected mainly at 0200 hours on the next day (Fig. 4). Spawning was recorded for 3 consecutive days during experiments 2–4. For each experiment, the total numbers of eggs spawned at the first spawning were 149,450, 115,340, and 41,690, respectively, and mean fertilization rates were 46.8 ± 9.5, 75.8 ± 1.6, and 52.9 ± 18.7 %, respectively. Intense spawning was observed between 1900 and 0200 hours, but primarily between 2100 and 2400 hours. The mean water temperature during the three continuous spawnings was approximately 18 °C in experiment 2 and about 20 °C in experiments 3 and 4.
Discussion The availability of adult fish that have completed vitellogenesis and spermatogenesis is a key factor to the successful induction of FOM and spawning using hCG and/or GnRHa. None of the T. japonicus raised in concrete tanks for more than 1 year underwent normal gametogenesis, with females either not starting or completing vitellogenesis and males having a lower gonadosomatic index than wild males, possibly due to the stress associated with longterm captivity [16]. Stress due to handling, chasing, and frequent netting interrupts the spawning cycle by inhibiting the recruitment of ovarian follicles for vitellogenic growth [23]. This phenomenon has been reported in T. japonicus, in which the majority of females had atretic oocytes when they were caught live by purse seine [24]. In our study, wild adult T. japonicus were caught by hook and line during the spawning season. This technique was adopted because the stress experienced after hook and line capture is lower than that from capture in a fishing net [25]. Consequently, adult T. japonicus females with oocytes that were [500 lm in diameter and spermiating males, both of which were suitable for induced spawning, were used in our study. Captive T. japonicus typically do not undergo spontaneous spawning in land tanks without hormonal manipulation [14]. Hormone-induced spawning has been achieved in other species of the family Carangidae, mainly those belonging to the genus Seriola, such as the goldstriped amberjack Seriola lalandi [26], the greater amberjack [18], and Japanese yellowtail Seriola quinqueradiata [27], all of which are important aquaculture species. In the greater
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Fig. 3 Multiple spawning of jack mackerel T. japonicus induced by gonadotropinreleasing hormone analog treatment in experiment 1. Top panel Average daily water temperature. Dashed line indicates 23 °C. Bottom panel Number of released eggs (sunken eggs and buoyant eggs), fertilization rate, and hatching rate
Fig. 4 Sunrise and sunset times (gray zone hours of darkness) and the timing of intense spawning (black box) in experiment 1
amberjack, multiple GnRHa pellets were found to induce continuous spawning [18]. GnRHa pellet implants are highly effective for inducing multiple spawning because GnRHa continually circulates in the blood to stimulate LH release from the pituitary [15]. However, because implanting a pellet might inflict damage to the body of a small pelagic species, we used a single GnRHa injection combined with molten coconut butter for our experiments. With this technique, GnRHa continuously circulates in the blood because the coconut butter solidifies rapidly in the fish [22]. The GnRHa treatment induced spawning 2 days posttreatment in experiments 1–3, whereas fish spawned 1 day
post-treatment in experiment 4. These different responses to GnRHa may be based on the time when the fish were captured from the wild. Fish used in experiments 1–3 were caught between the end of May and early June, whereas those used in experiment 4 were caught in the middle of June. Unlike the females in experiments 1–3, the majority of females in experiment 4 had ovulated eggs, indicating that this group was in an active spawning condition. Some female T. japonicus caught by hook and line fishing naturally spawned the next day, but continuous spawning has not been described [28]. These females may have ovulated when they were caught. However, we only used females without ovulated eggs, suggesting that the endogenous
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signal responsible for stimulating FOM and spawning in experiment 4 may have been activated in some females at the first spawning regardless of the GnRHa injection. A group of four females and five males exhibited multiple spawning after GnRHa treatment in experiment 1. In another study, a similar GnRHa injection method was used for another small pelagic species, the chub mackerel, and groups of females and males performed multiple spawning in that study also [29], similar to our observations. Plasma GnRHa degrades within about 1 week when injected in combination with molten coconut butter [22], suggesting that the continuous spawning observed 1 week after GnRHa treatment might have been controlled by the endogenous endocrine system in these fish. Therefore, the reproductive characteristics found 1 week after GnRHa injection can be considered to reflect the actual biological potency of T. japonicus; that is, data obtained from experiment 1 will be valuable for understanding T. japonicus spawning characteristics. Unlike experiment 1, spawning ended after a 3-day spawning period in experiments 2–4. Although the reason for this is unclear, food intake may play a role. In general, capital breeders store energy until the spawning period and do not feed throughout the entire reproductive season. In contrast, food intake influences the number of spawnings during the breeding season in fish species categorized as an income breeders, which adjust their food intake concurrently with breeding [30, 31]. As the closely related T. trachurus has been proposed to be an income breeder because it feeds throughout its spawning period [32], T. japonicus is also considered an income breeder. In our study, T. japonicus caught in the wild were difficult to feed, and they did not eat krill during experiments 2–4. Fortunately, however, the fish used in experiment 1 did consume feed and showed long-term continuous spawning, suggesting that food intake could maintain continuous spawning in a group of captive T. japonicus. During experiment 1, the captive group of T. japonicus spawned for 18 consecutive days between 3 and 20 June, or between 2 and 19 days post-injection of GnRHa. The water temperature was 20 °C at the beginning of spawning and exceeded 23 °C when continuous spawning stopped. Thereafter, the group of fish spawned once on June 23, 22 days post-injection, when the water temperature temporarily declined below 23 °C. According to field data from the East China Sea, the surface water temperature ranges from 15 to 25 °C in the spawning area of T. japonicus mainly between January and June [33]. Likewise, T. japonicus larvae are mainly collected in water at temperatures ranging from 21 and 23 °C [34]. The multiple spawning of T. japonicus in our study was observed to occur in the range of these reported water temperatures, indicating that a water temperature above 23 °C limits the spawning of this species.
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Four females were injected with GnRHa and reared in the same concrete tank in each experiment. The number of eggs collected was 115,340–149,450 at the first spawning in experiments 1–3 but decreased to about 20,000 at the third spawning. In experiment 4, the number of eggs collected was only 41,690 at the first spawning and decreased to \1,000 at the third spawning. This difference in the number of eggs between experiments 1–3 and 4 indicates that the fecundity of female T. japonicus caught during the active spawning season was lower than that of fish caught earlier in the season. As discussed above, fecundity observed within 1 week after GnRHa treatment may not be equal to real biological potency because exogenous GnRHa may enhance the release of LH during early spawning. Conversely, fecundity recorded 1 week after treatment can be considered to be a reflection of the real biological potency, as the GnRHa might have been depleted from the fish’s body. In experiment 1, one female each died on 13 and 15 June (12 and 14 days post-injection, respectively), after which the other two females spawned 8,320–33,400 eggs per day from 16 to 20 June (15–19 days post-injection). During this late spawning period, batch fecundity can be estimated at 4,160–16,700 eggs per female if both females spawned every day during this period, whereas it was 8,320–33,400 eggs per female if one female participated in each spawning. Therefore, we assume batch fecundity to be 4,160–33,400 eggs per female in our study, although this estimate is not precise. In general, batch fecundity of wild fish is estimated by counting the number of hydrated oocytes or germinal vesicle migrating (GVM) oocytes in the ovary [35]. Although there is little information on T. japonicus, its batch fecundity is estimated to be about 31,000 eggs for an average female of 230–290 mm FL [6]. This is similar to our estimated maximum value in females of about 310 mm FL. The batch fecundity of other Trachurus species has been estimated to be 205–208 oocytes per gram total BW for T. trachurus [36, 37] and 112 oocytes per gram BW (without ovaries) for T. symmetricus [38]. The batch fecundity of T. japonicus is predicted to be 10.4–83.5 oocytes per gram total BW (about 400 g BW) in our study, which is lower than that for other Trachurus species. In experiment 1, released eggs were collected every day from two females between 16 and 20 June, suggesting that a female T. japonicus has the ability to spawn daily and/or in 1-day or longer intervals. The spawning frequency of wild T. japonicus has been estimated to be 0.3 in the southern East China Sea throughout the spawning season, indicating that females spawn every 3.3 days on average [11]. In the closely related T. symmetricus, it is thought that females spawn in 1- to 3-day intervals [38]. Spawning frequency is generally estimated by observing the histological characteristics of GVM oocytes or POFs [39]. To
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estimate the spawning frequency of wild stocks, the criteria for the assessment of time elapsed until next spawning based on GVM oocytes or since recent spawning based on POFs should be evaluated in T. japonicus. Our results show that FOM and spawning can be induced in captive wildcaught T. japonicus, suggesting that rearing experiments can be performed in T. japonicus, similar to those performed in the chub mackerel [12], to further refine the estimation of spawning frequency. In all experiments, fertilized eggs appeared daily between 1900 and 0200 hours, particularly between 2100 and 2400 hours, indicating that T. japonicus spawn after sunset, with a peak at around midnight. This finding is consistent with information available on other species of Trachurus, in which spawning occurs overnight [37, 38]. During the spawning period in experiment 1, the highest fertilization rate occurred at the first spawning and then varied during subsequent spawnings, gradually decreasing to the last spawning. A similar trend has been observed in the natural spawning of captive greater amberjack [40]. In T. japonicus, the hatching rate of fertilized eggs was consistently high throughout the spawning period. Egg and sperm quality affect the ability of eggs to be fertilized and, consequently, to hatch. This effect has been described in fishes for which environmental factors (such as temperature and photoperiod) as well as nutrition, stress, and other factors are related to gamete quality; however, they are not well characterized [41]. In contrast, milt volume and sperm quality decline in male fishes exhibiting multiple spawning [42, 43]. Therefore, the fertilization success of T. japonicus might have decreased in parallel with a reduction in the physical condition of the male. On the contrary, the fertilization rate was generally high ([50 %) during the 3-day spawning period in experiments 3–4, with the exception of on 28 May (first spawning in experiment 2) and 18 June (third spawning in experiment 3). These results demonstrate that fertilized eggs can be continuously produced for at least 3 days after GnRHa treatment and were associated with a high fertilization rate. In conclusion, adult T. japonicus caught by hook and line were effectively induced to undergo FOM and spawning. Here, for the first time, we have demonstrated that GnRHa treatment induced multiple spawning between 1900 and 0200 hours in T. japonicus that were held in an outdoor concrete tank. Although only the fish in one experiment successfully demonstrated long-term continuous spawning, our data are very valuable because there is limited information on the reproductive characteristics of captive T. japonicus. Moreover, using the GnRHa treatment we successfully obtained fertilized eggs from T. japonicus in all trials, suggesting that larval experiments can be conducted using the method presented here. The experimental system we used to induce spawning may be useful for evaluating the reproductive characteristics of
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T. japonicus, as information related to stock assessment is currently limited to field data. Acknowledgments We thank the students in the Laboratory of Marine Biology, Kyushu University, and Dr. Michio Yoneda of the National Research Institute of Fisheries and Environment of Inland Sea, for their experimental support. This study was performed as part of the Establishment of Rearing Systems in Jack Mackerel Program, which is supported by the Fisheries Agency of Japan. These studies were also supported in part by a Grant-in-Aid for Scientific Research (23658163) from the Ministry of Education, Culture, Sports, Science, and Technology of Japan. M. N. is supported by JSPS Research Fellowship for Young Scientist.
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