鱼类生殖与发育

Spawning time,spawning frequency and fecundity of Japanese chub mackerel,Scomber japonicus in the waters around the Izu Islands,JapanTomohide Yamada a ,Ichiro Aoki a,*,Isamu Mitani baDepartment of Aquatic Bioscience,Graduate school of Agricultural and Life Science,The University of Tokyo,Bunkyo,Tokyo 113,JapanbKanagawa Prefectural Fishery Experimental Station,Youroushi,Jogashima,Misaki,Kanagawa 238-02,JapanReceived 4July 1997;accepted 5April 1998AbstractFemale Japanese chub mackerel,Scomber japonicus ,were collected in 1993from April to June (36days),in the water around Izu Islands,Japan,which is one of the primary spawning areas.Spawning time,spawning frequency and batch fecundity were determined by histological methods.Temporal frequency of hydrated oocytes and new postovulatory follicles showed that female chub mackerel spawned actively from 22.00to 24.00hours.The average spawning frequency was 17.4%during this sampling period.We estimated that chub mackerel spawned every 5.7days (6.3times)during these 36days.Fifteen females spawned almost every day.Twelve females which had hydrated oocytes in their ovaries were used for estimating batch fecundity.The average batch fecundity was 89200oocytes per female,and the relative batch fecundity was 158eggs per gram female wet weight.The batch fecundity was signi®cantly correlated with condition factor.This shows that batch fecundity was affected by nutritional state of spawning female.#1998Elsevier Science B.V .All rights reserved.Keywords:Japanese chub mackerel;Batch fecundity;Postovulatory follicle;Spawning frequency;Spawning time;Ovary histology1.IntroductionJapanese chub mackerel (Scomber japonicus )is one of the most important ®shery stocks in Japan.The size of this stock increased in the 1960s and remained high in the 1970s.The stock,however,decreased continu-ously in the 1980s and is currently at a low level.Spawning dynamics is a fundamental element in assessing and managing ®sh stocks.Maturation and spawning of Japanese chub mackerel have beenreported around the Izu Islands,Japan,which appears to be one of the main spawning grounds (Murayama et al.,1995;Yamada et al.,1996).Daily egg produc-tion methods (DEPM)(Alheit,1993)may be applied to estimate the spawning biomass of chub mackerel populations.Priede and Watson (1993)suggested that DEPM should be preferred for estimation of biomass in Atlantic mackerel (Scomber scombrus ).By this method,the spawning frequency de®ned as the ratio of the number of females and the batch fecundity as the number of eggs released per spawning,are essen-tial parameters.The spawning frequency and batch fecundity of chub mackerel have been reportedonly*Corresponding author.Tel.:+81338122111,ext.5307;fax:+81338120529;e-mail:aoki@hongo.ecc.u-tokyo.ac.jp 0165-7836/98/$±see front matter #1998Elsevier Science B.V .All rights reserved.P I I :S 0165-7836(98)00113-1by Dickerson et al.(1992)for the population off the west coast of North America.Similar data do not exist for the Japanese population located in the north-western Paci®c Ocean.The annual egg production method has been applied to the Japanese chub mackerel on the basis of the number of oocytes greater than 0.5mm diameter in the ovary (Watanabe,1983).However,serial spawners such as chub mackerel do not have annual egg pro-duction determined prior to the spawning season (Hunter et al.,1985).The objectives of the present study are to apply the DEPM to the Japanese chub mackerel stock,and in addition to investigate spawn-ing time,spawning frequency and batch fecundity of this species around the Izu Islands.2.Materials and methods 2.1.SamplingFemale chub mackerel were collected by hook-and-line or dip net ®shing conducted at night aboard the R.V .Enosima-maru in April±June 1993off the Izu Islands (Fig.1).A total of 192female chub mackerel was collected over a period of 36days (Table 1).The samples were strati®ed into 2-h intervals by the time of day to examine the spawning rhythm over 24-h periods.Samples were not obtained 22:00±04:00hours from 19to 20May;02:00±04:00hours on 28May and 18:00±02:00hours from 1to 2June.Although,wetried to catch chub mackerel in the daytime by hook-and-line,none was caught between 04:00and 18:00hours.Sea surface temperature at the sampling stations ranged from 16.58C to 18.88C.2.2.Fish measurementsThe ®sh were kept in cold storage at 2±58C on the ship,and then fork length (mm),and total body weight (g)were measured in the laboratory.After ovaries were removed,body weight without ovary (g)and ovary weight (g)were measured.Afterwards,ovary samples were preserved in 10%neutral buffered formalin.The mean fork length of all ®sh was 381mm.We considered all individuals in our samples to be capable of spawning,because their lengths were larger than the size at sexual maturity as estimated by Watanabe (1970).The gonad somatic index (GSI)and condition factor (CF)were de®ned asGSI Gonad Weight g a Somatic Weight g Â100CF Somatic Weight g a Fork Length 3 mm Â1002.3.Histological analysisA portion of each ovary from each of the 192females was embedded in paraf®n for histological examination.Sections (8m m)were stained with hematoxylin and eosin.As a preliminary examination,sections from six parts (right and left,fore,middle,and rear)of 12ovaries were examined to differentiate the maturation stage in relation to position in the ovary.No difference was found in maturation stage in respect to ovary position.Based on these ®ndings,a tissue sample from the middle part of the right ovary was used for histological examination.2.4.Classification of maturation stage of the oocyteand the postovulatory follicles The oocytes were classi®ed into the following ®ve maturation stages:primary yolk globule stage,sec-ondary yolk globule stage,tertiary yolk globule stage,migratory nucleus stage,and hydrated oocytes stage.We estimated the age of postovulatory follicles according to the criterion established byDickersonFig.1.Location of sampling station of Japanese chub mackerel (Scomber japonicus )in April,May and June 1993.Broken line 200m.84T.Yamada et al./Fisheries Research 38(1998)83±89et al.(1992):0day(0±24h after spawning),1day (24±48h after spawning),2days(over48h after spawning).We estimated the spawning time and spawning frequency by classifying reproductive states of females from the maturation stage of oocyte and age of the postovulatory follicle in ovaries,based on female samples of2-h segments.The reproduction states of females were classi®ed into the followings.1.Migratory nucleus oocytes:<24h prior to spawn-ing.2.Hydrated oocytes:spawning imminent.3.Hydrated oocytes and new postovulatory follicles: in the act of spawning.4.0day postovulatory:<24h after spawning.5.1day postovulatory follicles:24±48h after spawn-ing6.2days postovulatory follicles:>48h after spawn-ing.2.5.Estimation of batch fecundityBatch fecundity was estimated according to the method of Hunter et al.(1985),which was based on the number of hydrated oocytes in the ovary.The number of hydrated oocytes was counted using a microscope.Females that had both new postovulatory follicles and hydrated oocytes at the same time were not appropriate for batch fecundity estimation, because such females were considered to have begun to spawn the time of sampling.These specimens were excluded from the batch fecundity estimation.Thus, only12females were available for the estimation of the batch fecundity.3.Results3.1.Spawning timeTemporal patterns of reproductive states of females are illustrated in Fig.2.The frequencies of occurrence of the hydrated occytes were12%and15%for18:00±20:00hours and20:00±22:00hours,respectively,but they decreased to3%for22:00±24:00hours and to zero after24:00hour.In contrast,while the0day postovulatory follicles occurred about6%between 20:00and22:00hours,they appeared in30%of females after22:00hour.Females having both hydrated oocytes and new postovulatory follicles were found for20:00±02:00hours,though the percentage was small.The frequency of the individuals that had1Table1Number of samples,sea surface temperature(SST)of sampling stations,and mean fork length(FL)Æstandard deviation(SD)Date Sampling time(h)18±2020±2222±240±22±4SST(8C)16.516.717.317.217.1Mean FLÆSD(mm)345Æ29381Æ16382Æ21381Æ18389Æ24 19May Number9*13*SST(8C)17.918.3Mean FLÆSD(mm)365Æ28378Æ1527±28May Number1615*1514*SST(8C)17.217.617.117.2Mean FLÆSD(mm)390Æ22383Æ17378Æ27383Æ131June Number18* SST(8C)18.8Mean FLÆSD(mm)384Æ15 Total Number3347403438 FLÆSD(mm)374Æ30381Æ16381Æ23382Æ16386Æ20GSIÆSD8.14Æ3.018.89Æ3.628.49Æ3.009.07Æ2.558.35Æ2.23CFÆSD11.17Æ0.7411.13Æ0.8011.21Æ0.8211.33Æ0.6410.81Æ0.75 Fish were caught by hook-and-line and dipnet,but in several cases(*)only by hook-and-line.Blank columns no samples.Means of fork length,gonadosomatic index(GSI)and condition factor(CF)are also shown for2h sampling segmentsT.Yamada et al./Fisheries Research38(1998)83±8985day or 2day postovulatory follicles was independent of the time of day,about 10%.There were no sig-ni®cant differences in fork length,GSI and CF among female samples from different times of day (ANOV A,P <0.05).Spawning of the female started at around 20:00hour,with spawning activity peaking between 22:00and 24:00hours,and completed by 02:00hour.3.2.Spawning frequencyThe spawning frequency of a serial spawner was de®ned as the ratio of spawning females to all females (Hunter and Macewicz,1980).The average spawning frequency of the chub mackerel was estimated from the three independent ratios of spawning females:(1)the ratio of the females with the migratory oocytes,(2)the ratio of females with the hydrated oocytes and the new postovulatory follicles,(3)the ratio of the female with the 1day postovulatory follicles.While the average spawning frequencies on 26±27April and 19May were 8.0%and 7.6%,those on 27±28May and 1June were about 30%(Table 2).This shows seasonal variability of the spawning frequency.The average spawning frequency of all females during the entire sampling period (36days)was estimated to be 17.4%.Hence,female chub mackerel spawned on the average every 5.7days and 6.3times during those 36days.It was noted that 15females had migratory nucleus oocytes,hydrated oocytes,and postovulatoryfolliclesFig.2.Temporal changes in frequencies of the females with migratory nucleus oocytes (MN),hydrated oocytes (HO),and postovulatory follicles within 0±24h after spawning (PO a ),24±48h after spawning (PO b ),and 48h after spawning (PO c ).HO PO a indicates females with both hydrated oocytes and postovulatory follicles.Table 2Spawning frequencies of chub mackerel females,which were estimated from percentages of females in the three spawning states Date Number of mature females Spawning per day (%)MN HO,HO PO a ,PO a PO b Mean 19May 22 4.69.19.17.627±28May 6021.751.718.330.61June 1827.844.427.833.3All19215.126.610.417.4MN:Migratory nucleus oocyte.HO:Hydrated oocyte.PO a :Postovulatory follicles within 24h after spawning.PO b :Postovulatory follicles 24±48h after spawning.HO PO a :In the act of spawning.86T.Yamada et al./Fisheries Research 38(1998)83±89at the same time (Table 3).Twelve of these 15females had spawned on 2or 3successive days.The mean spawning interval was 1.20days during these 36days (Table 3).3.3.Batch fecundityMost of the samples used for estimating the batch fecundity were collected between 18:00and 22:00hours.Batch fecundity showed a wide variation among females.The maximum and minimum was 157600and 18900,respectively,while the average was 89200(Table 4).Relative batch fecundity was de®ned as,batch fecundity per gram female bodyweight without ovary.The average relative batch fecundity was calculated to be 158.The average fecundity per female during the 36day sampling period was estimated at 562000(spawning times (6.3)Âaverage batch fecundity (89200)).Although there was no signi®cant correlation between batch fecundity and fork length (r 0.219,P >0.05)and body weight (r 0.479,P >0.05),batch fecundity was clearly correlated with condition factor (r 0.721,P <0.05)(Fig.3).4.Discussion4.1.Spawning in relation to time of dayIn our study,the state of oocytes changed and the frequency of females with new postovulatory folliclesTable 3Numbers of chub mackerel females with migratory nucleus oocytes,hydrated oocytes,and postovulatory follicles simulta-neously,and mean spawning intervals of these females Spawning state Day interval between spawning (i )Number offemales (N )PO a PO b 14MN PO a14MN PO a PO b 13HO PO b 11MN PO b 23AverageiN /N 18/15 1.2MN:Migratory nucleus oocyte.HO:Hydrated oocyte.PO a :Postovulatory follicles within 24h after spawning.PO b :Postovulatory follicles 24±48h after spawning.Table 4Batch fecundity of chub mackerel females (n 12)with hydrated oocytes Date Fork length (mm)Body weight without ovary (g)Ovary weight (g)Batch fecundity Relative batch fecundity 26April 368556.371.08150014626April 371532.266.0733*******May 329366.535.84650012719May 393607.371.87430012227May 369549.794.410220018627May 380636.582.58990014127May 353482.272.182********May 385702.694.915760022427May 388587.748.7189003227May 362514.580.811390022127May 381605.5107.515120025027May 380603.883.079000131Mean372562.175.789200158Relative batch fecundity batch fecundity/body weight withoutovary.Fig.3.Relation between batch fecundity and condition factor (somatic weight (g)/fork length (mm)3)Â102.T.Yamada et al./Fisheries Research 38(1998)83±8987increased after22:00hour,while females with hydrated oocytes were not present after24:00hour. Watanabe(1970)collected eggs with a plankton net in time series in the spawning grounds,and estimated that spawning of chub mackerel gradually started after sunset with peak spawning activity between22:00and 24:00hours,so our results are consistent with his. The Japanese sardine,Sardinops melanostictus, spawns primarily between20:00and23:00hours (Matsuura,1992;Morimoto,1993;Murayama et al., 1994).The Japanese anchovy,Engraulis japonicus, discharges eggs actively between22:00and 24:00hours(Takano et al.,1983;Turuta,1992).Thus, the spawning times of such small pelagic®shes are similar.This may be a mechanism to reduce predation on newly spawned eggs by zooplanktivores.More-over,as adults are off their guard when spawning, night spawning could also insure the safety of small ®shes.4.2.Spawning frequencyThe histological results revealed seasonal changes in spawning activity.The average spawning frequency indicated that females spawned more actively in late May(30.6%)through early June(33.3%),than from late April(8.0%)to mid May(7.6%).In a study of chub mackerel from the west coast of North America,the average spawning frequency was 8.7%during sampling periods(101days)(Dickerson et al.,1992).Our estimate of the average spawning frequency of17.4%was higher than that of the North America mackerel.Our sample did not cover the entire spawning season and the high frequency was probably caused by our sampling period being concentrated at the peak of spawning.The spawning frequency may be low at the beginning and end of spawning season. Dickerson et al.(1992)reported that32of271 females spawned every1.3days.Similarly,15females of192chub mackerel females in our study spawned every1.2days.Daily spawning appears to occur at the peak of the spawning season.The spawning frequency estimation of Hunter and Goldberg(1980)is based on the assumption that a spawning population does not move in and out of the sampling area and during the spawning season. Although,we did not investigate the movement of the spawning®sh,in some tagging experiments,chub mackerel rarely moved within the spawning area in the peak of spawning season(I.Mitani,unpublished data). It has been reported that the disappearance time of the postovulatory follicles may be in¯uenced by ambient water temperature(Goldberg et al.,1984; Hunter and Macewicz,1985;Turuta,1992).The dragonet,Callionymus enneactiis,spawns every day at28±308C and postovulatory follicles of this species are not seen in ovaries15h after spawning(Takita et al.,1983).In the Japanese sardine,Sardinops malanostictus,postovulatory follicles are not seen 38h after ovulation at208C and48h after spawning at178C(M.Shiraishi,unpublished data).Descriptions by Dickerson et al.(1992)of the change in postovu-latory follicles of chub mackerel were based on rear-ing experiments at208C.In our study,the sea surface temperature in the sampling area was16.5±18.88C. The estimated age of postovulatory follicles may have been a little longer.4.3.FecundityOur estimate of average batch fecundity(89200 oocytes)was greater than that(68400oocytes)of Dickerson et al.(1992).This is due to the difference in body size.The average batch fecundity per gram body weight without ovary in our study(158oocytes/g)was close to(168oocytes/g)in Dickerson et al.(1992). Dickerson et al.(1992)estimated batch fecundity by calculating the migratory nucleus oocytes.The oocytes frequency method usually gives results similar to those based on counts of hydrated oocytes,if females with highly advanced oocytes are used (Hunter and Goldberg,1980;Laroche and Richardson, 1980).There was a signi®cant correlation between condi-tion factor and batch fecundity.This suggests that nutritional condition affects batch fecundity.One female in our samples had an extremely low fecundity; 18900(relative batch fecundity 32).There were many beta atresia oocytes and no yolked oocytes in this female,whereas,the other females did not have beta atresia oocytes in their ovaries.The presence of beta atresia oocytes and the absence of yolked oocytes indicate the end of spawning(Dickerson et al.,1992). Therefore,this female had most likely completed spawning for the season.The CF value of this female was the lowest of all the females.The batch fecundity88T.Yamada et al./Fisheries Research38(1998)83±89of the female was low possibly due to the consumption of nutrition by repeated times of spawning.For Atlan-tic mackerel,as spawning®sh migrate northwards the batch size decreases with progress of the spawning season(Watson et al.,1992).Thus,there may be a difference in batch fecundity between the start and end of the spawning season.In this study,only12females were sampled.More samples are needed to estimate more reliably batch fecundity.As batch fecundity in chub mackerel is likely to vary annually,it should be estimated annually in relation to appropriate environmental factors.AcknowledgementsWe would like to thank Dr.Manabu Shiraishi of the National Research Institute of Aquaculture,Dr. Nobuyuki Azuma of Hirosaki University,the captain and crew of the Enoshimamaru,and the staffs of Kanagawa Prefectural Fisheries Experiment Station.ReferencesAlheit,J.,e of the daily egg production method for estimating biomass of clupeoid fishes:a review and evaluation.Bull.Mar.Sci.53,750±767.Dickerson,T.,Macewicz,B.J.,Hunter,J.R.,1992.Spawning frequency and batch fecundity of chub mackerel Scomber japonicus1985.CalCOFI Rep.33,130±140. 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