Iranian Journal of Fisheries Sciences 19(5) 2705-2719 2020 DOI: 10.22092/ijfs.2020.122632

Reproduction, sexual maturity, and spawning ecology of Talang, Scomberoides commersonnianus, and Needlescaled , in Pakistan

Qamar N.1, 2*; Panhwar S.K.2; Wang P1

Received: December 2018 Accepted: December 2019 Abstract An analysis of sexual pattern, spawning ecology, and size at sexual maturity in two queenfishes (Talang queenfish, Scomberoides commersonnianus and needlescaled queenfish, S. tol) was made. Fish samples were collected monthly by gillnet and trawls from the northern Arabian Sea coast of Pakistan from July 2013 to June 2014. The gonad maturity was categorized in six developmental stages based on visual analysis (colour, morphology) and histological screening of the gonads. The males of Talang queenfish dominated the population with a ratio of 1:0.4 (♂ to ♀) whereas females were higher (1:1.6) in needlescaled queenfish population. Talang queenfish was reproductively active during summer with a peak in June and winter spawning season, which appeared from November to February. Needlescaled queenfish is repeatedly spawner, appeared to be in spawning in the summer and fall. Estimated size-at-sexual- maturity for Talang and needlescaled queenfish suggests that the minimum legal length (MLL) should not be set lower than 35, 38 cm TL respectively. This conservative MLL, equal to or more than a length at functional maturity of both queenfish species would safeguard immature individuals until they reach a size at which they can contribute to

Downloaded from jifro.ir at 8:27 +0330 on Thursday September 30th 2021 the reproductive capacity of the populations in the northern Arabian Sea coast.

Keywords: Age and length-at-sexual maturity, Legal landing size, Queenfishes, Northern Arabian Sea.

1-Key Laboratory of Pharmaceutical Engineering, Ministry of Education, College of Pharmaceutical Sciences, Zhejiang University of Technology, Hangzhou 310014 China 2-Fishery Biology Laboratory, Center of Excellence in Marine Biology, University of Karachi – 75270, Sidh, Pakistan *Corresponding author's Email: [email protected]; [email protected]

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Introduction (2016) described the population Talang queenfish, Scomberoides structure of S. tol and Megalaspis commersonnianus Lacepède, 1801 and cordyla, and also feeding habits in M. needlescaled queenfish, Scomberoides cordyla. The multi mood of oocytes in a tol (Cuvier, 1832), family , shad species Hilsa kelee has been are exploited as an important reported by Panhwar et al. (2012) in commercial fish species occurring in Pakistan. Knowing about the sexual inshore and offshore waters of Pakistan. cycle, reproductive potential, and sizes These species constitute a huge fraction of sexual maturity of two queenfishes in catches in terms of biomass to are essential prerequisites for effective overall commercial fishery landings. conservation as well as formulating Among thirty three species talang management strategies, and sustainable queenfish contribution is very high by use of high ecological and economic means of weight and number, species in the northern Arabian Sea unambiguously more valued species of coast, which are discussed. the family Carangidae in Pakistan (Qamar et al., 2016). A reproductive Materials and methods pattern in fishes is as diverse as their Sample collection and laboratory adoptions to numerous aquatic handling environments. Such types of diversity Fish samples of Scomberoides may concern sexuality, spawning commersonnianus and Scomberoides seasonality, behavior, sensitivity to tol were collected at monthly intervals environmental factors, and particular from July 2013 to June 2014 from gametogenic processes (Jalabert, 2005). commercial catches. Specimens were Downloaded from jifro.ir at 8:27 +0330 on Thursday September 30th 2021 Studying size at sexual maturity is an mainly caught with gillnets and trawls essential parameter to understand the on the northern Arabian Sea (Fig. 1). impact of fishing mortality on spawning Fresh specimens were transported to the stocks and the optimum fishery level Fishery Biology Laboratory, Center of (Polovina, 1987). In Australia, Griffith Excellence in Marine Biology of the et al. (2005) reported biological University of Karachi. Standard parameters which included the morphometric measurements were reproduction of Talang queenfish, taken (cm) as well as total body and however, the life history characteristics gonad weight (gram), and ovary colour. of the Scomberoides remains Initial sex assessment was made after largely unknown despite its huge dissecting each following method commercial importance. In Pakistan, described by Brown-Peterson et al. Panhwar et al. (2014) reported stocks of (2011). S. commersonnianus and Qamar et al.

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Figure 1: Red dotted area indicating main fish landing site (Karachi Fish Harbour) Paksitan

Gonad histology, sex ratios, and GS rotary microtome, stained with index Delafield’s hematoxylin, and Macroscopic analysis of gonad stages counterstained with eosin (Humason, was based on colour and presence of 1967). The monthly sex ratio (males to granulated material, whereas females) was estimated for total microscopic stages were also evaluated samples and was statistically tested for to determine the sex and developmental significant deviations from the expected stage. The histological sections of 1:1 ratio with Pearson’s chi-square

Downloaded from jifro.ir at 8:27 +0330 on Thursday September 30th 2021 gonadal material were made from goodness-of-fit test. The degree of tissues of 438 Talang queenfish, S. gonad maturation in males and females commersonnianus and 353 of was identified and classified closely needlescaled queenfish, S. tol. The following those of Brown-Peterson et method for assessing gametogenesis al. (2011). The monthly gonadosomatic and early life history stages closely index was calculated separately for followed those of Brown-Peterson et al. each sex: Gonad weight (2011). GSI  100 Sex determination was carried out Gonad freebody weight using the histological examination of whereas gonad free body weight was each gonad. A central piece of the calculated by subtracting gonad gonad was fixed in Davidson’s fixative (ovary/testes) weight from body weight. for 48 hours (Shaw and Battle, 1957). Spawning seasonality in both sexes was Subsequently, tissues were embedded determined by the monthly gonad in paraffin, sectioned at 5-7 µm using a weight (GSI) and also based on the

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histological characteristics of the Life span

gonads during the maturation cycle. Maximum age of sampled fish (tmax)can The spawning time and length period be calculated by following (West, for each species was the period between 1990), using the estimated parameters the first and last collection of the fish of the von Bertalanffy growth function:

specimens containing mature gonads. tmax = t0 + (3 / K).

Length at sexual maturity (L50%) Fecundity assessment The size at first maturity was estimated The relationship between fork total and by calculating proportion of mature gonad free body weight was described males and females using total length by the function F = aLb, where F = each size class at an interval of 2 cm number of eggs in thousands, L =

using equation: (Pi=Si/Ti) T (Quinn and length in centimeters, parameter a and b Deriso, 1999) where Si = number of constants. The value of parameters a sexually mature individuals of size and b were estimated by fitting linear class i; Ti = Total number of function F = Log a + b Log L. The individuals observed of size class i. The fecundity data were tested for normality logistic curve was represented by the and homogeneity with the coefficient of equation: where P=the variance (CV).

proportion of mature fish per size class, Temperature and precipitation L=average total length against each size An average temperature and classes; r = slope of curve; L50= total precipitation data was acquired from length at 50% maturity (Hunter et al., the SUPARCO / Meteriological 1989). department Karachi (Fig. 4).

Downloaded from jifro.ir at 8:27 +0330 on Thursday September 30th 2021 Age at sexual maturity Results The parameters of age and growth were Gonad histology, sex ratio and GSI calculated from length frequency data Talang queenfish sets with the von Bertalanffy growth Macroscopic examination of model equation: reproductive inactive and frozen fishes

was difficult, so histology was used for The age at first sexual maturity was confirmation. Histological sections of determined as: gonadal material were made from the 1 L  L t  t  log 50 (McPherson, 50 0 K L tissues of 438 individuals of S. 1965) commersonnianus. Males constituted a Where: t = age, L = asymptotic length significantly greater proportion of the where fish size does not grow and population. Males were more K=growth coefficient. susceptible to fishing pressure and mortality. The sex ratio was

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significantly different 1:0.4 males to square analysis =64.44, df =1, and females calculated for the total samples p<0.005 (Fig. 2a). and was statistically tested with Chi-

Figure 2: Description of male and female ratio in twelve sampling months (a) Talang and (b) needlescaled queenfishes sampled from July 2013 to June 2014, northern Arabian sea.

GSI of females begins to increase from late ripe, ripe, and running ripe were March to July, which indicates the considered as in spawning. The GS initiation of spawning during monsoon index of both sexes rises steadily from (Fig. 3). Actively spawning oocytes had immature to late ripe gonads due to the yolk granules and clear oil vacuoles presence of increasing percentages of while spermatozoa were crammed in spermatozoa and oil granules and falls Downloaded from jifro.ir at 8:27 +0330 on Thursday September 30th 2021 patches (colour plate). Another minor gradually during running to spent stages peak was started from November to due to shedding of eggs and sperms. January during post monsoon post- monsoon. The spawning in both sexes Needlescaled queenfish was determined by an assessment of The sex ratio 1:1.6estimated for males GSI and microscopic gonad to female of Scomberoides tol indicated characteristics. It is interpretable from that female was significantly in greater GS index that spawning season initiates proportion and was not statistically in March and lasts in July showing a significant ( =36.787, p<0.10) peak in June (1.44% F, 0.75% M) with calculated in this study (Fig. 2b). another season appeared from Among the entire sampled population November to February with a peak in size, class ranged from 24-30 was December (0.50%F, 0.45% M) (Fig. found to be dominated. The monthly 3a). Based on the microscopic gonad GS index was used to estimate temporal characteristic male and females in the variation in the males and females

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spawning (Fig. 3b). The GSI estimated value calculated in February for females and males showed peaked determining the presence of residuals of in June due to the presence of active oocytes and sperms respectively. reproductive phase, while the lowest

Figure 3: Temporal variations in gonadosomatic index in terms of male and female of Talang queenfish (a) and needlescaled queenfish (b) from northern Arabian Sea.

The calculated percentage GS index in of GS index in six developmental stages Downloaded from jifro.ir at 8:27 +0330 on Thursday September 30th 2021 six developmental stages in females are in males are immature stage (I) 0.23%; the immature stage (I) 0.25 g; stage early ripe stage (II) 0.36; late ripening early ripening (II) 0.52 g; late ripe stage stage (III) 0.43; ripe stage (IV) 1.66% (III) 1.10 g, ripe stage (IV) 3.51 g and and spent (V) 0.36% was calculated spent 0.50 g. The calculated percentage (Fig. 4).

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Plate I

Plate II Figure 4: Photomicrographs for different developmental stages Plate I (1A) female (2A) Male, Plate II (3A) female (4A) male of Talang queenfish and needlescaled queenfish, respectively (SG=spermatogonia, SCY= spermatocyst, ST=spermatids, GE= germinal epithelium, Lu= Lumen, CT= connective tissue, PG= primary growth oocyte, OG= oogonia, CA= cortical alveoli, N= nucleus, POF=post ovulatory follicle, GVM= germinal vesicle migrations, AO=atretic oocyte, MA=Macrophages aggregates, CT= connective tissues, OV=oil vacuoles,). Photograph @ 50 micron.

Gonad developmental in relation to the August to October. The early ripe (II Downloaded from jifro.ir at 8:27 +0330 on Thursday September 30th 2021 monsoon oscillation stage) females distingue from the Oscillation of monsoon that is a presence of primary oocytes and significant characteristic of the northern cortical alveoli appeared from the end Arabian Sea, enhance spawning of March up to April. The late ripe and efficacy of both of the species, the ripe (III and IV stage) females were variation of rain and temperature hike identified with oil droplets and zona during monsoon and off monsoon are radiata noted from May to August depicted in (Fig. 5). peaked in June. The females in running ripe (V stage) appeared in the Talang queenfish population in November, December and The microscopic evaluation suggests April characterized by the that oogenesis initiates in December postovulatory follicle and atretic and lasts up to March when most oocytes. females found immature (1 stage) with a peak occurring in January followed by

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Figure 5: Average temperature and precipitation recorded in the respective year 2013-2014, northern Arabian Sea coast of Pakistan.

The spent (VI stage) females were epithelium and the resting/spent (VI identified with recrudescence gonads stage) noted with residuals of unshaded observed in various months such as spermatozoa and expansion of February, April, May, and November to connective tissues in November to December. The process of December and their peak (38%) found spermatogenesis initiates when in February. immature (I stage) appeared in December to February and peaked in Needlescaled queenfish January, the immature males were also The microscopic gonad stages were observed in October. The individuals in categorized in six developmental Downloaded from jifro.ir at 8:27 +0330 on Thursday September 30th 2021 the early ripe (II stage) were recorded stages: I, immature; II, early ripe; III, in March and May. These were peaked late ripe; IV, ripe stage; V, running and in March with clearly seen abundant VI, recently spent stage. Most of the spermatocytes. Such conditions were immature females with thin translucent reappeared in September and ovary observed in November and very December. The late ripe and ripe (III few in December. The individuals of and IV stage) was initiated from April the early ripe stage were in considerable to June with the highest of individuals number with an abundance of in the ripe stage captured in June when secondary growth oocytes in February most of the spermatozoa packed in the and the lowest in May. Hundred percent lumen. The running ripe (V stage) of females with yolk plates were in a males observed in November with late ripe stage in June and fewer in centrally degenerated germinal October. The individuals in the running ripe from August to December with a peak stage were appeared in the population in September and rarely seen in

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November. The individuals went in with the highest recorded in September. spent condition from July, and these The spent male gonad was peaked in individuals significantly noted with December with abundant connective brown bodies and atretic oocytes in tissues. August and October. The males in the immature stage noted in various Length and age at sexual maturity months, and their peak found in March Talang queenfish with few spermatogonia. The The males and females attained length individuals entered in the next at first maturity in 35 and 39 cm of total developmental stage (early ripening) length respectively obtain from the noted in a substantial number in logistic fit model, whereas males February. The individuals in the late matured earlier than females. The age-

ripe stage with spermatids in patches at-maturity and tmax for combined sexes observed from March to May with the was 4.4 and 11.8 years respectively highest percentages in May. The ripe (Fig. 6). individuals appeared in May and peaked in June, nevertheless few males Needlescaled queenfish in a ripe condition were also noted in The males and females attained sexual November. The individuals in the maturity between the length of (38-39 running ripe stage with proliferated cm) total length and age 5.13 years. The

spermatozoa found in July to December tmax was calculated 7.9 years for both sexes (Fig. 6).

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Figure 6: Sigmoid curve fitted for both sexes of talang, S. commersonnianus and needlescaled queenfish, S. tol sampled in 2013-2014, northern Arabian Sea (L50 = 35, 39 for females and males, respectively age of maturity for combined sexes 4.4, tmax = 11.8 years estimated for talang queenfish; L50 = 38.1, 39 male and female respectively, age at maturity 5.13 year and tmax= 7.9 year).

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Reproductive potential (Fecundity fecundity and fish body variables such assessment) as fork length, and gonad-free body Talang queenfish weight is interpretable from the The reproductive potential (fecundity) coefficient of determination R2 values was estimated from ten ripe females (Tables 1 and 2). ranging from 57.5-112 cm TL and weighing 1140-10500 g,respectively. Needlescaled queenfish The number of eggs counted was Assessment of fecundity was made 95250-594783 CV= 0.590 with an from sixteen ripe females of IV-V average number of 398063 of eggs stages, measuring 38-68 cm TL and counted from females considered in the weighing 600-1700 g chosen in spawning stage. Linear regression was different months. applied to test the relationships between

Table 1: Regression estimation for batch fecundity expressed as number of eggs/g ovary-free body weight and FL for two Carangids in the Northern Arabian Sea coast. Species Equation Intercept Slope (b) SE of the R2 (a) estimate S. commersonnianus F= a+b FL 1.844 2.039 0.200 0.716 F= a+b GFBW 0.252 4.566 0.328 0.270 S. tol F= a+b FL 1.773 2.440 0.223 0.200 F= a+b GFBW 2.452 1.161 0.072 0.821

Table 2: The reproductive potential (fecundity) estimated for two Carangid species (Stage IV-V) in this study (CV= coefficient of variation). Name of the species Total length Body weight Min and Max eggs (average) CV (Range in cm) (Range in g) S. commersonnianus 57.5−112 1140−10500 95250±594783 (398063) 0.590 S. tol 38−68 600−1700 111974±417043 (233883) 0.454

Downloaded from jifro.ir at 8:27 +0330 on Thursday September 30th 2021 The counted number of eggs ranged the coefficient of determination (Tables 111974±417043 (CV=0.454), and the 1 and 2). average number of eggs counted for each ripe fish was 233,883. The Length-at-age relationship between fecundity and fork The fitted logistic growth curves for length and gonad-free body weight was Talang queenfish and needlescaled

Log10 F=1.773+2.440 Log10 FL, queenfishes were estimated for both 2 R =0.200; Log10 F=-1.161+2.452 Log10 sexes and relatively departed from each OFBW, R2 = 0.821 is interpretable from other (Fig. 7).

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Figure 7: Length-at-age data and logistic growth model estimated for Talang queenfish (A) and needlescaled queenfish (B).

Discussion activity is a general hypothesis. Annual gonad determination of two Besides, lipid constituents in gonads queenfishes demonstrated that both also influence the maturation cycle and species are repeatedly spawners that spawning period, which was studied in appeared with certain peaks in the Scomberoides lysan from Indian northern Arabian Sea coast. The sex waters(Norungee and Kawol, ratio Scomberoides commersonnianus 2011).The gonad maturation in S. tol appeared to be male-biased, the reason reached at advance stages during the for this biasness is unclear. summer and spring at the time when Nevertheless, biased sex ratios might be spawning takes place. Further due to sex-specific migration, multimode of eggs validates spawning differences in growth or mortality rates partiality. Due to the dearth of

Downloaded from jifro.ir at 8:27 +0330 on Thursday September 30th 2021 (Panhwar et al., 2012). The prevalence published literature on the reproductive of adult males in catches was different biology of S. tol, it was not possible to to that from observations made by compare the results of this study. Griffiths et al. (2005) who collected However, the reproductive periodicity 50% males and female of S. or spawning pattern could differ in commersonnianus in northern Australia. Carangid species, some Carangid shows The dominance of one sex to other dual reproductive pattern and some could be related to the differential spawns once a year (Conover, 1992; growth and mortality (Kaiser, 1973) or Cortés, 1999). In general, the maturity may be the earlier maturation of both could be impacted by temperature, sexes. Females typically spend food, and genetics influence. Our noticeably high effort in reproductive finding validates that both Talang development comparing to males (Gabr queenfish and needlescaled queenfish et al., 1998). Therefore, ovaries are partial spawning species, primarily reflecting the duration of fish spawning spawn in summer and winter observed

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in the northern Arabian Sea. Spawning al. (2005) reported that it is three years season and sexual maturation are vital a little bit earlier than queenfishes for estimating population dynamics and occurring in the Northern Arabian Sea. management of the species stocks Nevertheless, males often mature (Thulasitha and Sivashanthini, earlier than females. This is because the 2013).Two spawning seasons (summer liver plays an important role in and winter) were observed in S. regulating reproductive cycles by commersonnianus. Generally, most of stocking lipids and contributes in the the marine inhabitants in tropical seas process of vitellogenesis. Another spawn throughout the year while reason may be due to the habitat showed seasonal breeding (Hopper et preference of both sexes, which not al., 1998). In this context, Weatherly gratify the maturity at the same size. On and Gill (1987)stated that the spawning the sexual maturity, Griffiths et al. period in many bony fishes living in (2005)reported that females of S. lower latitude commences earlier and commersonnianus matured as 476 mm may last longer, it may be related to the in Australian water grew quickly in rate of the stress of the protracted early years of the age (up to 3 years), growing season and a small winter. and maximum age was calculated as 11 Koob and Callard (1999)reported from years. Nevertheless, growth estimation Sri Lankan water that Scomberoides of this species is relatively fair in lysan spawns twice a year with intensity Pakistan (Panhwar et al., 2014) than the occurred in September. Besides, it Australian waters. Both sexes of S. described that either sea temperature or commersonnianus sexually mature at photoperiod or both directly involved in the length of 35cm and 32cm at the age reproductive synchrony. It directly of 4.4 years, respectively. This length at related to biological production and maturity was contrasting with those Downloaded from jifro.ir at 8:27 +0330 on Thursday September 30th 2021 food availability as well as plankton reported on S. lysan (Norungee and compositions, which ultimately Kawol, 2011). The Carangids are fast influence the growth of fish. The growing up to the age of three years possibility of mortality during spawning than growth diminish up to their season is also high, and chances to maximum life i.e. 14 yr and at the produce atresic oocyte appeared. length of 120 cm TL (Griffiths et al., Size at sexual maturity data is acquired 2005; Panhwaret al., 2014). for assessing spawning stock biomass Talang queenfish found to be more and for locale reference points for fecund than, needlescaled queenfish, fishing seasons and dynamics. The egg counting from ripe females of length and age at the first sexual Talang queenfish was higher than maturity endorsed that needlescaled counted (Griffiths et al., 2005) earlier queenfish attained later than the Talang rom Australian waters. The assessment queenfish. In this context, Griffiths et of reproductive potential indicated that

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S. tol releases more eggs than S. References commersonnianus such variations may Brown-Peterson, N.J., Wyanski, be occurring due to environmental D.M., Saborido-Rey, F., Macewicz, adaptation that impacts on species to B.J. and Lowerre-Barbieri, S.K., 2011. A standardized terminology species. However, due to the dearth of for describing reproductive published literature on the reproductive development in fishes. Mar Coast potential of needlescaled queenfish, we Fish Dynamics, Management, and were not able to compare. Ecosystem Science [online serial] 3, There was no evidence of sexual 52–70. Doi:10.1080/19425120.2011.555724 dimorphism found in both queenfishes Conover, D.O., 1992. Seasonality and determined from histological sections the scheduling of life history at of male and female reproductive different latitudes. Fish Biology, 41, organs. Hence, it appeared that both 161-78, Doi:10.1111/j.1095- species are dioecious having two 8649.1992.tb03876.x distinct sexes. Queenfishes are Cortés, E., 1999. Standardized diet repeatedly spawner validated from compositions and trophic levels of monthly GSI oscillation and sharks. ICES Journal of Marine synchronous oocyte development, noted Science, 56,707-717. around the year. Assessment of size-at- Gabr, H.R., Hanlon, R.T., Hanafy, sexual-maturity endorses that minimum M.H. and Etreby, S.G., 1998. landing length (MLL) should not be set Maturation, fecundity and lower than 32, 38 TLcm for Talang and seasonality of reproduction of two needlescaled queenfishes, respectively. commercially valuable cuttlefish, This conservative MLL, equal to or Sepia pharaonic and S. dollfusi in more than length at functional maturity, the Suez Canal. Fisheries Research, would safeguard immature individuals Downloaded from jifro.ir at 8:27 +0330 on Thursday September 30th 2021 36, 99-115. until they reach a size at which can Griffiths, S.P., Fry, G.C. and Van der contribute to the reproductive capacity Velde, T.D., 2005. Age growth and of the populations. It is expected that reproductive dynamics of the Talang data and outputs of this study would queen fish, Scomberoides greatly help in guiding management commersonnianusin the northern decisions if conservation strategy Australia. Final report to the developed for queenfish fishery in the National Oceans Office, CSIRO, area. Cleveland, 39P. Hopper, D., Hunter, R. and Acknowledgement Richmond, C.L., 1998. Sexual The work is partially funded by HEC reproduction of the tropical sea and senior author thank ZUT, cucumber, Actinopyga mauritiana Hangzhou for awarding Post doctoral (Echinodermata: Holothuroidea), in fellowship.

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