Int. J. Aquat. Biol. (2022) 10(6): 524-536 ISSN: 2322-5270; P-ISSN: 2383-0956 Journal homepage: www.ij-aquaticbiology.com © 2022 Iranian Society of Ichthyology Original Article Reproductive biology of greasy grouper, Epinephelus tauvina and coral hind grouper Cephalopholis miniata (Family: Serranidae) in the southern Red Sea, Shalatien, Egypt Ezzat Mohammed-AbdAllah1, Azza El-Ganainy2, Mahmoud M. Farrag1, Mohsen A. Moustafa1, Alaa G.M. Osman1 1Department of Zoology, Faculty of Science, Al-Azhar University, Assiut Branch, 71524 Assiut, Egypt. 2National Institute of Oceanography and Fisheries, Fisheries Division, Egypt. s Article history: Received 7 October 2022 Accepted 21 December 2022 Available online 2 5 December 2022 Keywords: Gonadosomatic index Spawning season Grouper Abstract: Groupers are the main component of commercial fisheries in the Red Sea. The reproductive biology of Epinephelus tauvina and Cephalopholis miniata collected at the Shalatien landing site in the southern Egyptian Red Sea were investigated from January to December 2017. A total of 212 specimens of E. tauvina with a total length range of 23.6 to 70.3 cm and 243 specimens of C. miniata with a total length range of 17.4 to 42.1 cm were examined. Females of E. tauvina and C. miniata accounted for 61.7 and 61.9% of the total fish sampled, showing a 1:1.61 and 1:1.63 male-to-female sex ratio, respectively. The monthly distribution of maturity stages and gonadosomatic index values showed that the spawning season for both sexes was extended from April to October for E. tauvina and from April to September for C. miniata. The lengths at first sexual maturity of the males and females of E. tauvina were estimated at 49 and 48.1 cm, respectively, while those for C. miniata were estimated at 23.2 and 22.7 cm, respectively. All our results can help in the proper management of these valuable resources. Introduction The Shalatien fishing area is a productive area in the Egyptian sector of the Red Sea. Coral reef terraces characterize the coastal area of Shalatien in many regions. These coral reefs help break the waves and form protected areas with abundant food sources for different fishes (Mahmoud et al., 2009). In 2020, groupers (Serranidae) were highly abundant in the Shalatien fishery, representing approximately 34.5% of the fish production from the Shalatien landing site (GAFRD, 2020). Because of their commercial importance, they suffer from strong fishing pressure, which extends to overexploitation (Morris et al., 2000), resulting in a decrease in their population worldwide (Sadovy de Mitcheson et al., 2013; Rajan, 2015; Bulanin et al., 2017; Ohta et al., 2017; de Mitcheson et al., 2020). Many groupers form spawning aggregations at specific locations and times that are often associated Correspondence: Ezzat Mohammed-Abdallah DOI: https://doi.org/10.22034/ijab.v10i6.1774 E-mail: ezzatahmed1278.el@azhar.edu.eg DOR: https://dorl.net/dor/20.1001.1.23830956.2022.10.6.9.2 with the lunar cycle (Sadovy de Mitcheson and Colin, 2012; Osman et al., 2021). At these locations and times, they are especially vulnerable to fishing pressure from artisanal and commercial fisheries because of increased catchability (lethal effects) and decreased reproductive output at lowered animal densities (Sadovy de Mitcheson, 2016; Ohta et al., 2017). Many studies have reported that the total catch of groupers has decreased and that the stock has been overexploited (e.g., Sadovy, 2005; Tharwat, 2005; Mohammad, 2007; Grandcourt et al., 2009; Mohammed-AbdAllah, 2015; El-Ganainy, 2017; Osman et al., 2021). The Red List assessments for all 163 grouper species show that 25% of the species are considered to be at risk of extinction or categorized as being near threatened, but 30% of all species are considered to be data deficient (Sadovy de Mitcheson et al., 2013; IUCN, 2021). An understanding of fish reproductive strategies 526 Mohammed-Abdallah et al./ Reproductive biology of Epinephelus tauvina and Cephalopholis miniata is required to properly manage fisheries (Komolafe and Arawomo, 2007; Dinh, 2018). Knowledge regarding female maturity stages and spawning seasons is important to prevent catches during the spawning season (El-Ganainy, 1997; Osman et al., 2018). The sex ratio provides a useful tool for assessing fish's biological characteristics and estimating a population's reproductive potential (Sossoukpe et al., 2013; Sabrah et al., 2017). The gonadosomatic index (GSI) is widely used to measure the extent of reproductive investment, gonadal development and maturity of fish in relation to spawning (Ogunola et al., 2018; Khatun et al., 2021; Sabbir et al., 2021). The length and age at first sexual maturity are important parameters in fisheries research for evaluating the optimum age of the first capture and determining the minimum legal size that may be needed to preserve a suitable spawning stock of a species and to ensure the occurrence of at least one spawning event among mature fish (Lappalainen et al., 2016; Osman et al., 2018; Mawa et al., 2021). This work aimed to investigate the sex ratio, maturity, GSI and length at first sexual maturity of Epinephelus tauvina and Cephalopholis miniata in the Shalatien fishery to provide proper data for the conservation of their stocks. Materials and methods Random samples of E. tauvina and C. miniata were collected monthly from the Shalatien fishing port, which is one of the productive fishing grounds along the Egyptian Red Sea coast and located in the southern Red Sea, at Elba National Park, 520 km south of Hurghada, Egypt (Fig. 1). The samples were collected from January to December 2017. For each specimen, total length (TL) was measured to the nearest cm, and total weight (TW) was determined to the nearest 0.1 grams (g). Specimens were sexed by macroscopic dissection, and the gonads were weighed to the nearest 0.01 grams. The sex ratio was calculated from the formula of Sex ratio (M:F) = Number of Females/Number of males. This ratio was determined during different months and in different length groups. The Chi- square test at the 0.05 significance level was employed to determine the goodness of fit of the observed sex ratio to that of the theoretical sex ratio of 1:1 (M:F). The following formula of Wootton )1998( was used for the Chi-square test. χ2 = [(F-S)2/ S] + [(M-S)2/ S], where χ2 is the symbol for Chi- Square, F is the observed number of females, M is the observed number of males and S is the expected Figure 1. Map of the study area (Shalatien). 527 Int. J. Aquat. Biol. (2022) 10(6): 525-536 number of each sex (the hypothetical 1:1 ratio). The monthly variation in the maturity stage was determined. Six maturity stages were identified according to the scale of Gunderson (1993), with some modifications, as follows: (1) Thread: Sex cannot be determined at this maturity stage, and the gonads in individuals are filamentous, (2) Stage I (Immature or inactive): The gonads have a translucent appearance, and the testes are smaller and thinner than the ovaries, (3) Stage II (Resting): The gonads are translucent and enlarged and the testes do not contain sperm, while the ovaries possess a few small eggs, (4) Stage III (Active or developing): Gonads are larger than Stage II, and the testes are opaque without sperm; ovaries are translucent with small eggs, (5) Stage IV (Active- ripe or developed): Testes are white, and some sperm are expelled from the core when cut, and ovaries are opaque and solid with fully formed eggs, (6) Stage V (Spawning or Ripe-running): Gonads are enlarged and occupy most of the body cavity; milt and eggs are expelled from the genital openings when we press slightly on the two sides of the body, and (7) Stage VI (Spent): Ovaries are flaccid with few eggs, while the testes are almost empty. The GSI is an indirect method used to determine the spawning season of fish. It was calculated for each fish according to Sokal (1995) using the formula of GSI = (gonad weight/total fish weight) x 100. The length at first sexual maturity (Lm) represents the length at which 50% of individuals are mature during the spawning season. Individuals at stages III-VI were considered mature, and it was possible to determine their Lm values. After plotting the percentage of mature individuals against their mid-lengths (King, 1995), Lm was estimated as the point on the X-axis corresponding to the 50% point on the Y-axis. The equation used to estimate Lm from the logistic curve was as follows (Erisman et al., 2010): P = 1/ (1 + exp −r (Lt − Lm)), where P is the proportion of mature individuals in a length class, Lt is the total fish length, r is the intercept, and Lm is the slope. Results A total of 212 specimens of E. tauvina with a TL range of 23.6 to 70.3 cm, including 77 males, 124 female,s and 11 unsexed and 243 specimens of C. miniata with a TL range of 17.4 to 42.1 cm, including 91 males, 148 females and 4 unsexed were collected for reproductive biology studies (Table 1). Sex ratio: The overall sex ratio indicated the occurrence of more females than males for the two studied species. The ratio of males to females of E. tauvina was 1:1.61, and females accounted for 61.7% of the total sampled fish. The sex ratio of males to females of C. miniata was 1:1.63, and females accounted for 61.9% of the total sampled fish. The chi-squared analysis indicated a significant difference compared to the expected 1:1 ratio (χ2 = 10.53, df = 1, P<0.05 for E. tauvina and χ2 = 13.12, df = 1, P<0.05 for C. miniata). The monthly changes in the percentages of males and females are represented in Figure 2 for E. tauvina and Figure 3 for C. miniata. The variation in the male-to-female sex ratios of E. tauvina and C. miniata according to Species Sex n TL (cm) Total weight (g) Min Max Mean ± SD Min Max Mean ± SD E. tauvina Males 77 24.4 62.2 40.6±11.7 206.1 3350.3 1226.5±1050.0 Females 124 27.5 70.3 44.3±12.5 259.9 5015.3 1615.0±1339.3 Unsexed 11 23.6 26.6 25.3±1.0 189.5 265.1 231.8±25.2 Pooled 212 23.6 70.3 42.0±12.6 189.5 5015.3 1402.1±1245.8 C. miniata Males 91 20.2 42 29.5±5.9 135.4 1286.9 474.3±282.8 Females 148 17.4 42.1 27.5±5.0 75.6 1277.9 398.4±283.7 Unsexed 4 22.6 23.5 23.2±0.4 190 214.9 205.7±11.4 Pooled 243 17.4 42.1 28.1±6.1 75.6 1286.9 420.6±284.1 Table 1. Descriptive statistics of means of Epinephelus tauvina and Cephalopholis miniata during (2017) from Southern Red Sea, Shalatien, Egypt. 528 Mohammed-Abdallah et al./ Reproductive biology of Epinephelus tauvina and Cephalopholis miniata length groups is presented in Figures 4 and 5, respectively. Monthly distribution of maturity stages: The seasonal variation in the maturity stage was determined for each individual. The E. tauvina spawning period began in April because ripe gonads could be observed in the samples at that time, and the percentages of spawning individuals were 40 and 0 10 20 30 40 50 60 70 80 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec F re q u e n c y % Month Male Female Figure 2. Monthly variation in the percentages of males and females of Epinephelus tauvina from the southern Red Sea, Shalatien, Egypt. 0 10 20 30 40 50 60 70 80 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec F re q u e n c y % Month Male Female Figure 3. Monthly variation in the percentages of males and females of Cephalopholis miniata from the southern Red Sea, Shalatien, Egypt. 0 10 20 30 40 50 60 70 80 90 100 24 26 28 30 32 34 36 38 40 42 44 46 48 50 52 54 56 58 60 62 64 66 68 70 F re q u e n c y ( % ) Length group (cm) Male Female Figure 4. Percentages of males and females of Epinephelus tauvina according to length group. 529 Int. J. Aquat. Biol. (2022) 10(6): 525-536 45% of the males and females, respectively (Figs. 6, 7). This stage extended until September, revealing a long spawning season, with a peak in May for males (66%) and in June for females (67%). The first appearance of ripe gonads of C. miniata occurred in April, indicating the beginning of the spawning 0 10 20 30 40 50 60 70 80 16 18 20 22 24 26 28 30 32 34 36 38 40 42 F re q u e n c y ( % ) Length group (cm) Male Female Figure 5. Percentages of males and females of Cephalopholis miniata according to length group. 0 10 20 30 40 50 60 70 80 90 100 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec M a tu ri ty s ta g e % Month I II III IV V VI Figure 6. Monthly distribution of maturity stages (I: Inactive, II: Spent, III: Active, IV: Active-ripe, V: Ripe-running, VI: Spent) in male Epinephelus tauvina. 0 10 20 30 40 50 60 70 80 90 100 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec M a tu ri ty s ta g e % Month I II III IV V VI Figure 7. Monthly distribution of maturity stages (I: Inactive, II: Spent, III: Active, IV: Active-ripe, V: Ripe-running, VI: Spent) in female Epinephelus tauvina. 530 Mohammed-Abdallah et al./ Reproductive biology of Epinephelus tauvina and Cephalopholis miniata period. The percentages of individuals in this stage during this month were 15% and 17.3% of the males and females, respectively (Figs. 8, 9). This stage extended until August, revealing a long spawning season, with a peak in June for males (57%) and in May for females (55%). Gonadosomatic index (GSI): The overall GSI values were higher for females than for males in both 0 10 20 30 40 50 60 70 80 90 100 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec M a tu ri ty s ta g e % Month I II III IV V VI Figure 8. Monthly distribution of maturity stages (I: Inactive, II: Spent, III: Active, IV: Active-ripe, V: Ripe-running, VI: Spent) in male Cephalopholis miniata. 0 10 20 30 40 50 60 70 80 90 100 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec M a tu ri ty s ta g e % Month I II III IV V VI Figure 9. Monthly distribution of maturity stages (I: Inactive, II: Spent, III: Active, IV: Active-ripe, V: Ripe-running, VI: Spent) in female Cephalopholis miniata. 0.0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec A v e ra g e G S I Month Males Females Figure 10. Monthly variation in GSI values for Epinephelus tauvina from the southern Red Sea, Shalatien, Egypt. 531 Int. J. Aquat. Biol. (2022) 10(6): 525-536 species. The spawning season of E. tauvina was extended from April to October, while it spanned only from April to September for C. miniata. The highest value of this index was recorded in May for males and females of E. tauvina and C. miniata (Figs. 10, 11), and the lowest values for both sexes were recorded in January for E. tauvina and in December for C. miniata. Length at first sexual maturity (Lm): The Lm values for the males and females of E. tauvina were estimated at 49 and 48.1 cm (Fig. 12), respectively, while those for the males and females C. miniata were estimated at 23.2 and 22.7 cm (Fig. 13), respectively. 0.0 1.0 2.0 3.0 4.0 5.0 6.0 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec A v e ra g e G S I Month Males Females Figure 11. Monthly variation in GSI values for Cephalopholis miniata from the southern Red Sea, Shalatien, Egypt. 0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1 26 28 30 32 34 36 38 40 42 44 46 48 50 52 54 56 58 60 62 64 66P ro p o rt io n o f m a tu ri ty o f m a le Total Length (cm) P = 1/(1 + exp−0.2.8× (TL − 49.0)) (A) 0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1 26 28 30 32 34 36 38 40 42 44 46 48 50 52 54 56 58 60 62 64 66 P ro p o rt io n o f m a tu ri ty o f fe m a le Total Length (cm) P = 1/(1 + exp−0.3× (TL − 48.1)) (B) Figure 12. Logistic curves for the proportions of mature males (A) and females (B) of Epinephelus tauvina from the southern Red Sea, Shalatien, Egypt. 532 Mohammed-Abdallah et al./ Reproductive biology of Epinephelus tauvina and Cephalopholis miniata Discussion The application of the sex ratio is useful in studying spawning populations (Faltas, 1983; Sabrah et al., 2017). In the present study, the sex ratio of E. tauvina and C. miniata revealed that females dominated the catch during the whole period of study. Our results agree with those recorded by Ohta et al. (2017) for E. tauvina in the Yaeyama Islands and Wahbeh (2005) for C. miniata in the Aqaba Gulf, Jordan. According to Wahbeh (1992), Cherif et al. (2007) and Sabrah et al. (2017), the predominance of females may be connected with the higher catchability of females than males or due to the high mortality of females, as they are more vulnerable to fishing pressure. Chakroun-Marzouk and Ktari (2006) reported an unbalanced sex ratio favouring females in some species, revealing that natural mortality may be higher among males, while females may present high vulnerability to fishing. According to the length group’s evaluation, males of E. tauvina were dominant at smaller fish sizes and absent among larger fish sizes, while females of C. miniata were dominant at all sizes. The results are supported by Nikolsky (1963), who stated that males predominate in fish populations at early life stages, while females predominate later due to probable adaptive mechanisms. The sex ratio in these species could vary greatly; however, no studies have explicitly addressed the potential mechanisms explaining those patterns. The monthly distribution of maturity stages showed that the ripe stage for males and females of E. tauvina began in April, ended in September, and increased to its highest peak in May for males and in June for females. On the other hand, the ripe stage for males and females of C. miniata began in April, ended in August, and increased to its highest peak in May for both males and females. These results 0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1 16 18 20 22 24 26 28 30 32P ro p o rt io n o f m a tu ri ty o f m a le Total Length (cm) P = 1/(1 + exp−0.66× (TL − 23.2)) (A) 0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1 16 18 20 22 24 26 28 30 32 P ro p o rt io n o f m a tu ri ty o f fe m a le Total Length (cm) P = 1/(1 + exp−0.7× (TL − 22.7)) (B) Figure 13. Logistic curves of the proportions of mature males (A) and females (B) of Cephalopholis miniata from the southern Red Sea, Shalatien, Egypt. 533 Int. J. Aquat. Biol. (2022) 10(6): 525-536 indicate that both E. tauvina and C. miniata in the southern Red Sea, Shalatien, have a prolonged spawning season that extends from April to October for E. tauvina and from April to September for C. miniata. The GSI refers to the relationship between the gonadal weight and the fish somatic weight (Wootton, 1991), and the seasonal timing of reproduction is often identified based on changes in the GSI (Biswas, 1993; King, 2013; Ogunola et al., 2018). Our results revealed that the GSI differed between males and females of E. tauvina and C. miniata; the GSI for males was lower than that for females. These results suggest that the energy invested in gamete production by females is likely more than that invested by males (Patimar, 2008). The results showed that the GSI increased in both sexes of E. tauvina from April to October and in both sexes of C. miniata from April to September, indicating the timing of the spawning season in these species. These findings for E. tauvina agree to some extent with those found by Ohta et al. (2017) in the Yaeyama Islands, Japan, Abu-Hakima et al. (1982) in Kuwait and El-Ganainy (2017) in the Red Sea, Egypt, whose investigations of the spawning season of E. tauvina indicated that it occurs from March to June. Abu‐Hakima (1987) stated that E. tauvina collected from Kuwait spawned in April and May. El-Sayed (1999) recorded that E. tauvina in the Persian Gulf spawns in May and June, while members of this species from Kuwait spawn from March to May (Mathews and Samuel, 1987). The observed decrease in the GSI values during January for E. tauvina and December for C. miniata indicated the end of the spawning season and the beginning of the spent and resting periods. Likewise, the spawning season of C. miniata in the Aqaba Gulf, Jordan, was found to occur between May and October (Wahbeh, 2005). El-Ganainy (2017) stated that C. miniata collected from the Red Sea, Egypt, spawned in May and June. The spawning season of C. miniata is relatively long, which is consistent with the general pattern of longer spawning seasons among smaller groupers (Sadovy, 1996; Wahbeh, 2005). Differences between our results and the previous studies about the spawning seasons of investigated species may be attributed to differences in water temperature among locations (Jansen and Gislason, 2011; Osman et al., 2018), sampling techniques, geographic disparity and the sampling year of the studies (Soykan et al., 2020). Knowing the Lm of fish helps predict their harvestable size and hence has great value for fishery management (Sabrah et al., 2017). In the present study, E. tauvina reached first sexual maturity at 48.55 cm TL. The Lm values of E. tauvina found in the present study were longer than those reported by Ohta et al. (2017) in the Yaeyama Islands, Japan, Species Author Region Spawning season Sex ratio (M:F) Lm E . ta u v in a Abu-Hakima et al. (1982) Kuwait water March to June - 61.1 Mathews and Samuel (1987) Kuwait water March to May - - El-Sayed (1999) Persian Gulf off Qatar May to June - 53 Shakeel and Ahmed (1996) Maldives - - 37.5 Abu-Hakima (1987) Kuwait water April to May - - Ohta et al. (2017) Yaeyama Islands, Japan March to June 1:1.8 37.1 El-Ganainy ( 2017) Red Sea, Egypt May to June - 36.6 Present study Red Sea, Shalatien, Egypt April to October 1:1.61 48.55 C . m in ia ta Shakeel and Ahmed (1996) Maldives - - 20 Wahbeh (2005) Aqaba, Jordan May to October 1:1.28 - El-Ganainy (2017) Red Sea, Egypt May to June - 28.2 Present study Red Sea, Shalatien, Egypt April to September 1:1.63 22.95 Table 2. The spawning season, sex ratio and the length at first sexual maturity (Lm) of Epinephelus tauvina and Cephalopholis miniata found in the present study and in various regions by different authors. 534 Mohammed-Abdallah et al./ Reproductive biology of Epinephelus tauvina and Cephalopholis miniata Shakeel and Ahmed (1996) in the Maldives (37.3 cm) and El-Ganainy (2017) in the Red Sea, Egypt (36.6 cm), but smaller than those reported by El- Sayed (1999) in the Persian Gulf (53 cm) and Abu- Hakima et al. (1982) in Kuwait waters (61.1 cm) (Table 2). Our results revealed that C. miniata reached first sexual maturity at 22.95 cm. These findings roughly correspond to those obtained by Shakeel and Ahmed (1996) for C. miniata collected in the Maldives (20 cm) but are smaller than those estimated by El-Ganainy (2017) in the Red Sea, Egypt (28.2 cm). These differences in length and age at the first sexual maturity of investigated species in the present study and in the previous studies may be attributed to the length and age at first sexual maturity of fishes influenced by environmental factors like abundance and seasonal availability of food, predation, temperature, photoperiods and also the locality (Osman et al., 2018; Adekoya et al., 2019; Hossen et al., 2019; Soykan et al., 2020). It can be concluded that, both sexes of E. tauvina and C. miniata in the Shalatien landing site in the southern Red Sea, Egypt, showed a prolonged spawning season that extended from April to October in E. tauvina and from April to September in C. miniata. E. tauvina reached sexual maturity at 49 cm for males and 48.1 cm for females, while C. miniata reached sexual maturity at 23.2 cm for males and 22.7 cm for females. Fishing of spawning aggregations leads to a reduction in the average size of the individuals caught and a remarkable decline in the sex ratio. Establishing protected areas (or no-take zones) in the Red Sea is a valuable management option for protecting the size and the breeding populations of coral reef fish, especially groupers that aggregate to spawning. References Abu-Hakima R. (2006). Aspects of the reproductive biology of the grouper, Epinephelus tauvina (Forskål), in Kuwait waters. Journal of Fish Biology, 30: 213- 222. Abu-Hakima R., Al-Abdul-Elah K., El-Zahr C., Akatsu S., Al-Shoushi M., Abdullah M. (1982). Spawning season and fecundity of six commercially important food fishes found in Kuwait. Annual Research Report (Kuwait Institute for Scientific Research, Kuwait). 74 p. Adekoya E., Abdul W., Abdulraheem I., Bashir A., Folarin O. (2019). Seasonal Variation in The Biology of Chrysichthys auratus (Geoffroy Saint-Hillaire, 1809) in Ogun State Estuary, Nigeria. West African Journal of Applied Ecology, 27(1): 95-107. Biswas S. (1993). Manual of methods in fish biology, South Asian Publishers. 157 p. Bulanin U., Masrizal Masrizal Z.A.M. (2017). Hermaphroditism in the white spot grouper Epinephelus coeruleopunctatus (Pisces: Serranidae) harvested from Padang City waters, Indonesia. F1000 Research, 6 . Chakroun-Marzouk N., Ktari M.H. (2006). Caractéristiques de la reproduction et de la croissance pondérale relative de Pomadasys incisus (Haemulidae) du golfe de Tunis. Cybium 30(4): 333-342. Cherif M., Zarrad R., Gharbi H., Missaoui H., Jarboui O. (2007). Some biological parameters of the red mullet, Mullus barbatus L., 1758, from the Gulf of Tunis. Acta Adriatica, International Journal of Marine Sciences, 48(2): 131-144. de Mitcheson Y.J.S., Linardich C., Barreiros J.P., Ralph G.M., Aguilar-Perera A., Afonso P., Craig M.T. (2020). Valuable but vulnerable: Over-fishing and under-management continue to threaten groupers so what now? Marine Policy, 116: 103909. Dinh Q. (2018). Aspects of reproductive biology of the red goby Trypauchen vagina (Gobiidae) from the Mekong Delta. Journal of Applied Ichthyology, 34(1): 103-110. El-Ganainy A.A. (1997). Population dynamics of lizard fishes (Synodontidae) from the Red Sea. PhD thesis. Faculty Science, Suez Canal University, Ismailia, Egypt. El-Ganainy A.A. (2017). Stock assessment and gear description of the Red Sea and Gulf of Suez fisheries for their proper management. Final report submitted to Science and Technology development Fund (STDF), Ministry of Scientific Research, Egypt. 124 p . El-Sayed A.F.M.E., Abdel-Bary K. (1999). Reproductive biology of grouper fish Epinephelus tauvina (Family Serranidae) in the Persian Gulf waters. Indian Journal of Marine Sciences, 28: 89-91. Erisman B.E., Craig M.T., Hastings P.A. (2010). 535 Int. J. Aquat. Biol. (2022) 10(6): 525-536 Reproductive biology of the Panama graysby Cephalopholis panamensis (Teleostei: Epinephelidae). Journal of fish biology, 76(6): 1312- 1328. Faltas S.N. (1983). Study of purse-seine fisheries in Egyptian Mediterranean waters with special reference to the biology of Sardine in the catch. PhD thesis. Faculty of Science, Alexandria University, Egypt. GAFRD, General Authority for Fish Resources Development (2020). Annual fishery statistics report. Ministry of Agriculture Publications, Cairo, Egypt. Grandcourt E., Al Abdessalaam T., Francis F., Al Shamsi A., Hartmann S. (2009). Reproductive biology and implications for management of the orange‐spotted grouper Epinephelus coioides in the Southern Persian Gulf. Journal of Fish Biology, 74(4): 820-841. Gunderson D.R. (1993). Surveys of fisheries resources, John Wiley and Sons. 248 p. Hossen M., Hossain M., Pramanik M., Uddin N., Rahman M., Islam M., Nawer F. (2019). Biometry, sexual maturity, natural mortality and fecundity of endangered halfbeak Dermogenys pusilla (Zenarchopteridae) from the Ganges River in northwestern Bangladesh. Indian Journal of Geo- Marine Sciences, 48: 1548-1555. IUCN (2021). The IUCN Red List of Threatened Species. Version 2021-3. Jansen T., Gislason H. (2011). Temperature affects the timing of spawning and migration of North Sea mackerel. Continental Shelf Research, 31(1): 64-72. King M. (1995). Fisheries biology, assessment and management. Fishing News Books, Oxford, England, pp: 107-111. Komolafe O., Arawomo G. (2007). Reproductive strategy of Oreochromis niloticus (Pisces: Cichlidae) in Opa reservoir, Ile-Ife, Nigeria. Revista de Biología Tropical, 55(2): 595-602. Lappalainen A., Saks L., Šuštar M., Heikinheimo O., Jürgens K., Kokkonen E., Vetemaa M. (2016). Length at maturity as a potential indicator of fishing pressure effects on coastal pikeperch (Sander lucioperca) stocks in the northern Baltic Sea. Fisheries Research, 174: 47-57. Mahmoud H.H., Ezzat A.A., Ibrahim M.A. (2009). Assessment of inshore commercial fisheries of Halaieb/Shalatien area “Red Sea”. Egyptian Journal of Aquatic Research, 35: 148-164 . Mathews C., Samuel M. (1987). Growth, mortality and assessment for groupers from Kuwait. Kuwait Bulletin of Marine Science, 9(9-10): 173-191. Mawa Z., Hossain M.Y., Hasan M.R., Tanjin S., Rahman M.A., Sarmin M.S., Habib K.A. (2021). First record on size at sexual maturity and optimum catchable length of 10 marine fishes from the Bay of Bengal (Bangladesh) through multi-models approach: a key for sound fisheries management. Environmental Science and Pollution Research, 1-11. Mohammed A.S. (2007). Population dynamics and stock assessment of some species of genus Cephalopholis and genus Variola from the Red Sea M.Sc. thesis. Department of Zoology, Faculty of Science, Assiut University, Egypt. 117 p. Mohammed-AbdAllah E. (2015). Some fisheries and biological studies on the areolate grouper Epinephelus areolatus (Family, Serranidae) from the Gulf of Suez. M.Sc. thesis. Department of Zoology, Faculty of Science, Al-Azhar University, Egypt. 112 p. Morris A.V., Roberts C.M., Hawkins J.P. (2000). The threatened status of groupers (Epinephelinae). Biodiversity and Conservation, 9(7): 919-942. Moyle P. (2004). Hydromineral balance. Fishes: an Introduction to Ichthyology. 93 p. Nikolsky G.V. (1963). Ecology of fishes. Ecology of fishes, Academic press. Ogunola O.S., Onada O.A., Falaye A.E. (2018). Preliminary evaluation of some aspects of the ecology (growth pattern, condition factor and reproductive biology) of African pike, Hepsetus odoe (Bloch 1794), in Lake Eleiyele, Ibadan, Nigeria. Fisheries and Aquatic Sciences, 21(1): 12. Ohta I., Akita Y., Uehara M., Ebisawa A. (2017). Age- based demography and reproductive biology of three Epinephelus groupers, E. polyphekadion, E. tauvina, and E. howlandi (Serranidae), inhabiting coral reefs in Okinawa. Environmental Biology of Fishes, 100(11): 1451-1467. Osman A.G., El-Ganainy A., Abd-Allah E. (2018). Some reproductive aspects of the areolate grouper, Epinephelus areolotus from the Gulf of Suez. The Egyptian Journal of Aquatic Research, 44(1): 51-56. Osman H.M., El Ganainy A., Shaaban A.M., Saber M.A. (2021). Reproductive biology of the two commercially important grouper species Epinephelus summana and E. polyphekadion in the Egyptian coast of the Red Sea. Egyptian Journal of Aquatic Biology and Fisheries, 25(1): 665-679. 536 Mohammed-Abdallah et al./ Reproductive biology of Epinephelus tauvina and Cephalopholis miniata Patimar R. (2008). Some biological aspects of the sharpnose mullet Liza saliens (Risso, 1810) in Gorgan Bay-Miankaleh wildlife refuge (the southeast Caspian Sea). Turkish Journal of Fisheries and Aquatic Sciences, 8: 225-232. Rajan P. (2015). Conservation status of marine faunal diversity in India: An analysis of the indian wildlife (Protection Act) and IUCN threatened species. marine faunal diversity in India, Elsevier. pp: 461-471. Sabrah M.M., Heneish R.A., Alwany M.E., Ahmad M.I. (2017). Sexual maturity, spawning activity, sex ratio and fecundity of two Mullidae species dwelling the Gulf of Suez, Red Sea. The Egyptian Journal of Aquatic Research, 43(1): 83-91. Sadovy de Mitcheson Y. (2016). Mainstreaming fish spawning aggregations into fishery management calls for a precautionary approach. BioScience, 66(4): 295- 306. Sadovy de Mitcheson Y., Colin P. (2012). Reef fish spawning aggregations: biology, research and management. Fish and Fisheries Series, 35: 595-604. Sadovy de Mitcheson Y., Craig M.T., Bertoncini A.A., Carpenter K.E., Cheung W.W., Choat J.H., Cornish A.S., Fennessy S.T., Ferreira B.P., Heemstra P.C. (2013). Fishing groupers towards extinction: a global assessment of threats and extinction risks in a billion dollar fishery. Fish and Fisheries, 14(2): 119-136. Sadovy Y. (2005). Trouble on the reef: the imperative for managing vulnerable and valuable fisheries. Fish and Fisheries, 6(3): 167-185. Sadovy Y.J. (1996). Reproduction of reef fishery species. Reef fisheries, Springer. pp: 15-59. Shakeel H., Ahmed H. (1996). Exploitation of reef resources: grouper and other food fishes. Workshop on Integrated Reef Resources Management. Ministry of Fisheries and Agriculture, Republic of Maldives. 312 p. Sokal R.R. (1995). The principles and practice of statistics in biological research. Biometry, 451-554. Sossoukpe E., Nunoo F.K.E., Dankwa H.R. (2013). Population structure and reproductive parameters of the Longneck croaker, Pseudotolithus typus (Pisces, Bleeker, 1863) in nearshore waters of Benin (West Africa) and their implications for management. Agricultural Sciences, 4(6A): 9. Soykan O., Gülşahin A., Cerim H. (2020). Contribution to some biological aspects of invasive marbled spinefoot (Siganus rivulatus Forsskål 1775) from the Turkish coast of southern Aegean Sea. Journal of the Marine Biological Association of the United Kingdom, 100(3): 453-460. Tharwat A.A. (2005). Stock assessment of orange-spotted grouper Epinephelus coioides inhabiting the Persian Gulf at Saudi Arabia. Saudi Journal of Biological Sciences, 12(2): 81-89 . Wahbeh M.I. (1992). Aspects of the reproduction biology and growth of two species of goatfish (Mullidae) from Aqaba, Red Sea. Senckenbergiana Maritima. Frankfurt / Main, Alemania, 22: 255-264. Wahbeh M.I. (2005). Some Aspects of Reproduction and Growth of the Grouper, Cephalopholis miniata (Forsskål), the Blacktip Grouper, Epinephelus fasciatus (Forsskål), and the Lunartail Grouper, Variola louti (Forsskål) from the North-eastern Coast of the Gulf of Aqaba (Red Sea), Jordan. Pure Sciences, 32(2): 172-181. Wootton R.J. (1991). Fish ecology, Springer Science and Business Media. 212 p. Wootton R.J. (1998). Ecology of teleost fishes. Kluwer Academic Publs., Dordrecht, The Netherlands A-B. 392 p.