Mohammad I. Wahbeh * ABSTRACT
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1 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 Mohammad I. Wahbeh * ABSTRACT A total of 16 specimens of the coral grouper, Cephalopholis miniata (71 males, 89 females), 185 specimens of the blacktip grouper, Epinephelus fasciatus (6 males, 79 females), and 123 specimens of the lunartail grouper, Variola louti (56 males, 67 females) were collected from the north-eastern tip of the Gulf of Aqaba during the period January through December, 2. Monthly changes in the gonadosomatic index showed a distinctive spawning season during May-October in C. miniata and V. louti, and during June-September in E. fasciatus. A significant departure of the sex ratio from 1:1 was significant (χ 2 = 32.69, P <.1) in C. miniata only. The temporal distribution of males and females of the three groupers showed significant variability (F 11,55 = , P <.3). The von Bertalanffy growth curve parameters calculated from mean total-length-at-age were : L = 6.6 cm, K =.73 / yr, t o = for males, and L = 56.7 cm, K =.86/ year, t o = for for females of C. miniata, L = 31.2 cm, K =.132 / yr, t o = for males and L = 27.9 cm, K =.173 / yr, t o = -1.2 for females of E. fasciatus, corresponding to L = 65.7 cm, K =.2 / yr, t o = for males and L = 54.6 cm, K =.1 /yr, t o = for females of V. louti. The slope of the length-weight relationship indicated an isometric or an approximate isometric growth in the three species. KEYWORDS: Gonadosomatic index, protogyny, length frequency distribution, Von Bertalanffy, length-age relationship. INTRODUCTION The family Serranidae is a diverse group of fishes comprising four subfamilies of which Epinephelinae is the largest (Randall, 1986). Epinepheline serranids are generally found in shelf waters and are well represented in tropical and warm temperate latitudes (Randall and Ben-Tuvia, 1983; Fennessy and Sadvoy, 22). Only 23 species of Epinepheline serranids are known in the Red sea, most common of which in the Gulf of Aqaba belong to the genus Cephalopholis (Shpigel, 1985). Serranids are polygamnous fishes that live in welldefined social units, each consisting of up to 12 adult individuals dominated by a single male (Shpigel and Fishelson, 1989; 1991). Monandric protogyny has been reported to be characteristic of the genus Epinephelus * Department of Biological Sciences, University of Jordan. Received on 22/11/24 and Accepted for Publication on 18/4/25. (Smith, 1959; Sadvoy et al., 1994; Brulé et al., 2), while diandric protogeny has been reported for the genus Cephalopholis (Siau, 1994; Chan and Sadvoy, 22). However, not all studies have provided conclusive evidence of protogyny (Bullock et al., 1992; Fennessy and Sadvoy, 22). Published information on the groupers, Cephalopholis miniata, Epinephelus fasciatus, and Variola louti are scarce. Available studies have contributed observations on the diet, habitat, behavior, and classification (Smith, 1959; Randall and Ben-Tuvia, 1983; Shpigeland Fishelson, 1989;1991). The purpose of the present study is to provide information on some aspects of reproduction and growth of the aforementioned three most common speciesof groupers in the Gulf of Aqaba. MATERIALS AND METHODS Due to the absence of a commercial fishery in Aqaba, fish samples were collected monthly by gillnets and fish
2 traps over the period January through December, 2. After measuring the Total Length (TL) and whole Body Weight (BW) of each fish to the nearest.1cm and g, scales from above the lateral line were removed, cleaned well, and pressed between slides for later examination of growth rings. Following that the gonads of each fish were removed, blot-dried, weighed (GW) to the nearest mg, and used to calculate the gonadosomatic index according to Cailliet et al.(1987) formula: GSI = (GW/BW).. The von Bertalanffy growth formula was used to describe growth: L t = L (1-e k (t-t ) ), where L t is total length (cm), t is age (years), L is asymptotic length, k is the growth coefficient, and t is a hypothetical value corresponding to the age at zero length. The function was fitted to the observed TL at age using the method of Gulland (1969). The length-weight relationship was determined according to the equation: Log BW = log a + b (TL), where BW is whole body fish fresh weight (g), TL is total length (cm), a and b are constants. To plot lengthfrequency histograms, the data were grouped into 1 cm size intervals. The mean total lengths of the resulting modes representing different age groups were estimated by using the probability paper method (Hardings, 1949; Cassie, 195). RESULTS Reproduction: The distribution of males and females in the different age groups (Table 1) revealed a significant departure of the overall sex ratio from 1:1 (χ 2 = 32.64, P<.1) in Cephalopholis miniata only. The sex ratio varied with age and showed male predominance in age group 4 (58.1%) in C. miniata, and in age group 3 in E. fasciatus (7.8%) and V. louti 63 (66.7%). The temporal distribution of males and females (Table 2) did not show any significant departure of the overall sex ratio from 1:1 (χ 2 -test, P>.5) in any species. There was, however, a significant departure from 1:1 during the spawning months. Males of C. miniata predominated in June (66.7%) and July (71.9%), whereas males of E. fasciatus predominated in July (7.5%) and September (68.8%). In V. louti, males predominated in August (62.5%). Monthly variations in sex distribution were significant (F 11, 55 = , P<.1). Species differences in sex ratio were also significant (F 5, 55 = , P<.3). Monthly changes in the GSI of males and females (Fig. 1) indicate a short spawning season. Whereas the GSI increased in May, peaked in July, and declined in October in C. miniata and V. louti, it increased in June, peaked in July, and declined in September in E. fasciatus. Based on GSI, the size at sexual maturation was estimated as 15.8, 14.5, and 17.6cm for males, and as 15.5, 11.8, and 29. cm for females of C. miniata, E. fasciatus and V. louti, respectively. Age and Growth A total of 16 fish of C. miniata (71 males, 89 females), 185 fish of E. fasciatus (6 males, 79 females), and 123 V. louti fish (56 males, 67 females) were aged by counting scale growth rings. Two independent readers agreed on the age of 9 % of C. miniata (144 / 16), 96 % of E. fasciatus (177 / 185), and 87 % of V. louti (7 / 123). Agreed upon specimens were used to analyze age and growth data. Modes representing age groups are shown in lengthfrequency histograms (Fig. 2). Modes were not apparent for E. fasciatus. Histograms show an almost complete overlap of sizes of males and females in the three species. Based on the probability paper method, the expected mean TL of the different age groups was calculated (Table 3). Differences between observed and expected TL were not significant (χ 2 -test, P >.5). The growth curve (Fig. 3) showed a highly significant correlation TL and age in males of C. miniata (r 2 =.9976, P <.1), E. fasciatus (r 2 =.9994, P <.1), and V. louti (r 2 =.9946, P <.1). The corresponding coefficients in females were: r 2 =.9952, P <.1, r 2 =.9913, P<.1, and r 2 =.9812, P<.1, respectively. The regression slope, b, was (.611 for males,.616 for females) in C. miniata, (.459 for males,.56 for females) in E. fasciatus, and (.654 for males,.624 for females) in V. louti. Figure 3 also indicates that none of the three species has reached senility yet. The estimated von Bertalanffy growth function parameters (Table 4) were close for males and females within each species. The growth coefficient, K varied amongst the three species and was in the order: E. fasciatus > V. louti > C. miniata. The L, by contrast was in the order: V. louti > C. miniata > E. fasciatus
3 Some Aspects of Mohammad I. Wahbeh Table 1. Distribution at age of males and females of the groupers, Cephalopholis miniata, Epinephelus fasciatus, and Variola louti from Aqaba, Jordan. Age (Years) C.miniata E. fasciatus V.louti Males Females Males Females Males Females N % N % N % N % N % N % Σ N X df P <.1 >.5 >.5 Table 2. Temporal distribution of males and females of Cephalopholis miniata, Epinephelus fasciatus, and Variola louti in Aqaba, Jordan. Month C. miniata males females >.5 E. fasciatus males females >.5 V. louti males females >.5 Jan, 2 Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Σ N χ 2 d.f. P
4 5 Males 4 C.miniata E.fasciatus V.louti Gonadosomatic index Females Gonadosomatic index J F M A M J J A S O N D Time ( months ) Figure 1. Monthly changes in the gonadosomatic index of males and females of the groupers, C. miniata, E. fasciatus, and V. louti
5 Some Aspects of Mohammad I. Wahbeh Number of specimens Males Females C. miniata Number of specimens E. fasciatus Number of specimens V. louti Total length ( cm ) Figure 2. Length-frequency histograms of males and females of the three groupers, C. miniata, E. fasciatus, and V. louti
6 Figure 3. Linear growth curves of males and females of the three groupers, C. miniata, E. fasciatus, and V. louti. Mean total length (cm) Males C. miniata E. fasciatus V. louti Mean total length (cm) Females Age (Years)
7 Some Aspects of Mohammad I. Wahbeh Table 3. Observed and expected (calculated) total length (cm) of different age groups of The three groups, C. miniata, E. fasciatus, and V.louti. Age C. miniata V. louti Group Males Females Males Females O E O E O E O E χ df P >.5 >.5 >.5 >.5 O = Observed; E = Expected (calculated) Table 4. von Bertalanffy growth constants in males and females of Cephalopholis miniata, Epinephelus fasciatus, and Variola louti from Aqaba, Jordan. Species L ± SE K ± SE t ± SE n C. miniata males 6.6 ± ± ±.276 females 56.7 ± ± ±.365 E. fasciatus males 31.2 ± ± ±.194 females 27.9 ± ± ±.377 V. louti males 65.7 ± ± ±.451 females 64.6 ± 5.9. ± ± Table 5. Length-weight relationship in males and females of Cephalopholis miniata, Epinephelus fasciatus, and Variola louti from Aqaba, Jordan. Species a ± SE b ± SE r n C. miniata males females E. fasciatus males females V. louti males females.121 ± ± ±.98.3 ± ±.2.3 ± ± ± ± ± ± ±
8 The length-weight relationship in both sexes of the three groupers (Table 5) showed highly significant correlations. The regression slopes ranged from and 3.82 in males, and from to in females. Heilman and Philips, 2; Mackie, 2; Chan and Sadvoy, 22). The spawning seasons of C. miniata and V.louti are relatively long, which is consistent with the general pattern of longer spawning seasons among smaller groupers (Sadvoy, 1996). DISCUSSION Reproduction: The population structure of the groupers, C. miniata, E. fasciatus, and V. louti provides no evidence of protogynous hermaphroditism. The characteristics often associated with protogyny (Shapiro, 1987), such a bimodal size-frequency distribution and a female-biased sex ratio were not observed. Unlike the expected in protogynous species, the males of the three studied groupers did not exhibit a tendency to be larger, older, and less numerous than females. In addition, the smallest fish obtained was a male V. louti, which is unexpected in a protogynous species. Furthermore, little differences were found in the mean sizes of males and females of C. miniata (male mean TL = 19.6 ±.5, female mean TL = 2.8 ±.6) and E. fasciatus (male mean TL =17.6 ±.2, female mean TL = 17.4 ±.2). These results unexpected findings are most probably due to the small sample size. The difference between mean TL of V. louti males (26. ± 1.) and females (31.2 ± 1.) was significant. The closeness of male and female mean sizes at age, and the considerable overlap of their size distribution are unexpected, given that the three species studied here are assumed to be protogynous hermaphrodites. To explain such results, Sadvoy and Shapiro (1987) proposed a number of factors that may obscure differences in size and age between males and females. These factors include the failure of some females to change sex due to the absence of genetic or environmental cues, some females may change sex before sexual maturation, and female size at sex-reversal may differ among subpopulations of the same species. Similar results have been reported for other groupers elsewhere (Bullock et al., 1992; Wyansky et al., 2; Fennessy and Sadvoy, 22), indicating inconclusive evidence for protogyny. Spawning in groupers tends to be restricted to less than half the year, with many species spawning primarily during 1 to 2 months (Shapiro, 1987). The spawning season of C. miniata (May-October), E. fasciatus (June- September), and V. louti (May-October) is in agreement with this report. This also agrees with spawning seasons reported for groupers from elsewhere (Manickand- Age and Growth The oldest C. miniata fish collected was 9 years old (TL = 32.5 cm), which agrees with the maximum TL recorded in the Gulf of Aqaba (Shpigel and Fishelson, 1983). The oldest E. fasciatus was 7 years old (TL = 22.3 cm) and that of V. louti was 12 years old (TL = 51.6 cm). There is no record of maximum TL for the two species from the Gulf of Aqaba for comparison. However, maximum TL recorded from the Red Sea was 4 cm for E. fasciatus (Masuda et al., 1975) and 81 cm for V. louti (Randall and Ben-Tuvia, 1983), both of which are considerably larger than what was found in the present study. The differences may be related to differences between fishing methods and geographical location. The growth pattern of the three groupers is similar to that reported for other groupers from elsewhere in that they are long-lived and have low growth rates and high asymptotic lengths (Mathews and Samuel, 1987; Crabtree and Bullock, 1998; Chan and Sadvoy, 22). Species of Cephalopholis have been reported to have growth rates ranging from.11 to.49 cm / yr, and an asymptotic TL ranging from 18.2 to 45.1 cm (El-Etreby et al., 1993; Siau, 1994; Potts and Manooch, 1999). The reported values of K are higher than those reported here for C. miniata ( / yr), but values of L are lower (L = cm). Values of growth rates and asymptotic lengths reported for species of Epinephelus ranged between.6 and.247 cm / yr and between 9.3 and 2.6 cm, respectively (Romero et al., 1987; Johnson and Colins, 1994; Mackie, 2). The growth rates and asymptotic lengths of E. fasciatus (K = cm / yr, L = cm) and V. louti (K =.1 cm / yr, L = cm) are also within reported values. The variability in K and L is most probably due to differences in longevity and environmental conditions. Comparison of the growth performance of the three studied groupers using Φ, where Φ = Log K + 2 log L (Pauly and Munro, 1984) showed very close agreement between males and females of each species. The Φ value for C. miniata was 2.43 for males and females, 2.11 for males and 2.13 for females of E. fasciatus, 2.66 for males and 2.62 for females of V. louti. Comparison with other
9 Some Aspects of Mohammad I. Wahbeh species of groupers, Φ falls within the range ( ) reported for species of Cephalopholis (Matheson and Huntsman, 1984; Mathews and Samuel, 1987; Chan and Sadvoy, 22), and the range ( ) reported for species of Epinephelus (Romero et al., 1987; Bullock et al., 1992; Manichand-Heilman and Philip, 2). This indicates similar growth patterns. The length-weight relationship showed allometric growth in males (regression coefficient = ) and V. louti (regression coefficient = ), and in females of C. miniata (regression coefficient = ). Males of C. miniata ( b= 3.82 ) and females of E. fasciatus (b = ) and V. louti ( b = ) showed an isometric growth. Allometric growth may be related to the lack of a suitable food supply for larger fish ( Ricker, 1979 ). ACKNOWLEDGMENTS The author wishes to thank Professor M. Al-Zughul for his assistance in data analysis and for his comments on the manuscript. REFERENCES Brule, T., Calas-Marruffo, T., Tuz-sulub, A. and Déniel, C. 2. Evidence for Protogynous Hermaphroditism in the Serranid Fish Epinephelus drammandhayi (Perciformes: Serranidae) from Campeche Bank in the Southern Gulf of Mexico. Bull.Mar. Sci., 66: Bullock, L.H., Murphy, M.D., Godcharles, M. J. and Mitchel, M Age, Growth and Reproduction of Jewfish Epinephelus Itajara in the Eastern Gulf of Mexico. Fish. Bull., 9: Cassie, R.M The Analysis of Polymodal Frequency Distribution by the probability Method. N.Z. Sci. Rev., 8: Chan, T.C. and Sadvoy, Y. 22. Reproductive Biology, Age and Growth of the Chocolate Hind, Cephalopholis boenak (Bloch, 179), in Hong Kong. Mar. Fish. Res., 53: Crabtree, R.E. and Bullock, L.H Age, Growth and Reproduction of Black Grouper, Mycteroperca bonaci, in Florida Waters. Fish. Bull., 94: El-Etreby, S.G., Roberts, C.M., Ghobashy, A.A. and Zyadeh. M.A Coral Reef Groupers (Family: Serranidae) in South Sinai: Reproduction and Hermaphroditism in the Fish Cephalopholis hemistiktos (Rüppel, 183). J. Egyp.Germ.Soc.Zool., 12:1-19. Fennessy, S.T. and Sadvoy, Y. 22. Reproductive Biology of a Diandric Protogynous Hermaphrodite, the Serranid Epinephelus andrsoni. Mar. Freshwater Res., 53: Gulland, I.A Manual of Methods for Fish Stock Assessment. Part I. Fish. Population Analysis. FAO Man. Fish. Sci., (4). Harding, J.P The Use of Probability Paper for the Analysis of Polymodal Frequency Distribution. J. Mar. Biol. Ass. U.K., 28: Johnson, A.G. and Colins, L.A Age-size Structure of Red Grouper (Epinephelus moria), from the Eastern Gulf of Mexico. North.Gulf Sci., 13:1-6. Mackie, M. 2. Reproductive Biology of the Halfmoon Grouper, Epinephelus rivulatus, at Ningaloo Reef, Western Australia. Env. Biol. Fish., 57: Manickchand-Heileman, S. and Philip, D.A.T. 2. Age and Growth of the Yellowedge Grouper, Epinephelus flavolimbatus, and the Yellow-mouth Grouper, Mycteroperca interstitialis, off Trinidad and Tobago. Fish. Bull., 98: Masuda, H., Araga, C. and Yoshino, T Coastal Fishes of Southern Japan. Tokai University Press, Tokyo, 382. Matheson I.II, R.M. and Huntsman, G.R Growth, Mortality, and Yield-per-recruit Models for Speckled Hind and Snowy Grouper from the United States South Atlantic Bight. Trans. Am. Fish. Soc., 113: Mathews, C.P. and Samuel, M Growth, Mortality and Assessment for Groupers from Kuwait. Kuwait Bull. Mar. Sci., 9: Pauly, D. and Munro, J.L Once More on the Comparison of Growth in Fish and Invertebrates. ICLARM Fishbyte, 2:21. Potts, J.C. and Manooch III., C.S Observations on the Age and Growth on Graysby and Coney from the Southeastern United States. Trans. Am. Fish. Soc., 128: Randall, I.E. and Ben-tuvia, A A Review of the Groupers (Pisces: Serranidae: Epinephelinae) of the Red Sea, with Description of a New Species of Cephalopholis. Bull.Mar.Sci., 33: Randall, J.E Red Sea Reef Fishes. IMMEL, London, 192. Ricker, W.E Growth Rates and Models, In: Fish Physiology, VIII, Bioenergetics and Growth. W.S. Hoar, D.J. Randall, and J.R. Brett (eds.). Academic Press, New York. Romero, M.C., Barr, E.E.and Boa, A.G Algumos Aspectos Biologica-pesqueros de la Carbilla, Epinephelus
10 labriformes (Jenyns, 842). Acta Cient.Pot., 9: Sadvoy, Y. and Shapiro, D. Y Criteria for the Diagnosis of Hermaphroditism in Fishes. Copeia, 1987: Sadvoy, Y., and Colin, P.L Sexual Development and Sexuality in the Nassau Grouper. J.Fish Biol., 46: Sadvoy, Y., Rosaria, A. and Román, A Reproduction in an Aggregating Grouper, the Red Hind, Epinephelus guttatus. Env. Biol. Fish., 41: Sadvoy, Y Reproduction of Reef Fishery Species, In: Reef Fisheries. N.V.C. Polunin, and C.M. Roberts (eds.), Chapman and Hall, London. Shapiro, D.Y Reproduction in Groupers, In: Tropical Snappers and Groupers: Biology and Fisheries Management. J.J. Polovina, and S. Ralston (eds.). Westview Press, Colorado. Shpigel, M Aspects of the Biology and Ecology of the Red Sea Groupers of the Genus Cephalopholis (Serranidae, Teleostei). PhD Dissertation, Tel Aviv University. Shpigel, M. and Fishelson, L Habitat Partitioning between Species of the Genus Cephalopholis (Pisces: Serranidae) across the Fringing Reef of the Gulf of Aqaba (Red Sea). Mar. Ecol. Prog. Ser., 58: Shpigel, M. and Fishelson, L Territoriality and Associated Behavior in Three Species of the Genus Cephalopholis (Pisces: Serranidae) in the Gulf of Aqaba, Red Sea. J. Fish Biol., 38: Siau, C.L Population Structure, Reproduction and Sex Change in a Tropical East Atlantic Grouper. J.Fish Biol., 44: Smith, C.L Hermaphroditism in some Serranid Fishes from Bermuda Pap. Mich. Acad.Sci., Arts and Lett., 44: Von Bertalanffy A Quantitative Theory of Organic Growth. II. Inquiries on Growth Laws. Hum. Biol.,: Wyansky, D.M., White, D.B. and Barnas, C.A. 2. Growth, Population Age Structure, and Aspects of the Reproduction Biology of Snowy Grouper, Epinephelus niveatus, off North Carolina and South Carolina. Fish. Bull., 98: بعض ا وجه التكاثر والنمو لهامور المرجان سيفالوفوليس منياتا (فورسكال) وهامور الطرف الا سود ابنيفيلوس فاسياتوس (فورسكال) وهامور الذيل الهلالي فاريولا لوتي (فورسكال) من ساحل خليج العقبة الشمالي الشرقي (البحر الا حمر) الا ردن محمد ابراهيم وهبة* ملخص تم جمع 16 عينة من هامور المرجان سيفالوفوليس منياتا (71 ذكر ا 89 انثى) و 185 عينة من هامور الطرف الا سود ابنيفيلوس فاسياتوس (6 ذكور 79 انثى) و 123 عينة من هامور الذيل الهلالي فاريولا لوتي (56 ذكر ا 67 انثى) من الطرف الشمالي الشرقي لخليج العقبة وذلك خلال الفترة بين كانون الثاني وحتى نهاية كانون الا ول من عام 2. وقد ا ظهرت التغيرات الشهرية لمعامل غدد التناسل موسم تكاثر مميز ا خلال فترة ما بين ا يار وتشرين الثاني في كل من سيفالوفوليس منياتا وفاريولا لوتي وخلال فترة ما بين حزيران وا يلول في ابنيفيلوس فاسياتوس. وكان هناك حيود هام في نسبة الجنس عن (.1>P,32.69= 1:1 χ) 2 في سيفالوفوليس منياتا. كما بين التوزيع الزمني لا نواع الهامور الثلاثة تباينا هاما (.3>P F). 11,55,4.319= وكانت متغيرات منحنى فون برتالانفي للنمو على النحو التالي: K=.73/yr L =6.6cm t o =- K=.132/yr وL =31.2cm C.miniata للا ناث في t o =-1.73 K=.86/yr للذكور وL =56.7cm to= للذكور وL =27.9cm t o 1.2-= K=.173/yr للاناث في ابنيفيلوس فاسياتوس وهذا يقابل L =65.7cm t o 1.37-= K=.2/yr للذكور وL =54.6cm t o 1.45-= K=.1/yr للاناث في فاريولالوتي. وبين معامل انحدار العلاقة بين الطول والوزن نموا متقاسما ا و ما يقرب من ذلك في الانواع الثلاثة. * قسم العلوم الحياتية كلية العلوم الجامعة الا ردنية. تاريخ استلام البحث 24/11/22 وتاريخ قبوله 25/4/
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