1 Introduction

Family Mugilidae is widely spread and representing an important species for cultivation in fish farms. Mugil species, commonly known as mullets, are pelagic-coastal fishes worldwide distributed. Liza carinata commonly inhabit tropical and warm-temperate estuaries (McDowall, 1988; Blaber, 1997; Pombo et al., 2005). Laffaille et al., 1998; Laffaille et al., 2002; Torras et al., 2000; Cardona, 2001; and Almeida, 2003 indicated that mugilidae play a crucial ecological role where this fish community appears to be particulate organic matter transporter and could play a significant role in the global energy budgets of environment. This fish are valuable food sources and ecologically important as primary consumer at coastal and estuarine food chains, and also very representative species for rearing in fish farms (El-Halfawy, 2004; Katsugawa et al., 2006). In spite of the importance of mullets to fishery resources in the Suez Bay, no management policies have been established to protect this valuable resource in the Bay. L. carinata represented about 18% of the total catch of the Suez Bay during the last ten years (2002 - 2012) (GAFRD, 2012).

Some biological aspects of the species of this family were studied in Suez Bay and Bitter Lakes and different regions such as (Hotos et al., 2000; Ilkyaz et al., 2006; Lawson et al., 2010; El-Ganainy et al., 2014).

The aim of this work was to study certain biological parameters of L. carinata in the Suez Bay in order to improve current knowledge of the species for the purpose of rational use of resources and in order to compare these results with those of previous studies.

2 Materials and Methods

Living samples of Liza carinata were randomly taken monthly during November 2012 to October 2013 from Suez Bay. Fish were weighed (± 0.1 g) on an electronic balance, measured (±0.1 cm) and the ventral surface slit open. The gonads were separated, weighed and placed in 10% buffered formalin. The stage of gonad maturity was determined visually following (Abou-seedo and Stephen, 2004). The relationship between the length (L) and weight (W) of fish was expressed by the equation given by (Pauly, 1082). W = aL ^b, where W = Weight of fish in (g), L = Total length (TL) of fish in (cm), a = Constant (intercept), b = slope (change in weight per unit change in length). The “a” and “b” values were obtained from a linear regression of the length and weight of the fish measured. Length in exponent 3 expressed as a percentage was used to calculate the condition factor estimated from the relation below:

K= 100 W / L 3 Where, K = Condition factor, W = Weight of fish (g) and L = Length of fish (cm). Gonadosomatic Index (GSI%), (gonad weight / Gutted body weight X 100) and hepatosomatic Index (HSI%). (Liver weight / Gutted body weight X 100) were calculated for each fish and all values were averaged monthly.

To calculate fecundity, all available ovaries (56) recognized as III to V were placed in jars with formalin 4%. The egg mass of each ovary was weighed (w) and four subsamples were taken containing (n) eggs. The total number of yolked eggs (F) in the ovary (absolute fecundity) was calculated using the formula F= wn / x; where (x) is the weight of the subsample.

Statistical Analysis

The average of data among treatments was analyzed by one way ANOVA followed by Tukey test using SPSS software (Version 13). Results are presented as means ± standard error of the mean (SEM).

3 Results and Discussion

3.1 Length – weight relationship for female and male

The length and weight measurements of 718 specimens of male and female Liza carinata were used in order to correctly model the curvilinear relationship between length and weight. The relationship for female and male was almost strong, but female shows more strong relationship than male. This relationship is usually expressed by the equation:

W = a L^b

The “a” and “b” values were obtained from a linear regression of the length and weight of fish. The correlation (r²) that is the degree of association between the length and weight was computed from the linear regression analysis:

R = r²

1) Females

Female Liza carinata varied in total length from 10.8 to 18.2 cm and in weight from 11.5 to 73.64 gm, the estimated length – weight equation for the investigated female species (Figure 1) is:

W = 0.012L^2.946 (R = 0.874 5)

2) Males

Male Liza carinata varied in total length from 10.5 to 17.3 cm and in weight from 14.54 to 60.42 gm, the estimated length – weight equation for the investigated male species (Figure 2) is:

W = 0.034L^2.569 (R = 0.802 4)

The study of length - weight relationship is of paramount importance in fishery science, as it assists in understanding the general wellbeing and growth patterns in a fish population. It opined that length - weight relationship of fish varies depending upon the condition of life in an aquatic environment. Ideally, the regression coefficient “b” of a fish should be very close to 3.0 (Allen, 1938), however the cube law does not hold well throughout the life period and the weight gain in fish may not be always cube of its length gain (Rousenfell and Everhart, 1953). (Hile, 1936; Martin, 1949) opined that the value of “b” may range between 2.5 and 4.0. (Antony, 1967) recorded the value of “b” within a range of 2.0 to 5.4. Also (a) depends on weight and it can be used as status value (King, 2007).

The length - weight relationship for females and males of L. carinata showing high positive relationship with higher R - value (0.874 5) for females than males (0.802 4), the b value for females (2.946) is not significantly different from 3, but in males b has less value (2.569) which was significantly different from 3. Therefore, females showing isometric growth but males of L. carinata are showing negative allometric growth, indicated that the weight of fish were not too much for their length, this may be responsible for the slimmer shape of the body as it increase body length (Jobling, 2002), this result is similar to what (Grant et al., 1977) reported on the Australian mullet. This differs in b - values of males and females can explain by difference in length distribution of the two sexes. The high b - value of females than males also reported in many other studies (Table 1).

The obtained a, b and R - values in the present study are more or less similar to that mentioned in the previous table; (Le Cren, 1951) pointed out that the variation in “b” value is due to environmental factors, season, food availability, sex, life stage and other physiological factors.

3.2 Length frequency distribution for both sexes

The length frequency of male and female L. carinata was no largely differ from their length classes. The length classes were varied between a smallest one at 10.5 cm to a largest one 18.2 cm TL for both sex. For female the most representative length class was 15 to 15.9 cm TL. The lowest representative class for both sexes was 10 to 10.9 cm TL but for male the most representative length class was 14 to 14.9 cm, while the most representative length classes during the study were 13, 14 and 15 cm TL classes which clearly appeared by chart middle dominance values. There was no male representative in large length classes 18 cm TL; only females occupied this class (Figure 3).

In the present study the minimum and maximum length was recorded for all individuals was (10.5 - 18.2 cm), this is in agreement with (Hakimelahi et al., 2010) which recorded the same minimum and maximum length at (10 - 18.3 cm) respectively, although lengths of 20 cm was reported by (Carpenter et al., 1997), the maximum length was recorded for the same species was 22.5 cm and 23 cm by (Valinasab et al., 2006; Hashemi et al., 2013) in Khouzestan water, respectively. The morphological and reproductive characteristics, population sizes and genetic frequencies of species are adjusted to their environments by natural selection and species inhabiting different environments show different patterns of life history characteristics (Adams, 1980).

Females in the present study showed high aboundance in large sizes more than males, which confirmed with (Lawson et al., 2010) for the same species, (Albieri and Araújo, 2010) for Mugil liza and (Kasimoǧlu et al. 2011) for L. ramada.

3.3 Length at first sexual maturity (L₅₀) for female and male L. carinata

Length was a good indicator of maturity by the presence of a strong relationship between length and maturity farther more information of the mean size of at which individuals reached sexual maturity is valuable for the control of exploitation. The length of male and female L. carinata at first sexual maturity (L₅₀) was determined by the percentage distribution of mature and immature fishes for each length group. The females of 12 cm length are immature. The mature females appeared with percentage abundance 40 % at 13 cm length. The percentage of mature females L. carinata increased to reach L₅₀ at length 14.3 cm. All females at length 17 cm were mature (Figure 4).

The males of less than 12 cm length are immature. At length 12 cm the mature male appeared with a percentage of 45 % and increased gradually to reach percentage 50 % at length of 12.5 cm. At length 16 cm all male became sexually mature (Figure 5). Concluded from these results in the present work that females L. carinata reach sexual maturity at larger size than the males, similar to the result of (Hoda and Qureshi, 1989) on the same species from Pakistan and (Abou-Seedo and Stephen, 2004) from Kuwaiti waters, and with slight decrease from (Hakimelahi et al., 2011) which recorded L₅₀ for female of L. klunzingeri at (15.4 cm), but with slight increase from (Lawson et al. 2010) which recorded L₅₀ for (males – females) at (11.6 - 12.1 cm), respectively. It is implied as it is also evident from the current study that males mature earlier therefore their growth in slower that female’s similar result recorded by (Lembros et al., 2014; El-Ganainy et al., 2014). As a result of the high energy they need in earlier years for their growth and reproduction (Raiaguru, 1992), this result with a complete agreement with that reported by (Abou-Seedo and Stephen, 2004; Javadzadeh, 2004; Hashemi et al., 2013) for the same species and (Albieri and Araújo, 2010) for Mugil liza.

3.4 Condition factor (K)

The data of condition factor (K) available reflected a decrease of K value of female L. carinata from December (1.02) to January (0.99), increased to (1.11) in February and showed another decrease in March (1.10) and April (0.88) at which the lowest value was recorded, but increased afterwards to reach the maximum value in September (1.23). K value for male L. carinata showed the same decrease in value during winter from October (1.17) to reach the minimum value in January (0.97) followed by increase in February (1.06) till May (1.13). June showed a slight decrease of K value (1.12) while August represented the maximum K value (1.21). These results are represented graphically in (Figure 6).

In the present study low K value of female and male of L. carinata during the early spawning period from October to January was due to the fasting of fish as well as the gonadal maturation. Condition factor increase in spring (from March to May) in male and followed by slight decrease in June, which could be explained by a loss of organic matter associated with the laying period, while the female continued decreasing of K value in spring and this could explained due to losing of gonads weight after spawning period to reach the minimum in April. (K) Attained higher values in (September and August) for female and male, respectively.

The fish begin to feed vigorously before spawning period to help in maturation of gonads. The K value obtained for L. carinata in Suez bay ranged between (0.88 - 1.23) for all population, and it was greater than one during most of study time which suggests that the fish was in good condition. The ‘K’ value of L. ramada recorded in Gökova bay by (Kasimoǧlu et al., 2011) was 0.45 to 1.12. (Balik et al., 2011) records mean condition factor at 0.89 in Beymelek Lagoon. The value obtained in this study is within the range obtained by (Mohamed, 1982; Mahmoud, 1997; EL-Boray et al., 2012; Hashemi et al., 2013) for the same species but comparatively smaller than that obtained by (Albieri and Araújo, 2010) which may be due to different ecological conditions. (Javadzadeh, 2004; Hashemi et al., 2013) also recorded high K - value in spring and earlier summer for the same species. K value in the present study not closely associated with the gonado - somatic index and this result may suggest that the reproduction does not influence fish condition. The condition factor of fishes has been reported to be influenced by a number of factors such as the onset of maturity, Spawning (De - Silva and Silva, 1979; Al-Daham and Wahab, 1991), sex and maturity (Gowda et al., 1987; Doddamani and Shanbouge, 2001) and Pollution (Bakhoum, 1999; Devi et al., 2008). During the present study also the monthly fluctuations in condition factor seemed to be influenced by gonadal development, availability of food and gastral activity.

3.5 Maturity stages

Maturity stages, refers to the degree of ripeness of the ovaries and testes of fish. In the present study seven sexual maturity stages of L.carinata was classified according to the macroscopic scale used by (Abou-seedo and Stephen, 2004) with some modification. The maturity scale used in the present study is as follows:

3.5.1 Female maturity stage

Stage I (Immature): The ovaries are narrow, small, thread like, transparent in color and occupy 1/4 of the body cavity. In this stage sex cells are not discernible macroscopically and the two sexes are difficult to differentiate.

Stage II (Immature & recovering): The ovaries become larger in size than the previous stage. In this stage the ovary is light red or pink in color, translucent and occupies about 1/3 of the body cavity. The eggs become slightly visible.

Stage III (Developing): The ovaries undergo a further increase in size and the eggs become more visible by the naked eyes and occupying about 1/2 of the body cavity. The color of ovary changes to be reddish - yellow and presence to many blood capillaries around the organ.

Stage IV (Maturing): In this stage, 2/3 body cavity is occupied by the ovaries. The ovaries are long, broad, swollen, reddish – yellow in color. Eggs are highly visible and numerous and more blood capillaries are observed.

Stage V (Mature): The ovary is longer than the previous stages, completely swollen, long and almost filling the body cavity. Color, is reddish yellow or yellow. Large number of vitellogenic oocytes easily observed beneath a thin, transparent ovary wall, eggs are easily extruded with slight pressure on the belly of fish.

Stage VI (Spawning): The ovary after complete swollen starts to enter spawning phase and become partially spawning - ovary with slightly shrunken and flaccid but not completely hollow. In external appearance partially spawning ovary is similar to ovaries in stages IV or V and is very difficult to differentiate from external feature. The ovaries color turn to red or reddish – yellow with few crumpled.

Stage VII (Spent): Ovaries are flaccid but not fully empty, occupying about 1/2 body cavity deeper in color. Sometimes contain large opaque-yellow residual eggs. In this stage the ovary wall filled with blood capillaries.

Immature ovary of female L. carinata present all the year except in pre-spawning and spawning period, while stage II (Immature & recovering) found with more dominance than the previous stage .Inactive gonads started to appear from Febraury (9%) to August (15%). stage III was considered the most abundant stage for female during the study which recorded almost the year except from February to April with high dominance in October (28%) in pre - spawning period. Mature ovary with visible egg (stage IV) started to appear in September (30%) increasing to November (32%) when spawning activity was recorded and continued until January (14%), ovaries in (stage V) started to appear clearly from October (31%) and continued during most of spawning period. Stage (VI) was recorded in spawning period with high dominance in December (39%) and January (45%), while spent ovary (VII) was observed at the end of the spawning period in February (58%) and continued with low percentage in April (8%), and this result indicated that L. carinata in Suez Bay has a prolonged winter spawning season started from November to March (Figure 7).

3.5.2 Male maturity stage

Stage I (Immature): The testes are narrow ribbon like and transparent in color; occupying 1/4 of the body cavity. In this stage the two sexes difficult to differentiation.

Stage II (Immature& recovering): The testes were slightly thickened and elongated occupy 1/3 of the body cavity with developing white color can be detected.

Stage III (Developing): The testes are white ribbon, like band. They are broader, thicker and softer than those of the previous stages. The testes occupy 2/3 of the body cavity.

Stage IV (Maturing): The testes are white or creamy, elongated and broad occupying 3/4 of the body cavity. No milt exudates by pressure on gonad.

Stage V (Mature): The testes are white or creamy in color, approximately are filling the body cavity. The milt discharges by a gentle pressing on the abdomen.

Stage VI (Spawning): The testes are slightly flaccid and milt comes out by pressing or cutting the gonad and has a creamy color like the previous stage.

Stage VII (Spent): The testes are grayish in color, thin and flaccid occupying about 1/2 of the body cavity. The sperms keep inside the gonads without moving out however on pressing or cutting.

3.5.3 Monthly distribution of male maturity stages

Immature & recovery testis of male L. carinata present all the year except in January, while stage III & IV (Developing & Maturing ) found with more dominance from August to October .Mature and spawning stages occupied the spawning months than the previous stage, while spent testes started to appeared in the December (18%) and given a sudden increase in February (50%) (Figure 8).

In the present study, immature and recovering were found throughout the whole year. Similar results were reported by (McDonough et al., 2003; Assem et al., 2008) on Mugil cephalus. The maturity stages observed in the present study have been recorded in many other species of mullet in the following table the number of maturity stages will be mentioned for some species (Table 2).

The same morphological features were recorded by (Abou-Seedo and Stephen, 2004; Hakimelahi et al. 2011) for the same species.

3.6 Sex ratio

The fluctuation in the sex ratio for L. carinata in Suez bay expressed as a percentage of the individual sexes among the samples was examined from November (2012) to October (2013). The data represented in (Figure 9). In fish sex ratio varies considerably from species to species but in the majority of species it is close to 1:1 (as the hypothetical value) in which the prediction birth number of females and males are the same (Vazzoler, 1996). It differs from population to another of the same species and may vary from year to year in the same population (Nikolsky, 1963; EL-Halfawy et al., 2007).

The results showed that, females were dominant from September (61.8%) to December (51.1%), and males were dominant from February (53.5%) to June (56.1%), while there are no significant difference between number of males and females (p<0.5) in January and July, overall throughout the whole period of investigation the percentage of females to males were almost similar 1:1.

In the present study the sex ratio not constant throughout the different months, particularly after the breeding season. In the period after the spawning season, the males of L. carinata were dominant than females that is similar to (El-Mor, 1993), while females exceeded males before and during the breeding period, this may be due to migration of males for spawning elsewhere before females, this is in agreement with (Mahmoud, 1997) whose recorded the ratio for the same species. (Oliveira et al., 2011) recorded the same ratio (1M: 1.04F) for Mugil curema, and (Wijeyaratne, 1990) for Liza macrolepis, with slight differ from (1M:1.13F) which recorded by (Lawson, 2010) for the same species and (1M:1.14F) and (1F:1.26M) which evaluated by (Ergene, 2000; Kasimoǧlu, 2011), respectively for another species.

In contrast many authors recorded high differ of sex ratio from the hypotheses value (1:1) with a favor of females than males (Ilkyaz, 2006; Balik et al., 2011; Hakimelahi et al., 2011; Hashemi et al., 2013) detected sex ratio male : femal at (1:1.87; 1:2.7; 1:2.87; 1:1.77), respectively. This variety in sex ratio could be due to the differential fishing factors related to seasons and schooling in feeding and spawning grounds (Sarojini, 1958; Silva and De Silva, 1981; Silva and De Silva, 1982; Hoda and Qureshi, 1989; Abou - Seedo and Stephen, 2004).

3.7 Gonado - somatic index (GSI)

In the present study the gonado - somatic index (GSI) was monthly investigated during the period from November (2012) to October (2013).

3.7.1 Females GSI

The monthly variations of the GSI values are shown in (Figure 10). The average GSI for females were very small (0.921 ± 0.091) at the beginning of the developing and maturing stage that represented the pre-spawning period. It increased gradually at the mature and spawning period to reach very high value (8.883 ± 0.867) in December (spawning period). Then GSI decreased again to reach the minimum value (0.397 ± 0.047) in May at the end of spent stage.

3.7.2 Male GSI

The monthly fluctuations of GSI values are shown in (Figure 10). The average GSI for males were very small (0.075 ± 0.012) after the rearing period (immature and recovery stage). It was elevated to record (1.808 ± 0.172) in October. The spawning period demonstrated the highest peak for GSI in December (5.788 ± 0.517). From this peak GSI started to decrease in value until reached the minimum value (0.039 ± 0.002) in February at the end of rearing period.

In the present study GSI varied for female and male from (0.921 to 8.883) and from (0.039 to 5.788) respectively, showing relatively high GSI for females L. carinata (8.8) than males (5.7), GSI increase progressively with increase in the percentage of ripe individuals towards the spawning season (Mohamed, 2010). GSI showed the highest value with one peak in December for both sexes, this was the same with (Mahmoud, 1997; Abou – Seedo and Stephen, 2004; Hakimelahi et al. 2011; Hashemi et al,. 2013) for the same species, and with (Rheman et al. 2002) for L. parsia, while the smallest GSI value of L. carinata was recorded in February and May for males and females, respectively. On the contrary of (Albieri et al., 2010) recorded the peak of GSI in June for M.liza in Tropical bay. (EL – Halfawy et al., 2007) was recorded the highest value of males L. ramada closely related to the present study (5.03), and with a large increase for females (12.4) form L. carinata,while (Hsu et al., 2007) recorded a great increase of GSI value of M. cephalus for both male and female at (19-21) respectively, in Northeast of Taiwan.

The GSI can be used for determination of spawning period, which was recorded from November to March for females and males, showing prolonged spawning period which based on the presence of large number of males and females in stage V to VII (mature to spent) coupled with very high value of GSI recorded in this period. The following table (Table 3) mention the spawning periods for some species of mullet in different regions.

There are a slight variation in spawning time because of different environmental parameters, such as temperature, light, and salinity which cause changes in physiological activities and sunsequental spawning time (King, 2007).

3.8 Hepato - somatic index (HSI)

HSI fluctuated during the study period, males and females were parallel to each other, showing liver activity increased in the months of May to the highest peak in September (4.414 ± 0.389 and 5.034 ± 0.338) for (males and females) respectively (Figure 11), HSI decreased during the spawning period to reach the low level during this period at the peaked GSI month in December (1.781 ± 0.167 and 1.977 ± 0.093) for (males and females) respectively, due to consuming the fish the stored energy in the liver because of stopping feeding in this period due to reproduction.

In the present study the recorded values of HSI decreased during the spawning period and this is in agreement with which recorded by (Abou - Seedo and Stephen, 2004; Hakimelahi et al., 2011) for the same species. In contrast (Albieri and Araújo, 2010) reported the highest value of HSI in the reproductive period for M. liza in tropical Brazilian bay, and illustrated that due to accumulate large lipid deposit, primary triacylglycerols, which are subsequently mobilized to support gonad development causing increase of liver mass during the reproductive period, and decreased at the end of this period.

3.9 Fecundity

The size and weight of ripe females examined for fecundity estimation ranged from 14 cm to 18.3 cm TL and total weight ranged from 31.55 g to 75.22 g respectively. The number of eggs for all the broods examined ranged from 24 500 to 115 258 oocytes. The overall mean fecundity obtained by direct summation procedure for the fish population was 63.896 oocytes per fish.

The relationship of fecundity with fish total length and body weight were found to be linear and increasing with increasing fish length and body weight (Figure 12). Fecundity correlated more with the body length than body weight. Fecundity increases with body length, a relationship described by the equation.

F = 0.5908TL^4.1444        R = 0.9034

Where, F = fecundity, TL = total length of individual fish (cm).

The relationship of fecundity with body weight was expressed by the equation;

F = 313.8 W^1.354          R = 0.8286

Where F = fecundity, W = total body weight (Figure 13), the correlation too was significant.

The mean absolute fecundity of L. carinata in Suez bay was 63.896 oocytes per fish which was slightly higher than that recorded by (Mahmoud, 1997) which was 58 400 oocytes, and much lower than that recorded by (Abou - Seedo and Stephen, 2004) which was 127 350 oocytes for the same species , this may be related to environmental factors as indicated by (Wroblewski et al. 1999).The data showed that the fecundity varies considerably between individuals irrespective of their length and weight, so there were a difference in absolute fecundity for the same length group, This variation in fecundity may be due to different adaptations to environmental habitats (Witthames et al., 1995; Assem et al., 2015). Fecundity (F) in all the relations, the coefficient of correlation (r) was significant at 0.01. The absolute fecundity of L. carinata in Suez bay as other fishes increases with increase of length and weight (Table 4), but with different correlated values, the lowest (r) were with weight (0.82) while the highest were with length (0.89) which represented strong relationship between F and length more than F with weight (Figure 13) similar result was obtained by (Assem, 2008; El- Ganainy et al., 2014). On the contrary the F with weight in L. abu shows more relationship than F with length (Şahinӧz, 2011). In general the absolute fecundity has a linear relationship with length and weight and increases proportionally with them the same conclusion reached by (EL - Boray, 1993; Rheman, 2002; Albieri and Araújo, 2010; El - Ganainy et al., 2014).

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