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Seasonal reproduction biology of uroteuthis duvauceli (cephalopoda: loliginidae) in northern red sea, Egypt.

INTRODUCTION

Declining catches in many traditional fisheries have led to increased efforts to develop the potential of nontraditional species, especially invertebrates such as the cephalopods (Ozyurt et al. 2006). Fisheries for cephalopods--in particular, squid-have attracted interest worldwide during the past 2 decades (FAO 2005). Squid catches have increased substantially worldwide and this has highlighted the fact that their populations are highly variable. In 2002, about 2.2 million tons of various species were reported to be the world squid catch (FAO 2003). Among the commercial squid species is Uroteuthis duvauceli.

The distribution of the loligonid squids U. durauceli is extended in the Indo-Pacific between Mozambique and the Philippines (Amir et al. 2005). The presence of U. duvauceli was also reported in the Red Sea (Adam 1973). The species is considered to be important among the commercial invertebrates in the Gulf of Thailand (Mohamed 1993); therefore, it was the subject of some research work to investigate its stock assessment. The population dynamics of U. duvauceli in Saurashtra waters were studied by Kasim (1985). Also, an assessment of different squid stocks including U. duvauceli in the Gulf of Thailand was conducted by Silas et al. (1986) and Supongpan (1988). Besides population dynamics, the growth and mortality rates of U. duvauceli were examined (Meiyappan & Srinath 1989). Moreover, the reproductive biology of the species was studied (Rao 1988, Mohamed 1996). More recently, the age and sexual maturation of U. duvauceli were investigated in the Sea of Thailand (Sukramongkol et al. 2007). In northern Red Sea, Emam et al. (2007) investigated the morphology, morphometry, age, and growth of U. duvauceli in the Gulf of Suez. In the same region, Riad and Abd El-Hafez (2008) investigated the bioeconomics of U. duvauceli. Moreover, Riad (2008) documented the morphological and taxonomic studies of the same species. More recently, Gabr (2010) compared the nutritional values and bacteriological content in fresh and frozen U. duvauceli.

The reproductive biology of different cephalopod species have been the subject of many research investigations during the last 30 y (e.g., Durward et al. 1979, Worms 1980, Boyle & Knobloch 1982, Mangold-Wirz 1987, Moriyasu 1988, Arkhipkin 1992, Gabel-Deickert 1995, Gabr et al. 1999, Gabr & Riad 2008, Leporati et al. 2008, Poveda et al. 2009). In addition to the reproductive biology, the biochemical composition of the somatic tissues in the cephalopods has been studied thoroughly in a number of species, such as the cuttlefish Ommastrephes sloani (Takahashi 1960), the Newfoundland squid Illex illecebrouses (Jangaard & Ackman 1965), the small Patagonian octopus Octopus tehuelchus (Pollero & Iribarne 1988), Octopus vulgaris and O. defilippi (Rosa et al. 2002, Rosa et al. 2004), the cuttlefish Sepia officinalis (Ozyurt et al. 2006), and Loligoforbesi (Kilada & Riad 2008). Nevertheless, little is known about the seasonal variation of sexual maturity and biochemical composition of U. duvauceli in its northeasternmost distribution in the Red Sea.

Information on maturation and spawning of this species will contribute to knowledge of its general biology, population dynamics, and management of the stocks. Therefore, the current study was designed to address the lack of information regarding the reproduction biology of U. duvauceli in its northeasternmost distribution in the Red Sea. The work presents the first detailed study of seasonal variation in sexual maturity in reference to the biochemical composition of somatic tissues of the squid. The study also documents the spawning season of the species under investigation in the northern Red Sea and compares different morphometric characteristics of these animals and their contributions in the reproduction process.

MATERIALS AND METHODS

Morphometric Measurements

Seasonal samples of U. duvauceli (n = 590) were caught by trawlers operating in the northern part of the Gulf of Suez in the Red Sea between July 2009 and March 2010. All animals were kept frozen until they were processed. After thawing in room temperature, the dorsal mantle length (ML) and total length (TL) were measured to the nearest 0.1 cm. After recording the total body weight (TW), each specimen was dissected to separate different organs and the following measurements of weight were recorded in grams: mantle weight (MW); head weight, including arms and tentacles (HW); viscera weight, including gills, stomach, cecum, hepatopancreas, and ink sac (VW); ovary weight, including oviduct and oviducal gland (OW); testis weight (TW); and nidamental gland weight (NGW).

The relative growth in body by size (ML) and mantle thickness (MT) in addition to weight (TW, MW, HW, and VW) were described by sex after data of weight measurements were transformed to their natural logarithm as prescribed for allometric studies (Teissier 1948). A t-test was used to determine whether the slope coefficient b (i.e., allometric scaling factor) departed significantly from 1 (= isometry). The allometry is negative when b is less than 1 and is positive when b is greater than 1 (Teissier 1948). Regression was also used to describe the relationship of ML with TW and TL. Slopes of regressions were compared between sexes by analysis of covariance. Prior to analysis, normality and homogeneity of variances were verified by Kolmogorov-Smirnov and Bartlett tests, respectively. Two-way ANOVA was also used to determine whether there is a significant difference in various parameters between sexes and seasons. All statistical analyses were carried out using SYSTAT 2009 for Windows (version 13; SPSS Inc., Chicago, IL). Moreover, the sex ratio (male to female) was estimated in each season.

Length-Frequency Analysis

Pooled length-frequency data were prepared using 0.5-mm CL intervals. These data were divided into cohorts that are assumed to represent separate age classes by applying the method of Bhattacharya (1967) using the fish stock assessment tool FiSAT II (Gayanilo et al. 2005). The method estimates the mean length and SE at each year class.

Reproduction Biology

For each individual, sex was determined by checking the presence of the left arm IV hectocotylized (modified arm) typical for males (Richard 1967). The indices of reproductive status (Joy 1989, Pierce et al. 1994) were calculated for males and females in each season. The indices, the gonadosomatic index (GSI) for both sexes and the nidamental gland-somatic index (NSI) for the females, were calculated as follows:

GSI = 100 X GW/(BW-GW)

and

NSI = 100 x NGW/(BW-NGW)

where GW is the gonad weight, BW is the body weight, and NGW is the nidamental gland weight.

Besides indices, 1 of 3 maturity stages was assigned to the specimen collected in different seasons based on the color of accessory nidamental glands and size of the gonads according to Lipinski (1979). The 3 maturity stages are immature, with small gonads and white accessory nidamental glands; maturing, with orange accessory nidamental glands; and fully mature, with large gonads and pink accessory nidamental glands.

Biochemical Analysis

The length of each individual was measured to the nearest 0.01 mm and approximately 300 g was taken from the mantle of each specimen. Total protein, total lipids, and total carbohydrates were determined as a percentage: (wet weight of biochemical content measured in grams per gram of mantle tissue) in triplicates according to the procedure of the AOAC (1998). Total protein, lipids, and carbohydrates were plotted against the GSI to link the temporal variation of these parameters to the animal's reproduction. Fatty acids in the mantle samples of males and females in each season were determined using the procedure of Cohen et al. (1988). Fatty acid methyl esters were analyzed using gas liquid chromatography on a Hewlett Packard 6890 series fitted with a flame ionization detector and a split-splitless injector. The separation was carried out with helium as the carrier gas in an INNO wax capillary column, programmed from 150-200[degrees]C at 4[degrees]C/min, held for 10 min, and heated to 210[degrees]C for 15 min, then increased by l[degrees]C/min up to 220[degrees]C, and finally increased by 10[degrees]C/min up to 240[degrees]C. Fatty acid methyl esters were identified by comparison of their retention time with those of chromatographic Sigma standards. Peak areas were determined using the Varian software.

Besides fatty acids, the amino acids profile was determined for both sexes in each season using the method modified by Radwan (1975) in the following way. Proteins were hydrolyzed with 6 N hydrochloric acid (containing 0.1% phenol) in an MLS-1200 Mega Microwave System (Milestone), at 800 W, 160[degrees]C for 10 min. The hydrolysis was performed under inert and anaerobic conditions to prevent oxidative degradation of amino acids. The hydrolysates were filtered and dissolved in sodium citrate buffer (pH, 2.2). Amino acids were separated by ion exchange liquid chromatography in an automatic analyzer Biochrom 20 (Amersham Biosciences), equipped with a column filled with a polysulfonated resin (250 x 4.6 mm), using 3 sodium citrate buffers (pH, 3.20, 4.25, and 6.45; Amersham Biosciences) and 3 temperatures (50[degrees]C, 58[degrees]C, and 95[degrees]C). The detection of amino acids was done at 440 nm and 570 nm after reaction with ninhydrin (Amersham Biosciences). Amino acids were identified by comparison of their retention time with those of specific standards (Sigma) and were quantified with the software EZChrom Chromatography Data System (version 6.7; Scientific Software) using norleucine (Sigma) as an internal standard.

RESULTS

Sex Ratio and Morphometric Measurements

The size range and number of animals that were collected in each season are recorded in Table 1. Sex ratio estimation (Table 1) revealed that both sexes are present in almost equal ratios in the summer, fall, and winter seasons, although males outnumbered females and the ratio was 1.6:1 in favor of the males. The growth in various body parts was studied in reference to the ML to determine their nature of allometric growth (Table 2). In female and male animals, all body parts (except MT) scaled positively to ML. Meanwhile, MT scaled negatively in males (b = 0.035, [H.sub.0]: b = 1, t = -2.80, P < 0.01) and females (b = 0.029, [H.sub.0]:b= 1, t= 2.90, P<0.01).

Two-way ANOVA showed that the growth of different body parts varies in the 2 sexes and in different seasons (Table 3). All parameters were found to have significant difference over the 4 seasons (P < 0.01). There was a significant difference in TL as well as in ML in different sexes (P < 0.05). Meanwhile, there was no difference (P > 0.05) in the MT and TW in males and females, although the same parameters were significantly different in different seasons (P < 0.05). ANCOVA showed that although there is no difference in TW (Fig. 1) between the 2 sexes (P = 0.719), there was a significant difference between the 2 sexes in TL (P = 0.016).

Length-Frequency Analysis

The modal analysis conducted by FISAT revealed 2 modes in both male and female samples (Fig. 2). The mean of the first mode was larger in males (13.71 [+ or -] 2.17) than in females (9.61 [+ or -] 1.01). The same was found in the second mode, in which the males had a larger mean (19.53 [+ or -] 1.06) than the females (13.32 [+ or -] 1.46).

Reproduction Biology

The occurrence of mature females and males throughout the period of study was examined. Figure 3 illustrates the seasonal percentage composition of the maturity stages of both sexes. Males matured faster than females, as all males were fully mature during spring, whereas about 90% of the females were fully mature and the rest of the sample was maturing. It is clear that fully mature individuals were observed throughout the year for males and females.

[FIGURE 1 OMITTED]

[FIGURE 2 OMITTED]

To determine the spawning season, different maturity indices (GSI and NSI) were estimated (Fig. 4). All indices illustrated an annual cycle for both sexes. The GSI and NSI in the females had an identical trend as they showed a clear increase during spring, whereas the values of the 2 indices showed a decline between summer and winter seasons, and minimum values for both indices were observed in winter. For males, the GSI was low during summer and then it showed an increase in fall and winter before it declined in the spring.

Seasonal fluctuations in mean weight of individual body organs of somatic tissues (mantle, head, and viscera) and reproductive tissue (GSI) for female and male U. duvauceli are illustrated in Figure 5. These measurements displayed seasonal fluctuations and indicated the relative proportion that each body component contributed to the weight of the entire body. The MW was always the largest component proportionally, followed by the HW.

In females, the HW and MW decreased gradually as GSI increased (Fig. 5). MW decreased almost 50% of its weight between winter and spring, whereas HW decreased from 15 g to less than 10 g during the same period. In contrast, the GSI increased during the same period from 5-8. At the same time, the VW decreased between fall and winter, showing a similar trend to the GSI. Meanwhile, in males, these measurements had a near-similar trend to GSI. The GSI in males reached its peak in winter, whereas body part weights reached their maximum values in fall.

Biochemical Analysis

There were significant differences in total lipids, carbohydrates, and proteins between the 2 sexes (Table 4). Meanwhile, only total proteins were significant different between the 4 seasons (Table 4). Palmitic acid was the main saturated fatty acid (Table 5) that was recorded in the mantle of U. duvauceli in both sexes and in all seasons. Meanwhile, oleic acid was the predominant monounsaturated fatty acid in males and females and in all seasons. The amino acids profile is shown in Table 6. The glutamic acid and aspartic acid were dominant in the nonessential amino acids in both sexes in all seasons, whereas lysine, leucine, and threonine were the dominant among the essential amino acids.

[FIGURE 3 OMITTED]

There was a clear trend in the seasonal variations of proteins in both sexes as they declined to their minimum levels in spring before they increased during summer and fall (Fig. 6). Lipids, on the other hand, were at their highest levels in winter in females and continued to decrease until fall. Meanwhile, the carbohydrates showed a similar trend as GSI in both sexes: an increase from winter through fall in females, which was low in spring in males, then total carbohydrates increased until fall (Fig. 6).

DISCUSSION

Morphometric Measurements

The analysis of morphometric variation in U. duvauceli revealed clear effects of sex and season on the animal. The analysis showed that there is positive allometry in the growth of the weight and various size parameters in relation to ML. This may be related to the growth in the reproductive organs, which increase faster than ML. The results also indicated that the increase in HW and MW was significantly more than the increase in ML. This is also related to the reproduction biology, as it is suggested that the main energy source during spawning comes from somatic tissues rather than from the diet of the animal (discussed later).

[FIGURE 4 OMITTED]

The length-weight relationship showed that there is a significant difference between males and females. The females appeared to be heavier than the males of the same length, as the slopes were 2.32 and 2.19 for females and males, respectively. The same parameter was found to be 1.7-2.0 for males and 2.2-2.5 for females in Thailand (Chotiyaputta 1993, Chotiyaputta 1994). The difference in slope of the length-weight relationship may indicate the presence of sexual dimorphism, which is expressed as mature females having greater body weight compared with males of the same ML. Sexual dimorphism for U. duvauceli was reported in the Gulf of Thailand (Chotiyaputta 1994, Sukramongkol et al. 2007) and in India (Mohamed 1996). The difference in weight between females and males may be related to the fact that the weight of the female gonads and accessory reproductive organs constitute a greater proportion of the body weight in females than in males in larger sizes. This explains why the slopes of the length-weight relationship in males and females are closer to each other in small sizes, then the 2 regression lines diverge in larger animals.

Length-Frequency Analysis

Length-frequency analysis revealed the presence of 2 modes in both males and females, with larger mean ML of each mode in males. It is assumed that each mode is equal to a year in the animal's life, and therefore the presence of 2 modes may indicate that the animal may live up to at least 2 y. The absence of smaller animals in the sample may be the reason for the absence of more modes in smaller sizes, which demonstrates that the animal may live more than 2 y. Age of cephalopods can be determined by counting the annual bands in thin sections of the upper and lower beaks, as in Octopus vulgaris (Hernandez-Lopez & Castro-Hernandez 2001), statoliths in squids (Hendrickson 2004, Arkhipkin 2005, Challier et al. 2005, Lombarte et al. 2006, Miyahara et al. 2006, Hoving et al. 2007, Olyott et al. 2007). Few studies were conducted on the age determination in U. duvauceli (e.g., Emam et al. 2007, Sukramongkol et al. 2007). Emam et al. (2007) used the statoliths to count growth increments after assuming that they are deposited on a daily basis. The same study reported that U. duvauceli may live up to 161 days (<1 y) for a 184-mm-ML male, and described the relationship between age and ML as

ML = [39.5e.sup.00113t]

where ML is the mantle length in millimeters and t is the estimated age in days. By applying the equation to the findings of the current study, the maximum ML in males is 235 mm, and therefore, should be 194 days old. The 235-mm male was found to be [greater than or equal to]2 y old according to the length-frequency analysis, which contradicts the findings of Sukramongkol et al. (2007), who claim that the animal grows 23.5 cm in less than 200 days. On the other hand, Emam et al. (2007) used the modal analysis to estimate the age of a sample of the same species. They found out that U. duvauceli may live up to 18 mo, which is again different than what the current study concluded. Unfortunately, none of these studies have validated the daily deposition of the growth increments, and thus none of the results can be trusted until further investigations are done.

[FIGURE 5 OMITTED]

Sexual Maturity

In female U. duvauceli, spawning occurred between winter and spring, which means that the spawning may take place between November and early April. The spawning activity was associated with the relative decline in total somatic weight with maturation, and this may be attributed to a decline in MW, HW, and VW. However, the decrease in VW during the spawning season was less clear and remained almost constant. Meanwhile, the decline in MW and HW during the spawning season was more noticeable, as they decreased in spring about 50% of their weights in winter. This suggests that the energy requirements for maturation are probably provided from the mantle and head tissues. This was also observed in another cuttlefish, Sepia dollfusi (Gabr et al. 1999). Those authors described the pattern of allocation of resources to the growth of somatic and reproductive tissues, and indicated that spawning is fueled by energy and nutrients derived from reallocation of somatic reserves rather than the diet of the animal.

Sex ratio revealed that the number of males and females varied in the 4 seasons. The ratio was almost 1:1 in fall and summer. However, in winter and spring, the ratio was in favor of the males. The variation in the sex ratio appeared to be related to the reproduction biology of cephalopods. The samples of the current study were collected from deep waters in the Gulf of Suez. Similar to other cephalopod species, mature adults of U. duvauceli would return to shallow waters to spawn (Hatfield et al. 1990), which explains the absence of more female specimens during the spawning season in winter and early spring.

Biochemical Analysis

Marine invertebrates are known to store biochemical energy in the reproductive and/or somatic body parts to be used during the different phases of the life cycle (Giese 1959, Giese 1966, Giese 1969). Biochemical energy is more available by the ability of the animal to allocate environmental energy into biologically accessible units to be used during periods of increased synthetic activity such as reproduction and growth. Meanwhile, lipids, proteins, and carbohydrates show a clear correlation with GSI in females during the spawning season between winter and spring.

In U. duvauceli, total protein level declined at the end of the spawning season in spring in both males and females. It is documented that the contribution of muscular proteins is the main source of energetic reserves in some cuttlefish (Boucher-Rodoni et al. 1987, Castro et al. 1992, Gabr et al. 1999). The same observation was documented in another loligonid cephalopod, Loligo forbesi (Kilada & Riad 2008). The spawning season of L. forbesi in the Gulf of Suez coast is in spring and early summer (Gabr & Riad 2008); the fact that protein content attained the lowest values between spring and summer could be related to the maturation and spawning of the veined squid. The maturation process in many cephalopods results from the increased secretion of a gonadotropin by the optic glands (Wells & Wells 1959, Wells & Wells 1972, Wells & Wells 1975) and is associated with a reduction in somatic growth. The decrease in total protein in spring in females can be explained by the starvation during spawning and the consequent consumption of energy. Females perform significant effort for egg production, spawning, and brooding, and such effort must be energized by proteins, because they are the major organic constituents of the muscle (Rosa et al. 2002). Also, in various cephalopods, there is a negative correlation between protein concentration and GSI (Pierce et al. 1999, Kilada & Riad 2008). Also, O'Dor and Wells (1978) demonstrated that the activation of the optic glands inhibits protein synthesis and increases amino acid levels in the blood, which are fundamental to the formation of yolk protein. Thus, the release of muscle amino acids into the blood from the pool in the muscles induces a decrease of the protein content.

The dominant essential amino acids were lysine, leucine, and threonine. This was similar to what was encountered in the cephalopod Rossia macrosoma (Rosa et al. 2006). Rosa et al. (2006) documented that proteins increased significantly in the gonad throughout sexual maturation, with the highest values obtained during oogenesis. In the same studies, it was found that the major essential amino acids were leucine and lysine. On the other hand, the major nonessential amino acids were glutamic acid, and aspartic acid in U. duvauceli and R. macrosoma. The stomach analysis of U. duvauceli was not investigated thoroughly; however, in some individuals, the main stomach content was fish and molluscs, which indicates that the species is a carnivore and, therefore, most of its dietary carbon comes from these rich protein diets. These invertebrates have a large amino acid requirement for maintaining optimal growth, and a reduced capacity for catabolizing lipids and carbohydrates (O'Dor et al. 1984, O'Dor & Webber 1986). Arginine is the main substrate, intermediate, or end product of amino acid catabolism for energy (Villanueva et al. 2004). During aerobic work, it was shown that proline is depleted from cephalopod muscles (Storey & Storey 1978) and during anaerobic work (e.g., jet propulsion to attain maximum swimming speeds during escape or hunting), phospho-L-arginine is hydrolyzed and the arginine available will be condensed with pyruvate to form octopine, the main anaerobic end product (Finke et al. 1996). Moreover, alanine, glycine, and taurine were also proved to be crucial in energy metabolism through the formation of other opines--namely, alanopine, strombine, and tauropine, respectively (Rosa et al. 2006). This metabolic pathway (pyruvate reductases (i.e., opine dehydrogenases)) will ensure the continuous flux of glycolysis and a constant supply of ATP by maintaining the NADH-to-NAD ratio in the cytosol. Reproduction is one of the most energy-intensive periods of animal life cycles, and requirements for it demand a food intake above that required for maintenance. Tissue constituents of reproducing adults may be mobilized in the short term (and may be replaced later) to meet nutrient and energy needs for egg production.

Lipid content also exhibited significant seasonal variation, attaining high values in spring for males and spring in females, which suggests that the lipid levels could be related to oogenesis and spermatogenesis. At the same time, palmitic acid dominated the saturated fatty acids, whereas oleic acid showed the highest proportion in the unsaturated fatty acids. Palmitic acid also fluctuated in males in the 4 seasons, and its highest value was recorded in fall, then it declined in winter. In females, palmitic acid did not show clear variation in the 4 seasons. Similar results were obtained from cephalopods such as Todarodes pacificus (Takahashi 1960), Photloligo sp. (Moltschaniwskyj & Semmens 2000), R. macrosoma, (Rosa et al. 2006), and L. forbesi (Kilada & Riad 2008). These studies showed that lipid levels fell sharply with spawning and subsequently recovered. According to O'Dor et al. (1984), there is twice as much lipid in the eggs as are present in the digestive glands of octopuses, which suggests that lipid is the limiting nutrient in egg production. As in many marine invertebrates, sexual maturation and reproduction are the most energy-intense periods of the cephalopod life cycle. Somatic production exceeds gamete production during early life, but is later exceeded by gamete production, which eventually dominates tissue growth (Rodhouse 1998). The dominance of palmitic acid and oleic acid was documented in other cephalopods: R. macrosoma (Rosa et al. 2006) and L. forbesi (Kilada & Riad 2008). Rosa et al. (2006) compared the fatty acids concentration in males and females of R. macrosoma in different tissues. A significant increase in the fatty acid content was observed during maturation. Polyunsaturated fatty acids have a specific role in the maintenance of the structural and functional integrity of cell membranes (Sargent et al. 1999), and may be important for the survival of fast-growing phospholipid-rich cephalopod paralarvae (Navarro & Villanueva 2000).

[FIGURE 6 OMITTED]

Carbohydrate content revealed a similar trend in which the concentration had an inverse relationship with GSI. Therefore, as in other invertebrates, glycogen may be important for the maturation process and embryogenesis. Similar observations have been recorded for O. vulgaris (Rodriguez-Gonzalez et al. 2006) and L. forbesi (Kilada & Riad 2008), where the glycogen reserves increased significantly during maturation in the gonad and decreased significantly in the digestive gland and muscle. Carbohydrates are precursors of metabolic intermediates in the production of energy and nonessential amino acids, and as a component in ovarian pigments (Harrison 1990).

ACKNOWLEDGMENTS

The authors would like to thank Dr. I. Nawar for her assistance with the interpretation of the biochemistry results and valuable review of the manuscript.

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RAOUF KILADA (1),* ([dagger]) AND RAFIK RIAD (2)

(1) Department of Marine Science, Suez Canal University, Ismailia, Egypt; (2) National Institute of Oceanography and Fisheries, Alexandria, Egypt

* Corresponding author. E-mail: rkilada@unb.ca

([dagger]) Current address: Biology Department, University of New Brunswick, PO Box 5050, Saint John, NB, E2L 4L5 Canada
TABLE 1.
Number (n), mantle length range (in centimeters), mean mantle
length, and SE of mantle length for U. duvauceli.

                        Males

Season   n     Min.    Max.    Mean    SE

Fall       76   10.50   23.50   15.42   0.34
Winter     55   11.00   22.70   14.73   0.35
Spring    138    7.00   21.50   11.76   0.22
Summer     68    8.20   22.80   14.31   0.41

                        Females

Season   n    Min.    Max.    Mean    SE     Sex Ratio (M:F)

Fall      62    9.20   18.50   12.58   0.18     1.2:1
Winter    37   11.30   17.10   13.26   0.23     1.5:1
Spring    85    7.00   14.30   10.62   0.21     1.6:1
Summer    69   10.50   16.40   12.69   0.16     1:1

TABLE 2.
Intercepts (a) and slopes (b) for regression equations relating
mantle length to different size and weight measurements for U.
duvauceli.

                                         Male

y              x             a                  b         n

Ln TW          Ln ML    -0.813            2.188          337
                       (-0.899-0.726)    (2.111-2.265)

TL             ML       8.852             1.825          336
                       (7.108-10.596)    (1.701-1.950)

MT             ML       -0.020            0.029          337
                       (-0.073-0.033)    (0.025-0.033)

Ln VW          Ln ML    -2.439            1.813          285
                       (-2.862-2.017)    (1.435-2.190)

Ln HW          Ln ML    -1.305            2.093          327
                       (-1.428-1.183)    (1.984-2.201)

Ln MW          Ln ML    -0.974            2.173          328
                       (-1.061-0.887)    (2.095-2.250)

Ln testes Wt   Ln ML   -0.813             2.188          337
                       -0.899-0.726)     (2.111-2.265)

                                         Female

y              x             a                  b         n

Ln TW          Ln ML    -0.840            2.320          253
                       (-0.946-0.733)    (2.221-2.419)

TL             ML       4.664             2.82           253
                       (1.790-7.530)     (2.047-2.518)

MT             ML       -0.047            0.035          253
                       (-0.129-0.034)    (0.028-0.042)

Ln VW          Ln ML    -1.176            0.784          209
                       (-1.758-0.595)    (0.246-1.322)

Ln HW          Ln ML    -1.866            2.682          235
                       (-2.114-1.618)    (2.453-2.911)

Ln MW          Ln ML    -1.103            2.330          235
                       (-1.250-0.956)    (2.195-2.466)

Ln ovary Wt    Ln ML    -1.903            2.192          193
                       (-2.548-1.259)    (1.596-2.787)

                    Male

                       [+ or -]
y                r     Allometry

Ln TW          0.903   Positive

TL             0.712   Positive

MT             0.394   Negative

Ln VW          0.238   Positive

Ln HW          0.815   Positive

Ln MW          0.904   Positive

Ln testes Wt   0.903   Positive

                    Female

                       [+ or -]
y                r     Allometry

Ln TW          0.894   Positive

TL             0.590   Positive

MT             0.294   Negative

Ln VW          0.034   Isometric

Ln HW          0.694   Positive

Ln MW          0.830   Positive

Ln ovary Wt    0.304   Positive

TABLE 3.
Two-way ANOVA for various measurements of different body
parts for U. duvauceli between the 2 sexes and 4 seasons.

Parameter    Source        F Ratio  P Value

TL (cm)      Sex            12.463  0.000#
             Season         34.058  0.000#
             Sex x Season    2.186  0.089
ML (cm)      Sex            70.954  0.000#
             Season         54.423  0.000#
             Sex x Season    3.607  0.013
MT (cm)      Sex             0.008  0.929
             Season        100.872  0.000#
             Sex x Season    2.141  0.094
Ln total     Sex             1.088  0.297
weight (g)   Season        101.042  0.000#
             Sex x Season    4.034  0.007#

Bold type shows the significant difference.

Note: # shows the significant difference.

TABLE 4.
Two-way ANOVA to show the difference in biochemical
compositions of U. duvauceli between sexes
in different seasons.

Parameter       Source        F Ratio  P Value

Carbohydrates   Sex            24.535  0.000#
                Season         0.0001  0.984
                Sex x Season   17.197  0.001
Lipids          Sex           103.011  0.000#
                Season         12.755  0.007#
                Sex x Season  163.902  0.000#
Proteins        Sex           116.046  0.000#
                Season          0.609  0.458
                Sex x Season    4.777  0.034#

Bold type shows the significant difference.

Note: # shows the significant difference.

TABLE 5.
Fatty acids (micrograms per milligram of mantle dry weight) of
male and female U. duvauceli in different seasons.

                                                     Spring

                         Acids           Symbol   Male    Female

Saturated fatty          Trideca         C13:0     3.39   10.05
acids                    Myristic        C14:0     0.81    1.73
                         Palmitic        C16:0    45.4    33.12
                         Stearic         C18:0    14.1    11.96
                         Heptadecanoic   C17:0     0.43    1.89
                         Archidic        C20:0    --      --
                         Behenic         C22:0    18.4     5.78
                         Lignoceric      C24:0     4.93   15.9
[SIGMA]Saturated                                  87.4    80.43
Unsaturated fatty        Palmiboleic     C16:1     -       1.45
acids                    Heptadecenoic   C17:1     4.77    0.39
                         Oleic           C18:1     5.69   13.01
                         Eicosenoic      C20:1     2.1     3.42
[SIGMA]Monounsaturated                            12.6    18.27
                         Linoleic        C18:2    --       1.29
                         Docosadienoic   C22:2    --      --
[SIGMA]Polyunsaturated                            --       1.29
[SIGMA]Saturated Fatty                            12.6    19.56
  Acids
                                                     Summer

                         Acids           Symbol     Male    Female

Saturated fatty          Trideca         C13:0       4.15    6.79
acids                    Myristic        C14:0       0.86    0.07
                         Palmitic        C16:0      37.3    34.08
                         Stearic         C18:0      10.4    10.25
                         Heptadecanoic   C17:0       1.23    1.96
                         Archidic        C20:0      --       0.8
                         Behenic         C22:0       4.07    8.84
                         Lignoceric      C24:0       7.77   13.7
[SIGMA]Saturated                                    65.7    77.49
Unsaturated fatty        Palmiboleic     C16:1       2.17    2.79
acids                    Heptadecenoic   C17:1       0.74    0.46
                         Oleic           C18:1      25.2    15.18
                         Eicosenoic      C20:1       1.7     2.14
[SIGMA]Monounsaturated                              29.8    20.57
                         Linoleic        C18:2       4.44    1.93
                         Docosadienoic   C22:2      --      --
[SIGMA]Polyunsaturated                              --       1.93
[SIGMA]Saturated Fatty                              34.2    22.5
  Acids
                                                        Fall

                         Acids           Symbol     Male    Female

Saturated fatty          Trideca         C13:0      13       4.86
acids                    Myristic        C14:0      --      --
                         Palmitic        C16:0      59.9    30.69
                         Stearic         C18:0       1.79    7.28
                         Heptadecanoic   C17:0       0.27    0.85
                         Archidic        C20:0      --       1.17
                         Behenic         C22:0       0.63   --
                         Lignoceric      C24:0      17.7     5.24
[SIGMA]Saturated                                    93.4    50.09
Unsaturated fatty        Palmiboleic     C16:1       0.48    2.35
acids                    Heptadecenoic   C17:1      --       0.58
                         Oleic           C18:1       4.68   33.57
                         Eicosenoic      C20:1       0.45    1.36
[SIGMA]Monounsaturated                               5.61   37.86
                         Linoleic        C18:2       1.04   12.04
                         Docosadienoic   C22:2      --      --
[SIGMA]Polyunsaturated                               1.04   12.04
[SIGMA]Saturated Fatty                               6.65   49.9
  Acids
                                                        Winter

                         Acids           Symbol     Male    Female

Saturated fatty          Trideca         C13:0       4.6     3.93
acids                    Myristic        C14:0       1.25    0.63
                         Palmitic        C16:0      20.3    28.32
                         Stearic         C18:0       0.94   19.93
                         Heptadecanoic   C17:0       1.61    1.18
                         Archidic        C20:0       1.92    2.1
                         Behenic         C22:0       2.13   --
                         Lignoceric      C24:0       3.35    0.25
[SIGMA]Saturated                                    36.1    56.61
Unsaturated fatty        Palmiboleic     C16:1       1.51    0.58
acids                    Heptadecenoic   C17:1      --       0.1
                         Oleic           C18:1      17.4    31.47
                         Eicosenoic      C20:1       0       2.29
[SIGMA]Monounsaturated                              18.9    34.44
                         Linoleic        C18:2       8.89    6.64
                         Docosadienoic   C22:2      36.1     2.29
[SIGMA]Polyunsaturated                              45       8.93
[SIGMA]Saturated Fatty                              63.9    43.37
  Acids

Bold type shows the significant difference.

Note: # shows the significant difference.

TABLE 6.
Amino acids (grams per 100 g protein) of males and females U.
duvauceli in different seasons.

                                     Male (g/100 g protein)

Amino Acids                     Spring   Summer    Fall    Winter

Nonessential    Aspartic acid   12.01    13.15    11.41     8.96
  amino acids   Serine           5.15     4.47     5.71     5.87
  (NEAA)        Glutamic acid   20.4     17.12    16.95    13.52
                Proline          2.59     4.16     6.35     4.11
                Glycine          5.57     5.14     6.01     5.73
                Alanine          6.3      6.9      6.11     6.21
                Cystine          0.31     0.37     0.82     0.31
                [SIGMA] NEAA    52.33    51.31    53.36    44.71

Essential       Valine           4.32     3.61     3.25     3.13
  amino acids   Threonine        6.22     5.4      6.97     7.41
  (EAA)         Methionine       0.27     0.64     0.71     0.24
                Isoleucine       4.07     3.67     2.96     3.33
                Leucine          6.84     7.06     5.3      6.08
                Tyrosine         2.97     2.46     2.24     2.38
                Phenylalanine    3.27     3.1      2.46     2.74
                Histidine        1.24     1.61     0.67     2.56
                Lysine           7.37     6.89     4.29     7.53
                Ammonia          0.09     0.52     0.42     0
                Arginine         3.44     5.25     5.3      3.94
                [SIGMA] EAA     40.1     40.21    34.57    39.34
Total                           92.41    91.51    87.91    84.05

                                     Female (g/100 g protein)

Amino Acids                     Spring   Summer    Fall    Winter

Nonessential    Aspartic acid   10.79    10.53     9.75    11.41
  amino acids   Serine           4.98     2.77     5.07     5.35
  (NEAA)        Glutamic acid   17.96    21.3     15.6     15.62
                Proline          3.05     4.05     8.38     5.18
                Glycine          5.32     5.3      5.01     5.23
                Alanine          8.12     7.81     6.03     6.13
                Cystine          0.31     0.2      0.75     0.27
                [SIGMA] NEAA    50.53    51.96    50.59    49.19

Essential       Valine           4.6      3.52     2.89     2.32
  amino acids   Threonine        5.91     8.54     6.12     6.3
  (EAA)         Methionine       0.53     0.13     0.2      0.36
                Isoleucine       4.73     3.41     2.44     2.47
                Leucine          8.48     7.78     5.51     5.41
                Tyrosine         3.24     2.75     2.83     2.68
                Phenylalanine    4.38     3.34     2.59     2.51
                Histidine        0.85     1.83     1.63     1.98
                Lysine           7.03     6.41     5.5      5.26
                Ammonia          0.48     0.39     0.19     0.5
                Arginine         4.97     6.15     5.44     5.21
                [SIGMA] EAA     45.2     44.25    35.34    35
Total                           95.72    96.21    85.93    84.2
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Author:Kilada, Raouf; Riad, Rafik
Publication:Journal of Shellfish Research
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Date:Dec 1, 2010
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