Size at the Onset of Sexual Maturity in 7 Bivalve Species in Egyptian Waters

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Thalassia Salentina provided by ESE - Salento University Publishing Thalassia Sal. 39 (2017), 123-136 ISSN 0563-3745, e-ISSN 1591-0725 DOI 10.1285/i15910725v39p123 http: siba-ese.unisalento.it - © 2017 Università del Salento

KANDEEL EL-SAYED KANDEEL

Department of Zoology, Faculty of Science, Fayoum University, 63514 Fayoum, Egypt e-mail: [email protected]

SIZE AT THE ONSET OF SEXUAL MATURITY IN 7 BIVALVE SPECIES IN EGYPTIAN WATERS

SUMMARY

Egyptian beaches have extended over long distances and it has become necessary to look at how the exploitation of bivalves inhabiting these beaches. Onset of sexual maturity for 7 bivalve species in 4 sites of Egyptian waters was reported. Specimens were collected during summer and winter seasons. A total of 1870 individuals belonging to 4 families were examined under the microscope. The trend of decreasing size at maturity with increasing water temperature was reported. The trend of increasing size at maturity with decreasing latitude was much less clear in this study. The size at 50% maturity

(SM50) varied between 9.2 mm SL (for Cerastoderma glaucum in summer) and 16.6 mm SL (for Venerupis aurea in winter), and showed an average value of 12.7 mm SL (± 2.4 S.D.) for 5 commercial clams.

INTRODUCTION

The shell length at which the gonad begins to develop from rudimentary vir- gin state (undifferentiated or juvenile gonad) to the state at which the gonad is sexually differentiated is, usually, taken to be the size at onset of sexual maturity. The size at onset of maturity is important as it provides a minimum size limit for the control of exploitative fishing of young individuals (Agostinho, 2000). It also indicates population changes caused by pollution, overfishing or others (Weng, 1994). Not all members of a species mature at the same size (length) and many species reach sexual maturity at a particular age which corresponds to a broad range of individual lengths. Therefore, the estimation of the size at onset of maturity is important as it gives a particular size which represents the maturity size of the species. Weng (1994) and Roa et al. (1999) reported that the size at onset of maturity is commonly accepted as the “average size at which 50% of a population is mature”.

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The onset of sexual maturity varies in the different species and in the same species under different ecological conditions (Yankson, 1986; Darrigran et al., 1999). Water temperature is thought to be the major factor in the regional and seasonal differences in the size at maturity. Family Veneridae represents the most abundant and successful group of bivalves in Lake Timsah (Fouda and Abou-Zied, 1990; Ghobashy et al., 1992; Mohammed et al., 1992). The most common Veneridae in the Lake are Venerupis aurea (Gmelin, 1791) and Tapes (= Ruditapes) decussata (Lin- naeus, 1758). The two species are indigenous to the Mediterranean Sea and successfully colonized Lake Timsah by penetrating the Suez Canal (Fouda and Abou-Zied, 1990). V. aurea was first recorded from Lake Qarun by El- Shabrawy (2001). Both V. aurea and T. decussata are of great economic im- portance; being consumed in large quantities in the Suez Canal region and exported to some European countries (Kandeel, 2006). Donacidae inhabit exposed intertidal sandy beaches and form the larg- est group living in such highly dynamic environments (Brown and McLa- chlan, 1990). Donax variabilis (Say, 1822) and D. trunculus (Linnaeus, 1758) spreading in the Mediterranean coast of Egypt are the favorite food among the populations of the coastal cities (El-Ghobashy et al., 2011). The lagoon cockle Cerastoderma glaucum (Poiret, 1789) (Family: Cardii- dae) represents one of the historically most dominant species of the macrobenthos of Lake Qarun, Fayoum Depression (Fishar, 2000; El-Shabrawy, 2001) and Lake Timsah, Suez Canal (Mohammed et al.,1992; 2006). C. glaucum plays an important direct and indirect role in nutrient cycles. It is eaten by human and considered as a very cheap resource due to their occurrence in high densities. The indirect role is by sharing in food chain as some marine animals prey upon them (Kandeel et al., 2017). Mussels living in salt or brackish water are classified in the family My- tilidae which includes many genera such as Modiolus, Brachidontes and Mytilus (Seed and Suchanek, 1992). Two Indo-Pacific mytilids; M. arcuatulus (Hanley, 1843), and B. variabilis (Krauss, 1848) were found in high densities and create most of the fouling problems in the Suez Canal (Ghobashey et al., 1992; Mohammed et al., 1992). The study of the size at onset of maturity may provide information for future researches in biofouling of these mussels. This study reports the onset of sexual maturity for 7 bivalve species in the Mediterranean coast (Damietta shore), Lake Timsah, The Great Bitter Lake and Lake Qarun. The possible role of water temperature was discussed, also.

MATERIALS AND METHODS

Damietta shore (Mediterranean coast) and three lakes: Lake Timsah, Great Bitter Lake, Lake Qarun (supporting information online at https://www.in-

124 Thalassia Salentina n. 39-2017

gimage.com) were sampled to collect 7 species of bivalves belonging to 4 families (Table 1). Venerupis aurea and Tapes decussata were collected using quadrate measuring 25 x 25 cm. Quadrates were dug to a depth of 10 cm and sieved in the field through 1-mm screen. Donax variabilis and D. trunculus were sampled using a specially designed hand dredge (75 cm wide) similar to that used by local fishermen but incorporating a smaller mesh size bag (3 mm) to collect enough samples of juveniles. Cerastoderma glaucum was collected using 20 x 20 cm stainless steel grab sampler randomly placed in the substratum at about 2 m depth. Brachidontes variabilis sampling was carried out by quadrates; each measuring 10 x 10 cm. Mussels inhabiting the area of the quadrates were scraped from the rock surface using a sharp knife. For Modiolus arcutulus, core samples of sediment were taken from the surface of the mussel bed using 14 cm diameter circular plastic pipe. Samples were washed out carefully in situe through one mm size sieve. Collection of samples was carried out in summer (July/August) 2015 and winter (January/Feb- ruary) 2016. Collected samples were kept in labeled containers filled with 6% formaldehyde-seawater solution and then transported to the laboratory. In the laboratory, shell lengths (SL); (maximum distance on the anterior- posterior axis) of the entire specimens were measured to the nearest 0.1 mm by using a Vernier caliper. Smears of the sexual products (growing or mature oocytes in females and morphologically ripe spermatozoa in males) were examined under the microscope. Each specimen was categorized as imma- ture (juvenile) or mature (adult). For each species, the percentage of sexually mature individuals was plotted against shell length. The length at which 50% of the populations are sexually mature (SM50) was then estimated by fitting a logistic curve to the percentage mature by size using the methods discussed in Somerton (1980) and Torroglosa and Giménez (2016). The length at maturity was estimated for the samples collected during the two seasons.

RESULTS

Sample descriptive statistics and parameters of logistic curves of 7 bivalve species belonging to 4 families and collected from Egyptian waters are reported in Table 1.

Venerupis aurea The minimum size at maturity for V. aurea collected from Lake Timsah was 12 and 15 mm shell length during summer and winter seasons, respectively

(Fig. 1). Estimated sexual maturity (SM50) was 11.0 and 16.4 mm SL, respectively. For samples collected from Lake Qarun during summer and winter, the

125 Thalassia Salentina n. 39-2017

smallest mature clam was 12 and 15 mm SL and SM50 were 12.1 and 16.6 mm SL, respectively (Fig. 2).

110

100

% of maturity % of 30 Summer N = 112 20 Winter 10 N = 102 0

-10 10 11 12 13 14 15 16 17 18 19 20 Shell length (mm) Fig. 1. The percentage of maturity plotted against shell length (mm) of V. aurea collected from Lake Timsah during summer and winter seasons. The size at 50% maturity (11.0 and 16.4, respectively) is demonstrated. N = number of individuals examined.

Fig. 2. The percentage of maturity plotted against shell length (mm) of V. aurea collected from Lake Timsah during summer and winter seasons. The size at 50% maturity (11.0 and 16.4, respectively)110 is demonstrated. N = number of individuals examined.

100

% of maturity % of 30 Summer 20 N = 91 10 Winter 0 N = 79

-10 10 12 14 16 18 20

Shell length (mm)

Fig. 2. The percentage of maturity plotted against shell length (mm) of V. aurea collected fromFig .Lake 3. The percentageQarun duringof maturity summer plotted against and shell winter length (mm) seasons. of V. aurea The collected size fromat 50% maturity (12.1 and 16.6,Lake respectively) Qarun during summer is demonstrated. and winter seasons. The N size= number at 50% maturity of individuals (12.1 and 16.6, examined. respectively) is demonstrated. N = number of individuals examined.

126 Thalassia Salentina n. 39-2017

Tapes decussata The smallest mature specimens of T. decussata collected from Lake Timsah during summer and winter were 10 and 13 mm SL, respectively. The maximum size of immaturity was 13 and 17 mm SL and the SM50 was 11.1 and 15.2 mm SL for the two seasons, respectively (Fig. 3).

110

100

40 Summer N = 50 % of maturity % of 30

20 Winter 10 N = 44

-10 8 10 12 14 16 18

Shell length (mm)

Fig. 3. The percentage of maturity plotted against shell length (mm) of T. decussata collected from Fig. 4.Lake The percentage Timsah of duringmaturity plotted summer against shelland length winter (mm) seasons.of T. decussata The collected size at 50% ma- from Lake Timsah during summer and winter seasons. The size at 50% maturity is demonstrated turity is demonstrated(11.1 and 15.2, (11.1 respectively) and 15.2,is demonstrated respectively). N = number isof individualsdemonstrated. examined. N = number of individuals examined.

Donax variabilis D. variabilis collected from Damietta shore reached sexual maturity at a smaller size during summer than that reported for samples collected during winter (Fig. 4). The minimum size of maturity was 11 and 13 mm SL and SM50 were 12.2 and 14.7 mm SL for the two seasons, respectively.

Donax trunculus The smallest mature D. trunculus collected from Damietta shore during summer and winter were 11 and 13 mm SL, respectively. The maximum size of juveniles was 13 and 15 mm SL and the SM50 were 12.4 and 14.8 mm SL for the two seasons, respectively (Fig. 5).

Cerastoderma glaucum The minimum size at maturity for C. glaucum collected from Lake Timsah was 8 and 10 mm SL during summer and winter seasons, respectively (Fig. 6).

127 Thalassia Salentina n. 39-2017

110

100

40 Summer N = 112 % of maturiy % of 30 Winter 20 N = 68 10

-10 10 12 14 16 18 Shell length (mm) Fig. 4. The percentage of maturity plotted against shell length (mm) of D. variabilis collected from Damietta shore during summer and winter seasons. The size at 50% maturity (12.2Fig. 5. Theand percentage 14.7, ofrespectively) maturity plotted against is demonstrated. shell length (mm) of N D. variabilis= number collected of individuals examined. from Damietta shore during summer and winter seasons. The size at 50% maturity (12.2 and 14.7, respectively) is demonstrated. N = number of individuals examined.

110

100

50 % of maturity % of 40 Summer N = 119 30

20 Winter N = 56 10

-10 9 10 11 12 13 14 15 16 17 18

Shell length (mm)

Fig. 5. The percentage of maturity plotted against shell length (mm) of D. trunculus collected from Damietta shore during summer and winter seasons. The size at 50% maturity (12.4Fig. 6. Theand percentage 14.8, of respectively) maturity plotted against is demonstrated. shell length (mm) of D.N trunculus= number collected of individuals examined. from Damietta shore during summer and winter seasons. The size at 50% maturity (12.4 and 14.8, respectively) is demonstrated. N = number of individuals examined.

128 Thalassia Salentina n. 39-2017

Estimated SM50 was 9.2 and 11.1 mm SL, respectively. For samples collected from Lake Qarun during summer and winter, the smallest mature clams were

9 and 7 mm SL and SM50 was 9.8 and 11.1 mm SL mm, respectively (Fig. 7).

110

100

50 % of maturity % of 40

30 Summer 20 N = 86 10 Winter 0 N = 83 -10 6 8 10 12 14 16 Shell length (mm)

Fig. 6. The percentage of maturity plotted against shell length (mm) of C. glaucum collected from Lake Timsah during summer and winter seasons. The size at 50% maturity (9.2 and 11.3,Fig. 7. The respectively) percentage of maturity is demonstrated. plotted against shell N length = number (mm) of C.of glucum individuals collected from examined. Lake Timsah during summer and winter seasons. The size at 50% maturity (9.2 and 11.3, respectively) is demonstrated. N = number of individuals examined

Brachidontes variabilis The smallest mature specimens of B. variabilis collected from Great Bitter Lake during summer and winter was 7 mm SL (Table 1). The maximum size of immaturity was 10 and 11 mm SL and the SM50 was 8.3 and 9.2 mm SL for the two seasons, respectively (Fig. 8).

Modiolus arcutulus The minimum size at maturity for M. arcutulus collected from Great Bitter Lake was 4 and 6 mm SL during summer and winter seasons, respectively.

Estimated SM50 was 4.6 and 6.2 mm SL, respectively (Fig. 9). For samples collected from Lake Timsah during summer and winter, the smallest mature mussel was 4 mm SL. The SM50 was 4.6 and 4.4 mm SL and the maximum size of a juvenile were 5 and 6 mm SL for the two seasons, respectively (Fig. 10).

129 Thalassia Salentina n. 39-2017

110

100

40 % maturity of 30 Summer N = 158 20 Winter 10 N = 154 0

-10 6 8 10 12 14 Shell length (mm) Fig. 7. The percentage of maturity plotted against shell length (mm) of C. glaucum collected from Lake Qarun during summer and winter seasons. The size at 50% maturity (9.8 and 11.1, respectively) is demonstrated. N = number of individuals examined.

Fig. 8. The percentage of maturity plotted against shell length (mm) of C. glucum collected from Lake Qarun during summer and winter seasons. The size at 50% maturity (9.8 and 11.1, respectively) is demonstrated. N = number of individuals examined.

110

100

% of maturity % of 40

30 Summer N = 120 20 Winter 10 N = 100 0

-10 5 6 7 8 9 10 11 12 13 14 Shell length (mm) Fig. 8. The percentage of maturity plotted against shell length (mm) of B. variabilis collected from The Great Bitter Lake during summer and winter seasons. The size at 50% maturity (8.3 and 9.2, respectively) is demonstrated. N = number of individuals examined.Fig. 9. The percentage of maturity plotted against shell length (mm) of B. variabilis collected from The Great Bitter Lake during summer and winter seasons. The size at 50% maturity (8.3 and 9.2, respectively) is demonstrated. N = number of individuals examined.

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Family Species Locality Latitude Longitude T oC L limt N L min. SM50 L max. Veneridae Venerupis aurea Lake Timsah, Suez Canal 30o 33՝ - 30o35.0՝ N 32o16՝ - 32o19՝ E Summer 29.7 11-12 112 12 11.0 11 Family Species Locality Latitude WinterLongitude 16.3T oC 14L- 19limt 102N 15L min . 16.SM450 18L max . o o o o Veneridae Venerupis aurea Lake TimsahQarun, ,Fayoum Suez Canal Depretion 3029o 2533՝՝ -- 2930o 35.034.0՝՝ N 3230o1634՝ - 3230o19 49՝՝ E E Summer 29.728.6 11-1213 11291 12 11.012.1 1112 Winter 16.315.7 14-19 10279 15 16.16.64 18 Tapes decussata Lake Qarun,Timsah, Fayoum Suez Canal Depretion 2930o 2533՝՝ -- 2930oo 34.035.0՝՝ N 3032o34 16՝՝ -- 3032oo 1949՝՝ EE Summer 28.629.7 11 9--1413 9150 1210 12.11.11 1213 Winter 15.716.3 1412-1918 7944 1513 16.615.2 1817 o o o o Donacidae TapesDonax decussata variabilis LakeDamie Timsah,tta shore, Suez Mediterranean Canal 3031o 3326.8՝ -՝ 30- 3135.0o 28.6՝ N՝ N 3231o36.516՝ -՝ 32- 3119o44.4՝ E ՝ E coast Summer 29.731.0 109--1415 50112 1011 11.112.2 1143 Winter 16.316.5 12-18 4468 13 15.14.72 17 o o o o Donacidae Donax trunculusvariabilis Damie tta shore, Mediterranean 31o 26.8՝ - 31o 28.6՝ N 31o36.5՝ - 31o44.4՝ E coastDamie tta shore, Mediterranean Summer 31.0 10-1514 112119 11 12.12.42 1413 coast Winter 16.5 12-1816 6856 13 14.714.8 1715 o o o o Cardiidae DonaxCerastoderma trunculus Lake Timsah, Suez Canal 3130o 26.833՝ -՝ 30- 31o 35.0 28.6՝ N՝ N 3132o36.516՝ -՝ 32- 31o1944.4՝ E ՝ E glaucum Damie tta shore, Mediterranean Summer 31.029.7 107-13-14 11986 118 12.49.2 1312 coast Winter 16.516.3 129-15-16 5683 1310 14.811.3 1514 o o o o Cardiidae Cerastoderma Lake Timsah,Qarun, Fayoum Suez Canal Depretion 3029o 3325՝ - 3029o 35.034.0՝՝ N 3230o1634՝ - 3230o19 49՝՝ E E glaucum Summer 29.728.6 78-13 86158 89 9.29.8 12 Winter 16.315.4 96-1511 83154 107 11.311.1 1410 o o o o Mytilidae Brachidontes variabilis LakeGreat Qarun, Bitter Lake, Fayoum Suez Depretion Canal 2930o 2025՝՝ -- 3029o33 34.0՝ N ՝ N 3032o3423՝ - 3032o 4938՝ E Summer 28.629.3 86-1310 158120 97 9.88.3 1210 Winter 15.416.3 6-1112 154100 7 11.19.2 1011 o o o o Mytilidae BrachidontesModiolus arcutulus variabilis Great Bitter Lake, Suez Canal 30o20՝ - 30o33՝ N 32o23՝ - 32o 38՝ E Summer 29.3 63-160 12074 74 8.34.6 105 Winter 16.3 65-128 100102 76 9.6.22 117 o o o o Modiolus arcutulus GreatLake Timsah, Bitter Lake, Suez Suez Canal Canal 30o20 33՝՝ - - 30 30o3335.0՝ N՝ N 32o2316՝ - 32o 1938՝՝ EE Summer 29.329.7 3-6 74 4 4.6 5 Winter 16.3 53-87 102104 64 6.24.4 76 Lake Timsah, Suez Canal 30o 33՝ - 30o35.0՝ N 32o16՝ - 32o 19՝ E Summer 29.7 3-6 74 4 4.6 5 Table 1. Sample descriptive statistics and parameters of the onset of sexual maturity of 7 bivalve species collectedWinter from Damietta shore (Mediterranean16.3 3-7 coast) and104 3 Lakes 4 of Egyptian4.4 6 o waters. T C, mean water temperature; L limt., size limit at onset of maturity; N, number of individuals examined; L min., minimum size at maturity; SM50, the size of 50% maturity; L max., maximum size of immaturity. TableTab. 1. Sample 1. Sampledescriptive statistics descriptive and parameters of the statisticsonset of sexual maturity and of 7 parametersbivalve species collected fromof Damtheietta onset shore (Mediterranean of sexual coast) and maturity3 Lakes of Egyptian of o 7 bivalvewaters. T speciesC, mean water temperature; collected L limt., size fromlimit at onset Damietta of maturity; N, number shore of individuals (Mediterranean examined; L min., minimum sizecoast) at maturity; and SM50, the 3 size Lakes of 50% maturity; L max., maximum size of immaturity.

of Egyptian waters. T oC, mean water temperature; L limt., size limit at onset of maturity; N, number of individuals examined; L min., minimum size at maturity; SM 50, the size

of 50% maturity; L max., maximum size of immaturity.

110

100

% 0f maturity % maturity 0f 40 Summer 30 N = 74 20 Winter 10 N = 102 0

-10 2 3 4 5 6 7 8 9 10 11

Shell length (mm) Fig. 9. The percentage of maturity plotted against shell length (mm) of M. arcutulus collected from The Great Bitter Lake during summer and winter seasons. The size at 50% maturityFig. 10. (4.6The percentage and 6.2, of maturityrespectively) plotted against is demonstrated. shell length (mm) of M.N arcutulus= number collected of individuals examined. from The Great Bitter Lake during summer and winter seasons. The size at 50% maturity (4.6 and 6.2, respectively) is demonstrated. N = number of individuals examined.

131 Thalassia Salentina n. 39-2017

110

100

% maturity of 40

30 Summer N =74 20

10 Winter N = 104 0

-10 3 4 5 6 7 8

Shell length (mm) Fig. 10. The percentage of maturity plotted against shell length (mm) of M. arcutulus collected Fig.Lake 11. TheTimsah percentage during of maturity summer plotted againstand wintershell length seasons. (mm) of M. The arcutulus size collected at 50% maturity (4.6 and 4.4, respectively)from The Great Bitter is Lakedemonstrated. during summer andN winter= number seasons. ofThe individuals size at 50% maturity examined. (4.6 and 4.4, respectively) is demonstrated. N = number of individuals examined.

DISCUSSION

Temperature is considered the main environmental factor which regulates bivalve reproduction (Sastry, 1979). In venerid clams like Venerupis japonica (Holland and Chew, 1974), Mercenaria mercenaria (Manzi et al., 1985) and Tapes philippinarum (Meneghetti et al., 2004) a clear relation between temperature and gonadic activity has been established. Ojea et al. (2004) observed a positive relationship between temperature and gonad condition index (GCI) in Ruditapes decussatus. Laruelle et al. (1994) reviewed data on reproductive patterns in R. ducussatus throughout its geographical range and concluded that temperature has a positive effect on gametogenesis that may directly affect the metabolic rate of the animal, or indirectly affect the availability of the food. Venerupis aurea and Tapes decussata exhibited remarkable reproductive effort and spawned several times in Lake Timsah (Kandeel, 2006). Continu- ous gamete production and repeated spawning bouts have also been docu- mented for the mytilides Modiolus arcutulus and Brachidontes variabilis in Suez Canal Lakes (Kandeel, 2002) and the cardiids Cerastoderma glaucum in Lake Qarun (Kandeel, et al., 2013). Continuous gamete production may refer to the availability of food in Suez Canal Lakes and Qarun Lake through the

132 Thalassia Salentina n. 39-2017

year. Also, it seems that the relatively moderate water temperature in winter (monthly mean =16.3 oC) and warm in summer (monthly mean = 29.3 oC) are both within range of the clam’s and mussel’s normal metabolism. For this reasons enough samples of juveniles (N = 1870) were examined in the present study. For the studied species, samples collected during summer season reached sexual maturity at a size smaller than that reported for samples collected during winter. Also, the trend of increasing size at maturity with decreasing temperature was observed. Early maturation in warm environments and de- layed maturation in cold environments were, also reported for the majority of ectotherms (Angilleta et al., 2004). Venerupis aurea collected from Lake Timsah, Suez Canal (approximately 30o 33 ̀ - 30o35 ̀ N latitude) matures at a relatively smaller size (SM50 = 11.0 and 16.4 mm SL for summer and winter, respectively) than do individuals from Lake Qarun, Fayoum Depretion (ap- o o proximately 29 25 ̀- 29 34.0 ̀ N latitude). SM50 was 12.1 and 16.6 mm SL for the two seasons, respectively. However, the trend of increasing size at maturity with decreasing latitude was much less clear in all studied species. A distinct latitudinal variation in the patterns of shell growth and sexual maturation was detected in the venerid bivalve Phacosoma japonicum (Reeve) in the Japanese coast (Sato, 1994). Juveniles of C. glaucum from Lake Timsah (Mohammed et al., 2006), M. arcutulus from Great Bitter Lake and Lake Timsah and B. variabilis from Great Bitter Lake (Kandeel, 2002) are capable of spawning in the same year in which they themselves were spawned. Yankson (1986) reported that juvenile clams of C. glaucum mature and spawn within the same spawning season from which they themselves originated. However, additional studies are necessary to detect the accurate age at the onset of sexual maturity in the studied species.

REFERENCES

Agostinho C.S., 2000 - Use of otoliths to estimate size at sexual maturity in fish. Brazilian archives of Biology and Technology. On-line version ISSN 1678-4324. http://dx.doi.org/10.1590/S1516-89132000000400014 Angilletta M.G. Jr, Steury T.D, Sears M.W., 2004 - Temperature, growth rate, and body

size in ectotherms: fitting pieces of a life-history puzzle. Integrative and Compara- tive Biology, 44: 498-509. Brown A.C., Mclachlan A., 1990 - Ecology of Sandy Shores. Amsterdam, Elsevier, pp 392. Darrigran G.A., Penchaszadeh P.E., Damborenea M.C., 1999 - The reproductive cycle of Limnoperna fortunei (Dunker, 1857) (Mytilidae) from a neotropical temperate locality. Journal of Shellfish Research, 18: 361-365.

133 Thalassia Salentina n. 39-2017

El-Ghobashy A.E., Mohmmad S.Z, Kandeel S.K., El-Ghitany A.H., 2011 - Factors associ- ated with the distribution of the invasive bivalve clam Donax variabilis (Say,1822) at the area of the Mediterranean coast preferred by marine fish larvae, New Da- mietta, Egypt. Journal of American Science, 7 (1): 1051-1062. El-Shabrawy G.M., 2001 - Ecological studies on macrobenthos of Lake Qarun, El- Fayoum, Egypt. Journal of Egyptian Academic Society for Environmental Develop- ment (B-Aquaculture): 29-49. Fishar M.R.A., 2000 - Long-term changes (1974–1996) of benthic macroinvertebrates in Lake Qarun (Faiyoum – Egypt). Egyptian Journal of Aquatic Biology and Fishery, 4: 61-73. Fouda M.M., Abou-Zied M.M., 1990 - Bivalves of the Suez Canal lakes. Proceedings of Zoological Society of Egypt, 21: 231-240. Ghobashey A.A, Mohammed S.Z., Gabr H.R., Brand A.R., 1992 - Community structure and seasonal variation of Mollusca at Lake Timsah (Suez Canal). Journal of the Egyptian German Society of Zoology, 7 (B): 145-160. Holland A.D., Chew, K.K., 1974 - Reproductive cycle of the manila clam (Venerupis japonica), from Hood Canal, Washington. Proceedings of National Shellfisheries Association, 4: 53-58. Kandeel K.E, 2002 - Ecological and biological studies on some bivalves in Lake Tim- sah and the Bitter Lakes. Unpublished Ph.D. Thesis. Suez Canal University, Egypt. Kandeel K.E., 2006 - Quantitative assessment of gamete production in two commer- cially harvested clams, Venerupis aurea and Tapes decussata (Bivalvia: Veneridae) in Lake Timsah, Suez Canal, Egypt. Catrina, 1 (1): 41-52. Kandeel K.E., Mohammed S.Z., Mostafa A.M., Abd-Alla M.E., 2013 - Reproductive biology of the cockle Cerastoderma glaucum (Bivalvia: Cardiidae) from Lake Qarun, Egypt. Egyptian Journal of Aquatic Research, 39: 249-260. Kandeel E.K., Mohammed S.Z., Mostafa A.M., Abd-Alla M.E., 2017 - Population dy- namics of the cockle Cerastoderma glaucum: a comparison between Lake Qarun and Lake Timsah, Egypt. Turkish Journal of Fisheries and Aquatic Sciences, 17: 945-958. Laruelle F., Guillou J., Paulet Y.M., 1994 - Reproductive pattern of the clams, Rudi- tapes decussatus and R. philippinarum on intertidal flats in Brittany.Journal of the Marine Biological Association, U.K., 74: 351-366. Manzi J.J., Bobo M.Y., Burrell Jr. V.G., 1985 - Gametogenesis in a population of the hard clam, Mercenaria mercenaria, in north Santee Bay, South Carolina. Veliger, 28: 186-194. Meneghetti F., Moschino V., Da Ros L., 2004 - Gametogenic cycle and variations in oocyte size of Tapes philippinarum from the Lagoon of Venice. Aquaculture, 240: 473-488. Mohammad S.H., Mohallal M.E., Mohammed S.Z, Attia M.N., 2006 - Age and growth of the cockles Cerastoderma glaucum and Papyridea papyraca in Lake Timsah, Suez Canal. Catrina, 1: 25-32. Mohammed S.Z., Gabr H.R., Ghobashy A.F.A., Brand A.R., 1992 - Species composition and distribution of benthic molluscs in Lake Timsah (Suez Canal). Journal of the Egyptian German Society of Zoology, 7 (B): 161-174. Ojea J., Pazos A.J., Martinez D., Novoa S., Sanchez J.L., Abad M., 2004 - Seasonal variation in weight and biochemical composition of the tissues of Ruditapes decussatus in relation to the gametogenic cycle. Aquaculture, 238: 451-468.

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Roa R., Ernst B., Tapia F., 1999 - Estimation of size at sexual maturity: an evaluation of analytical and resampling procedures. Fishery Bulletin, 97: 570-580. Sastry A.N., 1979 - Pelecypoda (excluding Ostreidae). In: A.C. Giese and J.S. Pearse (eds.) Reproduction of Marine Invertebrates. New York, Academic Press, pp 113- 292. Sato S., 1994 - Analysis of the relationship between growth and sexual maturation in Phacosoma japonicum (Bivalvia: Veneridae). Marine Biology, 118: 663-672. Seed R., Suchanek T.H., 1992 - Population and community ecology of Mytilus. In: E. Gosling (ed.). The Mussel Mytilus: Ecology, Physiology, Genetics and Culture: Developments in Aquaculture and Fisheries Sciences, 25, Elsevier, pp 87-169. Somerton D. A., 1980 - A computer technique for estimating the size of sexual maturity in crabs. Canadian Journal of Fishery and Aquatic Science, 37: 1488-1494. Torroglosa M.U., Giménez J., 2016 - Size at first maturity of Brachidontes rodriguezii (d’Orbigny, 1846) from the South-western Atlantic Ocean. Journal of the Marine Biological Association of the United Kingdom. DOI: https://doi.org/10.1017/ S0025315416001636. Weng H.T., 1994 - Estimation of the size at first maturity, with reference to trumpeter whiting Sillago maculata Quoy and Gaimard. Journal of Fish Society Taiwan, 21 (3): 241-247. Yankson K., 1986 - Precocious sexual maturity in Cerastoderma glaucum (Bruguière) reared in the laboratory. Journal of Molluscan Studies, 52: 79-80.

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