Skip to main content
Download PDF

The gametogenic cycle and spawning of the short-necked clam, Paphia undulata Born, 1778 (Bivalvia: Veneridae) from Timsah Lake, Suez Canal, Egypt

BMC Zoology volume 8, Article number: 20 (2023) Cite this article

Abstract

Background

Paphia undulata, The Short-Necked Clam, is an edible marine bivalve that is consumed internationally and locally in Egypt. Overfishing and pollution have caused population declines in Egyptian fisheries during the last decade. Accurate reproductive biology knowledge is critical for designing long-term exploitation strategy for this resource. P. undulata spawning and gametogenic cycle research were carried out from January to December 2020 along Timsah Lake, Suez Canal, Egypt.

Results

These clams are functionally dioecious with a very low incidence of hermaphroditism. The sex ratio of the clam population was 1.0:1.07:0.04 for male, female and hermaphrodite respectively. The shell lengths of the collected clams were 4.64 ± 0.83 cm in males, 4.55 ± 0.9 cm in females and 4.19 ± 0.3 cm in hermaphrodite clams. The sizes at the onset of sexual maturity in both males and females were 2.1 cm and 2.5 cm respectively.

Conclusions

Reproductive studies revealed that this species has a prolonged spawning season that is not restricted to a specific period.

Peer Review reports

Introduction

The bivalve clam Paphia undulata Born, 1778 (Bivalvia: Veneridae) is economically and ecologically important as a food source and biomass and may affect on communities. This species forms a large proportion of the shellfish markets in many coastal countries all over the world. Furthermore, worldwide consumption of marine bivalves has increased with growing interest in the nutritional and health benefits of these products. The overall bivalve production in Egypt was estimated between 2,600 and 25,200 tones. Bivalves are a major source of protein for the community [1,2,3]. It's a good source of protein, containing approximately 68.77% crude protein on a "dry weight basis" [4,5,6,7], and it's high in proteins, particularly essential amino acids, which are considered an essential source of nutrients for many people, particularly in developing countries [8]. The clams are consumed locally in Egypt, and its population has declined across the Egyptian fisheries in the past decade. This is mainly attributed to overexploitation, pollution, and parasites [9,10,11,12]. Gametogenesis is the process in which gametocytes undergo cell division and differentiation to form haploid gametes [13]. The sex ratio is a fundamental indicator for reproduction success in dioecious species, in which, nearly equal numbers of males and females are produced, giving a balanced sex ratio, whereas the sex ratio can skew towards one sex in hermaphroditic species [14, 15].

The size at the commencement of sexual maturity is typically defined as the length of the shell at which the gonad transitions happen from its primitive virgin condition (undifferentiated or juvenile gonad) to the stage at which it is sexually differentiated. The study of size at first maturity is important as it establishes a minimum size limit to prevent fishing for immature clams without permission [16]. Additionally, it shows population shifts caused by overfishing, and other factors. Many species reach sexual maturity at a specific age that corresponds to a wide range of individual lengths because not all members of a species develop at the same size (length). The size at start of maturity is often regarded as the "average size at which 50% of a population is mature," according to Roa et al. and Kandeel [16, 17].

The awareness of the clams’ culture was initiated in the 1970s after it was noticed that the worldwide population hastily declined. Increasing coastal populations, improved harvesting efficiency and pollution were some of the reasons that were contributing to the decrease and maybe the destruction of the clams’ local stock from their geographical range [18]. Due to the commercial importance of P. undulata and its poly-culture potential, there is a need to re-assess its status considering that there are still no known management policies governing its exploitation. This study aims to assess the reproductive cycle, gametogenesis, and spawning season of P. undulata. The result is essential to predict the reconstitution of the clam natural populations and it is recommended to support large-scale artificial breeding. and the development of artificial breeding facility in this area.

Materials and methods

Study area and sample collection

Two hundred and eighty-four random samples of the clams were collected by shellfish local fishermen from Timsah Lake sandy shore at Ismailia City, Egypt (Fig. 1). During the period from January to December 2020 (lat. 32° 17` E; long, 30° 35`·N).

Fig. 1
figure 1

Map of the sampling site of P. undulata in Timsah Lake, Ismailia. (According to El-Sherbiny et al. [19])

Full size image

Timsah Lake is a small and shallow lake located near Ismailia City at the midpoint of the Suez Canal approximately 80 km south of Port Said City. It lies between 30º 33ʹE, 30º 35ʹ N latitude and 30º 16ˋand 30º 19ˋE longitude. Its surface area is approximately 16 km2 with depth variation between 3 and 16 m. from the western side, it is attached to a small shallow western lagoon which is nearly brackish. The significant-high variation of salinity in Timsah Lake from 40 ‰ in summer to 7.3 ‰ in winter was due to the presence of many freshwater sources such as Ismailia freshwater canal and wastewater discharge from the western lagoon [20].

The clams were transferred alive to the hydro lab of the National Institute of Oceanography and Fisheries in Hurghada and prepared for morphometric analysis. The shell length was measured to the nearest 0.05 mm using a vernier calliper. The total shell weight in grams was recorded using an electronic balance accurate to two decimal places. The soft tissues were removed from the shell to obtain the gonad-visceral mass, the gonad and visceral mass are not easily separated. The gonad mass was used to distinguish the sex via smear preparations. The gonads were prepared for histological analysis.

Sex ratio and size at the onset of sexual maturity

Sexes can’t be distinguished by macroscopic examination; therefore microscopic histological examination of gonads was performed to determine sex. Chi-square (χ2) analysis was used to test for significant differences between monthly sex ratio of the studied species. The size at the onset of sexual maturity is basically described as the lowest size or age at which fifty percent of individuals matured sexually. The data were plotted against shell length and then assessed by fitting a logistic curve to the percentage of mature by size using the methods discussed by Jagadis et al. and Torroglosa and Giménez [21, 22].

Histological studies

Standard procedures for histological preparation of P. undulata gonad tissues were followed [15, 23]. The protocol included: fixing 1 cm pieces of tissue in Bouin’s fluid for 24 h, dehydrating them in a graded series of alcohol, clearing in xylene, and embedding them in paraffin wax. Sections of 5 μm thickness were stained with hematoxylin–eosin. The histological slides were observed and photographed using a mounted digital camera in a light microscope (Model Optica B-150DB) with magnification from X4 to X40.

Gonadal development of P. undulata has been described and classified into five stages: (1) early active stage (EAS); (2) late active stage (LAS);(3) ripe (maturing) stage (RS); (4) partially spent (spawning) stage (PSS); and (5) spent stage (SS), with some modifications, based on the criteria of P. undulata [24, 25]. The reproductive cycles of the sexes were analyzed independently because gonadal development times differed between the sexes.

Results

Sex ratio and size at the onset of sexual maturity

Microscopic examination of P. undulata revealed no color differentiation, and both male and female gonads were creamy in colour regardless of sex, stage, and size. Thus, it is neither possible to determine the sex and nor characterize the gonad development of the present species microscopically. These clams were functionally dioecious with very low incidences of hermaphroditism. However, this species does not exhibit sexual dimorphism. The ripe gonads occupied almost the whole tissue of the mantle.

The results of 285 examined individuals of these clams showed that 135 (47.4%) clams were males, 144 (50.5%) were females, and only six individuals were hermaphrodites thus representing (2.1%) of the studied sample (Fig. 2). Hermaphrodite specimens were collected during January and February in the winter season and from June to August in the summer season. The sex ratio (male: female: hermaphrodite) of the clam population was 1.0:1.07:0.04 (p = 0.269) (Table 1). Shell lengths of the collected clams ranged from 2.31 to 6.22 mm (4.64 ± 0.83) in males, 2.05 to 5.97 (4.55 ± 0.9) in females and 3.70 to 4.36 (4.19 ± 0.3) in hermaphrodite clams. The average size at the onset of sexual maturity in P. undulata was 2.1 cm in males and 2.5 cm in females (Fig. 3).

Fig. 2
figure 2

Monthly frequency of Paphia undulata males, females and hermaphrodite (H) sampled from January to December 2020 from Timsah Lake

Full size image
Table 1 Monthly distribution of the different maturity stages and sex ratio for males, females and hermaphrodite (H) of Paphia undulata from January to December 2020
Full size table
Fig. 3
figure 3

The size at the onset of sexual maturity of Paphia undulata from Timsah Lake

Full size image

Gametogenesis

Histological study of the gonads, can distinguish the sexes of P. undulata. It was found that gametogenesis of the calms in both males and females (Fig. 4) can be categorized into five stages as;

  • Stage 1, Early active stage (EAS), in which sex can be distinguished and gametes proliferation began.

Fig. 4
figure 4

Photomicrograph of Gonadal development stages of Paphia undulata in both male and female with magnification 100 × except in A and enlarged portion of B in right panel (400X). Left panels: male; Right panels: female. A: early active stage; B: late active stage; C: ripe stage; D: partially spent stage; E: spent stage; CT: connective tissue; EF: empty follicle; F: follicle; FW: follicle wall; IFS: interfollicular space; L: lumen; MOC: mature oocyte; N: nucleus; NU; nucleolus; OC: mature oocyte; ROC: residual oocyte; SC: spermatocyte; SG: spermatogonia; SZ: spermatozoa; SZT: spermatozoa tail

Full size image

In females, oogonia characterized by a rounded shape with large nucleus surrounded by a thick layer of cytoplasm, the oogonia undergoes different stages of development, giving rise to oocytes, which are attached to the follicles’ wall, the oocytes are characterized by obvious chromatin nuclei, they are starting to fill the follicles, free oocytes absent in the lumen.

In males, rounded to expanded follicles filled with spermatogonia and spermatocytes were only present (Fig. 4A).

  • Stage 2, Late active stage (LAS),

In females: Follicles are filled with mature free oocytes in the follicles’ lumens, appeared with peduncle, they have prominent nucleus and nucleolus. The amount of these free oocytes is less than half of the total number of follicles components; attached oocytes are abundant, in addition, there is small ration of oogonia.

In males: spermatogonia, spermatocytes, spermatids and spermatozoa are abundant in the follicles, Spermatids and spermatozoa can be observed but in small amounts by high magnification (Fig. 4B).

  • Stage 3, Ripe (Maturing) Stage (RS),

In females, the follicles increase in size, occupy a large surface area and fuse with each other, many oocytes are free in the lumen of follicles, the shape of follicles is polygonal and their walls are thin epithelium layers.

In males, the follicles are mainly composed of large amounts matured spermatozoa with their flagellum pointing towards the center of the follicle, to form concentric bands or plugs; In very ripe specimens, spermatozoa bands are close to the follicle wall; the appearance of follicles are neat (Fig. 4C).

  • Stage 4, Partially Spent (spawning) Stage (PSS),

In females: some follicles are empty due to the releasing of free oocytes; the follicle walls are broken (Fig. 4D).

In males: spermatozoa are clearly visible in a swirling shape and account for the greatest portion of cells in the follicle; there is empty space in some follicles due to the release of mature spermatozoa;

  • Stage 5, Spent Stage (SS),

The follicles appear broken, scattered, and relatively empty,

In females: only residual oocytes found in the follicles, most of them are undergoing resorption; Many phagocytes are present (Fig. 4E).

In males, in advanced spent individuals, only residual spermatozoa are found in the lumen and undergoing resorption; there is a presence of phagocytes;

Gonadal cycle

The study shows that P. undulata has a continuous breeding season as the co-occurrence of different reproductive stages in all the monthly samples of the population are observed (Table 1). The presence of mature gonads in almost all months and the infrequent occurrence of spent stages are consistent with this species having a prolonged reproductive cycle (Figs. 5 and 6). However, variation in the intensity of the reproductive activities results in peaks or periodicity in the reproductive phases.

Fig. 5
figure 5

Monthly variation in the relative frequency of different spermatogenesis stages of male Paphia undulata from January to December 2020.EAS: early active stage; LAS: late active stage; RS: ripe (Maturing) stage; PSS: partially spent (spawning) stage; SS: spent stage

Full size image
Fig. 6
figure 6

Monthly variation in the relative frequency of different oogenesis stages of female Paphia undulata from January to December 2020. EAS: early active stage; LAS: late active stage; RS: ripe (Maturing) stage; PSS: partially spent (spawning) stage; SS: spent stage

Full size image

The annual gonad development of male P. undulata was represented in Fig. 5. Male gonads in the early active development stage were observed from December to February although the late active development stage was observed throughout the year except in October and November. The ripe (maturing) stage was observed throughout the year without exception. Spawning activity began in March and continued into December except in June and August. The annual gonad development of female P. undulate is given in Fig. 6. Female gonads in the early active development stage were observed from December to March but the late active development stage and the ripe (maturing) stages were observed throughout the year. Spawning activity prolonged from March to December.

Hermaphroditism

In the current study, six specimens out of 286 specimens of P undulata were found to be hermaphrodite thus representing 2.1% of the studied sample. In all specimens, testicles and ovaries were found next to each other but separated, Fig. 7 showed that the hermaphrodite gonad contains testicles and ovaries in the partially spent stage.

Fig. 7
figure 7

Photomicrograph of the hermaphrodite Paphia undulata shows spermatids and mature eggs, respectively. CT: connective tissue; SZ: spermatozoa; MOC: mature oocyte

Full size image

Discussion

The sex ratio (male:female) of the short-neck clam, P. undulata, was 1:1.07, which indicates that P. undulata is a dioecious organism. Some hermaphrodites were also encountered but in a low percentage. Males and females are equally represented in the population. This means that the population is still in equilibrium, wherein inbreeding and competition for mates does not occur [24, 25]. In general, the ratio of the sexes for dioecious bivalves is approximately 1:1 with the number of females often being slightly higher than the number of males [24, 26]. In some bivalves like Lithophaga lithophaga the ratio of males often being higher than the ratio of females (3.5:1) [27]. Previous studies on bivalve reproduction have found that the sex ratio was 1:1, including for Gafrarium pectinatum [28], Gafrarium tumidum [22], Donax trunculus [29], Anadara granosa [30], Blood cockles Anadara inaequivalvis [31], Scrobicularia plana [32], and Noah’s ark shell Arca noae [33].

Histological study of the gonads could distinguish sexes of P. undulata. It was found that P. undulata developed their gametes in different stages similar to other bivalves e.g. cockle, hard clam and manila clam etc. [25]. However, the duration of spawning was different, for example, most of the clams in temperate areas spawned in the spring and summer months as Pinctada fucata martensii, while the tropical clams spawned throughout the year [25].

P. undulata is a dioecious organism, with small numbers of hermaphrodites (2.1%). Nabuab et al. [24] found a small percentage of hermaphrodite (0.4%) at the same previous species, in the Central Philippines, but that species is still functionally dioecious. Kongasa and Drummond et al. [25, 34] interpreted the phenomenon of hermaphrodites in a dioecious mollusc as an unusual incidence. The unnatural condition of the environment may have caused that phenomenon. The sex change of clams has not been reported in short-necked clams P. undulata [21, 24].

P. undulata has a protracted or continuous breeding season as supported by the co-occurrence of different reproductive stages in all the population monthly samples. The presence of in almost monthly mature gonads and infrequent occurrence of spent stages is consistent with this species. However, variation in the intensity of the reproductive activities results in peaks or periodicity in the reproductive phases. Protracted breeding seasons with periodicity over an annual cycle are commonly exhibited by tropical bivalve species such as Scapharca inequivalvis [35], Anodontia edentula [36], and Gari elongata [37]. This is because seasonal patterns of gonad development result from responses to within-year changes in environmental factors [38, 39], although seasonal variation in the tropics may be minimal. The continuous gamete production in P. undulata may be a result of year-round food availability in the Suez Canal and Timsah Lake. Venerupi saurea and Tapes decussata have both been seen to produce gametes continuously and to spawn repeatedly in Timsah Lake due to the availability of food [40].

The onset size of sexual maturity varies both in the different species and same species under different ecological conditions [16]. The average size at the onset of sexual maturity of P. undulata in Timsah Lake was 2.5 cm and 2.1 cm for the females and males respectively. This value is greater than that of Sutthakorn and Tuaycharoen [41] who found that the smallest size at first maturity for the same species along the western coast of Thailand is 1.43 cm, while this is different from the Gulf of Thailand as in Trat province the size at first maturity is 4.25 cm. In addition, it is decreased to 3.2 cm as reported by Chatananthawej [42] in the same site and in Suratthani province it is 3.06 cm. Jindalikit [27] stated that the size at first mature of P. undulata in Mahachai Bay, Samut Sakhon province was 3.16 and 3.19 cm in both males and females, respectively while its size at first maturity found in Southern Negros Occidental, Central Philippines was 4.23 cm for males and 4.48 cm for females [43] and it was 4.26 cm for males and 4.48 cm for females [24]. The average size at sexual maturity in P. undulata was greater than 4.0 cm in Thailand [44]. However, additional studies are necessary to detect the relationship between an accurate age at the onset of sexual maturity and environmental factors in bivalves, especially temperature and latitude.

Conclusion

In conclusion, the reproductive cycle, gametogenesis, and spawning season of P. undulata from Timsah Lake were done around one year. It was found that this species developed its gametes in different stages, and has a prolonged reproductive cycle. P. undulata is a dioecious organism with small numbers of hermaphrodites. The sex change of clams has not been reported. The resultant information recommended to support and develop large-scale artificial breeding.

Availability of data and materials

Data and Materials are available from Mostafa A. M. Mahmoud on reasonable request.

References

  1. Villarta KA, del Norte-Campos AGC. Fishery of the short-necked clam Paphia undulata in Southern Negros Occidental. Central Philippines Sci Diliman. 2010;22(1):43–51.

    Google Scholar 

  2. Yu M, Zheng L, Wang X, et al. Comparative transcriptomic analysis of surf clams (Paphia undulate) infected with two strains of Vibrio spp reveals the identity of key immune genes involved in host defense. BMC Genomics. 2019;20:988. https://doi.org/10.1186/s12864-019-6351-4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Farghaly MI, Ali TE, Mitwally HM, Abdel Razek FA. First insight into the growth and population aspects of the carpet clam Paphia textile (Gmelin, 1791), the main bivalve species along the Suez Canal, Egypt. Egypt J Aquat Res. 2022;48:265–72.

    Article  Google Scholar 

  4. Ward O, Fahmy S, Alkaradawe R, Mohammad S. Biometric and histological studies of the shellfish Paphia undulata infested with parasites. Egypt J Aqua Biol Fish. 2020;24(6):383–92.

    Article  Google Scholar 

  5. He XQ, Cao WH, Zhao ZK, Zhang CH. Analysis of protein composition and antioxidant activity of hydrolysates from Paphia Undulate. J Food Nutr Res. 2013;1:30–6.

    Google Scholar 

  6. Mazrouh MM, Mourad MH. Biochemical composition and bioaccumulation of heavy metals in some seafood in the Mediterranean Coast of Egypt. Egypt J Aquat Biol Fish. 2019;23(1):381–90.

    Article  Google Scholar 

  7. Abd-El-Aziz NA. Preservation of Shellfish Undulate Venus (Paphia undulata) by canning with different treatments. Food Nutr Sci. 2021;12:859–73.

    CAS  Google Scholar 

  8. Hao L, Wang X, Cao Y, Xu J, Xue C. A comprehensive review of oyster peptides: preparation, characterisation and bioactivities. Rev Aquacult. 2021;14:120–38.

    Article  CAS  Google Scholar 

  9. Wang W, Yao HL. Method of preparing paraffin tissue section specimens with Bouin solution as fixative. J Qiqihar Univ Med. 2011;02:93 (in chinese).

    Google Scholar 

  10. Qin LY, Zhang RC, Liang YD, Wu LC, Zhang YJ, Mu ZL, Deng P, Yang LL, Zhou Z, Yu ZP. Concentrations and health risks of heavy metals in five major marketed marine bivalves from three coastal cities in Guangxi China. Ecotoxicol Environ Safe. 2021;223:1–13. https://doi.org/10.1016/j.ecoenv.2021.112562.

    Article  CAS  Google Scholar 

  11. El-Gamal MM. Detection of trematode larvae in Donax truculus (Mollusca: Bivalvia) from Egypt. Proc 6th Intl Conf Biol Sci (zool). 2010;6:296–305.

    Google Scholar 

  12. El-Wazzan E, Radwan EH. Histopathological study for evaluation of trematode larval infection in the carpet shell clam, Tapes decussatus, from three Egyptian clam fisheries. Egypt J Aquat Res. 2013;39(4):291–301.

    Article  Google Scholar 

  13. Chaves-Fonnegra A, Maldonado M, Blackwelder P, Lopez JV. Asynchronous reproduction and multi-spawning in the coral-excavating sponge Cliona delitrix. J Mar Biol Ass U K. 2016;96:515–28.

    Article  Google Scholar 

  14. Acarli S, Lök A, Kirtik A, Acarli D, Serdar S, Kucukdermenci A, Yigitkurt S, Yildiz H, Saltan AN. Seasonal variation in reproductive activity and biochemical composition of flat oyster (Ostrea edulis) in the HomaLagoon, Izmir Bay, Turkey. Scientia Marina. 2015;79:487–549.

    Article  CAS  Google Scholar 

  15. Hassan MM, Qin JG, Li X. Gametogenesis, sex ratio and energy metabolism in Ostrea angasi: implications for the reproductive strategy of spermcasting marine bivalves. J Molluscan Stud. 2017;84:38–45. https://doi.org/10.1093/mollus/eyx041.

    Article  Google Scholar 

  16. Kandeel EK. Size at the onset of sexual maturity in 7 bivalve species in Egyptian waters. Thalassia Salentina. 2017;39:123–36.

    Google Scholar 

  17. Roa R, Ernst B, Tapia F. Estimation of size at sexual maturity: an evaluation of analytical and resampling procedures. Fish Bull. 1999;97:570–80.

    Google Scholar 

  18. Van Wynsberge S, Andréfouët S, Gaertner-Mazouni N, Wabnitz CCC, Menoud M, Le Moullac G, et al. Growth, Survival and Reproduction of the Giant Clam Tridacna maxima (Ro¨ding 1798, Bivalvia) in Two Contrasting Lagoons in French Polynesia. PLoS One. 2017;12(1):e0170565. https://doi.org/10.1371/journal.pone.0170565.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. El-Sherbiny MM, Al-Aidaroos AM, Gab-Alla A. Seasonal composition and population density of zooplankton in Lake Timsah, Suez Canal, Egypt. Oceanologia. 2011;53(3):837–59.

    Article  Google Scholar 

  20. Hamed MA, El-Sawy MA, Abu El-Naga EH. Hydrochemistry and nutrients of Bitter and Timsah Lakes, Suez Canal. Egypt Egypt J Aquat Biol Fish. 2012;16(2):1–12.

    Article  Google Scholar 

  21. Torroglosa MU, Giménez J. Size at first maturity of Brachidontes rodriguezii (d’Orbigny, 1846) from the South-western Atlantic Ocean. J Mar Biol Asso UK. 2016. https://doi.org/10.1017/S0025315416001636.

    Article  Google Scholar 

  22. Jagadis I, Rajagopal S. Reproductive biology of Venus clam Gafarium tumidum (Roding, 1798) from Southeast coast of India. Aquat Res. 2007;38:1117–22.

    Article  Google Scholar 

  23. Wang WD. Breeding condition monitoring of Paphia undulate from the East Valley Roller in Fujian Sea Area in China. Anim Breed Feed. 2009;6:17–21.

    CAS  Google Scholar 

  24. Nabuab FM, Ledesma-Fernandez L, del Norte-Campos A. reproductive biology of the short-necked clam, Paphia undulata (Born 1778) from Southern Negros Occidental. Central Philippines, Sci Diliman. 2010;22(2):31–40.

    Google Scholar 

  25. Kongasa W. Reproductive biology of short-neck clams Marcia recens (Holten, 1802) at Tambon Koh Sarai, Satun Province. Thesis (M.Sc., Aquatic Science), Prince of Songkla University; 2019. p. 79. http://kb.psu.ac.th/psukb/handle/2016/12948.

  26. Jindalikit J. Reproductive biology of short necked clam Paphia undulata (Born, 1778). in Mahachai Bay, Samut Sakhon Province. Fisheries Research Paper No. 16/2000, Marine Fisheries Research and Development Bureau, Department of Fisheries, Bangkok, Thailand (In Thai); 2000.

  27. Khafage AR, Abdel Razek FA, El-Deeb RS, Taha SM, Omar HA, Attallah MA. Gonadal cycle and spawning of date mussel Lithophaga lithophaga (L.) (Bivalvia: Mytilidae) in Egyptian water. Egypt J Aquat Res. 2019;45:293–9.

    Article  Google Scholar 

  28. Gab-Alla AA-FA, Mohamed SZ, Mahmoud MAM, Soliman BA. Ecological and biological studies on some economic Bivalves in Suez Bay, Gulf of Suez, Red Sea, Egypt. J Fish Aqua Sci. 2007;2(3):178–194.

  29. Gaspar MB, Ferreira R, Monteiro CC. Growth and reproductive cycle of Donax trunculus L., (Mollusca: Bivalvia) off Faro, southern Portugal. Fish Res. 1999;41:309–16.

    Article  Google Scholar 

  30. Suwanjarat J, Pituksalee C, Thongchai S. Reproductive cycle of Anadara granosa at Pattani Bay and its relationship with metal concentrations in the sediments. Songklanakarin J Sci Technol. 2009;31(5):471–9.

  31. Sahin C, Duzgunes E, Okumus I. Seasonal variations in condition index and gonadal development of the introduced blood cockle Anadara inaequivalvis (Bruguiere, 1789) in the Southeastern Black Sea Coast. Turkish J Fish Aquat Sci. 2006;6:155–63.

    Google Scholar 

  32. Rodríguez-Rúa A, Prado MA, Romero Z, Bruzon M. The gametogenic cycle of Scrobicularia plana (da Costa, 1778) (Mollusc: Bivalve) in Guadalquivir estuary (C´ adiz, SW Spain). Aquacult. 2003;217(1–4):157–66.

    Article  Google Scholar 

  33. Peharda M, Mladineo I, Bolotin J, Kekez L, Skaramuca B. The reproductive cycle and potential protandric development of the Noah’s Ark shell, Arca noae L: Implications for aquaculture. Aquacult. 2006;252:317–27.

    Article  Google Scholar 

  34. Drummond L, Mulcahy M, Culloty S. The reproductive biology of the Manila clam, Ruditapes philippinarum, from the North-West of Ireland. Aquacult. 2006;254:326–40.

    Article  Google Scholar 

  35. Ledesma-Fernandez LN, del Norte-Campos AGC. Reproductive cycle of the ark shell Scapharca inaequivalvis (Brugiere, 1789) (Mollusca, Pelecypoda: Arcidae) in Banate Bay, west central Philippines. UPV J Nat Sci. 2004;9(1):111–23.

    Google Scholar 

  36. Samentar L, Formacion M, Geduspan J. Reproductive biology of the mud-dwelling clam, imbaw (Anodontia edentula) in Guimaras Province, Central Philippines. UPV J of Nat Sci. 2004;9:217–28.

    Google Scholar 

  37. Nabuab F, del Norte-Campos A. Some aspects of the reproduction in the elongate sunset clam Gari elongata (Lamarck 1818) from Banate Bay Area West Central Philippines. Sci Diliman. 2006;18:34–46.

    Google Scholar 

  38. Sastry AN. Pelecypoda (excluding Ostreidae). V. Mollusks: Pelecypoda and Lesser Classes. Acad Press: NY; 1979.

  39. Mackie GL. Bivalves. Mollusca. 1984;7:351–418. (eds A.S. Tompa, N.H. Verdonk and J.A.M. Van Den Biggelaar). Academic Press: New York.

    Google Scholar 

  40. Kandeel KE. Quantitative assessment of gamete production in two commercially harvested clams, Venerupis aurea and Tapes decussata (Bivalvia: Veneridae) in Lake Timsah, Suez Canal. Egypt Catrina. 2006;1(1):41–52.

    Google Scholar 

  41. Sutthakorn P, Tuaycharoen S. Biological aspects of short necked clam Paphia undulata (Born, 1778) off the west coast of Thailand. Bangkok: Marine Life History Unit, Andaman Sea Fisheries Research and Development Center, Marine Fisheries Division, Department of Fisheries. Technical Paper no. 24; 1993. pp. 54.

  42. Chatananthawej B. Management on short-necked clam fishery: a case study in Trat Province Fishing Ground. Master Degree of Science (Resources Management) Thesis. Graduate School. Bangkok: Kasetsart University; 1993.

    Google Scholar 

  43. del Norte-Campos A, Villarta KA. Use of population parameters in examining changes in the status of the short-necked clam Paphia undulata Born, 1778 (Mollusca, Pelecypoda: Veneridae) in Coastal Waters of Southern Negros Occidental. Sci Diliman. 2010;22(1):53–60.

    Google Scholar 

  44. Pongthana N. Breeding and rearing of short-necked clam Paphia undulata. Thai Mar Fish Res Bull. 1990;1:69–73.

    Google Scholar 

Download references

Acknowledgements

Not applicable.

Funding

Open access funding provided by The Science, Technology & Innovation Funding Authority (STDF) in cooperation with The Egyptian Knowledge Bank (EKB). There were no funds, grants, or other support were received during the preparation of this manuscript except personal funding from the authors themselves, but all experiments were done in and under the supervision of the National Institute of Oceanography and Fisheries.

Author information

Authors and Affiliations

  1. National Institute of Oceanography and Fisheries, Cairo, Egypt

    Mostafa A. M. Mahmoud & Mohamed H. Yassien

Authors
  1. Mostafa A. M. Mahmoud
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mohamed H. Yassien
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

M. Y. designed the study, collected the specimens and prepared wax blocks. M.M. carried out the slide sections preparation and analyzed the data. M.M. wrote the first draft of the manuscript M.Y. reviewed the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Mostafa A. M. Mahmoud.

Ethics declarations

Ethics approval and consent to participate

The study did not involve human participants or welfare of animals. The sampled species is not endangered and was not collected in protected area.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mahmoud, M.A.M., Yassien, M.H. The gametogenic cycle and spawning of the short-necked clam, Paphia undulata Born, 1778 (Bivalvia: Veneridae) from Timsah Lake, Suez Canal, Egypt. BMC Zool 8, 20 (2023). https://doi.org/10.1186/s40850-023-00182-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s40850-023-00182-9

Keywords

BMC Zoology

ISSN: 2056-3132

Contact us