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Hermaphroditism in Brachidontes pharaonis (Fischer, 1876) (Bivalvia: Mytilidae) from the Alexandria Coast, Egypt
Egyptian Journal of Aquatic Research xxx (2017) xxx–xxx
Contents lists available at ScienceDirect
Egyptian Journal of Aquatic Research journal homepage: www.sciencedirect.com/locate/ejar
Full length article
Hermaphroditism in Brachidontes pharaonis (Fischer, 1876) (Bivalvia: Mytilidae) from the Alexandria Coast, Egypt Fatma A. Abdel Razek a,⇑, Rabab S. El-Deeb a, Karolin K. Abdul-Aziz b, Hamdy A. Omar a, Amal R. Khafage a a b
National Institute of Oceanography and Fisheries, Cairo, Egypt Faculty of Science, Zoology Department, Damanhour University, Egypt
a r t i c l e
i n f o
Article history: Received 24 September 2017 Revised 5 October 2017 Accepted 7 October 2017 Available online xxxx Keywords: Hermaphroditism Brachidontes pharaonis Sex ratio Histology Alexandria Egypt
a b s t r a c t Brachidontes pharaonis (Fischer, 1876) was widely reported to cover completely hard substrates especially rocky shores with higher density in mid-littoral zones forming mytilid beds along Alexandria Coast, Egypt. During our study on the reproductive cycle of this species, one case out of 307 examined specimens was found to be hermaphrodite representing only 0.33% of the total sample. It had a shell length 28.25 mm and was collected during January 2017. The sex ratio of this population is different from 1:1, although this deference was not significant (X2 = 11.118, df = 11, P > 0.05). In this contribution, this case of hermaphroditism in B. pharaonis is described. The histological study showed the presence of male and female gametes in the same follicle and this was the most common situation in both lobes of the mantle. The male zone was showing different stages of spermatogenesis together with the female zones showed different stages of oogenesis with occurrence of young oocytes attached to the follicle wall. Ó 2017 National Institute of Oceanography and Fisheries. Hosting by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Introduction
Materials and methods
Brachidontes pharaonis is a species of mussel from the family Mytilidae which is native to the Indian Ocean and Red Sea (Gilboa, 1976). Considering its invasive potential and the recent warming trend of the Mediterranean, it has invaded more habitats, threatening indigenous bivalve species which may be, in the future, unable to compete with B. pharaonis in terms of reproductive effort and density as predicted by Sara et al. (2008). B. pharaonis is widely reported from the Western Pacific Ocean, Indian Ocean and the Red Sea (Morton, 1988). Its migration to the Mediterranean Sea through Suez Canal and from the Eastern African Coasts to Southern Africa was reported by Barash and Danin (1986). Few studies were done on its ecology, age structure, distribution and biometric relationships in the Red Sea, Gulf of Suez and Eastern Mediterranean Coast of Egypt by Mohamed (1992, 1997), Radwan (2014) and El-Sayed et al. (2016). To the knowledge of the authors, the present study is considered as the first record of the presence of hermaphroditism in B. pharaonis.
In the present study, three sites were selected along the coast of Alexandria City, as shown in Fig. 1. The three sites covered about 16 km along the coast. The sites (A) and (B) were of about 250 m and 100 m away from the coast, respectively. While site (C) is located in the Eastern Harbor in front of Kayed Bey Citadel at Alexandria. Sampling was done during the period from spring 2016 to winter 2017 using 1 m 1 m quadrat placed randomly along a 100 m 100 m transect. Water depth ranged from 1 to 6 m. Shell length was measured by using a digital Vernier Caliper (0.01 mm accuracy). For histological examination, monthly random samples with more than 8 mm shell length were collected. A total of 307 individuals were dissected, from each sample the mantle was removed and fixed directly into Davidson’s fixative (1 part glycerin, 1 part glacial acetic acid, 2 parts 37% formaldehyde, 3 parts 95% ethanol, and 3 parts isotonic sodium chloride 20–30%) (Kim et al., 2006) for 24 h. They were then stored in 70% ethyl alcohol until processing. The tissue was dehydrated with an ascending series of alcohol concentrations (80%, 90% and 100%), cleared with xylene, and then embedded in paraffin wax (40–50 °C). Sections were done from the wax block at thickness 5 lm using a manual microtome (KD-2258). Sections were then mounted on glass slides for further
Peer review under responsibility of National Institute of Oceanography and Fisheries. ⇑ Corresponding author. E-mail address: [email protected] (Fatma A. Abdel Razek).
https://doi.org/10.1016/j.ejar.2017.10.002 1687-4285/Ó 2017 National Institute of Oceanography and Fisheries. Hosting by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Please cite this article in press as: Razek, F.A.A., et al. Hermaphroditism in Brachidontes pharaonis (Fischer, 1876) (Bivalvia: Mytilidae) from the Alexandria Coast, Egypt. Egyptian Journal of Aquatic Research (2017), https://doi.org/10.1016/j.ejar.2017.10.002
2
Fatma A. Abdel Razek et al. / Egyptian Journal of Aquatic Research xxx (2017) xxx–xxx
staining with hematoxylin and eosin (Howard et al., 2004). Gonad sections were examined under a light microscope (OPTIKA B-150). Chi-square test was used to determine if there was any monthly deviation in the sex ratio of the examined individuals from a 1:1 ratio.
X2 ¼
X
ðO EÞ2 =E
where, X2 is chi-square test, (O) is the observed values in each month, and (E) is the expected values. Sections were photographed using a mounted digital camera (TOUCAMTM – UCMOS, 3.1 MP1/2, Model No. 3.2).
Results The gonad of B. pharaonis, as in other mytilidae, is very simple consisting of follicles in the mantle and in the visceral mass. During the present study one specimen out of 307 was found to be hermaphrodite, representing only 0.33% of the studied sample. The hermaphrodite individual had a shell length of 28.25 mm. We should note that all individual studied of B. pharaonis varied between 2 mm and 38 mm shell length. The sex ratio in Tables 1 and 2 did not differ much from 1:1 and chi-square value was (X2 = 11.118, df = 11, P > 0.05), i.e. non-significant differences. The microscopic examination of the two sides of the mantle is shown in Fig. 2. The follicles in the hermaphrodite individual in B. pharaonis are of three kinds, testes, ovaries and ovotestis at different stages of gamete maturation together with connective tissue. Male follicles were at late developmental stage with full ripe spermatozoa and with remarks of partial emission. The female follicles were partially spawned. Few female follicles showed signs of resorption. The presence of male and female gametes in the same follicle was the most common situation in the two lobes of the mantle. In these follicles there were male zones having maturing spermatocytes, and few spermatozoa. The female zones showed different stages of oogenesis. We notice here that the egg diameters for the hermaphrodite individual ranged between (15–50) mm and had an average size of 34.5 mm. It is to be mentioned that, young oocytes were found attached to the follicle’s wall as shown in Fig. 2.
Fig. 1. Locations of the sampling sites for the mussel Brachidontes pharaonis.
Table 1 Percentage of the examined individuals of B. pharaonis during the study period. Males Females Undifferentiated sex Hermaphrodite Total No.
135 (44%) 159 (51.8%) 12 (3.9%) 1 (0.3%) 307
Table 2 Monthly distribution of sex ratio of the examined individuals of B. pharaonis. Chi-square test on the sex ratio for males and females of B. pharaonis Number of Individuals examined Month
Mar.
Apr.
May
Jun.
Jul.
Aug.
Sep.
Oct.
Nov.
Dec.
Jan.
Feb.
Total No.
Males Females Undifferentiated sex Hermaphrodite Total No.
15 8 1
15 11
10 16 1
14 11 1
11 16
15 18
9 13 2
11 19
9 19 1
9 13 4
5 4 1
24
26
27
26
27
33
24
30
29
26
12 11 1 1 25
135 159 12 1 307
10
Observed values: Month
Mar.
Males 15 Females 8 Expected values:
Apr.
May
Jun.
Jul.
Aug.
Sep.
Oct.
Nov.
Dec.
Jan.
Feb.
15 11
10 16
14 11
11 16
15 18
9 13
11 19
9 19
9 13
12 11
5 4
Month
Mar.
Apr.
May
Jun.
Jul.
Aug.
Sep.
Oct.
Nov.
Dec.
Jan.
Feb.
Males Females
10.5612 12.4387
11.9387 14.0612
11.9387 14.0612
11.4795 13.5204
12.3979 14.6020
15.1530 17.8469
10.1020 11.8979
13.7755 16.2244
12.8571 15.1428
10.102040 11.897959
10.5612 12.4387
4.13265 4.86734
X2 = 11.118, df = 11, p-value = 0.43344, P > 0.05, not significantly different.
Please cite this article in press as: Razek, F.A.A., et al. Hermaphroditism in Brachidontes pharaonis (Fischer, 1876) (Bivalvia: Mytilidae) from the Alexandria Coast, Egypt. Egyptian Journal of Aquatic Research (2017), https://doi.org/10.1016/j.ejar.2017.10.002
Fatma A. Abdel Razek et al. / Egyptian Journal of Aquatic Research xxx (2017) xxx–xxx
3
Fig. 2. Photomicrographs of light microscope showing hermaphrodite case of Brachidontes pharaonis: A, A0 : right lobe of mantle, B, B0 : left lobe of mantle; Ct: connective tissue; Sz: spermatozoa; MOc: mature oocyte; ImOc: immature oocyte; Fw: follicle wall.
Discussion Class Bivalvia constitutes the second largest class in Mollusca, which in turn is the second largest animal phylum. The modes of sexual reproduction found in bivalves as reported by Coe (1943), range from simultaneous hermaphroditism, sequential hermaphroditism, to strict gonochorism or dioecious (i.e. species that exist as separate males and females). Consequently it is important that both juveniles and adults must be examined in order to be certain definitely about its sex. The case of hermaphroditism discussed in the present study represents about 0.33% out of a sample of 307 individuals taken from subsurface water (1–2.0 m depth) at ElAnfoushy site, in the Eastern Harbor of Alexandria City. The size of the hermaphrodite B. pharaonis was 28.25 mm (shell length) and was collected during January 2017. B. pharaonis, according to the present data was found to have a prolonged spawning period extending from April to October (El-
Deeb, 2017 unpublished data). Sara et al. (2008) mentioned that the spawning period of this species, like other temperate mytilids, especially submerged specimens was restricted to late spring and early summer months in Western Mediterranean. Hermaphrodite individuals occasionally have been found in species strictly considered gonochoristic (Heller, 1993), as well as in the mussel Aulacomya ater (Vinuesa, 1977) and the marine Perumytilus purpuratus, (Montenegro et al., 2010) from which two hermaphrodites were recorded (among 179) from the Northern Chilean Coast. The dioecious condition is the main fact in Mytilidae, which includes mostly marine and estuarine species as reported by Lee (1988), the scarce records of hermaphrodite individuals indicate that it could be an accidental incidence as mentioned by Ragone Calvo et al. (1998). The study of Delgado and Perez (2002) of R. decussatus clams proved that although this clam is considered to be strictly gonochoristic, there was an occasional occurrence of hermaphroditic individuals with possibility of sex reversal.
Please cite this article in press as: Razek, F.A.A., et al. Hermaphroditism in Brachidontes pharaonis (Fischer, 1876) (Bivalvia: Mytilidae) from the Alexandria Coast, Egypt. Egyptian Journal of Aquatic Research (2017), https://doi.org/10.1016/j.ejar.2017.10.002
4
Fatma A. Abdel Razek et al. / Egyptian Journal of Aquatic Research xxx (2017) xxx–xxx
Change of sex from male to female was recorded in Limnoperna fortunei kikuchi due to the effect of environmental conditions as recorded by Abdel-Razek (1983). Also the occurrence of sequential protandric hermaphrodite with only a single sex change during life history was found in Anadara granosa (L.) (Afiati, 2007). In Malaysia, Al-Barwani et al. (2013) reported two hermaphrodite individuals out of (317) of Perna viridis during June and September. In conclusion, the hermaphrodite individual in the present study of B. pharaonis could be a type of an occasional hermaphroditism. Additional studies are important to study the reasons of B. pharaonis fast propagation in most of marine areas in the Egyptian water and the reason of presence of hermaphrodite individuals in its population.
References Abdel-Razek, F.A., 1983. Ecological Studies on the fouling bivalve Limnoperna fortunei kikuchii HABE (PhD Thesis). Dep. of Fish., Fac. of Agri., Tokyo University, Japan. Afiati, N., 2007. Gonad maturation in Anadara granosa (L.) and Anadara antiquate (L.) (Bivalvia: Arcidae). J. Coast. Dev. 10 (2). Al-Barwani, S.M., Arshad, A., Amin, S.M.N., Bujang, J.S., 2013. Incidence of hermaphrodite in green mussel Perna viridis along the west coast of Peninsular Malaysia. Asian J. Anim. Vet. Adv. 8 (2), 376–382. El-Sayed, Awaad, El-Mobarak, Najat O., Nassef, Amr M., El-Hammady, Montaser A., El-Mekawy, Hosam A., 2016. Biometric relationships for the Bivalve mussel Brachidontes pharaonis population from the North-Western Coast of Suez Gulf, Egypt. Egypt. Acad. J. Biol. Sci. 8 (1), 61–73. Barash, A., Danin, Z., 1986. Further additions to the knowledge of Indo-Pacific Mollusca in the Mediterranean Sea. Spixiana 9, 117–141. Coe, W.R., 1943. Sexual differentiation in mollusks I. Pelecypods. Q. Rev. Biol. 18, 154–164. Delgado, M., Perez, A.C., 2002. Hermaphroditism in Ruditapes decussatus (L.) (Bivalvia) from the Galician coast (Spain). Sci. Mar. 66, 183–185.
El-Deeb, R.S., 2017. Biological and Ecological Studies on Some Mussel Species (Bivalvia: Mollusca) From the Mediterranean Sea, Alexandria, Egypt (M.Sc. Thesis). Faculty of Science, Damanhour University (Unpublished data). Gilboa, A., 1976. Experiments in Mytilids Recolonization (Ms. Dissertation). Hebrew University of Jerusalem Israel. Heller, J., 1993. Hermaphroditism in mollusks. J. Limn. Soc. 48, 19–42. Howard, D.W., Lewis, E.J., Keller, B.J., Smith, C.S., 2004. Histological Techniques for Marine Bivalve Mollusks and Crustaceans NOAA Technical Memorandum NOS NCCOS 5, p. 218. Kim, Y., Ashton-Alcox, K.A., Powell, E.N., 2006. Histological Techniques for Marine Bivalve Molluscs: Update. Silver Spring, MD, p. 76. NOAA Technical Memorandum NOS NCCOS, 27. Lee, S.Y., 1988. The reproductive cycle and sexuality of the green mussel Perna viridis (L.) (Bivalvia: Mytilacea) in Victoria Harbor, Hong Kong. J. Molluscan. Stud. 54, 317–325. Mohamed, S.Z., 1992. The interaction between adults and recruitments in the Brachidontes variabilis L. (Lamellibranchiata) bed in the Bitter Great Lake, Suez Canal. Q. Univ. Sci. J. 12, 228–232. Mohamed, S.Z., 1997. Influence of age structure of Brachidontes variabilis on the community structure of its associated fauna in the Greater Bitter Lake, Suez Canal. J. Egypt. German Zool. 24, 51–67. Montenegro, V.D., Olivares, P.A., Gonzalez, M.T., 2010. Hermaphroditism in marine mussel Perumytilus purpuratus Lamarck, 1819), (Mollusca: Mytilidae). Int. J. Morphol. 28 (2), 569–573. Morton, B., 1988. The population dynamics and reproductive cycle of Brachidontes variabilis (Bivalvia: Mytilidae) in Hong Kong mangrove. Malacol. Rev. 21, 109– 117. Radwan, N.A.F., 2014. Biological and Molecular Studies on Selected Molluscs Collected from the Egyptian Coastal Water (Ph.D. Thesis). Faculty of Science, Suez Canal University, Egypt, p. 194. Ragone Calvo, L.M., Walker, J.G., Burreson, E.M., 1998. Prevalence and distribution of QPX, quahog parasite unknown, in hard clams Mercenaria mercenaria in Virginia, USA. Dis. Aquat. Organ. 33, 209–219. Sara, G., Romano, C., Mazzola, A., 2008. A new Lessepsian species in the western Mediterranean (Brachidontes pharaonis) Bivalvia: Mytilidae, density, resource allocation and biomass. Mar. Biodivers. Rec., 1–8 Vinuesa, J.H., 1977. Sobre un caso de hermafroditismo en la cholga Aulacomya ater (Molina). Physis (Buenos Aires) 37, 63–65.
Please cite this article in press as: Razek, F.A.A., et al. Hermaphroditism in Brachidontes pharaonis (Fischer, 1876) (Bivalvia: Mytilidae) from the Alexandria Coast, Egypt. Egyptian Journal of Aquatic Research (2017), https://doi.org/10.1016/j.ejar.2017.10.002
Contents lists available at ScienceDirect
Egyptian Journal of Aquatic Research journal homepage: www.sciencedirect.com/locate/ejar
Full length article
Hermaphroditism in Brachidontes pharaonis (Fischer, 1876) (Bivalvia: Mytilidae) from the Alexandria Coast, Egypt Fatma A. Abdel Razek a,⇑, Rabab S. El-Deeb a, Karolin K. Abdul-Aziz b, Hamdy A. Omar a, Amal R. Khafage a a b
National Institute of Oceanography and Fisheries, Cairo, Egypt Faculty of Science, Zoology Department, Damanhour University, Egypt
a r t i c l e
i n f o
Article history: Received 24 September 2017 Revised 5 October 2017 Accepted 7 October 2017 Available online xxxx Keywords: Hermaphroditism Brachidontes pharaonis Sex ratio Histology Alexandria Egypt
a b s t r a c t Brachidontes pharaonis (Fischer, 1876) was widely reported to cover completely hard substrates especially rocky shores with higher density in mid-littoral zones forming mytilid beds along Alexandria Coast, Egypt. During our study on the reproductive cycle of this species, one case out of 307 examined specimens was found to be hermaphrodite representing only 0.33% of the total sample. It had a shell length 28.25 mm and was collected during January 2017. The sex ratio of this population is different from 1:1, although this deference was not significant (X2 = 11.118, df = 11, P > 0.05). In this contribution, this case of hermaphroditism in B. pharaonis is described. The histological study showed the presence of male and female gametes in the same follicle and this was the most common situation in both lobes of the mantle. The male zone was showing different stages of spermatogenesis together with the female zones showed different stages of oogenesis with occurrence of young oocytes attached to the follicle wall. Ó 2017 National Institute of Oceanography and Fisheries. Hosting by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Introduction
Materials and methods
Brachidontes pharaonis is a species of mussel from the family Mytilidae which is native to the Indian Ocean and Red Sea (Gilboa, 1976). Considering its invasive potential and the recent warming trend of the Mediterranean, it has invaded more habitats, threatening indigenous bivalve species which may be, in the future, unable to compete with B. pharaonis in terms of reproductive effort and density as predicted by Sara et al. (2008). B. pharaonis is widely reported from the Western Pacific Ocean, Indian Ocean and the Red Sea (Morton, 1988). Its migration to the Mediterranean Sea through Suez Canal and from the Eastern African Coasts to Southern Africa was reported by Barash and Danin (1986). Few studies were done on its ecology, age structure, distribution and biometric relationships in the Red Sea, Gulf of Suez and Eastern Mediterranean Coast of Egypt by Mohamed (1992, 1997), Radwan (2014) and El-Sayed et al. (2016). To the knowledge of the authors, the present study is considered as the first record of the presence of hermaphroditism in B. pharaonis.
In the present study, three sites were selected along the coast of Alexandria City, as shown in Fig. 1. The three sites covered about 16 km along the coast. The sites (A) and (B) were of about 250 m and 100 m away from the coast, respectively. While site (C) is located in the Eastern Harbor in front of Kayed Bey Citadel at Alexandria. Sampling was done during the period from spring 2016 to winter 2017 using 1 m 1 m quadrat placed randomly along a 100 m 100 m transect. Water depth ranged from 1 to 6 m. Shell length was measured by using a digital Vernier Caliper (0.01 mm accuracy). For histological examination, monthly random samples with more than 8 mm shell length were collected. A total of 307 individuals were dissected, from each sample the mantle was removed and fixed directly into Davidson’s fixative (1 part glycerin, 1 part glacial acetic acid, 2 parts 37% formaldehyde, 3 parts 95% ethanol, and 3 parts isotonic sodium chloride 20–30%) (Kim et al., 2006) for 24 h. They were then stored in 70% ethyl alcohol until processing. The tissue was dehydrated with an ascending series of alcohol concentrations (80%, 90% and 100%), cleared with xylene, and then embedded in paraffin wax (40–50 °C). Sections were done from the wax block at thickness 5 lm using a manual microtome (KD-2258). Sections were then mounted on glass slides for further
Peer review under responsibility of National Institute of Oceanography and Fisheries. ⇑ Corresponding author. E-mail address: [email protected] (Fatma A. Abdel Razek).
https://doi.org/10.1016/j.ejar.2017.10.002 1687-4285/Ó 2017 National Institute of Oceanography and Fisheries. Hosting by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Please cite this article in press as: Razek, F.A.A., et al. Hermaphroditism in Brachidontes pharaonis (Fischer, 1876) (Bivalvia: Mytilidae) from the Alexandria Coast, Egypt. Egyptian Journal of Aquatic Research (2017), https://doi.org/10.1016/j.ejar.2017.10.002
2
Fatma A. Abdel Razek et al. / Egyptian Journal of Aquatic Research xxx (2017) xxx–xxx
staining with hematoxylin and eosin (Howard et al., 2004). Gonad sections were examined under a light microscope (OPTIKA B-150). Chi-square test was used to determine if there was any monthly deviation in the sex ratio of the examined individuals from a 1:1 ratio.
X2 ¼
X
ðO EÞ2 =E
where, X2 is chi-square test, (O) is the observed values in each month, and (E) is the expected values. Sections were photographed using a mounted digital camera (TOUCAMTM – UCMOS, 3.1 MP1/2, Model No. 3.2).
Results The gonad of B. pharaonis, as in other mytilidae, is very simple consisting of follicles in the mantle and in the visceral mass. During the present study one specimen out of 307 was found to be hermaphrodite, representing only 0.33% of the studied sample. The hermaphrodite individual had a shell length of 28.25 mm. We should note that all individual studied of B. pharaonis varied between 2 mm and 38 mm shell length. The sex ratio in Tables 1 and 2 did not differ much from 1:1 and chi-square value was (X2 = 11.118, df = 11, P > 0.05), i.e. non-significant differences. The microscopic examination of the two sides of the mantle is shown in Fig. 2. The follicles in the hermaphrodite individual in B. pharaonis are of three kinds, testes, ovaries and ovotestis at different stages of gamete maturation together with connective tissue. Male follicles were at late developmental stage with full ripe spermatozoa and with remarks of partial emission. The female follicles were partially spawned. Few female follicles showed signs of resorption. The presence of male and female gametes in the same follicle was the most common situation in the two lobes of the mantle. In these follicles there were male zones having maturing spermatocytes, and few spermatozoa. The female zones showed different stages of oogenesis. We notice here that the egg diameters for the hermaphrodite individual ranged between (15–50) mm and had an average size of 34.5 mm. It is to be mentioned that, young oocytes were found attached to the follicle’s wall as shown in Fig. 2.
Fig. 1. Locations of the sampling sites for the mussel Brachidontes pharaonis.
Table 1 Percentage of the examined individuals of B. pharaonis during the study period. Males Females Undifferentiated sex Hermaphrodite Total No.
135 (44%) 159 (51.8%) 12 (3.9%) 1 (0.3%) 307
Table 2 Monthly distribution of sex ratio of the examined individuals of B. pharaonis. Chi-square test on the sex ratio for males and females of B. pharaonis Number of Individuals examined Month
Mar.
Apr.
May
Jun.
Jul.
Aug.
Sep.
Oct.
Nov.
Dec.
Jan.
Feb.
Total No.
Males Females Undifferentiated sex Hermaphrodite Total No.
15 8 1
15 11
10 16 1
14 11 1
11 16
15 18
9 13 2
11 19
9 19 1
9 13 4
5 4 1
24
26
27
26
27
33
24
30
29
26
12 11 1 1 25
135 159 12 1 307
10
Observed values: Month
Mar.
Males 15 Females 8 Expected values:
Apr.
May
Jun.
Jul.
Aug.
Sep.
Oct.
Nov.
Dec.
Jan.
Feb.
15 11
10 16
14 11
11 16
15 18
9 13
11 19
9 19
9 13
12 11
5 4
Month
Mar.
Apr.
May
Jun.
Jul.
Aug.
Sep.
Oct.
Nov.
Dec.
Jan.
Feb.
Males Females
10.5612 12.4387
11.9387 14.0612
11.9387 14.0612
11.4795 13.5204
12.3979 14.6020
15.1530 17.8469
10.1020 11.8979
13.7755 16.2244
12.8571 15.1428
10.102040 11.897959
10.5612 12.4387
4.13265 4.86734
X2 = 11.118, df = 11, p-value = 0.43344, P > 0.05, not significantly different.
Please cite this article in press as: Razek, F.A.A., et al. Hermaphroditism in Brachidontes pharaonis (Fischer, 1876) (Bivalvia: Mytilidae) from the Alexandria Coast, Egypt. Egyptian Journal of Aquatic Research (2017), https://doi.org/10.1016/j.ejar.2017.10.002
Fatma A. Abdel Razek et al. / Egyptian Journal of Aquatic Research xxx (2017) xxx–xxx
3
Fig. 2. Photomicrographs of light microscope showing hermaphrodite case of Brachidontes pharaonis: A, A0 : right lobe of mantle, B, B0 : left lobe of mantle; Ct: connective tissue; Sz: spermatozoa; MOc: mature oocyte; ImOc: immature oocyte; Fw: follicle wall.
Discussion Class Bivalvia constitutes the second largest class in Mollusca, which in turn is the second largest animal phylum. The modes of sexual reproduction found in bivalves as reported by Coe (1943), range from simultaneous hermaphroditism, sequential hermaphroditism, to strict gonochorism or dioecious (i.e. species that exist as separate males and females). Consequently it is important that both juveniles and adults must be examined in order to be certain definitely about its sex. The case of hermaphroditism discussed in the present study represents about 0.33% out of a sample of 307 individuals taken from subsurface water (1–2.0 m depth) at ElAnfoushy site, in the Eastern Harbor of Alexandria City. The size of the hermaphrodite B. pharaonis was 28.25 mm (shell length) and was collected during January 2017. B. pharaonis, according to the present data was found to have a prolonged spawning period extending from April to October (El-
Deeb, 2017 unpublished data). Sara et al. (2008) mentioned that the spawning period of this species, like other temperate mytilids, especially submerged specimens was restricted to late spring and early summer months in Western Mediterranean. Hermaphrodite individuals occasionally have been found in species strictly considered gonochoristic (Heller, 1993), as well as in the mussel Aulacomya ater (Vinuesa, 1977) and the marine Perumytilus purpuratus, (Montenegro et al., 2010) from which two hermaphrodites were recorded (among 179) from the Northern Chilean Coast. The dioecious condition is the main fact in Mytilidae, which includes mostly marine and estuarine species as reported by Lee (1988), the scarce records of hermaphrodite individuals indicate that it could be an accidental incidence as mentioned by Ragone Calvo et al. (1998). The study of Delgado and Perez (2002) of R. decussatus clams proved that although this clam is considered to be strictly gonochoristic, there was an occasional occurrence of hermaphroditic individuals with possibility of sex reversal.
Please cite this article in press as: Razek, F.A.A., et al. Hermaphroditism in Brachidontes pharaonis (Fischer, 1876) (Bivalvia: Mytilidae) from the Alexandria Coast, Egypt. Egyptian Journal of Aquatic Research (2017), https://doi.org/10.1016/j.ejar.2017.10.002
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Fatma A. Abdel Razek et al. / Egyptian Journal of Aquatic Research xxx (2017) xxx–xxx
Change of sex from male to female was recorded in Limnoperna fortunei kikuchi due to the effect of environmental conditions as recorded by Abdel-Razek (1983). Also the occurrence of sequential protandric hermaphrodite with only a single sex change during life history was found in Anadara granosa (L.) (Afiati, 2007). In Malaysia, Al-Barwani et al. (2013) reported two hermaphrodite individuals out of (317) of Perna viridis during June and September. In conclusion, the hermaphrodite individual in the present study of B. pharaonis could be a type of an occasional hermaphroditism. Additional studies are important to study the reasons of B. pharaonis fast propagation in most of marine areas in the Egyptian water and the reason of presence of hermaphrodite individuals in its population.
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Please cite this article in press as: Razek, F.A.A., et al. Hermaphroditism in Brachidontes pharaonis (Fischer, 1876) (Bivalvia: Mytilidae) from the Alexandria Coast, Egypt. Egyptian Journal of Aquatic Research (2017), https://doi.org/10.1016/j.ejar.2017.10.002