Maturation and Gonad Development of Yellowspotted Puffer Torquigener flavimaculosus (Osteichthyes: Tetraodontidae) from Iskenderun Bay, North-eastern Mediterranean

Abstract

Marine pufferfish of the family Tetraodontidae accumulate the highest levels of tetrodotoxin (TTX) in the ovary. The level of TTX accumulation is reported to differ between males and females and fluctuate through gonadal development and maturation stages. Therefore, in the present work, maturation and gonad development of Yellowspotted Puffer (Torquigener flavimaculosus) from Iskenderun Bay, North-eastern Mediterranean were investigated histologically and morphologically. Mean length and weight of specimens were 12.1±0.58 cm and 20.25±0.17 g respectively. Histological examination of the gonads showed that maturation occurs in every single male T. flavimaculosus collected in summer 2017. Moreover, vitellogenic and matured oocytes were also consistently found in every female collected during the summer months. These data suggest that both sexes are reproductively active at the same time of the year. Where the spawning season for both males and females was detected in summer. T. flavimaculosus was found to be dioecious. Five and six developmental stages were indicated for testis and ovaries, respectively. The developmental pattern of ovaries was categorized as the asynchronous or group synchronous type.

Keywords

• Yellowspotted Puffer,Gametogenesis,Histology,Iskenderun Bay

References

1. Acar, C., Ishizaki, S., Nagashima Y. (2017). Toxicity of the lessepsian pufferfish Lagocephalus scleratus from eastren Mediterranean coast of Turkey and species identification by rapid PCR amplification. EuropeanFood Research Technology, 243: 49-57.
2. Alonso, D., Khalilb, Z., Satkunanthanb, N. and Livettc, BG. (2003). Drug from the sea: Conotoxins as drug leads for neuropathic pain and other neurological conditions. Mini Reviews in Medicinal Chemistry, 3: 785-787.
3. Aydın, M. (2011). Growth, reproduction and diet of Pufferfish (Lagocephalus sceleratus, Gmelin, 1789) from Turkey’s Mediterranean sea coast. Turkish Journal of Fisheries and Aquatic Sciences, 11: 569-576.
4. Azman, A. M. N., Samsur M., Othman M. (2014). Distribution of tetrodotoxin among tissues of puffer fish from Sabah and Sarawak waters. Sains Malaysiana, 43(7): 1003-1011.
5. Bilecenoğlu, M. (2003). Kızıldeniz göçmeni balon balığı (Torquigener flavimaculosus Hardy & Randall, 1983), Türkiye kıyılarından ilk gözlemler. Sualtı Dünyası Dergisi, 74: 38-39.
6. Bilecenoğlu, M. (2005). Observation on the burrowing behaviour of the Dwarf Blaasop Torquigener flavimaculosus (Osteichthyes: Tetraodontidae) along the coast of Fethiye, Turkey. Zoology in the Middle East, 35: 29-34.
7. Bragadeeswaran S., Therasa D., Prabhu K & Kathiresan K. (2010). Biomedical and pharmacological potential of tetrodotoxin-producing bacteria isolated from marine pufferfish Arothron hispidus (Muller, 1841). The Journal of Venomous Animals and Toxins Including Tropical Diseases, 16(3): 421-431.
8. Corsini-Foka, M., Margies, P., Kondilatos, G., & Economidis, P. S. (2006). Torquigener flavimaculosus Hardy and Randall, 1983 (Pisces: Tetraodontidae) off Rhodes island marine area: a new alien fish in the Hellenic waters. Mediterranean Marine Science, 7(2), 73-76.

9. Çek, S. and Turan, F. (2007). Masculinization of Convict Cichlid (Cichlosoma nigrofasciatum) by Immersion in Tribulus terrestris extract. Aquaculture International, 15: 109-119.
10. Çek, Ş. and E, Yılmaz. (2007). Gonad development and sex ratio of Sharptooth catfish (Clarias gariepinus, Burchell 1822) cultured under laboratory conditions,’’ Turkish Journal of Zoology 37, 1-12.
11. Çek, Ş, (2006). Early gonadal development and sex differentiation in rosy barb (Puntius conchonius).’’ Animal Biology, 56(3), 335-350.
12. Çek, Ş., N. Bromage, C. Randal, & K. Rana. (2001). Oogenesis, Hepatosomatic and Gonadosomatic Indexes, and Sex Ratio in Rosy barb (Puntius conchonius).’’ Turkish Journal of Fisheries and Aquatic Sciences, 1(1), 33-41.
13. El-Dayem S. M. A., Fouda F. M., Ali E. H. A. (2013). The antitumor effects of tetrodotoxin and/or doxorubicin on ehrlich ascites carcinoma-bearing female mice. Toxicology and Industrial Health, 29(5);404-417.
14. Engin, S. and Seyhan, D. (2017). A new species of Pomatoschistus (Teleostei, Gobiidae): the Mediterranean’s smallest marine fish. Journal of. Fish Biology, doi:10.1111/jfb.13455
15. Erguden, D., & Gurlek, M. (2010). The Presence of Indo-Pacific Puffer Fish Torquigener filavimaculosus Harddy & Randall, 1983 In The Iskenderun Bay, The Eastern Mediterranean Coast of Turkey. Rapp. Comm. int. Mer Médit., 39.
16. Ergüden, D., Ergüden S. A., Gürlek M. (2015). Length-weight relationships fors ix fish species in Iskenderun bay (Eastern Mediterranean Sea coast of Turkey. Journal of Applied Ichthyology, 31, 1148-1149.
17. Farrag, M. M. S., El-Haweet, A. A. K., Akel, E. A., Moustafa, M. A. (2016). Occurrence of puffer fishes (Tetraodontidae) in the eastern Mediterranean Egyptian coast-filling in the gap. BioInvasions Records, 5(1): 47-54.
18. Fouda, F. M. (2005). Anti-tumor activity of tetrodotoxin extracted from the masked puffer fish Arothron diadematus. Egyptian Journal of Biology, 7; 1-13.
19. Froese, R & Pauly, D. (2013). Fishbase. World wide web electronic publication. www.Fishbase.org,version (06/2013). Golani, D. (1987). The Red sea pufferfish, Turquigener flavimaculosus Hardy and Randall 1983. A new suez canal migrant to the eastern mediterrenean (Pisces; Tetraodontidae). Senckenbergiana Maritima, 19; 339-343.
20. Golani, D & Lerner, A. (2007). A long-term study of the sandy shore ichthyofauna in the northern red sea (gulf of aqaba) with reference to adjacent mariculture activity. The Reffles Bullettin of zoology, 14: 255-264.
21. Grier, H. J. (1981). Cellular organisationof the testis and spermatogenesis in fishes. American Zoology: 21:345-357. Ha, D. V. & Sato S. (2013). The toxicity of the fishsource made from a tetrodotoxin-bearing puffer Torquigener gloerfelti. Tap Chi Khoa Hoc vᾁ Cong nghề Biền, 13(3): 261-265.
22. Hamasaki, M., Takeuchi, Y., Miyaki, K., Yoshizaki, G. (2013). Gonadal development and fertility of triploid grass puffer Takifugu niphobles induced by cold shock treatment. Marine Biotechnology, 15: 133-144.
23. Hardy, G.S., & Randall, J. E. (1983). Description of a new species of puffer fish (Tetraodontiformes: Tetraodontidae) from the Red Sea and adjacent. Israel Journal of Zoology, 32(1): 13-20.
24. Hardy, G. S. (1983). Revision of Australian species of Torquigener whitley (Tetraodontiformes: Tetraodontidae), and two new generic names for Australian puffer fishes. Journal of the Royal Society of New Zealand, 13(112): 1-48.
25. Ikeda, K., Emoto, Y., Tatsuno, R., Wang, JJ., Ngy, L., Taniyama, S., Takatani, T., Arakawa, O. (2010). Maturation-associated changes in toxicity of the pufferfish Takifugu poecilonotus. Toxicon, 55: 289-297.
26. Itoi, S., Ishizuka, K., Mitsuoka, R., Takimoto, N., Yokoyama, N., Detake, A., Takayanagi, C., Yoshikawa, S., Sugita, H. (2016). Seasonal changes in the tetrodotoxin content of the pufferfish Takifugu niphobles. Toxicon, 14: 53-58.
27. Itoi, S., Kozaki, A., Komori, K., Tsunashima, T., Noguchi, S., Kawane, M. Sugita, H. (2015). Toxic Takifugu pardalis eggs found in Takifugu niphobles gut implications for TTX accumulations in the pufferfish. Toxicon, 108: 141-146.
28. Itoi, S., Yoshikawa, S., Tatsuno, R., Suziki, M., Asahina, K., Yamamoto, S., Takanashi, S., Takatani, T., Arakawa, O., Sakakura, Y., Sugita. H. (2012). Difference in the localization of tetrodotoxin between the female and male fish pufferfish Takifugu niphobles during spawning. Toxicon, 60: 1000-1004.
29. Jal, S. & Khora, S. S. (2015). An overview on the origin and production of tetrodotoxin a potent neurotoxin. Journal of Applied Microbiology, 119: 907-916.
30. Kiriake, A., Ohta A., Suga E.,Matsumoto T., Shoichiro I., Nagashima Y. (2016). Comparison of tetrodotoxin uptake and gene exoression in the liver between juvenile and adult tiger pufferfish, Takifugu rubripes, Toxicon. 111: 6-12. Matsunaga, T., Ieda, R., Hosoya, S., Kuroyanagi, M., Suziki, S., Suetake, H., Tasumi, S., Suzuki Y., Miyadai, T., Kikuchi, K. (2014). An efficient molecular technique for sexing tiger pufferfish (fugu) and the occurrence of sex reversal in a hatchery population. Fish Science, 80; 933-942.
31. Nouguchi, T., Arakawa, O. (2008). Tetrodotoxin; distribution and accumulation in aquatic organisms and cases of human intoxication. Marine Drugs, 6(2): 220-242.
32. Priya, K. M., & Khora, S. S. (2013). Antimicrobial, hemolytic and cytotoxic activities of the puffer fish Arothron hispidus from the Southeast coast of India. International Journal of Drug Development & Research, 5(2): 317-322.
33. Sabour, W., Saad, A., Jawad, L. (2014). First record of the yellowspotted puffer Torquigener flavimaculosus Hardy &Randall, 1983 (Osteichthys: Tetraodontidae from the Mediterranean sea coasts of Syria. Thalassia Salentina, 36: 29-34.
34. Sabrah, M. M., El-Ganainy, A. A., Zaky M. A. (2006). Biology and toxicity of the pufferfish Logocephalus sceleratus (Gmelin, 1789) from the gulf of suez. Egyptian Journal of Aquatic Research, 32(1): 283-297.
35. Thattiyaphong, A., Unahalekhaka, J., Mekha, N., Nispa, W., Kluengklangdon, P., Rojanapantip, L. (2014). Efficiency of a rapid test for detection of tetrodotoxin in pufferfish. Journal of Immunoassay and Immunochemistry, 5: 111-119.
36. Turan, C. (2010). Status and trend of lessepsian species in marine waters of Turkey. FAO EastMed. 04: 109-118.
37. Turan, F.,Çek, Ş., Atık, E (2006). Productıon of Monosex Male Guppy, Poecılıa retıculata, by 17α-Methyltestosterone. Aquaculture Research, 37(2): 200-203.
38. Turan, C., Ergüden, D., Gürlek, M., Yaglıoğlu, D., Keskin, C (2007).Lessepsian Fishes of Turkey. In: Turan C (ed), Atlas and Systematics of Marine Bony Fishes of Turkey. Nobel Publishing House, Adana, Turkey.pp 531.
39. Yin, X., Kriake, A., Ohta, A., Kitani, Y., Shizaki, S., Nagashima, Y. (2017). A novel function of vitellogenin subdomain, vWF type D, as a toxin-binding protein in the pufferfish Takifugu pardalis ovary. Toxicon, 136: 56-66.