Sains Malaysiana 50(1)(2021): 93-99

http://dx.doi.org/10.17576/jsm-2021-5001-10

 

Oocyte Differentiation and Reproductive Health of Solitary Tunicate (Styela plicata) from Eastern Coast of Thailand

(Pembezaan Oosit dan Kesihatan Pembiakan Tunikat Bersendirian (Styela plicata) dari Pantai Timur Thailand)

 

SENARAT, S.1, KETTRATAD, J.2, BOONYOUNG, P.3, JIRAUNGKOORSKUL, W.4, KATO, F.5, MONGKOLCHAICHANA, E.6, KANEKO, G.7 & POOLPRASERT, P.8*

 

1Department of Marine Science and Environment, Faculty of Science and Fisheries Technology, Rajamangala University of Technology Srivijaya, Trang Campus, Sikao, Trang, 92150, Thailand

 

2Department of Marine Science, Faculty of Science, Chulalongkorn University, Bangkok, 10330, Thailand

 

3Divison of Health and Applied Science, Faculty of Science, Prince of Songkla University, Songkhla, 90110, Thailand

 

4Department of Pathobiology, Faculty of Science, Mahidol University, Bangkok, 10400, Thailand

 

5Amakusa Marine Biological Laboratory, Kyushu University, Kumamoto, 863-2507, Japan

.

6Department of General Education, Faculty of Science and Health Technology, Navamindradhiraj University, Bangkok, 10300, Thailand

 

7School of Arts and Sciences, University of Houston-Victoria, 3007 N. Ben Wilson St. Victoria

Texas, 77901, USA

 

8Program of Biology, Faculty of Science and Technology, Pibulsongkram Rajabhat University, Phitsanulok, 65000, Thailand

 

Diserahkan: 1 April 2019/Diterima: 21 Jun 2020

 

Abstract

Histopathological examination is a widely acknowledged technique to assess the reproductive health of aquatic organisms, but it has never been applied to the tunicate Styela plicata, a potential indicator species of water quality. In this study, we examined the oocyte differentiation of S. plicata obtained from the eastern coast of the Gulf of Thailand in order to provide basic information for future assessment of its reproductive health. The mature gonad of S. plicata comprised several ovo-testicular convoluted tubes, in which each tube was divided into apical and terminal portions. The ovarian tissue is located in the apical part of the tunicate body and contained oocytes of various differentiation stages (asynchronous development type) consisting of the four phases namely oogonial proliferation phase, primary growth phase, secondary growth phase (secondary growth and full-growth stages), and post-ovulatory phase. Changes in the morphology of oocytes and follicular cells were described for each differentiation stage. In addition, we unexpectedly observed a high prevalence of atretic follicles (24.5%), which might indicate the oocyte damage by environmental stresses. These findings would be useful for future assessment of reproductive histology of S. plicata and other tunicate species from environmental perspectives.

 

Keywords: Ascidian; histology; reproduction; Styela plicata; Thailand

 

ABSTRAK

Pemeriksaan histopatologi adalah teknik yang telah diakui secara meluas untuk menilai kesihatan reproduktif organisma akuatik, namun teknik ini tidak pernah digunakan untuk mengenal pasti Styela plicata iaitu sejenis spesies yang berpotensi untuk menjadi penunjuk kualiti air. Dalam kajian ini, kami mengkaji pembezaan oosit S. plicata yang diperoleh dari pantai timur Thailand sebagai maklumat asas bagi penilaian tahap kesihatan reproduktif pada masa hadapan. S. plicata yang matang gonad terdiri daripada beberapa tiub berlingkar ovo-testikular dengan setiap tiub dibahagikan kepada bahagian apeks dan hujung. Tisu ovari terletak di bahagian apikal daripada badan tunikat dan mengandungi oosit daripada pelbagai peringkat pembezaan (jenis pembangunan asingkroni) yang terdiri daripada empat fasa iaitu fasa percambahan oogonial, fasa pertumbuhan primer, fasa pertumbuhan sekunder (pertumbuhan sekunder dan peringkat pertumbuhan penuh) dan fasa pasca ovulasi. Perubahan dalam morfologi oosit dan sel folikel diterangkan untuk setiap tahap pembezaan. Di samping itu, kami secara tidak sengaja telah mencerap prevalensi folikel atretik yang tinggi (24.5%), yang mungkin menunjukkan kerosakan oosit oleh tekanan daripada alam sekitar. Penemuan ini dapat digunakan untuk penilaian masa akan datang mengenai histologi pembiakan S. plicata dan spesies tunikat yang lain daripada perspektif alam sekitar.

 

Kata kunci: Askidia; histologi; pembiakan; Styela plicata; Thailand

 

RUJUKAN

Adams, S.M. 2002. Biological indicators of aquatic ecosystem stress. American Fisheries Society 3: 104-112.

Anderson, E. & Albertini, D.F. 1976. Gap junctions between the oocyte and companion follicle cells in the mammalian ovary. Journal of Cell Biology 71: 680-686.

Bancroft, J.D. & Gamble, M. 2002. Theory and Practice of Histological Techniques. London: Churchill Livingstone.

Bawab, F.A.E., Michael, M.I.M., Khalil, S.H. & Saad, G.A. 2012. Studies on the reproductive and nervous systems of the protochordate Styela plicata (Lesueur, 1823) to correlate the nervous activity on reproduction. The Egyptian Journal of Aquatic Research 38: 125-145.

Bellante, A., Piazzese, D., Cataldo, S., Parisi, M.G. & Cammarata, M. 2016. Evaluation and comparison of trace metals accumulation indifferent tissues of potential bioindicator organisms: Macrobenthic filter feeders Styela plicata, Sabella spallanzanii and Mytilus galloprovincialis. Environmental Toxicology and Chemistry 35(12): 3062-3070.

Blazer, V.S. 2002. Histopathological assessment of gonadal tissue in wild fishes. Fish Physiology and Biochemistry 26: 85-101.

Chen, Y.T. & Dai, C.F. 1998. Sexual reproduction of the ascidian Polycarpa cryptocarpa kroboja from the northern coast of Taiwan. Acta Oceanogr Taiwan 37: 201-210.

Choi, Y., Lee, C., Rho, S. & Lee, Y. 2004. Reproductive cycle and spawning rhythm of the ascidian, Halocynthia hilgendorfi ritteri. Korean Journal of Biological Science 8: 33-40.

Cloney, R.A. 1990. Reproductive Biology of Invertebrates. New Delhi: Oxford & IBH Publishing.

Das, B.M. 1936. On the structure and function of the ascidian test. Journal of Morphology 69: 589-601.

Di Bella, M.A., Fedders, H., De Leo, G. & Leippe, M. 2011. Localization of antimicrobial peptides in the tunic of Ciona intestinalis (Ascidiacea, Tunicata) and their involvement in local inflammatory-like reactions. Results in Immunology 1(1): 70-75.

Dietrich, D.R. & Krieger, H.O. 2009. Histological Analysis of Endocrine Disruptive Effects in Small Laboratory Fish. New Jersey: John Wiley & Sons.

Endean, R. 1960. The blood cells of the ascidian, Phallrrsia ttzattlmillafa.Journal of Microscopical Science 101: 177-197.

Endean, R. 1955. Studies on the blood and test of some Australian ascidians. 11. The test of Pyrira sfolonifrra (Heller). Australian Journal of Marine and Freshwater Research 6: 139-156.

Fatma, A.S.M. 2009. Histopathological studies on Tilapia zillii and Solea vulgaris from Lake Qarun, Egypt. World Journal of Fish and Marine Science 1: 29-39.

Hamaguchi, S. 1993. Alterations in the morphology of nuages in spermatogonia of the fish, Oryzias latipes, treated with puromycin and actinomycin D. Reproduction Nutrition Development 33: 137-141.

Hinton, D.E., Segner, H. & Braunback, T. 2001. Toxic response of liver. In Target Organ Toxicity in Marine and Fresh Water Teleosts, edited by Shlenk, D. & Benson, W.H. London: CRC Press. pp. 224-268.

Honegger, T.G. 1986. Fertilization in ascidians: Studies on the egg envelop, sperm and gamete interaction in Phallusis mammillata. Developmental Biology 118(1): 118-128.

Johnson, R., Wolf, J. & Braunbeck, T. 2009. OECD Guidance document for the diagnosis of endocrine-related histopathology of fish gonads. Organisation for Economic Co-operation and Development, France.

Kawamura, K., Tiozzo, S., Manni, L., Sunanaga, T., Burighel, P. & De Tomaso, A.W. 2011. Germline cell formation and gonad regeneration in solitary and colonial ascidians. Developmental Dynamics 240: 299-308.

Kessel, R.G. 1983. Urochordata-Ascidiacea. In Reproductive Biology of Invertebrates, Vol. 1. edited by Adiyodi, K.G. & Adiyodi, R.G. New York: Wiley. pp. 655-734.

Kessel, R.G. 1966. Ultrastructure and relationships of ooplasmic components in tunicates. Acta Embryologiae et Morphologiae Experimentalis 9: 1-24.

Manni, L., Zaniolo, G. & Burighel, P. 1995. Oogenesis and oocyte envelope differentiation in the viviparous ascidian Botrylloides violaceus. Invertebrate Reproduction and Development 27: 167-180.

Manni, L., Zaniolo, G. & Burighel, P. 1994. An unusual membrane system in the oocyte of the ascidian Botryllus schlosseri. Tissue Cell 26: 212-222.

Manni, L., Zaniolo, G. & Burighel, P. 1993. Ultrastructural study of oogenesis in the compound ascidian Botryllus schlosseri (Tunicata). Acta Zoologica (Stockh) 75: 101-113.

Mayer, I., Shackley, S.E. & Rylan, J.S. 1988. Aspects of the reproductive biology of the bass, Dicentrarchus labrax L. A histological and histochemical study of oocyte development. Journal of Fish Biology 33: 609-622.

Mukai, H. 1977. Comparative studies on the structure of reproductive organs of four botryllid ascidians. Journal of Morphology 152: 363-380.

Mukai, H. & Watanabe, H. 1976. Studies on the formation of germ cells in a compound ascidian Botryllus primigenus Oka. Journal of Morphology 148: 337-362.

Mukai, H., Saito, Y. & Watanabe, H. 1987. Viviparous development in Botrylloides (compound ascidians). Journal of Morphology 193: 263-276.

Ogura, Y. & Sasakura, Y. 2013. Ascidians as excellent models for studying cellular events in the chordate body plan. Biological Bulletin 224: 227-236. 

Reverberi, G. 1971. Ascidians. In Experimental Embryology of Marine and Fresh-Water Invertebrates, edited by Reverberi, G. Amsterdam: North-Holland Publishing Co. pp. 507-550.

Sabbadin, A., Burighel, P. & Zaniolo, G. 1992. Some aspects of reproduction in ascidians. In Selected Symposia and Monographs, edited by Dallai, R. Modena: Mucchi. pp. 251-265.

Satoh, N. 1994. Developmental Biology of Ascidians. New York: Cambridge University Press.

Spanò, L., Tyler, C.R., van Aerle, R., Devos, P., Mandiki, S.N., Silvestre, F., Thomé, J.P. & Kestemont, P. 2004. Effects of atrazine on sex steroid dynamics, plasma vitellogenin concentration and gonad development in adult goldfish (Carassius auratus). Aquatic Toxicology 66: 369-379.

Sugino, Y.M., Tominaga, A., Takashima, Y. & Ishikawa, M. 1990. Early oogenesis in the ascidian Ciona savignyi. Invertebrate Reproduction and Development 17: 165-170.

Thongra-ar, W., Musika, C., Wongsudawan, W. & Munhapol, A. 2008. Heavy metals contamination in sediments along the eastern coast of the gulf of Thailand. Environment Asia 1: 37-45.

Tillitt, D.E., Papoulias, D.M., Whyte, J.J. & Richter, C.A. 2010. Atrazine reduces reproduction in fathead minnow (Pimephales promelas). Aquatic Toxicology 99: 149-159.

Tyler, C.R. & Sumpter, J.P. 1996. Oocyte growth and development in teleosts. Reviews in Fish Biology and Fisheries 6: 287-318.

Villa, L. & Patricolo, E. 2000. The follicle cells of Styela plicata (Ascidiacea, Tunicata): A SEM study. Zoological Science 17: 1115-1121.

Wallace, R.A. & Selman, K. 1990. Ultrastructural aspects of oogenesis and oocyte growth in fish and amphibians. Journal of Electron Microscopy Technique 16: 175-201.

Wallace, R.A. & Selman, K. 1981. Cellular and dynamic aspects of oocyte growth in teleost. American Zoologist 21: 325-343.

West, G. 1990. Methods of assessing ovarian development in fishes: A review. Journal of Marine and Freshwater Research 41: 199-222.

Zaniolo, G. 1981. Histology of the ascidian Botryllus schlosseritunic: In particular, the test cells. Bolletino di Zoologia 48: 169-178.

Zaniolo, G., Burighel, P. & Martinucci, G.B. 1987. Ovulation and placentation in Botryllus schlosseri (Ascidiacea): An ultrastructural study. Canadian Journal of Zoology 65: 1181-1190.

 

*Pengarang untuk surat-menyurat; email: poolprasert_p@psru.ac.th

   

 

sebelumnya