Ultrastructure of Oocyte Development in Anemone Clownfish, Amphiprion ocellaris (Cuvier, 1830)
Abstract
Histological studied the stages of oocytes development in Amphiprion ocellaris was classified into 5 stages based on nuclear characteristics, cytoplasmic content and zona radiata layers; chromatin nucleolar (OC1) stage, perinucleolar stages (OC2), cortical alveoli and oil droplets (OC3) stage, vitellogenesis stage (OC4) and maturation stage (OC5). According to ultrastructural studied, oogonium was characterized by a large nucleus with a prominent nucleolus. The chromatin-nucleolar stage (OC1), there was cytoplasmic differentiation, with the formation of Balbiani’s body (mitochondrial cloud). The perinucleolar stage (OC2), oocyte’s nucleus contained multiple nucleoli that were located around the inner membrane of germinal vesicle envelope. Electron dense material (nuage) was usually observed close to outer membrane of germinal vesicle envelope. Cortical alveoli and oil droplets stage (OC3), oocytes were distinguished by appearance of many cortical alveoli-like vesicles and oil droplets in cytoplasm. In this stage, zona radiata was observed as a thin layer around the oocyte . In vitellogenic stage (OC4), oocytes were larger, yolk granules containing a dense homogenate material were abundant in the cytoplasm. During maturation stage (OC5), the yolk granules fused to become yolk platelets in cytoplasm and the thickness of zona radiata were greatest, and divided into zona radiata interna (ZRi) and zona radiata externa (ZRe). Key words : Amphiprion ocellaris, oocyte, transmission electron microscopyReferences
Abdalla, F.C., Cruz-landim ,C. ( 2004). Occurrence and ultrastructural characterizationof “nuage” during
oogenesis and early spermatogenesis of Piaractus mesopotamicus Holmberge, 1887 (Teleostei).
Brazilian Journal of Biology, 64, 555-556.
Aboi-Munafi, A.B., Norazmi- Lockman, N.H., Asma, N.A., Sarmiza, S., Abduh., M.Y. (2011). Histological study on
the gonad of protandrous anemonefish (Amphiprion ocellaris). Journal of Animal and Veterinary
Advance, 10, 3031-3036.
Barr, W.A. (1968). Pattern of ovarian activity. In: E.J.W. Barrington and C.B. Jorgensen (eds.): Perspective in
Endocrinology: Hormones in the livers of Lower Vertebrates. pp. 164-238. Academic press, New York.
Bazzoli, N. (1992). Ovogenese em peixes teleˆ osteos neotropicais de´ agua´ doce. Tese (Doutorado em
Ciencias)—Instituto de Ciˆ encias Biolˆ ogicas,´ Universidade Federal de Minas Gerais, Belo Horizonte,
182 pp.
Begovac, P.C, Wallace, R. A. (1987). Ovary of the pipefish, Sygnathus scovelli. Journal of Morphology, 193,
117–133.
Begovac, P.C., Wallace. R.A. (1989). Major vitelline envelope proteins in pipefish oocytes originate within the follicle and are associated with Z3 layer. Journal of Experimental Zoology, 251, 56-73.
Brusle-Sicard, S., Reinboth, R. (1990). Protandric hermaphrodite peculiarities in Amphiprion frenatus
Brevoort(Teleostei, Pomacentridae). Journal of Fish biology, 36, 383-390.
Çakıcı, Ö Üçüncü, S, I.(2007). Oocyte Development in the Zebrafish, Danio rerio (Teleostei: Cyprinidae).
Journal of Fisheries and Aquatic Sciences, 24, 137–141.
Cárdenas, R., Chávez, M., González, J.L., Aley, P., Espinosa, J., Jiménez-García, L,F. (2008). Oocyte structure
and ultrastructure in the Mexican silverside fish Chirostoma humboldtianum (Atheriniforme: Atherinopsidae). Revista de biologia tropical, 56,1371-1380.
Casadevall, M., Delgado, E., Colleye ,O., Monserrat, S.B. Parmentier, E. (2009). Histological study of the
sex-change in the skunk clownfish Amphiprion akallopisos. The Open Fish Science Journal, 2, 55-58.
Coello, š., Grimm A.S. (1990). Development of Balbiani’s vitelline body in the oocyte of the antartic mackerel,
Scomber scombrus L. Journal of Fish Biolology, 36, 265-267.
Corriero, A., Acone, F., Desantis, S., Zubani, D., Deflorio, M., Ventriglia, G., Bridges, C.R. (2004). Histological
and immunohistochemical investigation on ovarian development and plasma estradiol levels in the
swordfish (Xiphias gladius L.) European Journal of Histochemistry , 48, 413-422.
Dhaneesh, K.V., Vinoth ,R., Swagat Gosh , S., Gopi, M., Ajith Kumar, T., Balasubramanian, T. (2013). Sundaresan, J., ed. "Hatchery Production of Marine Ornamental Fishes: An Alternate Livelihood
Option for the Island Community at Lakshadweep". Climate Change and Island and Coastal
Vulnerability (Capital Publishing Company), 17, 253–265.
Dong, C. H., Yang, S. T., Yang, Z. A., Zhang, L., Gui, J. F. (2004). A C-type lectin associated and
translocated with cortical granules during oocyte maturation and egg fertilization in fish.
Developmental Biology, 265, 341–354.
Dos Santos-Silva, A.P., de Siqueira-Silva, D.H., Ninhaus-Silveira, A., Veríssimo-Silveira, R. (2015).
Oogenesis in Laetacara araguaiae (Ottoni and Costa, 2009). Zygote, 24, 502-510.
Fricke, H., Fricke S. (1977). Monogamy and sex change by aggressive dominance in coral reef fish.
Nature, 266, 830–832.
Ghosh S., Ajith Kumar; T.T., Balasubramanian, T. (2012). Determining the level of parental care
relating fanning behavior of five species of clownfishes in captivity. Indian Journal of Geo-Marine
Sciences , 41,430-441.
Gills, D.J., Mckeown, B.A., Hay, D.E. (1990). Ultrastructural observations on the ovary and eggs, and
development of eggs adhesion in pacific herring (Clupea harengus pallasi). Canadian Journal of
Fisheries and Aquatic Sciences , 47, 1495-1504.
Godwin, J.R. (1994). Histological aspects of protandrous sex change in the anemonefish Amphiprion melanopus.
Journal of Zoology (London), 232, 199-213.
Grau, A., Crespo, S., Riera, F., Pou S., Sarasquete, M.C. (1996). Oogenesis in theamberjack Seriola
dumerili Risso, 1810. A histological, histochemical and ultrastructural study of oocyte development.
Scientia Marina, 60, 391-406.
Hamlet, W.C., Jezior, M., Spieler, R, (1999). Ultrastructural analysis of folliculogenesis in the ovary of the yellow
spotted stingray Urolophus jamaicensis. Annual Anatomy, 181, 159-172.
Higashino, T., Miura, T., Miura C., Yamauchi K. (2002). Histological studies on early oogenesis in barfin flounder
(Verasper moseri). Zoological Science , 19, 557–563.
Humason, G.L. (1962). Animal tissue technique. San Francisco, W.H. Freeman. Jalabert , B. (2005). In vitro oocyte
maturation and ovulation in rainbow trout (Salmo gairdneri), northern pike (Esox Lucius), and gold fish
(Carassius auratus) . Journal of the Fisheries Research Board of Canada, 33, 974-988.
Jalabert, B. (2005). Particularities of reproduction and oogenesis in teleost fish compared to mammals.
Reproduction Nutrition Development, 45, 261-279.
Jiang, Y.Q., Zhang, T.T., Yang, W.X. (2010). Formation of zona radiata and ultrastructural analysis of egg
envelope during oogenesis of Chinese perch Siniperca chuatsi. Micron, 41, 7–14.
Kayaba, T., Takeda, N., Adachi, S., Yamauchi, K. (2001). Ultrastructure of the oocytes of the Japanese eel
Anguilla japonica during artificially induced sexual maturation. Fisheries Science, 67, 870–879.
Kaviani, E.F., Shabanipour N., Mirnategh S.B. (2013). Light and electron microscope structural study of the
zona radiata in the oocyte of zebrafish (Danio rerio). Microscopy, 62, 377–382.
Kessel, R.G. (1983). Fibrogranular bodies, annulate lamellae and polyribosomes in the dragonfly oocytes.
Journal of Morphology, 176, 171-180.
Khoo, M.L., Das, S.K., Ghaffar, M.A. (2018). Growth pattern, diet and reproductive biology of the clownfish
Amphiprion ocellaris in waters of Pulau Tioman, Malaysia. The Egyptian Journal of Aquatic Research,
44, 233-239
Koç, N.D. (2010) . Electron and light microscopic investigations of follicular epithelium in vitellogenic oocyte of
zebrafish (Danio rerio). Journal of Fisheries Sciences, 4, 144-151.
Litsios, G., Sims, C.A., Wüest, R.O., Pearman, P.B., Zimmermann, N.E., Salamin, N. (2012). Mutualism with sea
anemones triggered the adaptive radiation of clownfishes. BMC Evolutionary Biology, 2, 212-217.
Lønning, 1972. S. (1972). Comparative electron microscopic studies of teleostean eggs with special reference to
the chorion. Sarsia, 49, 4 l-48.
Ma, X.X., Zhu, J.Q., Zhou, H., Yang, W.X .(2012) The formation of zona radiata in Pseudosciaena
crocea revealed by light and transmission electron microscopy. Micron , 43, 435–444.
Matsuyama, M., Nagahama, Y., Matsuura, S. (1991). Observations on ovarian follicle ultrastructure in the
marine teleost, Pagrus major, during vitellogenesis and oocyte maturation. Aquaculture, 92, 67-82.
Miura, S., Komatsu, T.M.H., Higa, M., Bhandari, R., Nakamura, S. Nakamura, M. (2003). Gonadal sex
differentiation in protandrous anemone fish, Amphiprion clarkia. Fish Physiology and Biochemistry,
28, 165-166
Miyazaki, K., Bilinski, S.M. (2006) Ultrastructural investigation of the ovary and oogenesis in the pycnogonids
Cilunculus armatus and Ammothella biunguiculata (Pycnogonida, Ammotheidae). Invertebrate Biology,
125, 346–353.
Mourente, G., Megina, G., Diaz-Salvago E. (2002). Lipids in female northern bluefin tuna (Thunnus thynnus L.)
during sexual maturation. Fish Physiology and Biochemistry, 24, 351-363.
Murty, S.V. (2002). Marine Ornamental Fish Resources of Lakshadweep. CMFRI, 72, 1-134.
Nagahama, Y. (1983). The functional morphology of teleost gonads. In W. S. Hoar, D. J. Randall, and E. M.
Donaldson (eds.), Fish physiology, Vol. IX, Reproduction, Part A, Endocrine tissues and hormones, pp.
223–275. Academic Press, New York, USA.
Nakamura, M., Miura, S.,Nozu, R., Kobayashi, Y. (2015). Opposite-directional sex change in functional
female protandrous anemonefish, Amphiprion clarkii: effect of aromatase inhibitor on the ovarian tissue.
Zoological Letters, 1, 30-35.
Santos, J.E., Padiha, G.E.V., Bomcompagni-Júnior O., Santos, G.B., Rizzo, E., Bazzoli, N. (2006). Ovarian
follicle growth in the catfish Iheringichthys labrosus (Siluriformes: Pimelodidae). Tissue and Cell, 38,
303–310.
Shabanipour, N., Heidari, B. (2004). A histological study of the zona radiata during late oocyte developmental
stages in the Caspian sea mugilid, Liza aurata (Risso 1810). Brazilian Journal of Morphological
Scence, 21, 91-195.
Shibatta, Y., Iwamatsu, T., Oba, Y., Kobayshi, D., Tanaka, M., Nagahama, Y., Suzuki, N., Yoshikuni, M. (2000).
Identification and cDNA cloning of alveoli, an extracellular metalloproteinase, which induces chorion
hardening of medaka (Oryzias latipes) eggs upon fertilization. The Journal of Biological Chemistry,
275, 8349–8354.
Shuman, C., Hodgson, G., Ambrose, R. (2005). "Population impacts of collecting sea anemones and
anemonefish for the marine aquarium trade in the Philippines". Coral Reefs, 24, 564–573.
Selman, K., Wallace, R. A. (1986). Gametogenesis in Fundulus heteroclitus. American Zoologist, 26,
173–192.
Selman K., Wallace, R.A., Barr V. (1988). Oogenesis in Fundulus heteroclitus. V. The relationship of yolk
vescicles and cortical alveoli. Journal Experimental Zoology, 246, 42-56.
Selman, K., Wallace, R.A. (1989). Cellular aspects of oocyte growth in teleosts. Zoological Science, 6,
211-231.
Stehr, C,M., Hawkes, J.W. (1983). The development of the hexagonally structured egg envelope of the C-O
sole (Pleuronichthys coenosus). Journal of Morphology, 178, 267-284.
Taylor, M. S., Hellberg, M.E. (2003). Genetic evidence for local retention of pelagic larvae in a Caribbean reef
fish. Science, 299,107–109.
Thiry, M., Poncin, P. ( 2005). Morphological changes of the nucleolus during oogenesis in oviparous teleost fish,
Barbus barbus (L.). Journal of Structural Biology, 152,1-13.
Tworzydlo. W., Kloc, M., Bilinski, S.M. (2009). The Balbiani Body in the female germline cells of an earwig,
Opisthocosmia silvestris. Zoological Science, 26, 754-757.
Tyler, C.R., Sumpter, J.P. (1996). Oocyte growth and development in teleosts. Reviews in Fish Biology and
Fisheries, 6, 287-318.
Uribe, M. C., Grier, H. J., Parenti, L. R. (2012). Ovarian structure and oogenesis of the oviparous goodeids
Crenichthys bailey (Gilbert, 1893) and Empetrichthys latos Miller, 1948 (Teleostei, Cyprinodontiformes).
Journal of Morphology, 273, 371–387.
Wallace, R.A, Selman, K. (1981). Cellular and dynamic aspects of oocyte growth in teleosts. American Zoologist,
21, 325-343.
Yueh, W., Chang,C. (2000). Morphological changes and competence of maturing oocytes in the Protandrous
Black Porgy, Acanthopagrus schlegeli. Zoological Studies, 39, 114-122.
oogenesis and early spermatogenesis of Piaractus mesopotamicus Holmberge, 1887 (Teleostei).
Brazilian Journal of Biology, 64, 555-556.
Aboi-Munafi, A.B., Norazmi- Lockman, N.H., Asma, N.A., Sarmiza, S., Abduh., M.Y. (2011). Histological study on
the gonad of protandrous anemonefish (Amphiprion ocellaris). Journal of Animal and Veterinary
Advance, 10, 3031-3036.
Barr, W.A. (1968). Pattern of ovarian activity. In: E.J.W. Barrington and C.B. Jorgensen (eds.): Perspective in
Endocrinology: Hormones in the livers of Lower Vertebrates. pp. 164-238. Academic press, New York.
Bazzoli, N. (1992). Ovogenese em peixes teleˆ osteos neotropicais de´ agua´ doce. Tese (Doutorado em
Ciencias)—Instituto de Ciˆ encias Biolˆ ogicas,´ Universidade Federal de Minas Gerais, Belo Horizonte,
182 pp.
Begovac, P.C, Wallace, R. A. (1987). Ovary of the pipefish, Sygnathus scovelli. Journal of Morphology, 193,
117–133.
Begovac, P.C., Wallace. R.A. (1989). Major vitelline envelope proteins in pipefish oocytes originate within the follicle and are associated with Z3 layer. Journal of Experimental Zoology, 251, 56-73.
Brusle-Sicard, S., Reinboth, R. (1990). Protandric hermaphrodite peculiarities in Amphiprion frenatus
Brevoort(Teleostei, Pomacentridae). Journal of Fish biology, 36, 383-390.
Çakıcı, Ö Üçüncü, S, I.(2007). Oocyte Development in the Zebrafish, Danio rerio (Teleostei: Cyprinidae).
Journal of Fisheries and Aquatic Sciences, 24, 137–141.
Cárdenas, R., Chávez, M., González, J.L., Aley, P., Espinosa, J., Jiménez-García, L,F. (2008). Oocyte structure
and ultrastructure in the Mexican silverside fish Chirostoma humboldtianum (Atheriniforme: Atherinopsidae). Revista de biologia tropical, 56,1371-1380.
Casadevall, M., Delgado, E., Colleye ,O., Monserrat, S.B. Parmentier, E. (2009). Histological study of the
sex-change in the skunk clownfish Amphiprion akallopisos. The Open Fish Science Journal, 2, 55-58.
Coello, š., Grimm A.S. (1990). Development of Balbiani’s vitelline body in the oocyte of the antartic mackerel,
Scomber scombrus L. Journal of Fish Biolology, 36, 265-267.
Corriero, A., Acone, F., Desantis, S., Zubani, D., Deflorio, M., Ventriglia, G., Bridges, C.R. (2004). Histological
and immunohistochemical investigation on ovarian development and plasma estradiol levels in the
swordfish (Xiphias gladius L.) European Journal of Histochemistry , 48, 413-422.
Dhaneesh, K.V., Vinoth ,R., Swagat Gosh , S., Gopi, M., Ajith Kumar, T., Balasubramanian, T. (2013). Sundaresan, J., ed. "Hatchery Production of Marine Ornamental Fishes: An Alternate Livelihood
Option for the Island Community at Lakshadweep". Climate Change and Island and Coastal
Vulnerability (Capital Publishing Company), 17, 253–265.
Dong, C. H., Yang, S. T., Yang, Z. A., Zhang, L., Gui, J. F. (2004). A C-type lectin associated and
translocated with cortical granules during oocyte maturation and egg fertilization in fish.
Developmental Biology, 265, 341–354.
Dos Santos-Silva, A.P., de Siqueira-Silva, D.H., Ninhaus-Silveira, A., Veríssimo-Silveira, R. (2015).
Oogenesis in Laetacara araguaiae (Ottoni and Costa, 2009). Zygote, 24, 502-510.
Fricke, H., Fricke S. (1977). Monogamy and sex change by aggressive dominance in coral reef fish.
Nature, 266, 830–832.
Ghosh S., Ajith Kumar; T.T., Balasubramanian, T. (2012). Determining the level of parental care
relating fanning behavior of five species of clownfishes in captivity. Indian Journal of Geo-Marine
Sciences , 41,430-441.
Gills, D.J., Mckeown, B.A., Hay, D.E. (1990). Ultrastructural observations on the ovary and eggs, and
development of eggs adhesion in pacific herring (Clupea harengus pallasi). Canadian Journal of
Fisheries and Aquatic Sciences , 47, 1495-1504.
Godwin, J.R. (1994). Histological aspects of protandrous sex change in the anemonefish Amphiprion melanopus.
Journal of Zoology (London), 232, 199-213.
Grau, A., Crespo, S., Riera, F., Pou S., Sarasquete, M.C. (1996). Oogenesis in theamberjack Seriola
dumerili Risso, 1810. A histological, histochemical and ultrastructural study of oocyte development.
Scientia Marina, 60, 391-406.
Hamlet, W.C., Jezior, M., Spieler, R, (1999). Ultrastructural analysis of folliculogenesis in the ovary of the yellow
spotted stingray Urolophus jamaicensis. Annual Anatomy, 181, 159-172.
Higashino, T., Miura, T., Miura C., Yamauchi K. (2002). Histological studies on early oogenesis in barfin flounder
(Verasper moseri). Zoological Science , 19, 557–563.
Humason, G.L. (1962). Animal tissue technique. San Francisco, W.H. Freeman. Jalabert , B. (2005). In vitro oocyte
maturation and ovulation in rainbow trout (Salmo gairdneri), northern pike (Esox Lucius), and gold fish
(Carassius auratus) . Journal of the Fisheries Research Board of Canada, 33, 974-988.
Jalabert, B. (2005). Particularities of reproduction and oogenesis in teleost fish compared to mammals.
Reproduction Nutrition Development, 45, 261-279.
Jiang, Y.Q., Zhang, T.T., Yang, W.X. (2010). Formation of zona radiata and ultrastructural analysis of egg
envelope during oogenesis of Chinese perch Siniperca chuatsi. Micron, 41, 7–14.
Kayaba, T., Takeda, N., Adachi, S., Yamauchi, K. (2001). Ultrastructure of the oocytes of the Japanese eel
Anguilla japonica during artificially induced sexual maturation. Fisheries Science, 67, 870–879.
Kaviani, E.F., Shabanipour N., Mirnategh S.B. (2013). Light and electron microscope structural study of the
zona radiata in the oocyte of zebrafish (Danio rerio). Microscopy, 62, 377–382.
Kessel, R.G. (1983). Fibrogranular bodies, annulate lamellae and polyribosomes in the dragonfly oocytes.
Journal of Morphology, 176, 171-180.
Khoo, M.L., Das, S.K., Ghaffar, M.A. (2018). Growth pattern, diet and reproductive biology of the clownfish
Amphiprion ocellaris in waters of Pulau Tioman, Malaysia. The Egyptian Journal of Aquatic Research,
44, 233-239
Koç, N.D. (2010) . Electron and light microscopic investigations of follicular epithelium in vitellogenic oocyte of
zebrafish (Danio rerio). Journal of Fisheries Sciences, 4, 144-151.
Litsios, G., Sims, C.A., Wüest, R.O., Pearman, P.B., Zimmermann, N.E., Salamin, N. (2012). Mutualism with sea
anemones triggered the adaptive radiation of clownfishes. BMC Evolutionary Biology, 2, 212-217.
Lønning, 1972. S. (1972). Comparative electron microscopic studies of teleostean eggs with special reference to
the chorion. Sarsia, 49, 4 l-48.
Ma, X.X., Zhu, J.Q., Zhou, H., Yang, W.X .(2012) The formation of zona radiata in Pseudosciaena
crocea revealed by light and transmission electron microscopy. Micron , 43, 435–444.
Matsuyama, M., Nagahama, Y., Matsuura, S. (1991). Observations on ovarian follicle ultrastructure in the
marine teleost, Pagrus major, during vitellogenesis and oocyte maturation. Aquaculture, 92, 67-82.
Miura, S., Komatsu, T.M.H., Higa, M., Bhandari, R., Nakamura, S. Nakamura, M. (2003). Gonadal sex
differentiation in protandrous anemone fish, Amphiprion clarkia. Fish Physiology and Biochemistry,
28, 165-166
Miyazaki, K., Bilinski, S.M. (2006) Ultrastructural investigation of the ovary and oogenesis in the pycnogonids
Cilunculus armatus and Ammothella biunguiculata (Pycnogonida, Ammotheidae). Invertebrate Biology,
125, 346–353.
Mourente, G., Megina, G., Diaz-Salvago E. (2002). Lipids in female northern bluefin tuna (Thunnus thynnus L.)
during sexual maturation. Fish Physiology and Biochemistry, 24, 351-363.
Murty, S.V. (2002). Marine Ornamental Fish Resources of Lakshadweep. CMFRI, 72, 1-134.
Nagahama, Y. (1983). The functional morphology of teleost gonads. In W. S. Hoar, D. J. Randall, and E. M.
Donaldson (eds.), Fish physiology, Vol. IX, Reproduction, Part A, Endocrine tissues and hormones, pp.
223–275. Academic Press, New York, USA.
Nakamura, M., Miura, S.,Nozu, R., Kobayashi, Y. (2015). Opposite-directional sex change in functional
female protandrous anemonefish, Amphiprion clarkii: effect of aromatase inhibitor on the ovarian tissue.
Zoological Letters, 1, 30-35.
Santos, J.E., Padiha, G.E.V., Bomcompagni-Júnior O., Santos, G.B., Rizzo, E., Bazzoli, N. (2006). Ovarian
follicle growth in the catfish Iheringichthys labrosus (Siluriformes: Pimelodidae). Tissue and Cell, 38,
303–310.
Shabanipour, N., Heidari, B. (2004). A histological study of the zona radiata during late oocyte developmental
stages in the Caspian sea mugilid, Liza aurata (Risso 1810). Brazilian Journal of Morphological
Scence, 21, 91-195.
Shibatta, Y., Iwamatsu, T., Oba, Y., Kobayshi, D., Tanaka, M., Nagahama, Y., Suzuki, N., Yoshikuni, M. (2000).
Identification and cDNA cloning of alveoli, an extracellular metalloproteinase, which induces chorion
hardening of medaka (Oryzias latipes) eggs upon fertilization. The Journal of Biological Chemistry,
275, 8349–8354.
Shuman, C., Hodgson, G., Ambrose, R. (2005). "Population impacts of collecting sea anemones and
anemonefish for the marine aquarium trade in the Philippines". Coral Reefs, 24, 564–573.
Selman, K., Wallace, R. A. (1986). Gametogenesis in Fundulus heteroclitus. American Zoologist, 26,
173–192.
Selman K., Wallace, R.A., Barr V. (1988). Oogenesis in Fundulus heteroclitus. V. The relationship of yolk
vescicles and cortical alveoli. Journal Experimental Zoology, 246, 42-56.
Selman, K., Wallace, R.A. (1989). Cellular aspects of oocyte growth in teleosts. Zoological Science, 6,
211-231.
Stehr, C,M., Hawkes, J.W. (1983). The development of the hexagonally structured egg envelope of the C-O
sole (Pleuronichthys coenosus). Journal of Morphology, 178, 267-284.
Taylor, M. S., Hellberg, M.E. (2003). Genetic evidence for local retention of pelagic larvae in a Caribbean reef
fish. Science, 299,107–109.
Thiry, M., Poncin, P. ( 2005). Morphological changes of the nucleolus during oogenesis in oviparous teleost fish,
Barbus barbus (L.). Journal of Structural Biology, 152,1-13.
Tworzydlo. W., Kloc, M., Bilinski, S.M. (2009). The Balbiani Body in the female germline cells of an earwig,
Opisthocosmia silvestris. Zoological Science, 26, 754-757.
Tyler, C.R., Sumpter, J.P. (1996). Oocyte growth and development in teleosts. Reviews in Fish Biology and
Fisheries, 6, 287-318.
Uribe, M. C., Grier, H. J., Parenti, L. R. (2012). Ovarian structure and oogenesis of the oviparous goodeids
Crenichthys bailey (Gilbert, 1893) and Empetrichthys latos Miller, 1948 (Teleostei, Cyprinodontiformes).
Journal of Morphology, 273, 371–387.
Wallace, R.A, Selman, K. (1981). Cellular and dynamic aspects of oocyte growth in teleosts. American Zoologist,
21, 325-343.
Yueh, W., Chang,C. (2000). Morphological changes and competence of maturing oocytes in the Protandrous
Black Porgy, Acanthopagrus schlegeli. Zoological Studies, 39, 114-122.
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