Cell and Tissue Research
Cell TissueRes. 201,361-368 (1979)
9 by Springer-Verlag 1979
Ultrastructural Observations on the Oogenesis of Triops cancriformis (Crustacea, Notostraca) II. Early Developmental Stages of the Oocyte Franca Sabelli Scanabissi and Massimo Trentini Institute of Zoology,Universityof Bologna,Italy
Summary. The first stages of the oogenesis of Triops cancriformis have been studied. At the outset the oocyte is smaller than the nurse cells. Meiosis begins with typical synaptonemal complexes. The significance of these complexes and of some other peculiar structures of germ cells, i.e., pore complexes and annuli within the nucleus, and annulate lamellae within the cytoplasm are discussed. The morphofunctional uniformity of some cytoplasmic structures (annulate lamellae, concentrically arranged ER, and yolk globules) in the oocyte as well as its nurse cells is also discussed. Key words: Oogenesis - Synaptonemal complexes - A n n u l a t e lamellae Notostraca (Triops cancriformis). The early stages in the oogenesis of Branchiopoda have been studied ultrastructurally in only two rather unrelated species, Artemia salina andDaphnia magna. The different morphofunctional features of the oogenesis of Artemia have been investigated by Anteunis (1965) and Anteunis et al. (1964, 1966a, b,c, 1968). Zaffagnini and Lucchi (1965) found intercellular bridges connecting the oocyte with its three nurse cells in Diphnia. Owing to the primitive morphological features of Notostraca as compared with other Branchiopoda (F16ssner, 1972; Wingstrand, 1978) we undertook a study of the oogenesis of Triops cancriformis with the aim of clarifying its phyletic position. In the first part of our study we examined the origin and differentiation of nurse cells (Trentini and Sabelli Scanabissi, 1978). In the present contribution the development of the oocyte during the same time period will be discussed. It is peculiar of Notostraca that the nurse cells develop more rapidly and are thus responsible for follicle growth. In the other Branchiopoda the increase in follicle size is due to oocyte growth only.
Send offprint requests to: Dr. F. Sabelli Scanabissi, Istituto di Zoologia, Via S. Giacomo 9, 1-40126 Bologna,Italy
0302-766X/79/0201/0361/$01.60
362
F. Sabelli Scanabissi and M. Trentini
Diameter of the oocyte Stage I
7.2+ 1 4 . 3
Stage II
9.7+ 18.9
Remarks
synaptonemal complexes
nucleolar increase concentric membranes ER
Stage Ill
20.4+ 40.5 pore complexesannuli - annulate lamellae vitellogenesis start
Stage IV
27.8+ 58.1
. - 9 ........J, . :,,, .o . i
Fig. 1. Scheme of early developmental stages of Triopscancriformisoocyte. Four stages determined on basis of nurse cell growth (Trentini and Sabelli Scanabissi, 1978)
Materials and Methods Materials and methods are the same as those reported in the preceding paper (Trentini and Sabelli Scanabissi, 1978). The four early stages of oocyte development are summarized in Figure 1.
Results I n the g e r m i n a l zone o f Triops cancriformis the o o g o n i a u n d e r g o two mitoses with i n c o m p l e t e cytokinesis, so t h a t four-celled units (one o o c y t e a n d three nurse cells, i n t e r c o n n e c t e d b y c y t o p l a s m i c bridges) are p r o d u c e d ; these units are the o v a r i a n follicles (Fig. 2). I n these follicles the oocyte nucleus is recognizable b y the presence o f o n l y one nucleolus; by c o n t r a s t the nurse cells have several nucleoli (Trentini a n d Sabelli Scanabissi, 1978). This difference will be m a i n t a i n e d in s u b s e q u e n t stages. A f t e r mitosis the o o c y t e u n d e r g o e s meiosis (stage I - Fig. 3); in fact s y n a p t o n e m a l c o m p l e x e s (SC) with the usual p a t t e r n ( W e s t e r g a a r d a n d v o n Wettstein, 1972, for review) b e c o m e visible in the nucleus. The central region o f SC is 900 A wide a n d l a t e r a l elements 300 A. It is interesting to r e m a r k t h a t the bivalents are a n c h o r e d to the n u c l e a r envelope; the l a t t e r b e c o m e s slightly i n d e n t e d at the insertion zone
Fig. 2. Germinal area showing oogonial mitosis (upper left) and follicle cells (stage I); three of the four cells interconnected by cytoplasmic bridges (arrows, at right). NC nurse cell. • 4700 Fig. 3. Stage I. Oocyte nucleus (NO) during meiotic prophase (pachytene) with nucleolus (no) and synaptonemal complexes. • 21,300 Fig. 4. Detail of Fig. 3. Note anchorage between one bivalent and nuclear envelope (ne). x 44,500
364
F. Sabelli Scanabissi and M. Trentini
Fig. 5. Stage II. Oocyte nucleolus (no) larger than that of stage I (compare with Fig. 3). At right, nurse cell (NC) with several nucleoli. O oocyte. • 7600. Inset: concentrically arranged ER. • 8100
(Fig. 4). The nucleolus persists during meiotic prophase. The first stage is also characterized by a high N/C ratio, by elongated mitochondria with dense matrix and thin cristae, by scarce ER, and a great number of associated and free ribosomes that give the cytoplasm a dark appearance (Fig. 3). At this stage the cytoplasm of the oocyte does not show any peculiar features compared to that of nurse cells. The nurse cells show a three-fold or four-fold increase in size during stage II; the oocyte on the contrary shows only a small increase, about 1/3 (Fig. 1). The oocyte nucleus maintains the same size and shows a slightly corrugated envelope: the nucleolus grows to four times its original size (Fig. 5). Several groups of concentrically arranged membranes are present in the oocyte cytoplasm (Fig. 5), similar to those found in nurse cells (Trentini and Sabelli Scanabissi, 1978). Figs. 6-10. Stages III and IV
Fig. 6. Oocyte nucleus with several pores (arrows), scattered chromatin, and nucleolus (no). Cytoplasm shows yolk globules (y) and endoplasmic reticulum (er). x 7200 Fig.7. Pore complexes (arrows) of oocyte's nuclear envelope. NO oocyte nucleus; C cytoplasm. x 13,150 Fig. 8. Group of annuli in oocyte nucleus. Note dense matrix surrounding annuli and granules within some of them; ne nuclear envelope, x 44,400 Fig. 9. Complex of annulate lamellae in oocyte cytoplasm. Note ribosomes associated with lateral cisternae (arrows). x 30,600 Fig. 10. Different-sized yolk globules (Y) surrounded by membranes of ER. x 10,700
Oocyte Development in Triops cancriformis
365
366
F. SabelliScanabissiand M. Trentini
The size of the oocyte and that of its nucleus increase conspicuously in subsequent stages (III, IV - Fig. 1). The corresponding nucleolus maintains the same size (Fig. 6). The nucleoplasm has a granulated appearance and shows small scattered chromatin masses (Figs. 6, 7). The nuclear envelope displays many pore complexes (Franke, 1974); these are regularly spaced and have a constant 600A diameter (Fig. 7). Groups of annuli with the same pore complex diameter are seen in the nucleoplasm. The arrays of annuli, each frequently containing a granule within, are included in a matrix denser than the surrounding nucleoplasm; they are very frequently found near the nuclear envelope and are made up of up to 40 units (Fig. 8). Groups of evenly arranged annulate lamellae (AL) are recognizable in the cytoplasm of the oocyte. The AL consist of numerous layers (up to 20) of paired annulated membranes with dense interposed matrix, simmetrically aligned and regularly spaced. Their lateral ends are frequently dilated to form cisternae more or less studded with ribosomes (Fig. 9). We have found AL, with the same frequency, in the cytoplasm of nurse cells. Another cytoplasmic feature of oocytes at these stages (III, IV) are several dark yolk globules of different sizes (up to 4 g). These globules are always surrounded by one or more layers of ER membranes (Fig. 10); the latter are probably residues of the concentric membrane whorls found in stage II. The yolk of oocytes is morphologically very similar to that of nurse cells (Trentini and Sabelli Scanabissi, 1978). Further aspects of vitellogenesis and of the development of the ovarian follicle will be considered in a subsequent study.
Discussion
The gradual increase in oocyte size, during stages II, III, IV, results in a germ cell that is still smaller than the nurse cells. However, the cytoplasmic activity of the four follicle cells continues side by side. In fact, the oocyte and its three nurse cells produce yolk with the same morphology and localization. Moreover, they show complexes of cytoplasmic AL. AL have thus far been observed in Crustacea by Ruthmann (1958), Kaye et al. (1961), Moses (1964) and Kessel (1968) in crayfish spermatocytes; by Anteunis (1965), Kessel (1968), Kessel and Beams (1968) in brine shrimp, lobster and crayfish oocytes, and by Herold et al. (1976) in hindgut of two species of Isopoda. The occurrence of cytoplasmic AL in every follicle cell of Triops cancriformis might indicate a high metabolic rate as suggested by Kessel (1968); they may be derived from the pore complexes and annuli within the nucleus (see Wischnitzer, 1970 and Maul, 1977, for reviews). According to the thesis of Wischnitzer (1970) the presence of ribosomes associated with the outermost membranes of AL suggests that the cisternae of RER arise from AL complexes. This possibility is strongly suggested in Triops caneriformis by the occurrence of AL following the decrease of concentric ER. With regard to nuclear activity, the presence of SC (stage I) shows that the oocyte undergoes meiosis, while the nurse cells do not. SC were thus far found in Crustacea only in spermatocytes (Moses, 1956; Comings et al., 1970; Wingstrand, 1972; Dudley, 1973), never in oocytes. The occurrence of SC in Triops cancriformis oocytes seems related to its reproductive biology. In fact, the specimens studied
Oocyte Development in Triops cancriformis
367
belong to maleless populations (absence of males is very frequent in Branchiopoda), so that the females studied probably reproduce by parthenogenesis. The occurrence of SC indicates this parthenogenesis as being meiotic, and confirms ultrastructurally the karyologic data of Longhurst (1955) and Trentini (1976). In conclusion, our observations on the early developmental stages of Triops cancriformis oocytes show that they have a morphofunctional uniformity with their nurse cells, i.e., concentrically arranged ER (stage II), and yolk globules and AL (stages III, IV). This uniformity of the four follicle cells is probably related to the persistence of intercellular bridges. This and the common origin of the four-celled follicle, corroborate our view that the nurse cells are abortive oocytes. In substance, what distinguishes the true oocyte from its sister cells, in the early stages, is the meiotic process and its slow rate of growth. References Anteunis, A.: Les membranes annel6es dans l'oeuf d'Artemia salina, l~tude de microscopie 61ectronique. Compt. Rend. Assoc. Anat. 124, 168-172 (1965) Anteunis, A., Fautrez-Firlefyn, N., Fautrez, J., Lagasse, A.: L'ultrastructure du noyau vitellin de l'oeuf d'Artemia salina. Exp. Cell Res. 35, 239-247 (1964) Anteunis, A., Fautrez-Firlefyn, N., Fautrez, J.: Apropos d'un complexe tubulo-mitochondrial ordonn6 dans le jeune oocyte d'Artemia saline. J. Ultrastruct. Res. 15, 122-130 (1966a) Anteunis, A., Fautrez-Firlefyn, N., Fautrez, J.: La structure des ponts intercellulaires "obtur6s" et "ouverts" entre oogonies et oocytes d'Artemia salina. Arch. Biol. (Li6ge) 77, 645-664 (1966b) Anteunis, A., Fautrez-Firlefyn, N., Fautrez, J.: L'incorporation de cellules nourricieres par l'oocyte d'Artemia salina, t~tude au microscope ~lectronique. Arch. Biol. (Li+ge) 77, 665-676 (1966c) Anteunis, A., Fautrez-Firlefyn, N., Fautrez, J.: Ultrastructure du nucl6ole expuls6 dans le cytoplasm de l'oocyte d'Artemia salina. C. R. Acad. Sci. (Paris) 266, 1862-1863 (1968) Comings, D.E., Okada, T.A.: Whole mount electron microscopy of meiotic chromosomes and the synaptonemal complex. Chromosoma (Berl.) 30, 269-286 (1970) Dudley, P.L.: Synaptonemal polycomplexes in spermatocytes of the gooseneck barnacle, Poelicipes polymerus Sowerby (Crustacea, Cirripedia). Chromosoma (Berl.) 40, 221-242 (1973) Fl6ssner, D.: Krebstiere, Crustacea. Kiemen- und Blattffisser, Branchiopoda. Fischl/iuse, Branchiura. Die Tierwelt Deutschlands 60, 1-501 (1972) Franke, W.W.: Structure, biochemistry, and functions of the nuclear envelope. Int. Rev. Cytol., Suppl. 4, 71-236 (1974) Herold, L., Goggins, J.A., Witkus, E.R., Vernon, G.M.: Annulate lamellae in hindgut epithelial cells of Isopoda. Protoplasma 87, 291-296 (1976) Kaye, G.I., Pappas, G.D., Yasuzumi, G., Yamamoto, H.: The distribution and form of the endoplasmic reticulum during spermatogenesis in the crayfish Carnbaroidesjaponicus. Z. Zellforsch. 53, 159-171 (1961) Kessel, R.G.: Annulate lamellae. J. ULtrastruct. Res., Suppl. 10, 5-82 (1968) Kessel, R.G., Beams, H.W.: Intranucleolar membranes and nuclear cytoplasmic exchange in young crayfish oocytes. J. Cell Biol. 39, 735-741 (1968) Longhurst, A.R.: The reproduction and cytology of the Notostraca (Crustacea, PhyUopoda). Proc. Zool. Soc. London 125, 671-680 (1955) Maul, G.G. : The nuclear and the cytoplasmic pore complex: structure, dynamics, distribution, and evolution. Int. Rev. Cytol., Suppl. 6, 75-186 (1977) Moses, MJ.: Chromosomal structures in crayfish spermatocytes. J. Biophys. Biochem. Cytol. 2, 215218 (1956) Moses, M.J.: The nucleus and chromosomes: a cytological study. In: Cytology and Cell Physiology. (G. Bourne, ed.) New York: Academic Press 1964 Ruthmann, A.: Basophilic lamellar systems in the crayfish spermatocyte. J. Biophys. Biochem. Cytol. 4, 267-274 (1958)
368
F. Sabelli Scanabissi and M. Trentini
Trentini, M.: Karyologic observations on Triops cancriformis (Phyllopoda, Notostraca). Boll. Zool. 43, 321-322 (1976) Trentini, M., Sabelli Scanabissi, F.: Ultrastructural observations on the oogenesis of Triops cancriformis (Crustacea, Notostraca). I. Origin and differentiation of nurse ceils. Cell Tissue Res. 194, 71-77 (1978) Westergaard, M., yon Wettstein, D.: The synaptonemal complex. Ann. Rev. Gen. 6, 71-110 (1972) Wingstrand, K.G.: Comparative spermatology of a pentastomid, Raillietiella hemidactyli, and a branchiuran crustacean Argulus foliaceus, with a discussion of pentastomid relationship. Kongl. Danske Vid. Selskab. Biolog. Skr. 19, 1 72 (1972) Wingstrand, K.G.: Comparative spermatology of the Crustacea Entomostraca. 1. Subclass Branchiopoda. Kongl. Danske Vid. Selskab. Biolog. Skr. 22, 1-66 (1978) Wischnitzer, S.: The annulate lamellae. Int. Rev. Cytol. 27, 65-100 (1970) Zaffagnini, F., Lucchi, M.L.: Indagini col microscopio elettronico sull'ovogenesi partenogenetica in Daphnia magna (Crustacea: Cladocera). I. Origine comune delrovocita e delle sue tre cellule nutrici. Arch. Zool. Ital. 50, 49-58 (1965)
Accepted May 3, 1979
Cell TissueRes. 201,361-368 (1979)
9 by Springer-Verlag 1979
Ultrastructural Observations on the Oogenesis of Triops cancriformis (Crustacea, Notostraca) II. Early Developmental Stages of the Oocyte Franca Sabelli Scanabissi and Massimo Trentini Institute of Zoology,Universityof Bologna,Italy
Summary. The first stages of the oogenesis of Triops cancriformis have been studied. At the outset the oocyte is smaller than the nurse cells. Meiosis begins with typical synaptonemal complexes. The significance of these complexes and of some other peculiar structures of germ cells, i.e., pore complexes and annuli within the nucleus, and annulate lamellae within the cytoplasm are discussed. The morphofunctional uniformity of some cytoplasmic structures (annulate lamellae, concentrically arranged ER, and yolk globules) in the oocyte as well as its nurse cells is also discussed. Key words: Oogenesis - Synaptonemal complexes - A n n u l a t e lamellae Notostraca (Triops cancriformis). The early stages in the oogenesis of Branchiopoda have been studied ultrastructurally in only two rather unrelated species, Artemia salina andDaphnia magna. The different morphofunctional features of the oogenesis of Artemia have been investigated by Anteunis (1965) and Anteunis et al. (1964, 1966a, b,c, 1968). Zaffagnini and Lucchi (1965) found intercellular bridges connecting the oocyte with its three nurse cells in Diphnia. Owing to the primitive morphological features of Notostraca as compared with other Branchiopoda (F16ssner, 1972; Wingstrand, 1978) we undertook a study of the oogenesis of Triops cancriformis with the aim of clarifying its phyletic position. In the first part of our study we examined the origin and differentiation of nurse cells (Trentini and Sabelli Scanabissi, 1978). In the present contribution the development of the oocyte during the same time period will be discussed. It is peculiar of Notostraca that the nurse cells develop more rapidly and are thus responsible for follicle growth. In the other Branchiopoda the increase in follicle size is due to oocyte growth only.
Send offprint requests to: Dr. F. Sabelli Scanabissi, Istituto di Zoologia, Via S. Giacomo 9, 1-40126 Bologna,Italy
0302-766X/79/0201/0361/$01.60
362
F. Sabelli Scanabissi and M. Trentini
Diameter of the oocyte Stage I
7.2+ 1 4 . 3
Stage II
9.7+ 18.9
Remarks
synaptonemal complexes
nucleolar increase concentric membranes ER
Stage Ill
20.4+ 40.5 pore complexesannuli - annulate lamellae vitellogenesis start
Stage IV
27.8+ 58.1
. - 9 ........J, . :,,, .o . i
Fig. 1. Scheme of early developmental stages of Triopscancriformisoocyte. Four stages determined on basis of nurse cell growth (Trentini and Sabelli Scanabissi, 1978)
Materials and Methods Materials and methods are the same as those reported in the preceding paper (Trentini and Sabelli Scanabissi, 1978). The four early stages of oocyte development are summarized in Figure 1.
Results I n the g e r m i n a l zone o f Triops cancriformis the o o g o n i a u n d e r g o two mitoses with i n c o m p l e t e cytokinesis, so t h a t four-celled units (one o o c y t e a n d three nurse cells, i n t e r c o n n e c t e d b y c y t o p l a s m i c bridges) are p r o d u c e d ; these units are the o v a r i a n follicles (Fig. 2). I n these follicles the oocyte nucleus is recognizable b y the presence o f o n l y one nucleolus; by c o n t r a s t the nurse cells have several nucleoli (Trentini a n d Sabelli Scanabissi, 1978). This difference will be m a i n t a i n e d in s u b s e q u e n t stages. A f t e r mitosis the o o c y t e u n d e r g o e s meiosis (stage I - Fig. 3); in fact s y n a p t o n e m a l c o m p l e x e s (SC) with the usual p a t t e r n ( W e s t e r g a a r d a n d v o n Wettstein, 1972, for review) b e c o m e visible in the nucleus. The central region o f SC is 900 A wide a n d l a t e r a l elements 300 A. It is interesting to r e m a r k t h a t the bivalents are a n c h o r e d to the n u c l e a r envelope; the l a t t e r b e c o m e s slightly i n d e n t e d at the insertion zone
Fig. 2. Germinal area showing oogonial mitosis (upper left) and follicle cells (stage I); three of the four cells interconnected by cytoplasmic bridges (arrows, at right). NC nurse cell. • 4700 Fig. 3. Stage I. Oocyte nucleus (NO) during meiotic prophase (pachytene) with nucleolus (no) and synaptonemal complexes. • 21,300 Fig. 4. Detail of Fig. 3. Note anchorage between one bivalent and nuclear envelope (ne). x 44,500
364
F. Sabelli Scanabissi and M. Trentini
Fig. 5. Stage II. Oocyte nucleolus (no) larger than that of stage I (compare with Fig. 3). At right, nurse cell (NC) with several nucleoli. O oocyte. • 7600. Inset: concentrically arranged ER. • 8100
(Fig. 4). The nucleolus persists during meiotic prophase. The first stage is also characterized by a high N/C ratio, by elongated mitochondria with dense matrix and thin cristae, by scarce ER, and a great number of associated and free ribosomes that give the cytoplasm a dark appearance (Fig. 3). At this stage the cytoplasm of the oocyte does not show any peculiar features compared to that of nurse cells. The nurse cells show a three-fold or four-fold increase in size during stage II; the oocyte on the contrary shows only a small increase, about 1/3 (Fig. 1). The oocyte nucleus maintains the same size and shows a slightly corrugated envelope: the nucleolus grows to four times its original size (Fig. 5). Several groups of concentrically arranged membranes are present in the oocyte cytoplasm (Fig. 5), similar to those found in nurse cells (Trentini and Sabelli Scanabissi, 1978). Figs. 6-10. Stages III and IV
Fig. 6. Oocyte nucleus with several pores (arrows), scattered chromatin, and nucleolus (no). Cytoplasm shows yolk globules (y) and endoplasmic reticulum (er). x 7200 Fig.7. Pore complexes (arrows) of oocyte's nuclear envelope. NO oocyte nucleus; C cytoplasm. x 13,150 Fig. 8. Group of annuli in oocyte nucleus. Note dense matrix surrounding annuli and granules within some of them; ne nuclear envelope, x 44,400 Fig. 9. Complex of annulate lamellae in oocyte cytoplasm. Note ribosomes associated with lateral cisternae (arrows). x 30,600 Fig. 10. Different-sized yolk globules (Y) surrounded by membranes of ER. x 10,700
Oocyte Development in Triops cancriformis
365
366
F. SabelliScanabissiand M. Trentini
The size of the oocyte and that of its nucleus increase conspicuously in subsequent stages (III, IV - Fig. 1). The corresponding nucleolus maintains the same size (Fig. 6). The nucleoplasm has a granulated appearance and shows small scattered chromatin masses (Figs. 6, 7). The nuclear envelope displays many pore complexes (Franke, 1974); these are regularly spaced and have a constant 600A diameter (Fig. 7). Groups of annuli with the same pore complex diameter are seen in the nucleoplasm. The arrays of annuli, each frequently containing a granule within, are included in a matrix denser than the surrounding nucleoplasm; they are very frequently found near the nuclear envelope and are made up of up to 40 units (Fig. 8). Groups of evenly arranged annulate lamellae (AL) are recognizable in the cytoplasm of the oocyte. The AL consist of numerous layers (up to 20) of paired annulated membranes with dense interposed matrix, simmetrically aligned and regularly spaced. Their lateral ends are frequently dilated to form cisternae more or less studded with ribosomes (Fig. 9). We have found AL, with the same frequency, in the cytoplasm of nurse cells. Another cytoplasmic feature of oocytes at these stages (III, IV) are several dark yolk globules of different sizes (up to 4 g). These globules are always surrounded by one or more layers of ER membranes (Fig. 10); the latter are probably residues of the concentric membrane whorls found in stage II. The yolk of oocytes is morphologically very similar to that of nurse cells (Trentini and Sabelli Scanabissi, 1978). Further aspects of vitellogenesis and of the development of the ovarian follicle will be considered in a subsequent study.
Discussion
The gradual increase in oocyte size, during stages II, III, IV, results in a germ cell that is still smaller than the nurse cells. However, the cytoplasmic activity of the four follicle cells continues side by side. In fact, the oocyte and its three nurse cells produce yolk with the same morphology and localization. Moreover, they show complexes of cytoplasmic AL. AL have thus far been observed in Crustacea by Ruthmann (1958), Kaye et al. (1961), Moses (1964) and Kessel (1968) in crayfish spermatocytes; by Anteunis (1965), Kessel (1968), Kessel and Beams (1968) in brine shrimp, lobster and crayfish oocytes, and by Herold et al. (1976) in hindgut of two species of Isopoda. The occurrence of cytoplasmic AL in every follicle cell of Triops cancriformis might indicate a high metabolic rate as suggested by Kessel (1968); they may be derived from the pore complexes and annuli within the nucleus (see Wischnitzer, 1970 and Maul, 1977, for reviews). According to the thesis of Wischnitzer (1970) the presence of ribosomes associated with the outermost membranes of AL suggests that the cisternae of RER arise from AL complexes. This possibility is strongly suggested in Triops caneriformis by the occurrence of AL following the decrease of concentric ER. With regard to nuclear activity, the presence of SC (stage I) shows that the oocyte undergoes meiosis, while the nurse cells do not. SC were thus far found in Crustacea only in spermatocytes (Moses, 1956; Comings et al., 1970; Wingstrand, 1972; Dudley, 1973), never in oocytes. The occurrence of SC in Triops cancriformis oocytes seems related to its reproductive biology. In fact, the specimens studied
Oocyte Development in Triops cancriformis
367
belong to maleless populations (absence of males is very frequent in Branchiopoda), so that the females studied probably reproduce by parthenogenesis. The occurrence of SC indicates this parthenogenesis as being meiotic, and confirms ultrastructurally the karyologic data of Longhurst (1955) and Trentini (1976). In conclusion, our observations on the early developmental stages of Triops cancriformis oocytes show that they have a morphofunctional uniformity with their nurse cells, i.e., concentrically arranged ER (stage II), and yolk globules and AL (stages III, IV). This uniformity of the four follicle cells is probably related to the persistence of intercellular bridges. This and the common origin of the four-celled follicle, corroborate our view that the nurse cells are abortive oocytes. In substance, what distinguishes the true oocyte from its sister cells, in the early stages, is the meiotic process and its slow rate of growth. References Anteunis, A.: Les membranes annel6es dans l'oeuf d'Artemia salina, l~tude de microscopie 61ectronique. Compt. Rend. Assoc. Anat. 124, 168-172 (1965) Anteunis, A., Fautrez-Firlefyn, N., Fautrez, J., Lagasse, A.: L'ultrastructure du noyau vitellin de l'oeuf d'Artemia salina. Exp. Cell Res. 35, 239-247 (1964) Anteunis, A., Fautrez-Firlefyn, N., Fautrez, J.: Apropos d'un complexe tubulo-mitochondrial ordonn6 dans le jeune oocyte d'Artemia saline. J. Ultrastruct. Res. 15, 122-130 (1966a) Anteunis, A., Fautrez-Firlefyn, N., Fautrez, J.: La structure des ponts intercellulaires "obtur6s" et "ouverts" entre oogonies et oocytes d'Artemia salina. Arch. Biol. (Li6ge) 77, 645-664 (1966b) Anteunis, A., Fautrez-Firlefyn, N., Fautrez, J.: L'incorporation de cellules nourricieres par l'oocyte d'Artemia salina, t~tude au microscope ~lectronique. Arch. Biol. (Li+ge) 77, 665-676 (1966c) Anteunis, A., Fautrez-Firlefyn, N., Fautrez, J.: Ultrastructure du nucl6ole expuls6 dans le cytoplasm de l'oocyte d'Artemia salina. C. R. Acad. Sci. (Paris) 266, 1862-1863 (1968) Comings, D.E., Okada, T.A.: Whole mount electron microscopy of meiotic chromosomes and the synaptonemal complex. Chromosoma (Berl.) 30, 269-286 (1970) Dudley, P.L.: Synaptonemal polycomplexes in spermatocytes of the gooseneck barnacle, Poelicipes polymerus Sowerby (Crustacea, Cirripedia). Chromosoma (Berl.) 40, 221-242 (1973) Fl6ssner, D.: Krebstiere, Crustacea. Kiemen- und Blattffisser, Branchiopoda. Fischl/iuse, Branchiura. Die Tierwelt Deutschlands 60, 1-501 (1972) Franke, W.W.: Structure, biochemistry, and functions of the nuclear envelope. Int. Rev. Cytol., Suppl. 4, 71-236 (1974) Herold, L., Goggins, J.A., Witkus, E.R., Vernon, G.M.: Annulate lamellae in hindgut epithelial cells of Isopoda. Protoplasma 87, 291-296 (1976) Kaye, G.I., Pappas, G.D., Yasuzumi, G., Yamamoto, H.: The distribution and form of the endoplasmic reticulum during spermatogenesis in the crayfish Carnbaroidesjaponicus. Z. Zellforsch. 53, 159-171 (1961) Kessel, R.G.: Annulate lamellae. J. ULtrastruct. Res., Suppl. 10, 5-82 (1968) Kessel, R.G., Beams, H.W.: Intranucleolar membranes and nuclear cytoplasmic exchange in young crayfish oocytes. J. Cell Biol. 39, 735-741 (1968) Longhurst, A.R.: The reproduction and cytology of the Notostraca (Crustacea, PhyUopoda). Proc. Zool. Soc. London 125, 671-680 (1955) Maul, G.G. : The nuclear and the cytoplasmic pore complex: structure, dynamics, distribution, and evolution. Int. Rev. Cytol., Suppl. 6, 75-186 (1977) Moses, MJ.: Chromosomal structures in crayfish spermatocytes. J. Biophys. Biochem. Cytol. 2, 215218 (1956) Moses, M.J.: The nucleus and chromosomes: a cytological study. In: Cytology and Cell Physiology. (G. Bourne, ed.) New York: Academic Press 1964 Ruthmann, A.: Basophilic lamellar systems in the crayfish spermatocyte. J. Biophys. Biochem. Cytol. 4, 267-274 (1958)
368
F. Sabelli Scanabissi and M. Trentini
Trentini, M.: Karyologic observations on Triops cancriformis (Phyllopoda, Notostraca). Boll. Zool. 43, 321-322 (1976) Trentini, M., Sabelli Scanabissi, F.: Ultrastructural observations on the oogenesis of Triops cancriformis (Crustacea, Notostraca). I. Origin and differentiation of nurse ceils. Cell Tissue Res. 194, 71-77 (1978) Westergaard, M., yon Wettstein, D.: The synaptonemal complex. Ann. Rev. Gen. 6, 71-110 (1972) Wingstrand, K.G.: Comparative spermatology of a pentastomid, Raillietiella hemidactyli, and a branchiuran crustacean Argulus foliaceus, with a discussion of pentastomid relationship. Kongl. Danske Vid. Selskab. Biolog. Skr. 19, 1 72 (1972) Wingstrand, K.G.: Comparative spermatology of the Crustacea Entomostraca. 1. Subclass Branchiopoda. Kongl. Danske Vid. Selskab. Biolog. Skr. 22, 1-66 (1978) Wischnitzer, S.: The annulate lamellae. Int. Rev. Cytol. 27, 65-100 (1970) Zaffagnini, F., Lucchi, M.L.: Indagini col microscopio elettronico sull'ovogenesi partenogenetica in Daphnia magna (Crustacea: Cladocera). I. Origine comune delrovocita e delle sue tre cellule nutrici. Arch. Zool. Ital. 50, 49-58 (1965)
Accepted May 3, 1979
