ULTRASTRUCTURE OF THE DINOFLAGELLATE POLYKRIKOS
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1 J. Cell Sci. 63, (1983) 245 Printed in Great Britain The Company of Biologists Limited 1983 ULTRASTRUCTURE OF THE DINOFLAGELLATE POLYKRIKOS I. DEVELOPMENT OF THE NEMATOCYST-TAENIOCYST COMPLEX AND MORPHOLOGY OF THE SITE FOR EXTRUSION JANE A. WESTFALL* Department of Anatomy and Physiology, Kansas State University, Manhattan, Kansas 66506, U.SA. PHYLLIS C. BRADBURY Department of Zoology, North Carolina State University, Raleigh, North Carolina 27650, U.SA. AND J. W. TOWNSENDf Department of Anatomy and Physiology, Kansas State University, Manhattan, Kansas 66506, U.SA. SUMMARY Development of the nematocyst-taeniocyst complex in the four-zooid stage of a dinoflagellate, Polykrikos kofoidi, was studied by electron microscopy. We observed the following stages: formation of large spherical bodies in islets of cytoplasm containing extensive rough endoplasmic reticulum and Golgi complexes; differentiation of an anlage of first the nematocyst and then the taeniocyst into a tandem pair; and, maturation of the complex into a nematocyst with operculum and capsule, and a taeniocyst with head, neck and body. In the intermediate stages of dinoflagellate cnidogenesis the structurally elaborate pattern of development differed from that of coelenterate nematocysts but in certain features the mature organelles of both groups were similar. Nematocyst-taeniocyst complexes migrated into chutes on zooids two and four near the junction of the annulus and sulcus at the flagellar bases. The specialized chute was partially lined by thimble-shaped organelles of unknown function. The taeniocyst protruded from the surface in association with a striated fibre whose structure and position were those of a trigger to discharge the two organelles. We found no cytostome in this holozoic colony; the structure of the chute suggested that it might also function as a cytostome. INTRODUCTION More than a hundred years ago, Biitschli (1873) described a barrel-shaped protozoon, Polykrikos schwartzi, that contained nematocysts (organelles with projectile filaments). It is general knowledge that cells containing nematocysts are characteristic of coelenterates, but it is less widely known that three different kinds of protists, including Polykrikos, endogenously form nematocysts. The projectile filaments of the protists Myxospora and Microspora are essential for the transmission of these parasites to new hosts and cnidogenesis is only part of the complex process of forming a spore (Lorn, 1969; VaVra, I976a,b). In coelenterates Author for correspondence. t Present address: Department of Pathology, University of Arkansas Medical Center, 4301 West Markham, Little Rock, Arkansas 72205, U.S.A.
2 246 J. A. Westfall, P. C. Bradbury andj. W. Townsend a single specialized cell forms nematocysts, which are used in catching and subduing prey. Polykrikos generates nematocysts resembling those of coelenterates, but it does so in single cells (zooids) that also carry on the functions of a whole animal (Faur6- Fremiet, 1913; Hovasse, 1965). The fine structure of the developmental stages of coelenterate nematocysts and protozoon polar capsules have been examined and compared (Westfall, 1966; Lorn, 1969; Loubes & Maurand, 1976). The morphogenesis of nematocysts in Polykrikos has only recently been studied at the ultrastructural level (Greuet & Hovasse, 1977), perhaps because it appears unpredictably in plankton samples and until recently has not been cultivated in the laboratory (Morey-Gaines & Ruse, 1980). Chatton (1914) described the formation of nematocysts in Polykrikos as an autonomous cyclic process, but much later (Chatton & Hovasse, 1944) it was determined that the taeniocyst was not a precursor to the nematocyst. Greuet (1972) named the taeniocyst and described its ultrastructure, as well as that of the nematocyst. Greuet & Hovasse (1977) reported the independent origin of the two organelles in P. schwartzi. The present electron-microscopic study of the four-zooid stage of the dinoflagellate Polykrikos kofoidi provides the first detailed description of: (1) the development and maturation of the nematqcyst-taeniocyst complex and (2) the morphology of a newly discovered extrusion site for these unique paired organelles. MATERIALS AND METHODS Specimens of a dinoflagellate, P. kofoidi (Chatton, 1914), were collected in plankton samples from Argyle Lagoon at the Friday Harbor Laboratories, University of Washington. All specimens of this colonial dinoflagellate had four zooids as shown by Kofoid & Swezy (1921). They were fixed for approximately 1 h in a cold solution of 2% glutaraldehyde in 0-4M-phosphate buffer and M- sodium chloride (ph 7-4) and post-fixed for about 45 min in a cold solution of 1 % osmium tetroxide in 0-4M-phosphate buffer and 0-75 M-sodium chloride (Dunlap, 1966). The specimens were then dehydrated in ethanol and embedded in Epon. Serial thin sections were stained with uranyl acetate followed by lead citrate; electron micrographs were taken with a Philips EM 301 at 80 kv. OBSERVATIONS We observed taeniocysts and nematocysts in various stages of development in every organism examined from our sample. The nematocyst anlage was the larger and more electron-lucent of the two organelles; the taeniocysts began development as an electron-dense sphere apical to the nematocyst primordium, to which it was connected by a vacuole shared by both organelles. We could establish a developmental sequence for the two organelles because of their tandem arrangement. This tandem association remained even in the final location of the paired organelles in a specialized channel (Fig. 1) on the ventral surface of the dinoflagellate. Cytoplasmic characteristics and anlagen formation There were numerous regions of rough endoplasmic reticulum and Golgi complexes in the cytoplasm of Polykrikos (Fig. 2). A Golgi complex with flattened saccules
3 Nematocyst-taeniocyst complex 247 Striated fibre Head - Taeniocyst Anterior chamber Stylet Nematocyst Capsule Posterior chamber Filament - Fig, 1. Diagram of tandem arrangement of a mature nematocyst-taeniocyst complex within a cytoplasmic chute in P. kofoidi. and numerous coated vesicles was often associated with a conspicuous patch of rough endoplasmic reticulum. Ribosomes attached to the membranes of the endoplasmic reticulum stained intensely, and the expanded cisternae were filled with a moderately electron-dense material. At the periphery of patches of rough endoplasmic reticulum the cisternae were swollen and lacked ribosomes. In some individuals, one or more large ovoid bodies appeared to be early nematocyst-taeniocyst anlagen (Fig. 3). These structures were close to the nucleus,
4 248 J. A. Westfall, P. C. Bradbury andj. W. Townsend Figs 2 and 3
5 Nematocyst-taeniocyst complex 249 where light microscopists had reported that the earliest stages of nematocyst formation occurred. They were conspicuous because of their relative size (approximately 5-6fjin in diameter) and homogeneity in a cytoplasm packed with organelles. As differentiation progressed, the anlagen became more granular and contained fibrous substructures with associated dense materials. With the first signs of opercular development, the anlage of the taeniocyst appeared just anterior to the developing nematocyst (Fig. 4). The cytoplasm associated with the two anlagen was contained within a common membrane. At the taeniocyst end, the cytoplasm contained accumulations of ribosomes, Golgi complexes, coated vesicles, and a large vacuole filled with fibrous material from which the electron-dense taeniocyst condensed. The membrane enclosed much less cytoplasm around the sides and posterior of the nematocyst, although this cytoplasm was dense with ribosomes and enclosed mitochondria and multivesicular bodies. An electron-lucent vacuole abutted the posterior end of the nematocyst primordium and indented the posterior cytoplasm. Differentiation of nematocyst and taeniocyst Nematocyst. Advanced stages of the nematocyst anlage (= nematogene) were enlarged and elongated. The outline of the future capsule was irregular, and beneath its membrane was a thin dense layer of primordial capsular wall material (Fig. 4). The anlagen of the anterior chamber (= introvert or ampulla) and the operculum were approximately in their final position, and their separate elements were represented in an ordered design by substances of different densities. These substances formed a diffuse and expanded pattern, not delimited by vacuoles or membranes, but recognizable as components of the future operculum and anterior chamber. The opercular region was separated from the capsular region by an infolding of the capsular wall (arrows, Figs 4,5). The fibrous matrixfilling the capsule was denser at the centre and formed a clearly discernible longitudinal fibrous strand (Fig. 4) that extended from the posterior pole to the base of the anterior chamber and laterally to the infolded capsular wall. A vacuole bridged the space between the developing nematocyst and taeniocyst and contributed its substance to both structures. An indentation into the operculum cupped the vacuole, and within the vacuole a dense line paralleled the indentation (Fig. 4). The vacuole also indented the base of the taeniocyst; and where it bulged into the taeniocyst, it had a narrow dense layer of material resembling the substance of the taeniocyst. Centrally the opercular anlage had a complex pattern resembling a bell; it formed the opercular valve that occluded an opening into the anterior chamber (Fig. 5). A central stylet extended from the base of the double-walled anterior chamber to Fig. 2. Cytoplasmic region of Polykrikos rich in rough endoplasmic reticulum {rer) and Golgi complexes (g) with coated vesicles (cv). Patches of rer have enlarged peripheral cisternae lacking ribosomes (arrows). Mitochondria (m). X Fig. 3. Presumed Golgi (g)-derivcd primordial body with a condensed substructure (arrows). X CEL63
6 250 J. A. Westfall, P. C. Bradbury andjf. W. Townsend Fig. 4
7 Nematocyst-taeniocyst complex 251 the opercular valve at its apex. It was bounded laterally by electron-dense wings (Fig. 4), which became the walls of the anterior chamber in a later stage (Fig. 5). The band of fine filaments at the base of the anterior chamber (Fig. 4) formed a hollow internal filament (Fig. 6) that presumably could be everted at discharge of the mature nematocyst. The outer wall of the anterior chamber was continuous with the thick double-walled capsule at its junction with the operculum (arrows, Fig. 5). When the filament appeared the capsular wall was thickened; the body was greatly elongated and undulating, so that it was difficult to obtain a single longitudinal section of the entire intermediate stage (Fig. 7). The posterior end of the developing capsule was thickened and abutted a fibrous body (= posterior cap) (Fig. 8), presumably formed from the posterior vacuole associated with the nematocyst primordium (Fig. 4). Taeniocyst. The developing taeniocyst (= taeniogene) originated in a large vacuole with an irregular outline (Fig. 4). Initially it was a large electron-dense sphere (approximately 6-4/im in diameter), which condensed from granular material in the vacuole. The size and general appearance of the sphere resembled the large lipid storage droplets in the cytoplasm, except that the sphere was slightly ovoid with strata of less dense material at either pole. The large and most electron-dense stratum occupied two-thirds of the sphere (Figs 4, 9, 10). This homogeneous dense area became the body of the mature taeniocyst. The light granular bands anterior to it Fig. 4. Early differentiation of a paired nematocyst-taeniocyst complex with a connecting vacuole (va) and cytoplasmic region (cy) common to both primordia. Note condensation of material from vacuole around taeniocyst anlage (T) and infolding of capsule wall of nematocyst (arrows) with differentiating operculum (o), anterior chamber (a) and capsule (c). A fibrous strand (fs) extends from base of anterior chamber to base of capsule and to infolded capsular wall. Posterior vacuole (pva). X7600. Fig. 5. Advanced differentiation of nematocyst-taeniocyst complex with spherical anlage of taeniocyst (T), central valve in operculum (o) and stylet (s) attached to base of doublewalled anterior chamber (a), connected (arrows), in turn, to capsule wall (cw). X Fig. 6. Filament (/) attached to base of anterior chamber (a) in serial section to Fig. 5. X Fig. 7. Elongated capsular region of developing nematocyst with coiled filament (f) cut transversely. X Fig. 8. Posterior end of developing nematocyst with double-walled capsule (civ) in contact with fibrous body (fb). Filament (/). X Fig. 9. Spherical anlage of taeniocyst with three major strata of different densities and peripheral condensation of granular material. X Fig. 10. Differentiating complex with large primordial taeniocyst (T) and opercular region (o) of nematocyst connected by a vacuole (va) in cytoplasm common to both organelles. X5600. Fig. 11. Advanced differentiation of taeniocyst with head (h) and neck (n) separated from the body (b) by a dense ring. Note fibrous material in vacuole (va) between taeniocyst and operculum (o) of nematocyst. Xll 200. Fig. 12. Operculum of nematocyst with cap (ca) over valve (v), dense collar (co) and junction to capsule (arrows). Compare with earlier stage of operculum in Fig. 11. X Fig. 13. Cross-section of mature nematocyst capsule with hollow internal filament (/). X
8 251 J. A. Westfall, P. C. Bradbury andj. W. Townsend Figs 5-8. For legend see p. 251.
9 Nematocyst-taeniocyst complex 253 Figs For legend see p. 251.
10 254 J. A. Westfall, P. C. Bradbury andj. W. Townsend formed the neck and head. The narrow fibrous layer at the base of the sphere was incorporated into a posterior articulation with the common vacuole of the nematocyst. In early stages of differentiation the sphere occupied a large vacuole filled with a flocculent material that was added to the sphere (Fig. 9). In advanced stages of differentiation the taeniocyst became closely bounded by a membrane; a dense ring separated the potential body from the future neck and head regions (Fig. 11). The body was homogeneous except for several faint, regularly spaced fibrils. The bridging vacuole (= intermediate piece) between the taeniocyst and the nematocyst contained fibrous strands extending between the two organelles. Operculum and mature capsule. At an advanced stage of taeniocyst development the nematocyst was compact, with a distinct operculum (Fig. 11). The operculum became elaborated into a cap covering a valve surrounded by a dense peripheral wall (Fig. 12). The operculum covered the apical region of the mature nematocyst, which was a tough impermeable double-walled capsule approximately 15/um X 5 fim. The mature filament was coiled tightly within the greatly shortened capsule, which was resistant to fixative and embedments and thus difficult to preserve in sectioned material (Fig. 13). Taeniocyst-nematocyst chute Near the flagellar insertions we observed a passage, which we termed a chute, enclosing a mature nematocyst and taeniocyst (Figs 14 16). The two organelles were separated by a distance of 5 fim. The taeniocyst, enveloped by the outer thecal membrane, protruded from the body and appeared as if in a position to fire, upon receiving a proper stimulus (Figs 14, 17). The nematocyst was situated deeper in the chute. Chute wall. At the opening of the chute the theca was interrupted except for its outer membrane (Figs 14, 17). A striated fibre parallel to the chute had a shape and position suggesting a trigger; it was attached to the fibrillar sheath that formed the chute wall (Fig. 15). The fibre was 0-3 fim in diameter and had a periodicity of 47 nm. Thimble-like protrusions (0-3 ^m in diameter) were embedded in the fibrillar sheath of the chute (Figs 14, 16, 18). They represented a new kind of organelle (chute organelles) found nowhere else in the body. In cross-section, each organelle had a central clear disc with a dense collar (Fig. 18 inset); in longitudinal section, a membrane covered the lateral and apical surface of each chute organelle (Fig. 18). These Fig. 14. Longitudinal section of mature taeniocyst with head (h), neck (n), and body (6) lying in chute (ch) above theca (t) and nematocyst (N) at base of chute. Chute organelles ( ); anterior wall (aw). X5800. Fig. 15. Longitudinal section through striated fibre (sf) on anterior wall of chute. Note perpendicular dense fibre (arrow) at end of chute and thin double-membrane (dm) forming posterior wall of chute with taeniocyst (T). X Fig. 16. Base of taeniocyst (T) within chute (ch) lined by fibrous wall with chute organelles ( ). Note posterior fibrous skirt (arrows) associated with taeniocyst. Xll 200. Fig. 17. Oblique section of taeniocyst (T) in chute above annulus with transverse flagellum (tf) and sulcus with longitudinal flagellum (If). Theca (t). X5000.
11 Nematocyst-taeniocyst complex i p. Figs 14-17
12 2S6 1. A. Westfall. P. C. Bradbury andjf. W. Townsend 21
13 Nematocyst-taeniocyst complex 257 organelles occurred at intervals on the fibrillar sheath as well as deeper in the chute, where they were restricted to the wall nearest the annulus. The part of the chute extending into the cytoplasm contained a fibrillar matrix, numerous chute organelles, a few multivesicular bodies and, in its centre, closepacked vacuoles (Fig. 16). The substructure of the chute and its organelles positioned a taeniocyst in readiness to fire. At the base of the chute a nematocyst was in line to enter after the taeniocyst was extruded (Fig. 14). To date, chutes have been identified only in zooids 2 and 4. Mature taeniocyst. Mature taeniocysts (approx. ll - 2/im X 2-2/an) were found in protrusions of the chute above the theca (Fig. 14). Cross-sections through a taeniocyst anchored within its chute revealed differences in the chute wall at various levels (Figs 19 22). Proximally, the taeniocyst emerged from an anteriorly thickened sheath wall containing chute organelles and microtubules (Figs 14, 18, 19). Two bands of longitudinally oriented microtubules were parallel to a broad striated fibre that came to a point above the apex of the taeniocyst (Figs 18, 22). A pair of longitudinally oriented dense rods (approx. 80 nm in diameter) were parallel to the inner band of microtubules (Figs 19-22). The body of the taeniocyst was filled with a lamellar structure, which was irregularly folded centrally, and concentrically compacted peripherally (Figs 19, 20). Concentric cortical lamellae also surrounded the doublewalled neck region that was continuous with the body (Figs 14, 21). The head, which capped the neck, resembled a stopper occluding the central opening in the neck of the taeniocyst (Fig. 22). DISCUSSION The results of our ultrastructural study on the development and maturation of the nematocyst-taeniocyst complex in Polykrikos confirmed those of Greuet & Hovasse (1977) and Greuet (1972) in showing that there are separate origins but synchronous development and tandem arrangement for two distinct organelles. We Fig. 18. Longitudinal section of anterior chute wall showing microtubules (mt) and chute organelles ( ). X Inset: cross-section of chute organelle showing spherical centre surrounded by dense band. X523OO. Fig. 19. Cross-section through body of taeniocyst (T) in chute with thickened anterior wall containing a chute organelle ( ), two bands of microtubules (mt) and the longitudinal striated fibre (sf). X Fig. 20. Cross-section through body of taeniocyst (T) in chute at higher level than Fig. 19. Note longitudinal striated fibre (sf) associated with outer row of microtubules and two small fibres (arrows) associated with inner row of microtubules. Body of taeniocyst contains membranous lamellae in medulla and cortex. X Fig. 21. Cross-section through chute at level of neck of taeniocyst (T). Note striated fibre (sf) and microtubules (mt) in anterior wall of chute and concentric lamellae around doublewall (arrows) of taeniocyst neck. X Fig. 22. Oblique-section through head (h) of taeniocyst (T) and vacuole (va) at tip of chute with membranous terminal containing the striated fibre (sf) and microtubules. X
14 258 Jf. A. Westfall, P. C. Bradbury andjf. W. Townsend have characterized the morphogenesis and maturation of these organelles in detail and shown for the first time their location in a specialized chute with a putative trigger organelle for discharge (Figs 23, 24). Mature dinoflagellate nematocysts are specialized cell organelles, like those of coelenterates (Westfall, 1966) and myxosporidians (Lorn, 1969), and like them they differ from microsporidian spores (Vavra, 19760,6). Comparative cnidogenesis Cnidogenesis in Polykrikos, like cnidogenesis in other organisms, begins with a proliferation of Golgi complexes and endoplasmic reticulum. Cnidogenesis in other organisms, however, is easy to recognize because it takes place in small cells whose only or major function is to form a nematocyst. Polykrikos is a colony of cells (zooids) that carry out the simultaneous functions of a whole animal. Light microscopists disagreed about the existence of Golgi complexes in Polykrikos (Chatton & Grasse, 1929; Hovasse, 1951), but the electron microscope reveals that Golgi complexes are always present and play an important role in forming the paired organelles in Polykrikos, as in other cnidogenic species. The nematocyst and taeniocyst lie within separate membranes; in addition, a Golgi-derived vacuole shared by both organelles supplies each organelle with substances necessary to grow and at the same time provides a mechanism for articulation of the nematocyst-taeniocyst complex. The Fig. 23. Diagram of probable sequence of formation of the nematocyst-taeniocyst complex in Polykrikos kofoidi. A. Primordium; B, early differentiation; c, advanced differentiation; D, mature complex.
15 Nematocyst-taeniocyst complex 259 nematocyst is a larger and visibly more complex organelle than the taeniocyst and has a much more elaborate pattern of morphogenesis. Even so, continuity is maintained between the two organelles throughout their development as well as in their final location before they are discharged through the chute. Cnidogenesis in coelenterates and Myxospora involves the formation of a long tube that extends from the capsule anlage into the cytoplasm (Westfall, 1966; Lorn, 1969). This external tube subsequently becomes the coiled filament within the nematocyst. The filament in Polykrikos condenses from a homogeneous matrix within the capsule. There is no external tube connected with its development, nor are there intracapsular Golgi complexes or rough endoplasmic reticulum. In Microspora the coiled filament within the spore is formed with contributions from the rough endoplasmic reticulum and Golgi complex (Vdvra, 1976a,6). Comparison of cnidogenesis in the Microspora with that of other groups is complicated by the fact that the spore is a nematocyst cell and the polar filament is not separated from the rest of the cell (for a review, see Loubes & Maurand, 1976). Similarities in cnidogenesis in coelenterates and Myxospora has served to link the two groups and sever the Myxospora from the Microspora. Cnidogenesis in Polykrikos produces a nematocyst that visibly resembles the coelenterate nematocyst but the stages of its differentiation are dissimilar. Transverse flagellum Longitudinal flagellum Fig. 24. Diagram illustrating the position of the nematocyst-taeniocyst complex within a cytoplasmic chute overlying the flagellar apparatus.
16 260 J. A. Westfall, P. C. Bradbury andjf. W. Townsend Functional morphology Little is known about the biology of Polykrikos and the function, of its nematocyst-taeniocyst complex. Earlier investigators always assumed that in Polykrikos the nematocyst were useful in feeding, but the discharge of nematocysts from a living intact Polykrikos has never been reported. The discharge of nematocysts upon their exposure to sea water when the dinoflagellate was ruptured or crushed has been described by several investigators (Faur6-Fremiet, 1913; Chatton, 1914; Kofoid & Swezy, 1921). Chatton (1914) illustrated the exploded nematocyst with its filament still attached to the everted anterior chamber, which led Kofoid & Swezy (1921) to suggest that eversion of the slender tube had occurred as in coelenterate nematocysts. The discovery of the chute, apparently a permanent site for release of the taeniocysts and nematocysts, still does not explain their function. Probably the chute has been seen earlier. Hovasse (1951) reports that Chatton observed the taeniocyst in a fissure in the annulus and at first thought it was being expelled. Then he thought that the fissure might be the mouth, and that the taeniocyst was helping capture food. Our observations of the taeniocyst projecting above the theca in association with a long striated fibre suggested a trigger mechanism for discharge of the taeniocyst. The chute, which was just below the annulus, may be the fissure that Chatton observed. The cytostome of other dinoflagellates is located in the sulcus near the origin of the transverse flagellum; no cytostome has yet been observed in Polykrikos. Perhaps the chute serves as a cytostome after ejection of the taeniocyst nematocyst complex. The thin membranes of the protruding chute are the only part of the surface not underlain by the other complex structures of the theca. The chute described here, however, is much too small to take in the large prey organisms reported in the food vacuoles of Polykrikos (Bovier-Lapierre, 1888; Kofoid & Swezy, 1921; Hovasse, 1951). A single large food vacuole crammed with semidigested material in our specimens testified that particulate food was ingested somewhere on the surface of the organism. We speculate that the taeniocyst uncoils as a ribbon that entangles the food organism and the nematocyst everts its filament to anchor the prey. Electron microscopy has confirmed that two complex and distinct organelles are formed in intimate association, although their purposes and function remain to be discovered. For 30 years ( ) the nematocysts of Polykrikos were cited as examples of organelles originating from cyclic autonomous replication. The partially differentiated nematocyst would supposedly induce the formation of what is now called a taeniocyst. After the nematocyst had matured and separated from the taeniocyst, the taeniocyst would then mature into a nematocyst that would induce the formation of another taeniocyst. In 1944 Chatton, provided with a wealth of sections and whole mounts of Polykrikos by Hovasse, repudiated his earlier theory because he could discover no unequivocal intermediate stage between a nematocyst and a taeniocyst. And now over 30 years later electron microscopy has provided the details of morphogenesis in two distinct organelles that come to lie in tandem in a specialized channel for extrusion.
17 Nematocyst-taeniocyst complex 261 This is contribution number j from the Kansas Agricultural Experiment Station. We thank Julia Dewey for collecting the specimens used in this study, David E. Sims for excellent technical assistance, Mallory Rooks Hoover for the drawings, Drs Robert D. Klemm and F. J. R. Taylor for helpful suggestions on the manuscript, and USPHS grant NS for financial support of the electron microscope. REFERENCES BOVIER-LAPIERRE, E. (1888). Nouvelles observations sur le Pfiridiniens appartenant au genre Polykrikos. C. r. Seanc. Soc. Biol. 40, BUTSCHLI, O. (1873). Einiges iiber Infusorien. Arch, mikrosk. Anat. EntwMech. 9, CHATTON, E. (1914). Les cnidocystes du P6ridinien Polykrikos Schwartzi Butschli. Archs Zool. exp.gen. 54, CHATTON, E. & GRASSE, P. P. (1929). Le chondriome, le vacuome, les vesicules osmiophiles, le parabasal, les trichocystes et les cnidocystes du Dinoflagelle' Polykrikos Schwartzi Butschli. C. r. Seanc. Soc. Biol. 100, CHATTON, E. & HOVASSE, R. (1944). Sur les premiers stades de la cnidogenfese chez le P6ridinien Polykrikos Schwartzi, Leurs rapports avec les dictyosomes. C. r. hebd. Seanc. Acad. Sci., Paris 218, DUNLAP, H. L. (1966). Oogenesis in Ctenophora. Ph.D. thesis, University of Washington, Seattle. FAUR -FREMIET, E. (1913). Sur les ne'matocystes et les trichocystes despolykrikos. Bull. Soc. zool. Fr. 38, GREUET, C. (1972). La nature trichocystaire du cnidoplaste dans le complexe cnidoplaste n6matocyste de Polykrikos schwartzi Butschli. C. r. hebd. Seanc. Acad. Sci., Paris 275, GREUET, C. &HOVASSE, R. (1977). A proposde la genese des ne'matocystes depo/yan'aossdiuiarlzi Butschli. Protistologica 13, HOVASSE, R. (1951). Contribution a l'e'tude de la cnidogfinese chez les P6ridiniens. I. Cnidogdnese cyclique chez Polykrikos Schwartzi Butschli. Archs Zool. exp. gen. 87, HOVASSE, R. (1965). Trichocystes, corps trichocystoides, cnidocystes et colloblastes. Protoplasmatologia m/f, KOFOID, C. A. & SWEZY, O. (1921). The free-living unarmored dinoflagellata. Univ. Calif. Mem. 5, LOM, J. (1969). Notes on the ultrastructure and sporoblast development in fish parasitizing myxosporidian of the genus Sphaervmyxa. Z. Zellforsch. mikrosk. Anat. 97, LOUBES, C. & MAURAND, J. (1976). Etude ultrastructurale de Pleistophora debaisieuxi Jirovec, 1943 (Microsporida): son transfert dans le genre Tuzetia Maurand, Fize, Michel et Fenwick, 1971 et remarques sur la structure et la genese du filament polaire. Protistologica 12, MOREY-GAINES, G. & RUSE, R. H. (1980). Encystment and reproduction of the predatory dinoflagellate, Polykrikos kofoidi Chatton (Gymnodiniales). Phycologia 19, VAVRA, J. (1976a). Structure of the microsporida. In Comparative Pathobiology, vol. 1, Biology of the Microsporida (ed. L. A. Bulla & T. C. Cheng), pp New York, London: Plenum. VAVRA, J. (19766). Development of the microsporida. In Comparative Pathobiology, vol. 1, Biology of the Microsporida (ed. L. A. Bulla&T. C. Cheng), pp New York, London: Plenum. WESTFALL, J. A. (1966). The differentiation of nematocysts and associated structures in the cnidaria. Z. Zellforsch. mikrosk. Anat. 75, (Received 1 September 1982-Accepted, in revised form, 12 April 1983)
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