Reinvestigation of vitellogenesis in Caryophyllaeus laticeps (Pallas, 1781) (Cestoda, Caryophyllidea, Caryophyllaeidae), monozoic tapeworm of Abramis brama (Pisces, Teleostei)

Reinvestigation of vitellogenesis in the caryophyllidean cestode Caryophyllaeus laticeps (Pallas, 1781) has been performed using light microscope (LM) and transmission electron microscopy (TEM), and cytochemical staining with periodic acid-thiosemicarbazide-silver proteinate (PA-TSC-SP) for glycogen. Vitellogenesis is generally similar to that reported in the past, however, some new observations were made. The present study reveals the first evidence of: (i) interstitial tissue in the vitelline follicles, (ii) lipid droplets in maturing and mature vitellocytes from vitelline follicles, and (iii) lamellar bodies in vitellocytes from the vitelloduct in C. laticeps. Projections of interstitial tissue surround each vitellocyte and the follicle periphery. The perinuclear cytoplasm of the interstitial tissue contains granular endoplasmic reticulum and vesicles of various size and density. Cytoplasmic osmiophobic lipid droplets and lamellar bodies, previously believed to be absent in most caryophyllid cestodes, are readily apparent in vitellocytes of C. laticeps. The origin and presumed function of these inclusions are discussed. On the other hand, the formation and storage of massive amounts of glycogen in the nucleus and large amounts in the cytoplasm of mature vitelline cells are similar to the condition found in other caryophyllids. Results are compared and contrasted with previous studies on vitellogenesis in other monopleuroid cestodes (Amphilinidea and Gyrocotylidea) as well as polypleuroid cestodes (Spathebothriidea) and the remaining strobilated Eucestoda.

Ultrastructure and cytochemistry of vitellogenesis and the vitellocytes of the bothriocephalidean cestode Clestobothrium crassiceps (Rudolphi, 1819), a parasite of the teleost fish Merluccius merluccius (L., 1758) (Gadiformes, Merlucciidae)

Vitellogenesis and vitellocytes of the bothriocephalidean cestode Clestobothrium crassiceps (Rudolphi, 1819), a parasite of the teleost fish Merluccius merluccius (L., 1758), were studied by means of transmission electron microscopy (TEM) and cytochemistry. During vitellogenesis, four developmental stages were distinguished at the TEM level: (I) a stem cell stage of the gonial type; (II) an early differentiation stage, predominantly exhibiting lipid and protein synthetic activity; (III) an advanced differentiation or vitellocyte maturation stage, primarily exhibiting active glycogenesis still accompanied by an increase in lipid accumulation; and (IV) a mature vitellocyte stage. Vitellogenesis involves: (1) an increase in cell volume; (2) an extensive development of parallel, frequently concentrically arranged, cisternae of granular endoplasmic reticulum (GER) that produce dense, proteinaceous shell-gobules; (3) the development of Golgi complexes engaged in the packaging of this material; (4) an accelerated accumulation of unsaturated and saturated lipid droplets, along with their continuous enlargement and fusion; (5) the formation of individual β-glycogen particles and α-glycogen rosettes and their accumulation in the form of glycogen islands scattered among lipid droplets in the cytoplasm of maturing and mature vitellocytes; and (6) the rapid accumulation of large, saturated lipid droplets accompanied by dense accumulations of α- and β-glycogen along with proteinaceous shell-globules or shell-globule clusters in the peripheral layer during the advanced stage of vitellocyte maturation. Vitellogenesis in C. crassiceps generally resembles that previously described for three other bothriocephalideans, but differs from that of other cestode orders. Cytochemical staining with periodic acid-thiocarbazide-silver proteinate for glycogen indicates a strongly positive reaction for β-glycogen particles and α-glycogen rosettes, which form several large glycogen accumulations around the large, saturated lipid droplets of maturing and mature vitellocytes. Some hypotheses concerning the interrelationships between patterns of vitellogenesis, the possible modes of egg formation, embryonic development and life cycles in cestodes, and their phylogenetic implications are commented upon.

Ultrastructural and cytochemical study on vitellogenesis in the diphyllidean cestode Echinobothrium euterpes (Echinobothriidae) and its phylogenetical implications

The first description of vitellogenesis in the Diphyllidea is presented in this paper. Though the type of vitellogenesis and mature vitellocyte in Echinobothrium euterpes appear to be unique among the Eucestoda, however, they somewhat resemble that observed in the two orders of the lower cestodes, Tetraphyllidea and Proteocephalidea. Vitellocyte maturation is characterized by: (1) an increase in cell volume; (2) extensive development of short, parallel, frequently concentric cisternae of GER that produce dense proteinaceous granules; (3) development of Golgi complexes engaged in packaging this material; (4) progressive formation of saturated lipid droplets; their continuous enlargement and fusion; (5) formation of small accumulations of glycogen particles scattered between and among lipid droplets in the cytoplasm of maturing vitellocytes; (6) concentration of dense proteinaceous granules in the peripheral layer of cytoplasm, around the cell plasma membrane; and (7) vacuolization of cytoplasm of mature vitellocytes accompanied by a rapid increase in its volume. A new, unreported type of dense proteinaceous granules, situated around the limiting plasma membranes of mature vitellocytes, is described. Vitellogenesis evidently differs from that with typical shell-globules and shell-globule clusters previously reported in other taxa of lower cestodes. Cytochemical staining with periodic acidthiosemicarbazide-silver proteinate for glycogen indicates a strongly positive reaction for glycogen particles between and around large unsaturated lipid droplets of the maturing and mature vitellocytes. Some hypotheses concerning the interrelationship between this pattern of vitellogenesis, possible mode of egg formation, embryonic development and diphyllidean life cycle, and their phylogenetic implications are drawn and discussed.

Ultrastructure and cytochemistry of vitellogenesis in Wenyonia virilis Woodland, 1923 (Cestoda, Caryophyllidea)

Vitellogenesis in Wenyonia virilis was examined by transmission electron microscopy (TEM), including the cytochemical detection of glycogen at the ultrastructural level with the periodic acid-thiosemicarbazide-silver proteinate (PA-TSC-SP) technique. Mature vitelline follicles have cells in various stages of development, progressing from immature cells of gonial type near the periphery of the follicle to maturing and mature vitellocytes towards the centre. Maturation is characterized by: (1) increase in cell volume; (2) increase in nuclear surface area restoring the N/C (nucleo-cytoplasmic) ratio; (3) nucleolar transformation; (4) extensive development of parallel cisternae of GER, the shell-protein producing units; (5) development of Golgi complexes, engaged in shell-granule/shell-globule formation and packaging; (6) synthesis and storage of glycogen in the cytoplasm; (7) simultaneous, independent formation and storage of intranuclear glycogen; (8) continuous fusion of small shell-granules into larger shell-globules and fusion of these into large shell-globule clusters with a progressive increase in the number and size of the latter; and (9) disintegration of GER in the medial layer of vitellocyte cytoplasm, degenerative changes and accumulation of glycogen and shell-globule clusters within the cytoplasm. The functional significance of numerous shell-globule clusters and the relatively small amount of nuclear and cytoplasmic glycogen is analysed. Unlike vitellogenesis of other caryophyllids, the nuclear glycogen of mature vitellocytes in W. virilis is randomly dispersed in the nucleoplasm and never forms a high central accumulation, the so-called “nuclear vacuole”. The nutritive function of vitellocytes appears greatly reduced in W. virilis, a fact perhaps related to the intrauterine development of the early embryos. The ultrastructure of vitellogenesis in W. virilis is compared with that in other lower cestodes, both monozoic and polyzoic. Conclusions concerning interrelationships of the vitellogenesis pattern of the ultrastructural cytochemistry of mature vitellocytes of W. virilis to intrauterine embryonation, absence of uterine glands and an extensive uterus characteristic for this species, are drawn and discussed.

Ultrastructure of vitellocytes in the cestode Progrillotia pastinacae Dollfus, 1946 (Trypanorhyncha, Progrillotiidae)

The present study describes the ultrastructure of mature vitellocytes of the trypanorhynch cestode Progrillotia pastinacae Dollfus, 1946 (Progrillotiidae), a parasite of the common stingray Dasyatis pastinaca (Linnaeus, 1758) (Dasyatidae). The vitelline cells of this species measure about 24 μm in length and about 20 μm in width. They have small, elongated, slightly lobulated nuclei, about 4–5 μm in length, with large dense elongated nucleoli and numerous irregularly-shaped dense clumps of heterochromatin. The extensive cytoplasm is rich in numerous cell organelles and cell inclusions. While the perinuclear cytoplasm contains numerous long parallel cisternae of GER, ribo-and polyribosomes, several Golgi complexes and mitochondria, the peripheral cytoplasm contains predominantly three types of cell inclusions: a great number of large lipid droplets, several shell globule clusters, and a very small amount of glycogen-like particles. The most characteristic features of vitellocytes in P. pastinacae are having almost no traces of glycogen and the great number of large, highly osmiophobic lipid droplets representing saturated fatty acids. The presence of large amounts of lipids also in two other trypanorhynchs, Grillotia erinaceus (Beneden, 1858) Guiart, 1927 and Dollfusiella spinulifera (Beveridge et Jones, 2000) Beveridge, Neifar et Euzet, 2004, is in strong contrast to the condition in the most evolved cestodes, Cyclophyllidea, that usually show no trace of lipids.