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)

Abstract

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

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

“…Interstitial tissue has been proposed to be involved in selection and distribution of nutrients transported from the parenchyma toward the vitellocytes of some cestodes (Xylander, 1988;Bruňanská et al, 2009), and monogeneans (Halton et al, 1974). In addition to the caryophyllideans, interstitial tissue has been observed also in spatheboth- riideans (Bruňanská et al, 2005;Poddubnaya et al, 2006), bothriocephalideans (Korneva, 2001;Levron et al, 2007;Świderski et al, 2011a), trypanorhynchs (Świderski et al, 2006b; 2012), nippotaeniideans (Korneva, 2002), and proteocephalideans (Korneva & Davydov, 2001). Interstitial cells may also occur in some trypanorhynchs (Świderski et al, 2006a, 2007, 2012).…”

Ultrastructure of vitellogenesis and vitellocytes in the trypanorhynch cestode Aporhynchus menezesi, a parasite of the velvet belly lanternshark Etmopterus spinax

“…TEM results in more recent studies on this subject have been dealt with in both the "Discussion" and " Table I" of a paper on vitellogenesis of the bothriocephalidean cestode Clestobothrium crassiceps [13].…”

“…However, variation in the formation and storage of embryonic nutritive reserves in the various cestode groups has been observed in relation to differences in the proportion and amounts of glycogen and lipids [see 7,13,28,34]. There are extreme cases, such as the caryophyllideans, where glycogen only is accumulated in both the vitellocyte cytoplasm and its nucleus [23,24,26,27); another such extreme example occurs in rhinebothriidean vitellocytes [29], where generally lipids only are accumulated in both the cytoplasm and the nucleus.…”

“…There are extreme cases, such as the caryophyllideans, where glycogen only is accumulated in both the vitellocyte cytoplasm and its nucleus [23,24,26,27); another such extreme example occurs in rhinebothriidean vitellocytes [29], where generally lipids only are accumulated in both the cytoplasm and the nucleus. A recent comparison of both types of embryonic nutritive reserves in the vitellocytes of lower cestodes was presented [13].…”

Early intrauterine embryonic development of the bothriocephalidean cestode Clestobothrium crassiceps (Rudolphi, 1819), a parasite of the teleost Merluccius merluccius (L., 1758) (Gadiformes: Merlucciidae)

“…One of the aims of the present study was not only to describe the ultrastructure of the intrauterine eggs of C. crassiceps, but also to relate this to the vitellogenesis of this parasite [29]. Vitellocytes in cestodes have two important functions, i.e.…”