Where are the sensory organs of Nybelinia surmenicola (Trypanorhyncha)? A comparative analysis with Parachristianella sp. and other trypanorhynchean cestodes

Abstract

The sensory organs in tegument of two trypanorhynchean species--Nybelinia surmenicola (plerocercoid) and adult Parachristianella sp. (Cestoda, Trypanorhyncha)--were studied with the aim of ultrastructural description and a comparative analysis. The Nybelinia surmenicola plerocercoid lacks papillae with sensory cilia on the bothria adhesive surface. We found an unciliated sensory organ within the median bothria fold. This unciliated free nerve ending contains the central electron-dense disc, three dense supporting rings, and broad root. The nerve ending locates in the basal matrix under the tegument. The tegument of N. surmenicola has a number of ultrastructural features which make it significantly different from other Trypanorhyncha: (i) the tegumental cytoplasm has a plicated constitution in a form of high apical and deep basal folds, (ii) numerous layers of the basal matrix are presented in the subtegument, and (iii) the squamiform and bristlelike microtriches N. surmenicola lack the base and the basal plate. In contrast, numerous ciliated and unciliated receptors were found in Parachristianella sp.: six types on the bothria and one type in the strobila tegument. Ultrastructural constitution of sensory organs in the form of ciliated free nerve endings as well as unciliated basal nerve endings of Parachristianella sp. has many common features inside Eucestoda. In comparison with other Trypanorhyncha, all Nybelinia species studied have less quantity of the bothrial sensory organs. This fact may reflect behavioral patterns of Nybelinia as well as phylogenetic position into Trypanorhyncha. Our observations of living animals conventionally demonstrate the ability of N. surmenicola plerocercoids to locomote in forward direction on the Petri dish surface. The participation of the bothrial microtriches in a parasite movement has been discussed.

Ultrastructure of the scolex of Orygmatobothrium schmittii (Cestoda: Phyllobothriidea)

“…In contrast to the diversity of shapes of the spinitriches (Chervy, ), the filitriches slightly differ internally in the relative length of the cap and the base, as it has been reported in some trypanorhynchs (Biserova et al, ; Palm et al, ). In O. schmittii, the spinitriches have caps that are longer than the base (cap/base length ratio up to 1:0.43), whereas most filitriches have short caps and longer bases (cap/base length ratio over 1:1.06), except on the apical suckers (ratio cap/base length ratio 1:0.37), and the distal bothridial surface (ratio cap/base length ratio 1:0.67–1.43).…”

“…Sensory receptors similar to the Type B receptor of O. schimittii (i.e., having a cilium, and two electro‐dense supporting rings) were observed in Gyrocotylidea (Allison, ), Diphyllobothriidea (Mustafina & Biserova, ), Cyclophyllidea (Webb & Davey, ), Trypanorhyncha (Biserova et al, ; Casado et al, ; Palm et al, ), and Onchoproteocephalidea (Brunanska et al, ). Some authors have suggested that these receptors might act as mechanoreceptors based on their position in attachment organs such as the rosette of gyrocotylideans, or the bothria of trypanorhynchs (Allison, ; Palm et al, ).…”

“…In spinitriches, the cap has been described as formed by an internal medulla and external cortex (e.g., bifid, hamulate, hastate, palmate, and pectinate spinitriches in Onchoproteocephalidea and Trypanorhyncha; Jones & Beveridge, ; Palm, Poynton, & Rutledge, ; Palm et al, ; Thompson et al, ), a massive medulla without cortex (i.e., coniform, gladiate, hamulate, hastate, palmate, pectinate, and trifid spinitriches in Bothriocephalidea, Cyclophyllidea, Diphyllidea, Diphyllobothriidea, Litobothridea, Onchoproteocephalidea, Phyllobothriidea, Tetraphyllidea, and Trypanorhyncha; e.g., Biserova, ; Biserova et al, ; Faliex, Tyler, & Euzet, ; Fyler, ; Gallagher, Caira, & Cantino, ; Hess & Guggenheim, ; Levron et al, ; McCullough & Fairweather, ; Palm, ; Thompson et al, ; Yoneva et al, ; Zd'árská, Scholz, & Nebesárová, ), or an internal medulla covered by a bilayer cortex (i.e., presumably coniform spinitriches in H. diminuta Cyclophylidea; Holy & Oaks, ). The gongylate spinitriches of O. schmittii have a well‐defined medulla and cortex, with lateral projections of the cytoplasmic membrane, adding more diversity to the internal morphology of the different spinitriches.…”

“…The capilliform filitriches on the apical suckers and the acicular filitriches on the glandulomuscular organs lack a baseplate. Some microtriches in other taxa have also been described as lacking baseplates, such as the “bristlelike electron‐dense microtriches” described by Biserova et al (), and the hamulate spinitriches in trypanorhynchs (Chervy, ; Palm, ). However, we cannot dismiss that the absence of baseplate might be related to an artifact due to optical limitations, or microthrix orientation during the sectioning.…”

“…In tapeworms, sensory receptors have been described as embedded in tegumental projections, immersed in the distal cytoplasm or sunk in tegumental pits (e.g., Biserova et al, ; Brunanska et al, ; Casado, Moreno, Urrea‐Paris, & Rodriguez‐Caabeiro, ). In O. schmittii, the receptors are either related to tegumental projections (Type A), or immersed in the distal cytoplasm (Type B).…”