Spermiogenesis and spermatozoon ultrastructure of the paruterinid cestode Notopentorchis sp. (Cyclophyllidea)

Abstract

Ultrastructural characters of the spermiogenesis and mature spermatozoon of Notopentorchis sp. (Cestoda, Cyclophyllidea, Paruterinidae), a parasite from Apus affinis (Aves, Apodiformes, Apodidae) from Gabon, are described by means of transmission electron microscopy. Cytochemical analysis for detection of glycogen was applied. Vestigial striated roots associated with the two centrioles are present in the zone of differentiation. The spermiogenesis is characterized by an external growth of free flagellum followed by a proximodistal fusion of the latter with cytoplasmic protrusion, thus, corresponding to the cestode spermiogenesis of the type III pattern described by Bâ and Marchand (Mem. Mus. Natl. Hist. Nat. 166:87-95, 1995). In the final stage of spermiogenesis, a single crested body appears at the base of the forming spermatozoon. The mature spermatozoon of Notopentorchis sp. is filiform and tapering at both extremities. It consists of five regions differing in their ultrastructural characteristics. The anterior extremity of the mature spermatozoon is characterized by the presence of an apical cone and a single crested body. The cytoplasm contains one axoneme of 9 + "1" type of the trepaxonematan Platyhelminthes, a periaxonemal sheath, a layer of twisted cortical microtubules, transverse intracytoplasmic walls, and granules of glycogen. The nucleus is coiled in spiral around the axoneme. The posterior extremity of the spermatozoon is characterized by the presence of electron-dense material. This structural organization corresponds to the morphology of cestode spermatozoon of type VII as defined by Levron et al. (Biol Rev 85: 523-543, 2010). The comparison of the results with those of the two previous studies on paruterinids suggests that several characters of the spermiogenesis and the mature spermatozoon are invariable, i.e. the type III spermiogenesis and the presence of vestigial striated roots, a single crested body, a periaxonemal sheath, and intracytoplasmic walls. The main differences of the sperm cells among members of this family are the lack of dense granules (as in Triaenorhina rectangula) and the presence of electron-dense material in the posterior extremity of the spermatozoon (as in Notopentorchis sp.).

Spermatological Characterization of the Cestode Meggittina gerbilli (Cyclophyllidea: Catenotaeniidae), a Parasite of Gerbils, Gerbillus gerbillus and Gerbillus campestris (Rodentia: Muridae) in Tunisia

“…Likewise, other cyclophyllideans did not fit the traditional type III spermiogenesis proposed by Bâ and Marchand [ 20 ]. These are the paruterinids Anonchotaenia globata , Notopentorchis sp., and Triaenorhina rectangula [ 28 , 36 , 37 ], and the taeniids Taenia parva and Taenia taeniaeformis [ 38 , 39 ]. Finally, a doubtful slight flagellar rotation, unsupported by the published TEM micrographs, has been mentioned in the metadilepidid Skrjabinoporus merops [ 40 ].…”

“…However, striated rootlets or similar structures are observed in some cyclophyllideans presenting spermiogenesis types III or IV. This is the case for the dipylidiids Dipylidium caninum , Joyeuxiella echinorhynchoides , and Joyeuxiella pasqualei , the paruterinids A. globata , Notopentorchis sp., and T. rectangula , and the taeniid T. taeniaeformis , which present striated rootlets or vestigial striated rootlets associated with the centrioles in a type III spermiogenesis [ 28 , 36 , 37 , 39 , 41 , 42 ]. Moreover, these structures are also present in the anoplocephalids Anoplocephaloides dentata , Gallegoides arfaai , and Mosgovoyia ctenoides , which follow a type IV spermiogenesis [ 43 , 44 , 45 ].…”

“…Thus, sperm cells with two axonemes are present in the orders Diphyllobothriidea, Spathebothriidea, Haplobothriidea, Onchoproteocephalidea, and Trypanorhyncha [21][22][23][46][47][48][49][50][51][52][53][54][55][56][57][58][59][60]. Contrarily, spermatozoa with one axoneme are present in the orders Caryophyllidea, Cyclophyllidea, Lecanicephalidea, Nippotaeniidea, Phyllobothriidea, and Tetrabothiidea [21][22][23][26][27][28][29][30][31][32][61][62][63][64][65][66][67][68][69][70][71][72]. In the order Diphyllidea, there are some discrepancies between the spermiogenesis process and the resulting spermatozoa.…”

“…In the Cestoda, there are numerous ultrastructural studies describing spermiogenesis and/or the spermatozoon, particularly in the order Cyclophyllidea [ 23 , 26 , 27 , 28 , 29 , 30 , 31 , 32 ]. However, in the Catenotaeniidae family, ultrastructural aspects of spermiogenesis and/or the spermatozoon have only been studied in two species, namely Catenotaenia pusilla (Goeze, 1782) (Catenotaeniinae Spassky, 1950) and Skrjabinotaenia lobata (Baer, 1925) (Skrjabinotaeniinae) [ 33 , 34 ].…”