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Parasitol Res (2003) 91: 175–186 DOI 10.1007/s00436-003-0936-0

O R I GI N A L P A P E R

Papa Ibnou Ndiaye Æ Sylvia Agostini Æ Jordi Miquel Bernard Marchand

Ultrastructure of spermiogenesis and the spermatozoon in the genus Joyeuxiella Fuhrmann, 1935 (Cestoda, Cyclophyllidea, Dipylidiidae): comparative analysis of J. echinorhynchoides (Sonsino, 1889) and J. pasqualei (Diamare, 1893)Received: 17 April 2003 / Accepted: 30 May 2003 / Published online: 9 August 2003 Ó Springer-Verlag 2003

Abstract This paper describes the ultrastructure of spermiogenesis and the mature spermatozoon of two Dipylidiidae cestodes, Joyeuxiella echinorhynchoides and J. pasqualei. In both species, spermiogenesis follows the type III described by Ba and Marchand for the cycloˆ phyllideans. Nevertheless,it is interesting to note the presence of striated roots associated with the centrioles. The spermatozoon presents the same ultrastructural features in J. echinorhynchoides and J. pasqualei. The apical cone in the anterior extremity of the sperm is more than 2.0 lm long in both J. echinorhynchoides and J. pasqualei. Both species present a single crest-like body, 150 nm thick in J.echinorhynchoides and 75 nm thick in J. pasqualei. The cortical microtubules are spiralled at an angle of 40–45° to the spermatozoon axis in both Joyeuxiella species. A periaxonemal sheath and glycogen granules are also described in the mature sperm. We also describe, for the first time, the disposition of glycogen granules in two opposed and spiralled cords in cestodes and the formation of the periaxonemalsheath in the final stage of spermiogenesis.

Introduction
The taxonomy of the dilepidid cestodes sensu lato at the family level and below has long been a subject of debate. Some authors have recognized one family, Dilepididae, with three subfamilies: Dilepidinae, Dipylidiinae and Paruterininae (e.g. Yamaguti 1959; Schmidt 1986).
P. I. Ndiaye Æ S. Agostini Æ J. Miquel (&) ` Laboratori deParasitologia, Facultat de Farmacia, Universitat de Barcelona, Av. Joan XXIII s/n, 08028 Barcelona, Spain E-mail: jordimiquel@ub.edu Fax: +34-93-4024504 B. Marchand Æ S. Agostini ´ ` ´ ´ Laboratoire Parasites et Ecosystemes Mediterraneens, ´ ´ Faculte des Sciences et Techniques, Universite de Corse, 20250 Corte, France

Others have given each of these subfamilies the rank of family (e.g. Matevosyan 1953,1963; Wardle et al. 1974). According to Jones (in Khalil et al. 1994), the revision of the group has resulted in the recognition of the families Dilepididae Fuhrmann, 1907; Metadilepididae Spasskii, 1959; Paruterinidae Fuhrmann, 1907 and Dipylidiidae Stiles, 1896. The Dipylidiidae are represented by only three genera: Dipylidium Leuckart, 1863; Diplopylidium Beddard, 1913 and Joyeuxiella Fuhrmann,1935, all parasites of carnivores. It has now been clearly demonstrated that spermatozoon and spermiogenesis ultrastructure reveal significant characters for phylogenetic inference in parasitic Platyhelminthes (Euzet et al. 1981; Justine 1991, 1998; Ba and Marchand 1995). In Cyclophyllidea, data are ˆ available for nine of the 15 families recognized by Khalil et al. (1994) (see Ndiaye et al. 2003).Ultrastructural studies of the male gamete in Dipylidiidae have only been carried out in Dipylidium caninum (Miquel and Marchand 1997; Miquel et al. 1998). In the present work, we describe the ultrastructural features of spermiogenesis and the spermatozoon of other Dipylidiidae species belonging to the genus Joyeuxiella, a genus that comprises only three species J. echinorhynchoides (Sonsino,1889), J. fuhrmanni (Baer, 1924) and J. pasqualei (Diamare, 1893) (see Jones 1983). The two species investigated in terms of their spermatozoa and spermiogenesis in the present work are J. echinorhynchoides and J. pasqualei. Following our study, the available ultrastructural data for three species belonging to two of the three genera of the Dipylidiidae allow us to establish several characteristics...
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