Spermiogenesis and spermatozoon ultrastructure of the bothriocephalidean cestode Clestobothrium crassiceps (Rudolphi, 1819), a parasite of the teleost fish Merluccius merluccius (Gadiformes: Merlucciidae)

Abstract

Spermiogenesis and the ultrastructure of the spermatozoon of the bothriocephalidean cestode Clestobothrium crassiceps (Rudolphi, 1819), a parasite of the teleost fish Merluccius merluccius (Linnaeus, 1758), have been studied by means of transmission electron microscopy. Spermiogenesis involves firstly the formation of a differentiation zone. It is characterized by the presence of two centrioles associated with striated rootlets, an intercentriolar body and an electron-dense material in the apical region of this zone. Later, two flagella develop from the centrioles, growing orthogonally in relation to the median cytoplasmic process. Flagella then undergo a rotation of 90° until they become parallel to the median cytoplasmic process, followed by the proximodistal fusion of the flagella with the median cytoplasmic process. The nucleus elongates and afterwards it migrates along the spermatid body. Spermiogenesis finishes with the appearance of the apical cone surrounded by the single helical crested body at the base of the spermatid. Finally, the narrowing of the ring of arched membranes detaches the fully formed spermatozoon. The mature spermatozoon of C. crassiceps is filiform and contains two axonemes of the 9+"1" trepaxonematan pattern, a parallel nucleus, parallel cortical microtubules and electron-dense granules of glycogen. The anterior extremity of the gamete exhibits a short electron-dense apical cone and one crested body, which turns once around the sperm cell. The first axoneme is surrounded by a ring of thick cortical microtubules that persist until the appearance of the second axoneme. Later, these thick cortical microtubules disappear and thus, the mature spermatozoon exhibits two bundles of thin cortical microtubules. The posterior extremity of the male gamete presents only the nucleus. Results are discussed and compared particularly with the available ultrastructural data on the former "pseudophyllideans". Two differences can be stablished between spermatozoa of Bothriocephalidea and Diphyllobothriidea, the type of spermatozoon (II vs I) and the presence/absence of the ring of cortical microtubules.

Spermatological characters in the diphyllobothriidean Schistocephalus solidus (Cestoda)

“…2006a, 2009), and it is also the typical pattern for the orders Spathebothriidea, Bothriocephalidea, Trypanorhyncha, Tetraphyllidea – Onchobothriidae, Tetraphyllidea – Phyllobothriidae and Proteocephalidea (Justine 1998; Levron et al. 2010; Marigo et al. 2011b, in press).…”

“…2005, 2006a,c; Šípková et al. 2010; Marigo et al. in press), and in Spathebothriidea, Trypanorhyncha, Tetraphyllidea, Proteocephalidea and Mesocestoididae (see Miquel et al.…”

A reinvestigation of spermiogenesis in Amphilina foliacea (Platyhelminthes: Amphilinidea)

“…The present paper shows that the intercentriolar body is present during spermiogenesis of A. foliacea and consists of three electron-dense plates delimited by two electron-lucent zones. Intercentriolar bodies of similar structure have been described in some caryophyllideans (Miquel et al 2008, Bruňanská 2009, 2010, Yoneva et al 2011, 2012a, b, Bruňanská and Kostič 2012, spathebothriideans (Bruňanská et al 2006, Bruňanská andPoddubnaya 2010), bothriocephalideans (Levron et al 2005, 2006a, Šípková et al 2010, 2011, Marigo et al 2012a) and mesocestoidid 'cyclophyllideans' (Miquel et al 2007). A more developed intercentriolar body composed of up to five electron-dense plates has been reported in the amphilinidean Austramphilina elongata (by Rohde and Watson 1986), and diphyllobothriideans (Levron et al 2006b(Levron et al , 2009a(Levron et al , 2013.…”

“…This remarkable character has been found in some other tapeworms, e.g. caryophyllideans (Bruňanská and Poddubnaya 2006, Gamil 2008, Miquel et al 2008, Bruňanská 2009, 2010, Yoneva et al 2011, 2012a, b, Bruňanská and Kostič 2012, spathebothriideans (Bruňanská et al 2006, Bruňanská andPoddubnaya 2010), bothriocephalideans (Bruňanská et al 2001, Levron et al 2005, 2006a, Šípková et al 2010, 2011, Marigo et al 2012a, diphyllobothriideans (Levron et al 2006b(Levron et al , 2009a(Levron et al , 2013 and proteocephalideans (Marigo et al 2012b). Apical electron-dense material has never been reported during spermiogenesis in the Digenea or Monogenea.…”

Ultrastructure of the sperm of Adelobothrium sp. (Cestoda: Lecanicephalidea)

“…; Bruňanská & Kostič ; Marigo et al. ,b). Although data on spermatozoan ultrastructure for members of most cyclophyllidean families are present in the literature, a mere 2% of the total species diversity within this very species‐rich order (~3000 described species; Caira & Littlewood ) has been studied.…”