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

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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 established between spermatozoa of Bothriocephalidea and Diphyllobothriidea, the type of spermatozoon (II vs I) and the presence/absence of the ring of cortical microtubules.

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Acknowledgments

We are grateful to the “Unitat de Microscòpia, Facultat de Medicina, Centres Científics i Tecnològics de la Universitat de Barcelona (CCiTUB)” for their support in the preparation of samples, particularly Núria Cortadellas and Almudena García. The present study was partially funded by the Spanish project CTM2009-08602. Adji Mama Marigo benefits from doctoral grants (2009–2010 no. 0000448124 and 2010–2011 no. 0000538056) of “Ministerio de Asuntos Exteriores y de Cooperación, Agencia Española de Cooperación Internacional para el Desarrollo MAEC-AECID”.

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  1. Laboratori de Parasitologia, Departament de Microbiologia i Parasitologia Sanitàries, Facultat de Farmàcia, Universitat de Barcelona, Av. Joan XXIII, sn, E08028, Barcelona, Spain

    Adji Mama Marigo, Jordi Torres & Jordi Miquel

  2. Institut de Recerca de la Biodiversitat, Facultat de Biologia, Universitat de Barcelona, Av. Diagonal, 645, E08028, Barcelona, Spain

    Adji Mama Marigo, Jordi Torres & Jordi Miquel

  3. Departament de Ciències Ambientals, Facultat de Ciències, Universitat de Girona, Campus de Montilivi, sn, E17071, Girona, Spain

    Eulàlia Delgado

  4. Laboratoire de Parasitologie, Département de Biologie animale, Faculté des Sciences, Université Cheikh Anta Diop de Dakar, Dakar, Senegal

    Cheikh Tidiane Bâ

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  1. Adji Mama Marigo
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  2. Eulàlia Delgado
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Marigo, A.M., Delgado, E., Torres, J. et al. Spermiogenesis and spermatozoon ultrastructure of the bothriocephalidean cestode Clestobothrium crassiceps (Rudolphi, 1819), a parasite of the teleost fish Merluccius merluccius (Gadiformes: Merlucciidae). Parasitol Res 110, 19–30 (2012). https://doi.org/10.1007/s00436-011-2446-9

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