Abstract
This study deals with first ultrastructure features of Acanthocephaloides incrassatus (Paleacanthocephala, Arhythmacanthidae), a parasite of the fish Anguilla anguilla, reported for the first time in a Mediterranean pond. The spermiogenesis of A. incrassatus shows original specificities which have never been pointed out to this day in ultrastructural studies on spermiogenesis: the centriolar derivative is divided into two parts of different densities: an electron-dense, and the other, electron-lucent; a ring form has been observed on each side of the axoneme; a centriole with one central element. After the elaboration of a flagellum of 9 + 2 pattern, the centriole migrates in a nuclear groove. Rapidly, the centriole disappears. Then, the flagellum migration occurs by a series of processes and gives rise to a spermatozoon. The spermatozoon of A. incrassatus presents its own specificities: it exhibits an evolution of the centriolar derivative characterized by only nine peripheral elements deprived of a central element in the anterior part, then nine peripheral and one central element, and finally, nine peripheral elements with two central elements. An assumption is emitted on a probable correspondence of the evolution of the derivative centriolar during the spermiogenesis and the evolution that occurs in the spermatozoon. Protein granules also show different sizes and forms, full or emptied of their contents compared with data on other Acanthocephala.
Similar content being viewed by others
References
Brunanska M, Nebesarova J, Scholz T, Fagerholm HP (2002) Ultrastructure of the spermatozoon of the pseudophyllidean cestode Eubothrium crassum (Bloch, 1779). Parasitol Res 88:285–291
Brunanska M, Nebesarove J, Scholz T, Fagerholm HP (2001) Spermiogenesis in the pseudophyllid cestode Eubothrium crassum (Bloch, 1779). Parasitol Res 87:579–588
Brunanska M, Poddubnaya LG (2006) Spermiogenesis in the caryophyllidean cestode Khawia armeniaca (Cholodkovski, 1915). Parasitol Res 99:449–454
Brunanska M, Scholz T, Nebesarova J (2003) Reinvestigation of the spermatozoon ultrastructure of the cestode Proteocephalus longicollis (Zeder, 1800), a parasite of salmonid fish. Parasitol Res 91:357–362
Carcupino M, Dezfuli BS (1995) Ultrastructural study of mature sperm of Pomphorhynchus laevis Müller (Acanthocephala, Paleacanthocephala) a fish parasite. Invertebr Reprod Dev 28(1):25–32
Carcupino M, Dezfuli BS (1999) Acanthocephala. In: Jamieson BGM (ed) Reproductive biology of invertebrates, vol IX, Progress in male gamete ultrastructure and phylogeny. Oxford and IBH publishing Co, New Dehli, pp 229–242
Crompton DWT (1970) An ecological approach to acanthocephalan physiology. Cambridge University Press, Cambridge
Crompton DWT, Nickol BB (1985) Biology of the Acanthocephala. Cambridge University Press, Cambridge
Crompton DWT, Nickol BB (2009) Biology of the Acanthocephala. Cambridge University Press, Cambridge
Foata J, Culioli JL, Marchand B (2005) Ultrastructure of spermiogenesis and the spermatozoon of Macracanthorhynchus hirudinaceus (Pallas, 1781) (Acanthocephala: Archiacanthocephala), a parasite of the wild boar Sus scrofa. J Parasitol 91(3):499–506
Foata J, Dezfuli BS, Pinelli B, Marchand B (2004) Ultrastructure of spermiogenesis and spermatozoon of Leptorhynchoides plagicephalus (Acanthocephala, Palaeacanthocephala), a parasite of the sturgeon Acipenser naccarii (Osteichthyes, Acipenseriformes). Parasitol Res 93(1):582–589
Guraya SS (1971) Morphological and histochemical observations on the acanthocephalan spermatogenesis. Acta Morphol Neerl Scand 9(1):75–83
Hyman HL (1951) The invertebrates: Acanthocephala, Aschelminthes, and Entoprocta. In: The pseudocoelompate Bilateria. McGraw-Hill, New York, pp 459–531, 3
Kennedy CR (2006) Ecology of the Acanthocephala. Cambridge University Press, New York
Levron C, Brunanska M, Marchand B (2005) Spermiogenesis and sperm ultrastructure of the pseudophyllidean cestode Triaenophorus nodulosus (Pallas, 1781). Parasitol Res 98(1):26–33
Marchand B, Mattei X (1976a) Présence de flagelles spermatiques dans les sphères ovariennes des Eoacanthocéphales. J Ultra Res 56(3):331–338
Marchand B, Mattei X (1976b) La Spermatogenèse des Acanthocéphales II. Variation du nombre de fibres centrales dans le flagelle spermatique d'Acanthosentis tilapiae Baylis, 1947 (Eocanthocephala, Quadrigyridae). J Ultra Res 55:391–399
Marchand B, Mattei X (1976c) Ultrastructure du spermatozoïde de Centrorhynchus milvus Ward, 1956 (Paleacanthocephala, Polymorphidae). C R Seances Soc Biol 170(1):237–240
Marchand B, Mattei X (1976d) La Spermatogenèse des Acanthocéphales I. L'Appareil Centriolaire et Flagellaire au Cours de la Spermiogenèse d'Illiosentis furcatus var africana Golvan, 1956 (Paleacanthocephala, Rhadinorhynchidae). J Ultra Res 54:347–358
Marchand B, Mattei X (1977a) Un type nouveau de structure flagellaire. Type 9 + n. J Cell Biol 72:707–713
Marchand B, Mattei X (1977b) La Spermatogenèse des Acanthocéphales III. Formation du dérivé centriolaire au cours de la spermiogenèse de Serrasentis socialis Van Cleava, 1924 (Paleacanthocephala, Gorgorhynchidae). J Ultra Res 59:263–271
Marchand B, Mattei X (1978a) La Spermatogenèse des Acanthocéphales. IV. Le dérivé nucléocytoplasmique. Bio Cell 31(1):79–90
Marchand B, Mattei X (1978b) La Spermatogenèse des Acanthocéphales. V. Flagellogenèse chez un Eoacanthocephala: Mise en place et Désorganisation de l'Axonème Spermatique. J Ultra Res 63:41–50
Marques JF, Santos MJ, Cabral HN (2009) Zoogeographical patterns of flatfish (Pleuronectiformes) parasites in the Northeast Atlantic and the importance of the Portuguese coast as a transitional area. Science Marine 73(3):1–5
Miquel J, Marchand B (1997) Ultrastructure of the spermatozoon of Dipylidium caninum (Cestoda, Cyclophyllidea, Dilepididae), intestinal parasite of Canis familiaris. Parasitol Res 83:349–355
Miquel J, Marchand B (1998) Ultrastructure of the spermatozoon of the bank vole tapeworm, Paranoplocephala omphalodes (Cestoda, Cyclophyllidea, Anoplocephalidae). Parasitol Res 84:239–245
Miquel J, Nourrisson C, Marchand B (2000) Ultrastructure of spermiogenesis and the spermatozoon of Opecoeloides furcatus (Trematoda, Digenea, Opecoelidae), a parasite of Mullus barbatus(Pisces, Teleostei). Parasitol Res 86(4):301–310
Ndiaye P, Miquel J, Marchand B (2003) Ultrastructure of spermiogenseis and spermatozoa of Taenia parva Baer, 1926 (Cestoda, Cyclophyllidea, Taeniidae), a parasite of the common genet (Genetta genetta). Parasitol Res 89(1):34–43
Petrochenko VI (1956) Acanthocephala of domestic and wild animals., vol 1. Ed. edn. K. I. Skrjabin, Moscow: Izdatel'stvo Akademii Nauk SSSR
Petrochenko VI (1958) Acanthocephala of domestic and wild animals., vol 2. Ed. edn. K. I. Skrjabin, Moscow: Izdatel'stvo Akademii Nauk SSSR
Quilichini Y, Foata J, Justine J-L, Bray RA, Marchand B (2009) Sperm ultrastructure of the digenean Siphoderina elongata (Platyhelminthes, Cryptogonimidae) intestinal parasite of Nemipterus furcosus (Pisces, Teleostei). Parasitol Res 105:87–95
Quilichini Y, Foata J, Marchand B (2007a) Ultrastructural study of the spermatozoon of Pronoprymna ventricosa (Digenea, Baccigerinae), parasite of the twaite shad Alosa fallax Lacepede (Pisces, Teleostei). Parasitol Res 101(4):1125–1130
Quilichini Y, Foata J, Marchand B (2007b) Ultrastructural study of the spermatozoon of Nicolla testiobliquum (Digenea, Opecoelidae) parasite of brown trout Salmo trutta (Pisces, Teleostei). Parasitol Res 101(5):1295–1301
Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212
Seck MT, Marchand B, Bâ CT (2007) Ultrastructure of spermiogenesis and the spermatozoon of Paramphistomum microbothrium (Fischoeder 1901; Digenea, Paramphistomidae), a parasite of Bos taurus in Senegal. Parasitol Res 101:259–268
Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultra Res 26:31–43
Watson NA, Rohde K (1992) Ultrastructure of sperm and spermatogenesis of Rugogaster hydrolagi, Schell 1973 (Platyhelminthes, Trematoda, Aspidogastrea, Rugogastridae). Parasitol Res 78:516–524
Whitfield PJ (1971) Spermiogenesis and spermatozoa ultrastructure in Polymorphus minutus (Acanthocephala). Parasitol 62:415–430
Yamaguti S (1963) Acanthocephala, vol V. Wiley, New York
Acknowledgments
Many thanks to the fishermen of Urbino ponds who have provided us fishes and thus permitted us to carry out this parasitological ultrastructural work.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Foata, J., Quilichini, Y., Dal Pos, N. et al. Ultrastructural study of spermiogenesis and the spermatozoon of Acanthocephaloides incrassatus (Molin, 1858) (Acanthocephala, Paleacanthocephala, Arhythmacanthidae) from Anguilla anguilla (Pisces, Teleostei) in Urbino ponds (Corsica Island). Parasitol Res 111, 271–281 (2012). https://doi.org/10.1007/s00436-012-2831-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-012-2831-z