Abstract
Spermiogenesis in progenetic and adult stages of Archigetes sieboldi Leuckart, 1878, a tapeworm parasitic in oligochaetes and fish respectively, has been examined using transmission electron microscopy and cytochemical staining for glycogen. General pattern of spermiogenesis is essentially like that of other caryophyllideans, i.e., apical dense material in the zone of differentiation in the early stages of spermiogenesis, rotation of free flagellum and a flagellar bud, and proximo-distal fusion. Interestingly, rotation of a free flagellum and flagellar bud to the median cytoplasmic process (MCP) has been observed unconventionally at > 90° only in progenetic stages. Typical striated roots associated with the centrioles occur rarely in A. sieboldi, and only in form of faint structures in advanced stages of spermiogenesis. In contrast to most caryophyllideans studied to date, penetration of the nucleus into the spermatid body has started before the fusion of the free flagellum with the MCP. This feature has been reported rarely but exclusively in the family Caryophyllaeidae. The unipartite mature spermatozoon of A. sieboldi is composed of one axoneme of the 9 + ‘1’ trepaxonematan pattern with its centriole, parallel nucleus, and parallel cortical microtubules which are situated in a moderately electron-dense cytoplasm with glycogen particles. An unusual arrangement of cortical microtubules in the two parallel rows in region I of the spermatozoon is described here for the first time in the Caryophyllidea. Ultrastructural data on spermiogenesis and the spermatozoon in A. sieboldi from tubuficids and carp are compared and discussed with those in other caryophyllideans and/or Neodermata.
Similar content being viewed by others
References
Agostini S, Miquel J, Ndiaye PI, Marchand B (2005) Dicrocoelium hospes Looss, 1907 (Digenea, Dicrocoeliidae): spermiogenesis, mature spermatozoon and ultrastructural comparative study. Parasitol Res 96:38–48
Bâ CT, Marchand B (1995) Spermiogenesis, spermatozoa and phyletic affinities in the Cestoda. In: Jamieson, BGM, Ausie J, Justine J-L (eds) advances in Spermatozoal phylogeny and taxonomy. Mém Mus natn Hist nat 166:87–95
Bruňanská M (2009) Spermatological characters of the caryophyllidean cestode Khawia sinensis Hsü, 1935, a carp parasite. Parasitol Res 105:1603–1610
Bruňanská M (2010) Recent insights into spermatozoa development and ultrastructure in the Eucestoda. In: Lejeune T, Delvaux P (eds) Human spermatozoa: maturation, capacitation and abnormalities. Nova Science Publishers, Inc., New York, pp 327–354
Bruňanská M, Kostič B (2012) Revisiting caryophyllidean type of spermiogenesis in the Eucestoda based on spermatozoon differentiation and ultrastructure of Caryophyllaeus laticeps (Pallas, 1781). Parasitol Res 110:141–149
Bruňanská M, Poddubnaya LG (2006) Spermiogenesis in the caryophyllidean cestode Khawia armeniaca (Cholodkovski, 1915). Parasitol Res 99:449–454
Bruňanská M, Poddubnaya LG (2010) Spermatological characters of the spathebothriidean tapeworm Didymobothrium rudolphii (Monticelli, 1890). Parasitol Res 106:1435–1442
Bruňanská M, Nebesářová J, Scholz T, Fagerholm H-P (2001) Spermiogenesis in the pseudophyllid cestode Eubothrium crassum (Bloch, 1779). Parasitol Res 87:579–588
Bruňanská M, Scholz T, Ibraheem MH (2004a) Ultrastructural particularities of the spermatozoon of the cestode Electrotaenia malopteruri (Fritsch, 1886) (Proteocephalidae: Gangesiinae), a parasite of Malapterurus electricus (Siluriformes: Malapteruridae) from the Nile, Egypt. Parasitol Res 93:114–120
Bruňanská M, Scholz T, Ibraheem MH (2004b) Ultrastructural characteristics of the spermatozoon of the cestode Corallobothrium solidum Fritsch, 1886 (Proteocephalidae: Corallobothriinae), a parasite of Malapterurus electricus (Siluriformes: Malapteruridae) from the Nile, Egypt. Parasitol Res 94:421–426
Bruňanská M, Scholz T, Ibraheem MH (2005) Spermiogenesis in the cestode Corallobothrium solidum Fritsch, 1886 (Proteocephalidae: Corallobothriinae), parasite of Malapterurus electricus (Siluriformes: Malapteruridae) from the Nile, Egypt. Acta Zool 86:55–61
Bruňanská M, Scholz T, Dezfuli B, Poddubnaya LG (2006) Spermiogenesis and sperm ultrastructure of Cyathocephalus truncatus (Pallas, 1781) Kessler, 1868 (Cestoda: Spathebothriidea). J Parasitol 92:884–892
Bruňanská M, Matey V, Nebesářová J (2012a) Ultrastructure of the spermatozoon of the diphyllobothriidean cestode Cephalochlamys namaquensis (Cohn, 1906). Parasitol Res 111:1037–1043
Bruňanská M, Poddubnaya LG, Xylander WER (2012b) Spermatozoon cytoarchitecture of Amphilina foliacea (Platyhelminthes, Amphilinidea). Parasitol Res 111:2063–2069
Bruňanská M, Poddubnaya LG, Xylander WER (2013) A reinvestigation of spermiogenesis in Amphilina foliacea (Platyhelminthes, Amphilinidea). Folia Parasitol 60:43–50
Bruňanská M, Bílý T, Nebesářová J (2015) Nippotaenia mogurndae Yamaguti et Myiata, 1940 (Cestoda, Nippotaeniidea): first data on spermiogenesis and sperm ultrastructure. Parasitol Res 114:1443–1453
Caira JN, Littlewood DTJ (2013) Worms, Platyhelminthes. In: Levin SA (ed) Encyclopedia of biodiversity, Academic press, vol 7, Waltham, pp 437–469
Calentine R (1964) The life cycle of Archigetes iowensis (Cestoda: Caryophyllaeidae). J Parasitol 50:454–458
Chervy L (2002) The terminology of larval cestodes or metacestodes. Syst Parasitol 52:1–33
Fuhrman O (1931) Dritte Klasse des Cladus Plathelminthes: Cestoides. In: Kükenthal W, Krumbach T (eds) Handbuch der Zoologie. Walter de Gruyter and Co., Berlin, pp 141–416
Gamil IS (2008) Ultrastructural studies of the spermatogenesis and spermiogenesis of the caryophyllidean cestode Wenyonia virilis (Woodland, 1923). Parasitol Res 103:777–785
Hoberg EP, Mariaux J, Brooks DR (2001) Phylogeny among the orders of the Eucestoda (Cercomeromorphae): integrating morphology, molecules and total evidence. In: Littlewood DTJ, Bray RA (eds) Interrelationships of the Platyhelminthes. Taylor and Francis, London, pp 112–126
Joyeux CH, Baer JG (1961) Classe des Cestodes. In: Grassé P-P (ed) Traité de Zoologie, Tome 4, Fasc, vol 1. Masson, Paris, pp 345–560
Justine J-L (1998) Spermatozoa as phylogenetic characters for the Eucestoda. J Parasitol 84:385–408
Justine J-L (2001) Spermatozoa as phylogenetic characters for the Platyhelminthes. In: Littlewood DTJ, Bray RA (eds) Interrelationships of the Platyhelminthes. Taylor and Francis, London, pp 231–238
Justine J-L (2003) Ultrastructure des spermatozoïdes et phylogénie des Neodermata. In: C. Combes C, Jourdane J (eds) Taxonomy, ecology and evolution of metazoan parasites. PUP, Perpignan, pp 359–380
Kazacos K, Mackiewicz JS (1972) Spermatogenesis in Hunturella nodulosa Mackiewicz and McCrae, 1962 (Cestoidea: Caryophyllidea). Z Parasitenkd 38:21–31
Levron C, Ternengo S, Marchand B (2003) Ultrastructure of spermiogenesis and the spermatozoon of Helicometra fasciata (Digenea, Opecoelidae), a parasite of Labrus merula (Pisces, Teleostei). Acta Parasitol 48:255–264
Levron C, Ternengo S, Marchand B (2004) Ultrastructure of spermiogenesis and the spermatozoon of Monorchis parvus Looss, 1902 (Digenea, Monorchiidae), a parasite of Diplodus annularis (Pisces, Teleostei). Parasitol Res 93:102–110
Levron C, Bruňanská M, Marchand B (2005) Spermiogenesis and sperm ultrastructure of the pseudophyllidean cestode Triaenophorus nodulosus (Pallas, 1781). Parasitol Res 98:26–33
Levron C, Bruňanská M, Poddubnaya LG (2006a) Spermatological characters of the pseudophyllidean cestode Bothriocephalus scorpii (Müller, 1776). Parasitol Int 55:113–120
Levron C, Bruňanská M, Poddubnaya LG (2006b) Spermatological characters in Diphyllobothrium latum (Cestoda, Pseudophyllidea). J Morphol 267:1110–1119
Levron C, Bruňanská M, Kuchta R, Freeman M, Scholz T (2006c) Spermatozoon ultrastructure of the pseudophyllidean cestode Paraechinophallus japonicus, a parasite of deep-sea fish Psenopsis anomala (Perciformes, Centrolophidae). Parasitol Res 100:115–121
Levron C, Sitko J, Scholz T (2009) Spermiogenesis and spermatozoon of the tapeworm Ligula intestinalis (Diphyllobothriidae): phylogenetic implications. J Parasitol 95:1–9
Levron C, Miquel J, Oros M, Scholz T (2010) Spermatozoa of tapeworms (Platyhelminthes, Eucestoda): advances in ultrastructural and phylogenetic studies. Biol Rev 85:523–543
Levron C, Yoneva A, Kalbe M (2013) Spermatological characters in the diphyllobothriidean Schistocephalus solidus (Cestoda). Acta Zool (Stockholm) 94:240–247
Mackiewicz JS (1981) Caryophyllidea (Cestoidea): evolution and classification. Adv Parasitol 19:139–206
Mackiewicz JS (2003) Caryophyllidea (Cestoidea): molecules, morphology and evolution. Acta Parasitol 48:143–154
Marigo AM, Eira C, Bâ CT, Miquel J (2011a) Spermatological characters of Acanthobothrium crassicolle Wedl, 1855 (Tetraphyllidea, Onchobothriidae), a parasite of the common stingray Dasyalis pastinaca. Acta Parasitol 56:191–201
Marigo AM, Świderski Z, Bâ CT, Miquel J (2011b) Spermiogenesis and ultrastructure of the spermatozoon of the trypanorhynch cestode Aporhynchus menezesi (Aporhynchidae), a parasite of the velvet belly, lanternshark Etmopterus spinax (Elasmobranchii: Etmopteridae). Folia Parasitol 58:69–78
Marigo AM, Delgado E, Torres J, Bâ CT, Miquel J (2012a) 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
Marigo AM, Levron C, Bâ CT, Miquel J (2012b) Ultrastructural study of spermiogenesis and the spermatozoon of the proteocephalidean cestode Barsonella lafoni de Chambrier et al., 2009, a parasite of the catfish Clarias gariepinus (Burchell, 1822) (Siluriformes, Clariidae). Zool Anz 251:17–159
Matoušková M, Bílý T, Bruňanská M, Mackiewicz JS, Nebesářová J (2018) Ultrastructure, cytochemistry and electron tomography analysis of Caryophyllaeides fennica (Schneider, 1902) (Cestoda: Lytocestidae) reveals novel spermatology characteristics in the Eucestoda. Parasitol Res 117:3091–3102
Miquel J, Świderski Z (2006) Ultrastructure of the spermatozoon of Dollfusiella spinulifera (Beveridge and Jones, 2000) Beveridge, Neifar and Euzet, 2004 (Trypanorhyncha, Eutetrarhynchidae). Parasitol Res 99:37–44
Miquel J, Feliu C, Marchand B (1999) Ultrastructure of spermiogenesis and the spermatozoon of Mesocestoides litteratus (Cestoda, Mesocestoididae). Int J Parasitol 29:499–510
Miquel J, Świderski Z, Neifar L, Eira C (2007) Ultrastructure of the spermatozoon of Parachristianella trygonis Dollfus, 1946 (Trypanorhyncha, Eutetrarhynchidae). J Parasitol 93:1296–1302
Miquel J, Świderski Z, Mackiewicz JS, Ibraheem MH (2008) Ultrastructure of spermiogenesis in the caryophyllidean cestode Wenyonia virilis Woodland, 1923, with re-assessment of flagellar rotation in Glaridacris catostomi Cooper, 1920. Acta Parasitol 53:19–29
Mokhtar-Maamouri F, Swiderski Z (1975) Étude en microscopie électronique de la spermatogénèse de deux cestodes Acanthobothrium filicolle benedenii Loennberg, 1889 et Onchobothrium uncinatum (Rud., 1819) (Tetraphyllidea, Onchobothriidae). Z Parasitenkd 47:269–281
Ndiaye PI, Miquel J, Fons R, Marchand B (2003a) Spermiogenesis and sperm ultrastructure of the liver fluke Fasciola hepatica L., 1758 (Digenea, Fasciolidae): transmission and scanning electron microscopy, and tubulin immunocytochemistry. Acta Parasitol 48:182–194
Ndiaye PI, Miquel J, Marchand B (2003b) Ultrastructure of spermiogenesis and spermatozoa of Taenia parva Baer, 1926 (Cestoda, Cyclophyllidea, Taeniidae), a parasite of the common genet (Genetta genetta). Parasitol Res 89:34–43
Olson PD, Poddubnaya LG, Littlewood DTJ, Scholz T (2008) On the position of Archigetes and its bearing on the early evolution of the tapeworms. J Parasitol 94:898–904
Poddubnaya LG (2003) Ultrastructure of reproductive organs and ducts in the progenetic species Archigetes sieboldi (Cestoda: Caryophyllidea). Zool Zh 82:1038–1050 (In Russian)
Poddubnaya LG, Mackiewicz JS, Kuperman BI (2003) Ultrastructure of Archigetes sieboldi (Cestoda: Caryophyllidea): relationship between progenesis, development and evolution. Folia Parasitol 50:275–293
Šípková L, Levron C, Freeman M, Scholz T (2010) Spermiogenesis and spermatozoon of the tapeworm Parabothriocephalus gracilis (Bothriocephalidea): ultrastructural and cytochemical studies. Acta Parasitol 55:58–65
Šípková L, Levron C, Oros M, Justine J-L (2011) Spermatological characters of bothriocephalideans (Cestoda) inferred from an ultrastructural study on Oncodiscus sauridae and Senga sp. Parasitol Res 109:9–18
Świderski Z (1985) Spermiogenesis in the proteocephalid cestode Proteocephalus longicollis. In: Timme AH (ed) Proceedings of the Electron Microscopical Society of South Africa, 24th annual conference. University of Natal, Pietermaritzburg, pp 181–182
Świderski Z (1986) Three types of spermiogenesis in cestodes. In: Imura T, Maruse S, Suzuki T (eds) Proc 11th Int Congr Electr Microsc, Kyoto, pp 2959-2960
Świderski Z, Mackiewicz JS (2002) Ultrastructure of spermatogenesis and spermatozoa of the caryophyllidean cestode Glaridacris catostomi Cooper, 1920. Acta Parasitol 47:83–104
Thiéry J-P (1967) Mise en évidence des polysaccharides sur coupes fines en microscopie électronique. J Microsc 6:987–1018
Waeschenbach A, Webster BL, Littlewood DTJ (2012) Adding resolution to ordinal level relationships of tapeworms (Platyhelminthes: Cestoda) with large fragments of mtDNA. Mol Phylogen Evol 63:834–847
Yoneva A, Levron C, Oros M, Orosová M, Scholz T (2011) Ultrastructure of spermiogenesis and mature spermatozoon of Breviscolex orientalis (Cestoda: Caryophyllidea). Parasitol Res 108:997–1005
Yoneva A, Levron C, Oros M, Orosová M, Scholz T (2012a) Spermiogenesis and spermatozoon ultrastructure of Hunterella nodulosa (Cestoda: Caryophyllidea), a monozoic parasite of suckers (Catostomidae) in North America. Folia Parasitol 59:179–186
Yoneva A, Levron C, Ash A, Scholz T (2012b) Spermatological characters of monozoic tapeworms (Cestoda: Caryophyllidea), including first data on a species from the Indomalayan catfish. J Parasitol 98:423–430
Yoneva A, Kuchta R, Scholz T (2013) Spermiogenesis and sperm ultrastructure of two species of Duthiersia, parasites of monitors, with a review of spermatological characters in the Diphyllobothriidea (Cestoda). Zool Anz 252:486–494
Acknowledgements
We would like to thank our colleague Mikuláš Oros (Slovakia) for providing invaluable help with collecting parasites. This study was supported by the Grant Agency of the Slovak Republic VEGA (project no. 2/0104/16 to MB). We acknowledge the core facility of the Institute of Parasitology, BC ASCR in České Budějovice, Czech Republic, supported by the MEYS CR (LM2015062 Czech-BioImaging). This research was undertaken within the framework of a joint research project nos. AV ČR-16-08 and SAV-18-21 supported by a bilateral agreement on scientific exchange and cooperation signed by the Czech and Slovak Academies of Sciences.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Section Editor: David Bruce Conn
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Bruňanská, M., Matoušková, M., Nebesářová, J. et al. First ultrastructural and cytochemical data on the spermatozoon and its differentiation in progenetic and adult Archigetes sieboldi Leuckart, 1878 (Cestoda, Caryophyllidea, Caryophyllaeidae). Parasitol Res 118, 1205–1214 (2019). https://doi.org/10.1007/s00436-019-06276-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-019-06276-z