Abstract
The ultrastructural characteristics of the mature spermatozoon of the aspidogastrean Rohdella amazonica (Aspidogastridae, Rohdellinae) were studied by means of transmission electron microscopy. The sperm cell shows two axonemes of the 9 + ‘1’ trepaxonematan pattern of Platyhelminthes, parallel cortical microtubules, a well-developed lateral expansion, external ornamentation of the plasma membrane, one mitochondrion, an electron-dense ring, a nucleus and granules of glycogen. The present results were compared with those observed in the aspidogastreans studied to date and in other Platyhelminthes. The lateral expansion and the electron-dense ring are typical characters for aspidogastreans. Although a lateral expansion has been described in other Platyhelminthes such as monogeneans and digeneans, the Aspidogastrea shows a much larger lateral expansion with both peripheral and internal microtubules. The dense ring is observed as a cylinder in a longitudinal view and shows a more granular appearance in sperm cells from the seminal vesicle in comparison to a more electron-dense appearance in sperm cells from the seminal uterine receptacle.
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References
Alves P, Vieira F, Santos C, Scholz T, Luque J (2015) A checklist of the Aspidogastrea (Platyhelminthes: Trematoda) of the World. Zootaxa 3918:339–396. https://doi.org/10.11646/zootaxa.3918.3.2
Bakhoum AJS, Torres J, Shimalov VV, Bâ CT, Miquel J (2011) Spermiogenesis and spermatozoon ultrastructure of Diplodiscus subclavatus (Pallas, 1760) (Paramphistomoidea, Diplodiscidae), an intestinal fluke of the pool frog Rana lessonae (Amphibia, Anura). Parasitol Int 60:64–74. https://doi.org/10.1016/jparint.2010.10.006
Bakhoum AJS, Miquel J, Ndiaye PI, Justine J-L, Falchi A, Bâ CT, Marchand B, Quilichini Y (2017) Advances in spermatological characters in the Digenea: review and proposal of spermatozoa models and their phylogenetic importance. Adv Parasitol 98:111–165. https://doi.org/10.1016/bs.apar.2017.04.001
Bakker KE, Diegenbach PC (1973) The ultrastructure of the spermatozoa of Aspidogaster conchicola Baer, 1826 (Aspidogastridae, Trematoda). Neth J Zool 23:345–346
Cable J, Tinsley RC (2001) Ultrastructure of spermiogenesis and spermatozoa of Discocotyle sagittata (Monogenea: Polyopisthocotylea: Discocotylinea). Folia Parasitol 48:209–216. https://doi.org/10.14411/fp.2001.034
Ehlers U (1984) Phylogenetisches system der Plathelminthes. Verh Naturwiss Ver Hambg (NF) 27:291–294
Giese EG, Silva MVO, Videira Mn, Furtado AP, Matos ER, Gonçalves EC, Melo FTV, Santos JN (2015) Rohdella amazonica n. sp. (Aspidogastrea:Aspidogastridae) from the Amazoninan banded puffer fish Colomesus psittacus (Bloch & Schneider, 1801). J Helminthol 89:288–293. https://doi.org/10.1017/S0022149X14000054
Ishida S, Yamashita Y, Teshirogi W (1991) Analytical studies of the ultrastructure and movement of the spermatozoa of freshwater triclads. Hydrobiologia 227:95–104. https://doi.org/10.1007/BF00027588
Jamieson BGM, Justine J-L (2017) Spermatozoa, spermatogenesis and fertilization in Schistosoma. In: Jamieson BGM (ed) Schistosoma: Biology. Pathology and Control. CRC Press, Boca Raton, pp 300–319
Justine J-L (1991a) Phylogeny of parasitic Platyhelminthes: a critical study of synapomorphies proposed on the basis of the ultrastructure of spermiogenesis and spermatozoa. Can J Zool 69:1421–1440. https://doi.org/10.1139/z91-203
Justine J-L (1991b) Cladistic study in the Monogenea (Platyhelminthes), based upon a parsimony analysis of spermiogenetic and spermatozoal ultrastructural characters. Int J Parasitol 21:821–838. https://doi.org/10.1016/0020-7519(91)90151-V
Justine J-L (1995) Spermatozoal ultrastructure and phylogeny in the parasitic Platyhelminthes. In: Jamieson BGM, Ausio J, Justine JL (eds) Advances in spermatozoa phylogeny and taxonomy. Mém Mus Natn Hist Nat 166:55–86
Justine J-L (1998) Spermatozoa as phylogenetic characters for the Eucestoda. J Parasitol 84:385–408. https://doi.org/10.2307/3284502
Justine J-L (2001) Spermatozoa as phylogenetic characters for the Platyhelminthes. In: Littlewood DTJ, Bray RA (eds) Interrelationships of Platyhelminthes. Taylor & Francis, London, pp 231–238
Justine J-L, Mattei X (1983) A spermatozoon with two 9 + 0 axonemes in a parasitic flatworm, Didymozoon (Digenea: Didymozoidae). J Submicrosc Cytol 15:1101–1105
Justine J-L, Mattei X (1985) A spermatozoon with undulating membrane in a parasitic flatworm, Gotocotyla (Monogenea, Polyopisthocotylea, Gotocotylidae). J Ultrastruct Res 90:163–171. https://doi.org/10.1016/0889-1605(85)90106-5
Justine J-L, Poddubnaya LG (2018) Spermiogenesis and spermatozoon ultrastructure in basal polyopisthocotylean monogeneans, Hexabothriidae and Chimaericolidae, and their significance for the phylogeny of the Monogenea. Parasite 25:7. https://doi.org/10.1051/parasite/2018007
Levron C, Suchanová E, Poddubnaya L, Oros M, Scholz T (2009) Spermatological characters of the aspidogastrean Aspidogaster limacoides Diesing, 1835. Parasitol Res 105:77–85. https://doi.org/10.1007/s00436-009-1367-3
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. https://doi.org/10.1111/j.1469-185X.2009.00114.x
Littlewood DTJ, Rohde K, Clough KA (1999) The interrelationships of all major groups of Platyhelminthes: phylogenetic evidence from morphology and molecules. Biol J Linn Soc 66:75–114. https://doi.org/10.1111/j.1095-8312.1999.tb01918.x
Litvaitis MK, Rohde K (1999) A molecular test of platyhelminth phylogeny: inferences from partial 28S rDNA sequences. Invertebr Biol 118:42–56
Miquel J, Martellet MR, Acosta L, Toledo R, Pétavy A-F (2018) Reinvestigation of the sperm ultrastructure of Hypoderaeum conoideum (Digenea: Echinostomatidae). Parasitol Res 117:3725–3732. https://doi.org/10.1007/s00436-018-6071-8
Ndiaye PI, Miquel J, Fons R, Marchand B (2003) Spermiogenesis and sperm ultrastructure of the liver fluke Fasciola hepatica L., 1758 (Digenea, Fasciolidae): scanning and transmission electron microscopy, and tubulin immunocytochemistry. Acta Parasitol 48:182–194
Ndiaye PI, Marchand B, Bâ CT, Justine J-L, Bray RA, Quilichini Y (2018) Ultrastructure of mature spermatozoa of three Bucephalidae (Prosorhynchus longisaccatus, Rhipidocotyle khalili and Bucephalus margaritae) and phylogenetic implications. Parasite 25:65. https://doi.org/10.1051/parasite/2018065
Quilichini Y, Foata J, Justine J-L, Bray RA, Marchand B (2010) Ultrastructural study of the spermatozoon of Heterolebes maculosus (Digenea, Opistholebetidae), a parasite of the porcupinefish Diodon hystrix (Pisces, Teleostei). Parasitol Int 59:427–434. https://doi.org/10.1016/j.parint.2010.06.002
Quilichini Y, Foata J, Justine J-L, Bray RA, Marchand B (2011) Spermatozoon ultrastructure of Gyliauchen sp. (Digenea: Gyliauchenidae), an intestinal parasite of Siganus fuscescens (Pisces: Teleostei). Biol Bull 221:197–205. https://doi.org/10.1086/BBLv221n2p197
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. https://doi.org/10.1083/jcb.17.1.208
Rohde K (1994) The minor groups of parasitic Platyhelminthes. Adv Parasitol 33:145–234. https://doi.org/10.1016/S0065-308X(08)60413-3
Rohde K (2001) The Aspidogastrea: an archaic group of Platyhelminthes. In: Littlewood DTJ, Bray RA (eds) Interrelationships of the Platyhelminthes. Taylor and Francis, London, pp 159–167
Rohde K (2002) Subclass Aspidogastrea Faust & Tang, 1936. In: Gibson DI, Jones A, Bray RA (eds) Keys to the Trematoda, vol 1. CAB International and The Natural History Museum, London, pp 5–14
Rohde K, Watson NA (1994) Spermiogenesis in Gonoplasius sp. (Platyhelminthes, Monogenea, Polyopsithocotylea, Microcotylidae). Acta Parasitol 39:111–116
Rohde K, Watson NA, Cribb T (1991) Ultrastructure of sperm and spermatogenesis of Lobatostoma manteri (Trematoda, Aspidogastrea). Int J Parasitol 21:409–419. https://doi.org/10.1016/0020-7519(91)90098-R
Schludermann C, Laimgruber S, Konecny R, Schabuss M (2005) Aspidogaster limacoides Diesing, 1835 (Trematoda, Aspidogastridae): a new parasite of Barbus barbus (L.) (Pisces, Cyprinidae) in Austria. Ann Naturhist Mus Wien 106B:141–144
Seck MT, Marchand B, Bâ CT (2008) Spermiogenesis and sperm ultrastructure of Cotylophoron cotylophorum (Trematoda, Digenea, Paramphistomidae), a parasite of Bos taurus in Senegal. Parasitol Res 103:157–166. https://doi.org/10.1007/s00436-008-0944-1
Thiéry JP (1967) Mise en évidence des polysaccharides sur coupes fines en microscopie électronique. J Microsc (Paris) 6:987–1018
Watson NA, Rohde K (1991) Ultrastructure of spermatogenesis and sperm of Multicotyle purvisi (Plathelminthes, Aspidogastrea). Zoomorphology 110:347–356. https://doi.org/10.1007/BF01668025
Watson NA, Rohde K (1992) Ultrastructure of sperm and spermatogenesis of Rugogaster hydrolagi, Schell 1973 (Platyhelminthes, Trematoda, Aspidogastrea, Rugogastridae). Parasitol Res 78:516–524. https://doi.org/10.1007/BF00931574
Watson NA, Rohde K (1995) Re-examination of Spermatogenesis of Multicotyle purvisi (Platyhelminthes, Aspidogastrea). Int J Parasitol 25:579–586. https://doi.org/10.1016/0020-7519(94)00170-S
Watson NA, Whittington ID, Rohde K (1995) Ultrastructure of spermiogenesis and spermatozoa in the monogeneans Concinnocotyla australensis (Polystomatidae) and Pricea multae (Gastrocotylidea). Parasite 2:357–366
Zamparo DZ, Brooks DR (2003) Phylogenetic systematic assessment of the Aspidobothrea (Platyhelminthes, Neodermata, Trematoda). Zool Scr 32:83–93. https://doi.org/10.1046/j.1463-6409.2003.00088.x
Acknowledgments
The authors wish to thank the personnel of the ‘Unitat de Microscòpia Electrònica, Facultat de Medicina, Centres Científics i Tecnològics de la Universitat de Barcelona (CCiTUB)’ for their support in the preparation of samples. JM is a member of the 2017-SGR-1008 research group.
Funding
This work was partly supported by CAPES post-doctoral fellowship to EGG (21/2018 PROCAD AMAZÔNIA-DRI-88881.314463/2019-01) and by ISPA-UFRA.
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Giese, E.G., Pinheiro, R.H.S., Świderski, Z. et al. Sperm characters of the aspidogastrean Rohdella amazonica (Aspidogastridae, Rohdellinae), a parasite of the banded puffer fish Colomesus psittacus. Parasitol Res 119, 137–144 (2020). https://doi.org/10.1007/s00436-019-06479-4
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DOI: https://doi.org/10.1007/s00436-019-06479-4