Advertisement

Sperm characters of the aspidogastrean Rohdella amazonica (Aspidogastridae, Rohdellinae), a parasite of the banded puffer fish Colomesus psittacus

  • Elane G. Giese
  • Raul Henrique S. Pinheiro
  • Zdzisław Świderski
  • Jordi MiquelEmail author
Helminthology - Original Paper
  • 30 Downloads

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.

Keywords

Rohdella amazonica Aspidogastrea Aspidogastridae Rohdellinae Sperm characters Ultrastructure 

Notes

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 information

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.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 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 CrossRefPubMedGoogle Scholar
  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 CrossRefPubMedGoogle Scholar
  3. 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 CrossRefPubMedGoogle Scholar
  4. Bakker KE, Diegenbach PC (1973) The ultrastructure of the spermatozoa of Aspidogaster conchicola Baer, 1826 (Aspidogastridae, Trematoda). Neth J Zool 23:345–346CrossRefGoogle Scholar
  5. 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 CrossRefPubMedGoogle Scholar
  6. Ehlers U (1984) Phylogenetisches system der Plathelminthes. Verh Naturwiss Ver Hambg (NF) 27:291–294Google Scholar
  7. 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 CrossRefGoogle Scholar
  8. 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 CrossRefGoogle Scholar
  9. 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 300–319CrossRefGoogle Scholar
  10. 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 CrossRefGoogle Scholar
  11. 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 CrossRefGoogle Scholar
  12. 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 166:55–86Google Scholar
  13. Justine J-L (1998) Spermatozoa as phylogenetic characters for the Eucestoda. J Parasitol 84:385–408.  https://doi.org/10.2307/3284502 CrossRefPubMedGoogle Scholar
  14. Justine J-L (2001) Spermatozoa as phylogenetic characters for the Platyhelminthes. In: Littlewood DTJ, Bray RA (eds) Interrelationships of Platyhelminthes. Taylor & Francis, London, pp 231–238Google Scholar
  15. Justine J-L, Mattei X (1983) A spermatozoon with two 9 + 0 axonemes in a parasitic flatworm, Didymozoon (Digenea: Didymozoidae). J Submicrosc Cytol 15:1101–1105Google Scholar
  16. 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 CrossRefGoogle Scholar
  17. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 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 CrossRefPubMedGoogle Scholar
  19. 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 CrossRefPubMedGoogle Scholar
  20. 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 CrossRefGoogle Scholar
  21. Litvaitis MK, Rohde K (1999) A molecular test of platyhelminth phylogeny: inferences from partial 28S rDNA sequences. Invertebr Biol 118:42–56CrossRefGoogle Scholar
  22. 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 CrossRefPubMedGoogle Scholar
  23. 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 48:182–194Google Scholar
  24. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 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 CrossRefPubMedGoogle Scholar
  26. 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 CrossRefPubMedGoogle Scholar
  27. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Rohde K (1994) The minor groups of parasitic Platyhelminthes. Adv Parasitol 33:145–234.  https://doi.org/10.1016/S0065-308X(08)60413-3 CrossRefPubMedGoogle Scholar
  29. 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 159–167Google Scholar
  30. 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 5–14CrossRefGoogle Scholar
  31. Rohde K, Watson NA (1994) Spermiogenesis in Gonoplasius sp. (Platyhelminthes, Monogenea, Polyopsithocotylea, Microcotylidae). Acta Parasitol 39:111–116Google Scholar
  32. 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 CrossRefPubMedGoogle Scholar
  33. 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:141–144Google Scholar
  34. 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 CrossRefPubMedGoogle Scholar
  35. Thiéry JP (1967) Mise en évidence des polysaccharides sur coupes fines en microscopie électronique. J Microsc (Paris) 6:987–1018Google Scholar
  36. 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 CrossRefGoogle Scholar
  37. 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 CrossRefPubMedGoogle Scholar
  38. 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 CrossRefPubMedGoogle Scholar
  39. Watson NA, Whittington ID, Rohde K (1995) Ultrastructure of spermiogenesis and spermatozoa in the monogeneans Concinnocotyla australensis (Polystomatidae) and Pricea multae (Gastrocotylidea). Parasite 2:357–366Google Scholar
  40. 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 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Laboratório de Histologia e Embriologia Animal, Instituto da Saúde e Produção AnimalUniversidade Federal Rural da AmazôniaBelémBrazil
  2. 2.Secció de Parasitologia, Departament de Biologia, Sanitat i Medi Ambient, Facultat de Farmàcia i Ciències de l’AlimentacióBarcelonaSpain
  3. 3.Instituto de Ciências e Tecnologia das ÁguasUniversidade Federal do Oeste do ParáSantarémBrazil
  4. 4.Witold Stefański Institute of ParasitologyPolish Academy of SciencesWarszawaPoland
  5. 5.Institut de Recerca de la Biodiversitat (IRBio)Universitat de BarcelonaBarcelonaSpain

Personalised recommendations