Abstract
This investigation of Calicotyle affinis is the first ultrastructural description of the male reproductive system of a monocotylid monogenean. It has revealed numerous characteristics which are either new or clarify those determined from previous light microscopical observations on the morphology of Calicotyle spp. These include numerous individual testes, each surrounded by its own basal lamina; an ejaculatory bulb delimited by a basal lamina surrounded by two independent internal and external bands of muscles; a bipartite, but not fully divided, muscular chamber (an internal seminal vesicle) in the proximal region of the ejaculatory bulb; well-developed unicellular prostatic glands localised outside the ejaculatory bulb, the cytoplasmic extensions of which pass into the ejaculatory bulb, to form the ducts which open into the lumen of ejaculatory duct; and a male copulatory organ in the form of a coiled penis tube containing throughout its lumen a long, hollow stylet. The penis tube appears to be a modified prolongation of the ejaculatory duct and is supported by a basal lamina and muscle layers. The stylet wall consists of a homogenous, dense material with a narrow, denser inner lining; it is funnel-shaped proximally but narrows imperceptibly towards the distal end of the penis tube, and appears to be a derivative of the basal laminae of the ejaculatory bulb and distal ejaculatory duct. A comparative analysis of the nature of the stylet in relation to those found in free-living platyhelminths forms part of a search for characters useful for understanding monocotylid origins and relationships.
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Arafa SZ, El-Naggar MM, Kearn GC (2014) On some ultrastructural features of the monogenean parasite Macrogyroductylus congolensis from Clarias gariepinus inhabiting the River Nile in Egypt. Acta Parasitol 59:238–246. https://doi.org/10.2478/s11686-014-0236-0
Brinkmann A Jr (1940) Contribution to our knowledge of the monogenetic trematodes. Årbok Bergen Mus Naturvit Rekke 1:1–117
Brinkmann A Jr (1952) Fish trematodes from Norwegian water. The history of fish trematode investigations in Norway and the Norwegian species of the order Monogenea. Årbok Universitet Bergen Naturvit Rekke 1:1–74
Brüggemann J (1984) Ultrastruktur und Differenzierung der prostatoiden Organe von Polystyliphora filum (Plathelminthes, Proseriata). Zoomorpholgy 104:86–95. https://doi.org/10.1007/bf00312022
Brüggemann J (1986) Ultrastructural investigations on the differentiation of genital hard structures in free-living platyhelminths and their phylogenetic significance. Hydrobiologia 132:151–156. https://doi.org/10.1007/bf00046242
Bullard S, Overstreet RM (2000) Calicotyle californiensis n. sp. and Calicotyle urobati n. sp. (Monogenea: Calicotylinae) from elasmobranchs in the Gulf of California. J Parasitol 86:939–944. https://doi.org/10.2307/3284801
Chisholm LA, Wheeler TA, Beverley-Burton M (1995) A phylogenetic analysis and revised classification of the Monocotylidae Taschenberg, 1879 (Monogenea). Syst Parasitol 32:159–191. https://doi.org/10.1007/bf00008827
Chisholm LA, Hansknecht TJ, Whittington ID, Overstreet RM (1997) A revision of the Calicotylinae Monticelli, 1903 (Monogenea: Monocotylidae). Syst Parasitol 38:159–183. https://doi.org/10.1023/a:1005844306178
Chisholm LA, Morgan JAT, Adlard RD, Whittington ID (2001) Phylogenetic analysis of the Monocotylidae (Monogenea) inferred from 28S rDNA sequences. Int J Parasitol 31:1537–1547. https://doi.org/10.1016/s0020-7519(01)00313-7
Cielecka D, Gryther-Ziecina B, Chromicz L (1994) Studies on the surface ultrastructure of Sobolevicanthus gracilis (Zeder, 1803) (Cestoda, Hymenolepididae). Acta Parasitol 39:131–137
Davydov VG, Korneva ZV (2002) Structure of the copulative apparatus of Sobolevicanthus gracilis (Cestoda: Cyclophyllidea). Parazitologiya 36:224–230 (In Russian)
Doe DA (1982) Ultrastructure of copulatory organs in Turbellaria. I. Macrostomum sp. and Microstomum sp. (Macrostomida). Zoomorphology 101:39–59. https://doi.org/10.1007/BF00312029
Doe DA (1986a) Ultrastructure of the copulatory stylet and accessory spines in Haplopharynx quadristimulus (Turbellaria). Hydrobiologia 132:157–163. https://doi.org/10.1007/bf00046243
Doe DA (1986b) Ultrastructure of the copulatory organ of Haplopharynx quadristimulus and its phylogenetic significance. Zoomorphology 106:163–173. https://doi.org/10.1007/bf00312205
Ehlers B, Ehlers U (1980) Struktur und Differenzierung penialer hartgebilde von Carenscoilia bidentata Sopott (Turbellaria, Proseriata). Zoomorphologie 95:159–167. https://doi.org/10.1007/bf00997909
Euzet L, Williams HH (1960) A re-description of the trematode Calicotyle stossichii Braun, 1899, with an account of Calicotyle palombi sp. nov. Parasitology 50:21–30. https://doi.org/10.1017/s0031182000025166
Glennon V, Chisholm L, Whittington ID (2006) A redescription of Calicotyle australis Johnston, 1934 (Monogenea: Monocotylidae) from the type-host Trygonorrhina fasciata (Rhinobatidae) off Adelaide, South Australia, including descriptions of live and silver stained larvae. Syst Parasitol 63:29–40. https://doi.org/10.1007/s11230-005-5501-z
Halton DW, Hardcastle A (1977) Ultrastructure of the male accessory ducts and prostate gland of Diclidophora merlangi (Monogenoidea). Int J Parasitol 7:393–401. https://doi.org/10.1016/0020-7519(77)90065-0
Janssen T, Vizoso DB, Schulte G, Littlewood DT, Waeschenbach A, Schärer L (2015) The first multi-gene phylogeny of the Macrostomorpha sheds light on the evolution of sexual and asexual reproduction in basal Platyhelminthes. Mol Phylogen Evol 92:82–107. https://doi.org/10.1016/j.ympev.2015.06.004
Kearn G, Whittington I (2015) Sperm transfer in monogenean (platyhelminth) parasites. Acta Parasit 60:567–600. https://doi.org/10.1515/ap-2015-0082
Lanfranchi A (1978) Morphology and taxonomy of two new otoplanids (Turbellaria: Proseriata) from the Ligurian Sea. Zool Scr 7:249–254. https://doi.org/10.1111/j.1463-6409.1978.tb00606.x
Levron C, Poddubnaya LG, Kuchta R, Freeman M, Wang Y-H, Scholz T (2008) SEM and TEM study of the armed male terminal genitalia of the tapeworm Paraechinophallus japonicus (Cestoda: Bothriocephalidea). J Parasitol 94:803–810. https://doi.org/10.1007/BF00312007
Maillard C, Caley J, Noisy D (1982) A scanning electron microscope study of the male copulatory sclerite of the monogenean Diplectanum aequans. Parasitology 84:63–64. https://doi.org/10.1017/s0031182000051660
Martens EE (1986) Comparative ultrastructure of copulatory organs having a stylet in the Proseriata (Turbellaria). Hydrobiologia 132:165–173. https://doi.org/10.1007/BF00046244
Nybelin O (1941) Dictyocotyle coeliaca n. g. n. sp. Ein Leibeshöhlebewohnender monogenetischer Trematode. Meddn Göteborgs Mus Zool Avd [Göteborgs K Vetensk Vitter Samh Handl, Ser B, 1(3)] 87:1–20
Poddubnaya LG, Mackiewicz JS (2009) Ultrastructure of the cirrus sac of echinophallid tapeworms (Cestoda, Bothriocephalidea) and the terminology of cirrus hard structures. Int J Parasitol 39:381–390. https://doi.org/10.1016/j.ijpara.2008.07.008
Poddubnaya LG, Mackiewicz JS, Bruňanská M, Dezfuli S (2005) Fine structure of the male reproductive ducts, vagina and seminal receptacle of Cyathocephalus truncatus (Cestoda: Spathebothriidea). Folia Parasitol 52:241–250. https://doi.org/10.14411/fp.2005.032
Timofeeva TA (1985) Morphological and ecological aspects of evolution in the Monocotylidae (Monogenea). Parazitol Sb 33:44–76 (In Russian)
Vaughan DB, Chisholm LA, Hansen H (2016) Electrocotyle whittingtoni n. gen., n. sp. (Monogenea: Monocotylidae: Heterocotylinae) from the gills of a captive onefin electric ray, Narke capensis (Narkidae) at Two Oceans Aquarium, Cape Town, South Africa. Parasitol Res 115:3575–3584. https://doi.org/10.1007/s00436-016-5123-1
Whittington ID, Barton DP, Lester RJG (1989) A redescription of Calicotyle australis Johnston, 1934 (Monogenea: Monocotylidae) from a new host, Rhinobatos batillum (Batiformes: Rhinobatidae) from Moreton Bay, Queensland. Syst Parasitol 14:145–156. https://doi.org/10.1007/bf00016909
Whittington ID, Deveney MR, Wyborn JS (2001) A revision of Benedenia Diesing, 1858 including a redescription of B. sciaenae (van Beneden, 1856) Odhner, 1905 and recognition of Menziesia Gibson, 1976 (Monogenea: Capsalidae). J Nat Hist 35:663–777. https://doi.org/10.1080/00222930152023090
Acknowledgements
The authors would like to thank the staff of the RV ‘Johan Ruud’, belonging to Tromsø University (Norway), for their help with the fishing. We are also grateful to the staff of the Centre of Electron Microscopy, I.D. Papanin Institute for the Biology of Inland Waters (Borok, Russia), for technical assistance. The present study was carried out within the framework of the state assignment of the Federal Agency for Scientific Organizations, Russia (theme no. AAAA-A18-118012690100-5) and supported by the Russian Foundation for Basic Research (project no. 15–04-02890-a to LGP) and the Grant Agency of the Slovak Republic, VEGA (project no. 2/0104/16 to MB)
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Poddubnaya, L.G., Hemmingsen, W., Bruñanská, M. et al. Ultrastructural characteristics of the male ducts and terminal genitalia of an endoparasitic monogenean, Calicotyle affinis Scott, 1911 (Monopisthocotylea: Monocotylidae), with the first detailed description of a copulatory stylet in a monogenean. Parasitol Res 117, 1503–1512 (2018). https://doi.org/10.1007/s00436-018-5831-9
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DOI: https://doi.org/10.1007/s00436-018-5831-9