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Ultrastructure of the uterus, embryonic envelopes and the coracidium of the enigmatic tapeworm Tetracampos ciliotheca (Cestoda: Bothriocephalidea) from African sharptooth catfish (Clarias gariepinus)

Abstract

Transmission electron microscopy (TEM) was used to study the ultrastructure of the uterus and egg morphology in the enigmatic bothriocephalidean tapeworm Tetracampos ciliotheca. The uterine wall, underlain by well-developed muscle bundles, consists of a syncytial epithelium which is characterized by the abundance of free ribosomes, mitochondria and cisternae of granular endoplasmic reticulum (GER). On the apical surface of the uterine epithelium, there is an abundant network of cytoplasmic microlamellae projecting into the uterine lumen. The lumen is filled with freely lying eggs which are located close to the uterine wall but do not contact with the microlamellae of the uterine epithelium. The developed eggs possess an oncosphere surrounded by four envelopes: (1) a thin egg shell; (2) an outer envelope; (3) a syncytial, ciliated inner envelope; and (4) the oncospheral membrane. The mature hexacanth is armed with three pairs of oncospheral hooks, as well as somatic and hook muscles and five types of cells (1) binucleated subtegumental cell, (2) somatic cells, (3) penetration gland cells, (4) nerve cells and (5) germinative cells. Considering the relative scarcity of descriptive and comparative studies on the ultrastructure of the uterus and egg morphology in the order Bothriocephalidea, we concluded that Tet. ciliotheca displays a unique type of egg development. Based on these results, we discuss plausible ideas relating to the function of these structures for consideration in future studies.

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Acknowledgements

We acknowledge the Laboratory of EM, Biology Centre of ASCR, institution supported by the MEYS CR (LM2015062 Czech-BioImaging) for allowing the use of their facilities and Hannes Erasmus, Wynand Malherbe, Ruan Gerber and Marelize Labuschagne (NWU_Water Research group) for their assistants during fieldwork in South Africa.

Funding

This study was supported by the Czech Science Foundation program EXPRO (project no. 19-28399). Research funding for RK’s visit to South Africa (SA) and field work in SA was received from the National Research Foundation (NRF) of SA (NRF project GERM160623173784, grant 105875, NJ Smit, PI).

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Correspondence to Aneta Yoneva.

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Any opinion, finding and conclusion or recommendation expressed in this publication is that of the authors and the NRF does not accept any liability in this regard.

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The necessary permit (HO 09/03/2017-125 NW, North West Province, Department of Rural, Environmental and Agricultural Development) and ethical clearance (North-West University AnimCare Ethics committee approval number NWU-00282-17-A5) for collecting, euthanizing and dissecting fish were obtained prior to sampling.

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Yoneva, A., Kuchta, R. & Smit, N. Ultrastructure of the uterus, embryonic envelopes and the coracidium of the enigmatic tapeworm Tetracampos ciliotheca (Cestoda: Bothriocephalidea) from African sharptooth catfish (Clarias gariepinus). Parasitol Res (2020). https://doi.org/10.1007/s00436-019-06496-3

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Keywords

  • Bothriocephalidea
  • TEM
  • Egg
  • Evolution
  • Oncosphere