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Ultrastructure of male Centrorhynchus globocaudatus (Acanthocephala) cement apparatus and function of cement gland secretion

Published online by Cambridge University Press:  09 June 2020

B. Sayyaf Dezfuli*
Affiliation:
Department of Life Sciences & Biotechnology, University of Ferrara, St Borsari 46, 44121Ferrara, Italy
S. Rubini
Affiliation:
Experimental Zooprophylactic Institute of Ferrara, St Modena 483, 44124Cassana Ferrara, Italy
J.A. DePasquale
Affiliation:
Morphogenyx Inc, PO Box 717, East Northport, NY11731, USA
F. Pironi
Affiliation:
Department of Life Sciences & Biotechnology, University of Ferrara, St Borsari 46, 44121Ferrara, Italy
*
Author for correspondence: B.S. Dezfuli, E-mail: [email protected]

Abstract

Cement glands are one of the most conspicuous and distinctive elements of taxonomic interest in male Acanthocephala. Cement glands vary in shape, number and arrangement in different classes of the taxon. The glands and their products have a fundamental role in the reproductive process. Light and electron microscopy were used to investigate the ultrastructure of the cement apparatus, which includes both cement glands and the cement reservoir, in mature males of Centrorhynchus globocaudatus (Zeder, 1800). Centrorhynchus globocaudatus is an enteric parasite of birds of prey, including Falco tinnunculus (Linnaeus, 1758) and Buteo buteo (Linnaeus, 1758) from the province of Ferrara (northern Italy). The four elongated cement glands of C. globocaudatus are situated posterior to the testes. Sections through the cement glands show each gland is surrounded by a fibrous envelope with an approximate thickness of 0.6 μm. Beneath this envelope is an outer cytoplasmic layer thickness ranging from 22 to 26 μm, which contains a number of nuclei with diameters variable from 20 to 22 μm. The cytoplasmic layer is filled with prominent free ribosomes and many mitochondria with lamellar cristae. Secretory granules, measuring from 1 to 1.3 μm in diameter, are formed within the cytoplasmic layer. The cytoplasmic layer surrounds the luminal area for storage of the cement material in each gland. Cement gland ducts arise from the gland and extend towards a common cement reservoir in close contact with the seminal vesicle and Saefftigen's pouch. Microtubules, large secretory granules and rest of undefined organelles were also observed within the cement reservoir.

Type
Research Paper
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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References

Abele, LG and Gilchrist, S (1977) Homosexual rape and sexual selection in acanthocephalan worms. Science 197, 8183.CrossRefGoogle ScholarPubMed
Amin, OM and Dezfuli, BS (1995) Taxonomic notes on Polyacanthocephalus kenyensis (Acanthocephala: Polyacanthorhynchidae) from Lake Naivasha, Kenya. Journal of Parasitology 81, 7679.CrossRefGoogle Scholar
Asaolu, SO (1981) Morphology of the reproductive system of male Moniliformis dubius (Acanthocephala). Parasitology 82, 297309.CrossRefGoogle Scholar
Balabanian, L, Chaudhary, AR and Hendricks, AG (2018) Traffic control inside the cell: microtubule-based regulation of cargo transport. The Biochemist 40, 1417.CrossRefGoogle Scholar
Barlan, K and Gelfand, VI (2017) Microtubule-based transport and the distribution, tethering, and organization of organelles. Cold Spring Harbor Perspectives in Biology 9, a025817.CrossRefGoogle ScholarPubMed
Brooks, DR and McLennan, DA (1993) Historical ecology: examining phylogenetic components of community evolution. pp. 267280in Ricklefs, RE and Schluter, D (Eds) In species diversity in ecological communities. Chicago, University of Chicago Press.Google Scholar
Buchsbaum, DR, Buchsbaum, M, Pearse, J and Pearse, V (2013) Animals without backbones: an introduction to the invertebrates, 3rd edn. 582 pp. London, University of Chicago Press.Google Scholar
Crompton, DWT (1985) Reproduction. pp. 213271in Crompton, DWT and Nickol, BB (Eds) Biology of the acanthocephala. Cambridge, Cambridge University Press.Google Scholar
Dezfuli, BS (2000) Study of cement apparatus, cement production and transportation in adult male Neoechinorhynchus rutili (Acanthocephala: Eoacanthocephala). Parasitology Research 86, 791796.CrossRefGoogle Scholar
Dezfuli, BS and De Biaggi, S (2000) Copulation of Acanthocephalus anguillae (Acanthocephala). Parasitology Research 86, 524526.CrossRefGoogle Scholar
Dezfuli, BS, Onestini, S, Carcupino, M and Mischiati, C (1998) The cement apparatus of larval and adult Pomphorhynchus laevis (Acanthocephala: Palaeacanthocephala). Parasitology 116, 437447.CrossRefGoogle Scholar
Dezfuli, BS, Capuano, S, Pironi, F and Mischiati, C (1999a) The origin and function of cement gland secretions in Pomphorhynchus laevis (Acanthocephala). Parasitology 119, 649653.CrossRefGoogle Scholar
Dezfuli, BS, Capuano, S, Giari, L, Pironi, F and Mischiati, C (1999b) Purification and characterization of a cement gland protein in acathocephalans. Helminthologia 39, 28.Google Scholar
Dezfuli, BS, Simoni, E and Mischiati, C (2001) The cement apparatus if larval and adult Acanthocephalus anguillae (Acanthocephala), with notes in the copulatory cap and origin of gland secretion. Parasitology Research 87, 299305.CrossRefGoogle Scholar
García-Varela, M and Nadler, SA (2006) Phylogenetic relationships among Syndermata inferred from nuclear and mitochondrial gene sequences. Molecular Phylogenetics and Evolution 40, 6172.CrossRefGoogle ScholarPubMed
Garey, JR, Schmidt-Rhaesa, A, Near, TJ and Nadler, SA (1998) The evolutionary relationships of rotifers and acanthocephalans. Hydrobiologia 387/378, 8391.CrossRefGoogle Scholar
Gazi, M, Sultana, T, Min, GS, Park, YC, García-Varela, M, Nadler, SA and Park, JK (2012) The complete mitochondrial genome sequence of Oncicola luehei (Acanthocephala: Archiacanthocephala) and its phylogenetic position within Syndermata. Parasitology International 61, 307316.CrossRefGoogle ScholarPubMed
Gillott, C (2003) Male accessory gland secretions: modulators of female reproductive physiology and behavior. Annual Review of Entomology 48, 163184.CrossRefGoogle ScholarPubMed
Lisitsyna, OI and Greben, OB (2015) Acanthocephalans of the genus Centrorhynchus (Palaeacanthocephala: Centrorhynchidae) of birds of Ukraine with the description of a new species. Vetnik Zoologii 49, 195210.CrossRefGoogle Scholar
Miller, DM and Dunagan, TT (1985) Functional morphology. pp. 73123in Crompton, DWT and Nickol, BB (Eds) Biology of the Acanthocephala. Cambridge, Cambridge University Press.Google Scholar
Near, TJ, Garey, JR and Nadler, SA (1998) Phylogenetic relationships of the Acanthocephala inferred from 18S ribosomal DNA sequences. Molecular Phylogenetics and Evolution 10, 287298.CrossRefGoogle ScholarPubMed
Parker, GA (1970) Sperm competition and its evolutionary consequences in the insects. Biological Reviews 45, 525567.CrossRefGoogle Scholar
Parshad, VR and Crompton, DWT (1981) Aspects of acanthocephalan reproduction. Advance in Parasitology 19, 73138.CrossRefGoogle ScholarPubMed
Pathak, D, Thakur, S and Mallik, R (2018) Fluorescence microscopy applied to intracellular transport by microtubules motors. Journal of Bioscience 43, 437445.CrossRefGoogle ScholarPubMed
Patt, DI and Patt, GR (1969) Epithelial tissues. pp. 7283in Patt, DI and Patt, GR (Eds) Comparative vertebrate histology. New York, Harper and Row Publisher.Google Scholar
Richardson, DJ, Martens, JK and Nickol, BB (1997) Copulation and sexual congress of Leptorhynchoides thecatus (Acanthocephala). Journal of Parasitology 83, 542543.CrossRefGoogle Scholar
Sielaff, M, Schmidt, H, Struck, TH, Rosenkranz, D, Mark Welch, DB, Hankeln, T and Herlyn, H (2016) Phylogeny of Syndermata (syn. Rotifera): mitochondrial gene order verifies epizoic Seisonidea as sister to endoparasitic Acanthocephala within monophyletic Hemirotifera. Molecular phylogenetics and evolution 96, 7992.CrossRefGoogle ScholarPubMed
Smales, LR (2015) Acanthocephala. pp. 317336in Schmidt-Rhaesa, A (Ed) Handbook of zoology. Cycloneuralia Gastrotricha and Gnathifera, Vol 3. Berlin, De Gruyter.Google Scholar
Van Cleave, HJ (1949) Morphological and phylogenetic interpretations of the cement glands in the Acanthocephala. Journal of Morphology 84, 427457.CrossRefGoogle ScholarPubMed