Hostname: page-component-76fb5796d-qxdb6 Total loading time: 0 Render date: 2024-04-28T20:53:03.802Z Has data issue: false hasContentIssue false
  • English
  • Français

New morphological and molecular perspectives about Macracanthorhynchus hirudinaceus (Acanthocephala: Oligacanthorhynchidae) from wild boar, Sus scrofa Linn., in Ukraine

Published online by Cambridge University Press:  13 December 2021

Omar M. Amin Open the ORCID record for Omar M. Amin [Opens in a new window] ,
Richard A. Heckmann ,
Sara Dallarés ,
María Constenla  and
Tetiana Kuzmina
Omar M. Amin*
Affiliation:
Institute of Parasitic Diseases, 11445 E. Via Linda 2-419, Scottsdale, Arizona85259, USA
Richard A. Heckmann
Affiliation:
Department of Biology, Brigham Young University, 1114 MLBM, Provo, Utah84602, USA
Sara Dallarés
Affiliation:
Department of Animal Biology, Vegetal Biology and Ecology, Universitat Autònoma de Barcelona, Cerdanyola, 08193Barcelona, Spain
María Constenla
Affiliation:
Department of Animal Biology, Vegetal Biology and Ecology, Universitat Autònoma de Barcelona, Cerdanyola, 08193Barcelona, Spain
Tetiana Kuzmina
Affiliation:
I. I. Schmalhausen Institute of Zoology. Vul. B. Khmelnytskogo, 15, Kyiv, 01030, Ukraine
*
Author for correspondence: E-mail: omaramin@aol.com
Get access Rights & Permissions [Opens in a new window]

Abstract

We make new morphological observations not previously reported for the old acanthocephalan Macracanthorhynchus hirudinaceus (Pallas, 1781) Travassos, 1917, described for the first time about 240 years ago. Our specimens were collected from the wild boar, Sus scrofa Linn., in Ukraine in 2005. We provide comparative morphometrics with other populations from Ukraine, Union of Soviet Socialist Republics, Europe, Brazil and the United States of America. Our specimens from the Ukraine had the smallest trunk (110–120 mm long), longest and thickest hooks, with the third hook being the largest, largest eggs, and a proboscis wider than long. We document the morphology of the proboscis, apical organ, hooks, hook roots, sensory pores, micropores, and eggs with scanning electron microscopy for the first time. We also provide chemical analysis of hooks and eggs using energy-dispersive X-ray analysis, discuss its micropores, and provide a new molecular profile based on 18S rDNA from a European population for the first time. Edge of hook tips feature high levels of calcium and phosphorous but the high level of sulphur is mostly found in the cortical layer of eggs. One new partial 18S rDNA sequence (482 nt length) was generated from an adult specimen of M. hirudinaceus. We present the first 18S rDNA published sequence for this cosmopolitan acanthocephalan obtained from Europe. The amplified region corresponded to the approximate middle region of the small subunit ribosomal ribonucleic acid gene, which is ~1800 nt in length. This molecular contribution is especially valuable in light of the extreme scarcity of genetic information about species of Macracanthorhynchus and of the family Oligacanthorhynchidae as a whole.

Keywords

Macaracanthorhynchus hirudinaceusSus scrofaUkrainedescriptionmolecular analysisEDXA
Type
Research Paper
Information
Journal of Helminthology , Volume 95 , 2021 , e73
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Amin, OM (2013) Classification of the Acanthocephala. Folia Parasitologica 60(4), 273–305.CrossRefGoogle ScholarPubMed
Amin, OM and Dailey, MD (1998) Description of Mediorhynchus papillosus (Acanthocephala: Gigantorhynchidae) from a Colorado, USA, population, with a discussion of morphology and geographical variability. Journal of the Helminthological Society of Washington 65(2), 189–200.Google Scholar
Amin, OM and Heckmann, RA (2017) Neoandracantha peruensis n. gen. n. sp. (Acanthocephala: Polymorphidae) described from cystacanths infecting the ghost crab Ocypode gaudichaudi on the Peruvian coast. Parasite 24, 1–15.Google Scholar
Amin, OM, Heckmann, RA, Radwan, NA, Mantuano, JS and Alcivar, MAZ (2009) Redescription of Rhadinorhynchus ornatus (Acanthocephala: Rhadinorhynchidae) from skipjack tuna, Katsuwonus pelamis, collected in the Pacific Ocean off South America, with special reference to new morphological features. Journal of Parasitology 95(3), 656–664.CrossRefGoogle ScholarPubMed
Amin, OM, Heckmann, RA, Halajian, A and El-Naggar, AM (2011) The morphology of an unique population of Corynosoma strumosum (Acanthocephala, Polymorphidae) from the Caspian Seal, Pusa caspica, in the land-locked Caspian Sea using SEM, with special notes on histopathology. Acta Parasitologica 56(4), 438–445.CrossRefGoogle Scholar
Amin, OM, Heckmann, RA and Zargar, UR (2017) Description of a new quadrigyrid acanthocephalan from Kashmir, with notes on metal analysis and histology, and a key to species of the subgenus Acanthosentis from the Indian subcontinent. Journal of Parasitology 103(5), 458–470.CrossRefGoogle Scholar
Amin, OM, Heckmann, RA and Ha, NV (2018) Descriptions of Acanthocephalus parallelcementglandatus (Echinorhynchidae) and Neoechinorhynchus (N.) pennahia (Neoechinorhynchidae) (Acanthocephala) from amphibians and fish in Central and Pacific coast of Vietnam, with notes on N. (N.) longnucleatus. Acta Parasitologica 63(3), 572–585.CrossRefGoogle Scholar
Amin, OM, Heckmann, RA, Dallarés, S, Constenla, M and Ha, NV (2019a) Morphological and molecular description of Rhadinorhynchus laterospinosus Amin, heckmann & Ha, 2011 (Acanthocephala, Rhadinorhynchidae) from marine fish off the Pacific coast of Vietnam. Parasite 26, 14.CrossRefGoogle Scholar
Amin, OM, Heckmann, RA, Sharifdini, M and Albayati, NY (2019b) Moniliformis cryptosaudi n. sp., (Acanthocephala: Moniliformidae) from the long-eared hedgehog Hemiechinus auratus (Gmelin) (Erinaceidae) in Iraq; a case of incipient cryptic speciation related to M. saudi in Saudi Arabia. Acta Parasitologica 64(1), 195–204.CrossRefGoogle Scholar
Amin, OM, Sharifdini, M, Heckmann, RA and Zarean, M (2020a) New perspectives on Nephridiacanthus major (Acanthocephala: Oligacanthorhynchidae) collected from hedgehogs in Iran. Journal of Helminthology 94, e133. 1–11. doi:10.1017/S0022149X20000073CrossRefGoogle Scholar
Amin, OM, Heckmann, RA, Dallarés, S, Constenla, M and Rubini, S (2020b) Description and molecular analysis of an Italian population of Centrorhynchus globocaudatus (Zeder, 1800) Lühe, 1911 (Acanthocephala: Centrorhynchidae) from Falco tinnunculus (Falconidae) and Buteo buteo (Accipitridae). Journal of Helminthology 94, e207. 1–21. doi: 10.1017/S0022149X20000887Google Scholar
Amin, OM, Sharifdini, M, Heckmann, RA, Rubtsova, N and Chine, HJ (2020c) On the Neoechinorhynchus agilis (Acanthocephala: Neoechinorhynchidae) complex, with the description of Neoechinorhynchus ponticus n. sp. from Chelon auratus Risso in the Black Sea. Parasite 27, 48. doi: 10.1051/parasite/2020044.CrossRefGoogle Scholar
Bhattacharya, SB (2003) First report on the occurrence of Macracanthorhynchus hirudinaceus (Pallas, 1781) and Polymorphus magnus Skrjabin, 1913 (Acanthocephala) in wild pig and garganey teal in India. Records of the Zoological Survey of India 101(part 1–2), 87–91.Google Scholar
Bizhga, B, Laçi, D and Gjoni, N (2013) Data about Macracanthorhynchus hirudinaceus in Albania. Anglisticum Journal 2, 176–181.Google Scholar
Byram, JE and Fisher, FM Jr (1973) The absorptive surface of Moniliformis dubius (Acanthocephala). 1. Fine structure. Tissue and Cell 5, 553–579.Google Scholar
Ciocco, RB, Carpinetti, BN, Rojas, P, Castresana, G and Notarnicola, J (2019) Endoparásitos de una población de cerdos silvestres (Sus scrofa) en Bahía Samborombón, Buenos Aires, Argentina [Endoparasites of a population of wild pigs (Sus scrofa) in Samborombón Bay, Buenos Aires, Argentina]. Revista Mexicana de Biodiversidad 90(1), e902851. [In Spanish.]CrossRefGoogle Scholar
Dollfus, RP (1953) Miscellanea Helminthologica Maroccana. XI. Sur cinq especes d'acanthocéphales dont une du herisson Aethechinus algirus (Duvernoy et Lereboullet, 1840) [Helminthologica Maroccana. XI. On five acanthocephalic species, including one from the hedgehog Aethechinus algirus (Duvernoy and Lereboullet, 1840)]. Archives de l'Institut Pasteur du Maroc 4(8), 541–562. [In French.]Google Scholar
García-Varela, M, Mendoza-Garfias, B, Choudhury, A and Pérez-Ponce de León, G (2017) Morphological and molecular data for a new species of Pomphorhynchus Monticelli, 1905 (Acanthocephala: Pomphorhynchidae) in the Mexican redhorse Moxostoma austrinum Bean (Cypriniformes: Catostomidae) in central Mexico. Systematic Parasitology 94(9), 989–1006.CrossRefGoogle Scholar
García-Varela, M, Masper, A, Crespo, EA and Hernández-Orts, JS (2021) Genetic diversity and phylogeography of Corynosoma australe Johnston, 1937 (Acanthocephala: Polymorphidae), an endoparasite of otariids from the Americas in the northern and southern hemispheres. Parasitology International 80, 102205. doi:10.1016/j.parint.2020.102205CrossRefGoogle Scholar
Gilbert, LI (2009) Insect development: Morphogenesis, molting and metamorphosis. 1st ed. p. 730. Amsterdam and Boston, Elsevier (Academic Press).Google Scholar
Golvan, YJ (1962) Le Phylum des Acanthocephala. La Class des Archiacanthocephala (A. Meyer 1931). Annales de Parasitologie Humaine et Comparee 37, 1–72.Google Scholar
Golvan, YJ (1994) Nomenclature of the Acanthocephala. Research and Reviews in Parasitology 54(3), 1–210.Google Scholar
Ha, NV, Amin, OM, Ngo, HD and Heckmann, RA (2018) Descriptions of acanthocephalans, Cathayacanthus spinitruncatus (rhadinorhynchidae) male and Pararhadinorhynchus magnus n. sp. (Diplosentidae), from marine fish of Vietnam, with notes on Heterosentis holospinus (Arhythmacanthidae). Parasite 25, 35.Google Scholar
Heckmann, RA, Amin, OM and Standing, MD (2007) Chemical analysis of metals in acanthocephalans using energy dispersive X-ray analysis (EDXA, XEDS) in conjunction with a scanning electron microscope (SEM). Comparative Parasitology 74(2), 388–391.CrossRefGoogle Scholar
Heckmann, RA, Amin, OM, Radwan, NAE, Standing, MD, Eggett, DL and El Naggar, AM (2012) Fine structure and energy dispersive X-ray analysis (EDXA) of the proboscis hooks of Radinorynchus ornatus, Van Cleave 1918 (Rhadinorynchidae: Acanthocephala). Scientia Parasitologica 13(1), 37–43.Google Scholar
Heckmann, RA, Amin, OM and El Naggar, AM (2013) Micropores of Acanthocephala, a scanning electron microscopy study. Scientia Parasitologica 14(3), 105–113.Google Scholar
Hoklova, IG (1986) The acanthocephalan fauna of terrestrial vertebrates of the USSR. p. 276. Moscow, Nauka.Google Scholar
Kaiser, JE (1891) Die Acanthocephalen und ihre entwicklung [The Acanthocephala and their development]. Bibliotheca Zoologica 7, 1–136. [In German.]Google Scholar
Kamimura, K, Yonemitsu, K, Maeda, K, Sakaguchi, S, Setsuda, A, Varcasi, A and Sato, H (2018) An unexpected case of a Japanese wild boar (Sus scrofa leucomystax) infected with the giant thorny-headed worm (Macracanthorhynchus hirudinaceus) on the mainland of Japan (Honshu). Parasitology Research 117, 2315–2322.CrossRefGoogle Scholar
Lee, RE (1992) Scanning electron microscopy and X-Ray microanalysis. p. 458. Englewood Cliffs, New Jersey, Prentice Hall.Google Scholar
Lei, M-T, Cai, J-Z, Li, C-H, Fu, Y, Sun, J, Ma, D-D, Li, Y-P- and Zhang, Y-M (2020) Prevalence and genetic diversity of Echinorhynchus gymnocyprii (Acanthocephala: Echinorhynchidae) in schizothoracine fishes (Cyprinidae: Schizothoracinae) in Qinghai-Tibetan Plateau, China. Parasites & Vectors 13, 357. doi:10.1186/s13071-020-04224-wCrossRefGoogle ScholarPubMed
Lisitsyna, OI (2019) Fauna of Ukraine, vol. 31. Acanthocephala. Kyiv, Naukova Dumka. 1–223 [In Russian].Google Scholar
Meyer, A (1932–1933) Acanthocephala. Dr. H.G. Bronns, Klassen und Ordnungen des Tier-Reichs, Leipzig, Akademische Verlagsgesellschaft, Band 4, Abt. 2, Buch 2, I-II Lief.: 1–582.Google Scholar
Meyer, A (1932) Dr. H. G. Bronns, Klassen und Ordnungen des Tierreichs. 4. Band. 2. Abt., 1. Buch Acanthocephala. Leipzig, Germany, Akademichie Verlagsgesellschaft.Google Scholar
Miller, DM and Dunagan, TT (1971) Studies on the Rostellar Hooks of Macracanthorhynchus hirudinaceus (Acanthocephala) from swine. Transactions of the American Microscopical Society 90(3), 329–335.CrossRefGoogle Scholar
Murray, RK, Granner, DK and Rodwell, VW (2006) Harper's illustrated biochemistry. 27th edn. p. 672. New York, McGraw-Hill.Google Scholar
Naidu, KV (2012) Fauna of India and the adjacent countries—Acanthocephala. p. 638. Kolkata, Zoological Survey of India.Google Scholar
O'Mahony, EM, Bradley, DG, Kennedy, CR and Holland, CV (2004) Evidence for the hypothesis of strain formation in Pomphorhynchus laevis (Acanthocephala): an investigation using mitochondrial DNA sequences. Parasitology 129(3), 341–347.CrossRefGoogle ScholarPubMed
Pallas, PS (1781) Bemerkungen über die Bandwürmer in Menschen und Thieren [Remarks on the tapeworms in man and animals]. Neue Nordische Beyträge zur Physikalischen und Geographischen Erd-und Völkerbeschreibung, Naturgeschichte und Oekonomie. St. Petersburg und Leipzig, I (I), 39–112. [In German.]CrossRefGoogle Scholar
Peters, W, Taraschewski, H and Latka, I (1991) Comparative investigations of the morphology and chemical composition of the eggshells of Acanthocephala. I. Macracanthorhynchus hirudinaceus (Archiacanthocephala). Parasitology Research 77(6), 542–549.CrossRefGoogle Scholar
Petrochenko, VI (1958) Acanthocephala of domestic and wild animals. Vol. 2. Moscow, Izdatel'stvo Akademii Nauk SSSR. (In Russian) (English translation by Israel Program for Scientific Translations, Ltd., Jerusalem, 1971, 478 pp.)Google Scholar
Pinacho-Pinacho, CD, García-Varela, M, Sereno-Uribe, AL and Pérez-Ponce de León, G (2018) A hyper-diverse genus of acanthocephalans revealed by tree-based and non-tree-based species delimitation methods: ten cryptic species of Neoechinorhynchus in Middle American freshwater fishes. Molecular Phylogenetics and Evolution 127, 30–45.CrossRefGoogle ScholarPubMed
Richardson, DJ (2005) Identification of cystacanths and adults of Oligacanthorhynchus tortuosa, Macracanthorhynchus ingens, and Macracanthorhynchus hirudinaceus based on probiscis and hook morphometrics. Journal of Arkansas Academy of Science 59, 205–209.Google Scholar
Rosas-Valdeza, R, Morrone, JJ, Pinacho-Pinacho, CD, Domínguez-Domínguez, O and García-Varela, M (2020) Genetic diversification of acanthocephalans of the genus Floridosentis Ward 1953 (Acanthocephala: Neoechinorhynchidae), parasites of mullets from the Americas. Infection, Genetics and Evolution 85, 104535. doi: 10.1016/j.meegid.2020.104535.CrossRefGoogle Scholar
Rubtsova, NY and Heckmann, RA (2019) Structure and morphometrics of Ancyrocephalus paradoxus (Monogenea: Ancyrocephalidae) from Sander lucioperca (Percidae) in Czechia. Helminthologia 56(1), 11–21.CrossRefGoogle Scholar
Rubtsova, NY and Heckmann, RA (2020) Morphological features and structural analysis of plerocercoids of Spirometra erinaceieuropaei (Cestoda: Diphyllobothriidae) from European pine marten, Martes martes (Mammalia: Mustelidae) in Ukraine. Comparative Parasitology 87, 109–117.CrossRefGoogle Scholar
Rubtsova, NY, Heckmann, RA, Smit, WS, Luus-Powell, WJ, Halajian, A and Roux, F (2018) Morphological studies of developmental stages of Oculotrema hippopotami (monogenea: Polystomatidae) infecting the eye of Hippopotamus amphibius (Mammalia: Hippopotamidae) using SEM and EDXA with notes on histopathology. Korean Journal of Parasitology 56(5), 463–475.CrossRefGoogle ScholarPubMed
Sarkari, B, Mansouri, M, Najjari, M, Derakhshanfar, A and Mowlavi, G (2016) Macracanthorhynchus hirudinaceus: the most common helminthic infection of wild boars in southwestern Iran. Journal of Parasitic Diseases 40(4), 1563–1566.CrossRefGoogle ScholarPubMed
Standing, MD and Heckmann, RA (2014) Features of acanthocephalan hooks using dual beam preparation and XEDS phase maps. In: Microscopy and Microanalysis Meeting, Hartford, Connecticut, U.S.A. Poster. Submission Number 0383–00501.CrossRefGoogle Scholar
Tamura, K, Stecher, G, Peterson, D, Filipski, A and Kumar, S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30(12), 2725–2729.CrossRefGoogle ScholarPubMed
Travassos, L (1917) Contribuições para o conhecimento da fauna helmintolojica brazileira. VI. Revisao dos acantocefalos brazileiros. Parte I. Fam. Gigantorhynchidae Hamann, 1892 [Contributions to the knowledge of the Brazilian helminthic fauna. SAW. Review of Brazilian acanthocephalus. Part I. Gigantorhynchidae Hamann, 1892]. Memórias do Instituto Oswaldo Cruz 9(I), 5–62. [In Portuguese.]CrossRefGoogle Scholar
Van Cleave, HJ (1953) Acanthocephala of North American mammals. Illinois Biological Monographs 23, 1–179.Google Scholar
Vardić Smrzlić, I, Valić, D, Kapetanović, D, Filipović, MV, Gjurčević, E and Teskeredžić, E (2015) Pomphorhynchus laevis (Acanthocephala) from the Sava River basin: new insights into strain formation, mtDNA-like sequences and dynamics of infection. Parasitology International 64(5), 243–250.CrossRefGoogle ScholarPubMed
Wang, B (2016) Keratin: structure, mechanical properties, occurrence in biological organisms, and efforts at bioinspiration. Progress in Materials Science 76, 229–318.CrossRefGoogle Scholar
Whitfield, PJ (1979) The biology of parasitism: An introduction to the study of associating organisms. p. 277. Baltimore, University Park Press.Google Scholar
Wright, RD and Lumsden, RD (1969) Ultrastructure of the tegumentary pore-canal system of the Acanthocephalan Moniliformis dubius. Journal of Parasitology 55(5), 993–1003.CrossRefGoogle Scholar
Xuesi, L, Fu, Z and Shuangmin, W (1982) Studies on the morphology of Macracanthorhynchus hirudinaceus (Pallas, 1781) and investigation of infection rate of pig in slaughter houses in Tangshan. Zoological Research 3(3), 295–302.Google Scholar