Hostname: page-component-75d7c8f48-665pl Total loading time: 0 Render date: 2026-03-23T01:12:15.167Z Has data issue: false hasContentIssue false
  • English
  • Français

Morphological and molecular characterization of plagiorchiid trematodes (Plagiorchis: Plagiorchiidae, Digenea) from bats with redescription of Plagiorchis mordovii Shaldybin, 1958

Published online by Cambridge University Press:  03 January 2024

N.Y. Kirillova Open the ORCID record for N.Y. Kirillova [Opens in a new window] ,
A.A. Kirillov Open the ORCID record for A.A. Kirillov [Opens in a new window] ,
S.V. Shchenkov Open the ORCID record for S.V. Shchenkov [Opens in a new window] ,
A.E. Knyazev Open the ORCID record for A.E. Knyazev [Opens in a new window]  and
V.A. Vekhnik Open the ORCID record for V.A. Vekhnik [Opens in a new window]
N.Y. Kirillova
Affiliation:
Laboratory for Biodiversity, Institute of Ecology of Volga River Basin RAS, Samara Federal Research Scientific Center RAS, Togliatti, 445003, Russia
A.A. Kirillov*
Affiliation:
Laboratory for Biodiversity, Institute of Ecology of Volga River Basin RAS, Samara Federal Research Scientific Center RAS, Togliatti, 445003, Russia
S.V. Shchenkov
Affiliation:
Department of Invertebrate Zoology, Saint Petersburg State University, St Petersburg, 199034, Russia
A.E. Knyazev
Affiliation:
Laboratory for Biodiversity, Institute of Ecology of Volga River Basin RAS, Samara Federal Research Scientific Center RAS, Togliatti, 445003, Russia
V.A. Vekhnik
Affiliation:
Laboratory for Biodiversity, Institute of Ecology of Volga River Basin RAS, Samara Federal Research Scientific Center RAS, Togliatti, 445003, Russia
*
Corresponding author: A.A. Kirillov; Email: parasitolog@yandex.ru
Get access Rights & Permissions [Opens in a new window]

Abstract

Five Plagiorchis spp. parasitize bats in European Russia: Plagiorchis elegans, Plagiorchis koreanus, Plagiorchis mordovii, Plagiorchis muelleri, and Plagiorchis vespertilionis. Their identification is difficult due to a high morphological similarity. The morphological variability of these species is poorly studied. The taxonomic position of P. mordovii remains debatable. The purpose of our study was to analyse Plagiorchis spp. from European bats using a combination of morphological and molecular-phylogenetic approaches and to establish the taxonomic position of the problematic species P. mordovii. Plagiorchis spp. were shown to be variable morphologically and morphometrically both from various host species and from different specimens of the same species. We presented a new taxonomic key for identification of the Plagiorchis spp. from European bats, provided a complete description of Plagiorchis mordovii, and confirmed the validity and the generic affiliation of this species.

Keywords

TrematodaPlagiorchis28S rRNAmolecular phylogenybats

Information

Type
Research Paper
Information
Journal of Helminthology , Volume 98 , 2024 , e2
Copyright
© The Author(s), 2024. 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.)

Article purchase

Temporarily unavailable

References

Alvarez, F, Rey, J, Quintero, P, Iglesias, R, Santos, M, and Sanmartin, L (1991) Helminth parasites in some Spanish bats. Wiadomosci Parazytologiczne 37(3), 321–329.Google ScholarPubMed
Anaconda Software Distribution (2020) Anaconda documentation. Anaconda Inc. Available at https://docs.anaconda.com/ (accessed 12 August 2023).Google Scholar
Anikanova, VS, Bugmyrin, SV, and Ieshko, EP (2007) Methods of the collection and studies of helminths of small mammals. Petrozavodsk, Karelian Scientific Center of RAS. [in Russian]Google Scholar
Bakke, TA and Mehl, R (1977) Two species of fluke recorded in bats in Norway. Fauna Oslo 30(4), 224–226. [in Norwegian]Google Scholar
Bowles, J, Blair, D, and McManus, DP (1992) Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Molecular and Biochemical Parasitology 54(2), 165–173. DOI: 10.1016/0166-6851(92)90109-w.CrossRefGoogle ScholarPubMed
Braun, M (1900) Trematoden der Chiroptera. Annalen des Naturhistorischen Museums in Wien 15(3), 215–236. [in German]Google Scholar
Chiriac, E and Barbu, P (1973) Comparative study of the helminth parasites of Chiroptera in Roumania. (1st communication). Analele - Universitatii Bucuresi (Biol. anim.) 22, 19–24.Google Scholar
Dawes, B (1946) The Trematoda. Cambridge, Cambridge University Press.Google Scholar
Demidova, TN and Vekhnik, VP (2004) Trematodes (Trematoda, Monorchiidae) of Myotis brandtii and M. mystacinus (Chiroptera, Vespertilionidae) in the Samarskaya Luka (Russia). Vestnik Zoologii 38(5), 71–74. [in Russian]Google Scholar
Devi, KR, Narain, K, Agatsuma, T, Blair, D, Nagataki, M, Wickramasinghe, S, Yatawara, L, and Mahanta, J (2010) Morphological and molecular characterization of Paragonimus westermani in northeastern India. Acta Tropica 116(1), 31–38. DOI: 10.1016/j.actatropica.2010.05.003.CrossRefGoogle ScholarPubMed
Esteban, JG, Botella, P, Toledo, R, and Oltra-Ferrero, JL (1999) Helminthfauna of bats in Spain. IV. Parasites of Rhinolophus ferrumequinum (Schreber, 1774) (Chiroptera: Rhinolophidae). Research and Reviews in Parasitology 59(1–2), 57–68.Google Scholar
Gouy, M, Guindon, S, and Gascuel, O (2010) SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution 27, 221–224. DOI: 10.1093/molbev/msp259.CrossRefGoogle ScholarPubMed
Groschaft, J and Tenora, F (1973) Trematodes of the genus Plagiorchis Lьhe, 1899 (Plagiorchiidae), parasites of bats in Afghanistan. Vestnik Ceskoslovenske Zoologicke Spolecnosti 37(4), 241–249.Google Scholar
Groschaft, J and Tenora, F (1974) Some remarks on the morphological variability of the species Plagiorchis vespertilionis (Mьller, 1780) and Plagiorchis koreanus Ogata, 1938 (Trematoda, Plagiorchiidae) parasitizing bats. Acta Universitatis Agriculturae 22(1), 115–130.Google Scholar
Gu, Z (2022) Complex heatmap visualization. Imeta 1(3), e43. DOI:10.1002/imt2.43.CrossRefGoogle Scholar
Gulyaev, VD, Orlovskaya, OM, and Dokuchaev, NЕ (2002) Helminths of bats from Magadan region. Plecotus et al. 5, 86–92. [in Russian]Google Scholar
Hillis, DM and Dixon, MT (1991) Ribosomal DNA: molecular evolution and phylogenetic inference. Quarterly Review of Biology 66, 411–453. DOI: 10.1086/417338.CrossRefGoogle ScholarPubMed
Ivashkin, VM, Kontrimavichus, VL, and Nazarova, NS (1971) Methods of the collection and studies of helminths of land mammals. Moscow, Nauka. [in Russian]Google Scholar
Katoh, K and Standley, DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30(4), 772–780. DOI: 10.1093/molbev/mst010.CrossRefGoogle ScholarPubMed
Kirillov, AA and Kirillova, NYu (2010) Morphological variability of Plagiorchis elegans (Rudolphi, 1802) (Trematoda: Plagiorchiidae) from lacertid lizards of the Middle Volga region. Proceedings of the Samara Scientific Center of RAS 12(1), 138–141. [in Russian]Google Scholar
Kirillov, AA, Kirillova, NYu, and Chikhlyaev, IV (2012a) Trematodes of terrestrial vertebrates of the Middle Volga region. Togliatti, Cassandra. [in Russian]Google Scholar
Kirillov, AA, Kirillova, NYu, and Vekhnik, VP (2012b) Trematodes (Trematoda) of bats (Chiroptera) from the Middle Volga region. Parazitologiia 46(5), 384–413. [in Russian]Google ScholarPubMed
Kirillov, AA, Ruchin, AB, and Artaev, ON (2015) Helminths of bats (Chiroptera) from Mordovia. Bulletin of Volzhsky University after V.N. Tatischev 4(19), 319–328. [in Russian]Google Scholar
Kirillov, AA, NYu, Kirillova, YuP, Krasnobayev, and Vekhnik, VP (2017) Parasitic worms of small mammals in Zhiguli State Nature Reserve. Moscow, Committee of RAS for the Conservation of Biological Diversity, A.N. Severtzov Institute of Ecology and Evolution of RAS. [in Russian]Google Scholar
Kirillova, NYu and Kirillov, AA (2017) Overview of helminths in small mammals in the Zhiguli State Reserve. Nature Conservation Research 2(2), 24–37. DOI: 10.24189/ncr.2017.007. [in Russian]CrossRefGoogle Scholar
Kirillova, NYu, Kirillov, AA, and Vekhnik, VP (2007) Trematodes of the brown long-eared bat Plecotus auritus (Chiroptera, Vespertilionidae) from Samarskaya Luka. Plecotus et al. 10, 75–81. [in Russian]Google Scholar
Kirillova, NYu, Kirillov, AA, Vekhnik, VP, Ruchin, AB, and Grishutkin, GF (2018) Helminths of bats (Chiroptera) in Smolny National Park: preliminary Data. Proceedings of Mordovia State Nature Reserve 21, 223–230. [in Russian]Google Scholar
Kirillova, NYu, Kirillov, AA, Vekhnik, VA, and Ruchin, AB (2023) Trematodes of small mammals (Soricomorpha, Erinaceomorpha, Chiroptera, Rodentia) in the Middle-Volga region (European Russia). Occurrence dataset. Version 1.6. Institute of Ecology of the Volga river basin of Russian Academy of Sciences. Available at https://doi.org/10.15468/gmt9ct\ (accessed 01 October 2023).CrossRefGoogle Scholar
Kochseder, G (1969) Untersuchungen ьber Trematoden und Cestoden aus Fledermдusen in der Steiermark. Sitzungsberichten der Цsterr. Akademie der Wissenschaften book series 8, 205–232. [in German]CrossRefGoogle Scholar
Krasnolobova, TA (1977) Principles of trematode taxonomy of genus Plagiorchis Luhe, 1899. Proceedings of Helminthological Laboratory of the USSR 27, 65–110. [in Russian]Google Scholar
Krasnolobova, TA (1987) Trematodes of fauna of the USSR. Genus Plagiorchis. Moscow, Nauka. [in Russian]Google Scholar
Kudlai, O, Pantoja, C, O’Dwyer, K, Jouet, D, Skirnisson, K, and Faltynkova, A (2021) Diversity of Plagiorchis (Trematoda: Digenea) in high latitudes: species composition and snail host spectrum revealed by integrative taxonomy. Journal of Zoological Systematics and Evolutionary Research 59(5), 937–962. DOI: 10.1111/jzs.12469.CrossRefGoogle Scholar
Kurochkin, YuV and Kurochkina, ZA (1962) To the helminth fauna of bats of the Astrakhan Nature Reserve. Proceeding Astrakhan Nature Reserve. Helminthological Issue 6, 127–134. [in Russian]Google Scholar
Lanza, B (1999) I parassiti dei pipistrelli (Mammalia, Chiroptera) della fauna italiana. Turin, Museo Regionale di Scienze Naturali. [in Italian]Google Scholar
Lebedeva, DI, Belkin, VV, Stanyukovich, MK, Bespyatova, LA, and Bugmyrin, SV (2020) First records of bat parasites in Karelia. Transactions of the Karelian Research Centre of the Russian Academy of Sciences 8, 120–125. DOI: 10.17076/bg1142.Google Scholar
Lord, JS, Parker, S, Parker, F, and Brooks, DR (2012) Gastrointestinal helminths of pipistrelle bats (Pipistrellus pipistrellus/Pipistrellus pygmaeus) (Chiroptera: Vespertilionidae) of England. Parasitology 139, 366–374. DOI: 10.1017/S0031182011002046.CrossRefGoogle ScholarPubMed
Matsaberidze, GV and Khotenovsky, IA (1967) To the trematode fauna of bats in Georgia. pp. 83–94 in Kurashvili, BE (Ed), Helminth fauna of animals and plants in Georgia. Tbilisi, Metsniereba. [in Russian]Google Scholar
Matskasi, I (1967) The systematico-faunistical survey of the trematode fauna of Hungarian bats I. Annales Historico-Naturales Musei Nationalis Hungarici 59, 217–238.Google Scholar
Matskasi, I (1973) А Bakony–Hegyseg kisemloseinek metely (trematodes) faunaja I. Vеszрrem Megyei Muzeumok Kцzlemenyei 12, 253–256. [in Hungarian]Google Scholar
Meszaros, F and Mas-Coma, S (1980) On some parasitic helminths from Spanish bats. Parasitologia Hungarica 13, 59–64.Google Scholar
Miller, MA, Pfeiffer, W, and Schwartz, T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. pp. 1–8 in Proceedings of the gateway computing environments workshop (GCE), New Orleans, Louisiana, 2010. New Orleans, IEEE.CrossRefGoogle Scholar
Müller, OF (1780) Zoologiae Danicae: seu Animalium Daniae et Norvegiae rariorum ac minus notorum icones. vol. 2. Havniae, Hallager, pp. 41–80. [in German]Google Scholar
Müller, OF (1784) Zoologiae Danicae: seu Animalium Daniae et Norvegiae rariorum ac minus notorum descriptiones et historia. vol. 2. Explicationi iconum fasciculi secundi eiusdem operi inserviens. Lipsiae, Muller. [in German]Google Scholar
Naumkin, DV and Sivkova, TN (2019) New data on bats (Chiroptera: Vespertilionidae) of the Ural region. Proceedings of Samara Scientific Center of RAS 21(2), 210–214. [in Russian]Google Scholar
Nylander, JAA (2004) MrModeltest v2. Program Distributed by the Author; Evolutionary Biology Centre, Uppsala: Uppsala University. Available at https://github.com/nylander/MrModeltest2/releases (accessed 01 July 2023).Google Scholar
Odening, K (1964) Exkretionssystem und systematische stellung exkretionssystem und systematische stellung einiger fledermaustrematoden aus Berlin und umgebung nebst bemerkungen zum Lecithodendrioiden komplex. Zeitschrift fur Parasitenkunde 24(5), 453–483. [in German]CrossRefGoogle Scholar
Ogata, T (1938) Contribution a la connaissance de la faune helminthologique Coreenne. I. Une nouvelle espece de trйmatode provenant de chauves-souris. Annotationes Zoologicae Japonenses 17, 581–586.Google Scholar
Orlovskaya, OM and Dokuchaev, NЕ (2017) Trematodes from the Siberian bat (Myotis sibirica) in Kamchatka. Bulletin of the North-East Scientific Center, Russia Academy of Sciences Far East Branch 3, 80–82. [in Russian]Google Scholar
Orlovskaya, OM, Dokuchaev, NЕ, Atrashkevich, GI, and Lazutkin, AN (2022) Trematoda Plagiorchis koreanus (Plagiorchiidae) from the Siberian bat (Myotis sibirica) from northern Priokhotye (Magadan Oblast). Bulletin of the North-East Scientific Center, Russia Academy of Sciences Far East Branch 3, 101–105. DOI: 10.34078/1814-0998-2022-3-101-105. [in Russian]CrossRefGoogle Scholar
Paradis, E and Schliep, K (2019) Ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35, 526–528. DOI: 10.1093/bioinformatics/bty633.CrossRefGoogle ScholarPubMed
Perez-Ponce de Leon, G and Hernandez-Mena, DI (2019) Testing the higher-level phylogenetic classification of Digenea (Platyhelminthes, Trematoda) based on nuclear rDNA sequences before entering the age of the ‘next-generation’ Tree of Life. Journal of Helminthology 93(3), 260–276. DOI: 10.1017/S0022149X19000191.CrossRefGoogle ScholarPubMed
R Core Team (2022) R: a Language and environment for statistical computing. R foundation for statistical computing. Available online: http://www.r-project.org/index.html (accessed on 22 December 2022).Google Scholar
Ricci, M (1995) Trematode parasites of Italian bats. Parassitologia 37(2–3), 199–214.Google ScholarPubMed
Ruchin, AB, Kirillov, AA, Chikhlyaev, IV, and Kirillova, NYu (2016) Parasitic worms of land vertebrates of the Mordovia Nature Reserve. Flora and fauna of reserves. vol. 124. Moscow, Сommittee of RAS for the Conservation of Biological Diversity. [in Russian]Google Scholar
Rysavy, B (1956) Cizopasni cervi netopyru (Microchiroptera) prezimujicich v nekterych jeskynich Ceskoslovenska. Ceskoslovenska Parasitologie 3, 161–179. [in Czech]Google Scholar
Shaldybin, LS (1964) Helminth fauna of mammals in Mordovia State Nature Reserve. Proceedings of Mordovia State Nature Reserve 2, 135–180. [in Russian]Google Scholar
Sharpilo, VP and Iskova, NI (1989) Trematodes. Plagiorchiata . Fauna of Ukraine. vol. 34. Kiev, Naukova Dumka. [in Russian]Google Scholar
Sharpilo, VP and Tkach, VV (1992) About type species of genus Plagiorchis Luhe, 1899 (Trematoda, Plagiorchiidae). Vestnik Zoologii 5, 8–15. [in Russian]Google Scholar
Shimalov, V (2021) The helminth fauna of the serotine bat Eptesicus serotinus (Chiroptera, Vespertilionidae) in southern Belarus. Annals of Parasitology 67(3), 549–552. DOI: 10.17420/ap6703.370.Google ScholarPubMed
Shimalov, VV, Demyanchik, MG, and Demyanchik, VT (2002) A study on the helminth fauna of the bats (Mammalia, Chiroptera: Vespertilionidae) in Belarus. Parasitology Research 88, 1011 DOI 10.1007/s004360100415.Google Scholar
Shimalov, VV, Demyanchik, MG, and Demyanchik, VT (2011) The helminth fauna of bats (Microchiroptera) in the Republic of Belarus. Proceedings of the National Academy of Sciences of Belarus. Biological Series 3, 104–110. [in Russian]Google Scholar
Skrjabin, KI and Antipin, DI (1958) Superfamily Plagiorchiidae Lьhe, 1901. pp. 75–634 in Skrjabin, KI (Ed), Essentials of trematodology. Trematodes of animals and man. vol. 14. Moscow, Academy of Sciences of the USSR. [in Russian]Google Scholar
Skvortsov, VG (1972) Trematodes of the family Plagiorchiidae Lьhe, 1901 from bats in Moldavia. Parasites of Animals and Plants 8, 46–50. [in Russian]Google Scholar
Soltys, A (1959) The helminth fauna of bats (Chiroptera) of Lublin palatinate. Acta Parasitologica Polonica 7(34), 599–613.Google Scholar
Suleman Ma, J, Khan, MS, Tkach, VV, Muhammad, N, Zhang, D, and Zhu, XQ (2019) Characterization of the complete mitochondrial genome of Plagiorchis maculosus (Digenea, Plagiorchiidae), Representative of a taxonomically complex digenean family. Parasitology International 71, 99–105. DOI: 10.1016/j.parint.2019.04.001.CrossRefGoogle Scholar
Sumer, N and Yildirimhan, HS (2017) DNA sequencing of Digenea nuclear lsrDNA of the whiskered brown bat, Myotis aurescens (Vespertilionidae: Chiroptera), from Turkey. Turkish Journal of Zoology 41, 64–66. DOI: 10.3906/zoo-1508-52.CrossRefGoogle Scholar
Sumer, N and Yildirimhan, HS (2018) Helminth parasites of the whiskered brown bat, Myotis aurescens (Kuzyakin, 1935) (Chiroptera: Vespertilionidae) from Turkey. Acta Zoologica Bulgarica 70(1), 113–116.Google Scholar
Sumer, N and Yildirimhan, HS (2019) Intestinal helminth parasites of two bat species of the Ggenus Myotis Kaup, 1829 (Chiroptera: Vespertilionidae) from Turkey, with DNA sequencing of helminth nuclear LSR rDNA. Acta Zoologica Bulgarica 71(2), 273–278.Google Scholar
Tamura, K, Stecher, G, and Kumar, S (2021) MEGA11: Molecular Evolutionary Genetics Analysis version 11. Molecular Biology and Evolution 38(7), 3022–3027. DOI: 10.1093/molbev/msab120.CrossRefGoogle ScholarPubMed
Tkach, VV (2008) Family Plagiorchiidae Lьhe, 1901. pp. 295–325 in Bray, RA, Gibson, DJ, and Jones, A (Eds), Keys to Trematoda. vol. 3. London, UK, CAB International and Natural History Museum,.CrossRefGoogle Scholar
Tkach, VV and Sharpilo, VP (1990) A new trematode species (Trematoda, Plagiorchiidae) from bats. pp. 11–13 in Akimov, IA (Ed), News of faunistics and taxonomy. Kiev, Naukova Dumka. [in Russian]Google Scholar
Tkach, V, Pawlowski, J, and Mariaux, J (2000a) Phylogenetic analysis of the suborder Plagiorchiata (Platyhelminthes, Digenea) based on partial lsrDNA sequences. International Journal of Parasitology 30(1), 83–93. DOI: 10.1016/s0020-7519(99)00163-0.CrossRefGoogle ScholarPubMed
Tkach, VV, Pawlowski, J, and Sharpilo, VP (2000b) Molecular and morphological differentiation between species of the Plagiorchis vespertilionis group (Digenea, Plagiorchiidae) occurring in European bats, with a re-description of P. vespertilionis (Muller, 1780). Systematic Parasitology 47, 9–22. DOI: 10.1023/A:1006358524045.CrossRefGoogle ScholarPubMed
Yamaguti, S (1958) Systema helminthum. The digenetic trematodes of vertebrates. vol. 1 and 2. New York, London, Interscience.Google Scholar
Yamaguti, S (1971) Synopsis of digenetic trematodes of vertebrates. Tokyo, Keigaku Publishing Co.Google Scholar
Zdzitowiecki, K (1970) Helminths of bats in Poland. I. Cestodes and trematodes of the family Plagiorchiidae. Acta Parasitologica Polonica 17(20), 175–188.Google Scholar
Zikmundova, J, Georgieva, S, Faltynkova, A, Soldanova, M, and Kostadinova, A (2014) Species diversity of Plagiorchis Lьhe, 1899 (Digenea: Plagiorchiidae) in lymnaeid snails from freshwater ecosystems in central Europe revealed by molecules and morphology. Systematic Parasitology 88(1), 37–54. DOI: 10.1007/s11230-014-9481-8.CrossRefGoogle Scholar
Supplementary material: File

Kirillova et al. supplementary material 1
Download undefined(File)
File 79.2 KB
Supplementary material: File

Kirillova et al. supplementary material 2
Download undefined(File)
File 73.8 KB
Supplementary material: File

Kirillova et al. supplementary material 3
Download undefined(File)
File 95 KB
Supplementary material: File

Kirillova et al. supplementary material 4
Download undefined(File)
File 78.5 KB