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OVERVIEW OF HELMINTHS IN BATS (CHIROPTERA, VESPERTILIONIDAE) IN THE MIDDLE VOLGA REGION
(EUROPEAN RUSSIA)
®N.Yu. Kirillova , A.A. Kirillov
Samara Federal Research Scientific Center RAS, Institute of Ecology of Volga River Basin RAS,
Russia
e-mail: parasitolog@yandex.ru
Received: 05.02.2024. Revised: 06.03.2024. Accepted: 11.03.2024.
In this study, we summarize up-to-date information on the species diversity of parasitic helminths in bats inhabiting the Middle Volga region. To one degree or another, all 16 species of bats living in the studied area were subjected to helminthological survey. According to our and literature data, 38 species of parasites were recorded in chiropterans: three tapeworms, 24 flukes, 98 nematodes, and one acanthocephalan. The core of this bat helminth fauna is formed by host-specific species that parasitize only chiropterans. The trematode Prosthodendrium cryptholecithum and nematode Physaloptera clausa, juv. are recorded for the first time in the bats in Russia. The trematodes Gyrabascus amphoraeformis and G. oppositus were recorded for the first time in the bats inhabiting the Middle Volga region. For three species of bat helminths, new hosts were revealed. The analysis of bat parasites showed that the helminth fauna of the Nyctalus noctula (19 helminth species), Myotis brandtii, Pipistrellus nathusii (15 species each) and Vespertilio murinus (14) is the most diverse. The widest range of final hosts among bats inhabiting the Middle Volga region is a characteristic for Plagiorchis koreanus, P. chilostomum and Pterothominx neopulchra (9 species each). Majority of bat helminths possesses a high degree of host specificity. Out of 38 parasite species found in representatives of the order Chiroptera, 34 species of helminths parasitize exclusively on bats. Only four species of helminths (Plagiorchis elegans, Ph. clausa, juv., Physocephalus sexalatus, juv., Moniliformis moniliformis, lrv.) demonstrate a broad degree of host specificity, parasitizing on other vertebrates.
Key words: acanthocephalans, bats, digeneans, flatworms, Mordovia, nematodes, parasitic worms, Samara region
https://dx.doi.org/10.24412/cl-31646-2686-7117-2024-34-5-22 License CC BY-NC 4.0
Cite: Kirillova N.Yu., Kirillov A.A. 2024. Overview of helminths in bats (Chiroptera, Vespertilionidae) in the Middle Volga Region (European Russia) // Proceedings of the Mordovia State Nature Reserve. Vol. 34. P. 5-22. https://dx.doi.org/10.24412/cl-31646-2686-7117-2024-34-5-22
Introduction
Bats (Chiroptera) are insectivorous animals with a unique lifestyle. These mammals have the ability to active flight that greatly affects their food chains. Chiropterans, due to their high degree of ecological isolation and specialization, are
hosts for unique helminth fauna. Most of their parasites have a high degree of host specificity (Khotenovsky, 1972; Thewissen & Babcock, 1992). Bat parasites characterized by strict host-specificity, indicate the long history and isolation of this taxonomic group of mammals (Khotenovsky, 1972).
The Middle Volga region is located approximately within 52-57° northern latitude and 45-56° eastern longitude, in the east of the Russian Plain (Mil'kov, 1953). This region includes the Republic of Chuvashia, Republic of Tatarstan, Republic of Mari El, Samara Region, Ulyanovsk Region, the western parts of the Republic of Bashkortostan and Orenburg Region, the eastern parts of the Republic of Mordovia, Penza and Nizhny Novgorod Regions, and the and the northernmost part of the Saratov Region.
The Volga basin in its middle course exhibits diverse landscapes, featuring coniferous and mixed forests in the northern region and steppe environments in the south. The largest central part of the area is occupied by forest-steppe (Gorelov et al., 1990). The location of the region within different natural zones determines the exceptional diversity of fauna and flora. Thus, plant communities of the Middle Volga region accounts for about 2050 species (Saksonov et al., 2006). Also, 85 species of mammals inhabit the Middle Volga region (Pavlinov, 2006; Ruchin et al., 2012; Smirnov & Vekhnik, 2014; Artaev & Smirnov, 2016; Smirnov et al., 2022; Mammals of Russia, 2024).
The territory of European Russia harbors 27 species of chiropterans. The bat fauna of the Middle Volga region consists of 16 species (Strelkov & Ilyin, 1990; Smirnov et al., 2007; Smirnov & Vekhnik, 2014; Mammals of Russia, 2024). The history of helminthological study of bats goes back about 60 years, if we count the works of Shaldybin (1964a,b) in the Mordovia State Nature Reserve as the start of research. During this time, the helminth fauna of all 16 bat species was subjected to helminthological research to varying degrees.
Helminthological studies of bats were conducted mainly in the territory of Mordovia and the Samara region. Data on the parasitic worms in bats inhabing the Middle Volga region is given in the works of Skarbilovich (1948), Shaldybin (1964a,b), Demidova and Vekhnik (2004). Artyukh (1950) did not identify the parasites found in bats to the species level. Since the 2000s, we have been conducting systematic research on bat helminths in the Middle Volga region.
Thus, the aim of this study is to review the helminth fauna in bats, inhabiting the territory of the Middle Volga region and to systematize data about bat parasitic worms taking into account recent conceptions.
Material and Methods
This work is based on the analysis of literature data and the results of our own studies of the helminth fauna in bats in the territory of the Republic of Mordovia and Samara region.
The databases Google Scholar and Russian scientific electronic library (eLIBRARY.ru) were used to search scientific literature on the helminths in bats from the Middle Volga region. We used both English and Russian characters in our search strings in the Russian database eLIBRARY.ru. Literature sources not indexed
in electronic databases were obtained from the library of the Mordovia State Nature Reserve. The analysis of literature on the research theme was conducted between 1960 and 2023.
Our own material on parasitic worms in bats was mainly collected from various sites within the protected areas of the Middle Volga region (Zhigulevsky State Nature Reserve, Mordovia State Nature Reserve, National Park "Samarskaya Luka" and National Park "Smolny") in the period from 2000 to 2023. The bats were caught using mist nets and mobile trap (Borisenko, 1999). We also collected weekly chiropterans that died of natural causes during wintering. Bats were examined through complete helminthological necropsy. Collection and handling of parasitological material was performed according to standard methods (Ivashkin et al., 1971; Anikanova et al., 2007). The identification of parasites was conducted in the Laboratory of Population Ecology of the Institute of Ecology of the Volga Basin of RAS (Togliatti, Russia).
The helminth taxonomy is based on the Global Cestode Database (http://tapewormdb.uconn.edu) and the Fauna Europaea (https://fauna-eu.org). The voucher specimens of parasitic helminths are deposited in the Parasitological collection at the Institute of Ecology of Volga Basin of RAS (Togliatti, Russia).
Results
Nowadays, the list of parasitic helminths in bats inhabiting the Middle Volga region accounts for 38 species including three cestodes, 24 trematodes, 10 nematodes and one acanthocephalan.
Parasite-Host checklist of helminths in bats (Chiroptera) from the Middle Volga region
Phylum Plathyhelminthes
Class Cestoidea
Family Hymenolepididae Ariola, 1899
1. Milina grisea van Beneden, 1873
Hosts: Plecotus auritus, Myotis nattereri.
Site: small intestine.
Localities: Zhigulevsky State Nature Reserve, Mordovia State Nature Reserve, National Park "Smolny" (Kirillov et al., 2017, 2018; Kirillov & Kirillova, 2017; Kirillova & Kirillov, 2017; Kirillova et al., 2023c; this study).
Widespread host-specific parasite of bats.
Distribution: Palearctic.
2. Vampirolepis balsaci (Joyeux et Baer, 1934) (= Staphylocystis syrdariensis (Skarbilovitsch, 1946) sensu Kirillov et al., 2017, 2018; Kirillov & Kirillova, 2017; Kirillova & Kirillov, 2017).
Hosts: Myotis mystacinus, M. brandtii.
Site: small intestine.
Localities: Zhigulevsky Nature Reserve, Mordovia Nature Reserve, National Park "Smolny" (Kirillov et al., 2017, 2018; Kirillov & Kirillova, 2017; Kirillova & Kirillov, 2017, 2022; Kirillova et al., 2023c; this study).
Host-specific parasite of bats.
Distribution: Palearctic.
3. V. spasskii Andreiko, Skvortzov et Konovalov, 1969 (= V. skrjabinariana (Scarbilovitsch, 1946) sensu Kirillov et al., 2017, 2018; Kirillov & Kirillova, 2017; Kirillova & Kirillov, 2017; Kirillova et al., 2018).
Hosts: Vespertilio murinus, Eptesicus nilssoni, E. serotinus, Nyctalus noctula, N. lasiopterus, N. leisleri.
Site: small intestine.
Localities: Zhigulevsky State Nature Reserve, Mordovia Nature Reserve, National Park "Samarskaya Luka", National Park "Smolny" (Kirillov et al., 2017, 2018; Kirillov & Kirillova, 2017; Kirillova & Kirillov, 2017; Kirillova et al., 2018, 2023c; this study).
Host-specific parasite of bats.
Distribution: Palearctic.
Class Trematoda
Family Plagiorchiidae Lühe, 1901
4. Plagiorchis elegans (Rudolphi, 1802)
Hosts: Plecotus auritus, Vespertilio murinus, Myotis daubentonii, Nyctalus noctula.
Site: Small intestine.
Localities: Zhigulevsky State Nature Reserve, Mordovia Nature Reserve, National Park "Smolny" (Kirillova et al., 2007a, 2023b,c, 2024; Kirillov et al., 2012, 2017, 2018; Ruchin et al., 2016; Kirillova & Kirillov, 2017; this study).
The trematode is obligate parasite of passerine birds. It is also found in other bird orders, in reptiles, shrews, bats and rodents.
Distribution: Holarctic.
5. P. koreanus Ogata, 1938
Hosts: Plecotus auritus, Vespertilio murinus, Eptesicus nilssoni, Myotis brandtii, M. mystacinus, M. daubentonii, M. dasycneme, M. nattereri, Nyctalus noctula, Pipistrellus nathusii.
Site: small intestine.
Localities: Zhigulevsky State Nature Reserve, Mordovia State Nature Reserve, National Park "Samarskaya Luka", National Park "Smolny" (Demidova & Vekhnik, 2004; Kirillova et al., 2007a, 2018, 2023a,b,c, 2024; Kirillov et al., 2012, 2015a,b, 2017, 2018; Kirillova & Kirillov, 2017, 2022; this study).
Host-specific parasite of bats.
Distribution: Cosmopolitan.
6. P. mordovii Schaldybin, 1958 (= Symmetricatesticula symmetrica (Schaldybin, 1958), Plagiorchis symmetrica Schaldybin, 1958; P. elegans sensu Demidova, Vekhnik (2004))
Hosts: Vespertilio murinus, Myotis brandtii, M. daubentonii, M. dasycneme. Site: small intestine.
Localities: Zhigulevsky State Nature Reserve, Mordovia State Nature Reserve, National Park "Smolny" (Demidova & Vekhnik, 2004; Kirillov et al., 2012, 2015a,b,
2017, 2018; Ruchin et al., 2016; Kirillova & Kirillov, 2017, 2022; Kirillova et al.,
2018, 2023a,b,c, 2024; this study). Host-specific parasite of bats. Distribution: Europe.
7. P. muelleri Tkach et Sharpilo, 1990
Hosts: Myotis mystacinus, M. brandtii, M. nattereri, Nyctalus noctula. Site: small intestine.
Localities: Zhigulevsky State Nature Reserve, Mordovia State Nature Reserve, National Park "Samarskaya Luka" (Demidova & Vekhnik, 2004; Kirillov et al., 2012, 2015a,b, 2017, 2018; Ruchin et al., 2016; Kirillova & Kirillov, 2017, 2022; Kirillova et al., 2023a,b,c, 2024).
Host-specific parasite of bats. Distribution: Holarctic.
8. P. vespertilionis (Muller, 1784)
Hosts: Vespertilio murinus, Myotis daubentonii, M. dasycneme, M. brandtii, Nyctalus noctula, N. leisleri. Site: small intestine.
Localities: Zhigulevsky State Nature Reserve, Mordovia State Nature Reserve, National Park "Smolny" (Schaldybin, 1964a,b; Demidova & Vekhnik, 2004; Kirillov et al., 2012, 2015a,b, 2017, 2018; Ruchin et al., 2016; Kirillova & Kirillov, 2017, 2022; Kirillova et al., 2018, 2023a,b,c, 2024; this study). Host-specific parasite of bats. Distribution: Palaearctic.
Family Lecithodendriidae (Lühe, 1901)
9. Lecithodendrium linstowi Dollfus, 1931
Hosts: Myotis daubentonii, M. brandtii, M. mystacinus, Nyctalus noctula, N. leisleri, Eptesicus nilssoni, Pipistrellus nathusii, P. kuhlii. Site: small intestine.
Localities: Zhigulevsky State Nature Reserve, Mordovia State Nature Reserve, National Park "Smolny", Samara city (Schaldybin, 1964a,b; Demidova & Vekhnik, 2004; Kirillov et al., 2012, 2015a,b, 2017, 2018; Ruchin et al., 2016; Kirillova & Kirillov, 2017, 2022; Kirillova et al., 2018, 2023a,b,c; this study). Widespread host-specific parasite of bats. Distribution: Palaearctic.
10. L. rysavyi Dubois, 1960
Hosts: Vespertilio murinus, Nyctalus noctula, N. leisleri, Eptesicus nilssoni, Pipistrellus pipistrellus, P. pygmaeus, P. nathusii.
Site: small intestine.
Localities: Zhigulevsky State Nature Reserve, Mordovia State Nature Reserve, National Park "Samarskaya Luka", National Park "Smolny", Zadelnoe village (Samara region) (Kirillov et al., 2012, 2017, 2018; Kirillova & Kirillov, 2017; Kirillova et al., 2018, 2023b,c; this study).
Widespread host-specific parasite of bats.
Distribution: Europe.
11. L. skrjabini Mazaberidse, 1963
Hosts: Vespertilio murinus, Nyctalus noctula, N. leisleri, Pipistrellus pipistrellus, P. pygmaeus, P. nathusii.
Site: small intestine.
Localities: Zhigulevsky State Nature Reserve, Mordovia State Nature Reserve, National Park "Samarskaya Luka", National Park "Smolny" (Kirillov et al., 2012, 2015a,b, 2017, 2018; Kirillova & Kirillov, 2017; Kirillova et al., 2018, 2023b,c; this study).
Widespread host-specific parasite of bats.
Distribution: Europe.
12. Prosthodendrium ascidia (Beneden, 1873)
Hosts: Myotis daubentonii, M. dasycneme, M. brandtii, M. mystacinus, M. nattereri, Pipistrellus nathusii.
Site: small intestine.
Localities: Zhigulevsky State Nature Reserve, Mordovia State Nature Reserve, National Park "Smolny" (Demidova & Vekhnik, 2004; Kirillov et al., 2012, 2017, 2018; Kirillova & Kirillov, 2017, 2022; Kirillova et al., 2018, 2023a,b,c; this study).
Widespread host-specific parasite of bats.
Distribution: Palaearctic.
13. P. chilostomum (Mehlis, 1831)
Hosts: Plecotus auritus, Myotis daubentonii, Myotis dasycneme, Myotis brandtii, Myotis mystacinus, Myotis nattereri, Nyctalus noctula, Nyctalus leisleri, Pipistrellus nathusii.
Site: small intestine.
Localities: Zhigulevsky State Nature Reserve, Mordovia State Nature Reserve, National Park "Samarskaya Luka", National Park "Smolny" (Demidova & Vekhnik, 2004; Kirillova et al., 2007a, 2018, 2023a,b, c; Kirillov et al., 2012, 2015a,b, 2017, 2018; Ruchin et al., 2016; Kirillova & Kirillov, 2017, 2022; this study).
Host-specific parasite of bats.
Distribution: Cosmopolitan.
14. P. cryptolecithum (Zdzitowiecki, 1969) (= P. longiforme (Bhalerao, 1926) ex parte sensu Kirillov et al 2012, 2017; Kirillova & Kirillov, 2022)
Hosts: Myotis dasycneme, M. brandtii.
Site: small intestine.
Localities: Zhigulevsky State Nature Reserve, Mordovia State Nature Reserve, National Park "Smolny" (Kirillova & Kirillov, 2022; Kirillova et al., 2023a,b; this study).
Host-specific parasite of bats. Previously known only from findings in chiropterans in Poland (Zdzitowiecki, 1969).
Distribution: Europe.
15. P. hurkovaae Dubois, 1960
Hosts: Myotis daubentonii, M. dasycneme, M. nattereri, Plecotus auritus.
Site: small intestine.
Localities: Zhigulevsky State Nature Reserve, Mordovia State Nature Reserve, National Park "Smolny" (Kirillov et al., 2012, 2017, 2018; Kirillova & Kirillov, 2017; Kirillova et al., 2018, 2022, 2023a,b,c; this study).
Host-specific parasite of bats.
Distribution: Palaearctic.
16. P. ilei Zdzitowiecki, 1969
Hosts: Nyctalus noctula, Pipistrellus nathusii, P. kuhlii, Eptesicus nilssoni.
Site: small intestine.
Localities: Zhigulevsky State Nature Reserve, Mordovia State Nature Reserve, National Park "Smolny", Samara city (Kirillov et al., 2012, 2017, 2018; Kirillova & Kirillov, 2017; Kirillova et al., 2018, 2023b,c; this study).
Host-specific parasite of bats.
Distribution: Europe.
17. P. longiforme (Bhalerao, 1926)
Hosts: Myotis daubentonii, M. brandtii, Plecotus auritus.
Site: small intestine.
Localities: Zhigulevsky State Nature Reserve, Mordovia State Nature Reserve, National Park "Samarskaya Luka", National Park "Smolny" (Demidova & Vekhnik, 2004; Kirillova et al., 2007a, 2023a,b,c; Kirillov et al., 2012, 2017, 2018; Kirillova & Kirillov, 2017, 2022; this study).
Widespread host-specific parasite of bats.
Distribution: Cosmopolitan.
18. Pycnoporus megacotyle (Ogata, 1939)
Hosts: Nyctalus leisleri, N. leisleri.
Site: small intestine.
Localities: Zhigulevsky State Nature Reserve, Mordovia State Nature Reserve, National Park "Smolny" (Kirillov et al., 2012, 2017, 2018; Kirillova & Kirillov, 2017; Kirillova et al., 2023b,c; this study).
Host-specific parasite of bats.
Distribution: Palaearctic.
19. P. heteroporus (Dujardin, 1845)
Hosts: Vespertilio murinus, Nyctalus noctula, Pipistrellus nathusii, P. kuhlii, P. pipistrellus, P. pygmaeus, Eptesicus nilssoni.
Site: small intestine.
Localities: Zhigulevsky State Nature Reserve, Mordovia State Nature Reserve, National Park "Samarskaya Luka", National Park "Smolny", Samara city, Nizhny Novgorod region (Schaldybin in Skarbilovich, 1948; Kirillov et al., 2012, 2015a,b, 2017, 2018; Kirillova & Kirillov, 2017; Kirillova et al., 2018, 2023b,c; this study).
Host-specific parasite of bats.
Distribution: Palaearctic.
Family Pleurogenidae Looss, 1899
20. Gyrabascus amphoraeformis (Modlinger, 1930) (= Alassogonoporus amphoraeformis Modlinger, 1930)
Hosts: Myotis daubentonii, M. brandtii.
Site: small intestine.
Localities: Mordovia State Nature Reserve, National Park "Smolny" (Kirillova et al., 2018, 2022, 2023b,c; this study).
Host-specific parasite of bats.
Distribution: Europe.
21. G. oppositus (Zdzitowiecki, 1969) (= Parabascus oppositus Zdzitowiecki,
1969)
Hosts: Nyctalus noctula, N. leisleri, Pipistrellus nathusii.
Site: small intestine.
Localities: Mordovia State Nature Reserve, National Park "Smolny" (Kirillova et al., 2018, 2022, 2023b,c; this study).
Host-specific parasite of bats.
Distribution: Europe.
22. Parabascus duboisi (Hurkova, 1961)
Hosts: Myotis daubentonii, M. dasycneme, M. brandtii, M. mystacinus, M. nattereri.
Site: small intestine.
Localities: Zhigulevsky State Nature Reserve, Mordovia State Nature Reserve, National Park "Samarskaya Luka", National Park "Smolny" (Demidova & Vekhnik, 2004; Kirillov et al., 2012, 2015a,b, 2017, 2018; Ruchin et al., 2016; Kirillova & Kirillov, 2017, 2022; Kirillova et al., 2022, 2023a,b,c; this study).
Host-specific parasite of bats.
Distribution: Palaearctic.
23. P. joannae (Zdzitowiecki, 1967)
Host: Pipistrellus nathusii.
Site: small intestine.
Localities: Mordovia State Nature Reserve, biological station of Mordovia State University, vicinity of Nizhny Satis village (Mordovia Republic) (Kirillov et al., 2015a,b; Ruchin et al., 2016; Kirillova et al., 2023a, b, c).
Host-specific parasite of bats.
Distribution: Europe.
24. P. lepidotus Looss, 1907
Hosts: Vespertilio murinus, Pipistrellus nathusii, Nyctalus noctula, N. leisleri, N. lasiopterus, Eptesicus nilssoni.
Site: small intestine.
Localities: Zhigulevsky State Nature Reserve, Mordovia State Nature Reserve, National Park "Samarskaya Luka", National Park "Smolny" (Schaldybin, 1964a,b; Kirillov et al., 2012, 2015a,b, 2017, 2018; Ruchin et al., 2016; Kirillova & Kirillov, 2017; Kirillova et al., 2018, 2022, 2023a,b,c; this study).
Host-specific parasite of bats.
Distribution: Palaearctic.
25. P. magnitestis Khotenovsky, 1985
Hosts: Eptesicus nilssonii, Nyctalus noctula.
Site: small intestine.
Localities: Zhigulevsky State Nature Reserve, National Park "Samarskaya Luka" (Kirillov et al., 2012, 2017, 2018; Kirillova & Kirillov, 2017; Kirillova et al., 2023b).
Host-specific parasite of bats.
Distribution: Europe.
26. P. semisquamosus (Braun, 1900)
Hosts: Nyctalus noctula, N. leisleri, N. lasiopterus, Pipistrellus nathusii, P. pipistrellus, P. pygmaeus, Eptesicus nilssoni, E. serotinus.
Site: small intestine.
Localities: Zhigulevsky State Nature Reserve, Mordovia State Nature Reserve, National Park "Samarskaya Luka", National Park "Smolny" (Kirillov et al., 2012, 2017, 2018; Ruchin et al., 2016; Kirillova & Kirillov, 2017; Kirillova et al., 2018, 2022, 2023b,c; this study).
Host-specific parasite of bats.
Distribution: Europe.
Species insertae sedis
27. Paralecithodendrium skrjabini Schaldybin, 1948
Hosts: Vespertilio murinus, Eptesicus nilssonii.
Site: small intestine.
Localities: Zhigulevsky State Nature Reserve, Mordovia State Nature Reserve, Nizhny Novgorod region (Schaldybin in Skarbilovich, 1948; Schaldybin, 1964a,b; Kirillov et al., 2012, 2015a,b, 2017, 2018; Ruchin et al., 2016; Kirillova & Kirillov, 2017; Kirillova et al., 2022, 2023b,c). Host-specific parasite of bats. Distribution: Europe.
Phylum Acanthocephala
Family Moniliformidae Van Cleave, 1925
28. Moniliformis moniliformis (Bremser, 1811), larvae
Host: Myotis nattereri. Site: small intestine.
Localities: Zhigulevsky State Nature Reserve (Kirillov et al., 2017, 2018; Kirillova & Kirillov, 2017).
Common parasite of rodents and carnivores. Distribution: Cosmopolitan.
Phylum Nematoda
Family Capillariidae Neveu-Lemaire, 1936
29. Pterothominx neopulchra (Babos, 1954) (= Thominx neopulchra (Babos, 1954)) Hosts: Vespertilio murinus, Myotis brandtii, M. daubentonii, M. dasycneme,
M. nattereri, Pipistrellus nathusii, Nyctalus noctula, N. lasiopterus, Eptesicus nilssonii. Site: stomach.
Localities: Zhigulevsky State Nature Reserve, Mordovia State Nature Reserve, National Park "Samarskaya Luka", National Park "Smolny" (Kirillov et al., 2006, 2015a,b, 2017, 2018; Kirillova et al., 2007b, 2008, 2018, 2023c; Kirillova & Kirillov, 2011, 2017; Ruchin et al., 2016; this study).
Host-specific parasite of bats from the family Vespertilionidae. Distribution: Palaearctic.
30. Aonchotheca eubursata (Skarbilovitsch, 1946) (= Skrjabinocapillaria eubursata (Skarbilovitsch, 1946))
Hosts: Nyctalus noctula, Myotis sp. (M. emarginatus E. Geoffroy, 1806 sensu Shaldybin, 1964a,b). Site: stomach.
Localities: Mordovia State Nature Reserve (Schaldybin, 1964a,b; Ruchin et al., 2016; Kirillova et al., 2023c).
Host-specific parasite of bats. Distribution: Palaearctic.
Class Chromadorea
Family Trichostrongylidae Leiper, 1908
31. Molinostrongylus alatus (Ortlepp, 1932)
Host: Myotis nattereri.
Site: small intestine.
Localities: Zhigulevsky State Nature Reserve, National Park "Smolny" (Kirillov et al., 2006, 2017, 2018; Kirillova et al., 2008, 2023c; Kirillova & Kirillov, 2011, 2017; this study).
Widespread host-specific parasite of bats from the families Vespertilionidae and Rhinolophidae.
Distribution: Palaearctic.
32. Molinostrongylus skrjabini Skarbilovitsch, 1934
Hosts: Vespertilio murinus, Nyctalus noctula, N. lasiopterus, Pipistrellus nathusii, Plecotus auritus.
Site: small intestine.
Localities: Zhigulevsky State Nature Reserve, Mordovia State Nature Reserve, National Park "Samarskaya Luka", National Park "Smolny" (Schaldybin, 1964a,b; Kirillova et al., 2007b, 2008, 2018, 2023c; Kirillova & Kirillov, 2011, 2017; Kirillov et al., 2015a,b; 2017, 2018; Ruchin et al., 2016; this study).
Widespread host-specific parasite of bats from the families Vespertilionidae and Rhinolophidae.
Distribution: Palaearctic.
33. Molinostrongylus spasskii Andrejko, Pintschuk et Skvorzov, 1968
Host: Myotis daubentonii.
Site: small intestine.
Localities: Zhigulevsky State Nature Reserve, Mordovia State Nature Reserve, National Park "Samarskaya Luka", National Park "Smolny" (Kirillov et al., 2006, 2015a,b, 2017, 2018; Kirillova et al., 2008, 2018, 2023c; Kirillova & Kirillov, 2011, 2017; Ruchin et al., 2016; this study).
Host-specific parasite of bats from the genus Myotis.
Distribution: Palaearctic.
34. M. vespertilionis Morosov et Spassky, 1961
Hosts: Pipistrellus nathusii, P. pipistrellus, Nyctalus leisleri.
Site: small intestine.
Localities: Zhigulevsky State Nature Reserve, Mordovia State Nature Reserve, National Park "Samarskaya Luka", National Park "Smolny" (Kirillova et al., 2007b, 2008, 2023c; Kirillova & Kirillov, 2011, 2017; Kirillov et al., 2015a,b, 2017, 2018; Ruchin et al., 2016; this study).
Host-specific parasite of bats from the family Vespertilionidae.
Distribution: Palaearctic.
Family Onchocercidae Leiper, 1911
35. Litomosa filaria Beneden, 1873
Host: Vespertilio murinus.
Site: body cavity.
Localities: Zhigulevsky State Nature Reserve, Mordovia State Nature Reserve, National Park "Smolny" (Kirillova & Kirillov, 2011, 2017; Kirillov et al., 2017, 2018; Kirillova et al., 2023c; this study).
Host-specific parasite of bats.
Distribution: Palaearctic.
Family Physalopteridae Railliet, 1893
36. Physaloptera clausa Rudolphi, 1819, juv.
Host: Pipistrellus nathusii.
Site: gastric mucosa.
Localities: Mordovia State Nature Reserve, National Park "Smolny" (Kirillova et al., 2023c; this study).
Common parasite of insectivores and hedgehogs. Bats are paratenic and probably abortive hosts.
Distribution: Holarctic.
Family Spirocercidae Chitwood et Wehr, 1932
37. Physocephalus sexalatus (Molin, 1860), juv.
Hosts: Plecotus auritus, Myotis dasycneme, M. brandtii, Nyctalus noctula, N. lasiopterus, P. nathusii, Eptesicus serotinus.
Site: walls of stomach and small intestine.
Localities: Zhigulevsky State Nature Reserve, Mordovia State Nature Reserve, National Park "Samarskaya Luka", National Park "Smolny" (Kirillov et al., 2006, 2015a,b, 2017, 2018; Kirillova et al., 2007b, 2008, 2023c; Kirillova & Kirillov, 2011, 2017, 2022; Ruchin et al., 2016; this study).
At the larval stage, it is a common parasite of vertebrates of various classes. Bats are paratenic and probably abortive hosts.
Distribution: Cosmopolitan.
Family Rictulariidae Railliet, 1916
38. Pterygodermatites bovieri (Blanchard, 1886) (= Rictularia bovieri (Blanchard, 1886))
Hosts: Myotis dasycneme, M. brandtii.
Site: small intestine.
Localities: Zhigulevsky State Nature Reserve (Kirillov et al., 2006, 2017, 2018; Kirillova & Kirillov, 2011, 2017, 2022; Kirillova et al., 2008, 2023c).
Host-specific parasite of bats from the family Vespertilionidae.
Distribution: Palaearctic.
Discussion
Over the 60-year period of helminthological study of bats in the Middle Volga region, 38 parasite species were recorded in 16 bat species. Thirty-four out of
38 species of helminths found in bats of the Middle Volga region, are specific parasites of chiropterans. For these helminths, bats serve as obligate hosts. Accidental findings of chiropteran parasites in hares (P. vespertilionis) and fish (P. chilostomum) were recorded (Kontrimavichus, 1955; Morozova & Zhokhov, 2016).
Four helminth species (trematode Plagiorchis elegans, nematodes Ph. clausa, juv., Physocephalus sexalatus, juv., Moniliformis moniliformis, lrv.,) show wide degree of host-specificity, being parasitized vertebrates from various taxonomic groups.
The characteristic feature of the helminth fauna in bats is that they have a small number of larval forms of parasites, which confirms the high degree of strong ecological isolation of this animals. The vast majority of helminths (35 species) in these flying mammals are represented by adult forms. Only three species of helminths are parasitized bats at the larval stage. For them bats of the Middle Volga region serve as paratenic and/or transit hosts.
Trematodes prevail in the helminth fauna of bats (24 species), which is due to the feeding of animals on semiaquatic insects - intermediate hosts of digeneans. Trematodes are represented by three families Lecithodendriidae (12 species), Pleurogenidae (7) and Plagiorchiidae (5). Nematodes make up about a quarter of the helminth fauna of bats (10 species). Of these, eight species are geohelminths, parasites with direct life cycle. Two nematode species (Physaloptera clausa, Physocephalus sexalatus) have an indirect life cycle. Nematodes are represented by six families: Trichostrongylidae (4 species), Capillariidae (2), Onchocercidae, Physalopteridae, Spirocercidae and Rictulariidae (one species each). Cestodes are represented by three species of the same family Hymenolepididae. Tapeworms have an indirect life cycle; bats are infected with these parasites through feeding on land invertebrates - intermediate hosts of cestodes. The acanthocephalan Moniliformis moniliformis, lrv. was recorded in bats only once in the Zhigulevsky State Nature Reserve (in the Natterer's bat Myotis nattereri). This is the first finding of acanthocephalans in bats (Kirillov et al., 2017). The bat was infected with acanthocephalan apparently by eating beetles from the families Tenebrionidae and Scarabaenidae, which serve as intermediate hosts for this acanthocephalan (Khokhlova, 1986).
The overwhelming majority (33 species) of the identifying helminths parasitize bats in the small intestine. Only five parasite species have a different localization in the host body. Thus, the nematodes P. neopulchra and A. eubursata parasitize in the stomach of bats, L. filaria - in the body cavity, and Ph. sexalatus - in the walls of the small intestine.
Among bats, Nyctalus noctula has the most diverse helminth fauna (19 species). Slightly fewer species were found in Myotis brandtii, Pipistrellus nathusii (15 species each) and Vespertilio murinus (14). Thirteen species of helminths each were recorded for Myotis daubentonii and Eptesicus nilssoni; 12 - for Myotis dasycneme, 11 - for Nyctalus leisleri, and 10 species - for Myotis nattereri. Less diverse is the helminth fauna of Plecotus auritus (8 species), Myotis mystacinus (6), Nyctalus lasiopterus and Pipistrellus pipistrellus (5 species each), and Pipistrellus pygmaeus (4). Three species of helminths were each found in Eptesicus serotinus and Pipistrellus kuhlii.
No helminth species was found to parasitize all infected bat species in the Middle Volga region. The trematode P. koreanus has the widest range of hosts (10 species) among the bats inhabiting the Middle Volga region. Prosthodendrium chilostomum, P. neopulchra (9 host species each), L. linstowi and P. semisquamosus (8 hosts each) are also often found among chiropterans.
The host range of the trematodes P. heteroporus, L. rysavii and the nematode P. sexalatus, juv. includes 7 species of bats each; the cestode V. spasskii, trematodes P. vespertilionis, P. ascidia, P. lepidotus and L. skrjabini - 6 host species each; the trematode P. duboisi - 5 species. The trematodes P. elegans, P. mordovii, P. muelleri, P. ilei, P. hurkovaae (4 host species each), as well as the trematodes P. longiforme, G. oppositus and M. vespertilionis (3 species each) have a smaller host range. Only two host species each have the cestodes M. grisea, V. balsaci, the trematodes P. magnitestis, P. cryptholecithum, P. megacotyle, G. amphoraeformis, P. skrjabini, the nematodes P. bovieri and A. eubursata. The remaning six species (trematode P. joannae, nematodes M. skrjabini, M. spasskii, L. filaria, P. clausa, juv. and acanthocephalan M. moniliformis, lrv.) were found only in one host species each.
More than the half of the parasite species (20) recorded in bats in the Middle Volga region have a Palaearctic distribution. Ten species of helminths are common only in Europe. Five helminth species are classified as cosmopolitan. Three species of bat parasites have a Holarctic distribution.
Conclusion
Thus, according to literature records and our data, 38 species of parasites are currently known for chiropterans of the Middle Volga region including three cestodes, 24 trematodes, 10 nematodes and one acanthocephalan. The helminth fauna of chiropterans was studied for the first time within the National Park "Smolny". Data on the parasitic worms of bats in the Mordovia State Nature Reserve were significantly expanded. The trematode Prosthodendrium cryptholecithum and nematode larva Physaloptera clausa are recorded for the first time in the bats from Russia. Additionally, the trematodes Gyrabascus amphoraeformis and G. oppositus are found for the first time in the chiropterans of the Middle Volga region. New bat hosts were identified for P. cryptholecithum (Myotis brandtii), G. oppositus (Pipistrellus nathusii, Nyctalus noctula, N. leisleri), Ph. clausa, juv. (Pipistrellus nathusii).
The helminth fauna of all 16 species inhabiting the Middle Volga region was studied to varying degrees. From a geographical standpoint, the Middle Volga region remains poorly explored, since the helminth fauna in bats was studied only in two out of 11 administrative units of the region. Hence, the research on helminth fauna in bats needs to be continued in this area. Exploring parasites in new territories within the Middle Volga region will undoubtedly broaden the catalog of chiropteran parasites.
Aсknowledgements
This study was performed within the research topic № 1023062000002-6-1.6.20;1.6.19 "Land vertebrates of the Middle Volga region and adjacent territories and their parasitic worms:
ecological, faunal and biological aspects of the organization and functioning of communities against the background of natural and anthropogenic changes" of the Institute of Ecology of the Volga River Basin, a branch of the Samara Federal Research Center of the Russian Academy of Sciences.
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ОБЗОР ГЕЛЬМИНТОВ ЛЕТУЧИХ МЫШЕЙ (CHIROPTERA, VESPERTILIONIDAE) СРЕДНЕГО ПОВОЛЖЬЯ (ЕВРОПЕЙСКАЯ РОССИЯ)
®Н.Ю. Кириллова , А.А. Кириллов
Самарский федеральный исследовательский центр РАН, Инситут экологии Волжского бассейна РАН, Россия e-mail: parasitolog@yandex.ru
В работе мы обобщили современные сведения о видовом разнообразии паразитических гельминтов рукокрылых, населяющих Среднее Поволжье. В той или иной степени, гельминтологическому обследованию были подвергнуты все 16 видов рукокрылых, обитающих на исследуемой территории. По нашим и литературным данным, у рукокрылых зарегистрировано 38 видов паразитов: 3 ленточных червя, 24 сосальщика, 98 нематод и один скребень. Ядро гельминтофауны летучих мышей составляют хозяиноспецифичные виды, паразитирующие только на рукокрылых. Трематода Prosthodendrium cryptholecithum и нематода Physaloptera clausa, juv. указаны для рукокрылых России впервые. А трематоды Gyrabascus amphoraeformis и G. oppositus обнаружены впервые для рукокрылых Среднего Поволжья. Для трех видов гельминтов летучих мышей выявлены новые хозяева. Анализ паразитов рукокрылых показал, что наиболее разнообразна гельминтофауна Nyctalus noctule (19 видов гельминтов), Myotis brandtii, Pipistrellus nathusii (по 15 видов соответственно) и Vespertilio murinus (14 видов гельминтов). Самый широкий круг окончательных хозяев среди
рукокрылых Среднего Поволжья характерен для Plagiorchis koreanus, P. chilostomum и Pterothominx neopulchra (по 9 видов у каждого). Большинство гельминтов летучих мышей обладают высокой степенью хозяиноспецифичности. Из 38 видов паразитов, обнаруженных у представителей отряда рукокрылых, 34 вида гельминтов паразитируют только у летучих мышей. Лишь четыре вида гельминтов (Plagiorchis elegans, Ph. clausa, juv., Physocephalus sexalatus, juv., Moniliformis moniliformis, lrv.) проявляют широкую степень специфичности к хозяину, паразитируя на других позвоночных.
Ключевые слова: дигенетические сосальщики, летучие мыши, Мордовия, нематоды, паразитические черви, плоские черви, Самарская область, скребни
