Article

Alexander А. Kirillov, PhD, Senior Researcher of the Laboratory of Population Ecology, Samara Federal Research Scientific Center of RAS, Institute of Ecology of Volga River Basin of RAS (445003, Russia, Samara Region, Togliatti, Komzina Street, 10); iD ORCID: https://orcid.org/0000-0002-4374-8858; e-mail: parasitolog@yandex.ru
Nadezhda Yu. Kirillova, PhD, Senior Researcher of the Laboratory of Population Ecology, Samara Federal Research Scientific Center of RAS, Institute of Ecology of Volga River Basin of RAS (445003, Russia, Samara Region, Togliatti, Komzina Street, 10); iD ORCID: https://orcid.org/0000-0002-4585-8970; e-mail: parasitolog@yandex.ru

Kirillov A.A., Kirillova N.Yu. 2021. Helminth fauna of reptiles in the National Park «Smolny», Russia. Nature Conservation Research 6(3): 9–22. https://dx.doi.org/10.24189/ncr.2021.034

Electronic Supplement. Stations of the research on reptile helminths in the National Park «Smolny», Russia (Link).

Reptiles are a common component of natural biological communities. They serve as the final and paratenic hosts of helminths and play an important role in the transmission of parasites. There are very few helminthological studies covering all species of reptiles from the same locality. This paper was aimed to study the species diversity of reptile helminths in the National Park «Smolny» (Russia). In 2018‒2020 we studied the helminth fauna of five reptile species by the method of complete helminthological dissection in 19 sites of the National Park «Smolny». A total of 27 species of parasites were noted in the studied species of snakes and lizards, including 14 trematodes, two cestodes and ten nematodes. We found the richest helminth fauna in Natrix natrix (17 species) and Lacerta agilis (11). The helminth fauna was less rich in Vipera berus (eight species) and Anguis fragilis (four species). We found only two species of helminths in Zootoca vivipara. Most of the parasites (16 species) are distributed through the Palaearctic. We found one species, the nematode Oswaldocruzia filiformis, in all five studied reptile species in the National Park «Smolny». The most widespread parasite species in reptiles was the nematode Rhabdias fuscovenosa, found in 12 out of 19 studied localities in the National Park «Smolny». We conducted a comparative analysis of the helminth fauna of reptiles in the National Park «Smolny» and reptiles from other areas of the Middle Volga Region, namely Mordovia State Nature Reserve, Samara Region and the National Park «Samarskaya Luka». It was found that the parasite composition of Anguis fragilis has a maximal similarity with the ones in other regions. The helminth fauna of Natrix natrix and Zootoca vivipara in the National Park «Smolny» is less similar to other compared areas of the Middle Volga Region. The least similarity of the helminth fauna with other studied regions was found for Vipera berus and Lacerta agilis. The similarity of the helminth fauna of certain reptile species from different areas of the Middle Volga Region is caused by the specificity of helminths, as well as the geographical proximity of the studied localities and the broad distribution of parasite species of reptiles. The nematode Agamospirura minuta, juv. in Natrix natrix, as well as in Vipera berus and Lacerta agilis were found for the first time in Russia, while the trematode Pleurogenoides medians was found for the first time in such a host as Lacerta agilis. We found for the first time the nematode larvae of Physocephalus sexalatus and Physaloptera clausa in Vipera berus in Russia. We revealed that Vipera berus and Lacerta agilis are new hosts for Physaloptera clausa, juv. and Oxysomatium brevicaudatum, respectively. We noted the cestode Spirometra erinaceieuropaei, plc. in reptiles (namely Natrix natrix) from the Middle Volga region for the first time. Three parasite species (cestode Spirometra erinaceieuropaei, trematode Alaria alata and nematode Physocephalus sexalatus) found in reptiles of the National Park «Smolny», have medical and veterinary value as causative agents of potential hazardous helminthiases.

cestodes, lizards, Middle Volga Region, nematodes, new host, parasites, snakes, trematodes

Received: 04.03.2021. Revised: 01.05.2021. Accepted: 18.05.2021.

Anikanova V.S., Bugmyrin S.V., Ieshko E.P. 2007. Methods of the collection and studies of helminthes of small mammals. Petrozavodsk: Karelian Research Centre of RAS. 145 p. [In Russian]
Bakanov A.I. 1987. Quantitative estimation of dominance in ecological communities. Borok. 64 p. The manuscript is deposited into VINITI on 08.12.1987, №8593-В87. [In Russian]
Bakiev A.G. 2007. Snakes of the Volga River Basin as nutrition objects for vertebrates. Current Studies in Herpetology 7(1/2): 124–132. [In Russian]
Bakiev A., Kirillov A., Kirillova N., Ruchin A., Klenina A., Gorelov R., Kostina N. 2020. Occurrence of the reptiles in the Volga River basin (Russia). Biodiversity Data Journal 8: e58033. DOI: 10.3897/BDJ.8.e58033
Ben Slimane B., Durette-Desset M.C., Chabaud A.G. 1993. Oswaldocruzia (Trichostrongyloidea) Parasites d'amphibiens des collections du Muséum de Paris. Annales De Parasitologie Humaine et Comparée 2: 88–100. DOI: 10.1051/parasite/199368288
Ben Slimane B., Lluch J., Durette-Desset M.C. 1995. Two new species of the genus Oswaldocruzia Travassos, 1917 (Nematode: Trichostrongylina: Molineidae) parasitizing Spanish amphibians. Research and Review in Parasitology 55(4): 209–215.
Ben Slimane B., Chabaud A.G., Durette-Desset M.C. 1996. Les Nématodes Trichostrongylina parasites d'Amphibiens et de Reptiles: problémes taxonomiques, phylétiques et biogéographiques. Systematic Parasitology 35(3): 179–206. DOI: 10.1007/BF00009639
Birlik S., Yildirimhan H.S., Ilgas Ç., Kumlutaş Y. 2018. Helminth fauna of spiny tailed lizard, Darevskia rudis (Bedriaga, 1886) (Sauria: Lacertidae) from Turkey. Helminthologia 55(1): 45–51. DOI: 10.1515/helm-2017-0057
Borkovcová M., Kopriva J. 2005. Parasitic helminths of reptiles (Reptilia) in South Moravia (Czech Republic). Parasitology Research 95(1): 77–78. DOI: 10.1007/s00436-004-1258-6
Bray R.A., Gibson D.I., Jones A. (Eds.). 2008. Keys to the Trematoda. Vol. 3. London: CAB International and Natural History Museum. 848 p.
Bykhovskaya-Pavlovskaya I.E. 1985. Parasites of fish, a study guide. Leningrad: Nauka. 123 p. [In Russian]
Chikhlyaev I.V., Kirillov A.A., Kirillova N.Yu. 2012. Trematodes (Trematoda) of amphibians from the Middle Volga Region. Report 2. Order Plagiorchiida. Parazitologiya 46(4): 290–313. [In Russian]
Chikhlyaev I.V., Ruchin A.B. 2014. The helminth fauna study of European common brown frog (Rana temporaria Linnaeus, 1758) in the Volga basin. Acta Parasitologica 59(3): 459‒471. DOI: 10.2478/s11686-014-0268-5
Chikhlyaev I.V., Ruchin A.B., Fayzulin A.I. 2016. The helminth fauna study of European common toad in the Volga Basin. Nature, Environment and Pollution Technology 15(3): 1103‒1109.
Durette-Desset M.C., Batcharov A., Ben Slimane B., Chabaud A.G. 1993. Some Oswaldocruzia (Nematoda: Trichostorngyloidea) parasites of Amphibia in Bulgaria. Redescription of Oswaldocruzia bialata (Molin, 1860). Helminthologia 30(1/2): 99–104.
Duscher G.G., Leschnik M., Fuehrer H.-P., Joachim A. 2014. Wildlife reservoirs for vector-borne canine, feline and zoonotic infections in Austria. International Journal for Parasitology: Parasites and Wildlife 4(1): 88–96. DOI: 10.1016/j.ijppaw.2014.12.001
Galdón M.A., Roca V., Barbosa D., Carretero M.A. 2006. Intestinal helminth communities of Podarcis bocagei and Podarcis carbonelli (Sauria: Lacertidae) in NW Portugal. Helminthologia 43(1): 37–41. DOI: 10.2478/s11687-006-0008-y
Grishutkin G.F., Lapshin A.S., Spiridonov S.N., Artaev O.N., Ruchin A.B., Kuznetsov V.A., Andreychev A.V. 2013. Vertebrates of the National Park «Smolny». Moscow. 55 p. (Flora and fauna of national parks. Vol. 9) [In Russian]
Halajian A., Bursey C.R., Goldberg S.R., Gol S.M.A. 2013. Helminth parasites of the European glass lizard, Pseudopus apodus (Squamata: Anguidae), and European grass snake, Natrix natrix (Serpentes: Colubridae), from Iran. Comparative Parasitology 80(1): 151–156. DOI: 10.1654/4588.1
Hammer Ø., Harper D.A.T., Ryan P.D. 2001. PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4(1): 9.
Kirillov A.A. 2000. Helminth fauna of reptiles of the Samara Region. Proceedings of Samara Scientific Centre of RAS 2(2): 324–329. [In Russian]
Kirillov A.A. 2012. Helminth fauna of reptiles of the Samara Region. Report 3. Common European Vipera berus (Linnaeus) and steppe V. renardi (Christoph) vipers. Samarskaya Luka: problems of regional and global ecology 21(4): 152‒156. [In Russian]
Kirillov A.A., Bakiev A.G. 2003. Study of helminths of vipers (Viperidae) in the Middle Volga Region. Samarskaya Luka: problems of regional and global ecology 13(13): 331–336. [In Russian]
Kirillov A.A., Kirillova N.Yu. 2011. Trematodes (Trematoda) of reptiles of the Middle Volga Region. Proceedings of Samara Scientific Centre of RAS 13(5): 139–147. [In Russian]
Kirillov A.A., Kirillova N.Yu. 2018. Overview of helminths in reptiles of the National Park «Samarskaya Luka» (Russia). Nature Conservation Research 3(Suppl.1): 73–82. DOI: 10.24189/ncr.2018.049 [In Russian]
Kirillov A.A., Kirillova N.Yu. 2019. Comparative analysis of the helminth fauna of Natrix natrix and Natrix tessellata (Reptilia, Colubridae) in the Samarskaya Luka National Park (Russia). Nature Conservation Research 4(4): 12–25. DOI: 10.24189/ncr.2019.059 [In Russian]
Kirillov A.A., Ruchin A.B., Fayzulin A.I., Chikhlyaev I.V. 2015. Helminths of reptiles in the Republic of Mordovia: preliminary data. Proceedings of the Mordovia State Nature Reserve 14: 243‒255. [In Russian]
Kirillov A.A., Kirillova N.Yu., Ruchin A.B. 2019. Overview of the Helminth Fauna of Slow Worms of Genus Anguis (Reptilia, Anguidae) in the Western Palearctic. Entomology and Applied Science Letters 6(1): 51‒65.
Kirillova N.Yu., Kirillov A.A. 2019. Wild vertebrates in the Midlle Volga Region as paratenic hosts of Physocephalus sexalatus (Nematoda, Spirocercidae). In: Ecological collection 7. Proceedings of Young Researchers. Togliatti: Institute of Ecology of Volga River Basin of RAS, «Anna». P. 218‒219. [In Russian]
Kirillova N.Yu., Kirillov A.A. 2020. Morphological variability of Oswaldocruzia filiformis (Nematoda: Molineidae) in reptiles inhabiting the protected areas of the Republic of Mordovia (Russia). IOP Conference Series: Earth and Environmental Science 607: 012007. DOI: 10.1088/1755-1315/607/1/012007
Kirillova N.Yu., Kirillov A.A., Shchenkov S.V., Chikhlyaev I.V. 2020. Oswaldocruzia filiformis sensu lato (Nematoda: Molineidae) from amphibians and reptiles in European Russia: morphological and molecular data. Nature Conservation Research 5(Suppl.2): 41–56. DOI: 10.24189/ncr.2020.041
Kirin D. 2002. New records of the Helminth fauna from grass snake, Natrix natrix L., 1758 and dice snake, Natrix tessellata Laurenti, 1768 (Colubridae: Reptilia) in South Bulgaria. Acta Zoologica Bulgarica 54: 49–53.
Kuzmin S.L., Semenov D.V. 2006. Synopsis of the fauna of amphibians and reptiles in Russia. Moscow: KMK Scientific Press Ltd. 139 p. [In Russian]
Kuzmin Y.I., Sharpilo V.P. 2000. On the paratenic parasitism by nematodes from the family Rhabdiasidae: parasites of anguid lizards (Anguidae). Vestnik Zoologii 34: 99–101. [In Russian]
Magurran A.E. 2004. Measuring Biological diversity. Oxford: Blackwell Publishing. 256 p.
Mihalca A.D., Gherman C., Ghira I., Cozma V. 2007. Helminth parasites of reptiles (Reptilia) in Romania. Parasitology Research 101(2): 491–492. DOI: 10.1007/s00436-007-0486-y
Möhl K., Grosse K., Hamedy A., Wüste T., Kabelitz P., Lücker E. 2009. Biology of Alaria spp. and human exposition risk to Alaria mesocercariae – a review. Parasitology Research 105(1): 1–15. DOI: 10.1007/s00436-009-1444-7
Murvanidze L., Lomidze Ts., Nikolaishvili K., Jankarashvili E. 2008. The annotated list of reptile helminthes of Georgia. Proceedings of the Institute of Zoology 23: 54–61.
Olson P.D., Cribb T.H., Tkach V.V., Bray R.A., Littlewood D.T.J. 2003. Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology 33(7): 733–755. DOI: 10.1016/S0020-7519(03)00049-3
Roca V., Belliure J., Santos X., Pausas J.G. 2020. New reptile hosts for helminth parasites in a mediterranean region. Journal of Herpetology 54(2): 268–271. DOI: 10.1670/18-133
Ruchin A.B., Kirillov A.A. 2012. Helminths of Natrix natrix L. in Mordovia. Biological Sciences of Kazakhstan 4: 344–348.
Ruchin A.B., Kirillov A.A., Chikhlyaev I.V., Kirillova N.Yu. 2016. Parasitic worms of land vertebrates of Mordovia State Nature Reserve. Moscow: Committee of RAS for the conservation of biological diversity. 72 p. (Flora and fauna of Nature Reserves. Vol. 124) [Russian]
Ryzhikov K.M. 1952. To the reservoir parasitism of Physocephalus sexalatus (Molin, 1860) – the nematode of pigs. Proceedings of the Helminthological Laboratory of AS USSR 6: 139–141. [In Russian]
Santos X., Martínez-Freiría F., Pleguezuelos J.M., Roca V. 2006. First helminthological data on Iberian vipers: Helminth communities and host-parasite relationships. Acta Parasitologica 51(2): 130–135. DOI: 10.2478/s11686-006-0020-x
Schmidt V., Mock R., Burgkhardt E., Junghanns A., Ortlieb F., Szabo I., Marschang R., Blindow I., Krautwald-Junghanns M.E. 2014. Cloacal aerobic bacterial flora and absence of viruses in free-living slow worms (Anguis fragilis), grass snakes (Natrix natrix) and European adders (Vipera berus) from Germany. Ecohealth 11(4): 571–580. DOI: 10.1007/s10393-014-0947-6
Sharpilo V.P. 1976. Parasitic worms of reptiles of the fauna of USSR. Kiev: Naukova Dumka. 286 p. [In Russian]
Sharpilo V.P., Biserkov V.A., Kostadinova J., Behnke M., Kuzmin Y.I. 2001. Helminths of the sand lizard, Lacerta agilis (Reptilia, Lacertidae), in the Palaearctic: faunal diversity and spatial patterns of variation in the composition and structure of component communities. Parasitology 123(4): 389–400. DOI: 10.1017/s0031182001008587
Shimalov V.V. 2010. Helminthofauna of reptiles in the Republic of Belarus. Parazitologiya 44(1): 22‒29. [In Russian]
Svitin R. 2015. New data on the morphology and distribution of Oswaldocruzia skrjabini (Nematoda, Molineidae). Vestnik Zoologii 46(3): 195–203. DOI: 10.1515/vzoo-2015-0052
Svitin R. 2017. Two new species of Oswaldocruzia (Nematoda, Molineidae) parasitising lizards in Ukraine. Zootaxa 4263(2): 358–368. DOI: 10.11646/zootaxa.4263.2.9
Tkach V.V., Pawlowski J., Mariaux J., Swiderski Z. 2001. Molecular phylogeny of the suborder Plagiorchiata and its position in the system of Digenea. In: D.T.J. Littlewood, R.A. Bray (Eds.): Interrelations of the Platyhelminthes. London: Taylor & Francis. P. 186–193.
Yildirimhan H.S., Bursey C.R., Goldberg S.R. 2007. Helminth parasites of the grass snake, Natrix natrix, and the dice snake, Natrix tessellata (Serpentes: Colubridae), from Turkey. Comparative Parasitology 74(2): 343–354. DOI: 10.1654/4285.1
Yildirimhan H.S., Karaman D., Bursey C.R. 2020. Helminth Fauna of the European green lizard, Lacerta viridis (Laurenti, 1768), from Bursa, Turkey. Comparative Parasitology 87(1): 56–67. DOI: 10.1654/1525-2647-87.1.56
Zając M., Wasyl D., Różycki M., Bilska-Zając E., Fafiński Z., Iwaniak W., Krajewska M., Hoszowski A., Konieczna O., Fafińska P., Szulowski K. 2016. Free-living snakes as a source and possible vector of Salmonella spp. and parasites. European Journal of Wildlife Research 62(2): 161–166. DOI: 10.1007/s10344-016-0988-y