Infection of Dice Snake, Natrix tessellata (Reptilia, Colubridae), with Eustrongylides excisus (Nematoda, Dioctophymatidae) in the Middle and Lower Dnipro River Basin

Keywords: eustrongylidosis, abundance, infection intensity, prevalence, Ukraine


Dice snakes can be a paratenic host for a stage IV of Eustrongylides excisus, Jagerskiold, 1909 larva due to specific diet of the snakes. The infection rate of E. excisus in Natrix tessellate (Laurenti, 1768) was studied in the basin of the middle and the lower Dnipro River in 2013–2017. We searched for nematodes in snakes from four sites: Prydniprovska Thermal Power Station, Majorova Balka, Zaporizhzhia; National Nature Park Velykyi Luh. The snakes from all studied areas had high prevalence of infection (more than 90 %). The lowest level of intensity (2.50 ± 0.60) and abundance (2.27 ± 0.58) were in ecosystems near Prydniprovska ТPP. There was no significant difference between infection parameters in snakes from other groups. Capsules with larva localized in the gastrointestinal tract, liver, muscles, and lung. The most infected was the gastrointestinal tract, statistical analysis showed significant differences with other organs. The lowest infection was found in the lung. Environmental pollution of the Dnipro River waters with pesticides and other pollutants accompanied by a climate change may influence on the E. excisus life cycle that needs additional studies.



Acipinar, H., Gaygusuz, O., Tarkan, A. S., Gursoy, C., Al, Z. 2006. Presence of an invasive fish species Carassius gibelio (Bloch, 1782) in the diet of the dice snake, Natrix tessellata (Laurenti, 1768). Journal of Fisheries and Aquatic Science, 1 (2), 213-217.

Bakiev, A., Kirillov, A., Mebert, K. 2011. Diet and parasitic helminths of dice snakes from the Volga Basin, Russia. Mertensiella, 18, 325-329.

Baranovski, B. A., Ivanko, I. A., Gasso, V. Y., Ponomarenko, O. L., Dubyna, D. V., Roshchyna, N. O., Karmyzova, L. O., Polevа, J. L., Nikolaieva, V. V. 2021. Biodiversity of the Regional Landscape Park Samara Plavni within the first large reservoir in Europe. Biosystems Diversity, 29 (2), 160-179.

Biserkov, V. 1996. New records of Nematodes and Acanthocephalans from snakes in Bulgaria. Comptes rendus de l'Academie Bulgare des Sciences, 49 (1), 76-78.

Bjelić-Čabrilo, O., Novakov, N., Ćirković, M., Kostić, D., Popović, E., Aleksić, N., Lujić, J. 2013. The first determination of Eustrongylides excisus Jägerskiöld, 1909 larvae (Nematoda: Dioctophymatidae) in the pike-perch Sander lucioperca in Vojvodina (Serbia). Helminthologia, 50 (4), 291-294.

Bulakhov, V. L., Gubkin, A. A., Ponomarenko, O. L., Pakhomov, O. Y. 2008. Biological Diversity of Ukraine. Dnipropetrovsk Region. Aves: Non-Passeriformes. Dnipropetrovsk University Press, Dnipropetrovsk [In Ukrainian].

Bulakhov, V.L., Gasso, V.Y., Pakhomov, O.Y., 2007. Biological Diversity of Ukraine. Dnipropetrovsk Region. Amphibians and Reptiles (Amphibia et Reptilia). Dnipropetrоvsk University Press, Dnipropetrovsk [In Ukrainian].

Bush, A. O., Lafferty K. D., Lotz J. M., Shostak. A W. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology, 83 (4), 575-583.

de Vasconcelos Melo, F. T., do Nascimento, L. D. C. S., Macedo, L. C., dos Santos, J. N., Kuzmin, Y. 2016. The morphology of free-living stages and immature parasites of Rhabdias paraensis (Nematoda: Rhabdiasidae), a parasite of Rhinella marina (Anura: Bufonidae) in Brazil. Acta Parasitologica, 61 (1), 42-51.

Dubinina, M. N. 1953. Dynamics of the parasite fauna of grass and dice snakes from the seaside area of the Volga delta. Studies of the Zoological Institute of Academy of Sciences USSR, 13, 171-190 [In Russian].

Düşen, S. 2012. First data on the helminth fauna of a locally distributed mountain frog, "Tavas frog" Rana tavasensis Baran & Atatür, 1986 (Anura: Ranidae), from the inner-west Anatolian region of Turkey. Turkish Journal of Zoology, 36 (4), 496-502.

Fagerholm, H. P. 1996. Nematode parasites of marine-and shore birds, and their role as pathogens. Bulletin of the Scandinavian Society for Parasitology, 6 (2), 16-30.

Gasso, V. Y. 2011. Grass snake populations' features of the forest biogeocoenoses in the Samara river area. Visnyk of Dnipropetrovsk University. Biology, Ecology, 19 (2), 136-142.

Gasso, V. Y., Hahut, A. N., Yermolenko, S. V., Hasso, I. A., Agca, C. A., Nedzvetsky, V. S., Sukharenko, E. V. 2020. Local industrial pollution induces astrocyte cytoskeleton rearrangement in the dice snake brain: GFAP as a biomarker. Biosystems Diversity, 28 (3), 250-256.

Göçmen, B., Çiçek, K., Yildiz, M. Z., Atatür, M. K., Dinçaslan, Y. E., Mebert, K. 2011. A preliminary study on the feeding biology of the dice snake, Natrix tessellata, in Turkey. Mertensiella, 18, 365-369.

Goncharov, S. L. 2017. Distribution of larvae of nematode Eustrongylides excisus Jägerskiöld, 1909 (Nematoda: Dioctophymatidae) in the body of predatory fish. Theoretical and Applied Veterinary Medicine, 5 (3), 5-9 [In Ukrainian].

Goncharov, S. L., Soroka, N. M., Pashkevich, I. Y., Dubovyi, A. I., Bondar, A. O. 2018. Infection of predatory fish with larvae of Eustrongylides excisus (Nematoda, Dioctophymatidae) in the delta of the Dnipro River and the Dnipro-Buh estuary in southern Ukraine. Vestnik Zoologii, 52 (2), 137-144.

Guardone, L., Ricci, E., Susini, F., Polsinelli, E., Guglielmone, G., Armani, A. 2021. First detection of Eustrongylides excisus (Nematoda: Dioctophymatidae) in big-scale sand smelt (Atherina boyeri) from the lake Massaciuccoli (Northwest Tuscany, Italy): implications for public health and seafood quality. Food Control, 120, 107517.

Gruschwitz, M., Lenz, S., Mebert, K., Lanka, V. 1999. Natrix tessellata (Laurenti, 1768) - Würfelnatter. In: Böhme, W., ed. Handbuch der Reptilien und Amphibien Europas, 3 (2), AULA-Verlag, Wiesbaden, 581-644.

Honcharov, S. L., Soroka, N. M., Halat, M. V., Dubovyi, A. I., Zhurenko, V. V., Halushko, I. A. 2022. Distribution of the nematodes of the genus Eustrongylides (Nematoda, Dioctophymatidae) in the world. Regulatory Mechanisms in Biosystems, 13 (1), 73-79.

Hutinec, B. J., Mebert, K. 2011. Ecological partitioning between dice snakes (Natrix tessellata) and grass snakes (Natrix natrix) in southern Croatia. Mertensiella, 18, 225-233.

Kirin, D. 2002. New records of the helminth fauna of grass snake, Natrix natrix L., 1758 and dice snake, Natrix tessellata Laurenti, 1768 (Colubridae: Reptilia) in South Bulgaria. Acta Zoologica Bulgarica, 54, 49-53.

Kornyushin, V. V., Smogorzhevskaya, L. A., Iskova, N. I. 2004. Circulation of helminthes in colonies of Pelicaniformes and Ciconiiformes in the south of Ukraine. Branta, 7, 241-277 [In Russian].

Kotenko, T. I., Shaitan, S. V., Starkov, V. G., Zinenko, O. I. 2011. The northern range limit of the dice snake (Natrix tessellata) in Ukraine and the Don River basin in Russia. Mertensiella, 18, 311-325.

Koyun, M., Birlik, S., Sümer, N., Yildirimhan, H. S. 2015. Helminth fauna of Eurasian marsh frog, Pelophylax ridibundus (Pallas, 1771) (Anura: Ranidae) from Bingöl, Eastern Anatolia, Turkey. Biharean Biologist, 9 (2), 128-132.

Kroik, A., Dorganova, L. 2016. Patterns of formation of hydrochemical of surface water in the area of the Dnieper thermal power station. Journal of Geology, Geography and Geoecology, 24 (2), 55-60.

Kurchenko, V. O., Sharamok, T. S. 2020. The hematological parameters of the Prussian carp (Carassius gibelio, (Bloch, 1782)) under the Zaporizhian (Dnipro) Reservoir conditions. Turkish Journal of Fisheries and Aquatic Sciences, 20 (11), 807-812.

Jablonski, D., Kautman, J. 2017. Melanism in Natrix tessellata (Serpentes: Colubridae) from Slovakia. Herpetology Notes, 10, 173-175.

Liu, Y., Mebert, K., Shi, L. 2011. Notes on distribution and morphology of the dice snake (Natrix tessellata) in China. Mertensiella, 18, 430-436.

Luiselli, L., Capizzi, D., Filippi, E., Anibaldi, C., Rugiero, L., Capula, M. 2007. Comparative diets of three populations of an aquatic snake (Natrix tessellata, Colubridae) from Mediterranean streams with different hydric regimes. Copeia, 2007 (2), 426-435.[426:CDOTPO]2.0.CO;2

Mihalca, A. 2011. Parasitism in the Dice Snake (Natrix tessellata): a Literature Review. Mertensiella, 18, 255-271.

Mihalca, A. D., Gherman, C., Ghira, I., Cozma, V. 2007. Helminth parasites of reptiles (Reptilia) in Romania. Parasitology Research, 101 (2), 491-492.

Nekrasova, O. D., Gavris, G. G., Kuybida, V. V. 2013. Changes in the northern border of the home range of the dice snake, Natrix tessellata (Reptilia, Colubridae), in the Dnipro basin (Ukraine). Vestnik zoologii, 47 (5), 67-71.

Rusconi, A., Prati, P., Bragoni, R., Castelli, M., Postiglione, U., Rigamonti, S., Sassera D., Olivieri, E. 2022. Occurrence of Eustrongylides excisus (Nematoda: Dioctophymatidae) in European Perch (Perca fluviatilis) and Great Cormorant (Phalacrocorax carbo) in Lake Annone, Northern Italy. The Journal of Parasitology, 108 (2), 209-216.

Saglam, N., Arikan, H. 2006. Endohelminth fauna of the marsh frog Rana ridibunda from Lake Hazar. Turkey. Diseases of Aquatic Organisms, 72 (3), 253-260.

Sargsyan, N., Arakelyan, M., Danielyan, F. 2016. Infestation of dice snake Natrix tessellata (Laurenti, 1768) by helminths in Armenia. Biological Journal of Armenia, 68 (1), 89-91.

Shakarboev, E. B., Kuchboev, A. E., Kamilova, Sh. I., Azimov, D. А. 1999. Helminthes of the tesselated shake Natrix tessellata in the fauna of Uzbekistan. Uzbekistan Biological Journal, 3, 48-51 [In Russian].

Sharpilo, V.P. 1976. Parasitic Worms of Reptilians of the Fauna of the USSR. Naukova Dumka, Kiev [In Russian].

Strilets, R. O. 2018. Regional Report on the State of Natural Environment in Dnipropetrovska Oblast for 2017. Department of Environmental and Natural Resources of the Dnipro Regional State Administration [In Ukrainian].

Šukalo, G., Đorđević, S., Gvozdenović, S., Simović, A., Anđelković, M., Blagojević, V., Tomović, L. 2014. Intra-and inter-population variability of food preferences of two Natrix species on the Balkan Peninsula. Herpetological Conservation and Biology, 9 (1), 123-136.

Weiperth, A., Potyó, I., Puky, M. 2014. Diet composition of the dice snake (Natrix tessellata Laurenti, 1768) in the Danube River catchment area. Acta Zoologica Bulgarica, 7, 51-56.

Yermolenko, S., Gasso, V., Hahut, A., Spirina, V. 2019. Helminth іnfracommunity of grass snake Natrix natrix (Reptilia, Colubridae) in differently transformed ecosystems. Conference: ComEc 2nd International Conference on Community Ecology (June 4-6, 2019, Bologna, Italy), 89.

Yesipova, N. B. 2013. The spread of parasitic nematodes in fish Eustrongylides excisus Zaporozhye (Dnipro) reservoir. Modern problems of theoretical and practical ichthyology. Materials of VI International Ichthyological Scientific-Practical Conference (October 9-11, 2013, Ternopil, Ukraine), 86-88 [In Russian].

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), 343-355.

Yossefi, M. R., Nikzad, R., Nikzad, M., Mousapour, A., Ramazanpour, S., Rahimi, M. T. 2014. High helmintic infection of the European grass snake, Natrix natrix and the dice snake, Natrix tessellata (Serpentes: Colubridae) from Iran. Asian Pacific Journal of Tropical Disease, 4, 263-267.

Zarubin, О. L., Zarubina, N. E., Gudkov, D. I., Volkova, Е. N., Beliaev, V. V., Kaglian, А. Е., Kostiuk, V. А., Maliuk, I. А., Nazarov, А. B., Belokon, А. S., Marenkov, О. N. 2013. Specific activity 137Cs at fishes of Ukraine. Current state. Nuclear Physics and Atomic Energy, 14 (2), 177-182 [In Ukrainian].

How to Cite
Yermolenko, S. V., Gasso, V. A., Hahut, A. M., & Spirina , V. A. (2022). Infection of Dice Snake, Natrix tessellata (Reptilia, Colubridae), with Eustrongylides excisus (Nematoda, Dioctophymatidae) in the Middle and Lower Dnipro River Basin. Zoodiversity, 56(4).