Comparative analysis of the helminth fauna in the dice snake Natrix tessellata (Reptilia, Colubridae) of different morphs

The purpose of the research is a comparative analysis of the helminth fauna in dice snakes of the grey and black morph inhabiting the Lower Volga region.

Materials and methods. A total of 32 grey and 41 black dice snakes Natrix tessellata from three habitats in the Astrakhan region, caught in 2004, 2005, and 2008, were examined using the method of complete helminthological dissection. The parasitological material was processed using standard methods. Statistical analysis was performed using the Shannon, Jaccard, Sorensen, Palia-Kovnatski dominance indices, and the Mann-Whitney criterion.

Results and discussion. A comparative analysis of the helminth fauna in dice snakes of the grey and black morph was conducted. A total of 21 species of parasitic worms were found in dice snakes examined: Cestoda – 1, Trematoda – 11, Nematoda – 8, Acanthocephala – 1. All these species of helminths were found in grey dice snakes. In black N. tessellata, 18 species of parasites were recorded. Paralepoderma cloacicola, Camallanus lacustris and Centrorhynchus aluconis were found only in grey morph of the dice snake. The analysis of the total helminth infection in dice snakes of different morphs did not reveal any significant differences, as well as pairwise comparison of the infection of reptiles by common parasite species. It was found that the structure and dominance of parasites in the helminth fauna of grey and black N. tessellata differs. Comparison of the helminth fauna of grey and black dice snakes in both qualitative and quantitative terms showed a high degree of similarity. Analysis of the helminth species diversity in dice snakes of different morphs revealed that the diversity of the parasite fauna of grey and black N. tessellata is approximately at the same level. Similar structure of helminths in dice snakes of different colors indicates the similarity of their topical and trophic niches. Relatively high infection of grey dice snakes with helminths is probably due to differences in physiology. It was established that both morphs of N. tessellata take part in the formation of the helminth fauna of the dice snake.

1. Anikanova V. S., Bugmyrin S. V., Ieshko E. P. Methods for collecting and studying helminths of small mammals. Petrozavodsk: monograph. Karelian Scientific Center of the Russian Academy of Sciences, 2007; 145. (in Russ.)

2. Bakanov A. I. Quantifying Dominance in Ecological Communities. Borok, 1987; 64. (in Russ.)

3. Bakiev A. G., Garanin V. I., Litvinov N. A., Pavlov A. V., Ratnikov V. Yu. Snakes of the Volga-Kama region. Samara: monograph. Samara Scientific Center of the Russian Academy of Sciences, 2004; 192. (in Russ.)

4. Bakiev A. G., Malenev A. L., Zaitseva O. V., Shurshina I. V. Snakes of the Samara region. Togliatti: Kassandra,2009; 170. (in Russ.)

5. Bykhovskaya-Pavlovskaya I. E. Fish parasites, study guide. Leningrad: Nauka, 1985; 123. (in Russ.)

6. Vershinin V. L. Morph Striata in members of the genus Rana (Amphibia, Anura) – reasons for adaptability to environmental changes. Zhurnal Obschej Biologii = Biology Bulletin Reviews. 2008; 69 (1): 65–71. (in Russ.)

7. Vershinin V. L., Vershinina S. D. Physiological similarity of morphs caused by homologous alleles in members of the family Ranidae. Uspekhi Sovremennoj Biologii = Biology Bulletin Reviews. 2013; 133 (5): 495–501. (in Russ.)

8. Darevsky I. S. Family Colubridae. Life of animals. V. 5. Moscow: Prosveshchenie, 1985; 280. (in Russ.)

9. Dobrinsky L. N., Malafeev Yu. M. Methodology for studying the intensity of carbon dioxide emission by small poikilothermic animals using an opticalacoustic gas analyzer. Ekologiya = Russian Journal of Ecology. 1974; 1: 73–78. (in Russ.)

10. Ishchenko V. G. Dynamic polymorphism of brown frogs of the USSR fauna. Moscow: Nauka, 1978; 148. (in Russ.)

11. Ishchenko V. G., Shchupak E. L. Ecological regulation of the genetic composition of the population of the long-legged wood Rаnа macrocnemis Boul. Ekologiya = Russian Journal of Ecology. 1975; 2: 54–64. (in Russ.)

12. Kalabekov A. L., Kibizova T. K. Analysis of infection of the long-legged wood (Rаna maсrоcnemis Bоu1, 1885) with trematode Нарlоmеtra brеviсаеса (Timon-David, 1962). Fauna and ecology of animals of the Caucasus. Ordzhonikidze: Publishing house of the North Ossetian State University, 1987; 9–14. (in Russ.)

13. Kireev V. A. Amphibians and reptiles. Elista: Kalmyk book publishing house, 1983; 112. (in Russ.)

14. Kirillov A. A., Kirillova N. Yu., Chikhlyaev I. V. Trematodes of Land Vertebrates from Middle Volga Region. Togliatti: Kassandra, 2012; 324. (in Russ.)

15. Kirillova N. Yu., Kirillov А. А. Reproductive structure of a hemipopulation of Cosmocerca ornata (Nematoda: Cosmocercidae) in marsh frogs Pelophylax ridibundus (Pallas, 1771) of several phenotypes. Sovremennaya Gerpetologiya = Current Studies in Herpetology. 2015; 15 (1/2): 55–62. (in Russ.)

16. Lada G. A. On genetic polymorphism of the marsh frog (Rana ridibunda) in the Central Black Earth Region. «Phenetics of natural populations»: proceeding of IV All-Union Conference. Moscow: Publishing House of the USSR Academy of Sciences, 1990; 151–152. (in Russ.)

17. Lebedinsky A. A. Helminth fauna of marsh frogs under anthropogenic impact and the relationship between invasion and their polymorphism. Animals in Natural Ecosystems. Nizhny Novgorod: Publishing house of Nizhny Novgorod Pedagogical University, 1994; 25–32. (in Russ.)

18. Magurran E. Ecological diversity and its measurement. Moscow: Mir, 1992; 181. (in Russ.)

19. Keys to parasites of freshwater fish of the USSR fauna. V. 3. Parasitic multicellular. Part 2 / edited by O. N. Bauer; Leningrad: Nauka,1987; 425. (in Russ.)

20. Petrochenko V. I. Acanthocephalans of domestic and wild animals. V. 2. Moscow: Publishing house of the USSR Academy of Sciences, 1958; 458. (in Russ.)

21. Skryabin K. I. Method of complete helminthological dissections of vertebrates, including humans. Moscow: Moscow State University Press, 1928; 45. (in Russ.)

22. Sudarikov V. E., Shigin A. A., Kurochkin Yu. V. Lomakin V. V., Stenko R. P., Yurlova N. I. Metacercariae of trematodes – parasites of freshwater aquatic organisms of Central Russia. V. 1. Moscow: Nauka, 2002; 296. (in Russ.)

23. Terentyev V. P. The nature of geographical variability of green frogs. Trudy Petergofkogo biologicheskogo instituta Leningradskogo gosudarstvennogo Universiteta = Proceedings of the Petergof Biological Institute of the Leningrad State University. 1962; 19: 98–121. (in Russ.)

24. Sharpilo V. P. Parasitic worms of reptiles of the USSR. Kiev: Naukova dumka, 1976; 287. (in Russ.)

25. Schwartz S. S., Ishchenko V. G. Dynamics of the genetic composition of populations of the moor frog. Byulleten' Moskovskogo Obshchestva Ispytatelei Prirody Otdel Biologicheskii = Bulletin of the Moscow Society of Naturalists. Biology Section. 1968; 73 (3): 127–134. (in Russ.)

26. Shchupak E. L. Inheritance of the dorsal stripe by individuals of the moor frog. Information materials of the Institute of Plant and Animal Ecology of the Ural Department of the Academy of Sciences of the USSR. Sverdlovsk: Ural Scientific Center of the Academy of Sciences of the USSR. 1977; 36–42. (in Russ.)

27. Anderson R. C. Nematode parasites of vertebrates: Their development and transmission. Wallingford, UK: CABI Publishing, 2000; 578.

28. Berger L., Smielowski J. Inheritance of vertebral stripe in Rana ridibunda Pall. (Amphibia, Ranidae). Amphibia-Reptilia. 1982; 3. 145–151.

29. Brannian R. E. Lungworms. Diseases of Amphibians and Reptiles. N. Y.: Plenum Press, 1984; 213.

30. Chu T. V. Studies on the life history of Rhabdias fuscovenosa var. catanensis (Rizzo, 1902). Journal of Parasitology. 1936; 22 (2): 140–160.

31. Gasc J. P., Cabela A., Crnobrnja-Isailović J. et al. Atlas of amphibians and reptiles in Europe. Collection Patrimoines Naturels 29. Paris: monograph. Societas Europaea Herpetologica, Muséum National d’Histoire Naturelle & Service du Patrimoine Naturel, 1997; 496.

32. Hoffman E. A., Blouin M. S. A review of color and pattern polymorphisms in anurans. Biological Journal of Linnean Society. 2000; 70 (4): 633–665. https://doi.org/10.1006/bijl.1999.0421

33. Ibrahim A. A. New records of the dice snake, Natrix tessellata, in the Suez Canal zone and Sinai. Amphibian and Reptile Conservation. 2012; 6 (2): 2–4.

34. Kirillov A. A., Kirillova N. Y., Bakiev A. G., Gorelov R. A. Ecological analysis of the helminth fauna in Natrix tessellata (Reptilia, Colubridae) from the Low Volga region (Russia). Inland Water Biology. 2023; 16 (2): 357–368. https://doi.org/10.1134/S1995082923020104

35. Mebert K. Geographic variation of morphological characters in the dice snake (Natrix tessellata). Mertensiella. 2011; 18. 11–19.

36. Mebert K., Masroor R., Chaudhry M. J. I. The dice snake, Natrix tessellata (Serpentes: Colubridae) in Pakistan: analysis of its range limited to few valleys in the Western Karakoram. Pakistan Journal of Zoology. 2013; 45 (2): 395–410.

37. Moriya K. Genetical studies of the pond frog, Rana nigromaculata. 1. Two types of Rana nigromaculata nigromaculata found in Takata district. Journal of Science of the Hiroshima University. Ser. B. 1952; 13 (19): 189–197.

38. Reshetnikov A. N., Sokolov S. G., Chikhlyaev I. V., Fayzulin A. I., Kirillov A. A., Kuzovenko A. E., Protasova E. N., Skomorokhov M. O. Direct and indirect interactions between an invasive alien fish (Perccottus glenii) and two native semi-aquatic snakes. Copeia. 2013; 1. 103–110.

39. Roepstorff A., Nansen P. Epidemiology, diagnosis, and control of helminth parasites of swine. Rome: FAO of the UN, 1998; 161.

40. Singh S. N. Studies on the Morphology and LifeHistory of Strongyloides mirzai n.sp. from Snakes in India. Journal of Helminthology. 1954; 28 (1–2): 25–34. https://doi.org/10.1017/s0022149x00032697

41. Sokolov S. G., Protasova E. N., Kholin S. K. Parasites of the introduced Amur sleeper, Perccottus glenii (Osteichthyes): Alpha-diversity of parasites and age of the host. Biology Bulletin. 2011; 38 (5): 500–508. https://doi.org/10.1134/S1062359011050141

42. Tuniev B., Tuniev S., Kirshney T., Mebert K. Notes om the Dice Snake (Natrix tessellata) from the Caucasian Isthmus. Mertensiella. 2011; 18. 343–356.

43. Yenmiş M., Bayrakcı Y., Ayaz D. Skin structure, coloration, and habitat utilization in typical and melanistic morphs of the grass snake (Natrix natrix). Science of Nature. 2022; 109. 22. https://doi. org/10.1007/s00114-022-01794-w