Parásitos nematodos de la rana de piscina (Pelophylax lessonae) en la cuenca del Río Volga

Parasitic nematodes of Pool Frog (Pelophylax lessonae) in the Volga Basin

Objetivo. Presentar una revisión moderna de la fauna de nematodos de la rana esculenta Pelophylax lessonae (Camerano, 1882) de las poblaciones de la cuenca del Río Volga Materiales y métodos. Este trabajo consolida los datos de diferentes trabajos helmintológicos de los últimos 80 años, respaldados por los resultados de nuestras propias investigaciones. Durante el período de 1936 a 2016 diferentes autores examinaron 1460 especímenes de rana esculenta, utilizando el método de autopsia helmintológica completa de 13 regiones de la cuenca del Río Volga. Resultados. En total se registraron 9 especies de nematodos. Nematodo Icosiella neglecta encontrado por primera vez en el huésped estudiado en el territorio de Rusia y la cuenca del Río Volga. Tres especies parecían estar más extendidas: Oswaldocruzia filiformis, Cosmocerca ornata e Icosiella neglecta. Para cada especie de helmintos se incluyó la siguiente información: posición sistemática, áreas de detección, localización, biología, lista de hospederos definitivos, nivel de especificidad del hospedero. Conclusiones. Los nematodos de la rana esculenta, excepto I. neglecta, pertenecen al grupo de helmintos transmitidos por el suelo (geohelmintos) y parasitan en estadios adultos. Algunas especies (O. filiformis, C. ornata, I. neglecta) están muy extendidas en el área de distribución del hospedador. Estos dos últimos son capaces de alcanzar altos índices de invasión y también de ser los parásitos subyacentes de la rana esculenta. Esto sucede debido a la especificidad del ciclo de vida de estas especies de nematodos y a la conexión a largo plazo del anfibio con el agua.

1. Cogalniceanu D, Szekely P, Samoila C, Iosif R, Tudor M, Plaiasu R, Stanescu F, Rozylowicz L. Diversity and distribution of amphibians in Romania. Zookeys. 2013; 296:35-57. https://doi.org/10.3897/zookeys.296.4872
2. Zeisset I, Hoogesteger T. A reassessment of the biogeographic range of northern clade pool frogs (Pelophylax lessonae). Herpetological J. 2018; 28(2):63-72. https://www.thebhs.org/publications/the-herpetological-journal/volume-28-number-2-april-2018/1801-02-a-reassessment-of-the-biogeographic-range-of-northern-clade-pool-frogs-i-pelophylax-lessonae-i
3. Dubey S, Leuenberger J, Perrin N. Multiple origins of invasive and ‘native’ water frogs (Pelophylax spp.) in Switzerland. Biological Journal of the Linnean Society. 2014; 112(3):442-449. https://doi.org/10.1111/bij.12283
4. Ratnikov VY, Blain HA. Holocene amphibians and reptiles from Voroncha (Belarus): Comparative osteology, paleopathology and paleobiogeography. Historical Biology. 2018; 30. https://doi.org/10.1080/08912963.2018.1506777
5. Hoogesteger T, Rahkonen J, Karhilahti A. Pool frog (Pelophylax lessonae) Camerano 1882 (Anura, Ranidae), an addition to the Finnish amphibian fauna. Memoranda Societatis pro Fauna et Flora Fennica. 2013; 89:25-31. URL Available in: https://journal.fi/msff/article/view/40883/10203
6. Bashinskiy IV, Osipov VV. Beavers in Russian forest-steppe - characteristics of ponds and their impact on fishes and amphibians. Russian J Theriology. 2016; 15(1):34-42. https://doi.org/10.15298/rusjtheriol.15.1.06
7. Hoffmann A, Plotner J, Pruvost NBM, Christiansen DG, Rothlisberger S, Choleva L, Mikulicek P, Cogalniceanu D, Sas-Kovacs I, Shabanov D, Morozov-Leonov S, Reyer HU. Genetic diversity and distribution patterns of diploid and polyploid hybrid water frog populations (Pelophylax esculentus complex) across Europe. Molecular Ecology. 2015; 24(17):4371-4391. https://doi.org/10.1111/mec.13325
8. Fayzulin AI, Zamaletdinov RI, Litvinchuk SN, Rosanov JM, Borkin LJ, Ermakov OA, et al. Species composition and distributional peculiarities of green frogs (Pelophylax esculentus complex) in Protected Areas of the Middle Volga Region (Russia). Nature Conservation Research. 2018; 3(Suppl. 1):1–16. http://dx.doi.org/10.24189/ncr.2018.056
9. Lukanov SP, Tzankov ND, Naumov BY. First documented records of Pelophylax lessonae (Camerano, 1882) (Amphibia: Ranidae) from Bulgaria. Acta Zool Bulgarica. 2017; 69(4):483-488. http://www.acta-zoologica-bulgarica.eu/downloads/acta-zoologica-bulgarica/2017/69-4-483-488.pdf
10. Canestrelli D, Nascetti G. Phylogeography of the pool frog Rana (Pelophylax) lessonae in the Italian peninsula and Sicily: multiple refugia, glacial expansions and nuclear-mitochondrial discordance. Journal of Biogeography. 2008; 35 (10):1923-1936. https://doi.org/10.1111/j.1365-2699.2008.01946.x
11. Korzikov VA, Aleksanov VV. On some factors driving the presence of amphibians in water bodies of the Upper Oka Basin (Central Russia). Nature Conservation Research. 2018; 3(Suppl. 1):110–119. http://dx.doi.org/10.24189/ncr.2018.059
12. Svitin R, Kuzmin Y. Oswaldocruzia duboisi (Nematoda, Molineidae): morphology, hosts and distribution in Ukraine. Vestnik Zoologii. 2012; 46(3): e1-e9. https://doi.org/10.2478/v10058-012-0017-x
13. Okulewicz A, Hildebrand J, Łysowski R, Buńkowska K, Perec-Matysiak A. Helminth communities of green and brown frogs from Poland (Lower Silesia Region). J Herpetology. 2014; 48(1):34-37. https://doi.org/10.1670/12-108
14. Vojtková L, Roca V. Parasites of the frogs and toads in Europe. Part II: Trematoda. Revista Española de Herpetología. 1994; 8:7–18.
15. Vojtková L, Roca V. Parasites of the frogs and toads in Europe. Part III: Nematoda, Cestoda, Acanthocephala, Hirudinea, Crustacea and Insecta. Revista Española de Herpetología. 1996; 10:13–27. URL Available in: https://www.herpetologica.es/publicaciones/revista-espanola-de-herpetologia/69-revista-espanola-de-herpetologia-10-1996
16. Popiołek M, Rozenblut-Kościsty B, Kot M, Nosal W, Ogielska M. Endoparasitic helminths of water frog complex in Poland: do differences exist between the parental species Pelophylax ridibundus and Pelophylax lessonae, and their natural hybrid Pelophylax esculentus? Helminthologia. 2011; 48(2):108–115. DOI: https://doi.org/10.2478/s11687-011-0020-8
17. Ruchin AB, Chikhlyaev IV, Lukijanov SV. Analysis of helminthofauna of Common spaedfoot Pelobates fuscus (Laurenti, 1768) and Moor frog Rana arvalis Nilsson, 1842 (Amphibia: Anura) at their joint habitation. Parazitologiia. 2009; 43(3):240–247. URL Available in: https://www.ncbi.nlm.nih.gov/pubmed/19637773
18. Ruchin AB, Kirillov AA, Chikhlyaev IV, Kirillova NY. Parasitic Worms of Land Vertebrates in Mordovia Reserve (Annotated List of Species). Moscow, Russia. 2016. URL Available in: https://zapoved-mordovia.ru/uploads/images/nauchnaia-rabota/izdania-zapovednika/124_Parazit_worms_MGPZ_2016.pdf
19. Chikhlyaev IV, Ruchin AB. The helminth fauna study of European common brown frog (Rana temporaria Linnaeus, 1758) in the Volga basin. Acta Parasitol. 2014; 59(3):459–471. DOI: http://dx.doi.org/10.2478/s11686-014-0268-5
20. Chikhlyaev IV, Ruchin AB, Fayzulin AI. The helminth fauna study of European common toad in the Volga basin. Nat Environ and Pollut Technol. 2016; 15(3):1103–1109. http://www.neptjournal.com/upload-images/NL-57-51-(49)D-574.pdf
21. Reshetnikov AN, Sokolov SG, Chikhlyaev IV, Fayzulin AI, Kirillov AA, Kuzovenko AE, et al. Direct and indirect interactions between an invasive alien fish (Perccottus glenii) and two native semi-aquatic snakes. Copeia. 2013; 1:103–110. https://doi.org/10.1643/CE-12-007
22. Chikhlyaev IV, Kirillov AA, Kirillova NY. Trematodes (Trematoda) of amphibians (Amphibia) of the Middle Volga region. 1. Orders Fasciolida, Hemiurida, Paramphistomida and Strigeida. Parazitol. 2012; 46(3):171–192. URL Available in: https://www.ncbi.nlm.nih.gov/pubmed/23082495
23. Chikhlyaev IV, Kirillov AA, Kirillova NY. Trematodes (Trematoda) of amphibians (Amphibia) of the Middle Volga region. 2. Order Plagiorchiida. Parazitol. 2012; 46(4):290–313. URL Available in: https://www.zin.ru/journals/parazitologiya/content/2012/prz_2012_4_6_Chikhlyaev.pdf
24. Ryzhikov KM, Sharpilov VP, Shevchenko NN. Helminths of Amphibian Fauna of the USSR. Nauka: Moscow, USSR; 1980. URL Available in: http://www.library.univ.kiev.ua/ukr/elcat/new/detail.php3?doc_id=1086877
25. Hodda M. Phylum Nematoda Cobb 1932. Animal Biodiversity: an Outline of Higher-Level Classification and Survey of Taxonomic Richness. Zootaxa. 2011; 3148: 63–95. URL Available in: https://www.mapress.com/zootaxa/2011/f/zt03148p095.pdf
26. Schaake M. Infectionsmodus und Infectionsweg der Rhabdias bufonis Schrank (Angiostomum nigrovenosum) und die Metamorphose des Genitalapparaten der Hermafroditischen Generation. Z. Parasitenk. 1931. 3(4):517-648. URL Available in: https://link.springer.com/article/10.1007%2FBF02146549
27. Hendrikx WML. Observations on the routes of infection of Oswaldocruzia filiformis (Nematoda: Trichostrongylidae) in amphibian. Z Parasitenkd. 1983; 69: 119-126. URL Available in: https://link.springer.com/article/10.1007/BF00934016
28. Durette-Desset MC, Batcharov A, Ben Slimane B, Chabaud AG. Some Oswaldocruzia (Nematoda: Trichostrongyloidea) parasites of Amphibia in Bulgaria. Redescription of Oswaldocruzia bialata (Molin, 1860). Helminthologia. 1993; 30:99–104.
29. Kirillova NY, Kirillov AA. Role of the Marsh frog tadpoles in the life cycle of Cosmocerca ornata (Nematoda: Cosmocercidae). Parasitology. 2015; 49(1):49–60. URL Available in: http://www.zin.ru/journals/parazitologiya/content/2015/prz_2015_1_5_Kirillova.pdf
30. Yumagulova GR. To the study of nematode Cosmocercoides skrjabini (Ivanitzky, 1940). Results of Biological Research of the Bashkir State University for 1998. Ufa: Russia; 1999.
31. Desportes C. Forcipomyia velox Winn et Sycorax silacea Curtis, vecteurs d’Icosiella neglecta (Diesing, 1850) filaire commune de la grenouille verte. Annales de Parasitologie Humaine et Comparee. 1942-1943; 19:53–68. URL Available in: https://www.parasite-journal.org/articles/parasite/pdf/1942/01/parasite1942-1943191p53.pdf
32. Chikhlyaev IV, Korzikov VA, Fayzulin AI. Materials for the helminth fauna of the Pool frog Pelophylax lessonae and the Common toad Bufo bufo (Amphibia, Anura) in Kaluga region. Bulletin of Samara Sci. Center of the RAS. 2016; 5(2):377–381. URL Available in: https://cyberleninka.ru/article/n/materialy-k-gelmintofaune-prudovoy-lyagushki-pelophylax-lessonae-i-seroy-zhaby-bufo-bufo-amphibia-anura-v-kaluzhskoy-oblasti
33. Kotova EN. Parasitic worms of fish and amphibians of the Klyazma river in the area of the Bolshevo Biological Station. Notes of the Bolshevo Biol Station. 1936; 9:139–140.
34. Kirillova YA, Egorov SV. The helminth fauna of anurans amphibians of the Ivanovo region. Editor: Bessonov, A.S. Theory and Practice to Combat Parasitic Diseases (Zoonoses). Issue 3. Moscow; Russia: 2002.
35. Borisova VI. Helminths of amphibians geographical distribution study. Parazitol. 1988; 22(6):471–475. URL Available in: https://www.zin.ru/journals/parazitologiya/content/1988/prz_1988_6_4_Borisova.pdf
36. Nosova KF. Helminth fauna of the Pool frog in Nizhny Novgorod region. Publishing House of NSPI; Nizhny Novgorod, USSR: 1993.
37. Kolodina AS, Pyatova MV, Ravkovskaya EA, Lada GA. To the question of nutrition and helminths of the Pool frog (Pelophylax lessonae) in the conditions of Tambov region. Bulletin of Tambov Univ. 2016; 21(5):1791–1796. DOI: http://dx.doi.org/10.20310 / 1810-0198-2016-21-5-1791-1796
38. Indiryakova TA, Romanova EM, Matveeva EA. Helminth fauna species diversity of amphibians in the Ulyanovsk region. Proceedings of OGAU. 2008; 1(17):172–176. URL Available in: https://cyberleninka.ru/article/n/vidovoe-raznoobrazie-gelmintofauny-amfibiy-na-territorii-ulyanovskoy-oblasti
39. Chikhlyaev IV. On the helminths of the Pool frog Rana lessonae Camerano, 1882 in Samara city. Mordovia State Bulletin. 2009; 1: 96–98. URL Available in: http://vestnik.mrsu.ru/content/pdf/09-1.pdf
40. Chikhlyaev IV. Materials on the helminth fauna of the Pool frog Pelophylax lessonae (Camerano, 1882) in Zhiguli Nature Reserve. Samarskaya Luka: Problems of Regional and Global Ecol. 2017; 26(4):244–248. URL Available in: https://cyberleninka.ru/article/n/materialy-k-gelmintofaune-prudovoy-lyagushki-pelophylaxlessonae-camerano-1882-v-zhigulevskom-zapovednike
41. Chikhlyaev IV, Ruchin AB, Fayzulin AI. Helminths of anurans amphibians (Anura, Amphibia) of the Mordovia Reserve. Proceedings of the Mordovia State Nature Reserve. 2015; 14:376–388. URL Available in: http://zapoved-mordovia.ru/biblio/Trudy_Mordovskogo_zapovednika_Vyp_14_2015.pdf
42. Smirnova MI, Gorshkov PK, Sizova VG. Helminth fauna of anurans amphibians in Tatarstan Republic. Institute of Biology of Academy of Sciences of the USSR; Kazan, USSR: 1987.
43. Bayanov MG. Helminths of amphibians in Bashkortostan. Editor: Bayanov M.G. Problems of Animal Ecology of Southern Ural. Issue. 5. Publishing House Bashkir University: Ufa, USSR; 1992. the Routes of Infecti