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Helminth Species and Infracommunities in Frogs Pelophylax ridibundus and P. esculentus (Amphibia: Ranidae) in Northern Ukraine

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Abstract

Purpose

The study aims to characterise and compare the helminth assemblages and helminth infracommunities in the marsh frog, Pelophylax ridibundus and the edible frog, P. esculentus collected in the northern part of Ukraine.

Methods

Occurrence and abundance of the helminths were analysed by calculating the prevalence, intensity, and mean abundance of infection; similarities between the infracommunities were estimated by the Bray–Curtis index and visualised using nMDS plots. Dissimilarities were estimated using the ANOSIM and SIMPER routines.

Results

In total, 27 helminth species were found in 143 frogs. Pelophylax ridibundus (n = 86) harboured 20 species of helminths, 24 species were found in P. esculentus (n = 57), and 17 species were shared by the two hosts. Oswaldocruzia bialata and larval Strigea sp. were absent in P. ridibundus, while they reached the prevalence of 30% and 10%, respectively, in P. esculentus. Cosmocerca ornata, Diplodiscus subclavatus, Opisthioglyphe ranae, and Codonocephalus urniger had significantly larger prevalence in P. ridibundus, whereas Haematoloechus asper was found to be more prevalent in P. esculentus. Acanthocephalus ranae, Icosiella neglecta, Haematoloechus variegatus, Pleurogenes claviger, Pleurogenoides medians, and Prosotocus confusus were equally common in both hosts. Helminth infracommunities in the two hosts had identical species richness (1–10 species, 4 on average); abundance was significantly higher in P. ridibundus.

Conclusions

Helminth assemblages of the two hosts in northern Ukraine are rather similar; however, small but significant differences were found in their species composition, parameters of infection in some species, and structure of helminth infracommunities.

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References

  1. Aho GM (1990) Helminth communities of amphibians and reptiles: comparative approaches to understanding patterns and processes. In: Esch GW, Bush AO, Aho GM (eds) Parasite communities: patterns and processes. Chapman and Hall, pp 157–196. https://doi.org/10.1007/978-94-009-0837-6_7

  2. Akulenko NM, Zhalai EI, Nekrasova OD (2012) Hybrid complex of green frogs—an accident, evolutionary reserve, or adaptation process with limited opportunities? In: Proceedings of the international conference "XXVI Liubishchevskiye Readings. Modern Problems of Evolution" (Russian Federation, Ulyanovsk, April 5–7, 2012), Ulyanovsk State Pedagogical University, pp 61–67 (in Russian)

  3. Baker MR (1987) Synopsis of the nematoda parasitic in amphibians and reptiles. Memorial University of Newfoundland, Occasional Papers in Biology

  4. Bannikov AG, Darevsky IS, Rustamov AK (1971) Amphibians and reptiles of the USSR. Izdatelistvo Mysl, Moscow

    Google Scholar 

  5. Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83(4):575–583. https://doi.org/10.2307/3284227

    Article  CAS  PubMed  Google Scholar 

  6. Chihlaev IV, Zamaletdinov RI, Fayzulin AI, Kuzovenko AE (2009) Trophic relations and fauna of helminths of Rana esculenta complex (Anura, Amphibia) of urbanized territories of Volga Basin. Pratsi Ukrainskogo Herpetologichnogo Tovarystva (Proc Ukr Herpetol Soc) 2:102–109 (in Russian)

    Google Scholar 

  7. Chikhlyaev I, Ruchin A (2014) The helminth fauna study of European common brown frog (Rana temporaria Linnaeus, 1758) in the Volga basin. Acta Parasitol 59(3):459–471. https://doi.org/10.2478/s11686-014-0268-5

    Article  PubMed  Google Scholar 

  8. Christiansen DG (2009) Gamete types, sex determination and stable equilibria of all-hybrid populations of diploid and triploid edible frogs (Pelophylax esculentus). BMC Evol Biol 9:135. https://doi.org/10.1186/1471-2148-9-135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. Plymouth, PRIMER-E

    Google Scholar 

  10. Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial (Plymouth routines in multivariate ecological research). PRIMER-E, Plymouth

    Google Scholar 

  11. Desportes C (1941) Nouvelles recherches sur la morphologie et sur l'évolution d'Icosiella neglecta (Diesing 1851), filaire commune de la grenouille verte. Annales de Parasitologie Humaine et Comparée 18(1–2–3):46–67. https://doi.org/10.1051/parasite/1941181046

    Article  Google Scholar 

  12. Desportes C (1942) Forcipomyia velox Winn et. Sycorax silacea Curtis, vecteurs d'Icosiella neglecta (Diesing) filaire commune de la grenouille verte. Annales de Parasitologie Humaine et Comparée 19(1–2–3):53–68. https://doi.org/10.1051/parasite/1942-1943191053

    Article  Google Scholar 

  13. Dubois A (1982) Klepton and synklepton: two new evolutionary systematics categories in zoology. Zoologische Jahrbücher. Abteilung für Systematik, Ökologie und Geographie. Jena 109:290–305

    Google Scholar 

  14. Durette-Desset MC, Batcharov G, Ben Slimane B, Chabaud AG (1993) Some Oswaldocruzia (Nematoda: Trichostrongyloidea) parasites of Amphibia in Bulgaria. Redescription of Oswaldocruzia bialata (Molin, 1860). Helminthologia 30:99–104

    Google Scholar 

  15. Frost DR (2019) Amphibian species of the world: an online reference. Version 6.0. American Museum of Natural History, New York. https://research.amnh.org/herpetology/amphibia/index.html. Accessed 24 June 2019

  16. Hamann MI, Kehr AI, González CE (2010) Helminth community structure of Scinax nasicus (Anura: Hylidae) from a South American subtropical area. Dis Aquat Org 93:71–82. https://doi.org/10.3354/dao02276

    Article  CAS  PubMed  Google Scholar 

  17. Hamann MI, Kehr AI, González CE (2012) Community structure of helminth parasites of Leptodactylus bufonius (Anura: Leptodactylidae) from northeastern Argentina. Zool Stud 51(8):1454–1463

    Google Scholar 

  18. Hamann MI, Kehr AI, González CE (2013) Helminth communities in the burrowing toad, Rhinella fernandezae, from Northeastern Argentina. Biologia 68(6):1155–1162. https://doi.org/10.2478/s11756-013-0272-5

    Article  Google Scholar 

  19. Hammer Ø (1999–2015) PAST, paleontological statistics, Version 3.10, Reference Manual. Natural History Museum, University of Oslo

  20. Herczeg D, Vörös J, Végvári Z, Kuzmin Y, Brooks DR (2016) Helminth parasites of the Pelophylax esculentus complex (Anura: Ranidae) in Hortobágy National Park (Hungary). Comp Parasitol 83(1):36–48. https://doi.org/10.1654/1525-2647-83.1.36

    Article  Google Scholar 

  21. Herczeg D, Vörös J, Christiansen DJ, Benovics M, Mikulíček P (2016) Taxonomic composition and ploidy level among European water frogs (Anura: Ranidae: Pelophylax) in eastern Hungary. J Zool Syst Evol Res 55(2):129–137. https://doi.org/10.1111/jzs.12158

    Article  Google Scholar 

  22. Hofmann A, Plötner J, Pruvost NBM, Christiansen DG, Röthlisberger S, Choleva L, Mikulíček P, Cogălniceanu D, Sas-Kovács I, Shabanov D, Morozov-Leonov S, Reyer H-U (2015) Genetic diversity and distribution patterns of diploid and polyploid hybrid water frog populations (Pelophylax esculentus complex) across Europe. Mol Ecol 24:4371–4391. https://doi.org/10.1111/mec.13325

    Article  Google Scholar 

  23. Holenweg AK, Reyer HU (2000) Hibernation behavior of Rana lessonae and R. esculenta in their natural habitat. Oecologia 123(1):41–47. https://doi.org/10.1007/s004420050987

    Article  PubMed  Google Scholar 

  24. Iskova NI, Sharpilo VP, Sharpilo LD, Tkach VV (1995) Catalogue of helminthes of Ukraine. Trematodes of Terrestrial Vertebrates, Kyiv (in Russian)

    Google Scholar 

  25. Kuzmin SL (2012) Amphibians of the former USSR. Tovarishchestvo Nauchnyh Izdaniy KMK, Moscow (in Russian)

    Google Scholar 

  26. Kuzmin Y, Khymyn M, Svitin R (2012) Parasitic nematodes and acanthocephalans of frogs (Rana arvalis, Pelophylax esculentus) from the territory of National Park “Prypiat-Stokhid”. Scientific Bulletin of the National Park “Prypiat-Stokhid” 2:17–23 (in Ukrainian)

  27. Lisitsyna OI (2019) Fauna of Ukraine, Acanthocephala, vol 31. Naukova Dumka, Kyiv

    Google Scholar 

  28. Maguza VS (1972) Helminths of amphibians of Polissia of Ukraine. Dissertation, Institute of Zoology, Kyiv (in Russian)

  29. Mazurmovich BN (1951) Parasitic worms of amphibians, their relationships with hosts and environment. Izdatelstvo Kievskogo Gosudarstvennogo Universiteta im. T. G. Shevchenko, Kyiv (in Russian)

    Google Scholar 

  30. Morozov-Leonov SYu, Mezhzherin SV, Nekrasova OD, Shabanov DA, Korshunov AV, Krutyak FF (2009) Inheritance of parental genomes by a hybrid form Ranaesculenta” (Amphibia, Ranidae). Russ J Genet 45(4):423–429. https://doi.org/10.1134/S1022795409040061

    Article  CAS  Google Scholar 

  31. Morozov-Leonov SYu (2019) Hemiclone diversity in the hybrid form Pelophylax esculentus-ridibundus (Amphibia, Ranidae) from the Prypyat, Dnestr and Southern Boug rivers basins. Cytol Genet 53(1):59–70. https://doi.org/10.3103/S0095452719010092

    Article  Google Scholar 

  32. Nekrasova OD (2002) Interspecific variability and colouring polymorphism of green frogs Rana esculenta complex (Amphibia, Ranidae) in hybrid populations. Vestnik Zoologii 36(4):47–54 (in Russian)

    Google Scholar 

  33. Nekrasova OD (2010) On the investigation of morphological peculiarities of green frogs of the Pelophylax esculentus complex (Amphibia) from urbanised territories based on the example of Kiev. In: Problems of study and protection of animal world in natural and anthropogenic ecosystems, proceedings of the international scientific conference devoted to the 50th Anniversary of the publication of regional report "Animal World of the Soviet Bukovyna" (Chernivtsi, November 13, 2009), DrukArt, Chernivtsi, pp 121–122 (in Russian)

  34. Nekrasova OD, Mezhzherin SV, Morozov-Leonov SYu (2004) Demographic structure of Rana esculenta (Amphibia, Ranidae) complex hybrid populations from the middle Dnieper basin. Vestnik Zoologii 38(6):47–56 (in Russian)

    Google Scholar 

  35. Nekrasova O, Mezhzherin S, Morozov-Leonov S (2005) Diagnostic traits in the morphology of green frogs (Rana esculenta complex) in the Middle Dnepr basin. In: Ananjeva N, Tsinenko O (eds) Proceedings of the 12th ordinary general meeting of the societas Europaea Herpetologica (12–16 August 2003), Saint-Petersburg, Russian Journal of Herpetology, vol 12(Suppl.), pp 77–79

  36. Nekrasova OD, Morozov-Leonov SYu (2001) Diagnostics of frogs of Rana esculenta complex (Amphibia, Ranidae) in hybrid populations in the environs of Dnieper. Vestnik Zoologii 35(5):45–50 (in Russian)

    Google Scholar 

  37. Niewiadomska K (2002) Family Diplostomidae Poirier, 1886. In: Gibson DI, Jones A, Bray RA (eds) Keys to the Trematoda, Volume 1. CAB International and the Natural History Museum, Wallingford, London, pp 167–196

  38. Okulewicz A, Hildebrand J, Łysowski R, Buńkowska K, Perec-Matysiak A (2014) Helminth communities of green and brown frogs from Poland (Lower Silesia region). J Herpetol 48(1):34–37. https://doi.org/10.1670/12-108

    Article  Google Scholar 

  39. Pisanets E (2007) Amphibians of Ukraine. Zoological Museum of the NMNH of NAS of Ukraine, Kyiv (in Russian)

    Google Scholar 

  40. Popiołek M, Rozenblut-Kościsty B, Kot M, Nosal W, Ogielska M (2011) 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 48(2):108–115. https://doi.org/10.2478/s11687-011-0020-8

    Article  Google Scholar 

  41. Reiczigel J, Abonyi-Tóth Z, Singer J (2008) An exact confidence set for two binomial proportions and exact unconditional confidence intervals for the difference and ratio of proportions. Comput Stat Data Anal 52:5046–5053. https://doi.org/10.1016/j.csda.2008.04.032

    Article  Google Scholar 

  42. Rezvantseva MV (2012) Comparative characteristic of helminth fauna of green frogs (Rana esculenta complex) in the east of Central Black Earth Region. Dissertation, A.N. Severtsov Institute of Ecology and Evolution, Moscow (in Russian)

  43. Rezvantseva MV, Lada GA, Aksyonov DS, Shabanov DA, Korshunov AV, Chikhlyaev IV, Borkin LJ, Litvinchuk SN, Rozanov JM (2010) Data on helminth fauna of green frogs (Rana esculenta complex) in the Kharkov Province. In: The theoretical and practical problems of parasitology, the materials of the international conference (November 30–December 3, 2010, Moscow), Moscow, pp 308–312 (in Russian)

  44. Rózsa L, Reiczigel J, Majoros G (2000) Quantifying parasites in samples of hosts. J Parasitol 86(2):228–232. https://doi.org/10.1645/0022-3395(2000)086[0228:QPISOH]2.0.CO;2

    Article  PubMed  Google Scholar 

  45. Ryzhikov KM, Sharpilo VP, Shevchenko NN (1980) Helminths of amphibians of the fauna of the USSR. Izdatelstvo "Nauka", Moscow (in Russian)

  46. Sharpilo VP (1976) Parasitic worms of reptiles of the fauna of the USSR. Naukova Dumka, Kyiv (in Russian)

    Google Scholar 

  47. Sharpilo VP, Iskova NI (1989) Fauna of Ukraine, Volume 34, Trematodes, Issue 3, Plagiorchiates (Plagiorchiata). Naukova Dumka, Kyiv (in Russian)

  48. Shimalov VV (2009) Helminth fauna of amphibians (Vertebrata: Amphibia) in the Republic of Belarus. Parazitologia 43(2):118–129 (in Russian)

    CAS  PubMed  Google Scholar 

  49. Spickett A, Junker K, Krasnov BR, Haukisalmi V, Matthee S (2017) Intra- and interspecific similarity in species composition of helminth communities in two closely-related rodents from South Africa. Parasitology 144(9):1211–1220. https://doi.org/10.1017/S003118201700049X

    Article  PubMed  Google Scholar 

  50. Svitin RS, Kuzmin YI (2012) Oswaldocruzia duboisi (Nematoda, Molineidae): morphology, hosts and distribution in Ukraine. Vestnik Zoologii 46(3):195–203

    Article  Google Scholar 

  51. Svitin RS (2016) Nematodes of the Genus Oswaldocruzia Travassos, 1917 of Western Palaearctic. Dissertation, Institute of Zoology, Kyiv (in Ukrainian)

Download references

Acknowledgements

The authors thank Dr. Mykhailo Khymyn for the organisation of fieldwork at the "Prypiat-Stokhid" National Nature Park. Advisory help of Dr. Vasyl Tkach (University of North Dakota, USA) and Dr. Eleonora Korol (National Museum of Natural History, Ukraine) in the identification of trematodes is sincerely appreciated.

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Correspondence to Yuriy Kuzmin.

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Kuzmin, Y., Dmytrieva, I., Marushchak, O. et al. Helminth Species and Infracommunities in Frogs Pelophylax ridibundus and P. esculentus (Amphibia: Ranidae) in Northern Ukraine. Acta Parasit. 65, 341–353 (2020). https://doi.org/10.2478/s11686-019-00164-3

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