Article

Article name ECOLOGICAL ANALYSIS OF THE HELMINTH FAUNA IN BUFO BUFO (AMPHIBIA: ANURA) FROM VARIOUS HABITATS
Authors

Igor V. Chikhlyaev, Senior Researcher of the Laboratory of Populational Ecology, Samara Federal Research Scientific Center of RAS, Institute of Ecology of Volga River Basin of RAS (445003, Russia, Samara region, Togliatti, Komzina str., 10); e-mail: diplodiscus@mail.ru
Alexander B. Ruchin, Dr. Sc., Associate Professor, Director of the Joint Directorate of the Mordovia State Nature Reserve and National Park «Smolny» (430005, Russia, Republic of Mordovia, Saransk, Krasnaya Street, 30); e-mail: ruchin.alexander@gmail.com
Alexander A. Kirillov, Senior Researcher of the Laboratory of Populational Ecology, Samara Federal Research Scientific Center of RAS, Institute of Ecology of Volga River Basin of RAS (445003, Russia, Samara region, Togliatti, Komzina str., 10); e-mail: parasitolog@yandex.ru

Reference to article

Chikhlyaev I.V., Ruchin A.B., Kirillov A.A. 2020. Ecological analysis of the helminth fauna in Bufo bufo (Amphibia: Anura) from various habitats. Nature Conservation Research 5(Suppl.2): 1–10. https://dx.doi.org/10.24189/ncr.2020.026

Section Research articles
DOI https://dx.doi.org/10.24189/ncr.2020.026
Abstract

In this study is made an ecological analysis of the species composition, structure of the helminth community and the invasion degree of Bufo bufo in different habitats in the National Park «Smolny» (Republic of Mordovia, Russia). In 2018–2019, they were collected in five biotopes with different spawning water bodies. Nine helminth species were found, including five Trematoda species and four Chromadorea (Nematoda) species. There are two groups of species. The first of them develops on terrestrial nematodes Rhabdias bufonis, Oswaldocruzia filiformis, Oxysomatium brevicaudatum, rather common, regardless of the habitat, with a high degree of invasion and dominating in the helminth community. The species of the second group develop in aquatic nematode Cosmocerca ornata, as well as trematodes which are rarer, locally and with a low infection rate. They are typical parasites of green frogs (genus Pelophylax). The diversity of helminthes and the structure of their component community depend on the type, nature of the spawning water body and the presence of green frogs. Individuals of B. bufo, spawning in stagnant water bodies where green frogs live, have a more diverse helminth species composition, because there are helminths of the second group, whose development is related to the aquatic environment. The structure of their community is more complex. Bufo bufo, when using flowing water bodies without green frogs for spawning, has a depleted helminth composition and a simplified structure of their community. The obtained results have demonstrated the influence of one allotopic amphibian species on the formation of helminth community of another species under conditions of temporary syntopic occurrence.

Keywords

European common toad, helminth community, National Park «Smolny», nematodes, parasites, spawning water body, syntopic occurrence, trematodes

Artice information

Received: 12.04.2020. Revised: 14.05.2020. Accepted: 16.05.2020.

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References

Aisien M.S.O., Uwagbae M., Edo-Taiwo O., Imasuen A.A., Ovwah E. 2015. Pattern of parasitic infections in anurans from a mangrove community of the Niger Delta, Nigeria. Zoologist 13: 50–55.
Aisien M.S.O., Omereji A.B., Ugbomeh A.P. 2017. Anuran parasites from three biotopes in Rivers State, Nigeria. Nigerian Journal of Parasitology 38(1): 128–135. DOI: 10.4314/njpar.v38i1.24
Altman I. 2010. Trematode parasites of the mudsnail Ilyanassa obsoleta: an analysis of parasite communities at different scales. PhD Thesis. Durham: University of New Hampshire. 151 p.
Askenderov A.D., Mazanaeva L.F., Mikhaylov R.A., Fayzulin A.I. 2018. Spawning water bodies and their role in conservation of rare amphibian species in the foothills of the Republic of Dagestan (Russia). Nature Conservation Research 3(Suppl.1): 83–97. DOI: 10.24189/ncr.2018.057 [In Russian]
Bókony V., Üveges B., Ujhegyi N., Verebélyi V., Nemesházi E., Csíkvári O., Hettyey A. 2018. Endocrine disruptors in breeding ponds and reproductive health of toads in agricultural, urban and natural landscapes. Science of the Total Environment 634: 1335–1345. DOI: 10.1016/j.scitotenv.2018.03.363
Burakova A.V., Baytimirova E.A. 2017. The species composition of parasites of Bufo bufo (Amphibia: Bufonidae) in the surrounding area of Visimsky State Nature Biosphere Reserve. Russian Journal of Parasitology 42(4): 320–324. [In Russian]
Burakova А.V., Vershinin V.L. 2016. Analysis of Parasitofauna in syntopically cohabitating representatives of Anura. Biological Communications 3(3): 31–36. DOI: 10.21638/11701/spbu03.2016.306 [In Russian]
Byhovskaya-Pavlovskaya I.Е. 1985. Parasites of fishes, a study guide. Leningrad: Nauka. 123 p. [In Russian]
Čađenović N., Stamenković S., Bjelić-Čabrilo O., Kralj S. 2018. On the diet of recent metamorphs and adults of the common toad, Bufo bufo (Linnaeus, 1758) (Anura: Bufonidae). Herpetozoa 30(3/4): 139–146.
Čavlović K., Buj I., Karaica D., Jelić D., Choleva L. 2018. Composition and age structure of the Pelophylax esculentus complex (Anura; Ranidae) population in inland Croatia. Salamandra 54(1): 11–20.
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. Korzikov V.A., Fayzulin A.I. 2016a. Materials for the helminth fauna of Pool frog, Pelophylax lessonae and European common toad, Bufo bufo (Amphibia, Anura) in the Kaluga region. Proceedings of Samara Scientific Centre RAS 18(5–2): 377–381. [In Russian]
Chikhlyaev I.V., Ruchin A.B., Fayzulin A.I. 2016b. The helminth fauna study of European common toad in the Volga Basin. Nature Environment and Pollution Technology 15(3): 1103–1109.
Chikhlyaev I.V., Kirillova N.Yu., Kirillov A.A. 2018a. Ecological analysis of trematodes (Trematoda) of marsh frog Pelophylax ridibundus (Ranidae, Anura) from various habitats of the National Park «Samarskaya Luka» (Russia). Nature Conservation Research 3(Suppl.1): 36–50. DOI: 10.24189/ncr.2018.039
Chikhlyaev I.V., Ruchin A.B., Fayzulin A.I. 2018b. An overview of the trematodes fauna of Pool frog Pelophylax lessonae (Camerano, 1882) in the Volga Basin, Russia: 1. Adult stages. Nusantara Bioscience 10(4): 256–262. DOI: 10.13057/nusbiosci/n100410
Chikhlyaev I.V., Ruchin A.B., Fayzulin A.I. 2019a. An overview of the trematodes fauna of Pool frog Pelophylax lessonae (Camerano, 1882) in the Volga Basin, Russia: 2. Larval stages. Nusantara Bioscience 11(1): 106–111. DOI: 10.13057/nusbiosci/n110118
Chikhlyaev I.V., Ruchin A.B., Fayzulin A.I. 2019b. Parasitic nematodes of Pool frog (Pelophylax lessonae) in the Volga Basin. Revista MVZ Cordoba 24(3): 7314–7321. DOI: 10.21897/rmvz1501
Cornish C.A., Oldham R.S., Bullock D.J., Bullock J.A. 1995. Comparison of the diet of adult toads (Bufo bufo L.) with pitfall trap catches. Herpetological Journal 5: 236–238.
Crnobrnja-Isailović J., Ćurćić S., Stojadinović D., Tomašević-Kolarov N., Aleksić I., Tomanović Ž. 2012. Diet composition and food preferences in adult common toads (Bufo bufo) (Amphibia: Anura: Bufonidae). Journal of Herpetology 46(4): 562–567. DOI: 10.1670/10-264
Düşen S. 2011. The helminth parasites of the two bufonid toads, European Common Toad, Bufo bufo (Linnaeus, 1758) and European Green toad, Bufo (Pseudepidalea) viridis Laurenti, 1768 (Anura: Bufonidae), collected from Denizli Province, Inner-West Anatolia Region, Turkey. Helminthologia 48(2): 101–107. DOI: 10.2478/s11687-011-0019-1
Dujsebayeva T.N. 2006. On the southern habitat boundary of Common toad, Bufo bufo (Linnaeus, 1758) in Eastern Kazakhstan. Current Studies in Herpetology 5/6: 50–60. [In Russian]
Fayzulin A.I., Zamaletdinov R.I., Litvinchuk S.N., Rosanov Ju.M., Borkin L.J., Ermakov O.A., Ruchin A.B., Lada G.A., Svinin A.O., Bashinsky I.V., Chikhlyaev I.V. 2018. Species composition and distributional peculiarities of green frogs (Pelophylax esculentus complex) in Protected Areas of the Middle Volga Region (Russia). Nature Conservation Research 3(Suppl.1): 1–16. DOI: 10.24189/ncr.2018.056 [In Russian]
Frolova E.N. 1975. Larva of trematodes in mollusks from lakes of South Karelia. Leningrad: Nauka. 184 p. [In Russian]
Ginetsinskaya T.A. 1968. Trematodes, their life circles, biology and evolution. Leningrad: Nauka. 411 p. [In Russian]
Ginetsinskaya T.A. 1983. Ecology of parasites of invertebrates. Free-living and parasitic invertebrates (morphology, biology, evolution): Proceedings of Research Institute of Leningrad State University 34: 189–210. [In Russian]
González C.E., Hamann M.I. 2007. The first record of amphibians as paratenic hosts of Serpinema larvae (Nematoda; Camallanidae). Brazilian Journal of Biology 67(3): 579–580. DOI: 10.1590/S1519-69842007000300026
Grabda-Kazubska B. 1971. Life cycle of Pleurogenes claviger (Rudolphi, 1819) (Trematoda: Pleurogenidae). Acta Parasitologica Polonica 19: 337–348.
Grabda-Kazubska B. 1980. Observations on the life cycle of Diplodiscus subclavatus (Pallas, 1760) (Trematoda, Diplodiscidae). Acta Parasitologica Polonica 27: 261–271.
Grabda-Kazubska B., Tenora F. 1991. SEM study on Cosmocerca ornata (Dujardin, 1845) and C. commutata (Diesing, 1851) (Nematoda, Cosmocercidae). Acta Parasitologica Polonica 36(1): 45–50.
Hamann M.I., Kehr A.I., González C.E. 2013. Biodiversity of trematodes associated with amphibians from a variety of habitats in Corrientes Province, Argentina. Journal of Helminthology 87(3): 286–300. DOI: 10.1017/S0022149X12000302
Hartwich G. 1975. Die Tierwelt Deutschlands. I. Rhabditida und Ascaridida. Mitteilungen aus dem Zoologischen Museum in Berlin 62: 1–256.
Hendrikx W.M.L. 1983. Observations on the routes of infection of Oswaldocruzia filiformis (Nematoda: Trichostrongylidae) in amphibia. Zeitschrift für Parasitekunde 69(1): 119–126. DOI: 10.1007/BF00934016
Imasuen A.A., Aisien M.S.O. 2015. Helminth parasites of Silurana tropicalis from the Okomu National Park, Edo State, Nigeria. Nigerian Journal of Parasitology 36(1): 61–66.
Johnson P.T.J., Wood Ch.L., Joseph M.B., Preston D.L., Haas S.E., Springer Yu.P. 2016. Habitat heterogeneity drives the host-diversity-begets-parasite-diversity relationship: evidence from experimental and field studies. Ecology Letters 19(7): 752–761. DOI: 10.1111/ele.12609
Jørgensen C.B., Hede K.E., Larsen L.O. 1978. Environmental Control of Annual Ovarian Cycle in the Toad Bufo bufo bufo L.: Role of Temperature. In: I. Assenmacher, D.S. Farner (Eds.): Environmental Endocrinology. Berlin: Springer. P. 28–36. DOI: 10.1007/978-3-642-66981-1_6
Ivanov A.Yu., Ruchin A.B., Fayzulin A.I., Chikhlyaev I.V., Litvinchuk S.N., Kirillov A.A., Svinin A.O., Ermakov O.A. 2019. The first record of natural transfer of mitochondrial DNA from Pelophylax cf. bedriagae into P. lessonae (Amphibia, Anura). Nature Conservation Research 4(2): 125–128. DOI: 10.24189/ncr.2019.020
Kalabekov A.L. 1976. Life circles of some trematodes of long-legged wood frog (Rana macrocnemis Boul.). In: V.I. Naniev (Ed.): Ecology and biology of animals in the northern slopes of the Central Caucasus. Ordzhonikidze: North Ossetia State University. P. 3–42. [In Russian]
Kehr A., Manly B.F.J., Hamann M.I. 2000. Coexistence of helminth species in Lysapsus limellus (Anura: Pseudidae) from an Argentinean subtropical area: Influence of biotic and abiotic factors. Oecologia 125(4): 549–558. DOI: 10.1007/s004420000480
Khotenovsky I.A. 1970. Family Pleurogenidae Looss, 1899. In: K.I. Skrjabin (Ed.): Trematodes of Animals and Man. Essentials of Trematodology. Vol. 23. Moscow: Nauka. P. 139–306. [In Russian]
Kirillov A.A. 2011. Helminth communities of grass snake Natrix natrix L. (Reptilia: Colubridae) from South of Middle Volga region. Proceedings of Samara Scientific Centre RAS 13(1): 127–134. [In Russian]
Kirillov A.A., Kirillova N.Yu. 2016. Analysis of the reproductive structure of the hemipopulation of the Cosmocerca ornata (Dujardin, 1845) (Nematoda: Cosmocercidae) in marsh frogs of different ages. Inland Water Biology 9(3): 310–318. DOI: 10.1134/S199508291603007X
Kirillova N.Yu., Kirillov A.A. 2017. Overview of helminths in small mammals in the Zhiguli State Reserve. Nature Conservation Research 2(2): 24–37. DOI: 10.24189/ncr.2017.007 [In Russian]
Kirillova N.Yu., Kirillov A.A. 2017b. To study of life cycle of amphibian parasite, Cosmocerca ornata (Nematoda: Cosmocercidae). In: S.A. Senator, O.V. Mukhortova, S.V. Saxonov (Eds.): Ecological proceedings of young scientists of the Volga region – 6. Togliatti. P. 192–194. [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]
Kolenda K., Kuśmierek N., Kadej M., Smolis A., Ogielska M. 2019. Road-killed toads as a non-invasive source to study feeding ecology of migrating population. European Journal of Wildlife Research 65(4): 55. https://doi.org/10.1007/s10344-019-1292-4
Korzikov V.A., Aleksanov V.V. 2018. On some factors driving the presence of amphibians in water bodies of the Upper Oka Basin (Central Russia). Nature Conservation Research 3(Suppl.1): 110–119. DOI: 10.24189/ncr.2018.059
Krizmanić I.I., Ivanović A.T. 2010. Population systems of the Pelophylax esculentus complex in the southern part of its range. Folia Zoologica 59(3): 215–222. DOI: 10.25225/fozo.v59.i3.a7.2010
Magurran A.E. 1992. Ecological diversity and its measurement. Moscow: Mir. 182 p. [In Russian]
Neuhaus W. 1940. Entwicklung und Biologie von Pleurogenoides medians Olss. Zoologische Jahrbücher, Abteilung fur Systematic 74: 207–242.
Orlova M.V., Orlov O.L. 2019. Conservation of animals' parasite species: problems and prospects. Nature Conservation Research 4(1): 1–21. DOI: 10.24189/ncr.2019.011 [In Russian]
Paunović A., Bjelić-Čabrilo O., Šimić S. 2010. The diet of water frogs (Pelophylax esculentus 'complex') from the Petrovaradinski Rit marsh (Serbia). Archives of Biological Sciences 62(3): 797–806. DOI: 10.2298/ABS1003797P
Pigulevsky S.V. 1952. Family Gorgoderidae Looss, 1901. Part 1. In: K.I. Skrjabin (Ed.): Trematodes of Animals and Man. Essentials of Trematodology. Vol. 7. Moscow: Publisher of AS USSR. P. 605–760. [In Russian]
Pigulevsky S.V. 1953. Family Gorgoderidae Looss, 1901. Part 2. In: K.I. Skrjabin (Ed.): Trematodes of Animals and Man. Essentials of Trematodology. Vol. 8. Moscow: Publisher of AS USSR. P. 251–615. [In Russian]
Ruchin A.B., Chikhlyaev I.V. 2017. Ecology of amphibians and reptiles of Mordovia. Report 4. European common toad, Bufo bufo (Linnaeus, 1758). Proceedings of the Mordovia State Nature Reserve 18: 172–183. [In Russian]
Ruchin A.B., Chikhlyaev I.V., Lukijanov S.V. 2009. Analysis of helminthofauna of common spaedfoot Pelobates fuscus (Laurenti, 1768) and moor frog Rana arvalis Nilsson, 1842 (Amphibia: Anura) at their joint habitation. Parazitologiya 43(3): 240–247.
Ryzhikov K.M., Sharpilo V.P., Shevchenko N.N. 1980. Helminthes of amphibians in the USSR fauna. Moscow: Nauka. 279 p. [In Russian]
Savinov V.A. 1963. Some new experimental data about nematode paratenic parasitism. In: Materials of scientific conference of All-Union community of helmintologists. Part 2. Moscow: AS USSR. P. 73–75. [In Russian]
Sessions S.K., Ruth S.B. 1990. Explanation for naturally occurring supernumerary limbs in amphibians. Journal of Experimental Zoology 254(1): 38–47. DOI: 10.1002/jez.1402540107
Skrjabin K.I. 1928. Method of complete helminthological dissection of vertebrates, including man. Moscow: Moscow State University. 45 p. [In Russian]
Skrjabin K.I. (Ed.). 1949. Trematodes of Animals and Man. Essentials of Trematodology. Vol. 3. Suborder Paramphistomatata (Szidat, 1936) Skrjabin et Schulz, 1937. Moscow; Leningrad: Nauka. 623 p. [In Russian]
Thiemann G.W., Wassersug R.J. 2000. Biased distribution of trematode metacercariae in the nephric system of Rana tadpoles. Journal of Zoology 252(4): 531–547. DOI: 10.1017/S0952836900220281
Tinsley R.C., Jackson H.C. 1988. Pulsed transmission of Pseudodiplorchis americanus (Monogenea) between desert hosts (Scaphiopus couchii). Parasitology 97(3): 437–452. DOI: 10.1017/S0031182000058844
Zharkikh T.L., Khristianovsky P.I., Bakirova R.T., Petrov V.Yu., Bulgakov E.A., Khuzhakhmetova D.E., Belimenko V.V., Platonov S.A. 2019. Dynamics of intestinal parasite infection in Przewalski's horses reintroduced to Pre-Urals Steppe, Orenburg State Nature Reserve (Russia). Nature Conservation Research 4(Suppl.2): 23–30. DOI: 10.24189/ncr.2019.027