Article

Igor V. Chikhlyaev, PhD, Senior Researcher of the Laboratory of Population Ecology, Institute of Ecology of the Volga River Basin of RAS (445003, Russia, Samara Region, Togliatti, Komzina street, 10); e-mail: diplodiscus@mail.ru
Nadezhda Yu. Kirillova, PhD, Senior Researcher of the Institute of Ecology of the Volga River Basin of RAS (445003, Russia, Samara Region, Togliatti, Komzina Street, 10); e-mail: parasitolog@yandex.ru
Alexander A. Kirillov, PhD, Senior Researcher of the Institute of Ecology of the Volga River Basin of RAS (445003, Russia, Samara Region, Togliatti, Komzina Street, 10); e-mail: parasitolog@yandex.ru

Chikhlyaev I.V., Kirillova N.Yu., Kirillov A.A. 2018. 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. https//dx.doi.org/10.24189/ncr.2018.039

A comparative analysis of the trematode fauna of the marsh frog Pelophylax ridibundus from different habitats of the National Park «Samarskaya Luka» is given. It is based on the authors' own materials collected in 1998‒2001 on three locations: on the coast of the Volga channel, floodplain lakes and nearby islands. Twenty-two trematode species were found. Differences in the composition of trematodes and the nature of infestation of amphibians from different biotopes have been revealed. It has been established that the diversity of trematodes and their infectivity are higher in amphibians in floodplain lakes with relatively constant environmental conditions. Frogs from river coast habitats with dynamic environmental conditions are less infected with the same diversity of species. Amphibians of isolated island habitats are characterised by relatively small number of trematode species and a low level of helminth invasion. The causes of differences in amphibian infestation by trematodes in different biotopes are complex. Diversity, high abundance of mollusks and arthropods (intermediate hosts) cause a high level of infestation of frogs with sexually mature flukes, transmitted through food chains. The high density of the amphibians themselves, and, accordingly, of the predators batrachophages, leads to intensive infestation of frogs by larval stages of trematodes. A literature review of the data on the influence of abiotic and biotic factors of the environment on amphibian trematode is given. The formation of the trematode fauna of frogs is influenced by a number of environmental factors acting in the aggregate: the hydrological regime of the reservoir, the diversity and density of populations of intermediate, reservoir and definitive hosts of trematodes in the biocoenosis.

different habitats, marsh frog, National Park «Samarskaya Luka», Pelophylax ridibundus, Russia, trematodes

Received: 22.03.2018

Altman I. 2010. Trematode parasites of the mudsnail Ilyanassa obsoleta: an analysis of parasite communities at different scales. PhD Thesis. Durham, New Hampshire: University of New Hampshire. 151 p.
Bakanov A.I. 1987. Quantitated estimation of dominance in ecological communities. Borok. 64 p. The manuscript was deposited in All-Union Institute of Scientific and Technical Information (VINITI) 08.12.1987, №8593‒В87. [In Russian]
Byhovskaya-Pavlovskaya I.Е. 1985. Parasites of fishes, a study guide. Leningrad: Nauka. 123 p. [In Russian]
Bulachov V.L., Konstantinova N.F. 1978. The influence of biocenotic factors on the helminths infestation of amphibians in forest ecosystems of the Dnieper surroundings. In: Abstracts of I All-Union Congress of parasitocenologists. Part 1. Kiev: Naukova Dumka. P. 59–61. [In Russian]
Chandra P., Gupta N. 2007. Habitat Preference and Seasonal Fluctuations in the Helminthofauna of Amphibian Hosts of Rohilkhand Zone, India. Asian Journal of Experimental Sciences 21(1): 69‒78.
Chikhlyaev I.V., Kirillov A.A., Kirillova N.Yu. 2012а. Trematodes (Trematoda) of amphibians (Amphibia) of the Middle Volga region. 1. Orders Fasciolida, Hemiuridae, Paramphistomidae and Strigeida. Parazitologiia 46(3): 171–192. [In Russian]
Chikhlyaev I.V., Kirillov A.A., Kirillova N.Yu. 2012b. Trematodes (Trematoda) of amphibians (Amphibia) of the Middle Volga region. 1. Order Plagiorchiida. Parazitologiia 46(4): 290–313. [In Russian]
Chikhlyaev I.V., Kirillova N.Yu., Kirillov A.A. 2012c. Characteristics of the life cycles of trematodes (Trematoda) of land vertebrates of the Middle Volga region. Proceedings of Samara Scientific Centre of RAS 14(5): 132–142. [In Russian]
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., Ruchin A.B., Alexeev S.K., Korzikov V.A. 2013. To the helminthofauna of the European common frog Rana temporaria Linnaeus, 1768 (Amphibia: Anura) from different habitats in the Kaluga region. Current Studies in Herpetology 13(1/2): 58–63. [In Russian]
Chikhlyaev I.V., Ruchin A.B., Fayzulin A.I. 2016. The helminth fauna study of European common toad in the Volga Basin. Nature, Environment and Pollution Technology 15(3): 1103‒1109.
Comas M., Ribas A. 2013. Why are the prevalence and diversity of helminths in the endemic Pyrenean brook newt Calotriton asper (Amphibia, Salamandridae) so low? Journal of Parasitology 89(2): 175–181. DOI: 10.1017/S0022149X13000710
Dobrovolsky А.А. 1965а. Life cycle of Pneumonoeces asper Looss, 1899 (Plagiorchiidae, Pneumonoecinae). In: Proceedings of the scientific conference of the All-Union society of helminthologists. Part. 4. Moscow: Publisher of AS USSR. P. 59–64. [In Russian]
Dobrovolsky А.А. 1965b. Some data about the life cycle of the flukes Opisthioglyphe ranae (Froelich, 1791) (Plagiorchiidae). Helminthologia 3: 205–221. [In Russian]
Dobrovolsky А.А. 1969. Life cycle of Paralepoderma cloacicola (Lühe, 1909) Dollfus, 1950 (Trematoda, Plagiorchiidae). Bulletin of Leningrad State University 21: 28–38. [In Russian]
Dogel V.A. 1938. Some results of work in the field of parasitology. Zoologicheskii zhurnal 17(5): 889–904. [In Russian]
Dogel V.A. 1947. Importance of parasitological data to solve zoogeographical issues. Zoologicheskii zhurnal 26(6): 481–492. [In Russian]
Dubinina M.N. 1950. Ecological study of marsh frog (Rana ridibunda Pall.) parasites in the Volga Delta. In: Parasitological Proceedings. Vol. 12. Leningrad: Publisher of Zoological Institute of AS USSR. P. 300–350. [In Russian]
Dusen S., Oz M. 2013. Helminth fauna of the Eurasian Marsh Frog, Pelophylax ridibundus (Pallas, 1771) (Anura: Ranidae), collected from Denizli Province, Inner-West Anatolia Region, Turkey. Helminthologia 50(1): 57–66. DOI: 10.2478/s11687-013-0108-4
Frolova E.N. 1975. Larvae of trematodes of mollusks in South Karelia lakes. Leningrad: Nauka. 184 p. [In Russian]
Ginetsinskaya T.A. 1959. To the fauna of cercariae in molluscs in the Rybinsk water reservoir. Part II. The influence of ecological factors on the infestation of molluscs by trematodes. Bulletin of Leningrad State University 21: 62–77. [In Russian]
Ginetsinskaya T.A. 1968. Trematodes, their life cycles, 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]
Ginetsinskaya T.A., Stein G.A. 1961. Peculiarities of invertebrates parasitofauna and the application of the basic rules of ecological parasitology to the characteristics of their infection. Bulletin of Leningrad State University 15: 60–72. [In Russian]
Grabda B. 1960. Life cycle of Haematoloechus similis (Looss, 1899) (Trematoda: Plagiorchidae). Acta Parasitologica Polonica 8(23): 357–366.
Grabda-Kazubska B. 1971. Life cycle of Pleurogenes claviger (Rudolphi, 1819) (Trematoda: Pleurogenidae). Acta Parasitologica Polonica 19(29): 337–348.
Hoberg E.P. 1996. Faunal diversity among avian parasite assemblages: the interaction of history, ecology, and biogeography in marine systems. Bulletin of the Scandinavian Society of Parasitology 6: 65‒89.
Johnson P.T.J., Wood Ch.L., Joseph M.B., Preston D.L., Haas S.E., Springe Y.P. 2016. Habitat heterogeneity drives the host-diversity-begets parasite-diversity relationship: evidence from experimental and field studies. Ecology Letters 19: 752–761. DOI: 10.1111/ele.12609
Khotenovsky I.A. 1970. Family Pleurogenidae Looss, 1899. In: K.I. Skrjabin (Ed.): Trematodes of animals and humans. Fundamentals of trematodology. Vol. 23. Moscow: Nauka. P. 136‒297. [In Russian]
Kirillov A.A., Kirillova N.Yu. 2011. Trematodes (Trematoda) of reptiles from Middle Volga region. Proceedings of Samara Scientific Centre of RAS 13(5): 139‒147. [In Russian]
Kirillov A.A., Kirillova N.Yu. 2013а. Trematodes of birds (Aves) from Middle Volga region. 1. Orders Brachylaimida, Cyclocoelida, Echinostomatida, Notocotylida and Opisthorchiida. Parazitologiia 47(1): 47–76. [In Russian]
Kirillov A.A., Kirillova N.Yu. 2013b. Trematodes of birds (Aves) from Middle Volga region. 2. Orders Plagiorchiida, Renicolida, Strigeida and Schistosomatida. Parazitologiia 47(2): 136–177. [In Russian]
Kirillov A.A., Kirillova N.Yu., Vekhnik V.P. 2012а. Trematodes (Trematoda) of bats (Chiroptera) from the Middle Volga region. Parazitologiia 46(5): 384‒413. [In Russian]
Kirillov A.A., Kirillova N.Yu., Chikhlyaev I.V. 2012b. Trematodes of land vertebrates of Middle Volga region. Togliatti: Cassandra. 329 p. [In Russian]
Kirillov A.A., Kirillova N.Yu., Chikhlyaev I.V. 2012c. Metacercariae and mesocercariae of trematodes in terrestrial vertebrates from the Middle Volga region. Morphology, systematics and ecology of parasites: Proceedings of Centre of Parasitology (Proceedings of HELAS) 47: 99‒119. [In Russian]
Kirillova N.Yu., Kirillov A.A. 2009. Trematodes (Trematoda) of small mammals from the Middle Volga region. Parazitologiia 43(3): 225‒239. [In Russian]
Koyun M., Birlik S., Sumer N., Yildirimhan H.S. 2015. Helminth fauna of Eurasian marsh frog, Pelophylax ridibundus (Pallas, 1771) (Anura: Ranidae) from Bingol, Eastern Anatolia, Turkey. Biharean Biologist 9(2): 128‒132.
Krichevskaya I.E. 1961. Parasites of tadpoles and yearlings of marsh frog (Rana ridibunda) in Volga Delta. Proceedings of the Astrakhan Reserve 5: 336–349. [In Russian]
Kuranova V.N. 1988. The helminthofauna of anuran amphibians of the Middle Ob floodplain, its sex-age and seasonal dynamics. In: Ecological problems of invertebrates. Tomsk: Publisher of Tomsk State University. P. 134–154. [In Russian]
Magurran A.E. 1992. Ecological diversity and its measurement. Moscow: Mir. 182 p. [In Russian]
Malinovskaya I.E. 1999. Flora of The Mordovo floodplain. In: Samarskaya Luka at the threshold of the Third Millennium. Togliatti: Publisher of Institute of Ecology of the Volga river basin of RAS, OSNP «Parkway». P. 116–120. [In Russian]
Marcogliese D.J. 2001. Distribution and abundance of sealworm (Pseudoterranova decipiens) and other anisakid nematodes in fish and seals in the Gulf of St. Lawrence: potential importance of climatic conditions. NAMMCO Scientific Publications 3: 113‒128.
Marcogliese D.J., Cone D.K. 1997. Parasite communities as indicators of ecosystem stress. Parassitologia 6: 65‒89.
Markov G.S., Rogosa M.L. 1953. Seasonal and microtonal differences in the parasitofauna of European common frog. Doklady Biological Sciences 91(1): 169–172. [In Russian]
Mohammad M.K., Shubber H.W.K., Al-Waaly A.B.M. 2015. Intestinal helminth parasites of the Eurasian marsh frog Pelophylax ridibundus (Pallas, 1771) (Amphibia: Ranidae) collected in Al-Diwaniya City, Middle of Iraq. Bulletin of Iraq Natural History Museum 13(4): 11‒20.
Muzzall P.M., Gillilland M.G., Summer C.S., Mehne C.J. 2001. Helminth communities of green frogs Rana clamitans Latreille, from Southwestern Michigan. Journal of Parasitology 87(5): 962‒968. DOI: 10.1645/0022-3395(2001)087[0962:HCOGFR]2.0.CO;2
Niewiadomska K. 1964. The life cycle of Codonocephalus urnigerus (Rudolphi, 1819) – Strigeidae. Acta Parasitologica Polonica 12(25): 283–296.
Niewiadomska K., Pojmanska T. 2011. Multiple strategies of digenean trematodes to complete their life cycles. Wiadomosci Parazytologiczne 57(4): 233–241.
Overstreet R.M. 1997. Parasitological data as monitors of environmental health. Parassitologia 39: 169‒175.
Pigulevsky S.V. 1952. Family Gorgoderidae Looss, 1901. Part 1. In: K.I. Skrjabin (Ed.): Trematodes of animals and humans. Fundamentals 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 humans. Fundamentals of trematodology. Vol. 8. Moscow: Publisher of AS USSR. P. 251–615. [In Russian]
Rahman W.A., Shakinah Z. 2015. Influence of some environmental parameters on some frog populations and their parasitic fauna. Journal of Veterinary Science and Technology 6(3): 227‒231. DOI: 10.4172/2157-7579.1000227
Rankin J.S. 1937. An ecological study of parasites of some North Carolina Salamanders. Ecological Monographs 7(2): 169‒269. DOI: 10.2307/1943289
Rankin J.S. 1945. An ecological study of the helminth parasites of amphibians and reptiles of Western Massachusetts and vicinity. Journal of Parasitology 31(2): 142‒150. DOI: 10.2307/3272938
Reshetnikov A.N., Sokolov S.G., Chikhlyaev I.V., Fayzulin A.I., Kirillov A.A., Kuzovenko A.E., Protasova E.N., Skomorokhov M.O. 2013. Direct and indirect interactions between an invasive alien fish (Perccottus glenii) and two native semi-aquatic snakes. Copeia 1: 103–110. DOI: 10.1643/CE-12-007
Rezvantseva M.V. 2013. Helminthofauna of marsh frogs in different water reservoirs in Tambov. Bulletin of Tambov State University 18(6): 3067‒3070. [In Russian]
Ruchin A.B., Chikhlyaev I.V., Lukijanov S.V. 2009. Analysis of helmintofauna of common spaedfoot Pelobates fuscus (Laurenti, 1768) and moor frog Rana arvalis Nilsson, 1842 (Amphibia: Anura) at their joint habitation. Parazitologiia 43(3): 240‒247. [In Russian]
Ryzhikov K.M., Sharpilo V.P., Shevchenko N.N. 1980. Helminths of amphibians of the USSR fauna. Moscow: Nauka. 279 p. [In Russian]
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. DOI: 10.3354/dao072253
Skrjabin K.I. 1928. Method of full helminthological dissection of vertebrates, including humans. Moscow: Publisher of Moscow State University. 45 p. [In Russian]
Skrjabin K.I. 1949. Trematodes of animals and humans. Fundamentals of trematodology. Vol. 3. Suborder Paramphistomatata. Moscow; Leningrad: Publisher of AS USSR. 624 p. [In Russian]
Skrjabin K.I., Antipin D.N. 1962. Superfamily Plagiorchioidea Dollfus, 1930. In: K.I. Skrjabin (Ed.): Trematodes of animals and humans. Fundamentals of trematodology. Vol. 20. Moscow: Nauka. P. 49–166. [In Russian]
Smirnova M.I., Sizova V.G. 1978. Helminthofauna of aquatic amphibians of the green zone of Kazan. In: Natural resources of the Volga-Kama region. Vol. 5. Kazan: Institute of Biology of AS USSR. P. 194–201. [In Russian]
Souza W.P., Grosholz E.D. 1991. The influence of habitat structure on the transmission of parasites In: S.S. Bell, E.D. McCoy, H.R. Mushinsky (Eds.): Habitat Structure. The physical arrangement of objects in space. Netherlands: Springer. P. 300‒324.
Sudarikov V.E. 1960a. Towards the biology of trematodes Strigea strigis (Schr., 1788) and S. sphaerula (Rud., 1803). Proceedings of the Helminthological Laboratory of AS USSR (HELAS) 10: 217–226. [In Russian]
Sudarikov V.E. 1960b. Order Strigeidida (La Rue, 1926) Sudarikov, 1959. In: K.I. Skrjabin (Ed.): Trematodes of animals and humans. Fundamentals of trematodology. Vol. 17. Part 2. Moscow: Publisher of AS USSR. P. 157–533. [In Russian]
Sudarikov V.E., Lomakin V.V., Semenova N.N. 1991. Trematode Pharyngostomum cordatum (Alariidae, Hall et Wigdor, 1918) and its life cycle in the conditions of the Volga delta. Helminths of animals: Proceedings of the Helminthological Laboratory of AS USSR (HELAS) 38: 142–147. [In Russian]
Sudarikov V.E., Shigin A.A., Kurochkin Yu.V., Lomakin V.V., Stenko R.P., Yurlova N.I. 2002. Metacercariae of trematodes – parasites of freshwater aquatic organisms in Central Russia. Vol. 1. Moscow: Nauka. 298 p. [In Russian]
Shevchenko N.N. 1965. Helminths fauna of the biocenosis of the Seversky Donets river and ways of its circulation in the middle flow of the river: Doctoral Thesis. Kharkiv. 45 p. [In Russian]
Shevchenko N.N., Vergun G.I. 1961. On the life cycle of amphibian trematodes Prosotocus confusus (Looss, 1894) Looss, 1899. Helminthologia 3(1–4): 294–298. [In Russian]
Stein G.A. 1959. Materials on the parasitology of arthropods of some lakes of Karelia. III. Larvae of Acanthocephala (Acanthocephala) from crustaceans. In: Ecological parasitology. Leningrad: Publisher of Leningrad State University. P. 195–204. [In Russian]
Tomba A.M. 2006. Effects of trematode parasites on habitat use and disturbance response of freshwater snails in the genus Elimia. PhD Thesis. Auburn, Alabama. 76 p.
Wisniewski L.W. 1958. Characterization of the parasitofauna of an eutrophic lake. Acta Parasitologica Polonica 6(1): 1–61.
Yeo S.E., Spieler R.E. 1980. Habitat effects on the occurrence of parasites inhabiting the sergeant major, Abudefduf saxatilis (Linnealus), with a list of parasites of caribbean damselfishes. Bulletin of Marine Science 30(Suppl. 1): 313‒324.
Yildirimhan H.S., Bursey C.R., Goldberg S.R. 2005. Helminth Parasites of the Caucasian Salamander, Mertensiella caucasica, from Turkey. Comparative Parasitology 72(1): 75‒87. DOI: 10.1654/4152