Comparative analysis of the helminth fauna of Apodemus flavicollis and Apodemus uralensis (Rodentia, Muridae) from the protected areas (European Russia)
DOI:
https://doi.org/10.5281/zenodo.11097952Keywords:
Myomorph rodents, yellow-necked mouse, ural field mouse, parasitic worms, syntopic species, protected areasAbstract
Closely related animal species living in similar conditions can enter into competitive relationships. The study of parasitic worms of animal hosts living in the same habitats is of great interest. We conducted a comparative analysis of the parasitic worms of cohabiting mice Apodemus flavicollis and Apodemus uralensis in the Mordovia Nature Reserve and the National Park “Smolny” (European Russia) in 2018–2022. A total of 1457 individuals of the two mouse species were examined by the complete helminthological necropsy: 635 A. flavicollis and 822 A. uralensis. In total 17 species of parasitic worms were recorded, including five cestodes, four trematodes, and eight nematodes. We found that the species diversity of helminths is higher in A. uralensis. All 17 species of parasites were identified in this rodent. The helminth fauna of A. flavicollis is less diverse and represented by 10 parasite species, also characteristic of A. uralensis, including three tapeworms, two flukes, and five nematodes. Apodemus flavicollis and A. uralensis inhabit similar forest habitats and are characterized by an average degree of similarity in helminth composition. The identified differences in the helminth fauna may be associated with the food preferences of these mouse species and the features of their microhabitats. Infection of the two mice with shared helminth species varied among the protected areas studied. At some sampling sites, the infection of A. flavicollis turned out to be higher, at others – of A. uralensis, which is due to changes in the moisture content of the forest floor and a different number of food items (invertebrates) that are intermediate hosts of helminths. The data obtained confirm the partial overlap of ecological niches of sympatric forest rodents, mainly in the spatial and trophic components.
References
Anikanova, V. S., Bugmyrin, S. V., & Ieshko, E. P. (2007). Methods of the collection and studies of helminths of small mammals. Karelia Scientific Center of RAS.
Arneberg, P. (2002). Host population density and body mass as determinants of species richness in parasite communities: comparative analyses of directly transmitted nematodes of mammals. Ecography, 25, 88–94.
Arneberg, P., Skorping, A., Grenfell, B., & Read, A. F. (1998). Host densities as determinants of abundance in parasite communities. Proceedings of the Royal Society of London B, 265, 1283–1289.
Artaev, O. N., & Grishutkin, O. G. (2014). Lakes of Mordovia. Mordovia Reserve, 6, 20–23.
Artaev, O. N., & Smirnov, D. G. (2016). Bats (Chiroptera; Mammalia) of Mordovia: specific structure and features of distribution. Nature Conservation Reserve, 1(1), 38–51. https://doi.org/10.24189/ncr.2016.004
Artaev, O. N., Ruchin, A. B., Bugaev, K. E., Grishutkin, G. F., Potapov, S. K., & Spiridonov, S. N. (2012). Vertebrates of the Mordovia State Nature Reserve. Committee of RAS for the conservation of Biological Diversity.
Averin, Yu. V., Lozan, M. N., Muntyanu, A. I., & Uspensky, G. A. (1979). Fauna of Moldova. Mammals. Shtiintsa.
Bakanov, A. I. (1987). Quantitated estimation of dominance in ecological communities; The manuscript was deposited in All-Union Institute of Scientific and Technical Information (VINITI) by 08.12.1987, No. 8593–B87; IBIW RAS Publishing.
Bolek, M. G., & Coggins, J. R. (2003). Helminth community structure of sympatric Eastern American toad, Bufo americanus americanus, Nortern Leopard frog, Rana pipiens, and Blue-spotted salamander, Ambystoma laterale, from Southestern Wisconsin. Journal of Parasitology, 89(4), 673–680. https://doi.org/10.1645/GE-70R
Carter, T. C., Menzel, M. A., Chapman, B. R., & Miller, K. V. (2004). Partitioning of food resources by syntopic Eastern Red (Lasiurus borealis), Seminole (L. seminolus) and Evening (Nycticeius humeralis) bats. American Midland Naturalist, 151, 186–191.
Churchfield, S. (1984). An investigation of the population ecology of syntopic shrews inhabiting water-cress beds. Journal of Zoology, 204(2), 229–240. https://doi.org/10.1111/j.1469-7998.1984.tb02372.x
Duvernell, D. D., Schaefer, J. F., Hancks, D. C., Fonoti, J. A., & Ravanelli, A. M. (2007). Hybridization and reproductive isolation among syntopic populations of the topminnows Fundulus notatus and F. olivaceus. Journal of Evolutionary Biology, 20(1), 152–164. https://doi.org/10.1111/j.1420-9101.2006.01213.x
Dwuznik, D., Gortat, T., Behnke, J. M., Gryczynska, A., Bednarska, M., Mikoszewski, A. S., Kozakiewicz, M., & Bajer, A. (2017). Comparison of helminth community of Apodemus agrarius and Apodemus flavicollis between urban and suburban populations of mice. Parasitology Research, 116, 2995–3006.
Fedynich, A. M., Pence, D. B., & Bergan, J. F. (1997). Helminth community structure and pattern in sympatric populations of double-crested and neotropic cormorants. Journal of the Helminthological Society of Washington, 64(2), 176–182.
Feliu, C., Spakulova, M., Casanova, J. C., Renaud, F., Morand, S., Hugot, J. P., Santalla, F., & Durand, P. (2000). Genetic and morphological heterogeneity in small rodent whipworms in southwestern Europe: Characterization of Trichuris muris and description of Trichuris arvicolae n. sp. (Nematoda: Trichuridae). Journal of Parasitology, 86, 442–449. https://doi.org/10.1645/0022‐3395(2000)086[0442:GAMHIS]2.0.CO;2.
Gause, G. F. (1934). The Struggle for Existence. Williams & Wilkins.
Genov, T. (1984). Helminths of insectivores and rodents in Bulgaria. Bulgarian Academy of Sciences.
Gorman, T. A., & Haas, C. A. (2011). Seasonal microhabitat selection and use of syntopic populations of Lithobates okaloosae and Lithobates clamitans clamitans. Journal of Herpetology, 45(3), 313–318. https://doi.org/10.1670/10-135.1
Grishutkin, O. G. (2013). Patterns of the distribution of swamps depending on the absolute marks of the relief on the territory of the Mordovia State Nature Reserve. Proceedings of Mordovia State Nature Reserve, 11, 259–263.
Grishutkin, G. F., Lapshin, A. S., Spiridonov, S. N., Artaev, O. N., Ruchin, A. B., Kuznetsov, V. A., & Andreychev, A. V. (2013). Vertebrate animals of National Park “Smolny”. Committee of RAS for the Reserve of Biological Diversity.
Gromov, I. M., & Erbaeva, M. A. (1995). Mammals of the fauna of Russia and adjacent territories. Lagomorphs and rodents. Zoological Institute of RAS.
Hammer, O., Harper, D. A. T., & Ryan, P. D. (2001). PAST: Paleontological statistics software package for education and data analysis. Version 2.16. Palaeontol. Electron, 4, 9.
Heym, A., Deichsel, G., Hochkirch, A., Veith, M., & Schulte, U. (2013). Do introduced wall lizards (Podarcis muralis) cause niche shifts in a native sand lizard (Lacerta agilis) population? A case study from south-western Germany. Salamandra, 49(2), 97–104.
Hofer, U., Bersier, L.-F., & Borcard, D. (2004). Relating niche and spatial overlap at the community level. Oikos, 106(2), 366–376. https://doi.org/10.1111/j.0030-1299.2004.12786.x
Kaicheen S.S., Mohd-Azlan J. 2022. Community structures of mid-sized to large-bodied mammals in tropical lowland and lower montane forests in Gunung Pueh National Park, Western Sarawak, Borneo. Nature Conservation Research 7(1): 70–79. https://dx.doi.org/10.24189/ncr.2022.009
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. https://dx.doi.org/10.24189/ncr.2019.059
Kirillov, A. A., Kirillova, N. Yu., & Chikhlyaev, I. V. (2012). Trematodes of land vertebrates of the Middle Volga region; Cassandra.
Kirillova, N. Yu. (2009). Dynamics of the helminth community of bank vole (Clethrionomys glareolus) in subsequent years. Povolzhskiy Journal of Ecology, 3, 219–227.
Kirillova, N. Y., Kirillov, A. A., & Vekhnik, V. P. (2022). Comparative analysis of the helminth fauna of Myotis brandtii and Myotis mystacinus (Chiroptera, Vespertiluonidae) in the Samarskaya Luka National Park (Russia). Nature Conservation Research, 7, 1–14. https://dx.doi.org/10.24189/ncr.2022.026
Kirillova, N. Y., Kirillov, A. A., & Vekhnik, V. A. (2023). The diversity of trematodes in Myotis bats (Chiroptera, Vespertilionidae) from the Samarskaya Luka (European Russia). Animals, 13, 3738. https://doi.org/10.3390/ani13233738
Kirillova, N. Y., Kirillov, A. A., Ruchin, A. B., Alpeev, M. A., Smirnov, D. G., & Vekhnik, V. P. (2024). Occurrence of small mammals in Mordovia State Nature Reserve and National Park “Smolny” (European Russia). Version 1.1. Joint Directorate of the Mordovia State Nature Reserve and National Park "Smolny". Occurrence dataset, https://doi.org/10.15468/wtucv2
Kozlov, V. I., & Tukhsanova, N. G. (1966). Nutrition of myomorph rodents. Proceedings Gorky State University, 75, 117–128.
Magurran, A. E. (2004). Measuring biological diversity. Blackwell Publishing.
Makarikov, A. A., & Tkach, V. V. (2013). Two new species of Hymenolepis (Cestoda: Hymenolepididae) from Spalacidae and Muridae (Rodentia) from eastern Palearctic. Acta Parasitologica, 58, 37–49. https://dx.doi.org/10.2478/s11686‐013‐0115‐0
Martínez-Sotelo J., Sánchez-Jasso J.M., Ibarra-Zimbrón S., Sánchez-Nava P. 2022. Zoonotic intestinal parasites in free-ranging dogs (Canis lupus familiaris): a risk to public health in a Mexican Protected Area. Nature Conservation Research 7(2): 21–31. https://dx.doi.org/10.24189/ncr.2022.015
Massoud, D., Lao-Perez, M., Ortega, E., Burgos, M., Jimenez, R., & Barrionuevo, F. J. (2021). Divergent seasonal reproductive patterns in syntopic populations of two murine species in southern Spain, Mus spretus and Apodemus sylvaticus. Animals, 11, 243. https://doi.org/10.3390/ani11020243
Mata-Silva, V., Bursey, C. R., & Johnson, J. D. (2008). Gut parasites of two syntopic species of whiptail lizards, Aspidoscelis marmorata and Aspidoscelis tessellata from the Northern Chihuahuan Desert. Boletin de la Sociedad Herpetologica Mexicana, 16(1), 1–4.
Navarro, P., Lluch J., & Font E. (2005). The component helminth community in six sympatric species of Ardeidae. Journal of Parasitology, 91(4), 775–779. https://doi.org/10.1645/GE-3342.1
Oliveira C.D.L., Café K.J.S.B., Batista V.S. 2022. Management plans for Protected Areas in Brazil reveal similarity between specific objectives and mammals as the main focus of conservation. Nature Conservation Research 7(3): 64–74. https://dx.doi.org/10.24189/ncr.2022.030
Ondrikova J., Miklisova D., Ribas A., & Stanko M. (2010). The helminth parasites of two sympatric species of the genus Apodemus (Rodentia, Muridae) from south-eastern Slovakia. Acta Parasitologica, 55(4), 369–378. https://doi.org/10.2478/s11686–010–0043–1
Pianka, E. R. (1981). Evolutionary ecology. Mir.
Poulin, R. (1998). Comparison of three estimators of species richness in parasite component communities. Journal of Parasitology, 84(3), 485–490.
Quentin, J. C. (1970) Morphogenese larvarie du spiruride Mastophorus muris (Gmelin, 1790). Annales de Parasitologie Humaine et Comparee, 45, 839–855.
Ramiez-Bautista, A., & Lemos-Espinal, J. A. (2004). Diets of two syntopic populations of frogs, Rana vaillanti and Rana brownorum, from a tropical rain forest in southern Veracruz, Mexico. Southwestern Naturalist, 49(3), 316–320. https://doi.org/10.1894/0038-4909(2004)049<0316:DOTSPO>2.0.CO;2
Ribble, D. O., & Stanley, S. (1998). Home ranges and social organization of syntopic Peromyscus boylii and P. truei. Journal of Mammalogy, 79(3), 932–941. https://doi.org/10.2307/1383101
Rossolimo, O. L., Pavlinov, I. Ya., Kruskop, S. V., Lisovsky, A. A., Spasskaya, N. N., Borisenko, A. V., & Panyutina, A. A. (2004). Mammal diversity. Part II. KMK.
Ruchin, A. B., & Chikhlyaev, I. V. (2013). Analysis of helminthofauna of the moor frog Rana arvalis Nilsson, 1842 and European common frog Rana temporaria Linnaeus, 1768 (Amphibia: Anura) at joint habitation. Current Studies in Herpetology, 13(3/4), 130–136.
Ryzhikov, K. M., Gvozdev, E. V. Tokobaev M. M., Shaldybin L. S., Matsaberidze G. M., Merkusheva I. V., Nadtochiy E. V., Khokhlova I. G., & Sharpilo L. D. (1978). Keys to the helminths in rodents of the USSR fauna. Cestodes and Trematodes. Nauka.
Ryzhikov, K. M., Gvozdev, E. V., Tokobaev M. M., Shaldybin L. S., Matsaberidze G. M., Merkusheva I. V., Nadtochiy E. V., Khokhlova I. G., & Sharpilo L. D. (1979). Keys to the helminths in rodents of the USSR fauna. Nematodes and Acanthocephala. Nauka.
Shaykenov, B. (1981). Helminths in Rodents from Kazakhstan. Nauka.
Simoes, R. O., Souza, J. G. R., Maldonado, Jr. A., & Luque, J. L. (2011). Variation in the helminth community structure of three sympatric sigmodontine rodents from the coastal Atlantic Forest of Rio de Janeiro, Brazil. Journal of Helminthology, 85, 171–178. https://doi.org/10.1017/S0022149X10000398
Sinsch, U., Balczun, C., Scheid, P., & Dehling, J. M. (2021). Component endoparasite communities mirror life-history specialization in syntopic reed frogs (Hyperolius spp.). Diversity, 13, 669. https://doi.org/10.3390/d131206
Smirnov, D. G., Kirillova, N. Yu., Kirillov, A. A., Ruchin, A. B., Vekhnik, V. A. (2022). New records of Nyctalus leisleri (Kuhl, 1817) and Myotis nattereri (Kuhl, 1817) (Mammalia: Chiroptera: Vespertilionidae) from National Park “Smolny” and its surroundings, Republic of Mordovia. Journal of Threatened Taxa, 14(8), 21553–21560.
Smith, E. P., & van Belle, G. (1984). Nonparametric estimation of species richness. Biometrics, 40, 119–129.
Smith, A. J., & Fedynich, A. M. (2012). Helminth community composition, structure and pattern in six dove species (Columbiformes: Columbidae) of South Texas. Journal of Parasitology, 98(1), 11–21. https://doi.org/10.1645/GE-2561.1
Vasil’ev, A. G., Lukyanova, L. E., & Gorodilova, Yu. V. (2023). Coupled variation of red-backed vole species in biotopes disturbed by windfall and fire in the Visim State Nature Reserve (the Middle Urals). Nature Conservation Research, 8(3), 24–46. https://dx.doi.org/10.24189/ncr.2023.020
Vekhnik, V. A., Vekhnik, V. P., Rozentsvet, O. A., & Bogdanova, E. S. (2019). Possible relations between reproduction of, the Yellow-necked mouse (Sylvaemus flavicollis) and oak yield. Russian Journal of Theriology, 18(1), 33–42. https://dx.doi.org/10.15298/rusjtheriol.18.1.04
Yoder, H. R., & Coggins, J. R. (2007). Helminth communities in five species of sympatric amphibians from three adjacent ephemeral ponds in Southeastern Wisconsin. Journal of Parasitology, 93(4), 755–760. https://doi.org/10.1645/GE-1077R.1
Zablotskaya, L. V. (1957). Materials on the ecology of the main species of myomorph rodents in the Prioksko-Terrasny Nature Reserve and adjacent forests. Proceedings of Prioksko-Terrasny Nature Reserve, 1, 170–241.
Zhigileva, O. N., & Kirina, I. Yu. (2015). Helminth infestation of the moor frog (Rana arvalis Nilsson, 1842) and the Siberian tree frog (Rana amurensis Boulenger, 1886) in Western Siberia. Contemporary Problems of Ecology, 8(2), 232–236. https://doi.org/10.1134/S1995425515020171
JWB applies the 