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Diversity, distribution and changes in communities of fleas on small mammals along the elevational gradient from the Pannonian Plain to the Carpathian Mountains

Published online by Cambridge University Press:  22 October 2020

Ivan Baláž Open the ORCID record for Ivan Baláž [Opens in a new window] ,
Michal Ševčík ,
Filip Tulis ,
Martina Zigová  and
Alexander Dudich
Ivan Baláž*
Affiliation:
Department of Ecology and Environmental Sciences, Faculty of Natural Sciences, Constantine the Philosopher University in Nitra, Trieda A. Hlinku 1, 949 74 Nitra, Slovakia
Michal Ševčík
Affiliation:
Department of Ecology and Environmental Sciences, Faculty of Natural Sciences, Constantine the Philosopher University in Nitra, Trieda A. Hlinku 1, 949 74 Nitra, Slovakia
Filip Tulis
Affiliation:
Department of Ecology and Environmental Sciences, Faculty of Natural Sciences, Constantine the Philosopher University in Nitra, Trieda A. Hlinku 1, 949 74 Nitra, Slovakia
Martina Zigová
Affiliation:
Department of Ecology and Environmental Sciences, Faculty of Natural Sciences, Constantine the Philosopher University in Nitra, Trieda A. Hlinku 1, 949 74 Nitra, Slovakia
Alexander Dudich
Affiliation:
Department of Ecology and Environmental Sciences, Faculty of Natural Sciences, Constantine the Philosopher University in Nitra, Trieda A. Hlinku 1, 949 74 Nitra, Slovakia
*
Author for correspondence: Ivan Baláž, E-mail: [email protected]
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Abstract

The causal chain of parasite–host–environment interactions, the so-called ‘dual parasite environment’, makes studying parasites more complicated than other wild organisms. A sample of 65 282 fleas taken from 336 different locations were analysed for changes in the distribution, diversity and compensation of flea communities found on small mammals along an elevational diversity gradient ranging from the Pannonian Plain to the base of the Carpathian summits. The fleas were divided into four groups, which were derived from changes in abundance and occurrence determined from cluster analysis. They are (1) flea species whose range seems unrelated to any change in elevation; (2) species that avoid high altitudes; (3) a group that can be subdivided into two types: (i) host-specific fleas and (ii) mountains species and (4) species opting for high altitudes on the gradient or preferring lower to middle elevations below 1000 m. Our study showed a unimodal pattern of flea diversity along the elevational gradient. It indicated that seasonality significantly conditions changes in biodiversity and patterns of spatial change along the elevational gradient, with specific flea species influenced by their host, while the impact of environmental conditions is more pronounced in opportunistic flea species.

Keywords

EulipotyphlaRodentiaSiphonapteraunimodal pattern
Type
Research Article
Information
Parasitology , Volume 148 , Issue 1 , January 2021 , pp. 63 - 73
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Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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References

Ambros, M (1998) Small mammals (Insectivora, Rodentia) in the earth traps of representative habitats of Bystričianska Valley in Vtáčnik Mts. Rosalia (Nitra) 13, 235–240 (in Slovak).Google Scholar
Anděra, M and Horáček, I (2005) We Recognize Our Mammals. Jihlava: Sobotáles (in Czech).Google Scholar
Baláž, I, Ambros, M, Tulis, F, Veselovský, T, Klimant, P and Augustiničová, G (2013) Rodents and insectivores of Slovakia, Prírodovedec. Nitra: Univerzita Konštantína Filozofa v Nitre, Fakulta prírodných vied (in Slovak).Google Scholar
Barry, RG (2008) Mountain Weather and Climate. UK: Cambridge University Press.CrossRefGoogle Scholar
Bartkowska, K (1973) Siphonaptera Tatr Polskich. Fragm Faun Pol Akad Nauk Inst Zool 10, 227–281 (in Polish).Google Scholar
Bates, D, Maechler, M, Bolker, B and Walker, S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.CrossRefGoogle Scholar
Beer, JR, Cook, EF and Schwab, RG (1959) The ectoparasites of some mammals from the Chiricahua Mountains, Arizona. The Journal of Parasitology 45, 605–613.CrossRefGoogle ScholarPubMed
Benton, AH and Altmann, HJ (1964) A study of fleas found on peromyscus in New York. Journal of Mammalogy 45, 31–36.CrossRefGoogle Scholar
Bonnefoy, X, Kampen, H and Sweeney, K (2008) Public Health Significance of Urban Pests. World Health Organization.Google Scholar
Brinck-Lindroth, G and Smit, FGAM (2007) The Fleas (Siphonaptera) of Fennoscandia and Denmark. Brill.CrossRefGoogle Scholar
Caminade, C, Kovats, S, Rocklov, J, Tompkins, AM, Morse, AP, Colón-González, FJ, Stenlund, H, Martens, P and Lloyd, SJ (2014) Impact of climate change on global malaria distribution. Proceedings of the National Academy of Sciences 111, 3286–3291.CrossRefGoogle ScholarPubMed
Combes, C (2001) Parasitism: The Ecology and Evolution of Intimate Interactions. Chicago and London: The University of Chicago Press.Google Scholar
Cox, TF and Cox, MA (2000) Multidimensional Scaling. Chapman and Hall/CRC.Google Scholar
Darskaya, NF (1970) Ecological comparisons of some fleas of the USSR fauna. Zoologicheskii Zhurnal 49, 729–745.Google Scholar
De Oliveira, GMB, da Silva, IW, Evaristo, AMCF, Serpa, MCAS, Campos, ANS, Dutra, V, Nakazato, L, de Aguiar, DM, Labruna, MB and Horta, MC (2020) Tick-borne pathogens in dogs, wild small mammals and their ectoparasites in the semi-arid Caatinga biome, northeastern Brazil. Ticks and Tick-borne Diseases 11, 101409.CrossRefGoogle ScholarPubMed
Dudich, A (1987) Flea synusias (Siphonaptera: Insecta) of alpine shrew (Sorex alpinus Schinz, 1837) in Western Carpathians. Biológia (Bratislava) 42, 603–616. [in Slovak].Google Scholar
Dudich, A (1989) Contribution to the knowledge of ectoparasites of small mammals of the Trnava Uplands and the Little Carpathians. Zborník Odborných Prác 6. Západoslovenského TOP-u 5, 76–91 (in Slovak).Google Scholar
Dudich, A (1992) Quantitative structure of the synthesis of ectoparasites of small mammals of the supramontaneous vegetation stage of the Western Tatras. Zborník prác o Tatranskom Národnom parku 32, 149–164 (in Slovak).Google Scholar
Dudich, A (1995) Synecological Study of Ectoparasites of Small Mammals of Spruce Forests in the Middle Beskydy. Technická univerzita vo Zvolene (in Slovak).Google Scholar
Eisen, RJ, Borchert, JN, Mpanga, JT, Atiku, LA, MacMillan, K, Boegler, KA, Montenieri, JA, Monaghan, A and Gage, KL (2012) Flea diversity as an element for persistence of plague bacteria in an East African plague focus. PLoS ONE 7, e35598.CrossRefGoogle Scholar
Fischer, A, Blaschke, M and Bässler, C (2011) Altitudinal gradients in biodiversity research: the state of the art and future perspectives under climate change aspects. Waldökologie, Landschaftsforschung und Naturschutz 11, 35–47.Google Scholar
Futák, J (1972) Fytogeografický prehľad Slovenska. Slovensko 2, 431–482 (in Slovak).Google Scholar
Gong, Z, Wu, H, Duan, X, Feng, X, Zhang, Y and Liu, Q (2005) Species richness and vertical distribution pattern of flea fauna in Heng-duan Mountains of western Yunnan, China. Biodiversity Science 13, 279–289.CrossRefGoogle Scholar
Grytnes, JA and McCain, CM (2007) Elevational trends in biodiversity. Encyclopedia of Biodiversity 5, 1–8.Google Scholar
Herczeg, R and Horváth, GF (2015) Species composition and nestedness of small mammal assemblages in two disturbed marshlands. North-Western Journal of Zoology 11, 83–193.Google Scholar
Hreško, J, Petrovič, F and Mišovičová, R (2015) Mountain landscape archetypes of the Western Carpathians (Slovakia). Biodiversity and Conservation 24, 3269–3283.CrossRefGoogle Scholar
Izakovičová, Z, Špulerová, J and Petrovič, F (2018) Integrated approach to sustainable land use management. Environments 5, 1–16.CrossRefGoogle Scholar
Jetz, W and Rahbek, C (2002) Geographic range size and determinants of avian species richness. Science (New York, N.Y.) 297, 1548–1551.CrossRefGoogle ScholarPubMed
Kamenišťák, J, Baláž, I, Tulis, F, Jakab, I, Ševčík, M, Poláčiková, Z, Klimant, P, Ambros, M and Rychlik, L (2019) Changes of small mammal communities with the altitude gradient. Biologia 74, 1–10.Google Scholar
Kelt, DA, Meserve, PL and Lang, BK (1994) Quantitative Habitat Associations of Small Mammals in a Temperate Rainforest in Southern Chile: Empirical Patterns and the Importance of Ecological Scale. https://doi.org/10.2307/1382471.CrossRefGoogle Scholar
Kraljik, J, Paziewska-Harris, A, Miklisová, D and Blaňarová, L (2016) Genetic diversity of Bartonella genotypes found in the striped field mouse (Apodemus agrarius) in Central Europe. Parasitology 143, 1437–1442.CrossRefGoogle Scholar
Krasnov, BR (2008) Functional and Evolutionary Ecology of Fleas: A Model for Ecological Parasitology. New York: Cambridge University Press.CrossRefGoogle Scholar
Krasnov, BR, Shenbrot, GI, Medvedev, SG, Vatschenok, VS and Khokhlova, IS (1997) Host-habitat relations as an important determinant of spatial distribution of flea assemblages (Siphonaptera). In On Rodents in the Negev Desert. Parasitology 114, 159–173.CrossRefGoogle Scholar
Krasnov, B, Shenbrot, G, Khokhlova, I, Medvedev, S and Vatschenok, V (1998) Habitat dependence of a parasite-host relationship: flea (Siphonaptera) assemblages in two gerbil species of the Negev Desert. Journal of Medical Entomology 35, 303–313.CrossRefGoogle ScholarPubMed
Krasnov, BR, Shenbrot, GI, Khokhlova, IS and Degen, AA (2004) Relationship between host diversity and parasite diversity: flea assemblages on small mammals. Journal of Biogeography 31, 1857–1866.CrossRefGoogle Scholar
Krasnov, BR, Shenbrot, GI, Mouillot, D, Khokhlova, IS and Poulin, R (2005) What are the factors determining the probability of discovering a flea species (Siphonaptera)? Parasitology Research 97, 228–237.CrossRefGoogle ScholarPubMed
Krasnov, BR, Stanko, M, Miklisova, D and Morand, S (2006) Habitat variation in species composition of flea assemblages on small mammals in central Europe. Ecological Research 21, 460–469.CrossRefGoogle Scholar
Krasnov, BR, Shenbrot, GI, Khokhlova, IS and Poulin, R (2007) Geographical variation in the ‘bottom-up’ control of diversity: fleas and their small mammalian hosts. Global Ecology and Biogeography 16, 179–186.CrossRefGoogle Scholar
Kratochvíl, J and Pelikán, J (1955) Notes on the arrival of the field vole in the Tatra National Park. Zoologické a entolomogické listy 4, 303–312 (in Czech).Google Scholar
Kurucz, K, Madai, M, Bali, D, Hedericz, D, Horváth, G, Kemenesi, G and Jacab, F (2018) Parallel survey of two widespread renal syndrome-causing zoonoses: Leptospira spp. and hantavirus in urban environment, Hungary. Vector-Borne and Zoonotic Diseases 18, 200–205.CrossRefGoogle ScholarPubMed
Kuznetsova, A, Brockhoff, PB and Christensen, RHB (2017) Lmertest package: tests in linear mixed effects models. Journal of Statistical Software 82, 1–26.CrossRefGoogle Scholar
Lomolino, MV (2001) Elevation gradients of species-density: historical and prospective views. Global Ecology and Biogeography 10, 3–13.CrossRefGoogle Scholar
Maestri, R, Shenbrot, GI and Krasnov, BR (2017) Parasite beta diversity, host beta diversity and environment: application of two approaches to reveal patterns of flea species turnover in Mongolia. Journal of Biogeography 44, 1880–1890.CrossRefGoogle Scholar
Magurran, AE (2004) Measuring Biological Diversity. Oxford, UK: Blackwell Science Ltd.Google Scholar
Maher, SP and Timm, RM (2014) Patterns of host and flea communities along an elevational gradient in Colorado. Canadian Journal of Zoology 92, 433–442.CrossRefGoogle Scholar
Mahnert, V (1972) Zum auftreten von Kleinsäuger-Flöhen auf ihren wirten in Abhängigkeit von Jahreszeit und Höhenstufen. Oecologia 8, 400–418.CrossRefGoogle Scholar
Marshall, AG (1981) The Ecology of Ectoparasitic Insects. Academic Press Inc. (London) Ltd.Google Scholar
McCain, CM (2004) The mid-domain effect applied to elevational gradients: species richness of small mammals in Costa Rica: species richness of small mammals along an elevational gradient. Journal of Biogeography 31, 19–31.CrossRefGoogle Scholar
McCain, CM (2005) Elevational gradients in diversity of small mammals. Ecology 86, 366–372.CrossRefGoogle Scholar
McCain, CM and Grytnes, JA (2010) Elevational gradients in species richness. In Chichester., W (ed.), Encyclopedia of Life Sciences. John Wiley & Sons, Ltd., pp. 1–10.Google Scholar
McCoy, ED (1990) The distribution of insects along elevational gradients. Oikos, 313–322.CrossRefGoogle Scholar
Meliyo, JL, Kimaro, DN, Msanya, BM, Mulungu, LS, Hieronimo, P, Kihupi, NI, Gulinck, H and Deckers, JA (2014) Predicting small mammal and flea abundance using landform and soil properties in a plague endemic area in Lushoto District, Tanzania. Tanzania Journal of Health Research 16, 161–172.CrossRefGoogle Scholar
Mena, JL and Medellín, RA (2017) Habitat complexity and small mammal diversity along an elevational gradient in southern Mexico. Mastozoología Neotropical 24, 121–134.Google Scholar
Mérő, TO, Lotnay, L and Lengyel, S (2015) Habitat management varying in space and time: the effects of grazing and fire management on marshland birds. Journal of Ornithology 156, 579–590.CrossRefGoogle Scholar
Oksanen, J, Blanchet, FG, Friendly, M, Kindt, R, Legendre, R, McGlinn, D, Minchin, PR, O'Hara, RB, Simpson, GL, Solymos, P, Stevens, MHH, Szoecs, E and Wagner, H (2019) vegan: Community Ecology Package. R package version 2.5-6. https://CRAN.R-project.org/package=vegan.Google Scholar
Petluš, P and Vanková, V (2009) The potential of landscape visual exposure for using of character landscape image evaluation. Physics and Geographical Magazine 7, 57–61.Google Scholar
Poulin, R (2007) Evolutionary Ecology of Parasites. Princeton University Press.CrossRefGoogle Scholar
Price, PW (1990) Host populations as resources defining parasite community organization. In Esch, GW, Bush, AO and Aho, JM (eds), Parasite Communities: Patterns and Processes. Dordrecht: Springer, pp. 21–40.CrossRefGoogle Scholar
Rahbek, C (1995) The elevational gradient of species richness: a uniform pattern? Ecography, 200–205.CrossRefGoogle Scholar
Rahbek, C and Graves, GR (2001) Multiscale assessment of patterns of avian species richness. PNAS 98, 4534–4539.CrossRefGoogle ScholarPubMed
R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Rosicky, B (1957) Fauna of the CSR, Volume 10: Fleas – Aphaniptera. Nakladatelstvi Československé Akademie Ved, Praha (in Czech).Google Scholar
Sapegina, VF (2000) Distribution of fleas (Siphonaptera) parasitizing of small mammals in Western Siberia. In Biodiversity and Dynamics of Ecosystems in North Eurasia. pp. 94–96.Google Scholar
Skuratowicz, W (1967) Fleas – Siphonaptera (Aphaniptera). Państwowe Wydawnictwo Naukowe (in Polish).Google Scholar
Slovak Hydrometeorological Institute (2020) Slovak Hydrometeorological Institute. SHMÚ.sk – Meteo/Počasie/Hydrológia/Kvalita ovzdušia.Google Scholar
Stanko, M (2014) Methods of Ecological Research of Small Mammals. Košice: Parazitologický ústav SAV (in Slovak).Google Scholar
Súľovský, M, Falťan, V, Skokanová, H, Havlíček, M and Petrovič, F (2017) Spatial analysis of long-term land-use development in regard to physiotopes: case studies from the Carpathians. Physical Geography 38, 470–488.CrossRefGoogle Scholar
Theodor, O and Costa, M (1967) A Survey of the Parasites of Wild Mammals and Birds in Israel. Part one. Ectoparasites. Jerusalem: The Israel Academy of Sciences and Humanities, London: H. A. Humphrey Ltd., 5, Great Russell Street, W.C.1.Google Scholar
Vatschenok, VS (1988) Fleas–Vectors of Pathogens Causing Diseases in Humans and Animals. Leningrad, USSR: Nauka Publishing House (in Russian).Google Scholar
Wang, Y, Naumann, U, Eddelbuettel, D, Wilshire, J and Warton, D (2020) mvabund: Statistical methods for analysing multivariate abundance data.Google Scholar