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Ectoparasites of Cave-Dwelling Bat Species in Bulgaria

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Abstract

The unique ecological conditions of Bulgarian caves allow them to be used by bats year-round, thereby providing an interesting model for research on host-parasite interactions, including the potential for transmission of different zoonotic pathogens. In this study, 142 cave-dwelling bats of thirteen species were caught in seven Bulgarian caves and examined for presence of ectoparasites. Bats were mist-netted at cave entrances between May 2020 and May 2021. All macroscopically visible ectoparasites were collected from each bat and stored separately in 96% ethanol. The greatest diversity of bat ticks, flies and fleas was observed on greater horseshoe bats Rhinolophus ferrumequinum and common bent-wing bats Miniopterus schreibersii. Spinturnix myoti was the dominant ectoparasite collected at almost all localities and in all bat species. There was no significant difference in parasite load or diversity between the four most abundant bat species, each being infested with two specimens of a single parasite species on average. Though Bulgarian caves are used year-round by a range of bat species, parasite load and diversity remain low during the hibernation and migration periods. Mixed clusters of bats allow for inter-specific transmission of otherwise species-specific ectoparasites.

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References

  • Balvín, O., T. Bartonička, N. Simov, M. Paunović, and J. Vilímova. 2014. Distribution and host relations of species of the genus Cimex on bats in Europe. Folia Zoologica 63: 281–289.

    Article  Google Scholar 

  • Beĭ-Bienko, G.I.A. 1970. Keys to the insects of the European part of the USSR: Diptera and Siphonaptera, vol. V. Leningrad: Nauka (In Russian).

    Google Scholar 

  • Beron, P. 2015. Cave fauna of Bulgaria, 450. Delhi: East-West Publishing.

    Google Scholar 

  • Beron, P., B. Petrov, and P. Stoev. 2011. The invertebrate cave fauna of the Western Rhodopes (Bulgaria and Greece). In Biodiversity of Bulgaria 4. Biodiversity of Western Rhodopes (Bulgaria and Greece) II, ed. P. Beron, 583–660. Sofia: Pensoft & National Museum of Natural History.

    Google Scholar 

  • Bruyndonckx, N., S. Dubey, M. Ruedi, and P. Christe. 2009. Molecular cophylogenetic relationships between European bats and their ectoparasitic mites (Acari, Spinturnicidae). Molecular Phylogenetics and Evolution 51: 227–237.

    Article  CAS  Google Scholar 

  • Christe, P., R. Arlettaz, and P. Vogel. 2000. Variation in intensity of a parasitic mite (Spinturnix myoti) in relation to the reproductive cycle and immunocompetence of its bat host (Myotis myotis). Ecology Letters 3: 207–212.

    Article  Google Scholar 

  • Christe, P., M.S. Giorgi, P. Vogel, and R. Arlettaz. 2003. Differential species-specific ectoparasitic mite intensities in two intimately coexisting sibling bat species: resource-mediated host attractiveness or parasite specialization? Journal of Animal Ecology 72: 866–872.

    Article  Google Scholar 

  • Dick, C.W., and B.D. Patterson. 2006. Bat flies-obligate ectoparasites of bats. In Micromammals and macroparasites: from evolutionary ecology to management, ed. S. Morand, B.R. Krasnov, and R. Poulin, 179–194. Tokyo: Springer-Verlag.

    Chapter  Google Scholar 

  • Estrada-Peña, A., A.D. Mihalca, and T.N. Petney. 2017. Ticks of Europe and North Africa: a guide to species identification, 404. Cham: Springer.

    Book  Google Scholar 

  • Giorgi, M.S., R. Arlettaz, F. Guillaume, S. Nussle, C. Ossola, P. Vogel, and P. Christe. 2004. Causal mechanisms underlying host specificity in bat ectoparasites. Oecologia 138: 648–654.

    Article  Google Scholar 

  • Hutson, A.M. 1984. Handbooks for the identification of British insects. Diptera, Hippoboscidae and Nycteribiidae, vol. 5. St Albans: Royal Entomological Society.

    Google Scholar 

  • Krištofík, J., and Š Danko. 2012. Arthropod ectoparasites (Acarina, Heteroptera, Diptera, Siphonaptera) of bats in Slovakia. Vespertilio 16: 167–189.

    Google Scholar 

  • Lourenço, S.I., and J.M. Palmeirim. 2007. Can mite parasitism affect the condition of bat hosts? implications for the social structure of colonial bats. Journal of Zoology 273: 161–168.

    Article  Google Scholar 

  • Lourenço, S.I., and J.M. Palmeirim. 2008. Which factors regulate the reproduction of ectoparasites of temperate zone cave-dwelling bats? Parasitology Research 104: 127–134.

    Article  Google Scholar 

  • Lučan, R.K. 2006. Relationships between the parasitic mite Spinturnix andegavinus (Acari: Spinturnicidae) and its bat host, Myotis daubentonii (Chiroptera: Vespertilionidae): seasonal, sex- and age-related variation in infestation and possible impact of the parasite on the host condition and roosting behaviour. Folia Parasitologica (ceske Budejovice) 53: 147–152.

    Article  Google Scholar 

  • Lučan, R.K., H. Bandouchova, T. Bartonička, J. Pikula, A. Zahradníková Jr., J. Zukal, and N. Martínková. 2016. Ectoparasites may serve as vectors for the white-nose syndrome fungus. Parasite Vectors 9: 16.

    Article  Google Scholar 

  • Orlova, M.V., M.K. Stanyukovich, and O.L. Orlov. 2015. Gamasid mites (Mesostigmata: Gamasina) parasitizing bats (Chiroptera: Rhinolophidae, Vespertilionidae, Molossidae) of Palaearctic boreal zone (Russia and adjacent countries). Tomsk: TSU Publishing House.

    Google Scholar 

  • Orlova, M.V., O.L. Orlov, D.V. Kazakov, and A.V. Zhigalin. 2017. Approaches to the identification of ectoparasite complexes of bats (Chiroptera: Vespertilionidae, Miniopteridae, Rhinolophidae, Molossidae) in the Palearctic. Entomological Review 97: 684–701.

    Article  Google Scholar 

  • Petrov, B. 2008. Bats – methodology for environmental impact assessment and appropriate assessment. A manual for developers, environmental experts and planning authorities. National Museum of Natural History-BAS pp. 88. https://www.moew.government.bg/static/media/ups/tiny/filebase/Nature/Biodiversity/Preporyki%20Rykowodstwa%20Dokladi/Prilepite_BG.pdf

  • Postawa, T., and A. Furman. 2014. Abundance patterns of Ectoparasites infesting different populations of Miniopterus species in their contact zone in Asia minor. Acta Chiropterologica 16 (2): 387–395.

    Article  Google Scholar 

  • Rodrigues, L., A. Zahn, A. Rainho, and J.M. Palmeirim. 2003. Contrasting the roosting behaviour and phenology of an insectivorous bat (Myotis myotis) in its southern and northern distribution ranges. Mammalia 67 (3): 321–336.

    Article  Google Scholar 

  • Sándor, A.D., A. Corduneanu, Á. Péter, A.D. Mihalca, L. Barti, I. Csősz, K. Szőke, and S. Hornok. 2019. Bats and ticks: host selection and seasonality of bat-specialist ticks in eastern Europe. Parasites & Vectors 12: 605.

    Article  Google Scholar 

  • Sharifi, M., F. Mozafari, N. Taghinezhad, and H. Javanbakht. 2008. Variation in Ectoparasite load reflects life history traits in the lesser mouse-eared bat Myotis blythii (Chiroptera: Vespertilionidae) in Western Iran. Journal of Parasitology 94 (3): 622–625.

    Article  Google Scholar 

  • Simov, N., T. Ivanova, and I. Schunger. 2006. Bat-parasitic Cimex species (Hemiptera: Cimicidae) on the Balkan Peninsula, with zoogeographical remarks on Cimex lectularius, Linnaeus. Zootaxa 1190: 59–68.

    Article  Google Scholar 

  • Skirmuntt, E.C., M. Escalera-Zamudio, E.C. Teeling, A. Smith, and A. Katzourakis. 2020. The potential role of endogenous viral elements in the evolution of bats as reservoirs for zoonotic viruses. Annual Review of Virology 7: 103–119.

    Article  CAS  Google Scholar 

  • Uhrin, M., P. Kaňuch, J. Krištofík, and L. Paule. 2010. Phenotypic plasticity in the greater mouse-eared bat in extremely different roost conditions. Acta Theriologica 55: 153–164.

    Article  Google Scholar 

  • Zahradníková, A., V. Kovacova, N. Martínková, M.V. Orlova, O.L. Orlov, V. Piacek, J. Zukal, and J. Pikula. 2018. Historic and geographic surveillance of Pseudogymnoascus destructans possible from collections of bat parasites. Transboundary and Emerging Diseases 65: 303308.

    Article  Google Scholar 

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Acknowledgements

We are grateful to Dr. Kevin Roche for correction and improvement of the English text. This research was supported by the Bulgarian National Science Fund (Grant No. KП-06-H31/14).

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Authors and Affiliations

  1. National Centre of Infectious and Parasitic Diseases, 26 Yanko Sakazov Blvd., 1504, Sofia, Bulgaria

    Nadya Ivanova-Aleksandrova, Radoslava Emilova & Irina Georgieva

  2. Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, 1 Tsar Osvoboditel Blvd., 1000, Sofia, Bulgaria

    Heliana Dundarova & Boyko Neov

  3. Faculty of Biology, Sofia University “St. Kliment Ohridski”, 8 Dragan Tsankov Blvd., 1164, Sofia, Bulgaria

    Rayna Antova

  4. Faculty of Biology, University of Plovdiv “Paisii Hilendarski”, 24 Tzar Assen’’ str., 4000, Plovdiv, Bulgaria

    Krasimir Kirov

  5. Department of Ecology and Diseases of Zoo Animals, Game, Fish and Bees, University of Veterinary Sciences Brno, Palackého tř. 1946/1, 612 42, Brno, Czech Republic

    Jiri Pikula & Kateřina Zukalová

  6. Institute of Vertebrate Biology of the Czech Academy of Sciences, Květná 8, 603 65, Brno, Czech Republic

    Jan Zukal

Authors
  1. Nadya Ivanova-Aleksandrova
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  2. Heliana Dundarova
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  4. Radoslava Emilova
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  5. Irina Georgieva
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Contributions

HD and JZ conceived and designed the study; HD organised the field trips and collected material, with support from RG, IG, RA, KK, JP, JZ and KZ; NIA performed ectoparasite analysis; HD, KZ and JZ analysed the data and drafted the manuscript, to which all authors contributed with critical comments.

Corresponding author

Correspondence to Heliana Dundarova.

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Ivanova-Aleksandrova, N., Dundarova, H., Neov, B. et al. Ectoparasites of Cave-Dwelling Bat Species in Bulgaria. Proc Zool Soc 75, 463–468 (2022). https://doi.org/10.1007/s12595-022-00451-4

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  • DOI: https://doi.org/10.1007/s12595-022-00451-4

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