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Assessing bat droppings and predatory bird pellets for vector-borne bacteria: molecular evidence of bat-associated Neorickettsia sp. in Europe

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Abstract

In Europe, several species of bats, owls and kestrels exemplify highly urbanised, flying vertebrates, which may get close to humans or domestic animals. Bat droppings and bird pellets may have epidemiological, as well as diagnostic significance from the point of view of pathogens. In this work 221 bat faecal and 118 bird pellet samples were screened for a broad range of vector-borne bacteria using PCR-based methods. Rickettsia DNA was detected in 13 bat faecal DNA extracts, including the sequence of a rickettsial insect endosymbiont, a novel Rickettsia genotype and Rickettsia helvetica. Faecal samples of the pond bat (Myotis dasycneme) were positive for a Neorickettsia sp. and for haemoplasmas of the haemofelis group. In addition, two bird pellets (collected from a Long-eared Owl, Asio otus, and from a Common Kestrel, Falco tinnunculus) contained the DNA of a Rickettsia sp. and Anaplasma phagocytophilum, respectively. In both of these bird pellets the bones of Microtus arvalis were identified. All samples were negative for Borrelia burgdorferi s.l., Francisella tularensis, Coxiella burnetii and Chlamydiales. In conclusion, bats were shown to pass rickettsia and haemoplasma DNA in their faeces. Molecular evidence is provided for the presence of Neorickettsia sp. in bat faeces in Europe. In the evaluated regions bat faeces and owl/kestrel pellets do not appear to pose epidemiological risk from the point of view of F. tularensis, C. burnetii and Chlamydiales. Testing of bird pellets may provide an alternative approach to trapping for assessing the local occurrence of vector-borne bacteria in small mammals.

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Acknowledgements

The study was organised in the Framework of EurNegVec COST action TD1303. Molecular biology work was partially performed using the logistics of the Center for Clinical Studies at the Vetsuisse Faculty of the University of Zurich.

Funding

DNA extractions and molecular analysis of A. phagocytophilum were supported by OTKA 115854. MG and KMS were supported by the Momentum Programme (LP2012-22) of the Hungarian Academy of Sciences.

Data availability

The sequences generated during the current study are available in the GenBank Repository, under accession numbers KP862896 [N. risticii], MF347694 and MF347695 [Rickettsia spp.]. All other relevant data are contained in the manuscript.

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Authors and Affiliations

  1. Department of Parasitology and Zoology, University of Veterinary Medicine, Budapest, 1078, Hungary

    Sándor Hornok, Krisztina Szőke, Sándor Szekeres & Nóra Takács

  2. Department of Zoology, Eszterházy Károly University, Eger, 3300, Hungary

    Péter Estók

  3. Centre for Infectious Disease Control, National Institute for Public Health and the Environment (RIVM), 3721, Bilthoven, The Netherlands

    Aleksandra Krawczyk, Arnout de Bruin & Hein Sprong

  4. Department of Animal Ecology and Ecophysiology, Radboud University Nijmegen, 6500 HC, Nijmegen, The Netherlands

    Anne-Jifke Haarsma

  5. Department of Evolutionary Zoology and Human Biology, Debrecen University, Debrecen, 4010, Hungary

    Dávid Kováts

  6. Department of Nature Conservation, Aggtelek National Park Directorate, Jósvafő, 3758, Hungary

    Sándor A. Boldogh

  7. Hungarian Ornithological and Nature Conservation Society, Budapest, 1125, Hungary

    Pál Morandini

  8. Plant Protection Institute, Centre for Agricultural Research, Hungarian Academy of Sciences, Budapest, 1022, Hungary

    Jenő Kontschán

  9. Clinical Laboratory and Center for Clinical Studies, Vetsuisse Faculty, University of Zürich, 8057, Zurich, Switzerland

    Marina L. Meli, Beatrice Weibel, Enikő Gönczi & Regina Hofmann-Lehmann

  10. SaBio, Instituto de Investigación en Recursos Cinegéticos (IREC-CSIC-UCLM-JCCLM), 13005, Ciudad Real, Spain

    Isabel G. Fernández de Mera & José de la Fuente

  11. Department of Veterinary Pathobiology, Center for Veterinary Health Sciences, Oklahoma State University, Stillwater, OK, 74078, USA

    José de la Fuente

  12. Institute for Veterinary Medical Research, Centre for Agricultural Research, Hungarian Academy of Sciences, Budapest, 1143, Hungary

    Miklós Gyuranecz & Kinga M. Sulyok

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  1. Sándor Hornok
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  2. Krisztina Szőke
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  3. Péter Estók
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  4. Aleksandra Krawczyk
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  5. Anne-Jifke Haarsma
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  6. Dávid Kováts
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  7. Sándor A. Boldogh
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  8. Pál Morandini
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  9. Sándor Szekeres
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  10. Nóra Takács
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  11. Jenő Kontschán
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  12. Marina L. Meli
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  13. Isabel G. Fernández de Mera
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  14. José de la Fuente
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  15. Miklós Gyuranecz
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  16. Kinga M. Sulyok
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  17. Beatrice Weibel
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  18. Enikő Gönczi
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  19. Arnout de Bruin
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  20. Hein Sprong
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  21. Regina Hofmann-Lehmann
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Corresponding author

Correspondence to Sándor Hornok.

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Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. Authorisation for bat capture was provided by the National Inspectorate for Environment, Nature and Water (No. 14/2138-7/2011). Bat banding licence numbers are TMF-14/32/2010 (DK) and 59/2003 (PE). Birds were not handled during the study, therefore no ethical approval was necessary for the collection of bird pellets (i.e., these were found exclusively in the resting sites of birds).

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Informed consent was obtained from all individual participants included in the study.

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Hornok, S., Szőke, K., Estók, P. et al. Assessing bat droppings and predatory bird pellets for vector-borne bacteria: molecular evidence of bat-associated Neorickettsia sp. in Europe. Antonie van Leeuwenhoek 111, 1707–1717 (2018). https://doi.org/10.1007/s10482-018-1043-7

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