Microbial Ecology

, Volume 76, Issue 4, pp 1076–1088 | Cite as

Eco-epidemiology of Novel Bartonella Genotypes from Parasitic Flies of Insectivorous Bats

  • Attila D. Sándor
  • Mihály Földvári
  • Aleksandra I. Krawczyk
  • Hein Sprong
  • Alexandra Corduneanu
  • Levente Barti
  • Tamás Görföl
  • Péter Estók
  • Dávid Kováts
  • Sándor Szekeres
  • Zoltán László
  • Sándor Hornok
  • Gábor FöldváriEmail author
Host Microbe Interactions


Bats are important zoonotic reservoirs for many pathogens worldwide. Although their highly specialized ectoparasites, bat flies (Diptera: Hippoboscoidea), can transmit Bartonella bacteria including human pathogens, their eco-epidemiology is unexplored. Here, we analyzed the prevalence and diversity of Bartonella strains sampled from 10 bat fly species from 14 European bat species. We found high prevalence of Bartonella spp. in most bat fly species with wide geographical distribution. Bat species explained most of the variance in Bartonella distribution with the highest prevalence of infected flies recorded in species living in dense groups exclusively in caves. Bat gender but not bat fly gender was also an important factor with the more mobile male bats giving more opportunity for the ectoparasites to access several host individuals. We detected high diversity of Bartonella strains (18 sequences, 7 genotypes, in 9 bat fly species) comparable with tropical assemblages of bat-bat fly association. Most genotypes are novel (15 out of 18 recorded strains have a similarity of 92–99%, with three sequences having 100% similarity to Bartonella spp. sequences deposited in GenBank) with currently unknown pathogenicity; however, 4 of these sequences are similar (up to 92% sequence similarity) to Bartonella spp. with known zoonotic potential. The high prevalence and diversity of Bartonella spp. suggests a long shared evolution of these bacteria with bat flies and bats providing excellent study targets for the eco-epidemiology of host-vector-pathogen cycles.


Chiroptera Bartonella Bat Fly Host-parasite Coevolution Nycteribiidae Pathogen Diversity 



Permission for bat capture was provided by the National Inspectorate for Environment, Nature and Water (Hungary), and the Underground Heritage Commission (Romania). Bat banding license numbers are 59/2003 (PE), 305/2015 (ADS), and TMF-493/3/2005 (TG). No live bat was harmed for this study. The authors thank C. Jére, I. Csősz, D. Bălășoiu, A. Telea, and A. Ionică for their contribution in the bat fly collection in Romania. We would like to express our thanks to Cristian Domșa for the help provided in the creation of the maps in Figs. 1 and 6. The survey was organized in the framework of the EurNegVec COST Action TD1303. This research was supported from the grant PN-II-RU-TE-2014-4-1389, the grant “In the light of evolution: theories and solutions” (GINOP-2.3.2-15-2016-00057), and the János Bolyai Research Scholarship of the Hungarian Academy of Science (to ADS and GF).

Authors’ Contributions

ADS initiated the study, did part of the sample collection, and wrote the manuscript. LB, AC, SH, TG, PE, ZL, and DK contributed important samples to the study. MF identified all bat flies. AK, SSz, and HS performed the molecular and phylogenetic analyses. GF organized part of the sample collection and contributed to the study design and manuscript preparation. All authors read and approved the final version of the manuscript.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary material

248_2018_1195_MOESM1_ESM.pdf (66 kb)
Figure S1 Neighbor-joining phylogenetic tree based on the multiple alignment of the gltaA gene, including Bartonella sequences obtained in this study. Clusters were assigned based on visual inspection of the tree. (PDF 65 kb)
248_2018_1195_MOESM2_ESM.pdf (31 kb)
Supplementary Figure S2 Neighbor-joining phylogenetic tree based on the pairwise alignment of an approx. 360 bp long fragment of the gltaA gene, including representative Bartonella sequences obtained in this study (highlighted by green fonts and 5 character codes) and representative sequences of other Bartonella spp. retrieved from GenBank. Sequences in blue represent Bartonella spp. related to bats or bat flies, while sequences in black denote Bartonella spp. from other host species, Bartonella spp. with known pathogenicity are highlighted in bold. (PDF 31 kb)
248_2018_1195_MOESM3_ESM.xlsx (11 kb)
Table S1 (XLSX 11 kb)
248_2018_1195_MOESM4_ESM.xlsx (36 kb)
Table S2 (XLSX 35 kb)
248_2018_1195_MOESM5_ESM.xlsx (11 kb)
Table S3 (XLSX 10 kb)
248_2018_1195_MOESM6_ESM.docx (15 kb)
Table S4 (DOCX 15 kb)
248_2018_1195_MOESM7_ESM.xlsx (11 kb)
Table S5 (XLSX 10 kb)


  1. 1.
    Tsang SM, Cirranello AL, Bates PJ, Simmons NB (2015) The roles of taxonomy and systematics in bat conservation. In: Voigt CC, Kingston T (eds) Bats in the Anthropocene: conservation of bats in a changing world. Springer International Publishing, pp 503–538Google Scholar
  2. 2.
    Teeling EC (2009) A molecular phylogeny for bats illuminates biogeography and the fossil record a molecular phylogeny for bats illuminates biogeography and the fossil record. Notes 307:580–584. CrossRefGoogle Scholar
  3. 3.
    Haelewaters D, Pfliegler WP, Szentiványi T, Földvári M, Sándor AD, Barti L, Camacho JJ, Gort G, Estók P, Hiller T, Dick CW, Pfister DH (2017) Parasites of parasites of bats: Laboulbeniales (Fungi: Ascomycota) on bat flies (Diptera: Nycteribiidae) in Central Europe. Parasit. Vectors 10:96. CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Dick CW, Patterson BD (2006) Bat flies-obligate ectoparasites of bats. In: Morand S, Krasnov BR, RP (eds) Micromammals and macroparasites: from evolutionary ecology to management. Springer-Verlag, Tokyo Berlin Heidelberg New York, pp 179–194CrossRefGoogle Scholar
  5. 5.
    Dick CW, Dittmar K (2014) Parasitic bat flies (Diptera: Streblidae and Nycteribiidae): host specificity and potential as vectors. In: Klimpel SMH (ed) Bats (Chiroptera) as vectors of diseases and parasites. Springer-Verlag, Berlin Heidelberg, pp 131–151CrossRefGoogle Scholar
  6. 6.
    Plowright RK, Eby P, Hudson PJ, Smith IL, Westcott D, Bryden WL, Middleton D, Reid PA, McFarlane RA, Martin G, Tabor GM, Skerratt LF, Anderson DL, Crameri G, Quammen D, Jordan D, Freeman P, Wang LF, Epstein JH, Marsh GA, Kung NY, McCallum H (2015) Ecological dynamics of emerging bat virus spillover. Proc. R. Soc. B Biol. Sci. 282:20142124. CrossRefGoogle Scholar
  7. 7.
    Mühldorfer K (2013) Bats and bacterial pathogens: a review. Zoonoses Public Health 60:93–103. CrossRefPubMedGoogle Scholar
  8. 8.
    Hornok S, Szőke K, Kováts D, Estók P, Görföl T, Boldogh SA, Takács N, Kontschán J, Földvári G, Barti L, Corduneanu A, Sándor AD (2016) DNA of piroplasms of ruminants and dogs in ixodid bat ticks. PLoS One 11:e0167735. CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Corduneanu A, Hrazdilová K, Sándor AD, et al (2017) Babesia vesperuginis, a neglected piroplasmid: new host and geographical records, and phylogenetic relations. Parasit. Vectors 10:598.
  10. 10.
    Hornok S, Szőke K, Tu VT, Kontschán J, Takács N, Sándor AD, Halajian A, Földvári G, Estók P, Plantard O, Epis S, Görföl T (2017) Mitochondrial gene heterogeneity of the bat soft tick Argas vespertilionis (Ixodida: Argasidae) in the Palaearctic. Parasit. Vectors 10:109. CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Gibson KE, Rikihisa Y, Zhang C, Martin C (2005) Neorickettsia risticii is vertically transmitted in the trematode Acanthatrium oregonense and horizontally transmitted to bats. Environ. Microbiol. 7:203–212. CrossRefPubMedGoogle Scholar
  12. 12.
    Evans NJ, Bown K, Timofte D, Simpson VR, Birtles RJ (2009) Fatal borreliosis in bat caused by relapsing fever spirochete, United Kingdom. Emerg. Infect. Dis. 15:1331–1333CrossRefGoogle Scholar
  13. 13.
    Hosokawa T, Nikoh N, Koga R, Satô M, Tanahashi M, Meng XY, Fukatsu T (2012) Reductive genome evolution, host–symbiont co-speciation and uterine transmission of endosymbiotic bacteria in bat flies. ISME J 6:577–587. CrossRefPubMedGoogle Scholar
  14. 14.
    Lei BR, Olival KJ (2014) Contrasting patterns in mammal-bacteria coevolution: Bartonella and Leptospira in bats and rodents. PLoS Negl. Trop. Dis. 8:e2738. CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Hanson A (1970) Isolation of spirochaetes from primates and other mammalian species. Br J Vener Dis 46:303–306. CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Concannon R, Wynn-Owen K, Simpson VR, Birtles RJ (2005) Molecular characterization of haemoparasites infecting bats (Microchiroptera) in Cornwall, UK. Parasitology 131:489–496. CrossRefPubMedGoogle Scholar
  17. 17.
    Segers FH, Kešnerová L, Kosoy M, Engel P (2017) Genomic changes associated with the evolutionary transition of an insect gut symbiont into a blood-borne pathogen. ISME J 11:1232–1244. CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Boulouis HJ, Chang CC, Henn JB et al (2005) Factors associated with the rapid emergence of zoonotic Bartonella infections. Vet. Res. 36:383–410. CrossRefPubMedGoogle Scholar
  19. 19.
    Chomel BB, Boulouis HJ, Breitschwerdt EB, Kasten RW, Vayssier-Taussat M, Birtles RJ, Koehler JE, Dehio C (2009) Ecological fitness and strategies of adaptation of Bartonella species to their hosts and vectors. Vet. Res. 40:29. CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Breitschwerdt EB (2014) Bartonellosis: one health perspectives for an emerging infectious disease. ILAR J. 55:46–58. CrossRefPubMedGoogle Scholar
  21. 21.
    Kosoy M, Bai Y, Lynch T, Kuzmin IV, Niezgoda M, Franka R, Agwanda B, Breiman RF, Rupprecht CE (2010) Bartonella spp. in bats, Kenya. Emerg. Infect. Dis. 16:1875–1881. CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Bai Y, Hayman DTS, McKee CD, Kosoy MY (2015) Classification of Bartonella strains associated with straw-colored fruit bats (Eidolon helvum) across Africa using a multi-locus sequence typing platform. PLoS Negl. Trop. Dis. 9:e0003478. CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Wilkinson DA, Duron O, Cordonin C, Gomard Y, Ramasindrazana B, Mavingui P, Goodman SM, Tortosa P (2016) The bacteriome of bat flies (Nycteribiidae) from the Malagasy region: a community shaped by host ecology, bacterial transmission mode, and host-vector specificity. Appl. Environ. Microbiol. 82:1778–1788. CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Anh PH, Van Cuong N, Son NT et al (2015) Diversity of bartonella spp. in bats, southern Vietnam. Emerg. Infect. Dis. 21:1266–1267. CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Han HJ, Wen HL, Zhao L, Liu JW, Luo LM, Zhou CM, Qin XR, Zhu YL, Zheng XX, Yu XJ (2017) Novel Bartonella species in insectivorous bats, Northern China. PLoS One 12:e0167915. CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Olival KJ, Dittmar K, Bai Y, Rostal MK, Lei BR, Daszak P, Kosoy M (2015) Bartonella spp. in a Puerto Rican bat community. J. Wildl. Dis. 51:274–278. CrossRefPubMedGoogle Scholar
  27. 27.
    McKee CD, Hayman DTS, Kosoy MY, Webb CT (2016) Phylogenetic and geographic patterns of bartonella host shifts among bat species. Infect Genet Evol 44:382–394. CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Hornok S, Kovács R, Meli ML, Gönczi E, Hofmann-Lehmann R, Kontschán J, Gyuranecz M, Dán Á, Molnár V (2012) First detection of bartonellae in a broad range of bat ectoparasites. Vet. Microbiol. 159:541–543. CrossRefPubMedGoogle Scholar
  29. 29.
    Veikkolainen V, Vesterinen EJ, Lilley TM, Pulliainen AT (2014) Bats as reservoir hosts of human bacterial pathogen, Bartonella mayotimonensis. Emerg. Infect. Dis. 20:960–967. CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Haysom K, Dekker J, Russ J et al (2013) European bat population trends. A prototype biodiversity indicator, Technical. European Environment Agency, BruxellesGoogle Scholar
  31. 31.
    Dietz C, von Helversen O, Nill D (2009) Bats of Britain, Europe and Northwest Africa. A & C Black, LondonGoogle Scholar
  32. 32.
    Theodor O (1967) An illustrated catalogue of the Rothschild collection of Nycteribiidae in the British Museum (Natural History), with keys and short descriptions for the identification of subfamilies, genera, species and subspecies. British Museum (Natural History) Publication 655, LondonGoogle Scholar
  33. 33.
    Theodor O, Moscona A (1954) On bat parasites in Palestine. I. Nycteribiidae, Streblidae, Hemiptera, Siphonaptera. Parasitology 44:157–245. CrossRefPubMedGoogle Scholar
  34. 34.
    Wielinga PR, Gaasenbeek C, Fonville M, de Boer A, de Vries A, Dimmers W, Akkerhuis op Jagers G, Schouls LM, Borgsteede F, van der Giessen JWB (2006) Longitudinal analysis of tick densities and Borrelia, Anaplasma, and Ehrlichia infections of Ixodes ricinus ticks in different habitat areas in the Netherlands. Appl. Environ. Microbiol. 72:7594–7601. CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Norman a F, Regnery R, Jameson P et al (1995) Differentiation of Bartonella-like isolates at the species level by PCR-restriction fragment length polymorphism in the citrate synthase gene. J. Clin. Microbiol. 33:1797–1803PubMedPubMedCentralGoogle Scholar
  36. 36.
    Dormann CF, Frund J, Bluthgen N, Gruber B (2009) Indices, graphs and null models: analyzing bipartite ecological networks. Open Ecol J 2:7–24. CrossRefGoogle Scholar
  37. 37.
    Core Team R (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, VienaGoogle Scholar
  38. 38.
    Bates D, Maechler M, Bolker B, Walker S (2015) lm4: Linear mixded-effects models using Eigen and S4Google Scholar
  39. 39.
    Morse SF, Dick CW, Patterson BD, Dittmard K (2012) Some like it hot: evolution and ecology of novel endosymbionts in bat flies of cave-roosting bats (Hippoboscoidea, Nycterophiliinae). Appl. Environ. Microbiol. 78:8639–8649. CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Morse SF, Olival KJ, Kosoy M et al (2012) Global distribution and genetic diversity of Bartonella in bat flies (Hippoboscoidea, Streblidae, Nycteribiidae). Infect Genet Evol 12:1717–1723. CrossRefPubMedGoogle Scholar
  41. 41.
    Brook CE, Bai Y, Dobson AP, Osikowicz LM, Ranaivoson HC, Zhu Q, Kosoy MY, Dittmar K (2015) Bartonella spp. in fruit bats and blood-feeding ectoparasites in Madagascar. PLoS Negl. Trop. Dis. 10:e0003532. CrossRefGoogle Scholar
  42. 42.
    Billeter S a, Hayman DTS, Peel aJ et al (2012) Bartonella species in bat flies (Diptera: Nycteribiidae) from western Africa. Parasitology 139:324–329. CrossRefPubMedGoogle Scholar
  43. 43.
    Judson SD, Frank HK, Hadly EA (2015) Bartonellae are prevalent and diverse in Costa Rican bats and bat flies. Zoonoses Public Health 62:609–617. CrossRefPubMedGoogle Scholar
  44. 44.
    Dietrich M, Tjale MA, Weyer J, Kearney T, Seamark ECJ, Nel LH, Monadjem A, Markotter W (2016) Diversity of bartonella and rickettsia spp. in bats and their blood-feeding Ectoparasites from South Africa and Swaziland. PLoS One 11:e0152077. CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Stuckey MJ, Boulouis HJ, Cliquet F, Picard-Meyer E, Servat A, Aréchiga-Ceballos N, Echevarría JE, Chomel BB (2017) Potentially zoonotic bartonella in bats from France and Spain. Emerg. Infect. Dis. 23:539–541. CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Szentiványi T, Estók P, Földvári M (2016) Checklist of host associations of European bat flies (Diptera: Nycteribiidae, Streblidae). Zootaxa 4205:101–126. CrossRefGoogle Scholar
  47. 47.
    Gutiérrez R, Morick D, Cohen C, Hawlena H, Harrus S (2014) The effect of ecological and temporal factors on the composition of Bartonella infection in rodents and their fleas. ISME J 8:1598–1608. CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Marshall AG (1982) Ecology of insects ectoparasitic on bats. In: Kunz TE (ed) Ecology of bats. Springer, US, Philadelphia, pp 369–401CrossRefGoogle Scholar
  49. 49.
    Petit E, Mayer F (1999) Male dispersal in the noctule bat (Nyctalus noctula): where are the limits? Proc. Biol. Sci. 266:1717–1722. CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Encarnacao J a, Kierdorf U, Wolters V (2006) Seasonal variation in nocturnal activity of male Daubenton ’ s bats , Myotis daubentonii ( Chiroptera : Vespertilionidae). Folia Zool. 55:237–246Google Scholar
  51. 51.
    Moussy C, Hosken DJ, Mathews F, Smith GC, Aegerter JN, Bearhop S (2013) Migration and dispersal patterns of bats and their influence on genetic structure. Mamm Rev 43:183–195. CrossRefGoogle Scholar
  52. 52.
    Ramos Pereira MJ, Salgueiro P, Rodrigues L, Coelho MM, Palmeirim JM (2009) Population structure of a cave-dwelling bat, Miniopterus schreibersii: does it reflect history and social organization? J Hered 100:533–544. CrossRefPubMedGoogle Scholar
  53. 53.
    Altringham JD, Senior P, Ruckstuhl KE, Neuhaus P (2005) Social systems and ecology of bats. In: Ruckstuhl KE, Neuhaus P (eds) Sexual segregation in vertebrates. Cambridge University Press, Cambridge, pp 280–302Google Scholar
  54. 54.
    Rodrigues L, Palmeirim JM (2008) Migratory behaviour of the Schreiber’s bat: when, where and why do cave bats migrate in a Mediterranean region? J. Zool. 274:116–125. CrossRefGoogle Scholar
  55. 55.
    Gutiérrez R, Vayssier-Taussat M, Buffet J-P, Harrus S (2017) Guidelines for the isolation, molecular detection, and characterization of Bartonella species. Vector-Borne Zoonotic Dis 17:42–50. CrossRefPubMedGoogle Scholar
  56. 56.
    Kosoy M, Morway C, Sheff KW, Bai Y, Colborn J, Chalcraft L, Dowell SF, Peruski LF, Maloney SA, Baggett H, Sutthirattana S, Sidhirat A, Maruyama S, Kabeya H, Chomel BB, Kasten R, Popov V, Robinson J, Kruglov A, Petersen LR (2008) Bartonella tamiae sp. nov., a newly recognized pathogen isolated from three human patients from Thailand. J. Clin. Microbiol. 46:772–775. CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Attila D. Sándor
    • 1
  • Mihály Földvári
    • 2
    • 3
  • Aleksandra I. Krawczyk
    • 4
  • Hein Sprong
    • 4
  • Alexandra Corduneanu
    • 1
  • Levente Barti
    • 5
  • Tamás Görföl
    • 6
  • Péter Estók
    • 7
  • Dávid Kováts
    • 2
  • Sándor Szekeres
    • 8
  • Zoltán László
    • 9
  • Sándor Hornok
    • 8
  • Gábor Földvári
    • 8
    • 10
    Email author
  1. 1.Department of Parasitology and Parasitic DiseasesUniversity of Agricultural Sciences and Veterinary MedicineCluj-NapocaRomania
  2. 2.Department of Evolutionary Zoology and Human BiologyUniversity of DebrecenDebrecenHungary
  3. 3.Natural History MuseumUniversity of OsloOsloNorway
  4. 4.Centre for Zoonoses & Environmental Microbiology, Centre for Infectious Disease ControlNational Institute for Public Health and the EnvironmentBilthoventhe Netherlands
  5. 5.Romanian Bat Protection Association – Central BranchOdorheiu SecuiescRomania
  6. 6.Department of ZoologyHungarian Natural History MuseumBudapestHungary
  7. 7.Department of ZoologyEszterházy Károly UniversityEgerHungary
  8. 8.Department of Parasitology and ZoologyUniversity of Veterinary MedicineBudapestHungary
  9. 9.Hungarian Department of Biology and EcologyBabeş-Bolyai UniversityCluj-NapocaRomania
  10. 10.Evolutionary Systems Research Group, Centre for Ecological ResearchHungarian Academy of SciencesTihanyHungary

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