Few vertebrate species dominate the Borrelia burgdorferi s.l. Life cycle

Environmental Research Letters

Volumn 11, Issue 4, 2016, Pages

  Hofmeester, T R ^a   Coipan, E C ^b   Van Wieren, S E ^a   Prins, H H T ^a   Takken, W ^a   Sprong, H ^b  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

Author keywords

deer; Ixodes ricinus; Lyme borreliosis; small mammals; thrushes; transmission maintenance

Indexed keywords

MAMMALS;

DEER; IXODES RICINUS; LYME BORRELIOSIS; SMALL MAMMALS; THRUSHES;

LIFE CYCLE;

BACTERIUM; BODY MASS; DEER; DISEASE INCIDENCE; DISEASE TRANSMISSION; DISEASE VECTOR; HEMOPHAGY; HOST SPECIFICITY; LIFE CYCLE; PASSERINE; SMALL MAMMAL; TICK;

EUROPE;

AVES; BORRELIA; BORRELIA BURGDORFERI; CERVIDAE; IXODES RICINUS; IXODIDA; IXODIDAE; MAMMALIA; RODENTIA; TURDIDAE; VERTEBRATA;

EID: 84964755800     PISSN: 17489318     EISSN: 17489326     Source Type: Journal    
DOI: 10.1088/1748-9326/11/4/043001     Document Type: Review

References (122)

1. Amore G, Tomassone L, Grego E, Ragagli C, Bertolotti L, Nebbia P, Rosati S and Mannelli A 2007 Borrelia lusitaniae in immature Ixodes ricinus (Acari: Ixodidae) feeding on common wall lizards in Tuscany, central Italy J. Med. Entomol. 44 303-7
2. Anderson J F and Magnarelli L A 1993 Epizootiology of lyme disease-causing borreliae Clinics Dermatology 11 339-51
3. Apollonio M, Andersen R and Putman R 2010 European Ungulates and their Management in the 21st Century (Cambridge: Cambridge University Press)
4. Baranton G, Postic D, Saintgirons I, Boerlin P, Piffaretti J C, Assous M and Grimont P A D 1992 Delineation of Borrelia burgdorferi Sensu Stricto, Borrelia garinii sp. nov., and group VS461 associated with Lyme borreliosis Int. J. Syst. Bacteriol. 42 378-83
5. Barbour A, Bunikis J, Fish D and Hanincova K 2015 Association between body size and reservoir competence of mammals bearing Borrelia burgdorferi at an endemic site in the northeastern United States Parasit. Vectors 8 299
6. Barton K 2014 MuMIn: Multi-model inference (http://CRAN.R-project.org/package=MuMIn)
7. Bown K J, Begon M, Bennett M, Birtles R J, Burthe S, Lambin X, Telfer S, Woldehiwet Z and Ogden N H 2006 Sympatric Ixodes trianguliceps and Ixodes ricinus ticks feeding on field voles (Microtus agrestis): potential for increased risk of Anaplasma phagocytophilum in the United Kingdom? Vector Borne Zoonotic Dis. 6 404-10
8. Boyard C, Vourc'h G and Barnouin J 2008 The relationships between Ixodes ricinus and small mammal species at the woodland-pasture interface Exp. Appl. Acarol. 44 61-76
9. Brinck P, Johnels A, Lundholm B, Svedmyr A, Zeipel G V and Zetterberg B 1967 Small mammals in sweden as hosts of tick-borne encephalitis virus and vagrant ectoparasites Oikos 18 124-34
10. Burnham K P and Anderson D R 2004 Multimodel inference: understanding AIC and BIC in model selection Sociological Methods Res. 33 261-304
11. Burri C, Schumann O, Schumann C and Gern L 2014 Are Apodemus spp. mice and Myodes glareolus reservoirs for Borrelia miyamotoi, Candidatus Neoehrlichia mikurensis, Rickettsia helvetica, R. monacensis and Anaplasma phagocytophilum? Ticks Tick Borne Dis. 5 245-51
12. Carbone C, Cowlishaw G, Isaac N J B and Rowcliffe J M 2005 How far do animals go? Determinants of day range in mammals Am. Nat. 165 290-7
13. Christova I and Gladnishka T 2005 Prevalence of infection with Francisella tularensis, Borrelia burgdorferi sensu lato and Anaplasma phagocytophilum in rodents from an endemic focus of tularemia in Bulgaria Ann. Agric. Environ. Med. 12 149-52 (www.aaem.pl/pdf/12149.htm)
14. Cook R D 1977 Detection of influential observation in linear regression Technometrics 19 15-8
15. Cosson J-F et al 2014 Genetic characterization of the human relapsing fever spirochete Borrelia miyamotoi in vectors and animal reservoirs of Lyme disease spirochetes in France Parasit. Vectors 7 233
16. Cramp S and Perrins C M 1994 Handbook of the Birds of Europe, the Middle East and North Africa: The Birds of the Western Palearctic (Oxford: Oxford University Press)
17. Dantas-Torres F, Chomel B B and Otranto D 2012 Ticks and tick-borne diseases: a one health perspective Trends Parasitol. 28 437-46
18. De Boer R, Hovius K E, Nohlmans M K and Gray J S 1993 The woodmouse (Apodemus sylvaticus) as a reservoir of tick-transmitted spirochetes (Borrelia burgdorferi) in The Netherlands Zentralbl. Bakteriol. 279 404-16
19. De Carvalho I L, Zeidner N, Ullmann A, Hojgaard A, Amaro F, Zé-Zé L, Alves M J, De Sousa R, Piesman J and Núncio M S 2010 Molecular characterization of a new isolate of Borrelia lusitaniae derived from Apodemus sylvaticus in Portugal Vector Borne Zoonotic Dis. 10 531-4
20. Dubska L, Literak I, Kocianova E, Taragel'ova V, Sverakova V, Sychra O and Hromadko M 2011 Synanthropic birds influence the distribution of Borrelia species: analysis of Ixodes ricinus ticks feeding on passerine birds Appl. Environ. Microbiol. 77 1115-7
21. Dubska L, Literak I, Kocianova E, Taragel'ova V and Sychra O 2009 Differential role of passerine birds in distribution of Borrelia spirochetes, based on data from ticks collected from birds during the postbreeding migration period in central Europe Appl. Environ. Microbiol. 75 596-602
22. Dubska L, Literak I, Kverek P, Roubalova E, Kocianova E and Taragel'ova V 2012 Tick-borne zoonotic pathogens in ticks feeding on the common nightingale including a novel strain of Rickettsia sp Ticks Tick Borne Dis. 3 265-8
23. Estrada-Peña A, Osácar J J, Pichon B and Gray J S 2005 Hosts and pathogen detection for immature stages of Ixodes ricinus (Acari: Ixodidae) in North-Central Spain Exp. Appl. Acarol. 37 257-68
24. Ferreri L, Giacobini M, Bajardi P, Bertolotti L, Bolzoni L, Tagliapietra V, Rizzoli A and Rosa R 2014 Pattern of tick aggregation on mice: larger than expected distribution tail enhances the spread of tick-borne pathogens PLoS Comp. Biol. 10 e1003931
25. Fietz J, Tomiuk J, Matuschka F R and Richter D 2014 Seasonal prevalence of Lyme disease spirochetes in a heterothermic mammal, the edible dormouse (glis glis) Appl. Environ. Microbiol. 80 3615-21
26. Franke J, Fritzsch J, Tomaso H, Straube E, Dorn W and Hildebrandt A 2010 Coexistence of pathogens in host-seeking and feeding ticks within a single natural habitat in central Germany Appl. Environ. Microbiol. 76 6829-36
27. Franke J, Hildebrandt A and Dorn W 2013 Exploring gaps in our knowledge on Lyme borreliosis spirochaetes - updates on complex heterogeneity, ecology, and pathogenicity Ticks Tick Borne Dis. 4 11-25
28. Gassner F, Takken W, Plas C L-V d, Kastelein P, Hoetmer A J, Holdinga M and van Overbeek L S 2013 Rodent species as natural reservoirs of Borrelia burgdorferi sensu lato in different habitats of Ixodes ricinus in The Netherlands Ticks Tick Borne Dis. 4 452-8
29. Gassner F, van Vliet A J H, Burgers S, Jacobs F, Verbaarschot P, Hovius E K E, Mulder S, Verhulst N O, van Overbeek L S and Takken W 2011 Geographic and temporal variations in population dynamics of Ixodes ricinus and associated Borrelia infections in The Netherlands Vector Borne Zoonotic Dis. 11 523-32
30. Gray J S 1998 The ecology of ticks transmitting Lyme borreliosis Exp. Appl. Acarol. 22 249-58
31. Gray J S, Kahl O, Janetzki C and Stein J 1992 Studies on the ecology of Lyme disease in a deer forest in County Galway, Ireland J. Med. Entomol. 29 915-20
32. Gray J S, Kahl O, Janetzki C, Stein J and Guy E 1995 The spatial distribution of Borrelia burgdorferi-infected Ixodes ricinus in the Connemara region of County Galway, Ireland Exp. Appl. Acarol. 19 163-72
33. Gray J S, Kirstein F, Robertson J N, Stein J and Kahl O 1999 Borrelia burgdorferi sensu lato in Ixodes ricinus ticks and rodents in a recreational park in south-western Ireland Exp. Appl. Acarol. 23 717-29
34. Gray J S, Robertson J N and Key S 2000 Limited role of rodents as reservoirs of Borrelia burgdorferi sensu lato in Ireland Eur. J. Epidemiol. 16 101-3
35. Gregory R D, Vorisek P, Van Strien A, Gmelig Meyling A W, Jiguet F, Fornasari L, Reif J, Chylarecki P and Burfield I J 2007 Population trends of widespread woodland birds in Europe Ibis 149 78-97
36. Hanincova K, Schafer S M, Etti S, Sewell H S, Taragel'ova V, Ziak D, Labuda M and Kurtenbach K 2003a Association of Borrelia afzelii with rodents in Europe Parasitology 126 11-20
37. Hanincova K, Taragel'ova V, Koci J, Schafer S M, Hails R, Ullmann A J, Piesman J, Labuda M and Kurtenbach K 2003b Association of Borrelia garinii and B-valaisiana with songbirds in Slovakia Appl. Environ. Microbiol. 69 2825-30
38. Harrison A, Bown K J, Montgomery W I and Birtles R J 2012 Ixodes ricinus is not an epidemiologically relevant vector of Bartonella species in the wood mouse (Apodemus sylvaticus) Vector Borne Zoonotic Dis. 12 366-71
39. Heidrich J 2000 Untersuchungen zur Prävalenz von Borrelia burgdorferi sensu lato beim rotfuchs (vulpes vulpes) in ostbrandenburg Unpublished PhD Freien Universität Berlin, Berlin
40. Heidrich J, Schonberg A, Steuber S, Nockler K, Schulze P, Voigt W P and Schein E 1999 Investigation of skin samples from red foxes (Vulpes vulpes) in eastern Brandenburg (Germany) for the detection of Borrelia burgdorferi s. l Zentralbl. Bakteriol. 289 666-72
41. Hellgren O, Andersson M and Råberg L 2011 The genetic structure of Borrelia afzelii varies with geographic but not ecological sampling scale J. Evol. Biol. 24 159-67
42. Heylen D, Tijsse E, Fonville M, Matthysen E and Sprong H 2013 Transmission dynamics of Borrelia burgdorferi s.l. in a bird tick community Environ. Microbiol. 15 663-73
43. Huang Z Y X, de Boer W F, van Langevelde F, Olson V, Blackburn T M and Prins H H T 2013 Species' life-history traits explain interspecific variation in reservoir competence: a possible mechanism underlying the dilution effect PLoS One 8 e54341
44. Hulinska D, Votypka J, Plch J, Vlcek E, Valešová M, Bojar M, Hulinsky V and Smetana K 2002 Molecular and microscopical evidence of Ehrlichia spp. and Borrelia burgdorferi sensu lato in patients, animals and ticks in the Czech Republic New Microbiol. 25 437-48
45. Humair P F and Gern L 1998 Relationship between Borrelia burgdorferi sensu lato species, red squirrels (sciurus vulgaris) and Ixodes ricinus in enzootic areas in Switzerland Acta Trop. 69 213-27
46. Humair P F, Peter O, Wallich R and Gern L 1995 Strain variation of Lyme disease spirochetes isolated from Ixodes ricinus ticks and rodents collected in two endemic areas in Switzerland J. Med. Entomol. 32 433-8
47. Humair P F, Rais O and Gern L 1999 Transmission of Borrelia afzelii from Apodemus mice and clethrionomys voles to Ixodes ricinus ticks: differential transmission pattern and overwintering maintenance Parasitology 118 33-42
48. Humair P F, Turrian N, Aeschilimann A and Gern L 1993a Borrelia burgdorferi in a focus of Lyme borreliosis: epizootiologic contribution of small mammals Folia Parasitol. 40 65-70
49. Humair P F, Turrian N, Aeschlimann A and Gern L 1993b Ixodes ricinus immatures on birds in a focus of Lyme borreliosis Folia Parasitol. 40 237-42
50. Jaenson T G T, Tälleklint L, Lundqvist L, Olsen B, Chirico J and Mejlon H 1994 Geographical distribution, host associations, and vector roles of ticks (Acari: Ixodidae, Argasidae) in Sweden J. Med. Entomol. 31 240-56
51. James M C, Furness R W, Bowman A S, Forbes K J and Gilbert L 2011 The importance of passerine birds as tick hosts and in the transmission of Borrelia burgdorferi, the agent of Lyme disease: a case study from Scotland Ibis 153 293-302
52. Jones K E, Patel N G, Levy M A, Storeygard A, Balk D, Gittleman J L and Daszak P 2008 Global trends in emerging infectious diseases Nature 451 990-3
53. Jongejan F and Uilenberg G 2004 The global importance of ticks Parasitology 129 S3-14
54. Kahl O, Gern L, Eisen L and Lane R S 2002 Ecological research on Borrelia burgdorferi sensu lato: terminology and some methodological pitfalls Lyme Borreliosis: Biology, Epidemiology and Control ed J S Gray et al (New York: CABI Publishing) pp 29-46
55. Kaiser A, Seitz A and Strub O 2002 Prevalence of Borrelia burgdorferi sensu lato in the nightingale (Luscinia megarhynchos) and other passerine birds Int. J. Med. Microbiol. 291 75-9
56. Kiffner C, Vor T, Hagedorn P, Niedrig M and Ruhe F 2011 Factors affecting patterns of tick parasitism on forest rodents in tick-borne encephalitis risk areas, Germany Parasitol. Res. 108 323-35
57. Kipp S, Goedecke A, Dorn W, Wilske B and Fingerle V 2006 Role of birds in Thuringia, Germany, in the natural cycle of Borrelia burgdorferi sensu lato, the Lyme disease spirochaete Int. J. Med. Microbiol. 296 125-8
58. Kjelland V, Ytrehus B, Stuen S, Skarpaas T and Slettan A 2011 Prevalence of Borrelia burgdorferi in Ixodes ricinus ticks collected from moose (Alces alces) and roe deer (Capreolus capreolus) in southern Norway Ticks Tick Borne Dis. 2 99-103
59. Kurtenbach K, De Michelis S, Etti S, Schafer S M, Sewell H S, Brade V and Kraiczy P 2002 Host association of Borrelia burgdorferi sensu lato - the key role of host complement Trends Microbiol. 10 74-9
60. Kurtenbach K, Dizij A, Seitz H M, Margos G, Moter S E, Kramer M D, Wallich R, Schaible U E and Simon M M 1994 Differential immune responses to Borrelia burgdorferi in European wild rodent species influence spirochete transmission to Ixodes ricinus L (Acari: Ixodidae) Infect. Immun. 62 5344-52 (http://iai.asm.org/content/62/12/5344.short)
61. Kurtenbach K, Hanincova K, Tsao J I, Margos G, Fish D and Ogden N H 2006 Fundamental processes in the evolutionary ecology of Lyme borreliosis Nat. Rev. Microbiol. 4 660-9
62. Kurtenbach K, Peacey M, Rijpkema S G T, Hoodless A N, Nuttall P A and Randolph S E 1998 Differential transmission of the genospecies of Borrelia burgdorferi sensu lato by game birds and small rodents in England Appl. Environ. Microbiol. 64 1169-74 (http://aem.asm.org/content/64/4/1169.short)
63. Lee K A 2006 Linking immune defenses and life history at the levels of the individual and the species Integr. Comp. Biol. 46 1000-15
64. LoGiudice K, Ostfeld R S, Schmidt K A and Keesing F 2003 The ecology of infectious disease: effects of host diversity and community composition on Lyme disease risk Proc. Natl Acad. Sci. USA 100 567-71
65. Mannelli A, Bertolotti L, Gern L and Gray J 2012 Ecology of Borrelia burgdorferi sensu lato in Europe: transmission dynamics in multi-host systems, influence of molecular processes and effects of climate change FEMS Microbiol. Rev. 36 837-61
66. Mannelli A, Nebbia P, Tramuta C, Grego E, Tomassone L, Ainardi R, Venturini L, De Meneghi D and Meneguz P G 2005 Borrelia burgdorferi sensu lato infection in larval Ixodes ricinus (Acari: Ixodidae) feeding on blackbirds in northwestern Italy J. Med. Entomol. 42 168-75
67. Margos G, Vollmer S A, Ogden N H and Fish D 2011 Population genetics, taxonomy, phylogeny and evolution of Borrelia burgdorferi sensu lato Infection Genetics Evol. 11 1545-63
68. Marsot M, Chapuis J L, Gasqui P, Dozières A, Masséglia S, Pisanu B, Ferquel E and Vourc'h G 2013 Introduced Siberian Chipmunks (Tamias sibiricus barberi) contribute more to Lyme borreliosis risk than native reservoir rodents PLoS One 8 e55377
69. Marsot M, Henry P Y, Vourc'h G, Gasqui P, Ferquel E, Laignel J, Grysan M and Chapuis J L 2012 Which forest bird species are the main hosts of the tick, Ixodes ricinus, the vector of Borrelia burgdorferi sensu lato, during the breeding season? Int. J. Parasitol. 42 781-8
70. Martello E, Mannelli A, Ragagli C, Ambrogi C, Selmi M, Ceballos L A and Tomassone L 2014 Range expansion of Ixodes ricinus to higher altitude, and co-infestation of smal` rodents with Dermacentor marginatus in the Northern Apennines, Italy Ticks Tick Borne Dis. 5 970-4
71. Martin L B, Weil Z M and Nelson R J 2007 Immune defense and reproductive pace of life in Peromyscus mice Ecology 88 2516-28
72. Mather T N, Wilson M L, Moore S I, Ribeiro J M C and Spielman A 1989 Comparing the relative potential of rodents as reservoirs of the Lyme disease spirochete (Borrelia burgdorferi) Am. J. Epidemiol. 130 143-50 (http://aje.oxfordjournals.org/content/130/1/143.short)
73. Matuschka F R, Eiffert H, Ohlenbusch A and Spielman A 1994 Amplifying role of edible dormice in Lyme disease transmission in central Europe J. Infect. Dis. 170 122-7
74. Matuschka F R, Fischer P, Musgrave K, Richter D and Spielman A 1991 Hosts on which nymphal Ixodes ricinus most abundantly feed Am. J. Trop. Med. Hyg. 44 100-7
75. Matuschka F R, Heiler M, Eiffert H, Fischer P, Lotter H and Spielman A 1993 Diversionary role of hoofed game in the transmission of Lyme disease spirochetes Am. J. Trop. Med. Hyg. 48 693-9
76. Matuschka F R, Lange R, Spielman A, Richter D and Fischer P 1990 Subadult Ixodes ricinus (Acari: Ixodidae) on rodents in Berlin West Germany J. Med. Entomol. 27 385-90
77. Medlock J M et al 2013 Driving forces for changes in geographical distribution of Ixodes ricinus ticks in Europe Parasit. Vectors 6 1
78. Mejlon H A and Jaenson T G T 1997 Questing behaviour of Ixodes ricinus ticks (Acari: Ixodidae) Exp. Appl. Acarol. 21 747-54
79. Michalik J, Hofman T, Buczek A, Skoracki M and Sikora B 2003 Borrelia burgdorferi s.l. in Ixodes ricinus (Acari: Ixodidae) ticks collected from vegetation and small rodents in recreational areas of the city of Poznań J. Med. Entomol. 40 690-7
80. Michalik J, Skotarczak B, Skoracki M, Wodecka B, Sikora B, Hofman T, Rymaszewska A and Sawczuk M 2005 Borrelia burgdorferi sensu stricto in yellow-necked mice and feeding Ixodes ricinus ticks in a forest habitat of west central Poland J. Med. Entomol. 42 850-6
81. Michalik J, Wodecka B, Skoracki M, Sikora B and Stańczak J 2008 Prevalence of avian-associated Borrelia burgdorferi s.l. genospecies in Ixodes ricinus ticks collected from blackbirds (Turdus merula) and song thrushes (T. philomelos) Int. J. Med. Microbiol. 298 129-38 (Suppl. 1)
82. Mogl C, de Mendonça P G, Harsch A and Hey J 2011 Potential for cofeeding transmission of tick-borne pathogens in common voles and roe deer - supportive molecular evidence from field samples Acta Zoologica Bulgarica 63 301-6
83. Niethammer J and Krapp F 1978 Handbuch der Säugetiere Europas (Wiesbaden: Aula-Verlag)
84. Ostfeld R S and Holt R D 2004 Are predators good for your health? Evaluating evidence for top-down regulation of zoonotic disease reservoirs Front. Ecol. Environ. 2 13-20
85. Ostfeld R S and Keesing F 2000 Biodiversity and disease risk: the case of lyme disease Conserv. Biol. 14 722-8
86. Ostfeld R S, Levi T, Jolles A E, Martin L B, Hosseini P R and Keesing F 2014 Life history and demographic drivers of reservoir competence for three tick-borne zoonotic pathogens PLoS One 9 e107387
87. Pacilly F C A, Benning M E, Jacobs F, Leidekker J, Sprong H, Van Wieren S E and Takken W 2014 Blood feeding on large grazers affects the transmission of Borrelia burgdorferi sensu lato by Ixodes ricinus Ticks Tick Borne Dis. 5 810-7
88. Pato F J, Panadero R, Vázquez L, López C M, Díaz P, Vázquez E, Díez-Baños P, Morrondo P and Fernández G 2013 Seroprevalence of Borrelia burgdorferi sensu lato in roe deer (Capreolus Capreolus) from Northwestern Spain J. Zoo. Wildl. Med. 44 660-5
89. Pérez D, Kneubühler Y, Rais O and Gern L 2012 Seasonality of Ixodes ricinus ticks on vegetation and on rodents and Borrelia burgdorferi sensu lato genospecies diversity in two Lyme borreliosis-endemic areas in Switzerland Vector Borne Zoonotic Dis. 12 633-44
90. Perkins S E, Cattadori I M, Tagliapietra V, Rizzoli A P and Hudson P J 2003 Empirical evidence for key hosts in persistence of a tick-borne disease Int. J. Parasitol. 33 909-17
91. Pfäffle M, Littwin N, Muders S V and Petney T N 2013 The ecology of tick-borne diseases Int. J. Parasitol. 43 1059-77
92. Pfäffle M, Petney T, Skuballa J and Taraschewski H 2011 Comparative population dynamics of a generalist (Ixodes ricinus) and specialist tick (I. hexagonus) species from European hedgehogs Exp. Appl. Acarol. 54 151-64
93. Pichon B, Gilot B and Perez-Eid C 2000 Detection of spirochaetes of Borrelia burgdorferi complexe in the skin of cervids by PCR and culture Eur. J. Epidemiol. 16 869-73
94. Pisanu B, Chapuis J-L, Dozières A, Basset F, Poux V and Vourc'h G 2014 High prevalence of Borrelia burgdorferi s.l. in the European red squirrel Sciurus vulgaris in France Ticks Tick Borne Dis. 5 1-6
95. Previtali M A, Ostfeld R S, Keesing F, Jolles A E, Hanselmann R and Martin L B 2012 Relationship between pace of life and immune responses in wild rodents Oikos 121 1483-92
96. Råberg L 2012 Infection intensity and infectivity of the tick-borne pathogen Borrelia afzelii J. Evol. Biol. 25 1448-53
97. Radzijevskaja J, Paulauskas A, Rosef O, Petkevičius S, Mažeika V and Rekašius T 2013 The propensity of voles and mice to transmit Borrelia burgdorferi sensu lato infection to feeding ticks Vet. Parasitol. 197 318-25
98. Randolph S E 2004 Tick ecology: processes and patterns behind the epidemiological risk posed by ixodid ticks as vectors Parasitology 129 S37-65
99. Randolph S E and Dobson A D M 2012 Pangloss revisited: a critique of the dilution effect and the biodiversity-buffers-disease paradigm Parasitology 139 847-63
100. Rauter C and Hartung T 2005 Prevalence of Borrelia burgdorferi sensu lato genospecies in Ixodes ricinus ticks in Europe: a metaanalysis Appl. Environ. Microbiol. 71 7203-16
101. R Core Team 2015 R: a language and environment for statistical computing (Vienna, Austria: R Foundation for Statistical Computing) (http://R-project.org/)
102. Richter D and Matuschka F R 2006 Perpetuation of the Lyme disease spirochete Borrelia lusitaniae by lizards Appl. Environ. Microbiol. 72 4627-32
103. Richter D, Schlee D B, Allgower R and Matuschka F R 2004 Relationships of a novel Lyme disease spirochete, Borrelia spielmani sp nov., with its hosts in central Europe Appl. Environ. Microbiol. 70 6414-9
104. Rózsa L, Reiczigel J and Majoros G 2000 Quantifying parasites in samples of hosts J. Parasitol. 86 228-32
105. Schmidt S et al 2014 Multiple infections of rodents with zoonotic pathogens in Austria Vector Borne Zoonotic Dis. 14 467-75
106. Silaghi C, Woll D, Hamel D, Pfister K, Mahling M and Pfeffer M 2012 Babesia spp. and anaplasma phagocytophilum in questing ticks, ticks parasitizing rodents and the parasitized rodents - analyzing the host-pathogen-vector interface in a metropolitan area Parasit. Vectors 5 191
107. Siński E, Pawełczyk A, Bajer A and Behnke J M 2006 Abundance of wild rodents, ticks and environmental risk of Lyme borreliosis: a longitudinal study in an area of Mazury Lakes district of Poland Ann. Agric. Environ. Med. 13 295-300 (www.aaem.pl/pdf/13295.htm)
108. Sprong H, Hofhuis A, Gassner F, Takken W, Jacobs F, van Vliet A J, van Ballegooijen M, van der Giessen J and Takumi K 2012 Circumstantial evidence for an increase in the total number and activity of borrelia-infected Ixodes ricinus in the Netherlands Parasit. Vectors 5 294
109. Tälleklint L and Jaenson T G T 1994 Transmission of Borrelia burgdorferi s.l. from mammal reservoirs to the primary vector of Lyme borreliosis, Ixodes ricinus (Acari: Ixodidae), in Sweden J. Med. Entomol. 31 880-6
110. Tälleklint L and Jaenson T G T 1997 Infestation of mammals by Ixodes ricinus ticks (Acari: Ixodidae) in south-central Sweden Exp. Appl. Acarol. 21 755-71
111. Taragel'ova V, Koci J, Hanincova K, Kurtenbach K, Derdakova M, Ogden N H, Literak I, Kocianova E and Labuda M 2008 Blackbirds and song thrushes constitute a key reservoir of Borrelia garinii, the causative agent of Borreliosis in Central Europe Appl. Environ. Microbiol. 74 1289-93
112. Tijsse-Klasen E, Fonville M, Reimerink J H J, Spitzen-van der Sluijs A and Sprong H 2010 Role of sand lizards in the ecology of Lyme and other tick-borne diseases in the Netherlands Parasit. Vectors 3 42
113. Václav R, Ficová M, Prokop P and Betáková T 2011 Associations between coinfection prevalence of Borrelia lusitaniae, anaplasma sp., and Rickettsia sp. in hard ticks feeding on reptile hosts Microb. Ecol. 61 245-53
114. van Strien A J, Bekker D L, La Haye M J J and van der Meij T 2015 Trends in small mammals derived from owl pellet data using occupancy modelling Mammalian Biol. - Z. Säugetierkunde 80 340-6
115. Vanwambeke S O, Sumilo D, Bormane A, Lambin E F and Randolph S E 2010 Landscape predictors of tick-borne encephalitis in Latvia: land cover, land use, and land ownership Vector Borne Zoonotic Dis. 10 497-506
116. Vazquez L, Panadero R, Dacal V, Pato F J, Lopez C, Diaz P, Arias M S, Fernandez G, Diez-Baos P and Morrondo P 2011 Tick infestation (Acari: Ixodidae) in roe deer (capreolus capreolus) from northwestern Spain: population dynamics and risk stratification Exp. Appl. Acarol. 53 399-409
117. Vor T, Kiffner C, Hagedorn P, Niedrig M and Ruhe F 2010 Tick burden on European roe deer (Capreolus capreolus) Exp. Appl. Acarol. 51 405-17
118. Vourc'h G, Marmet J, Chassagne M, Bord S and Chapuis J L 2007 Borrelia burgdorferi sensu lato in Siberian chipmunks (Tamias sibiricus) introduced in suburban forests in France Vector Borne Zoonotic Dis. 7 637-41
119. Wegner Z, Stańczak J, Racewicz M, Kubica-Biernat B and Kruminis-Łozowska W 1997 The etiological agent of lyme disease, Borrelia burgdorferi, in ticks (Acari: Ixodidae) from eastern Poland Zentralbl. Bakteriol. 286 93-106
120. Welc-Faleciak R, Bajer A, Behnke J M and Sinski E 2008 Effects of host diversity and the community composition of hard ticks (Ixodidae) on Babesia microti infection Int. J. Med. Microbiol. 298 235-42
121. Wood C L and Lafferty K D 2013 Biodiversity and disease: a synthesis of ecological perspectives on Lyme disease transmission Trends Ecol. Evol. 28 239-47
122. Xu G, Fang Q Q, Keirans J E and Durden L A 2003 Molecular phylogenetic analyses indicate that the Ixodes ricinus complex is a paraphyletic GROUP J. Parasitol. 89 452-7