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Effects of stress exposure in captivity on physiology and infection in avian hosts: no evidence of increased Borrelia burgdorferi s.l. infectivity to vector ticks

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Abstract

Exposure to environmental stressors, an increasingly recurring event in natural communities due to anthropogenic-induced environmental change, profoundly impacts disease emergence and spread. One mechanism through which this occurs is through stress-induced immunosuppression increasing disease susceptibility, prevalence, intensity and reactivation in hosts. We experimentally evaluated how exposure to stressors affected both the physiology of avian hosts and the prevalence of the zoonotic bacteria Borrelia burgdorferi sensu lato (s.l.), in two model species—the blackbird Turdus merula and the robin Erithacus rubecula captured in the wild, using xenodiagnoses and analysis of skin biopsies and blood. Although exposure to stressors in captivity induced physiological stress in birds (increased the number of circulating heterophils), there was no evidence of increased infectivity to xenodiagnostic ticks. However, Borrelia detection in the blood for both experimental groups of blackbirds was higher by the end of the captivity period. The infectivity and efficiency of transmission were higher for blackbirds than robins. When comparing different methodologies to determine infection status, xenodiagnosis was a more sensitive method than skin biopsies and blood samples, which could be attributed to mild levels of infection in these avian hosts and/or dynamics and timing of Borrelia infection relapses and redistribution in tissues.

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The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request

References

  1. Brearley G, Rhodes J, Bradley A, Baxter G, Seabrook L, Lunney D, Liu Y, McAlpine C (2013) Wildlife disease prevalence in human-modified landscapes. Biol Rev 88:427–442. https://doi.org/10.1111/brv.12009

    Article  PubMed  Google Scholar 

  2. Glaser R, Kiecolt-Glaser JK (2005) Stress-induced immune dysfunction: implications for health. Nat Rev Immunol 5:243–251. https://doi.org/10.1038/nri1571

    Article  CAS  PubMed  Google Scholar 

  3. Acevedo-Whitehouse K, Duffus ALJ (2009) Effects of environmental change on wildlife health. Philos Trans R Soc Lond Ser B Biol Sci 364:3429–3438. https://doi.org/10.1098/rstb.2009.0128

    Article  Google Scholar 

  4. Lafferty KD, Gerber LR (2002) Good medicine for conservation biology: the intersection of epidemiology and conservation theory. Conserv Biol 16:593–604

    Article  Google Scholar 

  5. Dobson A, Foufopoulos J (2001) Emerging infectious pathogens of wildlife. Philos Trans R Soc Lond Ser B Biol Sci 356:1001–1012

    Article  CAS  Google Scholar 

  6. Daszak P (2000) Emerging infectious diseases of wildlife - threats to biodiversity and human health. Science 287:1756–1756

    Article  Google Scholar 

  7. Gray J, Kahl O, Lane RS, Stanek G (2002) Lyme borreliosis: biology, epidemiology and control. CABI Publishing, New York

  8. Norte AC, Ramos JA, Gern L, Núncio MS, Lopes de Carvalho I (2013) Birds as reservoirs for Borrelia burgdorferi s.l. in western Europe: circulation of B. turdi and other genospecies in bird-tick cycles in Portugal. Environ Microbiol 15:386–397. https://doi.org/10.1111/j.1462-2920.2012.02834.x

    Article  CAS  PubMed  Google Scholar 

  9. Heylen D, Tijsse E, Fonville M, Matthysen E, Sprong H (2013) Transmission dynamics of Borrelia burgdorferi s.l. in a bird tick community. Environ Microbiol 15:663–673. https://doi.org/10.1111/1462-2920.12059

    Article  PubMed  Google Scholar 

  10. Dubska L, Literak I, Kocianova E, Taragelova V, 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

    Article  CAS  Google Scholar 

  11. Michalik J, Wodecka B, Skoracki M, Sikora B, Stanczak 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 298:129–138

    Article  CAS  Google Scholar 

  12. Mannelli A, Nebbia P, Tramuta C, Grego E, Tomassone L, Ainardi R, Venturini L, De Meneghi D, Meneguz PG (2005) Borrelia burgdorferi sensu lato infection in larval Ixodes ricinus (Acari : Ixodidae) feeding on blackbirds in northwestern Italy. J Med Entomol 42:168–175

    Article  Google Scholar 

  13. Humair PF, Postic D, Wallich R, Gern L (1998) An avian reservoir (Turdus merula) of the Lyme borreliosis spirochetes. Zentralbl Bakteriol 287:521–538

    Article  CAS  Google Scholar 

  14. Norte AC, Lopes de Carvalho I, Núncio MS, Ramos JA, Gern L (2013) Blackbirds Turdus merula as competent reservoirs for Borrelia turdi and Borrelia valaisiana in Portugal: evidence from a xenodiagnostic experiment. Environ Microbiol Rep 5:604–607. https://doi.org/10.1111/1758-2229.12058

    Article  PubMed  Google Scholar 

  15. Heylen D, Krawczyk A, Lopes de Carvalho I, Núncio MS, Sprong H, Norte AC (2017) Bridging of cryptic Borrelia cycles in European songbirds. Environ Microbiol 19:1857–1867. https://doi.org/10.1111/1462-2920.13685

    Article  PubMed  Google Scholar 

  16. Gylfe A, Bergstrom S, Lunstrom J, Olsen B (2000) Epidemiology - reactivation of Borrelia infection in birds. Nature 403:724–725

    Article  CAS  Google Scholar 

  17. Gern L, Siegenthaler M, Hu CM, Leuba-Garcia S, Humair PF, Moret J (1994) Borrelia burgdorferi in rodents (Apodemus flavicollis and A. sylvaticus): duration and enhancement of infectivity for Ixodes ricinus ticks. Eur J Epidemiol 10:75–80. https://doi.org/10.1007/bf01717456

    Article  CAS  PubMed  Google Scholar 

  18. Richter D, Klug B, Spielman A, Matuschka FR (2004) Adaptation of diverse Lyme disease spirochetes in a natural rodent reservoir host. Infect Immun 72:2442–2444. https://doi.org/10.1128/iai.72.4.2442-2444.2004

  19. Richter D, Spielman A, Komar N, Matuschka FR (2000) Competence of American robins as reservoir hosts for Lyme disease spirochetes. Emerg Infect Dis 6:133–138

    Article  CAS  Google Scholar 

  20. Norte AC, Lopes de Carvalho I, Nuncio MS, Araujo PM, Matthysen E, Albino Ramos J, Sprong H, Heylen D (2020) Getting under the birds’ skin: tissue tropism of Borrelia burgdorferi s.l. in naturally and experimentally infected avian hosts. Microb Ecol 79:756–769. https://doi.org/10.1007/s00248-019-01442-3

    Article  CAS  PubMed  Google Scholar 

  21. Kurtenbach K, Schäfer SM, de Michelis S, Etti S, Sewell H-S (2002) Borrelia burgdorferi sensu lato in the vertebrate host. In: Gray JS, Kahl O, Lane RS, Stanek G (eds) Lyme borreliosis: biology, epidemiology and control. CABI Publishing, New York, pp 117–150

    Chapter  Google Scholar 

  22. Leonhard S, Jensen K, Salkeld DJ, Lane RS (2010) Distribution of the Lyme disease spirochete Borrelia burgdorferi in naturally and experimentally infected western gray squirrels (Sciurus griseus). Vector Borne Zoon Dis 10:441–446. https://doi.org/10.1089/vbz.2009.0127

    Article  Google Scholar 

  23. Brown RN, Lane RS (1994) Natural and experimental Borrelia burgdorferi infections in woodrats and deer mice from California. J Wildl Dis 30:389–398. https://doi.org/10.7589/0090-3558-30.3.389

    Article  CAS  PubMed  Google Scholar 

  24. Newman EA, Eisen L, Eisen RJ, Fedorova N, Hasty JM, Vaughn C, Lane RS (2015) Borrelia burgdorferi sensu lato spirochetes in wild birds in northwestern California: associations with ecological factors, bird behavior and tick infestation. PLoS ONE 10:e0118146. https://doi.org/10.1371/journal.pone.0118146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. James MC, Furness RW, Bowman AS, Forbes KJ, 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

    Article  Google Scholar 

  26. Heylen D (2016) Ecological interactions between songbirds, ticks, and Borrelia burgdorferi s.l. in Europe. In: Braks MAH, van Wieren SE, Takken W, Sprong H (eds) Ecology and control of vector-borne diseases. Wageningen Academic Publishers, Wageningen, pp 91–101

    Google Scholar 

  27. Norte AC, Margos G, Becker NS, Albino Ramos J, Núncio MS, Fingerle V, Araújo PM, Adamík P, Alivizatos H, Barba E, Barrientos R, Cauchard L, Csörgő T, Diakou A, Dingemanse NJ, Doligez B, Dubiec A, Eeva T, Flaisz B, Grim T, Hau M, Heylen D, Hornok S, Kazantzidis S, Kováts D, Krause F, Literak I, Mänd R, Mentesana L, Morinay J, Mutanen M, Neto JM, Nováková M, Sanz JJ, Pascoal da Silva L, Sprong H, Tirri I-S, Török J, Trilar T, Tyller Z, Visser ME, Lopes de Carvalho I (2020) Host dispersal shapes the population structure of a tick-borne bacterial pathogen. Mol Ecol 29:485–501. https://doi.org/10.1111/mec.15336

    Article  PubMed  Google Scholar 

  28. Poupon MA, Lommano E, Humair PF, Douet W, Rais O, Schaad M, Jenni L, Gern L (2006) Prevalence of Borrelia burgdorferi sensu lato in ticks collected from migratory birds in Switzerland. Appl Environ Microbiol 72:976–979

    Article  CAS  Google Scholar 

  29. Humair PF, Turrian N, Aeschlimann A, Gern L (1993) Ixodes ricinus immatures on birds in a focus of Lyme borreliosis. Folia Parasitol 40:237–242

    CAS  Google Scholar 

  30. Olsen B, Jaenson TGT, Bergstrom S (1995) Prevalence of Borrelia burgdorferi sensu lato - infected ticks on migrating birds. Appl Environ Microbiol 61:3082–3087

    Article  CAS  Google Scholar 

  31. Lommano E, Dvorak C, Vallotton L, Jenni L, Gern L (2014) Tick-borne pathogens in ticks collected from breeding and migratory birds in Switzerland. Ticks Tick Borne Dis 5:871–882. https://doi.org/10.1016/j.ttbdis.2014.07.001

    Article  PubMed  Google Scholar 

  32. Norte A, de Carvalho I, Ramos J, Gonçalves M, Gern L, Núncio M (2012) Diversity and seasonal patterns of ticks parasitizing wild birds in western Portugal. Exp Appl Acarol 58:327–339. https://doi.org/10.1007/s10493-012-9583-4

    Article  CAS  PubMed  Google Scholar 

  33. Hau M, Haussmann MF, Greives TJ, Matlack C, Costantini D, Quetting M, Adelman JS, Miranda AC, Partecke J (2015) Repeated stressors in adulthood increase the rate of biological ageing. Front Zool 12:4. https://doi.org/10.1186/s12983-015-0095-z

    Article  PubMed  PubMed Central  Google Scholar 

  34. Rich EL, Romero LM (2005) Exposure to chronic stress downregulates corticosterone responses to acute stressors. Am J Phys Regul Integr Comp Phys 288:R1628–R1636. https://doi.org/10.1152/ajpregu.00484.2004

    Article  CAS  Google Scholar 

  35. Cyr NE, Earle K, Tam C, Romero LM (2007) The effect of chronic psychological stress on corticosterone, plasma metabolites, and immune responsiveness in European starlings. Gen Comp Endocrinol 154:59–66. https://doi.org/10.1016/j.ygcen.2007.06.016

    Article  CAS  PubMed  Google Scholar 

  36. Norris K, Evans MR (2000) Ecological immunology: life history trade-offs and immune defence in birds. Behav Ecol 11:19–26

    Article  Google Scholar 

  37. Norte AC, Costantini D, Araújo PM, Eens M, Ramos JA, Heylen DH (2018) Experimental infection by microparasites affects the oxidative balance in their avian reservoir host the blackbird Turdus merula. Tick Tick-Borne Dis 9:720–729

    Article  Google Scholar 

  38. Johnstone C, Reina R, Lill A (2012) Interpreting indices of physiological stress in free-living vertebrates. J Comp Physiol B 182:1–19. https://doi.org/10.1007/s00360-012-0656-9

    Article  Google Scholar 

  39. Courtney JW, Kostelnik LM, Zeidner NS, Massung RF (2004) Multiplex real-time PCR for detection of Anaplasma phagocytophilum and Borrelia burgdorferi. J Clin Microbiol 42:3164–3168. https://doi.org/10.1128/jcm.42.7.3164-3168.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Norte AC, Araújo PM, da Silva LP, Tenreiro PQ, Ramos JA, Núncio MS, Zé-Zé L, Lopes de Carvalho I (2015) Characterization through multilocus sequence analysis of Borrelia turdi isolates from Portugal. Microb Ecol 72:831–839. https://doi.org/10.1007/s00248-015-0660-1

    Article  PubMed  Google Scholar 

  41. Schutzer SE, Fraser-Liggett CM, Casjens SR, Qiu W-G, Dunn JJ, Mongodin EF, Luft BJ (2011) Whole-genome sequences of thirteen isolates of Borrelia burgdorferi. J Bacteriol 193:1018–1020. https://doi.org/10.1128/jb.01158-10

    Article  CAS  PubMed  Google Scholar 

  42. Johnson BJ, Happ CM, Mayer LW, Piesman J (1992) Detection of Borrelia burgdorferi in ticks by species-specific amplification gene. Am J Trop Med Hyg 47:730–741

    Article  CAS  Google Scholar 

  43. Hatchwell BJ, Wood MJ, Anwar M, Perrins CM (2000) The prevalence and ecology of the haematozoan parasites of European blackbirds, Turdus merula. Can J Zool 78:684–687

    Article  Google Scholar 

  44. Mata VA, da Silva LP, Lopes RJ, Drovetski SV (2015) The Strait of Gibraltar poses an effective barrier to host-specialised but not to host-generalised lineages of avian Haemosporidia. Int J Parasitol 45:711–719. https://doi.org/10.1016/j.ijpara.2015.04.006

    Article  PubMed  Google Scholar 

  45. Drovetski SV, Aghayan SA, Mata VA, Lopes RJ, Mode NA, Harvey JA, Voelker G (2014) Does the niche-breadth or trade-off hypothesis explain the abundance-occupancy relationship in avian haemosporidia? Mol Ecol 23:3322–3329. https://doi.org/10.1111/mec.12744

    Article  PubMed  Google Scholar 

  46. R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

  47. Feinstein AR (1975) XXXI. On the sensitivity, specificity, and discrimination of diagnostic tests. Clin Pharmacol Therap 17:104–116. https://doi.org/10.1002/cpt1975171104

    Article  CAS  Google Scholar 

  48. Dickens MJ, Earle KA, Romero LM (2009) Initial transference of wild birds to captivity alters stress physiology. Gen Comp Endocrinol 160:76–83. https://doi.org/10.1016/j.ygcen.2008.10.023

    Article  CAS  PubMed  Google Scholar 

  49. Davis AK, Maney DL, Maerz JC (2008) The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists. Funct Ecol 22:760–772. https://doi.org/10.1111/j.1365-2435.2008.01467.x

    Article  Google Scholar 

  50. Bishop CR, Athens JW, Boggs DR, Warner HR, Cartwright GE, Wintrobe MM (1968) Leukokinetic studies. 13. A non-steady-state kinetic evaluation of the mechanism of cortisone-induced granulocytosis. J Clin Invest 47:249–260. https://doi.org/10.1172/jci105721

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Dein JF (1986) Hematology. In: Harrison GJ, Harrison LR (eds) Clinical avian medicine and surgery. Sauders, London, pp 174–191

    Google Scholar 

  52. Biard C, Monceau K, Motreuil S, Moreau J (2015) Interpreting immunological indices: the importance of taking parasite community into account. An example in blackbirds (Turdus merula). Methods Ecol Evol 6:960–972. https://doi.org/10.1111/2041-210x.12371

    Article  Google Scholar 

  53. Dunn JC, Goodman SJ, Benton TG, Hamer KC (2013) Avian blood parasite infection during the non-breeding season: an overlooked issue in declining populations? BMC Ecol 13:30. https://doi.org/10.1186/1472-6785-13-30

    Article  PubMed  PubMed Central  Google Scholar 

  54. Bentz S, Rigaud T, Barroca M, Martin-Laurent F, Bru D, Moreau J, Faivre B (2006) Sensitive measure of prevalence and parasitaemia of haemosporidia from European blackbird (Turdus merula) populations: value of PCR-RFLP and quantitative PCR. Parasitology 133:685–692. https://doi.org/10.1017/s0031182006001090

    Article  CAS  PubMed  Google Scholar 

  55. Hellgren O, Križanauskienė A, Hasselquist D, Bensch S (2011) Low haemosporidian diversity and one key-host species in a bird malaria community in a mid-Atlantic island (São Miguel, Azores). J Wildl Dis 47:849–859. https://doi.org/10.7589/0090-3558-47.4.849

    Article  PubMed  Google Scholar 

  56. Dubska L, Literak I, Kocianova E, Taragelova V, Sverakova V, Sychra O, Hromadko M (2011) Synanthropic birds influence the distribution of Borrelia species: analysis of Ixodes ricinus ticks feeding on passerine birds. Appl Environ Microbiol 77:1115–1117

    Article  CAS  Google Scholar 

  57. Levin M, Levine JF, Yang S, Howard P, Apperson CS (1996) Reservoir competence of the southeastern five-lined skink (Eumeces inexpectatus) and the green anole (Anolis carolinensis) for Borrelia burgdorferi. Am J Trop Med Hyg 54:92–97

    Article  CAS  Google Scholar 

  58. Giery S, Ostfeld R (2007) The role of lizards in the ecology of Lyme disease in two endemic zones of the Northeastern United States. J Parasitol 93:511–517. https://doi.org/10.1645/GE-1053R1.1

    Article  PubMed  Google Scholar 

  59. Talleklint L, Jaenson TG (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 31:880–886

    Article  CAS  Google Scholar 

  60. Richter D, Schlee DB, Matuschka FR (2011) Reservoir competence of various rodents for the Lyme disease spirochete Borrelia spielmanii. Appl Environ Microbiol 77:3565–3570. https://doi.org/10.1128/aem.00022-11

  61. Caine JA, Coburn J (2015) A short-term Borrelia burgdorferi infection model identifies tissue tropisms and bloodstream survival conferred by adhesion proteins. Infect Immun 83:3184–3194. https://doi.org/10.1128/iai.00349-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Kurtenbach K, De Michelis S, Etti S, Schafer SM, Sewell HS, Brade V, Kraiczy P (2002) Host association of Borrelia burgdorferi sensu lato - the key role of host complement. Trends Microbiol 10:74–79

    Article  CAS  Google Scholar 

  63. Berndtson K (2013) Review of evidence for immune evasion and persistent infection in Lyme disease. Int J Gen Med 6:291–306. https://doi.org/10.2147/IJGM.S44114

    Article  PubMed  PubMed Central  Google Scholar 

  64. Barthold SW, Persing DH, Armstrong AL, Peeples RA (1991) Kinetics of Borrelia burgdorferi dissemination and evolution of disease after intradermal inoculation of mice. Am J Pathol 139:263–273

    CAS  PubMed  PubMed Central  Google Scholar 

  65. Barthold SW, de Souza MS, Janotka JL, Smith AL, Persing DH (1993) Chronic Lyme borreliosis in the laboratory mouse. Am J Pathol 143:959–971

    CAS  PubMed  PubMed Central  Google Scholar 

  66. Nardelli DT, Callister SM, Schell RF (2008) Lyme arthritis: current concepts and a change in paradigm. Clin Vaccine Immunol 15:21–34. https://doi.org/10.1128/CVI.00330-07

  67. Fischer CP, Wright-Lichter J, Romero LM (2018) Chronic stress and the introduction to captivity: how wild house sparrows (Passer domesticus) adjust to laboratory conditions. Gen Comp Endocrinol 259:85–92. https://doi.org/10.1016/j.ygcen.2017.11.007

    Article  CAS  PubMed  Google Scholar 

  68. Love AC, Lovern MB, DuRant SE (2017) Captivity influences immune responses, stress endocrinology, and organ size in house sparrows (Passer domesticus). Gen Comp Endocrinol 252:18–26. https://doi.org/10.1016/j.ygcen.2017.07.014

    Article  CAS  PubMed  Google Scholar 

  69. Dickens MJ, Romero LM (2009) Wild European starlings (Sturnus vulgaris) adjust to captivity with sustained sympathetic nervous system drive and a reduced fight-or-flight response. Physiol Biochem Zool 82:603–610. https://doi.org/10.1086/603633

    Article  PubMed  Google Scholar 

  70. Martin LB, Brace AJ, Urban A, Coon CAC, Liebl AL (2012) Does immune suppression during stress occur to promote physical performance? J Exp Biol 215:4097–4103. https://doi.org/10.1242/jeb.073049

    Article  PubMed  Google Scholar 

  71. Jones CR, Brunner JL, Scoles GA, Owen JP (2015) Factors affecting larval tick feeding success: host, density and time. Parasit Vectors 8:340–340. https://doi.org/10.1186/s13071-015-0955-6

    Article  PubMed  PubMed Central  Google Scholar 

  72. Wikel S (2013) Ticks and tick-borne pathogens at the cutaneous interface: host defenses, tick countermeasures, and a suitable environment for pathogen establishment. Front Microbiol 4. https://doi.org/10.3389/fmicb.2013.00337

  73. Keesing F, Brunner J, Duerr S, Killilea M, LoGiudice K, Schmidt K, Vuong H, Ostfeld RS (2009) Hosts as ecological traps for the vector of Lyme disease. Proc R Soc B 276:3911–3919. https://doi.org/10.1098/rspb.2009.1159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Jacquet M, Genne D, Belli A, Maluenda E, Sarr A, Voordouw MJ (2017) The abundance of the Lyme disease pathogen Borrelia afzelii declines over time in the tick vector Ixodes ricinus. Parasit Vectors 10:257. https://doi.org/10.1186/s13071-017-2187-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Kurtenbach K, Peacey M, Rijpkema SG, Hoodless AN, Nuttall PA, Randolph SE (1998) Differential transmission of the genospecies of Borrelia burgdorferi sensu lato by game birds and small rodents in England. Appl Environ Microbiol 64:1169–1174

    Article  CAS  Google Scholar 

  76. Humair PF, Rais O, Gern L (1999) Transmission of Borrelia afzelii from Apodemus mice and Clethrionomys voles to Ixodes ricinus ticks: differential transmission pattern and overwintering maintenance. Parasitol 118(Pt 1):33–42

    Article  Google Scholar 

  77. Schwan TG, Piesman J (2002) Vector interactions and molecular adaptations of Lyme disease and relapsing fever spirochetes associated with transmission by ticks. Emerg Infect Dis 8:115–121. https://doi.org/10.3201/eid0802.010198

    Article  PubMed  PubMed Central  Google Scholar 

  78. Horká H, Černá-Kýčková K, Skallová A, Kopecký J (2009) Tick saliva affects both proliferation and distribution of Borrelia burgdorferi spirochetes in mouse organs and increases transmission of spirochetes to ticks. Int J Med Microbiol 299:373–380. https://doi.org/10.1016/j.ijmm.2008.10.009

  79. Zeidner NS, Schneider BS, Nuncio MS, Gern L, Piesman J (2002) Coinoculation of Borrelia spp. with tick salivary gland lysate enhances spirochete load in mice and is tick species–specific. J Parasitol 88:1276–1278. https://doi.org/10.1645/0022-3395(2002)088[1276:cobswt]2.0.co;2

  80. Lefeuvre B, Cantero P, Ehret-Sabatier L, Lenormand C, Barthel C, Po C, Parveen N, Grillon A, Jaulhac B, Boulanger N (2020) Effects of topical corticosteroids and lidocaine on Borrelia burgdorferi sensu lato in mouse skin: potential impact to human clinical trials. Sci Rep 10:10552. https://doi.org/10.1038/s41598-020-67440-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Hyde JA (2017) Borrelia burgdorferi keeps moving and carries on: a review of borrelial dissemination and invasion. Front Immunol 8. https://doi.org/10.3389/fimmu.2017.00114

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Acknowledgements

We thank Camilo Carneiro, Afonso Rocha, João Gameiro da Silva, Estela Marques and Maria Clara Martins for help with fieldwork and maintenance of birds in captivity. Instituto da Conservação da Natureza e Florestas IP, Central Nacional de Anilhagem, Mata Nacional do Choupal and Tapada Nacional de Mafra provided conditions for fieldwork and bird ringing.

Funding

This study received financial support from Fundação para a Ciência e a Tecnologia by the strategic programme of MARE (MARE - UID/MAR/04292/2020) and the fellowship (SFRH/BPD/108197/2015) and transitory norm contract DL57/2016/CP1370/CT89 to ACN, and the Portuguese National Institute of Health. PMA was funded by an investigator contract from the project “PTDC/BIA-EVL/31569/2017 - NORTE -01-0145- FEDER-30288,” co-funded by NORTE2020 through Portugal 2020 and FEDER Funds, and by National Funds through FCT; RJL was funded by national funds (Transitory Norm contract DL57/2016/CP1440/CT0006).

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ACN, JAR and ILC conceived and designed the study. ACN and PMA performed the experiments and analysed the data. ACN, ILC, LA, HG, SS and RJL collected data and performed laboratory work. All authors contributed to the writing of the manuscript.

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Correspondence to A. C. Norte.

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The authors assert that all procedures contributing to this work comply with the ethical standards of the relevant national and institutional guides on the care and use of laboratory animals and were performed under licence of the competent authorities (Licence No. 694/2016/CAPT and No. 10/2017/CAPT).

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Norte, A.C., Araújo, P.M., Augusto, L. et al. Effects of stress exposure in captivity on physiology and infection in avian hosts: no evidence of increased Borrelia burgdorferi s.l. infectivity to vector ticks. Microb Ecol 83, 202–215 (2022). https://doi.org/10.1007/s00248-021-01738-3

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