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The Macroecology and Evolution of Avian Competence for Borrelia Burgdorferi: Supplemental Information

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The Macroecology and Evolution of Avian Competence for Borrelia Burgdorferi: Supplemental Information The macroecology and evolution of avian competence for Borrelia burgdorferi: Supplemental Information Daniel J. Becker, Barbara A. Han S1. Literature search S2. Variation in larval Bbsl prevalence S3. Trait-based analysis dataset S4. Phylogenetic meta-analysis S5. Phylogenetic factorization S6. Boosted regression trees S1. Literature search Figure S1. PRIMSA diagram documenting the data collection and inclusion process for Bbsl competence of avian hosts. We ran all systematic searches in January 2020 and supplemented results by extracting data from references cited in systematically identified studies. Records identified with Web of Additional records identified Science (n = 399) with PubMed (n = 210) and CAB Abstracts (n = 145) Identification Records after duplicates removed (n = 489) Screening Records screened Records excluded (n = 489) (n = 263) Full-text articles excluded for being Full-text articles reviews, not reporting assessed for eligibility larval tick Bbsl data, (n = 226) pooling tick life stages or bird species, or Eligibility reporting non-Bbsl Borrelia (n = 133) Studies included in qualitative synthesis (n = 93 + 9 from references) Studies included in Included quantitative synthesis (n = 93 + 9 from references) Included studies 1. Hubalek Z, Juricova Z, Halouzka J. A survey of free-living birds as hosts and lessors of microbial pathogens. Folia Zoologica. 1995;44: 1–11. 2. Piesman J, Dolan MC, Schriefer ME, Burkot TR. Ability of Experimentally Infected Chickens to Infect Ticks with the Lyme Disease Spirochete, Borrelia burgdorferi. The American Journal of Tropical Medicine and Hygiene. 1996;54: 294–298. doi:10.4269/ajtmh.1996.54.294 3. Wright SA, Lemenager DA, Tucker JR, Armijos MV, Yamamoto SA. An Avian Contribution to the Presence of Ixodes pacificus (Acari: Ixodidae) and Borrelia burgdorferi on the Sutter Buttes of California. J Med Entomol. 2006;43: 368–374. doi:10.1093/jmedent/43.2.368 4. Humair P-F, Postic D, Wallich R, Gern L. An Avian Reservoir (Turdus merula) of the Lyme Borreliosis Spirochetes. Zentralblatt für Bakteriologie. 1998;287: 521–538. doi:10.1016/S0934- 8840(98)80194-1 5. Muñoz-Leal S, Lopes MG, Marcili A, Martins TF, González-Acuña D, Labruna MB. Anaplasmataceae, Borrelia and Hepatozoon agents in ticks (Acari: Argasidae, Ixodidae) from Chile. Acta Tropica. 2019;192: 91–103. doi:10.1016/j.actatropica.2019.02.002 6. Franke J, Moldenhauer A, Hildebrandt A, Dorn W. Are birds reservoir hosts for Borrelia afzelii? Ticks and Tick-borne Diseases. 2010;1: 109–112. doi:10.1016/j.ttbdis.2010.03.001 7. Schneider SC, Parker CM, Miller JR, Page Fredericks L, Allan BF. Assessing the Contribution of Songbirds to the Movement of Ticks and Borrelia burgdorferi in the Midwestern United States During Fall Migration. EcoHealth. 2015;12: 164–173. doi:10.1007/s10393-014-0982-3 8. Pascucci I, Di Domenico M, Capobianco Dondona G, Di Gennaro A, Polci A, Capobianco Dondona A, et al. Assessing the role of migratory birds in the introduction of ticks and tick- borne pathogens from African countries: An Italian experience. Ticks and Tick-borne Diseases. 2019;10: 101272. doi:10.1016/j.ttbdis.2019.101272 9. Hanincová K, Taragelová V, Koci J, Schäfer SM, Hails R, Ullmann AJ, et al. Association of Borrelia garinii and B. valaisiana with songbirds in Slovakia. Appl Environ Microbiol. 2003;69: 2825–2830. 10. Hamer SA, Hickling GJ, Keith R, Sidge JL, Walker ED, Tsao JI. Associations of passerine birds, rabbits, and ticks with Borrelia miyamotoi and Borrelia andersonii in Michigan, USA. Parasites & vectors. 2012;5: 231. 11. Anderson JF, Magnarelli LA. Avian and mammalian hosts for spirochete-infected ticks and insects in a Lyme disease focus in Connecticut. The Yale journal of biology and medicine. 1984;57: 627. 12. Wright SA, Tucker JR, Donohue AM, Castro MB, Kelley KL, Novak MG, et al. Avian Hosts of Ixodes pacificus (Acari: Ixodidae) and the Detection of Borrelia burgdorferi in Larvae Feeding on the Oregon Junco. J Med Entomol. 2011;48: 852–859. doi:10.1603/ME11001 13. Norte AC, Ramos JA, Gern L, Núncio MS, Carvalho IL de. Birds as reservoirs for Borrelia burgdorferi s.l. in Western Europe: circulation of B. turdi and other genospecies in bird–tick cycles in Portugal. Environmental Microbiology. 2013;15: 386–397. doi:10.1111/j.1462- 2920.2012.02834.x 14. Taragel’ová V, Koči J, Hanincová K, Kurtenbach K, Derdáková M, Ogden NH, et al. Blackbirds and Song Thrushes Constitute a Key Reservoir of Borrelia garinii, the Causative Agent of Borreliosis in Central Europe. Appl Environ Microbiol. 2008;74: 1289–1293. doi:10.1128/AEM.01060-07 15. Norte AC, Carvalho IL de, Núncio MS, Ramos JA, Gern L. Blackbirds Turdus merula as competent reservoirs for Borrelia turdi and Borrelia valaisiana in Portugal: evidence from a xenodiagnostic experiment. Environmental Microbiology Reports. 2013;5: 604–607. doi:10.1111/1758-2229.12058 16. Sonenshine DE, Ratzlaff RE, Troyer J, Demmerle S, Demmerle ER, Austin WE, et al. Borrelia burgdorferi in Eastern Virginia: Comparison between a Coastal and Inland Locality. The American Journal of Tropical Medicine and Hygiene. 1995;53: 123–133. doi:10.4269/ajtmh.1995.53.123 17. Magnarelli LA, Stafford III KC, Bladen VC. Borrelia burgdorferi in Ixodes dammini (Acari: Ixodidae) feeding on birds in Lyme, Connecticut, U.S.A. Can J Zool. 1992;70: 2322–2325. doi:10.1139/z92-311 18. Levine JF, Sonenshine DE, Nicholson WL, Turner RT. Borrelia burgdorferi in ticks (Acari: Ixodidae) from coastal Virginia. Journal of medical entomology. 1991;28: 668–674. 19. Radzijevskaja J, Rosef O, Matulaitytė V, Paulauskas A. Borrelia burgdorferi sensu lato genospecies in Ixodes ricinus ticks feeding on passerine birds in southern Norway. Biologija. 2016;62. doi:10.6001/biologija.v62i2.3338 20. Kjelland V, Stuen S, Skarpaas T, Slettan A. Borrelia burgdorferi sensu lato in Ixodes ricinus ticks collected from migratory birds in Southern Norway. Acta Veterinaria Scandinavica. 2010;52: 59. doi:10.1186/1751-0147-52-59 21. Mannelli A, Nebbia P, Tramuta C, Grego E, Tomassone L, Ainardi R, et al. Borrelia burgdorferi sensu lato Infection in Larval Ixodes ricinus (Acari: Ixodidae) Feeding on Blackbirds in Northwestern Italy. J Med Entomol. 2005;42: 168–175. doi:10.1093/jmedent/42.2.168 22. Newman EA, Eisen L, Eisen RJ, Fedorova N, Hasty JM, Vaughn C, et al. Borrelia burgdorferi Sensu Lato Spirochetes in Wild Birds in Northwestern California: Associations with Ecological Factors, Bird Behavior and Tick Infestation. PLOS ONE. 2015;10: e0118146. doi:10.1371/journal.pone.0118146 23. Amore G, Tomassone L, Grego E, Ragagli C, Bertolotti L, Nebbia P, et al. Borrelia lusitaniae in immature Ixodes ricinus (Acari: Ixodidae) feeding on common wall lizards in Tuscany, central Italy. Journal of medical entomology. 2007;44: 303–307. 24. Cicuttin GL, De Salvo MN, Venzal JM, Nava S. Borrelia spp. in ticks and birds from a protected urban area in Buenos Aires city, Argentina. Ticks and Tick-borne Diseases. 2019;10: 101282. doi:10.1016/j.ttbdis.2019.101282 25. Hubalek Z, Anderson JF, Halouzka J, Hajek V. Borreliae in immature Ixodes ricinus (Acari: Ixodidae) ticks parasitizing birds in the Czech Republic. Journal of medical entomology. 2014;33: 766–771. 26. Heylen D, Krawczyk A, Carvalho IL de, Núncio MS, Sprong H, Norte AC. Bridging of cryptic Borrelia cycles in European songbirds. Environmental Microbiology. 2017;19: 1857– 1867. doi:10.1111/1462-2920.13685 27. Norte AC, Araújo PM, da Silva LP, Tenreiro PQ, Ramos JA, Núncio MS, et al. Characterization Through Multilocus Sequence Analysis of Borrelia turdi Isolates from Portugal. Microb Ecol. 2016;72: 831–839. doi:10.1007/s00248-015-0660-1 28. Miyamoto K, Sato Y, Okada K, Fukunaga M, Sato F. Competence of a migratory bird, red- bellied thrush (Turdus chrysolaus), as an avian reservoir for the Lyme disease spirochetes in Japan. Acta Tropica. 1997;65: 43–51. doi:10.1016/S0001-706X(97)00651-7 29. Richter D, Spielman A, Komar N, Matuschka FR. Competence of American robins as reservoir hosts for Lyme disease spirochetes. Emerg Infect Dis. 2000;6: 133–138. 30. Kurtenbach K, Carey D, Hoodless AN, Nuttall PA, Randolph SE. Competence of Pheasants as Reservoirs for Lyme Disease Spirochetes. J Med Entomol. 1998;35: 77–81. doi:10.1093/jmedent/35.1.77 31. Scott JD, Clark KL, Coble NM, Ballantyne TR. Detection and Transstadial Passage of Babesia Species and Borrelia burgdorferi Sensu Lato in Ticks Collected from Avian and Mammalian Hosts in Canada. Healthcare. 2019;7: 155. doi:10.3390/healthcare7040155 32. Scott JD, Lee M-K, Fernando K, Durden LA, Jorgensen DR, Mak S, et al. Detection of Lyme disease spirochete, Borrelia burgdorferi sensu lato, including three novel genotypes in ticks (Acari: Ixodidae) collected from songbirds (Passeriformes) across Canada. Journal of Vector Ecology. 2010;35: 124–139. doi:10.1111/j.1948-7134.2010.00068.x 33. Movila A, Alekseev AN, Dubinina HV, Toderas I. Detection of tick-borne pathogens in ticks from migratory birds in the Baltic region of Russia. Medical and Veterinary Entomology. 2013;27: 113–117. doi:10.1111/j.1365-2915.2012.01037.x 34. Stern C, Kaiser A, Maier WA, Kampen H. Die Rolle von Amsel (Turdus merula), Rotdrossel (Turdus iliacus) und Singdrossel (Turdus philomelos) als Blutwirte für Zecken (Acari: Ixodidae) und Reservoirwirte für vier Genospezies des Borrelia burgdorferi-Artenkomplexes. Mitt Dtsch Ges Allg Angew Ent. 2006;15: 349–356. 35. Gryczyńska A, Kowalec M. Different Competence as a Lyme Borreliosis Causative Agent Reservoir Found in Two Thrush Species: The Blackbird (Turdus merula) and the Song Thrush (Turdus philomelos). Vector-Borne and Zoonotic Diseases. 2019;19: 450–452. doi:10.1089/vbz.2018.2351 36. Dubska L, Literak I, Kocianova E, Taragelova V, Sychra O. 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.
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