Skip to main content
Log in

Assessing the Contribution of Songbirds to the Movement of Ticks and Borrelia burgdorferi in the Midwestern United States During Fall Migration

  • Original Contribution
  • Published:
EcoHealth Aims and scope Submit manuscript

Abstract

The geographic distributions of Ixodes scapularis (black-legged tick) and the bacterium Borrelia burgdorferi (the causative agent of Lyme disease) are expanding in the USA. To assess the role of migratory songbirds in the spread of this tick and pathogen, we captured passerines in central Illinois during the fall of 2012. We compared forested sites in regions where I. scapularis populations were either previously or not yet established. Ticks were removed from birds and blood samples were taken from select avian species. Ticks were identified by morphology and molecular techniques were used to detect B. burgdorferi and other tick-borne pathogens in ticks and avian blood samples. Ixodes spp. were detected on 10 of 196 migrants (5.1%), with I. scapularis larvae found on 2 individuals. Borrelia burgdorferi sensu stricto was detected in the blood of 9 of 29 birds sampled (31%), yet only 1 infected bird was infested by ticks. The ticks were mostly Haemaphysalis leporispalustris and I. dentatus larvae, and none tested positive for B. burgdorferi. Infestation of birds by Ixodes spp. differed significantly by region, while B. burgdorferi infection did not. These data suggest that migratory birds may play a larger role in the dispersal of B. burgdorferi than previously realized.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Allan BF, Goessling LS, Storch GA, Thach RE (2010) Blood meal analysis to identify reservoir hosts for Amblyomma americanum ticks. Emerging Infectious Diseases 16:433-440

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Altizer S, Bartel R, Han BA (2011) Animal migration and infectious disease risk. Science 331:296-331

    Article  CAS  PubMed  Google Scholar 

  • Anderson JF (1989) Epizootiology of Borrelia in Ixodes tick vectors and reservoir hosts. Reviews of Infectious Diseases 2:S1451-S1459

    Article  Google Scholar 

  • Anderson JF, Magnarelli LA, LeFebvre RB, Andreadis TG, McAninch JB, Perng G, Johnson RC (1989) Antigenically variable Borrelia burgdorferi isolated from cottontail rabbits and Ixodes dentatus in rural and urban areas. Journal of Clinical Microbiology 27:13-20

    PubMed Central  CAS  PubMed  Google Scholar 

  • Bacon RM, Kugeler KJ, Mead PS (2008) Surveillance for Lyme disease—United States, 1992–2006. Morbidity and Mortality Weekly Report 57:1-9

    Google Scholar 

  • Barbour AG, Fish D (1993) The biological and social phenomenon of Lyme disease. Science 260:1610-1616

    Article  CAS  PubMed  Google Scholar 

  • Battaly GR, Fish D, Dowler RC (1987) The seasonal occurrence of Ixodes dammini and Ixodes dentatus (Acari: Ixodidae) on birds in a Lyme disease endemic area of southeastern New York State. Journal of the New York Entomological Society 1987:461-468

    Google Scholar 

  • Bouseman JK, Kitron U, Kirkpatrick CE, Siegel J, Todd KS (1990) Status of Ixodes dammini (Acari: Ixodidae) in Illinois. Journal of Medical Entomology, 27:556-560

    Article  CAS  PubMed  Google Scholar 

  • Brinkerhoff RJ, Folsom-O’Keefe CM, Tsao K, Diuk-Wasser MA (2011a) Do birds affect Lyme disease risk? Range expansion of the vector-borne pathogen Borrelia burgdorferi. Frontiers in Ecology and the Environment 9:103-110

    Article  Google Scholar 

  • Brinkerhoff RJ, Folsom-O’Keefe CM, Streby HM, Bent SJ, Tsao K, Diuk-Wasser MA (2011b) Regional variation in immature Ixodes scapularis parasitism on North American songbirds: Implications for transmission of the Lyme pathogen, Borrelia burgdorferi. Journal of Medical Entomology 48:422-428

    Article  PubMed  Google Scholar 

  • Brownstein JS, Holford TR, Fish D (2005) Effect of climate change on Lyme disease risk in North America. EcoHealth 2: 38-46

    Article  PubMed Central  PubMed  Google Scholar 

  • Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. The Journal of Parasitology 83:575-583

    Article  CAS  PubMed  Google Scholar 

  • Centers for Disease Control and Prevention (1999) Appendix methods used for creating a national Lyme disease risk map. Morbidity and Mortality Weekly Report 48(07):21-24

    Google Scholar 

  • Clark K, Hendricks A, Burge D (2005) Molecular identification and analysis of Borrelia burgdorferi sensu lato in lizards in the southeastern United States. Applied and Environmental Microbiology 71:2616-2625

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cortinas M, Kitron U (2006) County-level surveillance of white-tailed deer infestation by Ixodes scapularis and Dermacentor albipictus (Acari: Ixodidae) along the Illinois River. Journal of Medical Entomology 43:810-819

    Article  PubMed  Google Scholar 

  • Dennis DT, Nekomoto TS, Victor JC, William S, Piesman J (1998) Reported distribution of Ixodes scapularis and Ixodes pacificus (Acari: Ixodidae) in the United States. Journal of Medical Entomology 35:629–638

  • Durden LA, McLean RG, Oliver JH Jr, Ubico SR, James AM (1997) Ticks, Lyme disease spirochetes, trypanosomes, and antibody to encephalitis viruses in wild birds from coastal Georgia and South Carolina. The Journal of parasitology 83:1178-1182

    Article  CAS  PubMed  Google Scholar 

  • Durden LA, Keirans JE (1996) Nymphs of the genus Ixodes (Acari: Ixodidae) of the United States: Taxonomy, identification key, distribution, hosts, and medical/veterinary importance. Thomas Say Publications in Entomology, Entomological Society of America

    Google Scholar 

  • Durden LA, Oliver JH, Kinsey AA (2001) Ticks (Acari: Ixodidae) and spirochetes (Spirochaetaceae: Spirochaetales) recovered from birds on a Georgia barrier island. Journal of medical entomology 38:231-236

    Article  CAS  PubMed  Google Scholar 

  • Guerra M, Walker E, Jones C, Paskewitz S, Cortinas MR, Stancil A, Beck L, Bobo M, Kitron U (2002) Predicting the risk of Lyme disease: Habitat suitability for Ixodes scapularis in the north central United States. Emerging Infectious Diseases 8:289-297

    Article  PubMed Central  PubMed  Google Scholar 

  • Gylfe Å, Bergström S, Lundstróm J, Olsen B (2000) Epidemiology: reactivation of Borrelia infection in birds. Nature 403: 724-725

    Article  CAS  PubMed  Google Scholar 

  • Hamer SA, Goldberg TL, Kitron UD, Brawn JD, Anderson TK, Loss SR, Walker ED, Hamer GL (2012) Wild birds and urban ecology of ticks and tick-borne pathogens, Chicago, Illinois, USA, 2005–2010. Emerging Infectious Diseases 18:21589-1595

    Article  Google Scholar 

  • Hamer SA, Hickling GJ, Sidge JL, Rosen ME, Walker ED, Tsao JL (2011) Diverse Borrelia burgdorferi strains in a bird-tick cryptic cycle. Applied and Environmental Microbiology 77:1999-2007

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hamer SA, Tsao JL, Walker ED, Hickling GJ (2010) Invasion of the Lyme disease vector Ixodes scapularis: Implications for Borrelia burgdorferi endemicity. EcoHealth 7:47-63

    Article  PubMed  Google Scholar 

  • Hammer B, Moter A, Kahl O, Alberti G, Göbel UB (2001) Visualization of Borrelia burgdorferi sensu lato by fluorescence in situ hybridization (FISH) on whole-body sections of Ixodes ricinus ticks and gerbil skin biopsies. Microbiology 147:1425-1436

    CAS  PubMed  Google Scholar 

  • Harrison BA, Engber BR, Apperson CS (1997) Ticks (Acari: Ixodidae) uncommonly found biting humans in North Carolina. Journal of Vector Ecology 22:6-12

    CAS  PubMed  Google Scholar 

  • Illinois Department of Public Health (2011) Known geographic distribution of Ixodes scapularis by county in Illinois, 2011. Springfield, IL

    Google Scholar 

  • Johnson RC, Schmid GP, Hyde FW, Steigerwalt AG, Brenner DJ (1984) Borrelia burgdorferi sp. nov.: Etiologic agent of Lyme disease. International Journal of Systematic Bacteriology 34:496-497

    Article  Google Scholar 

  • Keirans JE, Hutcheson H, Durden LA, Klompen J (1996) Ixodes scapularis (Acari: Ixodidae): Redescription of all active stages, distribution, hosts, geographical variation, and medical and veterinary importance. Journal of Medical Entomology 33:297-318

    Article  CAS  PubMed  Google Scholar 

  • Killilea M, Swei A, Lane R, Briggs C, Ostfeld R (2008) Spatial dynamics of Lyme disease: a review. EcoHealth 5:167-195

    Article  PubMed  Google Scholar 

  • Kinsey AA, Durden LA, Oliver JH Jr (2000) Tick infestations of birds in coastal Georgia and Alabama. Journal of Parasitology 86:251-254

    Article  CAS  PubMed  Google Scholar 

  • Kollars TM, Oliver JH (2003) Host associations and seasonal occurrence of Haemaphysalis leporispalustris, Ixodes brunneus, I. cookie, I. dentatus, and I. texanus (Acari: Ixodidae) in southeastern Missouri. Journal of Medical Entomology 40:103-107

    Article  PubMed  Google Scholar 

  • Kong F, Gilbert GL (2006) Multiplex PCR-based reverse line blot hybridization assay (mPCR/RLB) – a practical epidemiological and diagnostic tool. Nature Protocols 1:2668-2680

    Article  CAS  PubMed  Google Scholar 

  • Madhav NK, Brownstein JS, Tsao JI, Fish D (2004) A dispersal model for the range expansion of blacklegged tick (Acari: Ixodidae). Journal of Medical Entomology 41: 842-852

    Article  PubMed  Google Scholar 

  • Marra PP, Francis CM, Mulvihill RS, Moore FR (2005) The influence of climate on the timing and rate of spring bird migration. Oecologia 142:307-315

    Article  PubMed  Google Scholar 

  • McDonald JS, Miller KV (1993) A history of white-tailed deer restocking in the United States 1878 to 1992. Research Publication 93-1. The Quality of Deer Management Association, Watkinsville, GA

    Google Scholar 

  • Ogden N, Lindsay L, Hanincová K, Barker I, Bigras-Poulin M, Charron D, Heagy A, Francis C, O’Callaghan C, Schwartz I (2008) Role of migratory birds in introduction and range expansion of Ixodes scapularis ticks and of Borrelia burgdorferi and Anaplasma phagocytophilum in Canada. Applied and Environmental Microbiology 74:1780-1790

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ogden NH, Maarouf A, Barker IK, Bigras-Poulin M, Lindsay LR, Morshed MG, O’Callaghan CJ, Ramsay F, Waltner-Towes D, Charron DF (2006) Climate change and the potential for range expansion of the Lyme disease vector Ixodes scapularis in Canada. International Journal of Parasitology 36:63-70

    Article  CAS  PubMed  Google Scholar 

  • Owen JC (2011) Collecting, processing, and storing avian blood: A review. Journal of Field Ornithology 82:339-354

    Article  Google Scholar 

  • Peters, HS (1930) Ectoparasites and bird-banding. Bird-Banding 1: 51-60

    Article  Google Scholar 

  • Pichon B, Egan D, Rogers M, Gray J (2003) Detection and identification of pathogens and host DNA in unfed host-seeking Ixodes ricinus L. (Acari: Ixodidae). Journal of Medical Entomology 40:723-731

    Article  CAS  PubMed  Google Scholar 

  • Poole AE (2005) The birds of North America Online. Cornell Laboratory of Ornithology, Ithaca, NY. http://bna.birds.cornell.edu/BNA. Accessed July 3, 2013

  • Rand PW, Lacombe EH, Smith RP, Ficker J (1998) Participation of birds (Aves) in the emergence of Lyme disease in southern Maine. Journal of Medical Entomology 35:270–276

  • Rijpkema SG, Molkenboer MJ, Schouls LM, Jongejan F, Schellekens JF (1995) Simultaneous detection and genotyping of three groups of Borrelia burgdorferi sensu lato in Dutch Ixodes ricinus ticks by characterization of the amplified intergenic spaces region between 5S and 23S rRNA genes. Journal of clinical microbiology 33:3091-3095

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sauer JR Hines JE, Fallon JE, Pardieck KL, Ziolkowski DJ, Link WA (2014) The North American Breeding Bird Survey, results and analyses 1966–2012. Version 02.19.2014. USGS Patuxent Wildlife Research Center, Laurel, MD

  • Scott JD, Fernando K, Banerjee SN, Durden LA, Byrne SK, Banerjee M, Mann RB, Morshe MG (2001) Birds disperse Ixodid (Acarei: Ixodidae) and Borrelia burgdorferi-infected ticks in Canada. Journal of Medical Entomology 38:493–500

  • Smith RP, Rand PW, Lacombe EH, Morris SR, Holmes DW, Caporale DA (1996) Role of bird migration in the long-distance dispersal of Ixodes dammini, the vector of Lyme disease. Journal of Infectious Diseases 174:221-224

    Article  PubMed  Google Scholar 

  • Sonenshine DE (1979) Ticks of Virginia. Virginia Polytechnic Institute and State University, College of Agriculture and Life Sciences, Blacksburg, VA

    Google Scholar 

  • Telford SR III, Mather TN, Moore SI, Wilson ML, Spielman A (1988) Incompetence of deer as reservoirs of the Lyme disease spirochete. American Journal of Tropical Medicine and Hygiene 39:105-109

    PubMed  Google Scholar 

  • Telford SR, Spielman A (1989) Competence of a rabbit-feeding Ixodes (Acari: Ixodidae) as a vector of the Lyme disease spirochete. Journal of Medical Entomology 26:118-121

    Article  PubMed  Google Scholar 

  • Weisbrod AR, Johnson RC (1989) Lyme disease and migrating birds in the Saint Croix River Valley. Applied and Environmental Microbiology 55:1921–1924

Download references

Acknowledgments

This study was funded by the College of Agriculture, Consumer, and Environmental Science’s Office of Research and the School of Integrative Biology at the University of Illinois at Urbana-Champaign. We are grateful to numerous private landowners and public land managers for facilitating this research. We thank Jack Stenger for assistance with mist netting and Tyler Hedlund for assistance with tick identification.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to James R. Miller.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 27 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Schneider, S.C., Parker, C.M., Miller, J.R. et al. Assessing the Contribution of Songbirds to the Movement of Ticks and Borrelia burgdorferi in the Midwestern United States During Fall Migration. EcoHealth 12, 164–173 (2015). https://doi.org/10.1007/s10393-014-0982-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10393-014-0982-3

Keywords

Navigation