Role of migratory birds in introduction and range expansion of Ixodes scapularis ticks and of Borrelia burgdorferi and Anaplasma phagocytophilum in Canada

Abstract

During the spring in 2005 and 2006, 39,095 northward-migrating land birds were captured at 12 bird observatories in eastern Canada to investigate the role of migratory birds in northward range expansion of Lyme borreliosis, human granulocytic anaplasmosis, and their tick vector, Ixodes scapularis. The prevalence of birds carrying I. scapularis ticks (mostly nymphs) was 0.35% (95% confidence interval [CI] = 0.30 to 0.42), but a nested study by experienced observers suggested a more realistic infestation prevalence of 2.2% (95% CI = 1.18 to 3.73). The mean infestation intensity was 1.66 per bird. Overall, 15.4% of I. scapularis nymphs (95% CI = 10.7 to 20.9) were PCR positive for Borrelia burgdorferi, but only 8% (95% CI = 3.8 to 15.1) were positive when excluding nymphs collected at Long Point, Ontario, where B. burgdorferi is endemic. A wide range of ospC and rrs-rrl intergenic spacer alleles of B. burgdorferi were identified in infected ticks, including those associated with disseminated Lyme disease and alleles that are rare in the northeastern United States. Overall, 1.4[corrected]% (95% CI = 0.3 [corrected] to 0.41) of I. scapularis nymphs were PCR positive for Anaplasma phagocytophilum. We estimate that migratory birds disperse 50 million to 175 million I. scapularis ticks across Canada each spring, implicating migratory birds as possibly significant in I. scapularis range expansion in Canada. However, infrequent larvae and the low infection prevalence in ticks carried by the birds raise questions as to how B. burgdorferi and A. phagocytophilum become endemic in any tick populations established by bird-transported ticks.

FIG. 1.

Locations of bird observatories that participated in the study. Abbreviations for the names of Canadian provinces and U.S. states, respectively, are as follows: MB, Manitoba; ON, Ontario; QC, Quebec; NB, New Brunswick; NS, Nova Scotia; and MN, Minnesota; WI, Wisconsin; MI, Michigan; OH, Ohio; PA, Pennsylvania; NY, New York; NE, New England states; and ME, Maine. Filled triangles indicate the locations of bird observatories participating in the study: 1, Thunder Cape; 2, Pelee Island; 3, Long Point (comprising the Old Cut, Breakwater, and Tip observatories); 4, Haldimand (comprising the Ruthven, Rock Point, and Selkirk observatories); 5, Tommy Thompson Park, Toronto; 6, Prince Edward Point; 7, McGill, Montreal; 8, Atlantic, Nova Scotia.

FIG. 2.

An unrooted neighbor-joining distance tree of rrs-rrl IGS of B. burgdorferi. Reference sequences were taken from the work of Bunikis et al. (7). Sequences obtained in this study are in bold with identifying numbers prefixed by “RSP.” Nonparametric bootstrap values for nodes with ≥65% support in both NJ and MP analyses are shown above and below the branches, respectively. Tree topologies involving nodes with ≥65% bootstrap support were identical in both NJ and MP analyses.