Worldwide, wild birds play a vital role in the dispersal of ticks that harbour tick-borne pathogens, including Borrelia burgdorferi, the Lyme disease bacterium. Using PCR testing, we found 124 (31%) of 405 ticks (4 species), which were collected from 21 species of birds in far-western Canada, to be infected with B. burgdorferi. Transstadial transmission of B. burgdorferi occurred from larva to nymph, plus nymph to adult, in the avian coastal tick, Ixodes auritulus, collected from songbirds in British Columbia (B.C). Collectively, all 3 motile life stages (larva, nymph, adult) of this tick had an infection prevalence of 31% for B. burgdorferi, which suggests vector competency. A Pacific Wren was highly infested with I. auritulus immatures, and 20 (44%) of 45 ticks (2 nymphs, 43 larvae) were infected with B. burgdorferi. This heavy infestation shows the high potential to initiate a new population of ticks and to disseminate Lyme spirochetes. Epidemiologically, B. burgdorferi-infected I. auritulus larvae collected from the Spotted Towhee, Swainson’s Thrush, Pacific Wren, and Fox Sparrow suggest that these avian hosts act as reservoirs for B. burgdorferi. In this study, the western blacklegged tick, Ixodes pacificus, and Ixodes spinipalpis played a limited role in the enzootic transmission cycle of B. burgdorferi along coastal B.C. We document the first record of I. spinipalpis on a bird in Alberta. Because songbirds widely disperse Lyme disease vector ticks, primary health providers and the general public must be vigilant that outdoors people may be bitten by B. burgdorferi-infected ticks throughout far-western Canada.
Worldwide, Lyme disease (Lyme borreliosis) is present in more than 80 countries, and the causative agent infects a wide diversity of vertebrates, including wild birds. In the United States of America, this debilitating disease has been estimated to cost $1.3 billion annually [
Passerine birds (order: Passeriformes), commonly called songbirds, are hosts for certain hard-bodied ticks (Ixodida: Ixodidae) that carry pathogenic microorganisms. These blood-sucking ectoparasites carry a wide group of tick-borne pathogens, including the Lyme disease bacterium, Borrelia burgdorferi sensu lato (s.l.) Johnson, Schmidt, Hyde, Steigerwalt & Brenner (hence B. burgdorferi) [
Wild birds are capable of transporting ticks long distances during migratory flight. These tick-infested migrants are normally moving from winter grounds to breeding ranges and vice versa. Migratory birds carry attached ticks hundreds of kilometres within and between continents [
Ixodes auritulus, which is found exclusively on birds [
In North America, Ixodes muris parasitizes domestic and wildlife animals, such as mice, shrews, rats, and several species of birds [
Ixodes pacificus has a geographic range from southwestern Canada to northern Mexico (i.e., Baja California) [
Ixodes spinipalpis is a nidicolous tick in semiarid regions, and has a host range from southwestern Canada to Texas [
The present study was designed to determine: 1) the infection prevalence of B. burgdorferi in bird-feeding ticks and 2) pinpoint passerine species that are most heavily involved in tick infestations and enzootic maintenance of Lyme disease spirochetes.
Ticks were collected from wild-caught songbirds at various times of the year at 9 locations from Alberta and British Columbia, 2010-2012 (
also employed [
Dead ticks were directly tested using DNA extraction and polymerase chain reaction (PCR) analysis, whereas live ticks were cultured in Barbour-Stoenner-Kelly (BSK) medium and, subsequently, underwent DNA extraction and PCR amplification. The detailed PCR protocol that we used, including primers, and its accuracy in detecting B. burgdorferi in live, dried, and alcohol preserved specimens, was thoroughly described by Persing et al. [
The I. spinipalpis specimen (10-5A7), which was collected from a White-crowned Sparrow at Cypress Hills Interprovincial Park, Alberta, was deposited in the Biodiversity Institute of Ontario (University of Guelph, Guelph, Ontario, Canada) with accession number BIO-12-120.
A total of 405 Ixodes ticks consisting of 4 species were collected from 21 bird species by bird banders and wildlife rehabilitators in Alberta and British Columbia (B.C.), Canada (
No. of ticks positive/No. of ticks tested (%) | ||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Ixodes auritulus | I. muris | I. pacificus | I. spinipalpis | |||||||||||
Bird species | L | N | F | F | L | N | L | N | Infection prevalence (%) | |||||
Spotted Towhee Pipilo maniculatus Swainson | 2/2 | 6/16 | 1/1 | 0/0 | 0/0 | 0/3 | 0/1 | 1/1 | 10/24 (42) | |||||
Swainson’s Thrush Catharus ustulatus Nuttall | 1/2 | 24/36 | 1/8 | 0/0 | 0/0 | 0/0 | 0/0 | 0/0 | 26/46 (57) | |||||
Song Sparrow Melospiza melodia (Wilson) | 0/1 | 9/29 | 0/1 | 0/0 | 0/0 | 0/0 | 0/1 | 0/4 | 9/36 (25) | |||||
House Wren Troglodytes aedon Vieillot | 0/0 | 0/0 | 2/2 | 0/0 | 0/0 | 0/1 | 0/1 | 0/0 | 2/4 (50) | |||||
American Robin Turdus migratorius L. | 0/0 | 0/0 | 0/5 | 0/0 | 0/0 | 0/0 | 0/0 | 0/0 | 0/5 (0) | |||||
Bewick’s Wren Thryomanes bewickii (Audubon) | 0/0 | 1/2 | 0/1 | 0/0 | 0/0 | 0/0 | 0/0 | 1/1 | 2/4 (50) | |||||
Pacific Wren Troglodytes pacificus S.F. Baird | 19/43 | 1/3 | 2/4 | 0/0 | 0/0 | 0/0 | 0/0 | 0/0 | 22/50 (50) | |||||
Wilson’s Warbler Wilsonia pusilla (Wilson) | 0/2 | 1/2 | 0/0 | 0/0 | 0/0 | 0/0 | 0/0 | 0/0 | 1/4 (25) | |||||
Common Yellowthroat Geothlypis trichas (L.) | 0/0 | 0/4 | 0/1 | 0/1 | 0/0 | 0/0 | 0/0 | 0/0 | 0/5 (0) | |||||
Savannah Sparrow Passerculus sandwichensis (Gmelin) | 0/0 | 0/1 | 0/0 | 0/0 | 0/0 | 0/0 | 0/0 | 0/0 | 0/1 (0) | |||||
Lincoln’s Sparrow Melospiza lincolnii (Audubon) | 0/0 | 4/5 | 0/0 | 0/0 | 0/0 | 0/0 | 0/0 | 0/0 | 4/5 (80) | |||||
Fox Sparrow Passerella iliaca (Merrem) | 23/97 | 19/82 | 2/4 | 0/0 | 0/0 | 0/0 | 0/0 | 0/0 | 44/183 (24) | |||||
Golden-crowned Sparrow Zonotrichia atricapilla (Gmelin) | 0/0 | 0/0 | 0/1 | 0/0 | 0/0 | 0/0 | 0/0 | 0/0 | 0/1 (0) | |||||
Brown-headed Cowbird Molothrus ater (Boddaert) | 0/0 | 0/0 | 0/1 | 0/0 | 0/0 | 0/0 | 0/0 | 0/0 | 0/1 (0) | |||||
Puget Sound White-crowned Sparrow Zonotrichia leucophrys pugetensis (Forster) | 0/0 | 0/2 | 0/0 | 0/0 | 0/0 | 0/0 | 1/2 | 0/0 | 1/5 (20) | |||||
Oregon Junco Junco hyemalis oreganus (L.) | 0/0 | 1/3 | 1/2 | 0/0 | 0/0 | 0/0 | 0/0 | 0/0 | 2/5 (40) | |||||
Hermit Thrush Catharus guttatus (Pallas) | 0/11 | 0/3 | 1/1 | 0/0 | 0/0 | 0/0 | 0/0 | 0/0 | 1/15 (7) | |||||
White-throated Sparrow Zonotrichia albicollis (Gmelin) | 0/0 | 0/3 | 0/2 | 0/0 | 0/0 | 0/0 | 0/0 | 0/0 | 0/5 (0) | |||||
Orange-crowned Warbler Vermivora celata (Say) | 0/0 | 0/0 | 0/1 | 0/0 | 0/0 | 0/0 | 0/0 | 0/0 | 0/1 (0) | |||||
Chipping Sparrow Spizella passerina (Bechstein) | 0/0 | 0/1 | 0/1 | 0/0 | 0/1 | 0/0 | 0/0 | 0/0 | 0/3 (0) | |||||
MacGillivray’s Warbler Oporornis tolmiei (Townsend) | 0/0 | 0/1 | 0/0 | 0/0 | 0/0 | 0/0 | 0/0 | 0/0 | 0/1 (0) | |||||
Totals | 45/158 | 66/193 | 10/37 | 0/1 | 0/1 | 0/4 | 1/5 | 2/6 | 124/405 (31) | |||||
L, larva (e); N, nymph (s); F, female (s).
Using PCR amplification, 124 (31%) of 405 tested ticks were infected with B. burgdorferi. As well, 121 (31%) of 388 I. auritulus (females, nymphs, larvae) were infected. These numbers clearly show that wild birds are dispersing ticks and the human pathogen, B. burgdorferi, in the Canadian Far-West.
New host records in Canada include: 1) I. auritulus (nymph; B. burgdorferi-positive) on a Bewick’s Wren, 2) I. pacificus (larva; molted after 36 d) on an Orange-crowned Warbler, and 3) I. spinipalpis (larva; molted after 44 d) on a Puget Sound White-crowned Sparrow. A fully engorged I. auritulus nymph was collected from a Fox Sparrow on 8 November 2012, and constitutes the latest date in the bird banding season that we have collected this tick species. DNA sequencing was not conducted on any of the four B. burgdorferi isolates.
Our findings highlight four Ixodes species that are dispersed by passerine birds in far-western Canada. Along the West Coast, all 3 motile life stages of I. auritulus were well represented and the predominant tick species on residential and migratory songbirds. Notably, some of the passerines with attached B. burgdorferi-infected larvae are candidates for reservoir competency. In Alberta, we documented for the first time I. spinipalpis on birds east of the Rockies. Each of the 4 Ixodes species in our study is involved in the enzootic transmission cycle of B. burgdorferi.
The collection of a fully engorged I. spinipalpis nymph from a White-crowned Sparrow, Zonotrichia leucophrys (Forster) at Cypress Hills Interprovincial Park, Elkwater Lake, Alberta on 15 May 2010 constitutes the first record of this tick species on an avian host in this province. The nymph molted to a female in 60 d, and represents the northernmost reported recovery of I. spinipalpis on a songbird in North America.
In addition, 2 fully engorged I. spinipalpis larvae were collected from a House Wren, Troglodytes aedon (Viellot) on 9 June 2010 at the same location; these larvae molted to nymphs in 32 d and 33 d, respectively. One of these ticks was tested for B. burgdorferi, and it was negative.
Previously, I. scapularis immatures were reported in Alberta [
Also, I. spinipalpis immatures were previously collected from mammalian hosts on the east face of the Rocky Mountains and on the southern fringe of Alberta bordering Montana, USA [
The successful passage of viable B. burgdorferi during the larva-nymph and nymph-adult molts suggest vector competence of I. auritulus. In the present study, we document new reports of transstadial transmission of B. burgdorferi in I. auritulus (
In this study, we recorded heavy infestations of I. auritulus on certain songbirds during October. Most notably, we recovered 45 I. auritulus (2 nymphs, 43 larvae) from a Pacific Wren on 11 October 2010 at Rocky Point, B.C. and, of these ticks, 20 (1 nymph, 19 larvae) were positive for B. burgdorferi. In addition, 42 I. auritulus (4 nymphs, 38 larvae) were collected from a Fox Sparrow on 7 October 2010 at the same location; 18 of these ticks (2 nymphs, 16 larvae) were positive for B. burgdorferi. Because larvae were infected with B. burgdorferi in both cases, these infestations strongly suggest that these passerines are reservoir-competent hosts. Based on the close proximity to the state of Washington, USA, migratory songbirds could act as cross-border carriers of Lyme disease vector ticks, especially during southward fall migration. Collectively, I. auritulus is one of at least 4 congeneric species of ticks parasitizing wild birds in B.C. Epidemiologically, these resident and migratory birds could easily initiate new Lyme disease foci.
Tick ID. No. | Bird species | Date ticks collected | Life Stage pre-molt post-molt | Days to molt | Presence of B. burgdorferi |
---|---|---|---|---|---|
Larva-nymph molt | |||||
12-5A126B | Fox Sparrow | 15 Oct 2012 | Larva―nymph | 57 | Amplicon |
12-5A130A | Spotted Towhee | 17 Oct 2012 | Larva―nymph | 52 | Amplicon |
Nymph-adult molt | |||||
10-5A46 | Bewick’s Wren | 24 Aug 2012 | Nymph―female | 49 | Live culture |
11-5A62B | Lincoln’sSparrow | 11 Sep 2012 | Nymph―female | 47 | Amplicon |
11-5A62C | same host | 11 Sep 2012 | Nymph―female | 47 | Amplicon |
11-5A62D | same host | 11 Sep 2012 | Nymph―male | 43 | Amplicon |
11-5A64 | Swainson’s Thrush | 14 Sep 2012 | Nymph―male | 48 | Amplicon |
11-5A70A | Fox Sparrow | 06 Oct 2012 | Nymph―male | 54 | Amplicon |
11-5A70B | same host | 06 Oct 2012 | Nymph―male | 53 | Amplicon |
12-5A82 | Swainson’s Thrush | 11 Sep 2012 | Nymph―female | 55 | Amplicon |
12-5A142 | Fox Sparrow | 08 Nov 2012 | Nymph―male | 43 | Amplicon |
High tick infestations can occur when ground-foraging songbirds transect a microhabitat where gravid females lay their eggs. Wild birds eat ticks [
In addition, because I. auritulus only parasitizes birds, the presence of Lyme disease spirochetes in all 3 life stages of I. auritulus indicates that a large mammal, such as a Sitka black-tailed deer, Odocoileus hemionus sitkensis (Rafinesque), is not required to perpetuate B. burgdorferi in this enzootic transmission cycle. In essence, I. auritulus is an exemplar of a single tick species that can perpetuate B. burgdorferi.
Our findings are consistent with other tick studies that show that songbirds have the capability to initiate new tick populations in distant locations [
The relative number of I. pacificus and I. spinipalpis immatures was low because our sampling effort was mainly conducted during the post-fledging and autumn migration (mid-August to early November). In the western coastal bioregion, the peak questing activity for I. pacificus larvae is mid-summer, whereas, for nymphs, it is during the period of mid-April to mid-June. For I. spinipalpis immatures, larvae are active from April to September, while nymphs have host-seeking activity mainly from April to October [
The lack of B. burgdorferi infection in larval and nymphal I. pacificus in this study could be due to a number of ecological factors. The absence of B. burgdorferi in I. pacificus larvae substantiates the fact that this tick species does not exhibit transovarial transmission, and does not support the transfer of B. burgdorferi from gravid females to larval offspring and, therefore, unfed larvae are typically devoid of spirochetal infection [
A single I. muris female was collected from a Common Yellowthroat, Geothlypis trichas (L.), on 11 August 2010 at Revelstoke, B.C., and it tested negative for B. burgdorferi. Previously, I. muris specimens were collected from passerines in British Columbia and, in 2008 [
The presence of B. burgdorferi in larval ticks collected from songbirds exemplifies the fact that certain birds are reservoirs for spirochetes. Using uninfected xenodiagnostic larvae, Richter et al. [
mit borreliae to humans.
Across Canada, songbirds play a significant role in the epidemiology of Lyme disease. In central and eastern Canada, Scott and Durden [
In conclusion, resident and migratory songbirds are disseminators of borreliae. The present study provides additional evidence to show that all 3 motile stages of I. auritulus play a vital role in maintaining B. burgdorferi in the environment along the Pacific Coast. When B. burgdorferi-infected I. auritulus larvae and nymphs transmit spirochetes to Canadian songbirds, these avian hosts can transmit spirochetal infection to I. muris, I. pacificus and I. spinipalpis, which could act as bridge vectors and later bite humans. Passerines have the ability to quickly and easily move ticks and tick-associated pathogens long distances to new foci and, at the same time, act as reservoirs of B. burgdorferi. Most significantly, cohabitation of I. auritulus, I. muris, I. pacificus, and I. spinipalpis increase the public health risk of contracting Lyme disease along Canada’s Pacific Coast.
We thank the following bird banders for collecting ticks from songbirds: Yousif Attia, Emily Barnewall, Troy Blondin, Christina Carrieres, Marianne Dawson, Louise Dykslag, Jessie Fanucchi, Andrea Follet, Vanessa Garland, Christina Lam, Susanne Maidment, Ann Nightingale, Michal Pavlik, Brian Pomfret, Amélia Rousseau, Rick Schortinghuis, and Acacio Spencer-Hills. We are indebted to Elizabeth A. Alves for technical assistance and, for computer graphics, John Ward and Ashton Ropp. For financial support, we thank Lyme Ontario and the Canadian Lyme Disease Foundation.