3.1. Tick Collection
During the 4-year study period (2013–2016), a total of 1265 ixodid ticks representing 27 tick species belonging to four genera (Amblyomma
, five; Dermacentor
, three; Haemaphysalis
, one; Ixodes
, 18) were collected from avian and mammalian hosts Canada-wide (Table 1
, Table 2
, Table 3
, Table 4
, Table 5
and Table 6
). The tick–host associations consist of (1) 16 tick species taking a blood meal from birds; (2) 25 tick species feeding on mammals; and (3) 10 tick species that parasitize both birds and mammals. Overall, 14 of 27 tick species are known to bite humans (Table 1
]. However, Ixodes brunneus
is a true bird-associated tick [23
], and parasitism of humans by this ectoparasite would be very unlikely.
Eight co-infestations (seven double, one triple) were identified (Table 6
). The triple co-infestation consisted of Ixodes angustus
(male, female), Ixodes pacificus
(western blacklegged tick) (nymph, Bbsl-positive), and Ixodes spinipalpis
(nymph). When we looked at earlier tick–host studies [7
], and compared their findings with our dataset, we discovered a number of range extensions for certain tick species, namely I. cookei
, Ixodes gregsoni
(a mustelid-feeding tick), I. spinipalpis
, Ixodes rugosus
, and Ixodes texanus
(raccoon tick) (Figure 1
). From a medical standpoint, we collected an I. spinipalpis
nymph from a human; the nymph tested negative for Bbsl. Because I. spinipalpis
has vector competence for Bbsl, this tick species has the potential to transmit Lyme disease spirochetes to people.
In this study, we report many novel host records for ticks on birds and mammals (Table 6
). The two focal study areas comprise: (a) Pacific region: Metchosin-Victoria-Vancouver-Maple Ridge in southwestern British Columbia (Table 2
and Table 3
) and (b) Eastern region: London-St. Thomas-Simcoe-Toronto in southern Ontario (Table 4
and Table 5
). In southwestern B.C., 22 I. cookei
were collected from three different mammal species (American mink, Pacific raccoon, and striped skunk). In addition, I. pacificus
, Ixodes rugosus
, Ixodes soricis
(shrew tick), I. spinipalpis
, and I. texanus
were collected from mammals on Vancouver Island (Figure 1
). Excluding I. soricis
and including the avian coastal tick, Ixodes auritulus
, we put forward a 6-tick, enzootic maintenance transmission cycle of Lyme disease spirochetes in southeastern region of Vancouver Island.
In southwestern Ontario, 27 larval and nymphal specimens of A. longirostre, which are native to the Neotropics, were collected from neotropical songbirds during northward spring migration.
In order to answer a long-standing question of how long I. cookei live, we determined the longevity of one generation of I. cookei: 4201 days (11.51 years). The breakdown for the developmental life stages (egg, larva, nymph, and adult) was 55 days, 614 days, 919 days, and 2613 days (female), respectively. This dataset provides rudimentary information on the sustainment of I. cookei, and represent the longest living individuals for each developmental life stage.
We provide two novel tick–host records for blacklegged ticks, Ixodes scapularis (northern populations previously considered Ixodes dammini), on passerine birds. A fully engorged I. scapularis nymph was collected from a Bay-breasted Warbler, Setophaga castanea, on 15 May 2015 at Ste-Anne-de-Bellevue, Québec during spring migration. This replete nymph underwent ecdysis to a female in 72 days. Likewise, two I. scapularis larvae were collected from a hatch-year Tennessee Warbler, Vermivora peregrina, at Ruthven Park, Ontario on 1 September 2013 during fall migration.
In the Pacific region, the most common avian host parasitized by ticks was the Song Sparrow, whereas in the Eastern region, the Common Yellowthroat, a ground-foraging passerine, was most frequently parasitized by ixodid ectoparasites (Figure 2
We report 34 I. angustus
ticks (29 females, five males) parasitizing a red squirrel at East Sooke, British Columbia on 28 October 2013; this heavy tick infestation constitutes the first documentation of Bbsl-positive I. angustus
on this sciurid species in Canada (Figure 3
We collected 24 I. rugosus nymphs from a river otter at Esquimalt, B.C.; not only is this collection a new host record, it is the first account of this tick species on Vancouver Island. Additionally, we collected a single I. texanus female from a Pacific raccoon at Colwood, Vancouver Island; this collection is the southernmost record in British Columbia.
3.3. Spirochete Detection
We sampled a wide cross section of ticks collected coast to coast, and tested 18 tick species for Bbsl (Table 1
). Of the 18 tick species tested, 15 species (83%) were positive for Bbsl and, of these systemically infected ticks, 6 species bite humans. In the Western region, we collected 25 I. rugosus
nymphs (one from a striped skunk, and 24 from a river otter), but none was positive for Lyme disease spirochetes. It is noteworthy that 11 (35%) of 31 I. angustus
adults were positive for Bbsl. In the Pacific coastal region, we detected Bbsl in three tick species parasitizing birds (Table 2
) and, likewise, in seven tick species infesting mammals (Table 3
In southwestern B.C., 5 (23%) of 22 I. cookei
, which were collected from three different mammalian hosts (i.e., Pacific raccoon, American mink, and striped skunk) were positive for Bbsl (Table 3
). Specifically, the biogeographic breakdown for Bbsl-positive I. cookei
in southwestern B.C. was Mainland, 2 and Vancouver Is., 3. Our data provide newfound evidence of Lyme disease spirochetes in I. cookei
in far-western Canada.
A single I. soricis tick was collected from a roadkill vagrant shrew on the southern shoreline of Vancouver Island, B.C.; it was not tested for Lyme disease spirochetes, but instead, kept as a voucher specimen.
Notably, 17 (77%) of 22 I. auritulus larvae collected from a Fox Sparrow, Passerella iliaca, were positive for Bbsl, which suggests that this ground-frequenting songbird is a reservoir-competent host.
In the eastern Canadian region, we detected Bbsl in two tick species parasitizing birds (Table 4
) and, similarly, in four species infesting mammals (Table 5
). Notably, 16 (59%) of 27 I. scapularis
nymphs collected from ground-foraging songbirds during northward spring migration were infected with Lyme disease spirochetes. Additionally, we collected Bbsl-infected I. scapularis
larvae from a northern short-tailed shrew, which reaffirms that this small mammal is a reservoir-competent host.
In the laboratory (J.F.A.), the majority of cultures became contaminated, and only one culture produced motile spirochetes. This culture was PCR positive for Bbsl, but it was not sent for DNA sequencing.
Of epidemiological significance, 1 of 27 A. longirostre ticks was positive for Bbsl; this is the first report of a Bbsl-positive A. longirostre parasitizing a bird in North America. In addition, we provide the first report of Bbsl in I. brunneus and I. texanus in Canada.