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Article

Extensive Distribution of the Lyme Disease Bacterium, Borrelia burgdorferi Sensu Lato, in Multiple Tick Species Parasitizing Avian and Mammalian Hosts across Canada

by
John D. Scott
1,*,
Kerry L. Clark
2,
Janet E. Foley
3,
John F. Anderson
4,
Bradley C. Bierman
2 and
Lance A. Durden
5
1
International Lyme and Associated Diseases Society, Bethesda, MD 20827, USA
2
Environmental Epidemiology Research Laboratory, Department of Public Health, University of North Florida, Jacksonville, FL 32224, USA
3
Department of Medicine and Epidemiology, School of Veterinary Medicine, University of California, Davis, CA 95616, USA
4
Department of Entomology, Center for Vector Ecology and Zoonotic Diseases, The Connecticut Agricultural Experiment Station, New Haven, CT 06504, USA
5
Department of Biology, Georgia Southern University, Statesboro, GA 30458, USA
*
Author to whom correspondence should be addressed.
Healthcare 2018, 6(4), 131; https://doi.org/10.3390/healthcare6040131
Submission received: 13 September 2018 / Revised: 2 November 2018 / Accepted: 2 November 2018 / Published: 12 November 2018
(This article belongs to the Special Issue Lyme Disease and Related Tickborne Infections)
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Abstract

:
Lyme disease, caused by the spirochetal bacterium, Borrelia burgdorferi sensu lato (Bbsl), is typically transmitted by hard-bodied ticks (Acari: Ixodidae). Whenever this tick-borne zoonosis is mentioned in medical clinics and emergency rooms, it sparks a firestorm of controversy. Denial often sets in, and healthcare practitioners dismiss the fact that this pathogenic spirochetosis is present in their area. For distribution of Bbsl across Canada, we conducted a 4-year, tick–host study (2013–2016), and collected ticks from avian and mammalian hosts from Atlantic Canada to the West Coast. Overall, 1265 ticks representing 27 tick species belonging to four genera were collected. Of the 18 tick species tested, 15 species (83%) were positive for Bbsl and, of these infected ticks, 6 species bite humans. Overall, 13 of 18 tick species tested are human-biting ticks. Our data suggest that a 6-tick, enzootic maintenance cycle of Bbsl is present in southwestern B.C., and five of these tick species bite humans. Biogeographically, the groundhog tick, Ixodes cookei, has extended its home range from central and eastern Canada to southwestern British Columbia (B.C.). We posit that the Fox Sparrow, Passerella iliaca, is a reservoir-competent host for Bbsl. The Bay-breasted Warbler, Setophaga castanea, and the Tennessee Warbler, Vermivora peregrina, are new host records for the blacklegged tick, Ixodes scapularis. We provide the first report of a Bbsl-positive Amblyomma longirostre larva parasitizing a bird; this bird parasitism suggests that a Willow Flycatcher is a competent reservoir of Bbsl. Our findings show that Bbsl is present in all provinces, and that multiple tick species are implicated in the enzootic maintenance cycle of this pathogen. Ultimately, Bbsl poses a serious public health contagion Canada-wide.

1. Introduction

Lyme disease (Lyme borreliosis) is caused by members of the Borrelia burgdorferi sensu lato (Bbsl) complex [1]. This spirochetal bacterium is typically transmitted by certain blood-sucking, ixodid ticks (Acari: Ixodidae) to vertebrates, including humans. Bbsl infections present a wide spectrum of clinical manifestations from asymptomatic, to acute, to chronic, to fatal outcomes. Since Bbsl has diverse morphological forms, and is highly adaptive, this stealth pathogen can evade and slip by the immune system [2,3,4], and may instigate a persistent, life-altering spirochetosis [5,6]. Acarologists have documented 40 tick species parasitizing vertebrate hosts in Canada [7,8,9]; however, many of these tick species have not been tested for the presence of Bbsl.
Ticks have been present in Canada since antiquity. Based on phenology, migratory birds have been transporting ticks into Canada since the last ice age 10,000 years ago. Each year, neotropical and southern temperate songbirds transport ticks across the Canada-U.S. border into Canada during northward spring migration, and widely disperse bird-feeding ticks country-wide [10,11,12,13,14,15]. Likewise, long-distance migrating passerines (Passeriformes) import Amblyomma ticks, such as A. americanum (lone star tick), A. dissimile, A. humerale, A. maculatum (Gulf Coast tick), A. longirostre, and A. rotundatum into Canada from as far south as the northern part of South America [9,10,11,16,17]. The home ranges of A. dissimile and A. longirostre in north-central South America coincide with the migration patterns and wintering grounds of certain neotropical songbirds and, with plentiful energy reserves and southerly tailwinds, these passerine migrants provide rapid transport for Amblyomma ticks to Canada.
Using a mathematical computer model, researchers recently purported that A. americanum has the potential to establish in Montreal, Canada [18]. In contrast, our 3-year overwinter survival study at Fergus, Ontario, reveals that A. americanum larvae do not overwinter in southwestern Ontario (J.D.S., unpublished data). Even though A. americanum nymphs and adults may overwinter, larvae do not. When migrating songbirds transport larval and nymphal A. americanum ticks into Canada, they release fully engorged larvae and nymphs into the leaf litter and humus layer. During the late spring and early summer, replete larvae and nymphs undergo ecdysis (molt) to become nymphs or adults, respectively, and parasitize domestic and wildlife animals [19]. During the blood meal, this invasive tick species commonly transmits foreign pathogens to vertebrates, including humans.
Certain areas across Canada have Lyme disease foci where multiple species of ticks are present. For instance, Scott et al. documented 9 tick species in the vicinity of Kenora, Ontario, and eight species tested positive for Bbsl [20]. From a medical standpoint, five of these tick species are known to bite humans [21].
The primary aims of this study were to (i) ascertain the distribution of Bbsl-positive ticks across Canada; (ii) establish the prevalence of Bbsl in ticks parasitizing avian and mammalian hosts in certain regions; (iii) determine whether any tick species shifted their home range; and (iv) assess the number of tick species that potentially bite humans and inflict Lyme disease.

2. Materials and Methods

2.1. Tick Collection

Ticks were obtained from hosts by various means. They were collected from birds and mammals by bird banders, wildlife rehabilitators, and biologists. Ticks were also obtained from citizens who removed them from themselves, their pets, birds, and animals killed on roads. When ticks were collected by bird banders, birds were promptly aged, weighed, sexed, and then released to the wild. Attached ticks were removed with fine-pointed, stainless steel forceps. If ticks were damaged upon removal, they were placed in 2 mL micro tubes (Sarstedt) containing 94% ethyl alcohol. Otherwise, live ticks were put in a transparent, round-bottom, 8.5 mL polypropylene tube (15.7 mm × 75 mm, round based) (Sarstedt). The mouth of the tube was covered with tulle netting (3 cm diameter) to allow ventilation for ticks. A polyethylene push cap, with a 7-mm hole, was placed into the mouth of the tube to secure the tulle netting, and prevent tick escapes. Each tube, which contained the ticks from one host, was placed in a double-zipped plastic bag with a slightly moistened paper towel to maintain high humidity. All ticks were sent to the lab for identification (J.D.S.). With the exception of two specimens, these ticks were identified using taxonomic keys for larvae [22], nymphs [23], and adults [24]. Since all Amblyomma larvae molted to nymphs, nymphal keys were used for this genus [25,26,27]. Any ticks that were fully engorged were held to molt to the next life stage or, in the case of females, to lay eggs. Ixodes species were exposed to a long-day photoperiod of 16:8 h (L:D). Bird-feeding Amblyomma ticks from the Neotropics were held at a photoperiod of 12:12 h (L:D). Complete records (i.e., geographic location, tick collection date, tick species, developmental life stage, and host species) were logged for each tick collection.
We tabulated the life span of one generation of the groundhog tick, Ixodes cookei. We held eggs, larvae, nymphs, males, and females in outdoor housing units at 85% to 100% relative humidity year-round to see how long each life stage would live.
Ethical approval and informed consent are not required because removal of ticks is not an invasive procedure, and no personal identifiable data were obtained.

2.2. Spirochete Detection

After identification, ticks were sent to three different laboratories for Bbsl testing because the first two institutions had policy changes during this study, and halted tick testing. The 3 sequential phases were: February 2013–June 2013 (J.F.A.), July 2014–June 2015 (K.L.C.), and July 2015–November 2016 (J.E.F.). During the first phase (J.F.A.), bacteria from live ticks were cultured in Barbour-Stoenner-Kelly (BSK) medium, whereas dead ticks were processed directly for DNA extraction followed by PCR (polymerase chain reaction) amplification. The DNA detection protocol was previously described [28,29,30]. Even though Persing et al. employed both the flagellin (flaB) gene and the major outer surface protein A (OspA) gene [28], this lab (J.F.A.) only used the OspA gene. Bona fide negative and positive controls were utilized.
In the second phase of our study, ticks were put directly in 94% ethyl alcohol, and forwarded to the lab (K.L.C.). These ticks were tested using a nested PCR that amplifies a portion of the flagellin (flaB) gene of Bbsl, with slight variations from a previously described protocol [31]. The primary PCR assay, which targets a 497-nt fragment of the flaB gene, used the following primers, 271F: 5′-AAG-GAA-TTG-GCA-GTT-CAA-TCA-GG-3′ and 767R: 5′-GCA-TTT-TCT-ATT-TTA-GCA-AGT-GAT-G-3′. The secondary (nested) PCR amplified a 437-nt internal fragment using primers 301F: 5′-ACA-TAT-TCA-GAT-GCA-GAC-AGA-GG-3′ and 737R: 5′-GCA-TCA-ACT-GTA-GTT-GTA-ACA-TTA-ACA-GG-3′.
In the third phase, ticks were directly put in 94% ethyl alcohol, and sent promptly by courier to the lab (J.E.F.). The protocol used for detecting Bbsl is outlined in Barbour et al. [32].
Since the occurrence of B. miyamotoi, a relapsing fever group spirochete, is deemed to be rare (<1%), we did not screen ticks for this microorganism. The PCR primers that we used were designed and applied in the study to specifically detect known species in the B. burgdorferi sensu lato complex.
In this study, the infection rate is the number of ticks infected with Bbsl divided by the number of ticks tested.

2.3. Molecular Tick Identification of Ixodes cookei

In order to confirm the identification of I. cookei collected in southwestern British Columbia, we used molecular methodology, and barcoded a larval tick (17-5A85L) hatched from the eggs of a gravid female, which was collected at North Saanich, Vancouver Island. The molecular identification was conducted at the Centre of Biodiversity Genomics (CBG), University of Guelph with accession number BIO-18-060. The DNA extract is being held at −80 °C at the same location. The collection data and barcode sequence is stored in BOLD, and can be accessed in the BOLD dataset at: dx.doi.org./10.5883/DS-IGAK.

3. Results

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) [21]. 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 [7,33], 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.

3.2. Molecular Tick Identification of Ixodes cookei

A gravid I. cookei female was collected from a striped skunk on 15 June 2017 at Saanich, Vancouver Island, B.C. This female laid eggs that hatched into larvae (BIO-18-060), and one of these larvae was barcoded at BIO (Biodiversity Institute of Ontario), University of Guelph, Ontario. The barcoding analysis confirmed the identification as I. cookei, and the nucleotide sequence was deposited in GenBank with accession number: MH338173.
Based on a sequence length of 620 bp, this larva had a 99.8% similarity match to three other I. cookei in BOLD. This molecular tick identification verifies the establishment of I. cookei in southwestern B.C.

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.

4. Discussion

We detected Bbsl in 15 of 18 tick species tested, and unveiled multiple host records nationwide (Table 6). In certain regions of Canada, we encountered several tick species in a complex enzootic maintenance cycle of Bbsl. In one particular locality on the Pacific coast, we encountered several tick species parasitizing avian and mammalian hosts, and some of these host-seeking ticks bite humans. Surprisingly, we observed instances where ticks had shifted their host range, or were noted for the first time. Because we collaborated closely with biologists and wildlife rehabilitators in certain locations, we were able to collect a proportionally larger number of ticks in these areas. From the Atlantic Ocean to the Pacific Ocean, we detected the Lyme disease spirochete in a continuum of 15 different tick species.

4.1. Tick Vector Competency for B. burgdorferi Sensu Lato

In total, eight tick species in our study are known to be competent vectors of Lyme disease spirochetes. They include Ixodes affinis, I. angustus, Ixodes dentatus (rabbit-associated tick), Ixodes minor, Ixodes muris (mouse tick), I. pacificus, I. scapularis, and I. spinipalpis [38]. Because all motile life stages (larvae, nymphs, and adults) of I. auritulus had significant Bbsl infection prevalence, and this tick species is exclusively parasitizes birds, we further indicate that I. auritulus has vector competence for Bbsl (Table 2) [39].

4.2. Ticks as Bridge Vector for B. burgdorferi Sensu Lato

In this study, we uncovered eight tick co-infestations (seven double species, one triple species) on vertebrates. When a Bbsl-infected tick parasitizes its host, it can transmit spirochetes during its blood meal. If the host is spirochetemic, it can then act as a source of Lyme disease spirochetes to other cofeeding ticks, either the same tick species or a different tick species. When these engorging ticks have fed to repletion, they drop off and undergo ecdysis before they can transmit spirochetes to suitable vertebrate hosts, including humans. Depending on the developmental life stage of the tick, the molt normally takes five to eight weeks. Both I. pacificus and I. scapularis are noted as the primary bridge vectors of Lyme disease spirochetes to humans [40].

4.3. Dispersal of Vector-Borne Pathogens

During this study, four genera (i.e., Amblyomma, Dermacentor, Haemaphysalis, and Ixodes) of ticks were collected from wild birds and terrestrial mammals across Canada. With the exception of I. affinis, I. minor, and Amblyomma species, the remainder of tick species are established and survive successfully in Canada. Migratory songbirds import bird-feeding ticks into Canada annually during spring migration, and these songbird-transported ticks and associated avifauna may be infected with a wide range of vector-borne, zoonotic pathogens. These bird parasitisms include Bbsl [10,11,12,13,14,15,41], Anaplasma phagocytophilum [12,42], Babesia spp. [42], Bartonella spp. [43], and vector-borne viruses [44,45]. Neotropical passerines migrate across national and intercontinental borders, and become long-range vectors for any zoonotic pathogen that they harbor. Overall, dispersal of Bbsl-infected ticks along migration routes is an important mechanism in the establishment of new endemic foci of tick-borne diseases [46].

4.4. Metchosin-Victoria-Vancouver-Maple Ridge Region

In southwestern B.C., Lyme disease spirochetes were detected in a wide range of tick species and associated vertebrate hosts that serve as reservoirs (Figure 1 and Table 2 and Table 3). In this coastal region, we detected Bbsl in six different tick species, namely I. angustus, I. auritulus, I. cookei, I. pacificus, I. spinipalpis, and I. texanus (Table 6). Ecologically, three tick species (i.e., I. auritulus, I. pacificus, and I. spinipalpis) feed on wild birds, whereas five tick species (i.e., I. angustus, I. cookei, I. pacificus, I. spinipalpis, and I. texanus) parasitize mammals. In order to form an interconnecting link between birds and mammals, I. pacificus and I. spinipalpis provide a bridge for Lyme disease spirochetes; this bridge also extends to humans. Collectively, five of these tick species bite humans, specifically I. angustus [47,48], I. cookei [48,49,50], I. pacificus [51], I. spinipalpis [52,53,54,55], and I. texanus [48,49]. Any of these tick species have the potential to be a vector of Lyme disease spirochetes to humans in far-western Canada.
Since passerines and raptors are parasitized by bird-feeding ticks, they provide an interconnecting link for Bbsl back and forth across the Salish Sea. More epidemiologic details on avian and mammalian hosts in this region are provided in Table 6. In the Pacific Northwest, I. auritulus is the most frequently occurring tick species parasitizing wild birds, namely raptors [30] and passerines [39]. In addition, several mammals act as reservoirs in an ongoing enzootic maintenance cycle of Bbsl along B.C.’s Pacific coast (Table 3).
Along the Pacific B.C. coast, I. auritulus plays a vital role in maintaining the presence of Lyme disease spirochetes. In all, 49 (48%) of 102 I. auritulus (larvae, nymphs, and adults) in this study were infected with Bbsl. Similarly, Scott et al. detected Bbsl in 31% of I. auritulus [39]. Although I. auritulus only parasitizes avifauna, both birds and mammals eat these ixodid ectoparasites, and may become systematically infected by oral inoculation [56].

4.5. London-St. Thomas-Simcoe-Toronto Region

The most commonly occurring tick species in our study was the blacklegged tick (Table 4 and Table 5). East of the Rocky Mountains, I. scapularis [57,58] is the most prevalent tick species on passerine migrants during northward spring migration (Table 4). Ecologically, the peak questing activity of nymphs coincides with peak spring migration of northbound passerine migrants.
Bbsl-positive I. scapularis larvae were collected from a northern short-tailed shrew, which reinforces that this insectivore is a reservoir host. This parasitism is consistent with other researchers who found that this shrew is a reservoir-competent host [59,60,61]. Because there is no transovarial transmission of Bbsl in I. scapularis females [62], we are confident that the source of infection was this spirochetemic host. This high-energy insectivore burrows through leaf litter and the humus layer, and has ample opportunity to become parasitized by Bbsl-infected I. scapularis immatures, especially in a Lyme disease endemic area.

4.6. Geographical Distribution of Ticks

We document new Canadian foci where certain tick species have been collected for the first time. Our novel tick findings may have been oversights by earlier tick studies [7,8] or unnoticed biogeographical shifts. Any ticks that are not transported by wild birds must have a terrestrial mode of transportation to occupy a new area.
East of the Rocky Mountains, bird-feeding Ixodes ticks, such as I. affinis [14,15,63], I. brunneus [14,15], I. dentatus [14,15], I. minor [36], and I. scapularis [11,13,14,15] can be transported long distances by migrating songbirds. Along the Pacific coast, I. auritulus, which is exclusively on birds [23], can be transported from the lower mainland to offshore islands, and established in coastal ecosystems. Realistically, any bird-feeding ticks (e.g., I. auritulus, I. spinipalpis, and I. pacificus) can be transported by wild birds from British Columbia’s mainland to Vancouver Island, the Gulf Islands, and insular tracts of land.
In eastern Canada, we noticed a biogeographical shift in I. gregsoni. An archetype study reported this mustelid tick at Ignace, Ontario [33]. We report I. gregsoni 200 km further west at Jim Lake, Ontario (Figure 1).

4.7. Mammal Parasitisms Reflect Established Ticks

This study provides many mammalian, tick–host associations across Canada. The highlights of these first-time records of mammal parasitisms are reported in Table 6. Since terrestrial mammals have a localized home range, they typically signify that a given tick species is established in the vicinity.
In the present study, 25 (93%) of the 27 tick species parasitize mammalian hosts, including humans. Not only do mammal parasitisms signify the presence of a tick species in a locality, Bbsl-positive ticks indicate that Lyme disease spirochetes are cycling enzootically in the area. These established populations may be hundreds of kilometres from where the zoonotic pathogens were acquired. In particular, one established population of blacklegged ticks on Corkscrew Island, which is located in northwestern Ontario, has a Bbsl infection prevalence of 73%; this insular location has the highest mean infection prevalence of Lyme disease spirochetes in I. scapularis adults ever reported in Canada [64].
In the present tick-host-pathogen study, all of the I. dentatus and Ixodes marxi (eastern squirrel tick) were negative for Bbsl (Table 1). However, other studies report Bbsl-positive I. dentatus and Bbsl-positive I. marxi [14,65].

4.8. Ixodes cookei Established on Vancouver Island

We provide the first report of I. cookei in far-western Canada and the West Coast of North America. We collected five I. cookei (one female, one nymph, three larvae) from a Pacific raccoon at North Saanich; this tick collection is the first record of I. cookei west of Manitoba (Table 6). Additionally, a gravid female was collected from a striped skunk on Vancouver Island, and it laid eggs that subsequently produced viable larvae. One of these larvae was barcoded for tick identification, and confirmed as I. cookei. The parasitism of a terrestrial mammal is the only viable mode of passage to Vancouver Island. Since I. cookei is not a bird-feeding tick [23], it must have been introduced via a terrestrial host that serves as a reservoir. Not only were Bbsl-positive I. cookei collected on Vancouver Island, they were collected from mammals in the lower Fraser Valley on the B.C. mainland. In the case of I. cookei on Vancouver Island, we hypothesize that a traveller from an indigenous area in central or eastern Canada took a terrestrial animal, such as a dog, to Vancouver Island, B.C., and the mammalian host was infested with a gravid I. cookei female and a male. During the trip westward, the female mated with the male and, upon arrival, the replete female dropped off into the leaf litter in a woodland habitat and, subsequently, laid eggs that hatched into viable larvae. Thus, a new I. cookei population was initiated on Vancouver Island. Since I. cookei had not previously been discovered in southwestern British Columbia, we contend that this previously undetected population became established recently, and is clearly not attributed to climate change [66].

4.9. Composite 6-Tick Enzootic Cycle of Bbsl on Vancouver Island

Whenever there are two or more tick species feeding concurrently on a host, they can transmit Bbsl, via the reservoir host, from one cofeeding tick species to another cofeeding tick species. Alternatively, one tick species can infect a reservoir-competent host and, after the blood meal, another tick species can subsequently acquire Bbsl from this spirochetemic host. Regardless of the sequel of feeding, co-infestations provide a direct way to maintain an enzootic transmission cycle of Lyme disease spirochetes. Using six vertebrate hosts and six tick species (i.e., I. angustus, I. auritulus, I. cookei, I. pacificus, I. spinipalpis, and I. texanus) from this study, we show a complete enzootic circuit of Bbsl from one tick species to another (Figure 4). With the exception of I. auritulus, these tick species bite people. In essence, this continual interconnecting link fulfills a multifaceted enzootic maintenance cycle of Bbsl.

4.10. Amblyomma Ticks Transported to Canada

Amblyomma ticks are transported into Canada by neotropical songbirds from the Neotropics. In order for these ixodid ectoparasites to sustain the transcontinental flight, they must remain attached for sustained periods of time. In the case of A. americanum, larvae typically feed 3 to 6 days, whereas nymphs commonly feed 4 to 7 days (J.D.S., unpublished data). Because many neotropical songbirds are marathon flyers, they are capable of transporting neotropical ticks long distances. During the flight, bird-feeding ticks gradually take a blood meal, and are fully engorged when they arrive in Canada. Based on these circumstantial factors, certain neotropical songbirds (e.g., flycatchers, thrushes, and warblers) transport slow-feeding Amblyomma ticks thousands of kilometres to Canada.
With respect to Amblyomma ticks, we collected A. americanum, A. dissimile, A. longirostre, A. maculatum, and A. rotundatum from neotropical and southern temperate songbirds in central and eastern Canada during northward spring migration. Additionally, Scott et al. previously reported an A. americanum (nymph) on a neotropical songbird (Swainson’s Thrush) in northwestern Alberta during spring migration [13]. Based on winter hardiness studies in southwestern Ontario, which is the southernmost region in Canada, we determined that A. americanum larvae do not overwinter (J.D.S., unpublished data). After migration, songbird-transported A. americanum larvae and nymphs will undergo ecdysis in late spring, and subsequently bite vertebrates, including people. However, the larvae will neither survive subzero Canadian winters, nor sustain an A. americanum population. For example, a neotropical songbird can import an A. americanum nymph into Canada in May during northward spring migration. Over the next 35 to 60 days, this replete tick will molt to either a male or a female, and starts host-seeking. A female will typically bite dogs, outdoor cats, and humans in August. Additionally, songbirds can introduce ticks infected with pathogens from southern climes that cause invasive zoonoses in domestic and wildlife mammals in Canada. Based on the geographic origin of Amblyomma spp., it is highly unlikely that these invasive ticks from tropical or semi-tropical regions will colonize in Canada.

4.11. Long-Distance Transport of Neotropical Ticks to Canada

Notably, a Bbsl-positive A. longirostre larva was collected from a Willow Flycatcher at Toronto, Ontario; this bird parasitism provides the first report of Lyme disease spirochetes in this neotropical tick species in North America. The immature stages preferentially parasitize passerine birds, while adults are found on rodents. As adults, A. longirostre have the potential to transmit pathogens to other large mammals, including humans.
Overall, we collected 27 A. longirostre larvae and nymphs from neotropical songbirds during spring migration. A combination of ecological factors facilitate the fast, long-distance movement of Amblyomma ticks from Brazil to Canada. From a zoogeographical perspective, A. longirostre ticks have a home range in north-central South America; Brazil is a significant part of this indigenous area [26]. As well, many neotropical passerines, which migrate to the northern boreal forest, have their wintering grounds in Brazil. Certain songbirds, such as the Willow Flycatcher fly long distances during migratory flight. In fact, they will fly up to 8000 km to Canada during northward spring migration [67]. During fall migration, a Willow Flycatcher flew 2217 km for 48 h nonstop from Harrison, Illinois to Minatitlan, Veracruz, Mexico with a flight pace of 45 km/h, or 1109 km/day [68]. At this flight pace, a Willow Flycatcher could fly from Brazil to Canada, a distance of 5240 km, in 4.7 days. With adequate food reserves and sustained southerly tailwinds, a Willow Flycatcher has the potential to transport Amblyomma ticks from Brazil to Canada.

4.12. Avian Host Records for I. scapularis

We document the first host records of I. scapularis parasitizing a Tennesse Warbler and a Bay-breasted Warbler. Both of these neotropical songbirds have their breeding range primarily in the northern boreal forest. With respect to the Bay-breasted Warbler, a fully engorged I. scapularis nymph was collected from this ground-foraging songbird at Ste-Anne-de-Bellevue, Québec during north-bound spring migration; this parasitism is a new tick–host record.
During fall migration, two I. scapularis larvae were collected from a hatch-year Tennessee Warbler. This bird parasitism indicates that this fall migrant was parasitized by the two larvae at a more northern location. Since one larva was Bbsl-positive, the spirochetal infection could have been transmitted transovarially via the mother bird to her eggs, and passed onward to her offspring and, thus, to this fledgling. When the fledgling was parasitized by two I. scapularis larvae, one larva became infected. Since the Bbsl-infected larva had not had a previous blood meal, the mother bird could be a competent reservoir. Although it is possible that maternal–neonatal transmission of Lyme disease spirochetes occurred between the mother bird and its offspring, it is more likely that the fledgling was bitten by a Bbsl-infected tick while foraging for food after leaving the nest, and became spirochetemic. In essence, immature stages of I. scapularis parasitize migratory songbirds during bidirectional migrations. Nymphs typically parasitize passerine migrants in the late spring, whereas I. scapularis larvae commonly parasitize songbirds in late summer and early fall.

4.13. Novel Bird Parasitisms

Ticks normally bite wild birds on the head and neck [11]; however, we document a tick parasitizing its avian host in the buccal cavity. Specifically, a fully engorged I. scapularis nymph was detached from the base of the mouth of an American Kestrel nestling [37]. This 3-week-old nestling was collected at Mirabel, Québec shortly after leaving the nest. This bird parasitism reveals the first collection of I. scapularis from an American Kestrel in Canada.
Migratory songbirds, which are heavily infested with ticks, have the potential to initiate new foci of ticks hundreds of kilometers from their original source [42,55,69]. Even though spring passerine migrants transport ticks to northern latitudes, these engorged ticks may not molt to the next live stage. Each tick species has its own photoperiod requirements to activate and undergo ecdysis [19]. In the case of I. scapularis, this tick species requires at least 14 hours of daylight for larvae and nymphs to molt to the next developmental life stage [66]. In actuality, the expansion and establishment of I. scapularis in northern areas is limited by photoperiod.
In this study, we detected Lyme disease spirochetes in 17 (77%) of 22 I. auritulus larvae feeding on a Fox Sparrow. The presence of Bbsl in a replete I. auritulus larva does not automatically confirm that a bird is a reservoir-competent host. However, since I. auritulus larvae attached to Fox Sparrows have been consistently positive for Bbsl, it is highly likely that the Fox Sparrow is a competent reservoir of Lyme disease spirochetes. More specifically, our results are congruent with other studies that show Bbsl-positive I. auritulus larvae collected from Fox Sparrows [11,35]. In order to confirm reservoir competency in birds, Richter et al. conducted a xenodiagnostic study using spirochete-free I. scapularis larvae to show that certain passerines, such as the American Robin, are reservoir-competent hosts of Bbsl [70]. Since transovarial transmission of Bbsl is not apparent in I. auritulus females, we postulate that Fox Sparrows are reservoir-competent hosts.
Ixodes auritulus harbors a diversity of Bbsl genomospecies. For example, Scott et al. documented B. burgdorferi sensu stricto, plus three other genotypes, in bird-feeding I. auritulus ticks collected in southwestern B.C. [13]. In the same province, Scott et al. identified Borrelia lanei (formerly Borrelia genomospecies 2), which is another member of the Bbsl complex, in I. spinipalpis adults collected from an eastern cottontail along the southern fringe of Vancouver Island (Table 6) [34]. Additionally, Scott & Foley discovered Borrelia americana, a member of the Bbsl complex, in an I. auritulus tick collected from a ground-foraging songbird in British Columbia (Table 6) [35]. Moreover, Banerjee et al. isolated Borrelia bissettiae (formerly B. bissettii; culture number 1340) from I. angustus larvae in southwestern B.C. [71]. Since B. bissettiae is cycling enzootically in this coastal area, it is likely that this borrelial species is dispersed by wild birds and attached ticks.

4.14. Epidemiological Significance of Ticks on Songbirds

It is noteworthy that three tick species (i.e., I. affinis, I. dentatus, and I. minor) were transported into central and eastern Canada during northward spring migration [14,59,60]; two of these extralimital ticks (I. affinis and I. minor) are known to be enzootic vectors of Bbsl. Although I. affinis and I. minor seldom bite humans, it appears that they are more important enzootic vectors of Bbsl in the southeastern U.S.A. than I. scapularis [36]. Of epidemiologic significance, Bbsl-infected, songbird-transported I. scapularis ticks have been documented as far west and as far north as Peace River, Alberta [72]. In the same study, Bbsl-infected I. scapularis nymphs were also reported in Atlantic Canada in Cape Breton Island, Nova Scotia, and the province of Newfoundland and Labrador. East of the Rocky Mountains, Bbsl-positive I. scapularis have been collected from songbirds in all provinces (Alberta, Saskatchewan, Manitoba, Ontario, Quebec, New Brunswick, Prince Edward Island, Nova Scotia, and Labrador and Newfoundland) [9,10,11,12,13,14,15,37,59,72]. These bird parasitisms underpin the fact that people do not have to visit an endemic area to contract Lyme disease.
We collected bird-rabbit ticks, Haemaphysalis leporispalustris, from songbirds and lagomorphs in several areas Canada-wide, and some of these ticks were positive for Bbsl. Our findings are consistent with Banerjee et al. who cultured Lyme disease spirochetes from H. leporispalustris collected in northwestern Alberta [73]. It is worth mentioning that H. leporispalustris larvae and nymphs are the predominant tick species that parasitize fall passerine migrants in central and eastern Canada. Of note, H. leporispalustris, a bird- and lagomorph-feeding ectoparasite, has transcontinental distribution in Canada [8]. Songbirds widely disperse H. leporispalustris immatures, and lagomorphs are present in each province to act as terrestrial hosts. Lagomorphs are competent reservoirs of Bbsl, especially for the genomospecies B. andersonii [74,75]. In Table 6, we have highlighted some of the significant H. leporispalustris parasitisms that were positive for Bbsl. Although a rare occurrence, H. leporispalustris is known to bite humans [76].

5. Conclusions

Our findings show that Bbsl has wide distribution across Canada, and multiple tick species are involved in the enzootic maintenance cycle of this highly adaptive spirochete. Of 18 species tested, 15 were Bbsl-positive by PCR. Our data provide many tick–host firsts for indigenous and extralimital ticks parasitizing wild birds and terrestrial mammals coast to coast. The groundbreaking discovery of I. cookei on Vancouver Island suggests that this tick species has undergone a major geographic shift in Canada. In addition, wild birds transport bird-feeding ticks to new foci during long-distance migrations. Of special note, a Bbsl-positive A. longirostre was transported from the Neotropics by a Willow Flycatcher. In all, 16 of the 27 tick species in this study are bird-feeding ticks, and the majority are known to harbor and transmit tick-borne pathogens. Notably, six tick species were positive for Bbsl within the southeastern region of Vancouver Island, and suggest that these ectoparasites are involved in a 6-tick, enzootic maintenance cycle of Bbsl. Not only do wild birds widely disperse Lyme disease vector ticks countrywide, terrestrial mammals maintain Bbsl in numerous localized Lyme disease foci. Notably, 6 of 15 tick species that were infected with Bbsl bite humans. Ultimately, healthcare professionals must be cognizant that multiple tick species and their vertebrate hosts perpetuate Lyme disease spirochetes and associated tick-borne pathogens. These tick-borne zoonoses have spawned a major public health crisis throughout Canada.

Author Contributions

J.D.S. was responsible for study design and coordinating this tick–host project. J.F.A., B.C.B., K.L.C. and J.E.F. conducted molecular testing of ticks and analysis of PCR amplicons. L.A.D. confirmed the identification of ticks. All authors read and approved the final manuscript.

Funding

Funding was provided in part by the Mary Alice Holmes Memorial Foundation.

Acknowledgments

We thank wildlife rehabilitators, bird banders, biologists, veterinarians, citizen scientists, Fatal Light Awareness Program staff, and the public for collecting ticks from avian and mammalian hosts. We greatly appreciate technical assistance from Elizabeth Alves, Angela Bransfield, and Bonnie Hammond. We are indebted to Monica Young for conducting barcoding analysis. We are grateful to Amanda Green for computer graphics.

Conflicts of Interest

The authors declare no conflicts of interest.

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Healthcare 06 00131 g001 550
Figure 1. Map of western Canada showing baseline and current biographical distribution of five Ixodes spp. Black symbols represent benchmark sightings for the tick species [7,8]. Color symbols represent current sighting for I. cookei (blue square), I. gregsoni (green diamond), I. rugosus (orange star), I. spinipalpis (red dot), and I. texanus (mauve polygon).
Figure 1. Map of western Canada showing baseline and current biographical distribution of five Ixodes spp. Black symbols represent benchmark sightings for the tick species [7,8]. Color symbols represent current sighting for I. cookei (blue square), I. gregsoni (green diamond), I. rugosus (orange star), I. spinipalpis (red dot), and I. texanus (mauve polygon).
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Figure 2. Common Yellowthroat parasitized by two engorging I. scapularis nymphs, both together, anterior to left eye. One of the two nymphs was positive for B. burgdorferi sensu lato. Photo credit: Simon Duval.
Figure 2. Common Yellowthroat parasitized by two engorging I. scapularis nymphs, both together, anterior to left eye. One of the two nymphs was positive for B. burgdorferi sensu lato. Photo credit: Simon Duval.
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Figure 3. Red squirrel parasitized by 29 I. angustus females. Five males were copulating on the ventral surface of five females, and are not visible. Some of the I. angustus ticks on this host were positive for B. burgdorferi sensu lato. Photo credit: Christina Carrieres.
Figure 3. Red squirrel parasitized by 29 I. angustus females. Five males were copulating on the ventral surface of five females, and are not visible. Some of the I. angustus ticks on this host were positive for B. burgdorferi sensu lato. Photo credit: Christina Carrieres.
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Figure 4. A 6-tick cycle of Borrelia burgdorferi sensu lato on Vancouver Island, B.C. Collectively, these six tick species form an interconnecting link between multiple hosts in a multipart enzootic maintenance cycle of Bbsl. Five of these tick species bite humans.
Figure 4. A 6-tick cycle of Borrelia burgdorferi sensu lato on Vancouver Island, B.C. Collectively, these six tick species form an interconnecting link between multiple hosts in a multipart enzootic maintenance cycle of Bbsl. Five of these tick species bite humans.
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Table
Table 1. Tick species collected from avian and mammalian hosts in Canada, 2013–2016.
Table 1. Tick species collected from avian and mammalian hosts in Canada, 2013–2016.
Tick SpeciesTicks CollectedBites HumansTicks TestedTicks Bbsl-pos.
Amblyomma americanum5YesNTNT
Amblyomma dissimile1OccasionalNTNT
Amblyomma longirostre27Rare√+ve
Amblyomma maculatum3YesNTNT
Amblyomma rotundatum1RareNTNT
Dermacentor albipictus20Rare√+ve
Dermacentor andersoni16YesNTNT
Dermacentor variabilis175YesNTNT
Haemaphysalis leporispalustris178Rare√+ve
Ixodes affinis5Rare√+ve
Ixodes angustus37Yes√+ve
Ixodes auritulus88No√+ve
Ixodes banksi18Rare√+ve
Ixodes brunneus8Rare√+ve
Ixodes cookei65Yes√+ve
Ixodes dentatus2Occasional√−ve
Ixodes gregsoni17No√+ve
Ixodes marxi10Yes√−ve
Ixodes minor1RareNTNT
Ixodes muris31Yes√+ve
Ixodes pacificus31Yes√+ve
Ixodes rugosus25Rare√−ve
Ixodes soricis1RareNTNT
Ixodes spinipalpis43Occasional√+ve
Ixodes scapularis432Yes√+ve
Ixodes texanus18Rare√+ve
Ixodes uriae7YesNTNT
Total: 271265141815
NT, not tested; √, tick species tested; +ve, Bbsl positive; −ve, Bbsl negative.
Table
Table 2. Detection of Borrelia burgdorferi sensu lato in Ixodes ticks collected from avian hosts in the Metchosin-Victoria-Vancouver-Maple Ridge, British Columbia area, 2013–2016.
Table 2. Detection of Borrelia burgdorferi sensu lato in Ixodes ticks collected from avian hosts in the Metchosin-Victoria-Vancouver-Maple Ridge, British Columbia area, 2013–2016.
Bird SpeciesNumber of Ticks Borrelia burgdorferi-Positive Ticks/Number of Ticks Collected
No. of HostsIxodes auritulusIxodes pacificusIxodes spinipalpisInfection Rate (%)
LNFNN
American Robin, Turdus migatorius Linnaeus70/41/67/130/00/08/23 (35)
Pacific Wren, Troglodytes pacificus Baird30/11/20/00/01/12/4 (50)
Song Sparrow, Melopiza melodia (Wilson)90/02/25/60/00/07/8 (88)
Common Yellowthroat, Geothlypis trichas (L.)10/01/10/00/00/01/1 (100)
Fox Sparrow, Passerella iliaca (Merrem)317/224/60/00/00/021/28 (75)
Hermit Thrush, Catharus guttatus (Palla)20/50/00/00/00/00/5 (0)
Wilson’s Warbler, Cardellina pusilla (Wilson)10/01/10/00/00/01/1 (100)
Varied Thrush, Ixoreus naevius Gmelin10/01/10/00/00/01/1 (100)
Spotted Towhee, Pipilo maculatus Swainson20/05/60/00/00/05/6 (83)
Steller’s Jay, Cyanocitta stelleri (Gmelin)20/201/10/00/00/01/21 (5)
Purple Finch, Haemorhous purpureus (Gmelin)10/00/00/00/00/10/1 (0)
Swainson’s Thrush, Catharus ustulatus (Nuttall)30/00/03/30/00/03/3 (100)
House Wren, Troglodytes aedon (Vieillot)10/00/00/00/10/00/1 (0)
California Quail, Callipepla californica (Shaw)30/00/00/01/20/11/3 (33)
Cooper’s Hawk, Accipiter cooperii (Bonaparte)10/10/00/10/00/00/2 (0)
Totals: 154017/5317/2615/231/31/351/108 (47)
L, larva(e); N, nymph(s); F, female(s); Bb-pos., Borrelia burgdorferi sensu lato-positive.
Table
Table 3. Detection of Borrelia burgdorferi sensu lato in Ixodes ticks collected from mammalian hosts in the Metchosin-Victoria-Vancouver-Maple Ridge, British Columbia area, 2013–2016.
Table 3. Detection of Borrelia burgdorferi sensu lato in Ixodes ticks collected from mammalian hosts in the Metchosin-Victoria-Vancouver-Maple Ridge, British Columbia area, 2013–2016.
Mammal SpeciesNumber of Borrelia burgdorferi-Positive Ticks/Number of Ticks Collected
No. of HostsIxodes angustusIxodes cookeiIxodes pacificusIxodes spinipalpisIxodes texanusInfection Rate (%)
LNMFLNFLNMFLNMFNF
American red squirrel, Tamiasciurus hudsonicus (Erxleben)40/00/21/33/180/00/00/00/00/00/00/00/00/00/00/00/00/04/23 (17)
American mink, Neovison vison (Schreber)20/00/00/00/00/02/110/10/00/00/00/00/00/00/00/00/00/02/12 (17)
Brown rat, Rattus norvegicus (Berkenhout)20/00/00/02/20/00/00/00/00/00/00/00/00/00/00/00/00/02/2 (100)
Columbian black-tailed deer, Odocoileus hemionus columbianus (Richardson)20/00/00/00/00/00/00/00/00/00/10/30/00/00/00/00/00/00/4 (0)
Cottontail rabbit, Sylvilagus floridanus (J.A. Allen)100/00/00/11/20/00/00/00/11/20/00/00/11/52/81/50/00/06/25 (24)
Deer mouse, Peromyscus maniculatus (Wagner)10/00/00/00/00/00/00/00/00/00/00/00/32/20/00/00/00/02/5 (40)
Dog, domestic, Canis lupus familiaris (Linnaeus)40/00/00/00/00/00/00/00/00/00/10/70/00/00/00/00/00/00/8 (0)
Douglas squirrel, Tamiasciurus douglasii (Bachman)50/00/01/33/50/00/00/00/00/00/00/00/00/00/00/00/00/04/8 (50)
Human, Homo sapiens (Linnaeus)60/00/00/00/00/00/00/00/00/10/00/40/00/10/00/00/00/00/6 (0)
Muskrat, Ondatra zibethicus (Linnaeus)10/30/20/00/00/00/00/00/00/00/00/00/00/00/00/00/00/00/5 (0)
Pacific raccoon, Procyon pacificus (Merriam)100/00/00/00/00/30/11/20/00/00/00/00/00/20/11/21/21/64/19 (21)
Snowshoe hare, Lepus americanus Erxleben20/00/00/00/00/00/00/00/00/01/10/50/00/00/00/00/00/01/6 (17)
Striped Skunk, Mephitis mephitis (Schreber)40/50/00/00/00/00/12/30/00/00/00/00/00/00/00/00/20/02/11 (18)
Western gray squirrel, Sciurus griseus (Ord)50/00/00/02/40/00/00/00/00/01/11/10/10/00/01/20/00/05/9 (56)
Totals: 14580/80/42/711/310/32/133/60/11/32/41/200/53/102/93/91/41/632/143 (22)
L, larva(e); N, nymph(s); M, male(s); F, female(s); Bb-pos., Borrelia burgdorferi sensu lato-positive.
Table
Table 4. Detection of Borrelia burgdorferi sensu lato in Ixodes ticks collected from avian hosts in the London-St.Thomas-Simcoe-Toronto, Ontario area, 2013–2016.
Table 4. Detection of Borrelia burgdorferi sensu lato in Ixodes ticks collected from avian hosts in the London-St.Thomas-Simcoe-Toronto, Ontario area, 2013–2016.
Bird SpeciesNumber of Ticks Borrelia burgdorferi-Positive Ticks/Number of Ticks Collected
No. of HostsIxodes affinisIxodes brunneusIxodes minorIxodes murisIxodes scapularisInfection Rate (%)
NNFLLFLN
Hermit Thrush, Cathrus guttatus (Pallas)40/00/01/10/00/10/00/03/34/5 (80)
Black-throated Blue Warbler, Setophaga caerulescens (Gmelin)10/00/00/00/00/10/00/00/00/1 (0)
Blue Jay, Cyanocitta cristata (Linnaeus)30/00/00/00/00/00/00/17/107/11 (64)
Common Yellowthroat, Geothlypis trichas (Linneaus)50/00/00/0NT/10/00/00/01/41/4 (25)
Swainson’s Thrush, Catharus ustulatus (Nuttall)30/10/00/00/00/00/00/01/11/2 (50)
Tennessee Warbler, Oreothlypis peregrina (Wilson)10/00/00/00/00/00/01/20/01/2 (50)
White-throated Sparrow, Zonotrichia albicollis (Gmelin)30/00/10/00/00/00/10/00/10/3 (0)
Lincoln’s Sparrow, Melospiza lincolnii (Audubon)10/00/00/00/00/00/00/00/10/1 (0)
Mourning Warbler, Oporornis philadelphia (Wilson)10/00/00/00/00/00/00/01/11/1 (100)
Dark-eyed Junco, Junco hyemalis hyemalis (Linnaeus)30/10/00/20/00/00/00/00/00/3 (0)
House Wren, Troglodytes aedon (Vieillot)30/10/00/00/00/00/00/01/11/2 (50)
Baltimore Oriole, Icterus galbula (Linnaeus)10/00/00/00/00/00/00/01/21/2 (50)
Gray-cheeked Thrush, Catharus minimus (Lafresnaye)10/00/00/00/00/00/00/01/11/1 (100)
American Redstart, Setophaga ruticilla (Linnaeus)10/00/00/00/00/00/00/00/10/1 (0)
Winter Wren, Troglodytes hiemalis Vieillot10/00/00/00/00/10/00/00/00/1 (0)
Red-breasted Grosbeak, Pheucticus ludovicianus (Linnaeus)10/00/00/00/00/00/00/00/10/1 (0)
Totals: 16330/30/11/3NT/10/30/11/316/27 (59)18/41 (44)
L, larva(e); N, nymph(s); F, female(s); Bb-pos., Borrelia burgdorferi sensu lato-positive. NT, not tested.
Table
Table 5. Detection of Borrelia burgdorferi sensu lato in Ixodes ticks collected from mammalian hosts in the London-St. Thomas-Simcoe-Toronto, Ontario area, 2013–2016.
Table 5. Detection of Borrelia burgdorferi sensu lato in Ixodes ticks collected from mammalian hosts in the London-St. Thomas-Simcoe-Toronto, Ontario area, 2013–2016.
Mammal SpeciesNumber of Borrelia burgdorferi-Positive Ticks/Number of Ticks Collected
No. of HostsIxodes angustusIxodes cookeiIxodes scapularisIxodes texanusInfection Rate (%)
NMFNMFLNMFMF
Dog, domestic, Canis lupus familiaris Linnaeus20/00/00/00/00/00/00/00/00/02/50/00/02/5 (40)
Cat, domestic, Felis silvestris catus Linnaeus20/00/00/00/00/00/00/00/00/01/30/00/01/3 (33)
Striped skunk, Mephitis mephitis (Schreber)40/00/00/01/20/01/30/00/00/00/00/00/02/5 (40)
Weasel, Mustela erminea Linnaeus20/00/00/01/10/01/30/00/00/00/00/00/02/4 (50)
Eastern raccoon, Procyon lotor lotor Linnaeus50/00/00/00/00/00/00/00/00/00/00/56/86/13 (46)
Human, Homo sapiens Linnaeus40/00/00/00/00/00/00/00/00/21/20/00/01/4 (25)
American red fox, Vulpes vulpes fulvus Desmarest30/00/00/00/30/01/20/00/00/12/30/00/03/9 (33)
American red squirrel, Tamiasciurus hudsonicus (Erxleben)20/11/10/00/00/00/00/01/30/00/00/00/02/5 (40)
Groundhog, Marmota monax (Linnaeus)20/00/00/01/20/01/30/00/00/00/00/00/02/5 (40)
Northern short-tailed shrew, Blarina brevicauda (Say)10/00/00/00/00/00/02/31/20/00/00/00/03/5 (60)
Cottontail rabbit, Sylvilagus floridanus (J.A. Allen)20/00/00/00/00/00/00/00/10/00/10/00/00/2 (0)
Eastern chipmunk, Tamias striatus (Linnaeus)40/00/00/00/00/00/00/13/50/00/00/00/03/6 (50)
White-tailed deer, Odocoileus virginianus Zimmermann10/00/00/00/00/00/00/00/00/11/30/00/01/4 (25)
Horse, Equus caballus Linnaeus10/00/00/00/00/00/00/00/00/01/20/00/01/2 (50)
Muskrat, Ondatra zibethicus (Linnaeus)10/20/00/00/00/00/00/00/00/00/00/00/00/2 (0)
Totals: 15360/31/10/03/80/04/112/45/111/47/190/56/829/74 (39)
L, larva(e); N, nymph(s); M, male(s); F, female(s); Bb-pos, Borrelia burgdorferi sensu lato-positive.
Table
Table 6. Tick–host records for birds and mammals in Canada, and B. burgdorferi sensu lato in ticks, by province, 2013–2016.
Table 6. Tick–host records for birds and mammals in Canada, and B. burgdorferi sensu lato in ticks, by province, 2013–2016.
Geographical LocationHost SpeciesTick SpeciesLife StageCollection DateEpidemiological Significance
Alberta (AB)
CalgaryYellow-rumped WarblerI. spinipalpisN30 May 2014Bb-pos tick on a bird in AB
Pincher CreekSnowshoe hareHlpL, N8 May 2014Bb-pos tick in s. AB
LethbridgeAmerican RobinI. spinipalpisN7 May 2015HR in AB
British Columbia (BC)
MetchosinCottontail rabbitI. spinipalpisM, F7 February 2013HR
North SaanichRaccoonI. cookeiL, N, F26 February 2013HR in BC
BurnabyStriped skunkI. rugosusN11 April 2013HR
ColwoodRaccoonI. texanusF13 June 2013I. texanus on Vancouver Is
Beaver LakeMinkI. cookeiN, F27 June 2013Bb-pos I. cookei on mink in Canada
BurnabyStriped skunkI. cookeiF5 July 2013Bb-pos I. cookei on skunk in Canada
GibsonsDouglas squirrelI. angustusF1 September 2013HR of I. angustus in Canada
Rocky PointPacific WrenI. auritulusN31 August 2013Bb-pos I. auritulus on this host
AbbotsfordEastern gray squirrelI. angustusF3 June 2013HR
BurnabyEastern gray squirrelI. angustusF18 September 2013Bb-pos I. angustus on this host
Maple RidgeSnowshoe hareI. pac.; I. spin.M, F; F14 June 2013HR, Bb-pos; HR, Bb-pos; co-infest
MetchosinPacific WrenI. auritulusL22 June 2013HR
Rocky PointHouse WrenI. pacificusN22 June 2013HR
LadysmithCalifornia QuailI. spinipalpisN25 June 2013HR
Rocky PointVagrant shrewI. soricisF3 September 2013Southernmost collection in Canada
KamloopsBighorn SheepD. andersoniM, F20 May 2013HR
East SookeRed squirrelI. angustusM, F28 October 2013Bb-pos I. angustus on red squirrel
SecheltSnowshoe hareI. pacificusM, F26 March 2014Bb-pos I. pacificus on this host
North SaanichCottontail rabbitI. spinipalpisM, F5 May 2014Bb-pos I. spinipalpis on this host
KamloopsMooseD. andersoniM, F25 April 2014HR
SaanichCalifornia QuailI. pacificusN20 June 2014Bb-pos I. pacificus on this host
BurnabyBrown ratI. angustusF13 September 2014HR; Bb-pos I. angustus on this host
WeldonCat, domesticD. andersoniF14 May 2014HR
Rocky PointWilson’s WarblerI. auritulusN1 August 2014Bb-pos I. auritulus on this host
North VancouverDouglas squirrelI. angustusN, F13 August 2014Bb-pos I. angustus on this host
CoquitlamStriped skunkI. angustusN13 September 2014HR
BurnabySpotted TowheeI. auritulusN18 October 2014HR; Bb-pos
VancouverSteller’s JayI. auritulusN23 October 2014HR; Bb-pos
MervilleCooper’s HawkI. auritulusL, F17 February 2015I. auritulus on Cooper’s Hawk
MetchosinPurple FinchI. spinipalpisN24 April 2015HR
EsquimaltRiver otterI. rugosusN29 April 2015I. rugosus on Vancouver Is
MetchosinCottontail rabbitI. spinipalpisM, F3 May 2015Borrelia lanei, first in Canada [34]
Oak BayRaccoonI. spinipalpisF3 August 2015HR
MetchosinVaried ThrushI. auritulusN31 October 2015Borrelia americana, first in Canada [35]
SaanichPacific WrenI. spinipalpisN9 March 2015HR
VictoriaEastern gray squirrelI. spinipalpisL26 March 2015HR
MetchosinMuskratI. angustusL, N9 April 2016First report, tick on muskrat, Canada
SaanichCottontail rabbitI. ang; I. spin.F, N12 April 2016Co-infestation
VictoriaCottontail rabbitI. ang; I. spin.L, L27 May 2016Co-infestation
Central SaanichCottontail rabbitI. spin.; I. ang; I. pac.M, F; N; N6 September 2016Triple co-infestation
SookeAmerican minkI. cookeiN2 October 2016HR, Vancouver Is.
Manitoba (MB)
MordenSnowshoe hareHlpF17 May 2014HR in MB; Bb-pos
GardentonRed foxI. scapularisN, F19 May 2014HR in Canada
GuntonRaccoonD. variabilisM, F17 July 2014HR in MB
SteinbackGroundhogI. cookeiN30 July 2014HR in MB
New Brunswick (NB)
AlmaRed foxI. scapularisN23 June 2013HR in NB; Bb-pos
WoodstockGroundhogI. cookeiN9 July 2014HR in NB
FrederictonSouthern red squirrelI. scapularisN19 June 2016HR in NB; Bb-pos
Newfoundland and Labrador (NL)
BranchGray-cheeked ThrushHlpN27 July 2013HR in NL
Gannet IslandHumanI. uriaeN, F29 July 2013HR
Corner BrookSnowshoe hareHlpF20 May 2014HR in NL
Nova Scotia (NS)
Broad CoveRaccoonI. scapularisN17 June 2014HR in NS; Bb-pos
BrightonSouthern red squirrelI. scapularisN19 June 2014HR; Bb-pos
St. MartinsBovineI. scapularisN23 June 2014HR
GreenfieldRaccoonD. variabilisM, F4 July 2014HR in NS
KemptvilleGroundhogI. cookeiN, F22 July 2014HR in NS
LunenburgGroundhogI. cookeiN28 July 2014Bb-pos in NS
Ontario (ON)
Long PointHermit ThrushI. brunneusF18 April 2013Bb-pos I. brunneus
Port CarlingBeaverI. banksiF22 April 2013Bb-pos I. banksi; in sc. ON
OakvilleRaccoonI. texanusF5 May 2013Bb-pos I. texanus in ON
Silver LakeBeaverI. banksiN15 May 2013Bb-pos I. banksi in nw. ON
TorontoCommon YellowthroatI. minorL20 May 2013HR, I. minor in Canada [36]
TorontoWillow FlycatcherA. longirostreL23 May 2013Bb-pos A. longirostre in N. America
Long PointBlue JayI. scapularisN15 May 2013Bb-pos I. scap., HR
Long PointSwainson’s ThrushI. affinisN24 May 2014I. affinis in e. Canada
BellevilleRed foxI. cookeiN, F29 May 2013I. cookei in e. Canada
Thunder CapeLincoln’s SparrowI. den; I. scap.L; L, N15 May 2013Bb-pos I. scap. L & N; co-infest
LondonStriped skunkI. cookeiN, F11 August 2013Bb-pos I. cookei in eastern Canada
Ruthven ParkTennessee WarblerI. scapularisL1 September 2013HR in N. America
KenoraSnowshoe hareHlpN11 October 2013Bb-pos Hlp in ON
KenoraDogD. albipictusN9 December 2013Bb-pos D. albipictus
KenoraHumanI. cookeiN10 May 2013Bb-pos I. cookei on human, nw. ON
KenoraErmineI. gregsoniN, F2 December 2013HR; Bb-pos I. gregsoni
Long PointVeeryA. amer.L22 May 2013HR
Long PointMagnolia WarblerA. long.L24 May 2013HR
Long PointAcadian FlycatcherA. long.L30 May 2013HR
Thunder CapeChipping SparrowI. scapularisN23 May 2013Bb-pos I. scapularis on this host
Long PointVeeryA. rotundatumN26 May 2014HR; first report on a bird [17]
ArthurHumanI. cookeiN25 April 2014Bb-pos I. cookei on human
Barry’s BayBeaverI. banksiN, F3 May 2014Bb-pos I. banksi nymph, e. ON
TorontoWhite-throated SparrowI. brunneusN1 May 2014First record of I. brunneus nymph
TorontoCommon YellowthroatI. den; I. scap.L; 2L, N15 May 2014Co-infestation
TorontoHouse WrenI. scapularisN15 May 2014Bb-pos I. scapularis on this host
TorontoYellow WarblerA. long.L18 May 2014HR
TorontoGray-cheeked ThrushI. scapularisN26 May 2014Bb-pos I. scapularis on this host
KenoraRed-backed voleI. murisF1 June 2014HR; Bb-pos
KenoraSnowshoe hareHlpN3 June 2014Bb-pos in ON
Long PointBrown ThrasherI. scapularisN1 June 2014Bb-pos in Canada
St. ThomasShort-tailed weaselI. cookeiF6 June 2014HR; Bb-pos
WalsinghamEastern chipmunkI. scapularisN3 July 2014Bb-pos
KeewatinDog, domesticI. murisF7 July 2014Bb-pos; HR with nw. ON
Fort FrancesPorcupineD. variabilisM, F18 July 2014HR in nw. ON
KenoraSnowshoe hareHlp; D.alb.L, N, F; N28 July 2014HR (D. albipictus); co-infest
KenoraRed foxD. variabilisF18 July 2014HR in nw. ON
KeewatinNorthern short-tailed shrewI. murisF23 July 2014Bb-pos; HR in nw. ON
KenoraDeer mouseI. angustusF1 August 2014Bb-pos; HR in ON
VeronaHumanI. scapularisF28 September 2014Bb-pos in e. ON
TorontoHermit ThrushI. murisL17 October 2014HR; larval I. muris, s. ON
KanataRusty BlackbirdI. brunneusF30 April 2015HR; on this host
Ruthven ParkChestnut-sided WarblerA. longirosreL11 May 2015HR; in N. America
TorontoSwainson’s ThrushI. affin; I. scap.N, N24 May 2015Co-infestation; I. scapularis Bb-pos
TorontoVeeryA. dissimileN24 May 2015HR on bird in N. America [16]
TorontoAmerican RedstartI. scapularisN26 May 2015HR in Canada
BelmontEastern chipmunkI. scapularisN9 June 2015Bb-pos
KeewatinCat, domesticI. murisF17 July 2015Bb-pos; HR in nw. ON
TorontoBlack-throated blue WarblerI. murisL28 August 2015HR; larval I. muris, s. ON
TorontoWinter WrenI. murisL6 October 2015HR; larval I. muris, s. ON
TorontoDark-eyed JuncoI. murisF20 October 2015HR; larval I. muris, s. ON
Ruthven ParkRuby-crowned KingletHlpL21 October 2015HR; in Canada
Willard LakeMartenI. marxiF28 October 2015HR; in Canada
Thunder CapeNashville WarblerI. scapularisN27 October 2015HR; in Canada
Anglican IslandRed foxI. cookeiN14 April 2016HR; nw. ON
Long PointSlate-colored JuncoI. affinisN17 April 2016HR; in Canada
Ruthven ParkHouse WrenI. affinisN28 April 2016HR; in Canada
Long PointBaltimore OrioleI. scapularisN18 May 2016HR; in Canada
TorontoRed-breasted GrosbeakI. scapularisN9 May 2016HR; in Canada
FloradaleDog, domesticA. mac.F27 August 2016HR; in Canada
Jim LakeAmerican minkI. gregsoniN5 November 2016Farthest west in Canada
Barry’s BayFisherI. cookeiF31 December 2016HR; in s. ON
Prince Edward Island (PE)
BrudenellCat, domesticI. scapularisF19 May 2014HR in PE; Bb-pos
MontagueEastern chipmunkI. scapularisN19 June 2014HR; in PE
GeorgetownWhite-throated SparrowI. scapularisN30 May 2015HR; in PE; Bb-pos
Québec (QC)
Ste-Anne-de-BellevueCommon GrackleI. brunneusF26 May 2014HR; in Canada
ChicoutimiSnowshoe hareHlpN17 June 2014Bb-pos Hlp in QC
Ste-Anne-de-BellevueCanada WarblerHlpL24 August 2014Bb-pos; reservoir host
CoaticookRed foxI. scapularisN17 June 2014HR; in QC
VictoriavilleGroundhogI. cookeiN25 July 2014Bb-pos; in QC
Ste-Anne-de-BellevueAmerican RedstartI. murisL, N14 August 2014Bb-pos; in QC
Ste-Anne-de-BellevueHouse WrenI. murisF31 August 2014Bb-pos; in QC
Ste-Anne-de-BellevueBay-breasted WarblerI. scapularisF15 May 2015HR; in N. America
Ste-Anne-de-BellevueNorthern WaterthrushI. affin; I. scap.N, N23 May 2015Bb-pos I. scapularis; co-infestion
Ste-Anne-de-BellevueCommon YellowthroatI. affinisN26 May 2015Bb-pos; HR in QC
Ste-Anne-de-BellevueVeeryI. scapularisN26 May 2016Bb-pos; in QC
St-Patrice-de-SherringtonBrown ThrasherI. scapularisN23 June 2016HR; in QC
MirabelAmerican KestrelI. scapularisN29 June 2016HR; in Canada [37]
KeewatinMeadow voleI. murisN11 August 2016HR; in nw. ON
Ste-Anne-de-BellevueMagnolia WarblerI. scapularisL25 August 2016HR; in Canada
Saskatchewan (SK)
OxbowSnowshoe hareHlpL, N6 May 2014HR; in SK
SaskatoonStriped skunkD. variabilisF1 July 2014HR; in SK
Meadow LakeSnowshoe hareHlpF19 May 2015Bb-pos Hlp in SK
L, larvae; N, nymph(s); M, male(s); F, female(s). co-infest., co-infestation; e., eastern; sc., southcentral; s., southern; nw., northwest; HR, new host record; Bb-pos, Borrelia burgdorferi positive; D. alb., Dermacentor albipictus; Hlp, Haemaphysalis leporispalustris; I. affin, Ixodes affinis; I. ang, Ixodes angustus; I. den, Ixodes dentatus; I. pac., Ixodes pacificus; I. scap, Ixodes scapularis; I. spin., Ixodes spinipalpis; A. amer., Amblyomma americanum; A. long., Amblyomma longirostre; A. mac., Amblyomma maculatum.

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MDPI and ACS Style

Scott, J.D.; Clark, K.L.; Foley, J.E.; Anderson, J.F.; Bierman, B.C.; Durden, L.A. Extensive Distribution of the Lyme Disease Bacterium, Borrelia burgdorferi Sensu Lato, in Multiple Tick Species Parasitizing Avian and Mammalian Hosts across Canada. Healthcare 2018, 6, 131. https://doi.org/10.3390/healthcare6040131

AMA Style

Scott JD, Clark KL, Foley JE, Anderson JF, Bierman BC, Durden LA. Extensive Distribution of the Lyme Disease Bacterium, Borrelia burgdorferi Sensu Lato, in Multiple Tick Species Parasitizing Avian and Mammalian Hosts across Canada. Healthcare. 2018; 6(4):131. https://doi.org/10.3390/healthcare6040131

Chicago/Turabian Style

Scott, John D., Kerry L. Clark, Janet E. Foley, John F. Anderson, Bradley C. Bierman, and Lance A. Durden. 2018. "Extensive Distribution of the Lyme Disease Bacterium, Borrelia burgdorferi Sensu Lato, in Multiple Tick Species Parasitizing Avian and Mammalian Hosts across Canada" Healthcare 6, no. 4: 131. https://doi.org/10.3390/healthcare6040131

APA Style

Scott, J. D., Clark, K. L., Foley, J. E., Anderson, J. F., Bierman, B. C., & Durden, L. A. (2018). Extensive Distribution of the Lyme Disease Bacterium, Borrelia burgdorferi Sensu Lato, in Multiple Tick Species Parasitizing Avian and Mammalian Hosts across Canada. Healthcare, 6(4), 131. https://doi.org/10.3390/healthcare6040131

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