The tick, Ixodes minor Neumann (Ixodida: Ixodidae), a blood-sucking ectoparasite of birds and small mammals, is indigenous along the coastal southeastern United States of America (South Carolina, Georgia, Florida) (Clark et al. Reference Clark, Oliver, McKechnie and Williams1998, Reference Clark, Oliver, Grego, James, Durden and Banks2001) and in Central America (Guglielmone et al. Reference Guglielmone, Estrada-Peña, Keirans and Robbins2003). This tick species serves as an enzootic vector of the spirochetal bacterium, Borrelia burgdorferi Johnson, Schmid, Hyde, Steigerwalt, and Brenner sensu lato (s.l.), which causes Lyme disease (Lyme borreliosis) (Oliver et al. Reference Oliver, Lin, Clark, Banks, Durden and James2003), and manifests in humans as a multisystemic illness. If left untreated or inadequately treated, this spirochetosis can be a persistent infection and, eventually, may result in neurological paralysis, blindness, dementia, total disability and, in some cases, result in fatal outcomes (Liegner et al. Reference Liegner, Duray, Agricola, Rosenkilde, Yannuzzi and Ziska1997; Cameron Reference Cameron2010). Worldwide, the B. burgdorferi s.l. complex includes at least 21 different genospecies, of which B. chilensis Ivanova et al. (Reference Ivanova, Tomova, González-Acuña, Murúa, Moreno and Hernández2013) is the most recently documented and, in the southeastern United States of America, five (B. americana Rudenko et al.; B. andersonii Marconi et al.; B. bissettii Postic et al.; B. carolinensis Rudenko et al.; and B. burgdorferi sensu stricto (s.s.) Baranton et al.) have been identified in people, ticks, birds, and rodents (Felz et al. Reference Felz, Chandler, Oliver, Rahn and Schriefer1999; Oliver et al. Reference Oliver, Lin, Clark, Banks, Durden and James2003; Rudenko et al. Reference Rudenko, Golovchenko, Grubhoffer and Oliver2009a, Reference Rudenko, Golovchenko, Lin, Gao, Grubhoffer and Oliver2009b; Clark et al. Reference Clark, Leydet and Hartman2013). Based on DNA sequencing and phylogenetic analysis, Lin et al. (Reference Lin, Oliver and Gao2004) showed significant genetic diversity of Borrelia isolates from ticks and rodents collected in the southeastern United States of America. These diverse genotypes can be present in I. minor, and dispersed locally or transcontinentally by songbirds (Scott and Durden Reference Scott and Durden2009; Ogden et al. Reference Ogden, Margos, Aaensen, Drebot, Feil and Hanincová2011). During a borrelial study, Durden et al. (Reference Durden, McLean, Oliver, Ubico and James1997) isolated B. burgdorferi s.l. from the blood of a Northern Cardinal, Cardinalis cardinalis (Linnaeus) (Passeriformes: Cardinalidae), parasitised by I. minor and from 23 of 56 (43%) immature I. minor collected from birds in the coastal southeastern United States of America.
Immatures (larvae, nymphs) of I. minor parasitise several ground-frequenting songbirds (Passeriformes), including the House Wren, Troglodytes aedon Viellot (Passeriformes: Troglodytidae), Eastern Towhee, Pipilio erythrophthalmus (Linnaeus) (Passeriformes: Emberizidae) (Keirans and Clifford Reference Keirans and Clifford1978) and, likewise, the Carolina Wren, Thryothorus ludovicianus (Latham) (Passeriformes: Parulidae), Northern Cardinal, and Northern Waterthrush, Seiurus noveboracensis (Gmelin) (Passeriformes: Parulidae) (Durden et al. Reference Durden, Oliver and Kinsey2001). Both southern temperate and Neotropical passerines annually transport B. burgdorferi-infected ticks from the southeastern United States of America to distant northern breeding grounds during spring migration (Scott et al. Reference Scott, Fernando, Banerjee, Durden, Bryne and Banerjee2001; Morshed et al. Reference Morshed, Scott, Fernando, Beati, Mazerolle and Geddes2005; Ogden et al. Reference Ogden, Lindsay, Hanincová, Barker, Bigras-Poul and Charron2008; Scott and Durden Reference Scott and Durden2009; Scott et al. Reference Scott, Lee, Fernando, Durden, Jorgensen and Mak2010; Hamer et al. Reference Hamer, Goldberg, Kitron, Brawn, Anderson and Loss2012; Scott et al. Reference Scott, Anderson and Durden2012). Migratory songbirds have the flight speed and capacity to fly long distances in short periods of time, which potentially allows them to carry engorged ticks from the southern United States of America to Canada before these ixodid ectoparasites complete their blood meals. Therefore, they can introduce a diversity of B. burgdorferi s.l. genotypes associated with Lyme disease and other tick-associated pathogens (Scott and Durden Reference Scott and Durden2009; Crowder et al. Reference Crowder, Matthews, Schutzer, Rounds, Luft and Nolte2010; Mathers et al. Reference Mathers, Smith, Cahill, Lubelczyk, Elias and Lacombe2011). Since I. minor ticks are considered to have vector competence for B. burgdorferi s.l., they can retain spirochetes in their midgut, and infect suitable zoonotic hosts, such as rodents and songbirds in their new locales.
With respect to mammalian hosts in the southeastern United States of America, I. minor has been collected from the cotton mouse, Peromyscus gossypinus (Le Conte) (Rodentia: Cricetidae); hispid cotton rat, Sigmodon hispidus Say and Ord (Rodentia: Cricetidae); eastern woodrat, Neotoma floridana (Ord) (Rodentia: Cricetidae); house mouse, Mus musculus Linnaeus (Rodentia: Muridae); and Norway rat, Rattus norvegicus (Berkenhout) (Rodentia: Muridae) (Oliver et al. Reference Oliver, Chandler, James, Sanders and Hutcheson1995, Reference Oliver, Lin, Clark, Banks, Durden and James2003), and these rodent hosts can maintain B. burgdorferi s.l. infections in their bodies for years (Oliver et al. Reference Oliver, Lin, Clark, Banks, Durden and James2003). The latter two rodents are common in parts of Canada, and could act as vertebrate hosts for I. minor.
The present study elucidates long-distance dispersal patterns of extralimital ticks in Canada. Stutchbury et al. (Reference Stutchbury, Tarof, Done, Gow, Kramer and Tautin2009) used light-level geolocators on certain Neotropical songbirds, and documented the pace of long-distance flight for these passerine migrants to be more than 575 km/day. In our study, the flight path from Savannah, Georgia, United States of America to Toronto, Ontario, Canada is ~1300 km, and can be flown in three to five days by Neotropical and southern-temperate migrants. This is the normal period of time for a larval or nymphal I. minor to become fully engorged, and have a complete blood meal. Upon arrival, a replete I. minor larva may drop into cool, moist leaf litter, and moult to a nymph and, subsequently, the unfed nymph can parasitise a songbird or small mammal. Of note, Savannah, Georgia is mid-range for indigenous I. minor (Durden and Keirans Reference Durden and Keirans1996), and the locality of the first North American collection of I. minor; at that time, Smith and Gouck (Reference Smith and Gouck1947) described it as Ixodes bishoppi Smith and Gouck, but this name was later shown to be a junior synonym of I. minor.
At least six Ixodes species ticks are known to be carried into central and eastern Canada during spring migration. The blacklegged tick, Ixodes scapularis Say, is a competent vector of B. burgdorferi s.l., and is the most common Ixodes tick imported by migratory songbirds. As well, five other Ixodes species; namely, Ixodes affinis Neumann; Ixodes brunneus Koch; the rabbit-associated tick, Ixodes dentatus Marx; the mouse tick, Ixodes muris Bishopp and Smith, and newly recorded species, I. minor, are transported into Canada. Of these six bird-feeding Ixodes ticks, all are reported in the southeastern United States of America (Durden and Keirans Reference Durden and Keirans1996).
Pertinent to our study, I. minor is known to harbour at least four B. burgdorferi s.l. genospecies: B. americana, B. bissettii, B. carolinensis, and B. burgdorferi s.s. (Oliver et al. Reference Oliver, Chandler, James, Huey, Vogel and Sanders1996, Reference Oliver, Lin, Clark, Banks, Durden and James2003; Rudenko et al. Reference Rudenko, Golovchenko, Grubhoffer and Oliver2009a, Reference Rudenko, Golovchenko, Lin, Gao, Grubhoffer and Oliver2009b). Recently, Rudenko et al. (Reference Rudenko, Golovchenko, Belfiore, Grubhoffer and Oliver2014) elucidated cross-species recombination of genes normally found in B. burgdorferi s.s.in another Borrelia genospecies (B. americana) isolated from I. minor immatures collected from a Carolina Wren in South Carolina. Hence, I. minor can act as a vector of bird-associated strains of Lyme disease spirochetes, and exacerbate a public health risk. After bird-conveyed I. minor detach in northern latitudes and, subsequently moult, B. burgdorferi s.l. variants may be introduced into the mammalian population, especially rodents. Although vector competence studies have not been done in the laboratory, I. minor shows a positive association with B. burgdorferi s.l. infection in rodents and songbirds (Clark et al. Reference Clark, Oliver, Grego, James, Durden and Banks2001).
During the physical examination of passerines, a partially engorged larval tick was collected from a Common Yellowthroat, Geothlypis trichas (Linnaeus) (Passeriformes: Troglodytidae), at Toronto, Ontario, Canada, on 20 May 2013. Using the ixodid larval key of Clifford et al. (Reference Clifford, Anastos and Elbl1961), we initially identified the specimen as I. minor. The physical characteristics of our specimen were compared with larval progeny of a bred I. minor male and female and, similarly, with scanning electron micrographs of a confirmed (bred) larval I. minor that will be used in a forthcoming guide to larval ixodids of the United States of America, which also includes Canadian species, by L.A.D. and colleagues (in preparation). The bred specimens are in the United States National Tick Collection (Georgia Southern University, Statesboro, Georgia, United States of America). This novel, bird-tick finding is the northernmost discovery of this tick species, and constitutes the premiere recognition of I. minor in Canada. Because of the special significance of this extralimital tick, we have not tested it for B. burgdorferi, and have kept it intact as a voucher specimen; it has been placed in the Biodiversity Institute of Ontario (University of Guelph, Guelph, Ontario, Canada) with accession number, BIO-13–116.
Borrelia burgdorferi s.l. elicits variable antibody responses in infected Lyme disease patients (Stricker Reference Stricker2007). Conventional Lyme disease serology testing often misses the presence of antibodies to B. burgdorferi s.l., especially in immune-suppressed patients (Cadavid et al. Reference Cadavid, O’Neill, Schaefer and Pachner2000). Because Lyme disease serology test kits only demonstrate antibodies against 1–3 strains, they can miss antibodies to several Borrelia group variants, including those noted in the southeastern United States of America. Some researchers report true sensitivity of an estimated 44–56% for the two-tier serology system for Lyme disease, and lower, when commercial testing is used in clinical practice evaluation (Stricker and Johnson Reference Stricker and Johnson2008; Sperling and Sperling Reference Sperling and Sperling2009; Sperling et al. Reference Sperling, Middelveen, Klein and Sperling2012). However, I. minor can introduce genospecies and/or genotypes of B. burgdorferi s.l. (i.e., B. americana, B. andersonii, B. bissettii, B. carolinensis, and B. burgdorferi s.s.), which are not represented in current Lyme disease serology test kits. With the exception of B. carolinensis, all of these genospecies have been detected in humans. Pathologically, Clark et al. (Reference Clark, Leydet and Hartman2013) recently documented B. americana, B. andersonii, and B. burgdorferi s.s. in Lyme disease patients in Georgia and Florida. Consequently, patients can exhibit false negative serology and, yet, have bona fide Lyme disease (Rudenko et al. Reference Rudenko, Golovchenko, Lin, Gao, Grubhoffer and Oliver2009b, Clark et al. Reference Clark, Leydet and Hartman2013). Since migratory passerines introduce an estimated 50 million Lyme disease vector ticks into Canada annually during northward spring migration (Ogden et al. Reference Ogden, Lindsay, Hanincová, Barker, Bigras-Poul and Charron2008; Scott et al. Reference Scott, Lee, Fernando, Durden, Jorgensen and Mak2010), there is ample opportunity for I. minor to bring several diverse B. burgdorferi s.l. variants from the southern United States of America, including recombinant genotypes.
Although I. minor seldom bites humans (Oliver et al. Reference Oliver, Lin, Clark, Banks, Durden and James2003), this tick may introduce new B. burgdorferi s.l. genotypes into reservoir-competent, mammalian hosts in new foci. Regardless of where Canadian patients reside, they may become infected with pathogenic Lyme disease-causing spirochetes harboured by songbird-transported Ixodes ticks from the southeastern United States of America. Notably, I. minor extends its extralimital range into Canada, and is one of six Ixodes tick species that can introduce genetically diverse variants of B. burgdorferi s.l.
Acknowledgements
The authors thank Bronwyn Dalziel and Nigel Shaw for making the tick collection. They are indebted to Irene Pages for French translation of the Abstract. For financial support, they are grateful to the Canadian Lyme Disease Foundation and Lyme Ontario.