We document Amblyomma dissimile Koch (Acari: Ixodidae) parasitizing a bird in Canada. A partially engorged A. dissimile nymph was collected from a Veery, Catharus fuscescens (Stephens) (Passeriformes: Turdidae), in Toronto, Ontario during spring migration. This constitutes the first authentic host record of A. dissimile on a bird in North America and, likewise, on a Veery, plus a new distributional record in Canada. Veeries could theoretically transport A. dissimile from as far south as southeastern Brazil, a distance of over 7,500 km. Experimentally, A. dissimile can transmit Ehrlichia ruminantium (Ricksettiales), which causes heartwater, a severe disease of cattle and other ungulates. Since a fully engorged A. dissimile nymph could likely molt during the summer in northern latitudes, this tick species could potentially parasitize local reptiles, people or ungulates, and cause autochtonous disease. Because A. dissimile is known to harbor rickettsiae in South America and is a laboratory vector of E. ruminantium, the medical and veterinary profession must be vigilant that A. dissimile may pose a health risk.
Introduction
Amblyomma dissimile Koch is a hard-bodied tick (Acari: Ixodida: Ixodidae) that feeds primarily on toads (Anura), turtles (Testudines), and lizards (Squamata) but is also known to parasitize mammals belonging to at least 10 families (Guglielmone & Nava 2010). Notably, A. dissimile has been reported on cattle, goats, sheep (Bovidae), rabbits (Lagomorpha), rodents (Rodentia), and humans (Guglielmone & Nava 2010). This tick species also has a host-parasite relationship with crocodiles (Crocodilia). The commonest hosts harboring all parasitic stages (larvae, nymphs, adults) of A. dissimile are: cane toad, Rhinella marina (Linnaeus) (formerly Bufo marinus); Boa constrictor Linnaeus, and Iguana iguana (Linnaeus) (Guglielmone & Nava 2010). The focal host range for A. dissimile is in the Neotropics where all three of these vertebrate hosts are indigenous. Biogeographically, A. dissimile has a natural host range that extends from northern Argentina to southern Mexico, the Caribbean Islands, and southern Florida (Jones et al. 1972, Nava et al. 2007). This obligate, hematophagous ectoparasite is now established throughout much of the Neotropics, and also the southernmost fringe of the Nearctic Region.
Ticks are vectors of many infectious agents of human and other animal diseases (Nicholson et al. 2009). Under experimental conditions A. dissimile is an efficient vector between goats of Ehrlichia ruminantium Dumler (Rickettsiales) (formerly Cowdria ruminantium), which causes fatal heartwater in cattle, goats, sheep and other ungulates (Jongejan 1992).
Several Amblyomma species from the Neotropics and southern United States have been reported on songbirds (Passeriformes) in Canada during northward spring migration. These Amblyomma spp. include: A. americanum (Linnaeus) (Scott et al. 2001, 2010), A. humerale Koch (Morshed et al. 2005), A. inornatum (Banks) (Ogden et al. 2008a), A. longirostre (Koch) (Scott et al. 2001, 2010, 2012), A. maculatum Koch (Scott et al. 2001, 2010, 2012; Ogden et al. 2008a), A. rotundatum Koch (Scott & Durden 2015a), and A. sabanerae Stoll (Scott et al. 2001, 2010, 2012; Scott & Durden 2015b). Within the Great Lakes region, Hamer et al. (2012) also reported A. nodosum Neumann, a neotropical tick from Brazil, collected from a migratory songbird at the southern end of Lake Michigan. In Louisiana, Mukherjee et al. (2014) recorded A. longirostre, A. nodosum A. maculatum and A. calcaratum Neumann from northward migrating songbirds. Additionally, Ixodes ticks, such as I. affinis Neumann and I. minor Neumann, which are indigenous to the southeastern United States and Central America, have been reported on Neotropical songbirds in Canada during spring migration (Scott et al. 2012, Scott & Durden 2015c).
Fairchild et al. (1966) reported an A. dissimile male on a Boat-billed Heron, Cochlearius cochlearius Linnaeus, in Panama. Scofield et al. (2011) documented a partially engorged nymph from a Blue-winged Macaw, Primolius marcana Vieillot, in the State of Pará, Brazil.
Migratory Neotropical songbirds have an inherent capacity of flying long distances in a short period of time, and reaching Canada (Scott et al. 2012, Scott & Durden 2015a, Scott & Durden 2015b, Scott & Durden 2015c). This capability allows them to transmit ixodid ticks long distances while the attached ticks are taking a blood meal. Subsequently, these engorged ticks are imported and released in Canada during northward spring migration.
Our objective was to continue to monitor tick species that are coming into Canada via Neotropical and southern temperate songbirds and to determine what pathogens these attached ticks may be carrying.
Materials and methods
Bird banders collected a partially engorged nymphal tick from a wild-caught Veery, Catharus fuscescens (Stephens) on 24 May 2015 at Toronto, Ontario, Canada (43.6178° N, 79.3425° W). After measurements and physical examination of this bird, the banders employed super-fine, stainless steel tweezers to remove the tick. The tick was inserted in a 8.5 mL polypropylene tube (15.7 X 75 mm) with a label listing collection and background information. A 7-mm hole in the polyethylene pushcap (15.7 mm diameter) provided ventilation for the tick. Tulle netting covered the inside of the push-cap to prevent the tick from escaping. This tube was placed in a self-sealing, double-zippered plastic bag with slightly moistened paper towel, and sent by regular mail to the lab (JDS). Taxonomic identification keys for Amblyomma spp. nymphs were used for morphological identification (Keirans & Durden 1998, Martins et al. 2010). After preliminary identification (JDS), the live, nymphal tick was sent via overnight courier to LAD for confirmation of identification. In order to slow down the movement of the tick, it was held on a cold plate for physical examination.
The Amblyomma sp. nymph (15-5A48) was kept alive in high relative humidity (90–95%) for 37 d to see if it would molt to an adult. Since this partially engorged nymph would not molt, it was put in 94% ethyl alcohol. Dorsal and ventral close-up photographs of the A. dissimile nymph were taken using a Nikon Multizoom AZ100M steroscopic microscope with a Nikon DS-Fi1 camera.
Because of the special significance of this nymph, we did not test it for tick-borne pathogens and, instead, have kept it intact as a voucher specimen. The nymphal tick has been deposited in the Biodiversity Institute of Ontario (University of Guelph, Ontario, Canada) with accession number BIO-15-092.
Results
The nymph (Figure 1) exhibited the following physical characteristics: coxa I with 2 spurs, coxa II with only 1 spur, cornua absent, auriculae absent, hypostome dentition 2.5/2.5, dorsum of body lacking dense pilosity, and scutum sparsely punctated. Based on these distinctive physical characteristics, the ixodid nymph was confirmed as A. dissimile.
Discussion
We provide a novel discovery of bird parasitism which illustrates that certain migratory songbirds can transport A. dissimile to Canada during northward spring migration. Our findings underscore the fact that passerine migrants transport ticks much farther than previously hypothesized by some researchers. At the same time, we show that A. dissimile has a northward extralimital range within the Western Hemisphere into Canada.
Neotropical passerines can transport ticks hundreds of kilometers during migration from wintering grounds to breeding grounds. Ogden et al. (2008b) postulated that songbirds can fly a maximum distance of 425 km during a 5-day engorgement period. In contrast, other researchers have documented Neotropical and southern temperate passerines transporting ixodid ticks much greater distances (Scott et al. 2001, Morshed et al. 2005, Scott et al. 2010, Hamer et al. 2012, Scott & Durden 2015a, Scott & Durden 2015b, Scott & Durden 2015c, Scott 2015). Leberman & Browne (1976) documented a Red-eyed Vireo, Vireo olivaceus (L.) flying 483 km from Pennsylvania to North Carolina on an overnight flight. As well, Brewer et al. (2000) reported a White-throated Sparrow, Zonotrichia albicollis (Gmelin), flying 681 km from Bradley, Ontario (in Chatham-Kent) to Lakeview Heights, Ontario in a single day. From the northern edge of the range of A. dissimile, the distance is approximately 1990 km from southern Florida (Miami) to Toronto, Ontario. Since the wintering range of Veeries is in southeastern Brazil, and the geographic range of A. dissimile extends as far south as northern Argentina, the Veery could have transported this tick as far as 7500 km during its migratory flight. Neotropical and southern temperate passerines are clearly capable of transporting slow-feeding Amblyomma ticks much greater distances than previously surmised.
In addition, Stutchbury et al. (2009) used light-sensitive geolocators (nano-tags) to track the daily flight path of migratory passerines, and found that certain Neotropical songbirds have a flight pace of 750 km/d or more, and followed a doglegged pattern during northward spring migration. Using geolocators, DeLuca et al. (2015) tracked Blackpoll Warblers, Setophaga striata (Forster), during fall migration flying an average of 62 h for an average distance of 2540 km (923 km/day) on their non-stop flight over the Atlantic Ocean. These passerine migrants depart from the northeastern United States and Maritime Provinces and fly directly to Hispaniola or Puerto Rico and, potentially, directly to their wintering range in the northern part of South America. When a passerine migrant has plentiful energy reserves before and during the migratory flight, it can fly more than 10 times the distance conjectured by some researchers. South winds, warm temperatures, body condition, and bird species can greatly enhance rapid movement while en route to their breeding range and nesting grounds. The presence of the A. dissimile nymph on the Veery at Toronto during spring migration underscores a much greater flight pace and distance than some researchers have speculated.
Corn et al. (2011) suggested that A. dissimile was imported into Florida from the Neotropical region on reptiles. However, we suggest that A. dissimile could have been introduced into southern Florida from the Caribbean Islands, Central America or South America via migratory passerines. In southern Florida, A. dissimile is sympatric with A. rotundatum (Oliver et al. 1993); both tick species are amphibian- and reptile-feeding ticks in the southern maritime Nearctic Region. It seems feasible that a fully engorged A. dissimile, which has a similar home range as A. rotundatum, could molt to an adult in northern latitudes, because an A. rotundatum nymph has previously molted to a female in Canada (Scott & Durden 2015a). Furthermore, a heavily infested, ground-foraging passerine has the potential to aid in the establishment of new foci of ticks and associated pathogens at stopover sites or nesting grounds, especially when suitable hosts are present in these localities (Anderson et al. 1990, Scott et al. 2014).
Adult A. dissimile are primarily found on snakes (Jones et al. 1972, Guglielmone & Nava 2010, Verbel-Vergara et al. 2015), but they are also reported on lizards, iguana and toads. The commonest hosts of all three parasitic life stages of A. dissimile in the Neotropics are the cane toad (Rhinella marina), Boa constrictor, and Iguana iguana (Guglielmone & Nava 2010).
As an ectoparasite, A. dissimile has the potential to transport ricksettsiae to mammalian hosts, including people. Although primarily a reptile-associated parasite, this tick species is also reported to parasitize cattle, goats, sheep, rabbits, rodents, and humans (Guglielmone & Nava 2010). Based on experimental studies with A. dissimile, Jongejan et al. (1992) found that A. dissimile is a competent vector of E. ruminantium, the causative agent of cowdriosis or heartwater, a severe rickettsial disease of ruminants in sub-Saharan Africa and the Caribbean. According to these findings, A. dissimile could play an important role in the maintenance of rickettsiae among certain amphibian, reptilian, and mammalian hosts. Moreover, Candidatus Rickettsia columbianensi, a rickettsial bacterium of unknown pathogenicity that is associated with A. dissimile, was recently reported from Colombia (Miranda et al. 2012). After feeding as a larva or nymph, and subsequently molting to the next life stage, an infected A. dissimile nymph or female could bite, and potentially transmit E. ruminantium or other rickettsiae to a suitable vertebrate host. In essence, the wide diversity of vertebrate hosts for A. dissimile provides greater opportunity of this tick species to acquire rickettsiae from infected hosts, and transmit them to other hosts.
The ability of Neotropical Amblyomma spp. ticks attached to northward migrating songbirds to introduce spotted fever group (SFG) rickettsiae into North America was recently demonstrated by Mukherjee et al. (2014) who recorded six distinct SFG rickettsiae in four species of Amblyomma ticks collected from songbirds in Louisiana. Additionally, Andoh et al. (2015) molecularly detected several different Rickettsia and Ehrlichia strains, some of which were very similar to known human pathogens, in exotic ticks (Amblyomma spp. and Hyalomma spp.) collected from exotic amphibians and reptiles that had been brought into Japan for the pet trade. Andoh et al. (2015) emphasized the potential for these pathogens to be transferred from non-native ticks to humans in Japan. Of course, the same would be true for North America whether the ticks were purposely imported for the pet trade or introduced naturally on migrating birds.
It is highly unlikely that A. dissimile would become established in Canada. Amblyomma spp. larvae, in particular, succumb to frigid Canadian winters. However, whenever a rickettsiae-infected A. dissimile is imported into Canada via a passerine migrant during spring migration, it could molt to the next life stage during the warm summer. It could then feed on and infect a local reptile (e.g., American five-lined skink, Pleistiodon fasciatus (Linnaeus)), which is found across southern Ontario. Such a reptilian host could in theory serve as an enzootic reservoir for rickettsiae. Subsequently, a larval or nymphal Ixodes scapularis Say could potentially act as a bridge vector to other vertebrate hosts, including ungulates or humans.
In conclusion, we document the first authentic report of A. dissimile parasitizing a bird in North America. Likewise, we provide the first host record of this tick on a bird in Canada. The presence of a nymphal A. dissimile on a Veery collected in southern Canada extends both the known northward extralimital range of this tick species and underscores the rapid, long-distance flight of migratory passerines during the tick engorgement period. With the presence of a partially engorged A. dissimile on a Veery, 23 species of ticks have now been recorded to parasitize birds in Canada. The medical and veterinary profession must be vigilant that migratory songbirds may be able to transport rickettsiae-infected A. dissimile as far north as Canada, and potentially cause serious illness.
Acknowledgments
We thank Charlotte England and Nigel Shaw for collecting the engorged Amblyomma dissimile tick from the Veery. We gratefully acknowledge the expertise of Kellyn Hawley in taking the photographs of the A. dissimile nymph. This research was supported by Lyme Ontario.
