Introduction

Ticks are vectors of many human and other animal disease agents (Nicholson et al. 2009). Amblyomma rotundatum Koch, 1844 is a hard-bodied tick (Acari: Ixodida: Ixodidae) that is typically found on amphibians and reptiles. This parthenogenetic tick has a biogeographical range from Argentina to Mexico, including the Caribbean Islands (Jones et al. 1972, Guglielmone et al. 2003, Nava et al. 2007, Voltzit 2007, Guzman-Corejo et al. 2011) and southern part of Florida (Oliver et al. 1993, Corn et al. 2011). Zoogeographically, A. rotundatum is now established in localized areas within the southernmost fringe of the Nearctic Region. In South America, this obligate, hematophagous ectoparasite is also known to feed on certain mammals, including humans (Guglielmone & Nava 2010). Of note, severe parasitic infestations of A. rotundatum on amphibians and reptiles can cause exsanguination and death (Keirans & Durden 1998).

Some other Neotropical and southern Nearctic Amblyomma species have been previously reported during spring migration on songbirds (Passeriformes) in Canada. These songbird-carried Amblyomma ticks 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; Ogden et al. 2008a), A. maculatum Koch (Scott et al. 2001, 2010, 2012), and A. sabanarae Stoll (Scott et al. 2001, 2010, 2012). In addition, Ixodes ticks, such as I. affinis and I. minor, are transported from the southeastern United States and the Neotropics by passerines (Scott et al. 2012, Scott & Durden 2014).

Extralimital transport of ticks between continents by wild birds can occur, during hemispheric and intercontinental flight (Hoogstraal & Kaiser 1961, Olsen et al. 1995, Bjoersdorff et al. 2001). Other Neotropical ticks, such as Amblyomma nodosum Neumann, an extralimital tick in the Nearctic Region, have been collected from passerine migrants in the Great Lakes Region (Hamer et al. 2012).

We present a novel phenomenon of bird parasitism showing that Neotropical passerines can transport A. rotundatum ticks to Canada during northward spring migration, and substantiate long-distance transit of bird-feeding ticks within the Western Hemisphere.

Materials and methods

A fully engorged nymphal tick was collected from a wild-caught Veery, Catharus fuscescens(Stephens) (Passeriformes: Turdidae), band number 2681-88949, on 26 May 2014 at the Tip (42.55ºN, 80.05ºW) of Long Point, Ontario, Canada, which juts out into Lake Erie. The live nymphal tick was placed in a 4-dram (12 mL) polystyrene vial with a vented cap made of tulle netting. In order to facilitate receiving live ticks in the laboratory, one drop of water was added to the paper towel inside the vial. Next, the vial was inserted into a self-sealing plastic bag with slightly moistened paper towel to retain high humidity. Taxonomic keys for Amblyomma nymphs and females respectively by Keirans & Durden (1998), Martins et al. (2010) and Jones et al. (1972) were used.

In order to allow the nymphal tick to molt to an adult, the specimen was held between 18–22ºC and relative humidity of 90–95% with a photoperiod of 16:8 (L:D). These climatic settings reflect field conditions in tick habitats during late May to early July in southeastern Canada. The fully engorged nymph was checked weekly to ensure that the humidity was optimal, that it was not spoiled by deleterious microorganisms or invasive endoparasites, and the molt was in progress. At molt, the exoskeleton was stored in a 2 mL micro tube containing 94% ethyl alcohol. The Amblyomma sp. nymph was compared to the scanning electron micrographs and the redescription of Amblyomma by Keirans & Oliver (1993). After the nymph-adult molt, the female was kept alive for 2 mo to ensure it was fully mature and sclerotized before confirming the identification. The Amblyomma sp. female was compared to the line drawings of Robinson (1926) and Boero (1957). The live Amblyommafemale was sent by overnight courier to LAD for further examination. The female was assessed morphologically, and compared with similar Amblyomma females in the U.S. National Tick Collection.

Because of the special significance of this bird-parasitizing, Neotropical Amblyomma tick, we did not test it for pathogens, and have kept it intact as a voucher specimen. This tick, reference number14-5A71, has been deposited in the Biodiversity Institute of Ontario (University of Guelph, Guelph, Ontario, Canada) with accession number, BIO-14-120.

Results

After collection from the Veery, the fully engorged A. rotundatum nymph molted to a female in 44 d. When the female matured, and was fully sclerotized (Fig. 1), it was stored in 94% ethyl alcohol. Upon preservation, tunnelling by an endoparasite was evident in the right, latero-posterior section of the idiosoma; its presence did not impede the completion of the tick molt. The mature Amblyommafemale displayed two short, rounded spurs on coxae I-IV. The presence of 2 spurs on all coxae is characteristic of Amblyomma species associated with reptiles and/or amphibians, including A. argentinae, A. dissimile, and A. rotundatum, each of which parasitizes both reptiles and amphibians. The hypostome has 3/3 dentition and the tip is very slightly truncated. Although scutal punctations are slightly more numerous and evenly distributed than in most reference specimens in the U.S. National Tick Collection, the mature female was confirmed as A. rotundatum (Fig. 1).

FIGURE 1.

Amblyomma rotundatum, unfed female, dorsal view live, legs recoiled in a defensive stance. This Neotropical tick was originally collected as an attached nymph from a Veery, Catharus fuscescens, and held to molt to a female. The beige colored area in the right latero-posterior area of the idiosoma suggests activity of an endoparasite. Photo credit: Alan Bibby

Discussion

We provide the first documentation of A. rotundatum on a bird, and the first record of this tick species in Canada. We conducted a thorough examination of the literature, and have not found any reference to this species on an avian host. Labruna et al. (2007) reported immature stages of A. longirostre Koch, Amblyomma calcaratum Newmann, A. nodosum, and Amblyomma cajennense (F.) on birds in Brazil. Moreover, Ogrzewalska et al. (2009) reported immatures of Amblyomma coelebsNeumann, Amblyomma ovale Koch, and Amblyomma naponense (Packard) on birds in Brazil. In addition to these Amblyomma ticks, Keirans and Durden (1998) reported immatures of A. americanum, Amblyomma imitator Kohls, A. inornatum, A. maculatum and Amblyomma tuberculatum Marx on birds in the United States.

Bird parasitism and long-distance migration is a subtle dispersal mechanism for certain species of extralimital ticks and their associated pathogens. Our study highlights the introduction of A. rotundatum into southern Canada by a Veery during northward spring migration. In Brazil, this tick species is known to harbour Rickettsia bellii, which can cause spotted fever Rickettsiosis in humans (Labruna et al. 2004). Also, Rickettsia amblyommii, a putative human pathogen, has been detected in Amblyomma in South America. Additionally, Rickettsia parkeri has been detected in Amblyommaspecies ticks collected in Brazil, and is known to cause human spotted fever (Medeiros et al. 2011). Likewise, R. parkeri is associated with A. maculatum (Parker 1940, Paddock et al. 2004), which is indigenous in areas bordering the Gulf of Mexico (Sumner et al. 2007); immature stages of this tick species are transported into Canada on passerine migrants (Scott et al. 2001, 2010, 2012). Migratory songbirds clearly have great potential to widely disperse immature stages of Amblyomma ticks within the Western Hemisphere and, after molting, these ticks could parasitize various vertebrate hosts, including humans, and transmit zoonotic pathogens. These findings may have epidemiological significance in Canada.

The distance that songbirds transport ticks has been in dispute. Ogden et al. (2008b) conjectured that the maximum distance which a songbird can carry immature Ixodes scapularis Say during a 5-day blood meal, is 425 km. In contrast, multiple researchers have documented that Neotropical and southern temperate songbirds can transport ixodid ectoparasites much greater distances (Scott et al.2001, 2010, 2012; Morshed et al. 2005, Hamer et al. 2012, Scott & Durden 2014). Stutchbury et al.(2009) used light-sensitive geolocators (nano-tags) to track the daily movement patterns and the flight path of passerine migrants, and found that some Neotropical songbirds can have a flight pace of 750 km/day or more, and follow a doglegged pattern during northward spring migration. Passerines can fly as much as 950 km/day during migratory flight (Smith et al. 1996) and, when heavily infested, can initiate new foci of ticks (Anderson & Magnarelli 1984, Scott et al. 2014). Rapid northward migration is aided by southerly winds, warm temperature, body condition, in addition to bird species. At the northern fringe of the A. rotundatum range, in Florida, the direct flight path is approximately 1800 km from southern Florida (Miami) to Long Point, Ontario. Neotropical and southern temperate passerine migrants are clearly capable of transporting slow-feeding immature stages of Amblyomma ticks much greater distances than previously claimed.

Veeries have a wintering range in southeastern South America, principally in southern Brazil. This bioregion also encompasses the indigenous range of A. rotundatum. The initial tick infestation could have originated in this Brazilian region. The fully engorged nymph could have attached to the Veery for 10-12 days during its migratory flight to its breeding grounds in southern Canada. The flight distance from southeastern Brazil to Long Point, Ontario for this bird parasitism may have been as far as 7500 km.

Notably, an attached female A. rotundatum has been recorded to cause tick paralysis in a snake; namely, a Southern Black Racer, Coluber constrictor priapus Dunn & Wood, in southern Florida (Hanson et al. 2007). Removal of this tick restored the snake to full mobility within 18 h. This specific example A. rotundatum parasitism is noteworthy because it shows the potential lethal nature of this tick species to cause tick paralysis.

Since passerines can be parasitized by A. rotundatum immatures, we now have substantive evidence to show that Neotropical migrants may have been the means by which this tick species became established in Florida. In the springtime, passerine migrants could easily transport immature A. rotundatum northward from avian wintering grounds in Central and South America, or the Caribbean Islands. If a passerine migrant was heavily infested with A. rotundatum immatures, and released them in one tick-conducive, maritime-like environment with suitable hosts, it could certainly start a new tick population. Even though it was supposed that A. rotundatum was imported on the cane toad, Rhinella marina (Linnaeus), formerly Bufo marinus, as an integrated pest management agent to control pest beetles between 1955 to 1964 (Oliver et al. 1993), we suggest migratory passerines as an alternative means of tick introduction. Since A. rotundatum typically reproduces by parthenogenesis, theoretically, only a single replete nymph, which subsequently molts to a female, would be needed in a new geographic locality to initiate a new colony. Because A. rotundatum was not apparently native to Florida, this novel bird parasitism casts a new perspective on how this tick species may have been introduced into the southeastern United States.

Based on the native range of A. rotundatum, it is highly unlikely that an immature A. rotundatumwould have the winter hardiness to survive frigid, sub-zero, Canadian winters. Even though A. rotundatum is established in southern Florida, it is primarily a Neotropical tick.

In conclusion, the discovery of an A. rotundatum nymph on a Veery at Long Point, Ontario constitutes the northernmost report of this tick species. This collection also provides a new distributional record for A. rotundatum; biogeographically, we document this ixodid ectoparasite much further north than its established range. Significantly, we report the first-ever record of A. rotundatum on an avian host, and, synchronously, on a Veery. Health-care professionals should take heed that R. bellii-infected immature stages of A. rotundatum and other ticks and vector-borne pathogens may be introduced into Canada by migratory songbirds. Before the frosty fall weather arrives in Canada, Amblyomma ticks may molt during the early summer and, during the late summer, parasitize and infect people with tick-borne pathogens.