New Records of Ticks (Acari: Ixodidae) From Dogs, Cats, Humans, and Some Wild Vertebrates in Alaska: Invasion Potential

Abstract

During 2010–2016, tick specimens were solicited from veterinarians, biologists, and members of the public in Alaska. Eight species of ticks were recorded from domestic dogs. Some ticks were collected from dogs with recent travel histories to other countries or other U.S. states, which appears to explain records of ticks not native to Alaska such as Amblyomma americanum (L.) (lone star tick), Ixodes scapularis (Say) (blacklegged tick), and Ixodes ricinus (L.). However, we recorded Dermacentor variabilis (Say) (American dog tick) from dogs (and humans) both with and without travel history, suggesting that this nonindigenous tick could be establishing populations in Alaska. Other ticks commonly recorded from dogs included the indigenous Ixodes angustus Neumann and the invasive Rhipicephalus sanguineus (Latreille) (brown dog tick). Domestic cats were only parasitized by one tick species, the native I. angustus . Six species of ticks were recorded from humans: A. americanum (with and without travel history), Dermacentor andersoni Stiles (Rocky Mountain wood tick; travel associated), D. variabilis (with and without travel history), Haemaphysalis leporispalustris (Packard) (rabbit tick, native to Alaska), I. angustus , and R. sanguineus. Ixodes angustus predominated among tick collections from native mammals. Also, Ixodes texanus Banks (first record from Alaska) was collected from an American marten, Martes americana (Turton), H. leporispalustris was recorded from a snowshoe hare, Lepus americanus Erxleben, and Ixodes auritulus Neumann was collected from a Northwestern crow, Corvus caurinus Baird. The establishment of D. variabilis , D. andersoni , A. americanum , and/or I. scapularis in Alaska would have strong implications for animal and human health.

ticks, Alaska, new records, medical-veterinary importance

Historically, the tick fauna of Alaska has been fairly well documented, with seven established species of hard ticks (Acari: Ixodidae) reported from this state: Haemaphysalis leporispalustris (Packard) (rabbit tick), Ixodes angustus Neumann, Ixodes auritulus Neumann, Ixodes howelli Cooley and Kohls, Ixodes signatus Birula, Ixodes uriae White, and the invasive (now established) Rhipicephalus sanguineus (Latreille) (brown dog tick; Bishopp and Trembley 1945 , Keirans and Clifford 1978 , Murrell et al. 2003 , Durden and Keirans 1996 , Walker et al. 2000 ). Four of these species, I. auritulus , I. howelli , I. signatus , and I. uriae , are associated with avian hosts ( Keirans and Clifford 1978 , Durden and Keirans 1996 ). Recent tick submissions to the Office of the Alaska State Veterinarian in Anchorage and the Alaska Department of Fish and Game in Fairbanks have revealed that additional species of ticks are being collected in Alaska. Some of these ticks have significant veterinary and medical importance. In this paper, we document these tick species and discuss their relevance with respect to invasion potential and animal and human health in Alaska.

Materials and Methods

During 2010–2016, the Alaska Department of Fish and Game and Office of the State Veterinarian solicited tick specimens collected from pets, wildlife, and humans from veterinarians, biologists, and members of the public. Information on any travel history of pets and humans was also requested. Ticks were submitted from domestic dogs ( Canis lupus ), domestic cats ( Felis catus ), humans, and various native wild vertebrates from several locations in Alaska. Most tick specimens received were morphologically intact but a few were missing part or all of the hypostome or part of the capitulum. Ticks were identified using standard guides ( Cooley 1946 , Brinton et al. 1965 , Keirans and Clifford 1978 , Keirans and Litwak 1989 , Durden and Keirans 1996 , Hillyard 1996 , Kleinjan and Lane 2008 ) and deposited in the University of Alaska Museum of the North (UAM) in Fairbanks. Tick specimens from this study and their UAM accession numbers can be accessed via the link http://arctos.database.museum/saved/Ticks-specimens . The accession number for the entire UAM tick donation from this study is “UAM-2014.15-UAM-Ticks-Ento,” and each individual accession number is preceded by “UAM:Ento:” Most submissions consisted of one tick specimen, but several submitters stated that additional specimens were present (but not submitted) on the same host individual, especially for dog hosts. Tick identifications were provided to submitters who were also advised of any potential health problems related to parasitism by the ticks.

Results

Ticks were received from 29 different localities in Alaska and from nine different species of vertebrate hosts ( Tables 1–3 ). Ten different species of ticks were recorded during this survey. Table 1 lists data for the eight species of ticks recorded from domestic dogs, including two native tick species ( I. angustus and I. auritulus ), one invasive but established species ( R. sanguineus ), four species that are indigenous to other regions of North America ( Amblyommaamericanum (L.)—lone star tick, Dermacentorandersoni (Stiles)—Rocky Mountain wood tick, Dermacentorvariabilis (Say)—American dog tick, and Ixodesscapularis —blacklegged tick), and one species native to the Palaearctic region, Ixodes ricinus (L.). Table 2 lists the six species of ticks recorded from humans representing three species known to be established in Alaska ( H. leporispalustris , I. angustus , and R. sanguineus ), and three extralimital species that occur in other geographical areas of North America ( A. americanum , D. andersoni , and D. variabilis ). Table 3 lists the single native tick species ( I. angustus ) recorded from domestic cats and the four tick species recorded from six species of native vertebrates representing three native species ( H. leporispalustris , I. angustus , and I. auritulus ) previously known from Alaska and one species, Ixodes texanus Banks, representing a new state record.

Table 1.

Ticks recorded from domestic dogs, Alaska, 2011–2016

Tick species (stages a )	No. dogs	Month(s)	Localities b	Recent dog travel history
Amblyomma americanum (1♀)	1	VIII	ER	No travel history
Dermacentor andersoni (1♂, 1♀)	2	I, VIII	A, S	1 visited CA; 1 visited OR
Dermacentor variabilis (7♂, 12♀)	19	IV, V, VI, VII, VIII	A, C, F, H, J, NP, S, V, W	13 visited CO, KS, LA, MA, MN, ND, NY, OR, PA, RI, or WA; owner of 1 visited NE; 5 with no travel history
Ixodes angustus (30♀, 3N)	33	IV, V, VI, VII, VIII, XI, XII	A/K, H, J, K, P, S, W	3 visited CA, MN, or WA; 30 with no travel history
Ixodes auritulus (1♀)	1	VI	S	Relocated from OR
Ixodes ricinus (2♀)	2	V, VI	F, J	1 imported from Austria, 1 imported from Germany
Ixodes scapularis (2♀)	2	V, VI	J, S	1 relocated from MN, 1 visited WI
Rhipicephalus sanguineus (4♂, 19♀)	19	I, III, IV, V, VI, VII, VIII, IX, XII	A, C, F, H, MI, NR, P, S, W	1 visited TX; 1 imported from Japan; 17 with no travel history.

^a N, nymphs.

^b A, Anchorage; A/K, Anchorage/Kenai; C, Chugiak; ER, Eagle River; F, Fairbanks; H, Homer; J, Juneau; K, Kodiak; MI, Mitkof Island; NP, North Pole; NR, Nome River; P, Palmer; S, Sitka; V, Valdez; W, Wasilla.

Table 2.

Ticks recorded from humans, Alaska, 2011–2016

Tick species (stages a )	No. humans	Month(s)	Localities b	Recent host travel history
Amblyomma americanum (2♂, 1N)	2	IV, V	F, G	1 traveled (TN)
Dermacentor andersoni (1♂)	1	V	A	Visited OR
Dermacentor variabilis (1♂, 4♀, 1N)	6	V, VI, VII	A, D, F, FW, NP, W	5 traveled (PA, RI, SD, TN, WI, WY); 1 with no travel history
Haemaphysalis leporispalustris (1N)	1	VII	H	None
Ixodes angustus (1♀, 1N)	2	VI, X	C, G	None
Rhipicephalus sanguineus (1♀)	1	IV	B	None

^a N, nymphs.

^b A, Anchorage; B, Bethel; C, Cordova; D, Denali National Park; F, Fairbanks; FW, Fort Wainwright; G, Gustavus; H, Haines; NP, North Pole; W, Willow.

Table 3.

Ticks recorded from other hosts and vegetation, Alaska, 2010–2016

Host species	Tick species (stages a )	No. hosts	Months	Localities b
Domestic cat ( Felus catus)	Ixodes angustus (13♀, 5N)	16	V, VI, VII, VIII, XI, XII	A, AP, BL, ER, H, J, K, P, PT
American Marten ( Martes americana )	Ixodes angustus (1♀)	1	III	K
American Marten ( Martes americana )	Ixodes texanus (2♀)	1	XII	CL
Ermine ( Mustela ermine )	Ixodes angustus (1♀)	1	III	MI
Snowshoe Hare ( Lepus americanus )	Haemaphysalis leporispalustris (3♀)	1	V	F
Snowshoe Hare ( Lepus americanus )	Ixodes angustus (1♀)	1	VI	A
“Squirrel”	Ixodes angustus (4♀)	2	VII	A, P
Southern Redback vole ( Myodes gapperi )	Ixodes angustus (7♂, 12♀, 3N, 7L)	2	V, VIII	A, W
Northwestern Crow ( Corvus caurinus )	Ixodes auritulus (1♀)	1	VI	S
On vegetation	Ixodes angustus (2♀)	NA	VI	MC
Crawling in vet. clinic	Amblyomma americanum (1♂)	NA	V	KO

None of the hosts listed had travel history outside of Alaska.

^a N, nymphs; L, larvae.

^b A, Anchorage; AP, Anchor Point; BL, Big Lake; CL, Connell Lake; D, Denali National Park; ER, Eagle River; F, Fairbanks; H, Homer; J, Juneau; K, Ketchikan; KO, Kotzebue; MC, Montana Creek; MI, Mitkof Island; P, Palmer; PT, Petersburg; S, Sitka; W, Wasilla.

Discussion

Keirans and Durden (2001) highlighted the ability of several species of ticks to invade and, in some cases, establish in the United States. Further, Ogden et al. (2013) documented changing geographical ranges of certain species of ticks and emphasized how this can influence the transmission of tick-borne pathogens, particularly for Borrelia burgdorferi Johnson, Schmid, Hyde, Steigerwalt and Brenner s.l., the causative agent of Lyme disease. Several of the records of nonindigenous ticks reported here for Alaska can apparently be attributed to recent out-of-state or out-of-country travel by dogs accompanying their owners, dogs being imported or translocated from other regions, or by human travel. Presumably, one or more ticks from the extralimital region attached to the host and remained attached when that host returned or was transported to Alaska. These scenarios likely describe most of the Alaska records we report for A. americanum , D. andersoni , I. ricinus , I. scapularis , and D. variabilis.

Nevertheless, five of 19 collections from dogs and one of five collections from humans of D. variabilis were not associated with host travel outside of Alaska ( Tables 1 and 2 ). James et al. (2015) documented the known and predictive geographical distribution of D. variabilis in the United States and did not report any records of this tick from Alaska. However, there are previous records of this tick outside of its established range in North America via attachment to translocated livestock and, especially, to domestic dogs ( Sonenshine 1979 , Dergousoff et al. 2013 ). Further, Dergousoff et al. (2013) documented recent range extensions of D. variabilis in the Canadian Prairies such that this tick and the congeneric D. andersoni now share a zone of sympatry at least 200 km wide. Yunik et al. (2015) reported that adult D. variabilis could survive for two consecutive winters in Manitoba, Canada, near their northern distributional limit, a trait that would also promote long-term off-host survival of this tick in Alaska. It seems likely that D. variabilis has been invading Alaska by attaching to dogs being brought into the state from other regions of North America where this tick is established. Vacationing humans taking pet dogs with them to regions with established D. variabilis populations and then returning to Alaska (with ticks attached to their dogs) may account for much of this tick translocation. We suspect that D. variabilis will continue to spread in Alaska mainly as an ectoparasite of domestic dogs, but native canids such as wolves, coyotes, and foxes are also at risk of parasitism by this tick and of contracting pathogens transmitted by it.

Although we cannot confirm the establishment in Alaska of other extralimital tick species, several species of medical–veterinary importance are obviously being brought into Alaska attached to returning travelers or their accompanying pets, notably domestic dogs. Future introductions of these ticks in this manner could result in the establishment of one of more of these species. We suggest that D. andersoni could become established in Alaska in this way because it shares some of the same hosts (including dogs) as D. variabilis ( James et al. 2006 ) and range extensions for this species have already been recorded in Canada near its known northern distributional limits ( Dergousoff et al. 2013 ).

Similarly, northern populations of both the eastern Nearctic species I. scapularis and of the Palaearctic species I. ricinus could feasibly tolerate the Alaskan climate and become established. Significant range expansion of I. scapularis in the United States in the past ∼20 yr has been documented ( Eisen et al. 2016a ), and continued range extensions of this tick in North America have been predicted ( Eisen et al. 2016b ). Rhipicephalus sanguineus is also evidently being brought into Alaska on imported or returning dogs ( Table 1 ), but this invasive species was already known to be established in the state ( Walker et al. 2000 ).

It is questionable whether or not the eastern Nearctic species A. americanum could survive the Alaskan winters since this tick belongs to a mainly tropical, subtropical, and warm temperate genus, members of which cannot apparently tolerate very cold winters ( Springer et al. 2014 ). Nevertheless, A. americanum has expanded its range in the northern Atlantic U.S. states in recent decades and has been recorded as far north as Maine ( Keirans and Lacombe 1998 , Springer et al. 2014 ). Also, Ludwig et al. (2016) modeled the effect of climate and climate-independent factors on the life cycle of A. americanum , with their simulations suggesting that parts of southern Canada are suitable for the survival and reproduction of this tick. Although two of the hosts for the A. americanum specimens—one collected from a dog ( Table 1 ) and one from a human ( Table 2 )—had no travel history outside of Alaska, one of the owners of the dog had recently traveled to Georgia, Pennsylvania, and Texas, and it is possible that this tick was inadvertently brought into Alaska on the owner or in his luggage. Similarly, the adult male A. americanum found crawling (on a counter) in a veterinary clinic in Kotzebue ( Table 3 ) could have been brought into Alaska on a pet that had recently traveled to, or been imported from, an eastern or central U.S. state.

In addition to the above-mentioned extralimital species, there is concern that the winter tick, Dermacentor albipictus Packard, a widespread ectoparasite of ungulates in North America ( Brinton et al. 1965 ), could be introduced into Alaska ( Zarnke et al. 1990 ). This is of particular concern in light of exacerbated climate change in far northern regions including the Arctic ( Kutz et al. 2009 ) and recent records of D. albipictus on elk ( Cervus elaphus L.), moose ( Alces alces (L.)), caribou ( Rangifer tarandus (L.)), and/or mule deer ( Odocoileus hemionus (Rafinesque)) in British Columbia ( Bridger 2015 ), Northwest Territories ( Kashivakura 2013 ), and the Yukon Territory (H. Schwantje, J. Harms and B. Elkin, Personal Communication, 2015). Invasion and establishment of D. albipctus in Alaska would have significant negative impacts on the health of native and introduced ungulates ( Zarnke et al. 1990 ). Ticks from ungulates were not received during this study, and it is recommended that future tick surveys in Alaska specifically include these hosts.

Our records of human parasitism by six species of ticks in Alaska compare with three species ( D. variabilis , I . angustus , and I. uriae ) recorded from humans in Alaska by Merten and Durden (1999) . Interestingly, the nonnative D. variabilis was recorded in both surveys, reinforcing the invasion potential for this tick. Similarly, the indigenous I. angustus was recorded from humans in both surveys, possibly reflecting the widespread distribution and low host specificity for this tick. The record of a nymph of H. leporispalustris from a human ( Table 2 ) is unusual, but the record of the avian-associated but indigenous I. uriae from a human by Merten and Durden (1999) also reflects a very atypical host association.

The three indigenous species of ticks we recorded in Alaska, H. leporispalustris , I. angustus , and I. auritulus , are of interest. Ixodes angustus was the most commonly collected tick during this study, and it parasitized seven host species including domestic dogs and cats, humans, American marten ( Martes americana (Turton)), ermine ( Mustela erminea L.), snowshoe hare ( Lepus americanus Erxleben), southern redback vole ( Myodes gapperi (Vigors)), and squirrels (either Glaucomys sabrinus (Shaw)—northern flying squirrel, or Tamiasciurus husonicus (Erxleben)—red squirrel; Tables 1–3 ). In a previous study, Murrell et al. (2003) recorded I. angustus as the only tick species parasitizing 12 species of native mammals (rodents and shrews) in southern Alaska. Similarly, Anstead et al. (2013) reported I. angustus to be the predominant tick parasitizing native small mammals in Kootenay National Park, British Columbia. In light of these reports, our records of I. angustus from native voles and squirrels in Alaska are not surprising. However, our records of I. angustus from a snowshoe hare, an American marten, and from several domestic cats were not anticipated. When comparing our data for ticks collected from dogs and cats, it is also somewhat surprising that I. angustus was the only tick species we recorded from cats. In other regions of North America, domestic cats can be parasitized by A. americanum , D. variabilis , I. scapularis , and other species of ticks ( Akucewich et al. 2002 ). Our records of the rabbit tick, H. leporispalustris , from a snowshoe hare were expected. Also, our record of the avian tick, I. auritulus , from a Northwestern crow ( Table 3 ) was not surprising whereas our record of this tick species from a dog ( Table 1 ) appears to be the first record of this morphologically distinct tick from a mammal. Lastly, our record of the carnivore-associated tick, Ixodes texanus , from an American marten represents the first record of this tick from Alaska. However, this tick is widely distributed across North America and has previously been recorded from the western states of California, Oregon, and Washington and the western Canadian Province of British Columbia ( Keirans and Clifford 1978 , Durden and Keirans 1996 ).

All of the tick species we recorded in this study have medical and veterinary importance beyond being nuisance biters. Amblyomma americanum is a vector of several pathogens in the southeastern, south-central and Atlantic United States including Ehrlichia chaffeensis Anderson, Dawson, Jones and Wilson (the causative agent of Human Monocytic Ehrlichiosis) and Ehrlichia ewingii Anderson, Greene, Jones and Dawson (the causative agent of a form of granulocytic ehrlichiosis in both dogs and humans) ( Childs and Paddock 2003 , Killmaster et al. 2014 ). More recently, A. americanum has been implicated in the transmission of Heartland and Bourbon viruses to humans ( Kosoy et al. 2015 ). Both D. andersoni and D. variabilis are vectors of Rickettsia rickettsii (Wolbach) (the causative agent of Rocky Mountain spotted fever) in their respective ranges ( James et al. 2006 , 2015 ) and some attached individual females of these species can also cause tick paralysis ( Durden and Mans 2016 ). Both D. andersoni and D. variailis can also transmit the causative agents of tularemia, Q fever, and bovine anaplasmosis ( James et al. 2006 , 2015 ). Dermacentor andersoni is also a vector of Colorado Tick Fever virus ( James et al. 2006 ). The indigenous Haemaphysalis leporispalustris is an enzootic vector of the causative agents of tularemia, Q fever, and Rocky Mountain spotted fever ( Strickland et al. 1976 ) whereas I. angustus is a vector of a nonzoonotic strain of Babesia microti (Franca) to voles across North America, including Alaska ( Goethert et al. 2006 ). Scott et al. (2010) characterized three novel strains of Borrelia burgdorderi sensu lato from I. auritulus in far western Canada and suggested that this tick may be involved in an avian enzootic transmission cycle of Lyme disease spirochetes that could overlap with mammal transmission cycles through bridge vectors. Both I. ricinus and I. scapularis are the most important vectors of B. burgdorferi in their respective ranges and are also vectors of several additional zoonotic agents ( Hamer et al. 2007 , Coipan et al. 2013 ). The carnivore-associated tick, I. texanus , has also been recorded as an ectoparasite of dogs ( Durden and Keirans 1996 ) and (rarely) humans ( Merten and Durden 1999 ) and has been implicated as a likely vector of Babesia lotori Anderson, Magnarelli and Sulzer to raccoons ( Durden and Keirans 1996 ). In North America, R. sanguineus mainly parasitizes dogs and is an important vector of both Babesia canis (Piana and Galli Valerio) (a causative agent of canine babesiosis) and Ehrlichia canis (Donatien and Lestoquard) (a causative agent of canine ehrlichiosis; Walker et al. 2000 ). However, R , sanguineus will also parasitize humans ( Merten and Durden 1999 ), and this tick has recently been implicated as a novel vector of R. rickettsii to humans in northern Mexico and the southwestern United States ( Demma et al. 2005 , Eremeeva et al. 2011 ).

Collectively, the tick species we record here from Alaska have considerable medical–veterinary importance and are known to transmit a formidable variety of pathogens to humans, pets, and native wildlife. Ticks should be collected from vertebrates, including humans and pets, in Alaska on an ongoing basis in order to determine whether any tick species are invading or establishing within the state and to monitor the potential introduction of any tick-borne diseases associated with these ticks.

Acknowledgments

Thanks to Derek Sikes of University of Alaska Museum of the North for accessioning tick specimens from this study and to the many veterinarians, biologists, and members of the public who submitted specimens especially Phillip Mooney, Jeff Selinger, Richard Lowell, Kristian Larson, Tom Lohuis, Mike Taras, and Holley Dennison.