Communication First Report of scapularis Parasitizing a North American Porcupine in Canada

John D. Scott

Department of Medicine and Epidemiology, School of Veterinary Medicine, University of California, Davis, CA 95616, USA; [email protected]

Abstract: Adult females of the blacklegged , Ixodes scapularis (: ), were collected from a North American porcupine, Erethizon dorsatum, in eastern Ontario, Canada. This porcupine indicates that an established population of I. scapularis is present in the local vicinity. This tick species is known to parasitize more than 150 different vertebrate hosts, including the North American porcupine. The presence of I. scapularis ticks parasitizing a North American porcupine constitutes a new tick-host record in Canada.

Keywords: tick-host record; north American porcupine; Erethizon dorsatum; ectoparasite; herbivore; blacklegged ticks; Ixodes scapularis; parasitism; Canada

1. Introduction The North American porcupine, Erethizon dorsatum (Rodentia: Erethizontidae), also   known as the Canadian porcupine, is a herbivore rodent. This meso-mammal is one of the largest members in the rodent family, and has wide distribution across continental Citation: Scott, J.D. First Report of North America. This woodland denizen is native to coniferous and mixed forests across Ixodes scapularis Ticks Parasitizing a southern Canada, and its distribution extends southward into northeastern, north-central, North American Porcupine in and western United States as far south as the northern fringe of Mexico. Ecologically, Canada. Parasitologia 2021, 1, 45–49. free-ranging porcupines have a home range of up to 28 ha. This arboreal herbivore is https://doi.org/10.3390/ covered with a coat of quills that arm it from predators. Once a porcupine is threatened, parasitologia1020006 it will hide its face, swat its tail at its assailant, and thrust an arsenal of quills in multiple directions to strike its attacker. The sharp, needle-like quills are painful, and prudent Academic Editor: Theo De Waal attackers retreat. In the spring and summer, porcupines feed on berries, seeds, grasses, leaves, roots, and stems. In the winter, North American porcupines feed on the inner Received: 16 February 2021 bark of trees. As these herbivore rodents forage for food, they make direct contact with Accepted: 25 March 2021 Published: 1 April 2021 low-lying vegetation where ticks are questing. Blacklegged ticks, Ixodes scapularis (Acari: Ixodidae), are indigenous across North

Publisher’s Note: MDPI stays neutral America east of the Rocky Mountains [1]. Ixodidae, commonly referred to as hard ticks, with regard to jurisdictional claims in are predominantly blood-feeding ectoparasites of mammals and birds although several published maps and institutional affil- species feed on reptiles [1]. Tiny ticks maintain a stealth presence in the natural environ- iations. ment, and covertly parasitize North American porcupines. These quill-laden rodents are primarily nocturnal, but will defend themselves at any time of day. In Wisconsin, wildlife rehabilitators collected I. scapularis adults from several North American porcupines [2]. The locality where the free-ranging porcupine was found is in the Great Lakes-St. Lawrence forest region which consists primarily of red pine, eastern white pine, eastern Copyright: © 2021 by the author. Licensee MDPI, Basel, Switzerland. hemlock, yellow birch, sugar maple, and red oak [3]. In a tick-host study conducted across This article is an open access article Ontario with veterinarians, wildlife rehabilitators, and the public, acarologists previously distributed under the terms and detected I. scapularis ticks on domestic dogs, cats, and humans in the same precambrian conditions of the Creative Commons area (Canadian Shield) [4]. Although porcupines have feeding activities in trees, these Attribution (CC BY) license (https:// spiny rodents will have direct contact with low-lying vegetation when they are feeding at creativecommons.org/licenses/by/ ground level. If present, this is where I. scapularis ticks are questing. Depending on the time 4.0/). of year and their developmental life stage, I. scapularis ticks conduct host-seeking activities

Parasitologia 2021, 1, 45–49. https://doi.org/10.3390/parasitologia1020006 https://www.mdpi.com/journal/parasitologia Parasitologia 2021, 1, FOR PEER REVIEW 2

ground level. If present, this is where I. scapularis ticks are questing. Depending on the time of year and their developmental life stage, I. scapularis ticks conduct host-seeking Parasitologia 2021, 1 activities anytime through the day. Several blacklegged ticks collected within a single46 col- lection period (a single year) indicate that a reproducing population of I. scapularis is pre- sent [5,6]. anytime through the day. Several blacklegged ticks collected within a single collection 2. Resultsperiod (a single year) indicate that a reproducing population of I. scapularis is present [5,6]. The North American porcupine was found on the side of the road north of Westport, 2. Results Ontario on County Road 10 (44.687° N, 76.385° W), which is situated within the Canadian The North American porcupine was found on the side of the road north of Westport, Shield (Figure 1). The injured porcupine was taken to Sandy Pines Wildlife Centre, Ontario on County Road 10 (44.687◦ N, 76.385◦ W), which is situated within the Canadian NapShieldanee, (Figure Ontario,1). The and injured a wildlife porcupine rehabilitator was taken to examined Sandy Pines it. Wildlife Since theCentre, head Napanee, had visible trauma,Ontario, it is and believed a wildlife that rehabilitator the porcupine examined was it.struck Since by the a head passing had visible vehicle. trauma, Based it on is a x- ray,believed veterinary that the technicians porcupine was also struck found by a a diaphramaticpassing vehicle. hernia. Based on Due a x-ray, to the veterinary severity of trauma,technicians the North also found American a diaphramatic porcupine hernia. was promptly Due to the euthanized severity of trauma,upon arrival, the North and five partiallyAmerican engorged porcupine I. scapularis was promptly females euthanized were collected. upon arrival, and five partially engorged I. scapularis females were collected.

Figure 1. Map showing geographic location where Northern American porcupine was found parasitized with I. scapularis females. Figure 1. Map showing geographic location where Northern American porcupine was found parasitized with I. scapularis females. 3. Discussion The collection of five engorged I. scapularis females feeding on a North American 3. Discussionporcupine is a novel discovery in Canada (Figure2). Based on a literature search [ 2,7–9] and the Canadian National Collection, the author affirms that this mammalian parasitism is The collection of five engorged I. scapularis females feeding on a North American the first documentation of I. scapularis parasitizing a North American porcupine in Canada. porcupineThe is blacklegged a novel discovery tick parasitizes in Canada a wide (Figure diversity 2). of Based vertebrates on a (avian,literature mammalian, search [2,7–9] andreptilian), the Canadian which National include moreCollection, than 150 the vertebrate author affirms species that [1,10 this]. Thismammalian tick species parasitism is is theknown first todocumentation harbour a broad of I. diversity scapularis of parasitizing tick-borne pathogens, a North American including nineporcupine different in Can- ada.pathogens/pathogen groups [10,11]. Previously, the author barcoded an I. scapularis collected from a raptor (American Kestrel) for confirmation by molecular identification of this tick species [12]. Since the larval and nymphal stages of blacklegged ticks are transported by migratory songbirds, these tick-borne, zoonotic pathogens are widely dispersed in the temperate zone of North America, especially during northward, spring migration [9,13–23]. When a songbird is heavily infested with I. scapularis larvae and nymphs, passerine birds can start a new population of ticks [24–26]. Nymphal I. scapularis Parasitologia 2021, 1 47

Parasitologia 2021, 1, FOR PEER REVIEW ticks have been reported on songbirds as far north as Newfoundland and Labrador3 [19], north-central Saskatchewan [17], and northwestern Alberta [13,19]. With the exception of Newfoundland and Labrador, North American porcupines inhabit these forested areas.

Figure 2.FigureBlacklegged 2. Blacklegged tick, Ixodes tick, scapularis Ixodes scapularis:(a) male,: ( (ab)) male, unfed ( female,b) unfed and female, (c) fully and engorged (c) fully female;engorged 9.7 fe- mm, full body length.male; 9.7 mm, full body length. The ratio of males and females in ixodid ticks is generally 1:1 (Figure1). Even though The blackleggedmales maytick parasitizes have been present a wide on diversity the host porcupine,of vertebrates they (avian, were not mammalian, observed. Males are reptilian), whichblack include (Figure more2), and than inconspicuous 150 vertebrate with thespecies naked [1,10]. eye, and This frequently tick species undetected is on known to harbourdark-coloured, a broad diversity furry or spiny of tick .-borne If pathogens, a male was including present, it couldnine dif mateferent with one or pathogens/pathogenmore females.groups [10,11]. Alternatively, Previously, mating the can author occur on barcoded vegetation an before I. scapularis the female col- acquires lected from a raptora host. (American The presence Kestrel) of five for attached confirmation females on by the molecular porcupine identification illustrates that of the North this tick speciesAmerican [12]. Since porcupine the larval is aand mating nymphal venue forstagesI. scapularis of blackleggedmales and ticks females. are trans- ported by migratoryThe songbirds, five I. scapularis these tickfemales-borne, on zoonotic a single North pathogens American are widely porcupine dispersed indicate that an established population of I. scapularis is present in the home range of the host [5,6]. When in the temperate zone of North America, especially during northward, spring migration the females have taken complete blood meals, and have mated with males, the gravid [13–23]. When afemales songbird will is lay heavily eggs in infested the spring, with and I. start scapularis a new generationlarvae and of nymphs,I. scapularis passer-ticks [11]. As a ine birds can starthost a new of I. scapularis populationadults, of ticks a porcupine [24–26]. can Nymphal be involved I. scapularis in the reproduction ticks have and been propagation reported on songbirdsof this tick as species,far north especially as Newfoundland if the male and and female Labrador have [19], mated north on this-central host, and the Saskatchewan [17],female and engorges, northwestern and obtains Alberta a complete [13,19]. blood With meal the from exception the porcupine. of Newfound- Additionally, the land and Labrador,porcupine North parasitism American indicates porcupines that aninhabit established these populationforested areas. of I. scapularis is present in The ratio ofthis males locality and [females5,6]. in ixodid ticks is generally 1:1 (Figure 1). Even though males may have beenIn present summary, on the the author host porcupine, endorses a newthey tick-host were not association observed. for Males blacklegged are ticks in Canada. This rodent parasitism provides the first published report of I. scapularis black (Figure 2), and inconspicuous with the naked eye, and frequently undetected on parasitizing a North American porcupine in Canada. dark-coloured, furry or spiny animals. If a male was present, it could mate with one or more females. Alternatively,4. Materials and mating Methods can occur on vegetation before the female acquires a host. The presence ofFive fiveI. scapularisattachedfemales females were on collectedthe porcupine from an illustrates injured North that American the North porcupine American porcupineby wildlife is a mating rehabilitators venue on for 17 I. October scapularis 2020 males using and super-fine, females. stainless steel forceps. They The five I. scapulariswere then placedfemales in on a 2 a mL single micro North tube containingAmerican 94%porcupine ethyl alcohol. indicate The that engorged an ticks established populationwere sent of toI. scapularis an acarology is present identification in the home lab (J.D.S.) range located of the inhost Fergus, [5,6]. Ontario.When Ticks the females havewere taken morphologically complete blood identified meals, using and a have stereoscopic mated microscopewith males, (Olympus the gravid SZX16) and females will lay taxonomiceggs in the keys spring, and scanningand start electron a new microscopegeneration photosof I. scapularis [1,27]. ticks [11]. As a host of I. scapularisFunding: adults,This researcha porcupine received can no externalbe involved funding. in the reproduction and propa- gation of this tick species, especially if the male and female have mated on this host, and Institutional Review Board Statement: Not applicable. An care permit is not required to the female engorges, and obtains a complete blood meal from the porcupine. Addition- remove a tick from a host. In this case, the ticks were removed after the porcupine was euthanized. ally, the porcupine parasitism indicates that an established population of I. scapularis is present in this localityInformed [5,6]. Consent Statement: Not applicable. In summary,Data the Availability author endorses Statement: a newThe wildlife tick-host supervisor association provided for the blacklegged basic background ticks information,in Canada. This rodentand the parasitism names of participants provides were the notfirst released. published report of I. scapularis parasi- tizing a North American porcupine in Canada.

4. Materials and Methods Five I. scapularis females were collected from an injured North American porcupine by wildlife rehabilitators on 17 October 2020 using super-fine, stainless steel forceps. They were then placed in a 2 mL micro tube containing 94% ethyl alcohol. The engorged ticks were sent to an acarology identification lab (J.D.S.) located in Fergus, Ontario. Ticks were morphologically identified using a stereoscopic microscope (Olympus SZX16) and taxo- nomic keys and scanning electron microscope photos [1,27]. Parasitologia 2021, 1 48

Acknowledgments: The author thanks the staff of Sandy Pines Wildlife Centre for collecting ticks and providing background information on the porcupine. The author is indebted to Amanda Green for computer graphics and grateful to Susan Finkle for facilitative support. Conflicts of Interest: The author declares no conflict of interest.

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