Modeling Potential Habitat for Amblyomma Tick Species in California
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insects Article Modeling Potential Habitat for Amblyomma Tick Species in California Emily L. Pascoe 1,*, Matteo Marcantonio 2 , Cyril Caminade 3,4 and Janet E. Foley 1 1 Department of Medicine and Epidemiology, School of Veterinary Medicine, University of California, Davis, CA 95616, USA 2 Department of Pathology, Microbiology, and Immunology, School of Veterinary Medicine, University of California, Davis, CA 95616, USA 3 Department of Epidemiology and Population Health, Institute of Infection and Global Health, University of Liverpool, Liverpool CH64 7TE, UK 4 Health Protection Research Unit in Emerging and Zoonotic Infections, University of Liverpool, Liverpool L69 3GL, UK * Correspondence: [email protected] Received: 20 April 2019; Accepted: 2 July 2019; Published: 8 July 2019 Abstract: The Amblyomma genus of ticks comprises species that are aggressive human biters and vectors of pathogens. Numerous species in the genus are undergoing rapid range expansion. Amblyomma ticks have occasionally been introduced into California, but as yet, no established populations have been reported in the state. Because California has high ecological diversity and is a transport hub for potentially parasitized humans and animals, the risk of future Amblyomma establishment may be high. We used ecological niche modeling to predict areas in California suitable for four tick species that pose high risk to humans: Amblyomma americanum, Amblyomma maculatum, Amblyomma cajennense and Amblyomma mixtum. We collected presence data in the Americas for each species from the published literature and online databases. Twenty-three climatic and ecological variables were used in a MaxEnt algorithm to predict the distribution of each species. The minimum temperature of the coldest month was an important predictor for all four species due to high mortality of Amblyomma at low temperatures. Areas in California appear to be ecologically suitable for A. americanum, A. maculatum, and A. cajennense, but not A. mixtum. These findings could inform targeted surveillance prior to an invasion event, to allow mitigation actions to be quickly implemented. Keywords: Amblyomma; invasive species; MaxEnt; species distribution modeling; ticks 1. Introduction The Amblyomma genus of ticks comprises typically aggressive and generalist species of considerable human and veterinary medical importance [1]. In addition to injury and potential secondary infections associated with insertion of the long mouth parts of Amblyomma ticks [2,3], some species can transmit pathogens to humans and other animals [1]. In the USA, the lone star tick (Amblyomma americanum) often feeds on humans and can transmit Ehrlichia chaffeensis (causative agent of human monocytic ehrlichiosis), Ehrlichia ewingii (agent of human granulocytic ehrlichiosis), Coxiella burnetii (agent of Q fever), and Francisella tularensis (agent of tularemia) [4–8]. Though not apparently a vector of Borrelia burgdorferi sensu stricto (agent of Lyme disease) [9,10], A. americanum can transmit the southern tick-associated rash illness (STARI) pathogen, causing a disease clinically similar to Lyme borreliosis [11]. The Gulf Coast tick, Amblyomma maculatum, is an important vector of Rickettsia parkeri to humans [12,13] and Hepatozoon americanum, a pathogenic protozoan of dogs and wild canids [14]. The Gulf Coast tick can also transmit Ehrlichia ruminantium (agent of heartwater), which, although Insects 2019, 10, 201; doi:10.3390/insects10070201 www.mdpi.com/journal/insects Insects 2019, 10, x 2 of 20 Insects 2019, 10, 201 2 of 19 and wild canids [14]. The Gulf Coast tick can also transmit Ehrlichia ruminantium (agent of heartwater), which, although not currently present in the USA, could lead to high rates of livestock notmortality currently if introduced present in the[15,16]. USA, Ticks could in lead the to Amblyomma high rates ofcajennense livestock species mortality complex, if introduced including [15,16 A.]. Tickscajennense in the sensuAmblyomma stricto (further cajennense referencedspecies as complex, A. cajennense including) and A.Amblyomma cajennense mixtumsensu, strictoare considered (further referencedthe most important as A. cajennense vectors) of and RickettsiaAmblyomma rickettsii mixtum (agent, are of consideredRocky Mountain the most spotted important fever) vectorsin Central of Rickettsiaand South rickettsii America(agent [17]. of Rocky Mountain spotted fever) in Central and South America [17]. GeographicGeographic rangesranges ofof AmblyommaAmblyomma speciesspecies areare rapidlyrapidly expandingexpanding duedue toto changeschanges inin climateclimate andand land-use,land-use, andand increasedincreased movementsmovements andand rangesranges ofof humanhuman andand animalanimal hostshosts [[18].18]. BothBoth A.A. americanumamericanum andand A.A. maculatummaculatum areare nativenative toto southeasternsoutheastern coastalcoastal USA,USA, butbut areare consideredconsidered invasiveinvasive duedue toto theirtheir rapidlyrapidly expandingexpanding westwardwestward andand northwardnorthward distributions,distributions, particularlyparticularly A.A. americanumamericanum whichwhich nownow hashas establishedestablished populationspopulations extendingextending inlandinland intointo midwesternmidwestern statesstates [[19,20]19,20] (Figure(Figure1 ).1). AmblyommaAmblyomma cajennensecajennense isis currentlycurrently onlyonly presentpresent inin thethe southernmostsouthernmost statesstates ofof thethe USA,USA, andand itsits rangerange extendsextends southsouth toto northernnorthern ArgentinaArgentina andand easteast toto thethe Caribbean,Caribbean, makingmaking itit oneone ofof thethe mostmost widelywidely distributeddistributed ticksticks inin thethe NewNew World [[21].21]. The The native native range range of of A.A. mixtum mixtum extendsextends from from Mexico Mexico and and Central Central America America to towestern western Ecuador Ecuador [22] [22 and] and includes includes the the West West Indies Indies [23]; [23]; this this tick tick is is now now invasive invasive in in Texas Texas [24]. [24]. However,However, despitedespite multiple multiple introductions introductions of A.of americanumA. americanuminto Californiainto California (usually (usually on imported on imported cattle), therecattle), are there currently are currently no known no establishedknown established populations populations of Amblyomma of Amblyommaspp. ticks spp. in ticks the state in the [25 state,26]. Nevertheless,[25,26]. Nevertheless, California California may be at riskmay of be invasion at risk due of toinvasion high ecological due to high diversity ecological that already diversity supports that manyalready other supports ticks andmany suitable other ticks host and species suitable [27– 30host]. Inspecies addition, [27–30]. California In addition, is a hub California for vast is global a hub movementsfor vast global of people,movements animals, of people, and goods, animals, imposing and goods, a high imposing likelihood a ofhigh introduction likelihood ofof non-endemicintroduction ticks.of non-endemic For example, ticks. in 2017 For example, approximately in 2017 675,000 approximately cattle were 675,000 imported cattle into were the stateimported [31]. Whileinto the eff stateorts are[31]. made While to preventefforts are concurrent made to importation prevent concurrent of ticks, with importation such large-scale of ticks, movements with such of large-scale livestock, asmovements well as people of livestock, and domestic as well pets as whichpeople do and not domestic undergo pets quarantine, which do introduction not undergo of Amblyommaquarantine, speciesintroduction into California of Amblyomma poses species a real threat. into California poses a real threat. Figure 1. The current USA distributions of Amblyomma americanum (the lone star tick) and A. maculatum Figure 1. The current USA distributions of Amblyomma americanum (the lone star tick) and A. (the Gulf Coast tick) based on the generation of a convex polygon around geolocations for each species maculatum (the Gulf Coast tick) based on the generation of a convex polygon around geolocations for from the scientific literature and online databases collected for MaxEnt modeling (see Supplementary each species from the scientific literature and online databases collected for MaxEnt modeling (see Materials for full list of geolocations). Supplementary Materials for full list of geolocations). Targeted surveillance may be one of the most effective ways of preempting tick invasion. SurveillanceTargeted can surveillance be informed may by be species one of distribution the most modelingeffective ways (SDM), of apreempting method that tick predicts invasion. the possibleSurveillance range can of abe species informed based by on species ecological distribu variablestion thatmodeling sustain (SDM), species a survival. method Similarthat predicts modeling the methodspossible haverange successfully of a species preempted based on tick ecological establishment variables in novel that ranges, sustain for examplespecies thesurvival. establishment Similar ofmodelingIxodes scapularis methodsin have Canada successfully [32,33], andpreempted the retrospective tick establishment range expansion in novel of ranges,I. scapularis for exampleacross thethe easternestablishment USA [34 of]. TheIxodes potential scapularis distribution in Canada of A. [32,33], americanum and inthe the re USAtrospective has been range predicted expansion using SDMof I. methodsscapularis [ 35across–38], butthe typicallyeastern