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Journal of Medical Entomology logoLink to Journal of Medical Entomology
. 2022 Jul 1;59(5):1646–1659. doi: 10.1093/jme/tjac082

Northward Expansion of Amblyomma americanum (Acari: Ixodidae) into Southwestern Michigan

Peter D Fowler 1,✉, S Nguyentran 2, L Quatroche 3, M L Porter 4, V Kobbekaduwa 5, S Tippin 6, Guy Miller 7, E Dinh 8, E Foster 9,✉, J I Tsao 10,11
Editor: Holly Gaff
PMCID: PMC9989843  PMID: 35776508

Abstract

Amblyomma americanum (Linnaeus) (Acari: Ixodidae) (lone star tick) is an aggressive, generalist parasite that vectors numerous important human and animal pathogens. In recent decades its geographic range has expanded northwards from endemic regions in the southeastern and southcentral United States. In 2019 five questing A. americanum ticks, comprising two life stages were detected at one site in southwestern Michigan, satisfying one CDC criterium for an established population for the first time in recent history in the state. To better characterize the extent of emerging A. americanum, we conducted active surveillance (i.e., drag sampling) in summer 2020 throughout Michigan’s southern counties and detected one adult A. americanum from each of six widespread sites, including where they had been detected in 2019. A larger established population was identified at another site in Berrien County, which yielded 691 A. americanum comprising three life stages, and questing phenologies here were similar to that reported for other endemic regions. Statewide surveillance in 2021 revealed no A. americanum outside of Berrien County, but establishment criteria were met again at the two sites where established populations were first detected respectively in 2019 and 2020. These observations may represent the successful invasion of A. americanum into Michigan. Data from passive (1999–2020) and active surveillance (2004–2021) efforts, including a domestic animal sentinel program (2015–2018), are reported to provide context for this nascent invasion. Continued active surveillance is needed to help inform the public, medical professionals, and public health officials of the health risks associated with this vector.

Keywords: Amblyomma americanum, distribution, Michigan, surveillance

Amblyomma americanum (Linnaeus) (Acari: Ixodidae), also known as the lone star or turkey tick, is a medically important generalist parasite known for its aggressive behavior (Stafford et al. 2018, Molaei et al. 2019). Heavy infestations on wildlife have been reported to cause morbidity and mortality (Bolte et al. 1970, Stafford et al. 2018). A. americanum is also known to vector a number of pathogens responsible for disease in both humans and domestic animals (Jaworski et al. 2017, Madison-Antenucci et al. 2020, Kennedy and Marshall 2021). Bites from this tick have also been linked with the recently discovered alpha-gal syndrome (AS), otherwise known as the tick-associated red meat allergy (Cabezas-Cruz et al. 2019, Crispell et al. 2019, de la Fuente et al. 2020, Sharma and Karim 2021), which, if serious, can result in anaphylaxis (Pattanaik et al. 2018).

A recent publication based on historical reports of A. americanum suggests that this tick was established in Michigan, New York, and New England in the late 18th and early 19th century (Rochlin et al. 2022), but that subsequent clear cutting of forests as well as overexploitation of wildlife may have led to its extirpation. Reforestation and other wildlife management practices beginning in the early 20th century resulted in the growth and spread of its main host, the white-tailed deer, Odocoileus virginianus [Zimmerman] (artiodactyla: Cervidae), and possibly the wild turkey, Meleagris gallopavo [Linnaeus] (galliformes: Phasianidae) (Paddock and Yabsley 2007). Increased woodlands also created more habitat for A. americanum itself by providing leaf litter suitable to protect the tick from desiccation (Paddock and Yabsley 2007, Tsao et al. 2021). These factors have been hypothesized to facilitate the northern expansion of A. americanum from endemic areas in the south central and southeastern United States since the mid-1900s (Paddock and Yabsley 2007, Springer et al. 2014, Sonenshine 2018, Molaei et al. 2019). Additionally, the trend of warmer and shorter winters beginning in the late 20th century associated with anthropogenic climate change may be providing additional opportunities for this tick to become established in areas farther north (Sonenshine 2018). Models suggest that the northward invasion of A. americanum is likely to continue in the coming decades (Springer et al. 2015, Raghavan et al. 2019, Sagurova et al. 2019). Detecting, further characterizing, and refining predictions about the northward expansion can help prepare the public and medical professionals for the emergence of diseases associated with this vector.

Recently, breeding populations of A. americanum have been documented in southern New England (Stafford et al. 2018, Telford et al. 2019) and in states surrounding the Great Lakes, established populations of which have been spreading northwards in Illinois (Gilliam et al. 2020, Lyons et al. 2021), Indiana (Wojan et al. 2021), and Ohio (Fitak et al. 2014). Although there have been increases in A. americanum detected by the public in Wisconsin (Christenson et al. 2017) and southern Ontario (Nelder et al. 2019), established populations have not yet been declared in those areas (at the time of manuscript submission). As of July 2019, the Minnesota Department of Public Health has not reported any established populations of A. americanum although these ticks have been reported by residents since 1998 (Minnesota Department of Health 2019) and established populations have been identified in nearby counties to the west in South Dakota (Black et al. 2021) and to the south in Iowa (Springer et al. 2014).

Although A. americanum in Michigan have been documented by passive surveillance since the mid-1980s (Walker et al. 1998, MDHHS 2021a) there is a lack of evidence supporting the existence of any established breeding populations (Walker et al. 1998). Here we present such data for one county in Michigan. To better understand the context of this invasion, we also summarize detections of A. americanum reported in historical passive and active surveillance efforts dating back to 2004 designed to detect Ixodes scapularis (Say) because there is a high degree of overlap between A. americanum and I. scapularis in habitat use and temporal activity (Lindsay et al. 1998, Kollars et al. 2000, Guerra et al. 2002, Allan 2009, CDC 2020). We further include data from active surveillance also focused on detecting I. scapularis carried out by the Berrien County Health Department (BCHD) from 2019 to 2021.

Methods

Passive Surveillance

Records of resident-submitted ticks to the Michigan Department of Agriculture began in 1999. In 2015 the Michigan Department of Health and Human Services (MDHHS) took over the program, which continues to the present. Data were retrieved from the public database on the MDHHS Michigan Environmental Public Health Tracking website (MDHHS 2021a). Ticks are reported by the submitter’s most likely county of exposure or county of residence when the county of exposure is uncertain. Submitted ticks were identified to species using dichotomous morphological keys (Brinton et al. 1965, Sonenshine 1979, Keirans and Litwak 1989, Durden and Keirans 1996, Faulkner and Reinhard 2014, Dubie et al. 2017, Egizi et al. 2019). Although the program was in operation in 2014, data from this year were not available for this analysis.

Active Surveillance by Drag Sampling

Site Selection

From 2004 to 2016, much of the sampling by Michigan State University (MSU) was conducted to track the invasion of I. scapularis mainly in Michigan’s western lower peninsula (Hamer et al. 2010), but this was expanded to southeastern Michigan beginning in 2015. In 2010, to better define the range of I. scapularis, surveillance was broadened to cover 21 counties across Michigan’s lower peninsula. Beginning in 2017, surveillance became more widespread across the state to sample counties that previously had been sampled less frequently or not at all. In 2019 BCHD began conducting surveillance for questing I. scapularis. Although the specific monitoring objectives varied from year to year, site selection and sampling protocols were similar between MSU and BCHD. Public land (e.g., city, county and state parks, state forests, state wildlife game areas, and national forests) with suitable habitat for I. scapularis were selected. Much like I. scapularis, A. americanum is frequently found in deciduous forests containing leaf litter that helps protect ticks from desiccation (Hair and Howell 1970, Childs and Paddock 2003, Allan 2009, Kensinger and Allan 2011). In 2020, the number of sites per county sampled by MSU was increased relative to that in prior years to increase the likelihood of detecting A. americanum in southern Michigan: 55 primary sites were selected after consulting local public health departments, local parks departments, and other regional authorities to identify sites with suitable habitat and public access. Sites with insufficient area to sample (less than 1,000 m2) or unsuitable habitat (little to no deciduous forest, or lack of a managed trail) upon first visits were not repeated.

Surveillance Methods and Sampling Frequency

Active surveillance by drag sampling (Falco and Fish 1992) aimed at detecting the spread of I. scapularis has been ongoing in Michigan since 2002 (Foster 2004). Based on CDC guidelines for the active surveillance of questing prostriate (CDC 2019) and metastriate ticks (CDC 2020), a minimum of 1,000 m2 were sampled per visit per site by dragging a 1-m2 white corduroy cloth (fleece in 2010) along trail edges in contact with understory and leaf litter where ticks were likely questing. In larger parks, two transects with a minimum of 800 m2 each were sampled in different areas of the park. Sampling was performed on rain-free days throughout the day unless relative humidity dropped below 40%. Collected ticks were placed in 70–90% ethanol and brought back to the lab for species identification using dichotomous morphological keys (Brinton et al. 1965, Sonenshine 1979, Keirans and Litwak 1989, Durden and Keirans 1996, Faulkner and Reinhard 2014, Dubie et al. 2017, Egizi et al. 2019).

In 2004–2019 and 2021, because the main objective of our surveillance was to document the distribution of I. scapularis and Lyme disease risk, the bulk of the sampling effort generally occurred from May to July to target the nymphal stage of this tick. This time frame also encompasses part of the adult and much of the nymphal host-seeking period of A. americanum, according to reported phenologies in other states (Sonenshine 1979, Schulze et al. 1986, Kollars et al. 2000, Telford et al. 2019). Sites were sampled at least once during these years. In 2020, COVID-19 restrictions delayed sampling efforts by MSU, but sites with appropriate habitat and area were sampled a minimum of three times from 8 June to 23 July 2020. Sites where A. americanum was detected during the first three visits were sampled an additional time (i.e., four times total) to attempt to detect multiple life stages or multiple specimens. Figures were generated in ArcGIS Pro v. 2.8.3 and compiled in Adobe Illustrator v. 24.1.2.

Active Surveillance by Sampling Companion Canines

From 2015 to 2018 veterinary clinics and/or shelters throughout Michigan were recruited to survey companion canines for ticks during routine health checks. Veterinary workers were asked to inspect thoroughly a minimum of 60 patients (3 per day) over a period of at least 30 days when adult I. scapularis ticks would be active in Michigan, targeting April–June. A. americanum frequently parasitizes companion canines (Sonenshine 1979, Saleh et al. 2019) and this timeframe overlaps the activity period of adult A. americanum as well as part of that of the nymphal activity period. Only canines who had not traveled more than 30 miles from their residence during the 10 d prior to their health visit were included in the study. Clinics were instructed to report data on all canines inspected, including those who did not present with ticks. All ticks were stored in 70% ethanol and submitted to MSU for identification as described above. The activities herein are considered standard veterinary care and involve samples collected using noninvasive techniques; an approved exemption (20 May 2015) from filing an animal use form is on file with the MSU Institutional Animal Care and Use Committee.

Characterization of the Phenology of A. americanum

Because both adults and nymphs were detected at one site, Grand Mere State Park (GMSP), early in the surveillance period in 2020, weekly sampling beyond the surveillance window was performed at the site to detect larvae as well as to describe the host-seeking phenology of A. americanum. Sampling in the fall ceased after two consecutive visits failed to yield any A. americanum. Host-seeking phenologies for each tick life stage were characterized by determining the density of ticks per site visit in ticks per m2 and displaying the percentage of the total tick density for the season for each respective visit.

Results

Passive Surveillance

Fig. 1 shows the numbers of ticks submitted by county to the Michigan Department of Agriculture and Rural Development from 1999 to 2013 and MDHHS from 2015 to 2020 excluding 2014 for which data were not available. Fig. 2 shows the total number of ticks submitted from 2009 to 2020; A. americanum submissions accounted for 1.8% (0.6–3.0% range) of all ticks submitted each year. Submissions varied spatially and from year to year with no apparent trends given the spatial distribution of Michigan residents.

Fig. 1.

Fig. 1.

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Numbers of Dermacentor variabilis, Ixodes scapularis, Amblyomma americanum, and other species submitted annually to the Michigan Department of Agriculture (1999–2013) and Michigan Department of Health and Human Services (2015–2020). On average, 3.2% ± 1.7% SD of all ticks submitted annually were A. americanum. Data source: MiTracking- Michigan Environmental Public Health Tracking; no data are available for 2014.

Fig. 2.

Fig. 2.

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Amblyomma americanum submitted annually to the Michigan Department of Agriculture (2009–2013) and the Michigan Department of Health and Human Services (MDHHS) from 2015 to 2020. Data source: MiTracking- Michigan Environmental Public Health Tracking. Numbers in each county represent the number of community- submitted A. americanum by county of residence. No data were available for 2014. *Human population heatmap for each county is given for reference based on 2020 census date (collated by Esri 2021) with lighter being lower population (less than 182,000) and darker being higher population (over 1.5 million).

Active Surveillance

Drag Sampling (2004–2021)

Between 2004 and 2016, 628,140 m2 were sampled from 35 counties located in the Lower Peninsula (Hamer et al. 2010). Four A. americanum were recovered, all from southwestern Michigan: one adult female in Barry County (2004), one adult female from Allegan County (2005), one adult female in Van Buren County (2005), and one nymph in Barry County (2007) (Table 1).

Table 1.

Questing Amblyomma americanum detected by active surveillance (drag sampling) in Michigan from 2004 to 2021 by life stage and county

Year County No. of Amblyomma americanum detected
Adult male Adult female Nymph Larvae
2004 Barry – 1 – –
2005 Allegan – 1 – –
Van Buren – 1 – –
2007 Barry – – 1 –
2017 Van Buren 1 – – –
2019 Berrien 1 – 4 –
Muskegon – 1 – –
2020 Berrien 1 3 32 409
Branch 1 – – –
Huron 1 – – –
Ingham 1 – – –
2021 Berrien 5 1 45 50
Total 11 8 82 459
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Sampling in 2004–2016 was focused on the western side of the state (with a few exceptions – 2010 was broadened to better identify the range of I. scapularis). Beginning in 2017 active surveillance was carried out statewide except in 2020 when surveillance efforts focused on southern counties. See text for details. Only years when A. americanum were detected are included. Additional counties surveyed during this time period where A. americanum were not found include: Bay, Benzie, Calhoun, Cass, Charlevoix, Clinton, Ionia, Iosco, Iron, Isabella, Jackson, Kalamazoo, Kent, Lapeer, Leelanau, Livingston, Manistee, Mason, Montcalm, Oakland, Oceana, Osceola, Ottawa, Roscommon, Saginaw, Sanilac, St. Clair, Tuscola, Wayne.

Fig. 3 shows the distribution of sampling effort across Michigan from 2017 to 2021 including the efforts by BCHD (2019–2021, Berrien County). Ingham County has a site marked by a yellow star which was sampled at regular intervals throughout the season to monitor regional activity of the target species, normally I. scapularis; only the first three visits to this site are included in the effort calculations as these efforts do not represent surveillance across the county and would skew effort reported in the figure (Fig. 3). From a total of 212,989 m2 sampled in 2017, only one adult male A. americanum was recovered (Barry County). From 467,688 m2 sampled in 2018, no A. americanum were detected. From 511,330 m2 sampled in 2019, five A. americanum of two life stages (1 adult male and 4 nymphs) were recovered, all at a single site in Berrien County and fulfilling one of the CDC criteria for classifying an established population (CDC 2020). BCHD sampled 12,000 m2, that same year (2019) but no other A. americanum were detected. In 2020, a total of 265,745 m2 were sampled at 55 sites across 24 counties in southern Michigan by MSU between 8 June and 23 July. In total, 2,918 ticks were collected (Table 2) comprised of I. scapularis (90.3%), Dermacentor variabilis (Say) (7.8%), A. americanum (1.2%), I. dentatus (Marx) (0.01%), Haemaphysalis leporispalustris (Packard) (0.1%), and a single Ixodes cookei (Packard). Of the 55 sites sampled, A. americanum was found at seven sites in five counties across southern Michigan (from west to east: Berrien, Branch, Cass, Ingham, and Huron). Only one site, located in Berrien County, yielded both more than one A. americanum and multiple life stages. An additional 25,000 m2 were sampled from 5 sites in Berrien County between 11 May to 30 July in 2020 by the BCHD, which revealed a single A. americanum from two sites. In 2021, statewide surveillance by MSU for I. scapularis resumed; 373,378 m2 were sampled and an additional 38,000 m2 were sampled by BCHD. A. americanum was only detected in Berrien County, where multiple ticks were detected at two sites, GMSP and Warren Dunes State Park (WDSP).

Fig. 3.

Fig. 3.

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Drag sampling effort by county (m2) from 2017 to 2021. Black dots mark field sampling sites. dots with circles mark sites where A. americanum were found. (A) Sampling effort for 2017, 2018, 2019, 2021; (B) Sampling effort for 2020 from 8 June to 23 July (See Table 1). The square marks the established population of A. americanum at Grand Mere State Park (detected in this study). The star marks a site sampled regularly as a reference for I. scapularis to ensure they are active regionally when sampling other sites. Only the first three visits for this site (i.e., during the nymphal host-seeking period) were included in the effort calculations for each year so as not to skew overall county effort.

Table 2.

Total numbers of each tick species and life stage collected by drag sampling by county from 8 June to 23 July 2020 in southern Michigan

County Effort (m2) Species
Ixodes scapularis Dermacentor variabilis Amblyomma americanum Other
AM AF N L AM AF N AM AF N
Allegan 5,381 1 7 8 – 7 8 – – – –
Barry 5,625 – – 16 23 – – – – – –
Berrien 42,039 26 26 278 309 22 32 4 3 3 26 I. dentatus 1L, 3N
Branch 12,529 – – 2 – 1 1 – 1 – –
Calhoun 10,855 5 3 52 1 3 2 – – – – I. dentatus 2N
Cass 25,161 – 3 128 835 1 8 – – 1 – I. dentatus 1N
Clinton 1,870 1 – 4 1 – – – – – –
Hillsdale 8,060 – – 8 31 4 4 – – – –
Huron 10,277 1 4 3 – – – – 1 – – H. lep. 1N
Ingham 4,700 8 7 250 82 – – – 1 – –
Jackson 16,513 3 – 36 9 1 3 – – – –
Kalamazoo 12,850 2 3 184 31 1 3 – – – – I. dentatus 3N
Lapeer 10,999 – – 3 2 – 1 – – – – I. dentatus 1N
Lenawee 20,487 – – 3 – 12 20 – – – – I. cookei 1AF
Monroe 11,336 – – – – 10 7 – – – – I. dentatus 1N
Oakland 5,678 1 1 3 – 1 – – – – –
Sanilac 1,560
St. Clair 4,986 – 1 28 3 – – – – – –
St. Joseph 9,300 – – 63 – 3 7 – – – – I. dentatus 1N
Tuscola 4,296 – – 5 – – – – – – – Ixodes spp. 1L
Van Buren 5,732 5 3 52 6 21 30 – – – – H. lep. 1N
Washtenaw 10,230 5 3 25 5 1 1 – – – – I. dentatus 1N
Wayne 26,806 1 – 21 6 3 5 – – – – D. variabilis 1L
Total 265,745 59 61 1172 1344 91 132 4 6 4 26 19
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AM, adult male; AF, adult female; N, nymph; L, larva; H. lep., Haemaphysalis leporispalustris; I. dentatus, Ixodes dentatus; I. cookei, Ixodes cookei; D. variabilis, Dermacentor variabilis; Ixodes spp., unidentifiable Ixodes species due to damage to specimen.

Berrien County Active Surveillance

Table 3 summarizes the total sampling effort in Berrien County and numbers of A. americanum detected from 2019 to 2021 at all the sites that were sampled. Four parks were sampled all three years; two other parks were sampled only once. From the four parks sampled each year, A. americanum was detected at three sites (Table 3). At one site, WDSP, the status of A. americanum was considered established in 2019 and again in 2021. Surprisingly only one A. americanum was found at this site in 2020 despite similar effort. At a second site, GMSP, A. americanum was not detected in 2019. However, multiple stages, including larvae, were detected in both 2020 and 2021, suggesting the presence of an established and breeding population. At the third site, Love Creek Nature Center, A. americanum were detected in only one year, 2020.This site yielded two adult A. americanum, thus not reaching the threshold criteria for an established population. Total sampling effort per site for all three years ranged from 26,003 m2 to 57,165 m2, and the total distance sampled at WDSP and GMSP was ~1.5–2 times more than the other two sites, where no A. americanum were detected or reported.

Table 3.

Active surveillance effort for Berrien County from 2019 to 2021 and status level for Amblyomma americanum detections (per site per year) as defined by the CDC as more than 6 ticks or more than one life stage found in a given calendar year (Springer et al. 2014)

Site year # Of visits Area dragged (m2) Total Amblyomma americanum collected Establishment status
Larvae Nymphs Adults
Grand Mere State Park
2019 6 6,600 0 0 0
2020 24 36,365 409 32 5 Established
2021 12 14,200 50 42 5 Established
Total 57,165
Warren Dunes State Park
2019 9 14,820 0 4 1 Established
2020 9 12,671 0 0 1 Reported
2021 11 12,858 0 4 1 Established
Total 40,349
Love Creek Nature Center
2019 2 2,000 0 0 0 Not detected
2020 11 16,232 0 0 2 Reported
2021 10 12,000 0 0 0 Not detected
Total 30,232
Madeline Bertrand County Park
2019 2 2,600 0 0 0 Not detected
2020 10 13,803 0 0 0 Not detected
2021 9 9,600 0 0 0 Not detected
Total 26,003
Galien River County Park
2020 4 6667 0 0 0 Not detected
Total 6,667
Lincoln Township Beach
2019 1 1000 0 0 0 Not detected
Total 1,000
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Total effort for each site is reported for each year and includes sampling performed by both Michigan State University and the Berrien County Health Department. Two sites were sampled only for one year. Total numbers of A. americanum are reported for each site for each year. (Note: As per CDC convention, the lone star tick status of Berrien County as a whole was considered established as of 2019, given the findings at Warren Dunes State Park.)

Sampling Companion Canines (2015–2018)

Study periods varied over the four years, but all included the periods when adult and nymphal A. americanum would be expected to be active (Table 4). At least 300 animals representing 16–69 counties per year were examined for a total of 4,097 animals examined. No A. americanum were detected in three of the four study years. In 2016, when 2,510 individuals were examined, a single adult female A. americanum was collected from a dog residing in Muskegon County.

Table 4.

On-host Amblyomma americanum detected by active surveillance of companion canines with no travel history in Michigan from 2015 to 2018 by participating veterinary clinics or shelters.

Year
2015 2016 2017 2018
Dates animals were examined 5/1–6/5 2/10–6/3 4/3–7/26 5/13–7/27
No. clinics/shelters submitting data 30 48 26 8
No. of animals examined 391 2519 887 300
No. of counties represented 31 69 42 16
No. of animals infested with A. americanum 0 1a 0 0
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a One adult female A. americanum was detected from an animal residing in Muskegon County.

Characterization of the phenology of A. americanum at GMSP

In total, 448 A. americanum were sampled at GMSP between 11 June and 12 October 2020, including 409 larvae, 32 nymphs, 3 adult males, and 2 adult females. Seasonal activity for A. americanum and the now endemic I. scapularis (for comparison) are presented in Fig. 4. A. americanum adults were detected only in June. Nymphs were active from June to September but were most active in June. Larvae were first detected in August, peaked in September, and were not detected in October. I. scapularis adults were detected in June, late September, and October, with greatest numbers in October. Nymphal I. scapularis were detected from June to September and peaked in June. Larval I. scapularis were detected throughout the study period, with the first peak in July followed by a second peak in September.

Fig. 4.

Fig. 4.

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Phenology of each questing life stage of (A) Amblyomma americanum and (B) Ixodes scapularis at Grand Mere State Park (Berrien County) from 11 June 2020 to 10 October 2020 (ended after 2 consecutive visits in the fall where no A. americanum were detected). See the square on the map in Fig. 2 for the location of the field site.

Discussion

Since the mid-1980s, detections of A. americanum in Michigan have been recorded by passive surveillance (Walker et al. 1998, Hamer et al. 2009, MDHHS 2021a); however, until recently, active surveillance efforts only rarely detected A. americanum. Applying the CDC’s operational definition for established tick populations (CDC 2020), we report the first records of established populations of A. americanum in Michigan in recent history, and according to CDC convention, the lone star tick status of Berrien County should be considered established since 2019. To provide evidence that this invasion is recent and geographically limited we collated the results of prior surveillance efforts in Michigan comprising passive surveillance for ticks in general and active surveillance for I. scapularis specifically. Weekly surveillance at one site where a breeding population of A. americanum was detected allowed us to characterize the seasonal activity of this newly establishing tick in Michigan, which appears to be similar to that in other areas where A. americanum are established.

Previous Active Surveillance in Michigan (2004–2019)

In the past two decades, active surveillance failed to detect an established population of A. americanum in Michigan. Between 2004 and 2018, 841,129 m2 were sampled throughout the state and only four adult and one nymphal A. americanum were detected despite sampling in suitable habitats during phenologically appropriate times of the year (Hamer et al. 2010). Furthermore, examination of >4,000 companion canines over four years (2015–2018) across Michigan resulted in the detection of one A. americanum tick attached to one dog, who resided in a county in the Lower Peninsula along Lake Michigan. An earlier study aimed at understanding the invasion of I. scapularis into Michigan, similarly, made use of veterinary clinics to collect ticks. Out of 345 ticks collected from 2001 to 2002 only three A. americanum were identified (Hamer et al. 2009). While all these efforts may have missed some cryptic populations, especially in less sampled regions (e.g., Michigan’s upper peninsula), the findings together suggest that there were no widespread established populations of A. americanum within Michigan during this timeframe.

Given the previously mentioned dearth of A. americanum in Michigan, we were surprised to find four nymphs and an adult at a WDSP in 2019. For nymphs to be detected in an area, they may have been derived from a locally hatched larvae that fed on local hosts, thereby representing a locally reproducing population. On the other hand, they may have been derived from larvae that had hatched elsewhere and then were introduced into the area by dispersing hosts. For example, animals, such as deer, coyote, or birds, dispersing from northwest Indiana, or other areas in southwest Berrien County with undetected A. americanum populations may have introduced larvae. In either of these cases, introduction of larvae would be from within the same local region, suggesting a successful invasion of A. americanum into Michigan. If considering longer-range introductions by migratory songbirds, given A. americanum larvae generally host-seek in late summer (Telford et al. 2019), it is unlikely that they would have introduced larvae from the endemic regions in southeastern or south-central United States or even populations in southern Indiana or Illinois, as fall migrating songbirds are traveling in the opposite direction. Although it is possible for nymphs to be dispersed northwards by spring migrating songbirds, multiple successful events (e.g., molting, finding an adult host, finding a mate, ovipositing, and larval hatching) as well as surviving the local abiotic conditions would need to follow for these engorged nymphs to result in local larval ticks. A high volume of migrating birds landing and/or stopping over in an area may elevate the chances of such introductions. However, introductions of dispersing larvae, nymphs, or adults from nearby established populations by A. americanum’s more frequently used terrestrial hosts, such as the white-tailed deer, might be more likely.

Targeted surveillance for A. americanum in (2020) and statewide surveillance (2021)

Given the finding of multiple life stages of A. americanum at WDSP in southwestern Michigan and given the presence of established A. americanum populations in northwestern Indiana counties that border southwestern Michigan, (ISDH 2021) surveillance conducted by MSU in 2020 focused on southern counties. A. americanum were detected at a greater number of sites and counties in 2020 than in any previous year, and this may have been due in part to greater sampling effort per county compared with that in previous years. First, although sampling effort per site was similar in 2020 compared to 2019 (approximately 3–4 visits/site), it was generally greater compared to that in prior years. Second, in 2020 we attempted to increase the concentration of sites from ~1–2 sites per county to 3–5 sites per county. Even with this increased coverage of southern Michigan, only one county (Berrien) yielded more than one site where A. americanum were detected, and only one site, GMSP in Berrien County, revealed more than one life stage. It is not surprising that sampling a greater density of sites may result in a greater number of detections of A. americanum. Although the sample size is small (n = 5), the detections outside of Berrien County were all adults, which may represent adventitious nymphs dispersed by spring migrating songbirds (Stafford et al. 2018). At one of the sites outside Berrien County where an adult A. americanum was detected in 2020, ~ bi-weekly sampling May–October in 2019 and 2021 did not result in any detections of A. americanum.

A. americanum Tick Emergence in Berrien County

In the early 2000s Berrien County was sampled frequently because it is also where established populations of I. scapularis were first detected in the Lower Peninsula (Foster et al. 2004). Because of limited resources and the need to monitor other areas where the establishment status of I. scapularis was less known, Berrien County was sampled less intensively (i.e., number of sites and frequency of visits per year) by MSU after the early 2000s. Beginning in 2019, sampling effort in Berrien County increased in large part due to the initiation of surveillance by the BCHD as part of a MDHHS-funded program to increase surveillance efforts for invasive I. scapularis and associated pathogens in Michigan. MSU efforts also increased in 2020 following the discovery of multiple life stages of A. americanum at WDSP in 2019.

Although A. americanum were collected each year (2019–2021) at WDSP, the tick collections only met one of the CDC criteria for established populations (detecting at least two life stages in one calendar year) in 2019 and 2021. The numbers of ticks collected each year were low, never achieving the other criterium of detecting at least six ticks. In contrast, data from GMSP suggest that A. americanum either were not yet established at that site in 2019, or more likely, were present at an abundance below our threshold of detection, and then appear to be steadily increasing in 2020 and 2021. Established populations of A. americanum have now been detected in Berrien County for three consecutive years, 2019–2021.

No established populations of A. americanum were detected outside WDSP and GMSP, suggesting that either further spread has not yet occurred, or that the level of sampling effort was inadequate to detect low density emerging populations. Future research may investigate differences in abiotic and biotic factors among sites to understand variation in initial establishment success of A. americanum. For instance, both WDSP and GMSP are located along Lake Michigan, whereas other sites are found further inland. Proximity to Indiana’s established populations, from which Berrien County’s A. americanum likely originated, may have increased invasion success. Interestingly, WDSP, where A. americanum appears to be establishing at a slower rate compared to GMSP, is closer to the Indiana populations. In fact, WDSP is ~48 km from the Indiana Dunes National Park and Indiana Dunes State Park, where A. americanum are abundant (L. Green, IDOH, personal communication).

This recent detection of an emerging population of A. americanum in Michigan after two decades of active surveillance, may not actually represent an entirely new expansion in their range. Rochlin et al. (2022) recently published a review of historical records, which make a convincing argument that A. americanum may have been present in southern Michigan during the early 1800s. Specifically they recount how Michigan Agricultural College (now MSU) Professor of Zoology and Entomology Albert John Cook reported common encounters with the tick as a child in the woods of Michigan but how, at the time of his writing (1878), they were less prevalent. Rochlin attributes this decline of A. americanum to a combination of logging, conversion of forest to agricultural land, and unmanaged hunting of white-tailed deer (Rochlin et al. 2022). Given these reports, our findings may simply represent a reestablishment of A. americanum in its historic range.

Definition of Established Populations and Consideration of Passive Surveillance

The criteria for considering a tick species as being established in a given county is important to consider as we seek to understand their spread. Established tick populations as defined by current CDC recommendations (CDC 2019, CDC 2020) involve either finding more than one life stage or finding at least six ticks in that county in a calendar year (Dennis et al. 1998, Springer et al. 2014, Nelder et al. 2019). Passive surveillance data previously have also been used to fulfill these criteria (Dennis et al. 1998, Springer et al. 2014). Many public health agencies have community tick submission programs, and more recently, there have been nongovernmental agencies or labs that also have been set up to receive ticks for surveillance (Nieto et al. 2018, Kopsco et al. 2021; Porter et al. 2021a,b). While community-submitted ticks can be an important source of data for informing risk, they can be unreliable for determining whether a tick population is established in a given area, especially if travel history is not taken into account, and tick exposure may have occurred elsewhere in a tick endemic area. This may be a particularly important point for an aggressive tick species such as A. americanum as multiple ticks are commonly found feeding on a single host. A single dog traveling to an endemic area can easily bring back enough ticks to consider a county established. In cases like this, the number of separate submissions of a tick from a county in a given year may provide more insight into prevalence and risk than the total number of ticks. Passive surveillance from people, companion animals, and livestock must take travel history into account in order to be reliable and useful. MDHHS attempts to include only data with no out-of-state history, but travel history is not always known. A. americanum submitted to the MDHHS for the last decade fulfill CDC criteria for some Michigan counties in some years, but the numbers vary widely from year to year (with no proportional increase over time), and no county is consistently represented (Figs. 1 and 2). Thus, while some Michigan residents have encountered A. americanum ever since passive surveillance programs have been in place (Walker et al. 1998, MDHHS 2021a), the lack of spatial and temporal trends does not support the hypothesis of local established populations. Additionally, active surveillance from those same years does not provide evidence for any established populations in those areas. It will be interesting to see if increased rates of A. americanum submissions do occur in the future, especially from areas where we believe it is establishing, although other factors (e.g., awareness and adoption of ticks submission program and population size) may affect submission rates.

Other sources of community science data that may be a valuable addition to health department passive surveillance (Cull 2022). One crowd-sourced database that has been used increasingly for scientific research on biodiversity is iNaturalist (https://www.inaturalist.org), whereby people can submit records of organisms observed in a specific location and time. Thus, theoretically, there should be no uncertainty with location information if it is provided accurately. A photograph submitted to iNaturalist in May of 2020 revealed a questing adult male A. americanum at GMSP prior to us discovering an established population there later that year. Only three A. americanum were reported to iNaturalist in Michigan during 2020, and interestingly, two of those were from Berrien County. While locations and exposure details made publicly available may be more detailed in some of these cases, details cannot always be verified, and photographs are not as reliable for species identification as those verified under a microscope by qualified experts, especially when ticks are engorged. Even though community science data may provide valuable insights with little effort, especially with increased use by the public, how these data are interpreted and used should be carefully considered (Eisen and Eisen 2021).

More stringent criteria have been proposed by Nelder et al. 2019, specifically requiring that active surveillance is needed to confirm an established population. They further suggest that a population be confirmed for three consecutive years with at least six specimens from a given locale collected, including at least one drag-sampled tick and at least one nymph. Using those criteria, at the time of writing, A. americanum is not considered to be established in southeastern Ontario, although many, presumably adventitious ticks have been submitted (Nelder et al. 2019). While these criteria may seem excessive, they may be warranted, especially when establishment data are being used to train ecological niche models used to predict the northward spread of this vector in the coming years (Springer et al. 2015, Raghavan et al. 2019).

Importance of Abiotic Factors for Establishment and Invasion

After A. americanum are introduced into an area, biotic and abiotic factors will affect establishment and invasion success. Given the generalist nature of A. americanum, and the abundance of their main host, the white-tailed deer in Michigan, invading A. americanum are not likely to be host-limited. Instead, they likely are more limited by off-host survivorship success and mate-finding success, which will be overcome by increasing propagule pressure. Abiotic factors likely play a particularly critical role in population establishment along the northern edge of its distribution; these include leaf litter composition, temperature, humidity, day length, and seasonality (Ludwig et al. 2016). Cold winters are known to limit the survivorship of overwintering ticks (Semtner and Hair 1976, Kaizer et al. 2015, Linske et al. 2019, Bacon et al. 2021), so it might not be purely coincidental that both in New England and the northern central United States, populations of A. americanum are emerging initially along coastal habitats, which have more moderate winters relative to areas further inland. It is unknown how A. americanum may have been introduced into northwest Indiana, whether via terrestrial hosts or migrating birds, but there are records of low numbers of A. americanum collected via a combination of passive and active surveillance from the three northwest counties bordering Lake Michigan since the late 1990s and evidence of established populations since 2005. The Indiana Department of Health (IDOH) has been drag sampling A. americanum consistently for the last decade at the Indiana Dunes National Park and Indiana Dunes State Park, where there are robust populations (L. Green, IDOH, personal communication). Besides the moderating effect of Lake Michigan on winter conditions, the oak upland coastal dune forests along Lake Michigan provide sheltered areas with highly suitable microhabitat (i.e., thick leaf litter) that further insulate ticks from cold and desiccation (especially in the “valleys” on the leeward sides of dunes). Ixodes scapularis in Michigan’s Lower Peninsula likely invaded from northwestern Indiana and emerged faster northwards along Lake Michigan than it did farther inland (Hamer et al. 2010). Given A. americanum’s lower tolerance for cold winters, the invasion of this tick might follow a similar pattern. Additionally, if introduced, A. americanum may establish and emerge on the eastern side of the state along the Lake Erie and Lake Huron coastlines where the proximity to the lakes help create more moderate conditions facilitating winter survival.

Models have recently predicted that climate change resulting in longer summers and milder winters may increase the survival and therefore establishment probability of A. americanum farther north (Raghavan et al. 2019, Sagurova et al. 2019); correspondingly, these models predict that much of southern Michigan is already suitable for A. americanum tick establishment (Raghavan et al. 2019, Sagurova et al. 2019). It should be noted, however, that some ecological niche models (Springer et al. 2015, Raghavan et al. 2019) rely on passive surveillance data (Springer et al. 2014) that resulted in categorizing some Michigan counties as having established A. americanum populations, which as discussed previously, had not been confirmed through active surveillance at the time (Walker et al. 1998). Sagurova et al. (2019), however, uses a mechanistic model (Ludwig et al. 2016) based on regional climate and tick development rates, which does not rely on these data. Interestingly, their results suggest that southern Michigan (as well as southern Ontario and Quebec) has been suitable for A. americanum for decades. While they predict that A. americanum’s range will move farther north in the coming century due to climate change, it may not be primary factor driving the current northward expansion and other factors such as those proposed by Rochlin et al. (2022) may be playing a more important role.

Seasonal Activity of A. americanum Emerging in Michigan and Implications for Public Health

Frequent sampling at GMSP in 2020 provided us insight into the phenologies of the three questing life stages of A. americanum in southwestern Michigan (Fig. 4). Unfortunately, due to COVID-19 related restrictions, MSU was unable to begin surveillance until 12 June 2020. Although BCHD started surveillance at GMSP on 17 May 2020, they did not detect any A. americanum. Of note, the same day BCHD surveyed GMSP (17 May 2020), a member of the public submitted a photograph of an adult male A. americanum to iNaturalist (Fig. 5), indicating species presence and activity (https://www.inaturalist.org/observations/46454907). This photograph is the first record of this tick at this site, illustrating that community science may help identify the continued invasion of this tick. Although based on low tick numbers, the phenological trends during the study period were consistent with those described in endemic areas further south and east (Sonenshine 1979, Schulze et al. 1986, Kollars et al. 2000, Carroll 2011, Gilliam et al. 2018). Assuming established A. americanum populations will continue to increase in abundance, continued monitoring encompassing early spring through fall will result in a greater confidence in observed patterns. Increased tick abundance may also result in broader activity periods than currently observed. For instance, more nymphs may be observed later in the summer, and some larvae may be detected in early summer, as has been noted recently in Long Island and Massachusetts (Telford et al. 2019).

Fig. 5.

Fig. 5.

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Photograph of a questing adult male Amblyomma americanum found by Burnley Traux and captured by Joseph Hinds on 17 May 2020 at Grand Mere State Park and originally submitted to iNaturalist. Photograph is reproduced here with permission from the photographer and represents the first record of A. americanum at this site.

Although there are differences in phenologies between A. americanum and I. scapularis, there is some important overlap, especially during peak nymphal activity, but also in early season adult activity. Coincident phenologies have practical implications for public health. First, as we have leveraged here in Michigan, efforts to survey for I. scapularis, which generally target the nymphal host-seeking period because of their preeminent epidemiological role, should also detect nymphal A. americanum, and to lesser extent adults, thereby increasing the likelihood of detecting and characterizing emerging A. americanum. Second and similarly, public health messaging that typically occurs in spring to prevent Lyme disease by spreading awareness of important prevention measures, will also help reduce risk and negative impacts of A. americanum-associated diseases. Third, it is important for the public and healthcare workers to recognize different tick species and how they are associated with different diseases to prevent misdiagnosis and improper treatment of tick-borne diseases (e.g., over-diagnosis and treatment of Lyme disease and under-diagnosis and treatment of an A. americanum-associated disease) (Egizi et al. 2017). For example, post-tick antibiotic prophylaxis of Lyme disease (Lantos et al. 2021) can be provided for patients who detect a nymphal or adult I. scapularis that has fed for at least 36 h and that had been acquired from a high Lyme disease incidence area such as Berrien County (MDHHS 2021b). The coincident activity of I. scapularis and A. americanum nymphs, however, creates an additional challenge to determine the species of these small feeding nymphs. This uncertainty may affect the decision to recommend post-tick antibiotic prophylaxis, which is recommended for the prevention of Lyme disease but is not recommended for ehrlichiosis (Heitman et al. 2016).

Additional Considerations for Public Health in Emerging Areas

A. americanum is of special concern in emerging areas as medical professionals in the region may not be familiar with many of its associated diseases. Pathogens of concern for human health that A. americanum are known to vector have been summarized in a recent review by Madison-Antenucci et al. 2020 and include Ehrlichia chaffeensis, the causative agent of human monocytic ehrlichiosis (HME), E. ewingii, and the rare but highly fatal Heartland and Bourbon viruses (Madison-Antenucci et al. 2020). For example, the numbers of A. americanum submitted to a passive surveillance program in central New Jersey have been increasing over the last decade and have overtaken that of I. scapularis (Egizi et al. 2017, 2019). There are significantly fewer than expected cases of HME than Lyme disease relative to the estimated encounter rates of E. chaffensis infected A. americanum to Borrelia burgdorferi-infected I. scapularis. This may suggest an under-reporting or misdiagnosis of HME in these areas (Egizi et al. 2017). Similarly, an increase in mild cases of spotted fever rickettsias (potentially caused by Rickettsia amblyommatis, which have been detected in a high proportion of A. americanum) should be expected, but should not be mistaken for the much more severe Rocky Mountain spotted fever (Behravesh et al. 2016). One of the most concerning conditions associated with A. americanum is the recently discovered alpha-gal syndrome (AS). In A. americanum endemic areas, AS is the leading diagnosed cause of anaphylaxis (Pattanaik et al. 2018). One recent case study (Houchens et al. 2021), describes a Michigan resident (with no travel history outside of the state) who arrived at an emergency room with severe anaphylaxis. The details in this report demonstrate the potential severity of AS and the difficulty in diagnosing this unusual condition, especially in areas where A. americanum is newly emerging and awareness of AS may not be prevalent in the medical community (Houchens et al. 2021).

Conclusion

Models have predicted that A. americanum would expand its range northward into Michigan (Molaei et al. 2019, Sagurova et al. 2019), but until 2019, active surveillance had not detected any established population. Here we report both an established A. americanum population at the northern extent of its range as well as the seasonal activity. Negative surveillance data in preceding years suggest that these findings most likely represent a nascent invasion rather than a long established but undetected population. Phenological patterns observed also provide insights into the public health risks posed by this tick over the course of the year and can help inform optimal time frames for future surveillance efforts. Due to limited resources and time, collected ticks have not yet been submitted for pathogen testing. Given similar host and habitat requirements, if the previous invasion of I. scapularis into Michigan is any indication (Hamer et al. 2010, Lantos et al. 2017, MDHHS 2020), we can expect to see A. americanum expanding its range in Michigan in the coming years, potentially following similar spatial and temporal trends. Educating public health officials and the medical communities, for both humans and companion animals, about the diseases associated with this tick and how to differentiate them from other endemic tick-borne diseases is recommended.

Acknowledgments

We thank S. Hamer, G.J. Hickling, and E.D. Walker for their contributions to beginning the long-term surveillance studies of invasive ticks in Michigan from which subsequent efforts have grown. Similarly, we thank E.D. Walker for providing additional insight into the data from Walker et al. 1998 as well as having coordinated and published that valuable work, which provides a baseline from which to compare subsequent distributions of ticks over time. For assistance in the field and lab, we thank S. Altus, C. Anderson, D. Arsnoe, I. Arsnoe, M. Bammer, K. Beeson, A. Dunivant, K. Fake*, S. Froehlich, M. Gleason*, G. Grzesiak, T. Hamilton, S. Haupt*, D. Houvener, T. Kerr, S. Kim, J. Kryda*, A. Larson, M. Lien, A. Luchenbill, C. Mann, M. Orbain, G. Pang, J.Pastori, M. Regalado, B. Reith, M. Rice, M. (Rosen) Clayson, J. Schroeder, M. Soja, N. Spala, J. Stych, A. Talbott, D. Tedesco, M. Volk, A. Walker, H. Waters, K. Wickens, B. Wilson*, A. Yackley, G. Yarandi, S. Zohr, and many other assistants who contributed to earlier, published work. We thank Burnley Traux and Joey Hinds for their contributions to the iNaturalist data cited. We thank our agency partners who variously started and continue to maintain the Michigan Department of Health and Human Services (MDHHS) community tick submission program; developed, funded, and facilitated active invasive vector surveillance efforts conducted by local health departments; and provided suggestions for MSU active surveillance efforts based on public health risks. They include R. Eisen, M. Poplar, R. Reik, J. Sidge, K. Signs, and M. G. Stobierski. We furthermore thank L. Green from the Indiana Department of Health for providing historical knowledge and guidance on sampling for A. americanum in northern Indiana. Land use permission was graciously provided by the Michigan Department of Natural Resource, National Park Service, United States Department of Agriculture Forest Service, Michigan State University (MSU), many county parks offices, nature centers, land conservancies, universities, and other public and private entities. We are grateful for many sources of funding supporting the work presented here. First and foremost, the majority of the active surveillance efforts for invasive ticks in the Tsao lab has been generously supported by the Michigan Lyme Disease Association (MLDA), facilitated by the L. Lobes. Drag surveillance by the Tsao lab in 2019 was largely funded by Contract E20193274-00 from MDHHS. Funding for the companion animal surveillance study was provided by the College of Veterinary Medicine Endowed Companion Animal Fund (RT082792), the MLDA, and greatly facilitated by L. Penman and Boehringer Ingelheim Animal Health. Drag surveillance by the Berrien County Health Department was funded in part by the MDHHS, and the MDHHS community tick submission program is supported with funds from the Epidemiology and Laboratory Capacity (ELC) for Prevention and Control of Emerging Infectious Diseases Cooperative Agreement from the Centers for Disease Control and Prevention, award number CDC-RFA-CK19-1904. We thank the MSU Comparative Medicine and Integrative Biology program for fellowship funding for P.F., M.P., and V.K. and to the Hal and Jean Glassen Foundation for Conservation Medicine Fellowship funding for V.K. and other students who contributed to this work. M.P., V.K., and J.T. also have been funded by the CDC Midwest Center of Excellence in Vector-Borne Diseases (U50723K866) under a subcontract to Michigan State University from the University of Wisconsin (L. Bartholomay, S. Paskewitz, principal investigators). This publication was supported by Cooperative Agreement #U01 CK000505, funded by the Centers for Disease Control and Prevention including funding for S.N., L.Q., and several other research fellows listed above with asterisks (*) who contributed to surveillance efforts. Its contents are solely the responsibility of the authors and do not necessarily represent the official views of the Centers of Disease Control and Prevention or the Department of Health and Human Services.

Contributor Information

Peter D Fowler, Comparative Medicine & Integrative Biology, Michigan State University, East Lansing, MI 48824, USA.

S Nguyentran, Department of Fisheries & Wildlife, Michigan State University, East Lansing, MI 48824, USA.

L Quatroche, Department of Fisheries & Wildlife, Michigan State University, East Lansing, MI 48824, USA.

M L Porter, Comparative Medicine & Integrative Biology, Michigan State University, East Lansing, MI 48824, USA.

V Kobbekaduwa, Comparative Medicine & Integrative Biology, Michigan State University, East Lansing, MI 48824, USA.

S Tippin, Berrien County Health Department, Benton Harbor, MI 49023, USA.

Guy Miller, Berrien County Health Department, Benton Harbor, MI 49023, USA.

E Dinh, Michigan Department of Health and Human Services, Lansing, MI 48933, USA.

E Foster, Michigan Department of Health and Human Services, Lansing, MI 48933, USA.

J I Tsao, Department of Fisheries & Wildlife, Michigan State University, East Lansing, MI 48824, USA; Department of Large Animal Clinical Sciences, Michigan State University, East Lansing, MI 48824, USA.

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