Ixodes scapularis (Acari: Ixodidae) Distribution Surveys in the Chicago Metropolitan Region

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1 Ixodes scapularis (Acari: Ixodidae) Distribution Surveys in the Chicago Metropolitan Region Author(s): Jennifer Rydzewski, Nohra Mateus-Pinilla, Richard E. Warner, Jeffrey A. Nelson, and Tom C. Velat Source: Journal of Medical Entomology, 49(4): Published By: Entomological Society of America DOI: URL: BioOne ( is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne s Terms of Use, available at Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research.

2 SHORT COMMUNICATION Ixodes scapularis (Acari: Ixodidae) Distribution Surveys in the Chicago Metropolitan Region JENNIFER RYDZEWSKI, 1 NOHRA MATEUS-PINILLA, 2 RICHARD E. WARNER, 1 JEFFREY A. NELSON, 3 AND TOM C. VELAT 4 J. Med. Entomol. 49(4): 955Ð959 (2012); DOI: ABSTRACT Considering recent studies conþrming an increased risk of contracting Lyme disease near metropolitan Chicago, we surveyed a more comprehensive area to assess whether the geographical distribution and establishment of Ixodes scapularis (Say) populations across northeast Illinois are widespread or limited in occurrence. From May through October 2008 and from April through October 2009, 602 I. scapularis ticks of all three life stages (larva, nymph, adult) were collected from sites in Cook, DuPage, Lake, and McHenry counties in northeast Illinois. The surveys were conducted by drag sampling vegetation in public-access forested areas. I. scapularis comprised 56.4% of ticks collected (n 1,067) at 17 of 32 survey sites. In addition, four other tick species were incidentally collected: Dermacentor variabilis (Say), Haemaphysalis leporispalustris (Packard), Ixodes dentatus (Marx), and Amblyomma americanum (L.). This study updates the I. scapularis distribution in northeast Illinois. Our random sampling of suitable tick habitats across a large geographic area of the Chicago metropolitan area suggests a widespread human exposure to I. scapularis, and, potentially, to their associated pathogens throughout the region. These results prompt continued monitoring and investigation of the distribution, emergence, and expansion of I. scapularis populations and Borrelia burgdorferi transmission within this heavily populated region of Illinois. KEY WORDS Ixodes scapularis, tick, Lyme disease, Chicago metropolitan area Lyme disease, the most common vector-borne disease of humans in the United States, is caused by Borrelia burgdorferi sensu stricto. The spirochete is transmitted by the blacklegged tick, Ixodes scapularis (Say) in the Midwest (Burgdorfer et al. 1982, Steere et al. 1983). Typically, immature I. scapularis acquire B. burgdorferi infection when taking a bloodmeal from an infected small mammal reservoir host (Mather et al. 1989, Fish 1993, Bunikis et al. 2004). As incidental hosts of I. scapularis, humans can acquire B. burgdorferi infection when bitten by an infected nymph or adult tick. If left untreated during the early stages, Lyme disease can affect the skin, musculoskeletal, cardiac, and central nervous systems, ultimately leading to long-term severe joint pain and neurological damage (Steere et al. 2004). The number of human Lyme disease cases in Illinois has increased from 35 reported cases in 2000Ð136 cases in 2009 (Illinois Department of Public Health [IDPH] 2011a). 1 Department of Natural Resources and Environmental Sciences, University of Illinois at Urbana-Champaign, 1102 South Goodwin Ave., Urbana, IL Corresponding author: Illinois Natural History Survey, Prairie Research Institute, University of Illinois at Urbana-Champaign, 1816 S. Oak Street, Champaign, IL ( nohram@illinois.edu). 3 North Park University, 3225 West Foster Ave, Chicago, IL Forest Preserve District of DuPage County, 3 S. 580 Naperville Road, Wheaton, IL Both the vector tick and spirochete were once limited in the Midwest to a small area in Minnesota and Wisconsin (Davis et al. 1984, Callister et al. 1988). Although I. scapularis was initially detected along the Rock River in Ogle County, IL, in the late 1980s (Bouseman et al. 1990), Illinois has not historically been considered a Midwestern endemic focus for Lyme disease (Picken et al. 1995). Studies assessing the presence of I. scapularis near major metropolitan areas, such as Milwaukee and Chicago, in the early 1990s showed no evidence of tick populations within these areas (Callister et al. 1991). However, Picken et al. (1995) suggested that Illinois may eventually be considered an area of focal endemicity for both I. scapularis and B. burgdorferi based on the positive Þndings of several studies (Kitron et al. 1991, Nelson et al. 1991). The distributions of the tick vector, I. scapularis, and of B. burgdorferi, have continued expanding in Illinois over the past 20 yr, but the extent of their spread is not well known (Rydzewski et al. 2011). Expansion of I. scapularis geographic distribution in northern Illinois has typically followed along riparian corridors via dispersal and migration of abundant white-tailed deer populations, the main host for adult I. scapularis (Bouseman et al. 1990, Kitron et al. 1991, Cortinas and Kitron 2006). Support for this evidence of expanding I. scapularis distribution in Illinois is described by a Midwest habitat model predicting forested habitats /12/0955Ð0959$04.00/ Entomological Society of America

3 956 JOURNAL OF MEDICAL ENTOMOLOGY Vol. 49, no. 4 along the Des Plaines River in northeast Illinois as a suitable route for I. scapularis establishment (Guerra et al. 2002). As the tickõs distribution spreads farther south into the state, it is being discovered in new locales such as fragmented prairie habitats (Rydzewski et al. 2011). By 2007, Jobe et al. conþrmed the presence of B. burgdorferi-infected I. scapularis at sites in northeast Illinois located less than one mile from Chicago city limits, and they suggested that Lyme disease could become a signiþcant health concern around this heavily populated metropolitan area. The risk of Lyme disease exposure continues to increase throughout Illinois, most recently emerging in the northeast and east central areas of the state (Jobe et al. 2006, 2007; Rydzewski et al. 2011). To date, mapping the spatial distribution of I. scapularis establishment within Illinois has been limited to nonstandardized reporting (IDPH 2011b). There are numerous natural areas and parks in and around the Chicago metropolitan region. Many homes in this urbanðsuburban area are within close proximity to a matrix of fragmented woodlots and forested areasñ ideal habitat for small mammal hosts and I. scapularis populations. However, most homeowners are unaware of any residential or peridomestic risk of contracting Lyme disease, essentially in their own backyard (Guerra et al. 2002, Jobe et al. 2007). Lacking a conventional state-wide system for surveying I. scapularis, areas of tick presence could be overlooked or underreported (Madhav et al. 2004). Based on recent detections of I. scapularis in northeast Illinois, we recognized the need to assess a larger geographic range of northeast Illinois, a heavily populated area at risk for Lyme disease after exposure to infected blacklegged ticks. Expanding upon previous surveys to measure the geographic distribution of I. scapularis throughout the Chicago metropolitan region of northeast Illinois (Jobe et al. 2006, 2007), we used timed dragging surveys over a 2-yr period to assess tick occurrence in selected public-access forested areas frequented by large numbers of visitors. By collecting and identifying ticks over a large geographic range, we clariþed whether I. scapularis distribution is limited or widespread throughout the northeast Illinois region. Materials and Methods Thirty-two survey sites were selected from publicaccess forested areas throughout Cook (n 10), Du- Page (n 11), Lake (n 10), and McHenry (n 1) counties in northeast Illinois (Fig. 1). Several sites within each county had previously known presence of I. scapularis (Jobe et al. 2007), while the remaining selected sites were not surveyed previously, or I. scapularis presence was unknown (J. Nelson and T. Velat, personal communication). Sites were selected to cover a large geographic area throughout the metropolitan region, including six sites within Chicago city limits. Surveys took place during the collection period of May through October 2008 or April through Fig. 1. Relative abundance of I. scapularis collected at 32 survey sites in Cook, DuPage, Lake, and McHenry counties of northeast Illinois 2008Ð2009. October 2009 to coincide with peaks in adult activity in the spring and fall and nymph activity in the early summer (Fish 1993). Four sites were surveyed in both 2008 and To maximize tick collection efforts, sites were visited up to Þve times during each Þeld season. Questing ticks were collected via drag sampling for three person-hours per site visit. Sampling was performed during the late morning and late afternoon on days with no rain, little to no wind, and a temperature between 10 and 30 C to avoid wet vegetation and excessively cold or hot temperatures. Standardized tick drags, made of 1-m 2 white corduroy attached to a wooden dowel (Mather et al. 1996, DiukÐWasser et al. 2006), were pulled across leaf litter and low vegetation along trail edges and over short transects ( 25 m) perpendicular to trails in forested sites. The drags were checked at 30 s intervals; attached ticks of all three life stages (larvae, nymphs, and adults) were removed and placed in sealed vials Þlled with 70% ethanol. IdentiÞcation of the ticks to species and life stage was performed under a dissecting microscope using a morphological identiþcation key (Sonenshine 1979). Tick collection data, including site, date, species, and number of individuals were entered into a database before specimens were added to the research collection. All procedures were approved under biosafety protocols at the University of Illinois Urbana- Champaign, and appropriate research collection permits were obtained from landowners. ArcMap (Environmental Systems Research Institute 2011) was used to plot site locations and to map the distribution of total collected ticks.

4 July 2012 RYDZEWSKI ET AL.: Ixodes scapularis SURVEYS IN CHICAGO REGION 957 Table 1. Survey sites visited and ticks collected in northeast Illinois counties Site County Year Visits I. scapularis D. variabilis Other Total ticks C1 a Cook /1/ C2 Cook /0/ C3 Cook /0/ C4 Cook /0/ C5 Cook /2/ C6 a Cook /17/ C1 a Cook /0/ C6 a Cook /11/ C7 Cook /0/ C8 Cook /0/ C9 Cook /1/ C10 Cook /0/ D1 DuPage /1/ D2 DuPage /10/ D3 DuPage /1/ D4 a DuPage /2/ D5 a DuPage /1/ D6 DuPage /1/ D7 DuPage /0/ D4 a DuPage /0/ D5 a DuPage /0/ D8 DuPage /0/ D9 DuPage /0/ D10 DuPage /0/ D11 DuPage /0/ L1 Lake /14/ L2 Lake /2/ L3 Lake /0/ L4 Lake /0/ L5 Lake /11/ L6 Lake /0/ L7 Lake /0/ L8 Lake /0/ L9 Lake /45/ L10 Lake /0/ M1 McHenry /0/ I. scapularis is divided by no. of individuals collected for each life stage: larva/nymph/adult. Other includes no. of H. leporispalustris, I. dentatus, and A. americanum collected. a Site was surveyed in both 2008 and Results In total, 1,067 ticks were collected from 30 of 32 sites. There were 602 I. scapularis ticks (152 larvae, 120 nymphs, and 330 adults) collected from 17 of 32 sites (Table 1). In addition to I. scapularis, Dermacentor variabilis (Say) (n 321: 1 larva, 1 nymph, 319 adults), Haemaphysalis leporispalustris (Packard) (n 60: 55 larvae, 5 nymphs), Ixodes dentatus (Marx) (n 83 larvae), and Amblyomma americanum (L.) (n 1 adult) were also collected (Table 1). The highest number of I. scapularis were collected in Lake County (n 358), followed by DuPage County (n 140), and Cook County (n 100). Only one site was surveyed in McHenry County in 2009, and four I. scapularis were collected. In 2008, 15 sites were surveyed, and 296 I. scapularis were collected. In 2009, 17 new sites and four previous sites from 2008 were surveyed with 306 I. scapularis collected. The Centers for Disease Control and Prevention (CDC) deþnes a tick population as established in an area if all three life stages or at least six individuals of a single stage are collected (Dennis et al. 1998). Therefore, 14 surveyed sites meet this requirement for established I. scapularis populations. Discussion The results of this study yield a valuable snapshot of the current geographic distribution of questing I. scapularis in northeast Illinois, which can be compared with historical data and aid future studies to monitor changes and predict areas of new establishment of I. scapularis populations. During an initial study of the area surrounding Chicago and Milwaukee in the early 1990s, no I. scapularis were found, and B. burgdorferi was only recovered from two small mammals (Callister et al. 1991). These results led to the conclusion that northeastern Illinois and southeastern Wisconsin were not yet included in the Midwestern Lyme disease focus (Callister et al. 1991). However, by 2006, Jobe et al. began Þnding I. scapularis at sites surrounding the Chicago area in Cook, DuPage, and Lake Counties. In less than 20 yr, I. scapularis had become established in northeast Illinois. Because a proportion of those ticks tested positive for B. burgdorferi, Lyme disease became an emerging concern (Jobe et al. 2007). Because only a few sites had been surveyed at that time, the extent of I. scapularis distribution and establishment were still unknown. This study has clariþed the distribution of I. scapularis in a larger geographic area of northeast Illinois and has established baseline data for many public-access forested areas in the region. Because I. scapularis were found at 17 of the 32 sites between 2008 and 2009 (Fig. 1), we postulate that the blacklegged tick is widely distributed throughout the study area of northeast Illinois where suitable habitat is available. We are conþdent that surveying more sites in the region would result in discovering more established populations of I. scapularis. Similar to the results of a study focused on I. scapularis expansion along the Illinois River (Cortinas and Kitron 2006), I. scapularis also appears to be expanding its established range along the Des Plaines River, substantiating the riparian corridor hypothesis of I. scapularis population expansion (Bouseman et al. 1990, Kitron et al. 1991). Interestingly, the highest numbers of I. scapularis were collected at sites L1 and L9, forested areas adjacent to the shoreline of Lake Michigan (Table 1; Fig. 1), suggesting suitable tick habitat with ideal microclimate conditions and abundant host availability in this area. Similarly, a tick collection survey in MichiganÕs Lower Peninsula found the highest numbers of I. scapularis along the coastal transect compared with the inland transect; in fact, all but one I. scapularis came from coastal sites (Hamer et al. 2010). Ecological differences in habitat allowing for more successful introduction and establishment of I. scapularis populations near the shoreline may explain detecting higher numbers of I. scapularis compared with inland sites (Sonenshine et al. 1995, Hamer et al. 2010). Increased urbanization has resulted in smaller and fewer forested natural areas, yet recent studies show I. scapu-

5 958 JOURNAL OF MEDICAL ENTOMOLOGY Vol. 49, no. 4 laris appears to be adapting to fragmented habitats (Rydzewski et al. 2010, Hamer et al. 2010). The areas where the fewest I. scapularis were found consisted of predominantly mesic to wet-mesic grassy sites, speciþcally in Lake County west of the shoreline and in southeast Cook County (Fig. 1). This type of habitat is not believed to be suitable for the maintenance of abundant I. scapularis populations (Brown and Burgess 2001). Overall, I. scapularis appears to be well distributed throughout northeast Illinois (Fig. 1) where suitable habitat is available, similar to the areas predicted in the Midwest habitat suitability model (Guerra et al. 2002). These results suggest the need for public awareness of I. scapularis occurrence within forested areas of Cook, DuPage, and Lake Counties, especially near the shoreline of Lake Michigan. Residents and visitors of the fragmented urbanðsuburban landscapes of the Chicago metropolitan region may become vulnerable to tick bites and to an increased risk of Lyme disease as the distribution of established, infected I. scapularis populations continue to expand. To better assess the prevalence of B. burgdorferi infection, we need to expand the detection of the spirochete within these areas, especially where I. scapularis are present. Sampling efforts to track the potential spread of I. scapularis and B. burgdorferi in Illinois and across the Midwest should continue, as changes in land use can alter wildlife-vector-pathogen interactions and inßuence disease emergence. Because northeast Illinois is so densely populated and forested areas are frequently visited by high volumes of people, signiþcant peridomestic and recreational exposure could have strong impacts on human health. The results of this study provide baseline information to build public awareness about the potential exposure to vector ticks and tick-borne diseases, such as Lyme disease. It also provides evidence for developing disease prevention efforts and implementing environmental management strategies to control further spread of vector ticks and their associated pathogens. Acknowledgments We thank N. Rivera, S. Alvarez, M. Ulrich, M. Nichols, E. Phillips, and K. Carberry for their contributions in the Þeld. The authors also thank L. Haramis at the Illinois Department of Public Health and W.M. Brown at the University of Illinois Urbana-Champaign for providing valuable input to this study. This work was conducted under approved University of Illinois Biosafety protocols. Funding for this project was provided by the University of Illinois at Urbana-Champaign: Earth and Society Initiative, Department of Natural Resources and Environmental Sciences, and the Illinois Natural History Survey. 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