Journal of Medical Entomology

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Journal of Medical Entomology 43(2):166-176. 2006
doi: 10.1603/0022-2585(2006)043[0166:SPOHIS]2.0.CO;2

Spatiotemporal Patterns of Host-Seeking Ixodes scapularis Nymphs (Acari: Ixodidae) in the United States

M. A. Diuk-Wassera, A. G. Gatewooda, M. R. Cortinasb, S. Yaremych-Hamerc, J. Tsaoc, U. Kitronb, G. Hicklingc, J. S. Brownsteind, E. Walkerc, J. Piesmane, and D. Fisha

aDepartment of Epidemiology and Public Health, Yale School of Medicine, 60 College St., New Haven, CT 06520–8034

bCollege of Veterinary Medicine, University of Illinois, 2001 S. Lincoln Ave., Urbana, IL 61802

cFisheries and Wildlife Department, Wildlife Disease Ecology and Conservation Medicine, Michigan State University, 13 Natural Resources Bldg., East Lansing, MI 48824

dChildren’s Hospital Boston, Harvard Medical School, 300 Longwood Ave, Boston, MA 02115

eEntomology and Ecology Activity, Bacterial Zoonoses Branch, DVBID–NCID–CDC, P.O. Box 2087, Fort Collins, CO 80522

Abstract

The risk of Lyme disease for humans in the eastern United States is dependent on the density of host-seeking Ixodes scapularis Say nymphal stage ticks infected with Borrelia burgdorferi. Although many local and regional studies have estimated Lyme disease risk using these parameters, this is the first large-scale study using a standardized methodology. Density of host-seeking I. scapularis nymphs was measured by drag sampling of closed canopy deciduous forest habitats in 95 locations spaced among 2° quadrants covering the entire United States east of the 100th meridian. Sampling was done in five standardized transects at each site and repeated three to six times during the summer of 2004. The total number of adults and nymphs of the seven tick species collected was 17,972, with 1,405 nymphal I. scapularis collected in 31 of the 95 sites. Peak global spatial autocorrelation values were found at the smallest lag distance (300 km) and decreased significantly after 1,000 km. Local autocorrelation statistics identified two significant high-density clusters around endemic areas in the northeast and upper Midwest and a low-density cluster in sites south of the 39th parallel, where only 21 nymphs were collected. Peak nymphal host-seeking density occurred earlier in the southern than in the most northern sites. Spatiotemporal density patterns will be combined with Borrelia prevalence data as part of a 4-yr survey to generate a nationwide spatial risk model for I. scapularis-borne Borrelia, which will improve targeting of disease prevention efforts.

Received: July 4, 2005; Accepted: November 17, 2005

Keywords: Ixodes scapularis nymphs, Borrelia burgdorferi, spatial clustering, phenology, risk mapping



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Fig. 1. Density per 1,000 m2 (log scale) of the most abundant species of ticks (nymphs and adults pooled) collected in each of the 95 study sites. The grid used to select the sampling sites is displayed in the background as well as the 100th meridian, western limit of the study area

Fig. 2. Illustration of sampling protocol within each sampling site. Five trails were identified in the five largest areas of deciduous forest in the park. In each trail two parallel 100-m transects were dragged for ticks and the start of each transect was recorded with a GPS. Both the number of steps to the start of the transect and the angle were determined using a random number generator

Fig. 3. Spatial correlogram showing the dependence of Moran’s I, the spatial autocorrelation coefficient, on the distance between sampling sites, grouped into 300-km categories. Spatial autocorrelation exceeds zero significantly for all lags

Fig. 4. Mean density of host-seeking I. scapularis nymphs per 1,000 m2 dragged in each site. Density categories are no ticks (circle with cross), low (0–0.7 nymph per 1,000 m2), moderate (0.7–8.2 nymphs per 1,000 m2), and high (8.2–48 nymphs per 1,000 m2). The four subfigures show clustering patterns of nymphal I. scapularis density based on the Getis-Ord Gi* statistic at different distances (d). Quadrants were colored according to the Gi* value for the sampling site within them. Red quadrants (Gi* higher than 1.96) represent significant high-density clusters, green quadrants (Gi* lower than −1.96) represent significant negative clusters, yellow areas (Gi* between 0 and 1.96) are high-density clusters that are not statistically significant, and light blue areas (Gi* between −1.96 and 0) are low-density clusters that are not statistically significant

Fig. 5A. Density of I. scapularis nymphs per 1,000 m2 (y-axis) collected in each visit (date in x-axis) from northeast sampling sites. The best fitting curve (linear or quadratic) is shown for each collection. R2 values are shown for those curves that had a significant fit (P < 0.05)

Fig. 5B. Density of I. scapularis nymphs per 1,000 m2 (y-axis) collected in each visit (date in x-axis) from upper Midwest sampling sites. The best fitting curve (linear or quadratic) is shown for each collection. R2 values are shown for those curves that had a significant fit (P < 0.05)

table

Table 1. Numbers of adults and nymphs of all tick species collected during the study

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