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Distribution of Ixodes dammini (Acari: Ixodidae) in Residential Lawns on Prudence Island, Rhode Island MARY C. CARROLL, HOWARD S. GINSBERG,1 KERWIN E. HYLAND, AND RENJIE HU Department of Zoology, Vector-Borne Disease Research Group, University of Rhode Island, Kingston, R.I. 02881

KEY WORDS Ixodes dammini, distribution, Lyme disease

LYME BORRELIOSIS is currently the most common vector-borne illness in the United States, with >8,000 human infections reported in 1 yr (CDC 1991a). The disease is prevalent in Rhode Island with an incidence rate of 10.12 reported cases per 100,000 population (CDC 1991b), which is the third highest in the Northeast. Ixodes dammini Spielman, Clifford, Piesman & Corwin is the principal vector of Lyme borreliosis (or Lyme disease) in the northeastern United States (Lane et al. 1991). High densities of /. dammini infected with Lyme disease spirochetes, Borrelia burgdorferi Johnson, Schmid, Hyde, Steigerwalt & Brenner, have been reported from Prudence Island in Narragansett Bay, RI (Anderson et al. 1986, Mather & Mather 1990). The nymphal stage of I. dammini, which is responsible for most human cases of Lyme disease, dwells primarily in leaf litter and groundlevel vegetation in the woods (Ginsberg & Ewing 1989, Siegel et al. 1991). Therefore, residential lawns do not provide optimal habitat for /. dammini, and mowing further lowers tick numbers (Wilson 1986). Nevertheless, recent studies on the distribution of questing /. dammini suggest that Lyme disease is often contracted in residential settings (Falco & Fish 1988). Maupin et al. (1991) suggested that the occurrence of nymphal I. dammini in residential

1 National Park Service Coastal Research Center & Department of Plant Sciences/Entomology, Woodward Hall, University of Rhode Island, Kingston, RI 02881.

lawns in Westchester County, NY, was associated with the presence of adjacent woodlots. We examined the relationship between relative tick abundances on lawns and adjacent woodlots by flagging lawns adjacent to other lawns and lawns adjacent to the woods. We also studied the distribution of ticks within residential lawns by flagging at graduated distances from adjacent woodlots. Materials and Methods Study Site. Prudence Island, in Narragansett Bay, RI, is 8 km long and 0.8 km wide and consists mainly of second-growth deciduous forest on 1,528 ha. Dominant woody vegetation includes black cherry, Prunus serotina Ehrhart, and arrowwood, Viburnum recognitum Fernald, along with abundant woody vines, especially poison ivy, Rhus radicans L., and bittersweet, Celastrus scandens L. About 100 permanent residents live on the island, increasing to nearly 1,500 during the summer. The wooded habitat on the island sustains abundant wildlife populations, including a large deer herd as well as a high concentration of /. dammini. Field Techniques. Residential properties involved in this study were placed into one of two categories: lawns backing on other lawns (lawn properties) and lawns backing on woods (wood properties). Residential lawns that did not fit clearly into either category were excluded. Properties within each category were assigned numbers, and lawns were selected for study with a random-number table. To avoid possible bias

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J. Med. Entomol. 29(6): 1052-1055 (1992) ABSTRACT The distribution of nymphal Ixodes dammini Spielman, Clifford, Piesman & Corwin in residential lawns was assessed by flagging on Prudence Island, RI. The number of ticks per sample was five times greater in lawns adjacent to woods than in lawns adjacent to other lawns. Relative tick abundance was negatively correlated with distance from the woods, but the decline was gradual. Spirochete prevalence in ticks did not differ among lawn types or at different distances from the woods. Therefore, barriers that keep people away from the wood edge probably lower the risk of acquiring Lyme disease, but there is still a risk. Even with physical barriers at lawn—wood edges, personal precautions to prevent tick bites should be followed.

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10 LAWNS ADJACENT TO THE WOODS LAWNS ADJACENT TO OTHER LAWNS

6-

i2 O

30 MAY

13 JUNE

26-27 JUNE

10-11 JULY

25 JULY

DATE Fig. 1. Relative abundance of nymphal 7. dammini in residential lawns adjacent to woods and in lawns adjacent to other lawns, Prudence Island, 1991. Error bars are ± one SE.

log-linear models was used to compare the numbers of ticks collected in wood versus lawn properties at different times of the season (June versus July samples), and among lawns (comparing the six pairs of lawns sampled throughout June and July). The overall ratio of the number of ticks in wood versus lawn properties was compared with expected ratios of 1:1 and 5:1 using x* tests. The proportion of ticks infected with spirochetes was compared in wood and lawn properties by calculating jf from a 2 x 2 contingency table (+/— versus wood/lawn). The correlation of relative tick abundances with distance from the woods was assessed with Spearman's rank correlation coefficient. Relative abundances were compared at different distances from the woods with Friedman's 2-way ANOVA by ranks, and infection rates were compared by calculating y2 from a 2 x 4 table (+/— versus 4 distance categories). The Statview II statistical package (Feldman et al. 1988) was used for statistical tests, except for the three-way ANOVA with log-linear models, which was performed with the BIOM package (Sokal & Rohlf 1981). Results The numbers of nymphal I. dammini collected in lawns adjacent to woods and in lawns adjacent to other lawns are plotted in Fig. 1. The overall numbers of ticks were far greater in lawns adjacent to woods (2.4 ± 0.5 [mean ± SE] ticks per sample) than in lawns adjacent to other lawns (0.5 ± 0.1) (Mann-Whitney U test, ^ = n2 = 39, U = 328.5, Z = -4.6, P = 0.0001). A three-way ANOVA with log-linear models showed no three-way interactions between lawn type, time

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from location on the island, lawns were sampled from each of the three major residential developments on the island (the east side, southeast side, and west side developments) so that the same number of lawn properties and wood properties were selected from each development. To compensate for the uneven distribution of properties in the three different sections, 18 wood and lawn properties were selected from the east side, 5 wood and lawn properties from the southeast side, and 2 wood and lawn properties were selected from the west side development. Tick sampling was performed biweekly from the end of May through July using a standard "flagging" technique. This method involved dragging a 1-m2 piece of white flannel flag over grass, leaf litter, and other vegetation. Ticks on the flag after a 2-min sample were removed using forceps and placed in a glass vial with a mesh top, which was then placed in a plastic bag with moist cotton. Eight such flagging samples were taken in each lawn. In lawns adjacent to woods, two samples were taken at each of four different distances from the woods. In all distance samples, flagging was conducted in straight transect lines parallel to the wood edge. Samples 1 and 5 were taken at the wood edge, 2 and 6 were taken 1—2 m from the wood edge, 3 and 7 were taken 2—4 m, and 4 and 8 were taken >4 m from the wood edge. To avoid sampling bias, all sample categories were alternated between M.C.C. and R.H. Spirochete Determinations. Nymphal deer ticks collected from all sites were examined for the presence of B. burgdorferi with a direct fluorescent antibody technique. Each tick was dissected on a clean microscope slide with a drop of phosphate-buffered saline (pH 7.4), the tick exoskeleton was discarded and the midgut tissue smeared under a coverslip, which was then removed. This preparation was allowed to air-dry at room temperature and was fixed with 100% acetone for 10 min. Slides were then allowed to dry and were stored at 0°C. Slides to be examined were placed in a humid chamber for 20 min at room temperature, after which 22 /A of diluted (1:100) fluorescein-labeled polyclonal antibody conjugate (Kirkegaard and Perry Laboratories, Gaithersburg, MD) was added to each slide. The slides were covered with aluminum foil and incubated for 30 min at 37°C, then removed from the incubator, uncovered, and rinsed in PBS (pH 7.4) for 20 min. The slides were then allowed to dry, mounting media (PBS/glycerin 1:9) was added, and a coverslip was placed on each. The slides were examined for spirochetes at 400 x using a compound microscope with a reflected light fluorescence attachment. Statistical Analysis. The numbers of ticks collected in lawn properties versus wood properties were compared with a Mann-Whitney U test. A three-way analysis of variance (ANOVA) using

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Discussion On Prudence Island, relative tick abundance was five times higher in lawns adjacent to woods than in lawns adjacent to other lawns. This distribution may result, in part, from the greater C/) abundance of immature /. dammini in woods cc than in open habitats (Ginsberg & Ewing 1989, UJ Q. Siegel et al. 1991, Maupin et al. 1991). In conC/) trast, B. burgdorferi infection rates in hosto seeking nymphs did not differ between the different lawn types. Infection rates were comparable with those found in wooded habitats on Prudence Island in 1990, when 40% (n = 20) of nymphs taken from the north end of the island and 27% (n = 11) of nymphs taken from the south < 1m 1-2m 2-4m > 4m end were infected (M.C.C. & R.H., unpublished data). Our data indicate that the risk of acquiring DISTANCE FROM WOODS Lyme disease is greater in lawns backing on Fig. 2. Relative abundance of nymphal I. dammini woodlots than in lawns backing on other lawns in residential lawns at different distances from the because of the greater abundance of ticks in the edge of the woods. Error bars are one SE. lawns backing on woods. These findings corroborate those of Maupin et al. (1991), who found of season, and lawn pair and no two-way inter- higher tick abundance on larger properties, actions among these variables. Therefore, the which were more likely than small properties to differences between wood and lawn properties have woodlots. The apparent gradual decline in relative tick were consistent at different times of season and among lawns. These differences were also con- abundances with distance from the woods, and sistent among the three residential develop- the variability within each distance category, ments sampled ( / = 0.978, df = 2, P = 0.61). The suggest that staying away from the wood edge ratio of the number of ticks collected in wood might lower the risk of encountering infected properties to those in lawn properties differed ticks but will not eliminate the risk. Therefore, from 1:1 ( / = 34.26, df = 1, P < 0.01) but not barriers that keep people on the lawn and away from 5:1 ( / = 0.0035, df = 1, P > 0.90). There- from the wood edge may have some value, but fore, relative tick abundances in lawns adjacent personal precautions should still be followed to to woods were about five times greater than in avoid tick bites. Barriers that would limit movement of ticks or their hosts from the woods onto lawns adjacent to other lawns. Overall, 31.0% of the nymphal I. dammini the lawn (e.g., wall-type fences, 1- or 2-m sand or were infected with spirochetes. Spirochete prev- gravel borders at the interface between lawn and alence did not differ between wood and lawn wood edge) might further reduce tick densities properties ( / = 0.0736, df = 1, P = 0.786), with in lawns, but this has not been demonstrated. infection rates in lawns adjacent to other lawns of Maupin et al. (1991) also suggested the use of 31.25% (n = 16), and in lawns adjacent to woods wood chips or tree bark as lawn-wood borders. However, these substrates are similar to the leaf of30.95%(n = 84). litter habitat of immature ticks and may serve as The relative abundances of I. dammini tick habitat. If used, these substrates should be nymphs collected in lawns at different distances modified or treated to render them unsuitable as from the wood edge are shown in Fig. 2. Relative tick habitat. Further investigation is needed on abundances declined consistently with inthe effects of various types of borders on movecreased distance from the woods, so Spearman's ment of ticks carried by hosts, as well as on ticks rank correlation coefficient was rs = — 1 (P < crawling from wood edges into lawns, before de0.05). However, the significance of differences in finitive recommendations can be given. Personal relative tick abundances at different distances precautions remain an important adjunct to any from the woods was marginal (Friedman two- physical method to limit tick densities in resiway ANOVA by ranks, four distances, six lawns, dential lawns. / = 7.5, P = 0.0568), probably because of high variability among samples. The proportion of ticks infected with spirochetes did not differ sigAcknowledgments nificantly at different distances from the woods ( / = 5.128, df = 3, P = 0.163). Infection rates We thank the residents of Prudence Island who alwere 35.0% (n = 40) within 1 m of the wood lowed us to use their lawns as sample sites; their hosedge, 28.0% (n = 25) at 1-2 m from the woods, pitality was greatly appreciated. We also thank Allan 15% (n = 20) at 2-4 m, and 50% (n = 14) at >4 m. Beck, Roger Greene, and Tom Parker for their assis-

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tance. Richard Casagrande, Roger LeBrun, and Joseph Piesman gave constructive comments on early drafts of the manuscript. The research was supported by grant 91-7 from The Pesticide Relief Fund, Rhode Island Department of Environmental Management. References Cited

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tribution of lxodes dammini (Acari: Ixodidae) and Lyme disease spirochetes on Fire Island, New York. J. Med. Entomol. 26: 183-189. Lane, R. S., J. Piesman & W. Burgdorfer. 1991. Lyme borreliosis: relation of its causative agent to its vectors and hosts in North American and Europe. Annu. Rev. Entomol. 36: 587-609. Mather, T. N. & M. E. Mather. 1990. Intrinsic competence of three ixodid ticks (Acari) as vectors of the Lyme disease spirochete. J. Med. Entomol. 27: 646-650. Maupin, G. O., D. Fish, J. Zultowsky, E. G. Campos & J. Piesman. 1991. Landscape ecology of Lyme disease in a residential area of Westchester County, New York. Am. J. Epidemiol. 133: 1105-1113. Siegel, J. P., U. Kitron & J. K. Bouseman. 1991. Spatial and temporal distribution of lxodes dammini (Acari: Ixodidae) in a northwestern Illinois state park. J. Med. Entomol. 28: 101-104. Sokal, R. R. & F. J. Rohlf. 1981. Biometry, 2nd ed. Freeman, San Francisco. Wilson, M. L. 1986. Reduced abundance of adult lxodes dammini (Acari: Ixodidae) following destruction of vegetation. J. Econ. Entomol. 79: 693696. Received for publication 18 February 1992; accepted 26 May 1992.

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Anderson, J. F., R. C. Johnson, L. A. Magnarelli, F. W. Hyde & J. E. Myers. 1986. Peromyscus leucopus and Microtus pennsylvanicus simultaneously infected with Borrelia burgdorferi and Babesia microti. J. Clin. Microbiol. 23: 135-137. Centers for Disease Control (CDC). 1991a. Lyme disease surveillance—United States, 1989-1990. Morbidity and Mortality Weekly Report 40: 417420. 1991b. Lyme disease surveillance summary. Centers for Disease Control/Division of Vector-borne Infectious Diseases 2(3): 1-12. Falco, R. C. & D. Fish. 1988. Prevalence of lxodes dammini near the homes of Lyme disease patients in Westchester County, New York. Am. J. Epidemiol. 127: 826-830. Feldman, D., J. Gagnon, R. Hofmann & J. Simpson. 1988. Statview II. Abacus Concepts, Inc., Berkeley, CA. Ginsberg, H. S. & C. P. Ewing. 1989. Habitat dis-

lxodes dammini

Distribution of Ixodes dammini (Acari: Ixodidae) in residential lawns on Prudence Island, Rhode Island.

The distribution of nymphal Ixodes dammini Spielman, Clifford, Piesman & Corwin in residential lawns was assessed by flagging on Prudence Island, RI. ...
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