Vegetational Associations of Host-seeking Adult Blacklegged Ticks, Ixodes scapularis Say (Acari: Ixodidae), on Dairy Farms in Northwestern Wisconsin

Vegetational Associations of Host-seeking Adult Blacklegged Ticks, Ixodes scapularis Say (Acari: Ixodidae), on Dairy Farms in Northwestern Wisconsin

Vegetational Associations of Host-seeking Adult Blacklegged Ticks, Ixodes scapularis Say (Acari: Ixodidae), on Dairy Farms in Northwestern Wisconsin E...

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Vegetational Associations of Host-seeking Adult Blacklegged Ticks, Ixodes scapularis Say (Acari: Ixodidae), on Dairy Farms in Northwestern Wisconsin E. T. SCHMIDTMANN,* J. L. SCHLATER,† G. O. MAUPIN,‡ and J. W. MERTINS† *Arthropod-borne Animal Diseases Research Laboratory, Agricultural Research Service, USDA, University of Wyoming, Laramie 82071 †National Veterinary Services Laboratories, Veterinary Services, Animal and Plant Health Inspection Service, USDA, Ames, IA 50010 ‡Centers for Disease Control, Division of Vector-borne Infectious Diseases, Fort Collins, CO 80522

ABSTRACT

INTRODUCTION

As a measure of the risk for exposure to Lyme disease, we estimated the distribution of host-seeking adults of the blacklegged tick, Ixodes scapularis Say, on dairy farms in Barron County in northwestern Wisconsin. Vegetation ecotypes that were common to 18 farms that were representative of the county were surveyed by flag sampling. Tick prevalence and abundance, which were similar during fall and spring periods, were very low in farmhouse yards and forage croplands; only a single male was collected from 17 lawns. Sampling of 18 pastures with lactating cows also yielded only a single I. scapularis. In contrast, I. scapularis adults were captured in 9 of 37 samples from 18 pastures with heifers and dry cows; in those pastures, ticks were associated with woods and secondary vegetation or margins of pastures adjacent to woodlands. Blacklegged ticks were most prevalent and numerous in ungrazed woodlands; adults were captured in 27 of 53 samples on 13 of 15 farms, particularly when evidence of white-tailed deer, Odocoileus virginianus (Zimmermann), was apparent. The risk of encountering adult blacklegged ticks on dairy farms in Barron County, Wisconsin is therefore greatest in woodlands habitat. The presence of adult ticks in pastures with heifers and dry cows establishes an ecological basis for the exposure of dairy cattle to adult I. scapularis. Pastures with lactating cows, farmhouse yards, and forage croplands represent negligible risk. ( Key words: ticks, dairy cattle, risk of encounter, Lyme disease)

The blacklegged tick, Ixodes scapularis Say, a primary vector of Borellia burgdorferi Johnson, Schmid, Hyde Steigerwalt, and Brenner, the etiologic agent of Lyme disease in the United States ( 1 ) , is well established in woodland communities of the Northeast, Mid-Atlantic, and Upper Midwest in the US (13, 30). The presence of blacklegged tick populations in deciduous and coniferous woodlands ( 2 2 ) reflects favorable microclimatic factors ( 2 0 ) and suitable hosts for immature and adult stages, notably white-footed mice, Peromyscus leucopus (Rafinesque) (16), and white-tailed deer, Odocoileus virginianus (31), respectively. Human risk for exposure to blacklegged ticks and Lyme disease is, therefore, commonly associated with occupational and recreational activities that occur outdoors (12, 28), although nymphal and adult blacklegged ticks may also occur on lawns and ornamental shrubbery of suburban residential premises in the northeastern states (5, 11, 19, 29). As evidenced by the presence of antibodies to B. burgdorferi in cattle and horses (3, 14, 15, 17), domestic livestock also are exposed to the feeding of blacklegged ticks. However, apart from the documentation of blacklegged ticks in pastures bordered by woodlands on horse farms in Maryland (26), information is lacking about the ecological conditions that expose livestock to I. scapularis. The purpose of this study was to assess the presence of adult blacklegged ticks on dairy farms in northwestern (Barron County) Wisconsin as a measure of risk for exposure to tick-borne pathogens, especially Lyme disease. The status of Lyme disease in livestock has been reviewed by Parker and White ( 2 1 ) and Bushmich ( 4 ) and discussed by Ji and Collins (14). Ixodes scapularis is well established, and Lyme disease is endemic in northwestern Wisconsin (10). The physiography of Barron County, which supports approximately 2100 dairy farms, reflects weathered, older glacial drift, with a flat to rolling topography,

Received April 22, 1997. Accepted October 14, 1997. 1998 J Dairy Sci 81:718–721

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clay-silt soils, and fewer lakes than adjacent areas that were glaciated more recently during the Wisconsin Period (18). Uncultivated lands other than wetlands are largely woodlands of mixed oaks, Quercus spp.; sugar maple, Acer saccharum Marshall; paper birch, Betula papyrifera Marshall; and white pine, Pinus strobus L. MATERIALS AND METHODS Dairy Farms Farms were surveyed in October and May to coincide with the bimodal host-seeking phenology of adult I. scapularis in the Upper Midwest (23). Farms were selected in a random sequence from a list of dairies representing townships that had concentrations of dairying in central, eastern, western, northern and southern geographic areas of Barron County. Fifteen farms were selected initially for survey, but inclement weather and daytime temperatures of less than 7.2°C (45°F), which suppress blacklegged tick activity ( 8 ) , limited the survey in October to 9 dairies. In May, 9 other farms that were representative of the county were identified and surveyed. This group was selected from a list of farms, each of which had two family members who tested positive for antibodies to B. burgdorferi (direct fluorescent antibody test) based on sera taken in August 1991 (Centers for Disease Control, Atlanta, GA, 1991, unpublished data). Aerial photographs (Soil Conservation Service) were used to delineate in part the primary vegetational areas on each farm into five principal vegetation types or ecotypes. These ecotypes were 1 ) farmhouse yard vegetation, including lawn, ornamental plantings, and vegetation along windbreak trees (shelterbelt); 2 ) pasture with lactating cows, which was generally open pasture adjacent to the milking barn and devoid of vegetation other than grass but that occasionally included scattered deciduous trees; 3 ) pasture with heifers or dry cows, which was open pastureland, generally separate from the barn, often including areas of woodland or secondary vegetation but, on some farms, with scattered deciduous trees; 4 ) ungrazed woodlands, which were deciduous woods with mixed conifers ungrazed by cattle; and 5 ) cultivated corn or alfalfa cropland. Tick Sampling The presence of host-seeking adult blacklegged ticks was assessed in October by flagging; a 1-m2 flannel cloth was attached to a 38-mm diameter dowel rod and was pulled with a cord over and through

representative vegetation. A tick sweep of similar dimensions was used in May ( 7 ) ; this method is a modification of the tick flag that effectively captures both host-seeking adult and nymphal ticks in mixed types of vegetation. Respective ecotypes were sampled similarly. In the fall survey, we standardized the flag sampling among farms by counting the number of 10-m segments conducted and then estimating the time that elapsed for each vegetational ecotype. Small areas, such as lawns and ornamental vegetation, were sampled for up to 5 min, and larger areas, such as pastures and woodlands, were sampled for 10- or 15-min periods. Forage cropland was sampled in linear transects of 20-min duration in October. In the spring survey, we recorded elapsed time for sampling each ecotype using the same conditions for time and ecotype that were employed in the fall survey. Time was measured with a timer, and the flag or sweep was examined for ticks at each 10-m interval. Data Analysis The numbers of male and female blackleggged ticks captured in each 10-m sample for each ecotype were summed across farms by fall and spring periods. Inspection of the data revealed no consistent differences between male and female ticks by ecotype or by survey period; thus, the sex of the ticks was not considered in analysis of the data. Weighted least squares mean values were calculated for each ecotype to correct for variable variance. An ANOVA ( 2 5 ) was computed to examine the effects of farm, ecotype, survey period, and interactions among those variables. Least squares means were tested for significance by paired comparisons (25). Significance was preset at P = 0.05. RESULTS AND DISCUSSION Table 1 presents the prevalence and abundance of adult blacklegged ticks by vegetational ecotype. Tick abundance in vegetation associated with farmhouse yards, pastures with lactating cows, pastures with heifers and dry cows, and ungrazed woodlands did not differ between fall and spring periods ( F = 0.13; P = 0.72). Both tick abundance and prevalence were very low in farmhouse yards; 1 tick was collected from 17 lawns, and no ticks were taken from samples of 21 ornamental plant beds or vegetation bordering 11 spruce or pine tree windbreaks (shelterbelts). The risk of encountering adult I. scapularis in farmhouse yards in Barron County is therefore negligible and thus differs from suburban residential areas in the northeastern United States where adult blacklegged Journal of Dairy Science Vol. 81, No. 3, 1998

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TABLE 1. Association between adult Ixodes scapularis and vegetation ecotypes on dairy farms in Barron County, Wisconsin. Ticks Ticks in ecotypes captured

Ecotype

(no./no.) 1 Farmhouse yard Lawn Ornamentals Windbreak Total Pasture, lactating cows Open grass Deciduous trees Wooded or brushy Total Pasture, heifers, and dry cows Deciduous trees Wooded or brushy Total Ungrazed woodlands Total 1Number

(no./min)

1/17 0/19 0/11 1/47

1/105 0/120 0/95 1/325

0/14 0/2 1/2 1/18

0/75 0/20 1/30 1/125

0/7 9/30 9/37

0/85 17/265 17/350

27/53

70/505

of positive samples out of total number of samples.

ticks are found in ornamental vegetation and on lawns of yards adjacent to tick-infested woodlands (5, 11, 19, 29). This disparity is probably because dairy farmhouses in Barron County are commonly surrounded by cultivated cropland, and we encountered no adult I. scapularis in 8 corn and 9 alfalfa fields on 5 farms. The absence of blacklegged ticks in 17 of 18 pastures used for grazing lactating cows indicates that those cows have a low risk for exposure to adult blacklegged ticks. The exposure to sunlight and grazed condition of grass pasture, which is inimical to survival of I. scapularis ( 2 ) , contrasts with the shaded leaf litter of woodlands, which is conducive to I. scapularis populations. Blacklegged tick nymphs and adults have been found along the margins of pastures adjacent to tick-infested woodlands on horse farms in Maryland (26), but most pastures with lactating cows that we sampled in Barron County were bordered by habitat that was unfavorable for ticks, such as barns, drylots, farmhouses, and croplands. In contrast to results from pastures with lactating cows, blacklegged ticks were present in 9 of 37 samples taken from pastures with heifers or dry cows on 6 of 12 farms. These pastures were generally remote from milking barns and often bordered or included woodlands; host-seeking ticks here were invariably associated with brushy and wooded areas or the pasture margins that were adjacent to woodlands. The presence of host-seeking ticks in pastures with heifers and dry cows, which presumably represent Journal of Dairy Science Vol. 81, No. 3, 1998

extensions of the tick populations in adjacent woodlands, establishes an ecological basis for the exposure of dairy cattle to adult I. scapularis. Ji and Collins ( 1 4 ) reported antibodies to B. burgdorferi flagellin in 7% of cows and 66% of herds in Barron County and showed a correlation between antibody seroprevalence and the geographic distribution of I. scapularis in Wisconsin. These collective data are evidence of exposure in dairy cattle to feeding by I. scapularis, some of them infected with B. burgdorferi. The data do not, however, imply that cattle develop clinical signs of Lyme disease infection because studies conducted to determine whether infection with B. burgdorferi causes clinical disease in cattle have been inconclusive (14). We also observed that adult blacklegged ticks were scarce in those pastures where understory vegetation and leaf litter were sparse, presumably because of cattle browsing. Leaf litter provides microclimatic conditions that are essential to the survival of subadult I. scapularis (27). A reduction in understory vegetation and leaf litter also may alter the activity of rodents or deer that serve as hosts and, thus, may reduce tick density. In addition, the movements of cattle within the pastures may have depleted numbers of questing ticks before our survey. The latter interpretation is supported by the capture of adult ticks in 5 of 8 wooded pastures with heifers or dry cows in May, which was before cattle were released from winter housing. Adult blacklegged ticks were most abundant and prevalent in ungrazed woodlands ( t = –2.16; P = 0.04) where ticks were present in 27 of 53 such areas on 13 of 18 farms (Table 1). Host-seeking adults were particularly common in areas where trails and droppings of white-tailed deer were evident among understory vegetation. White-tailed deer are primary hosts for adult I. scapularis (31), a relationship that is in part mediated by glandular secretions from deer leg glands that influence tick host-seeking on vegetation bordering trails ( 5 ) . Thus, in areas where the blacklegged tick is endemic, such as northwestern Wisconsin, the risk for exposure to adult ticks and tick-borne pathogens on dairy farmlands (e.g., Barron County) is highest in ungrazed woodlands, but dairy cattle also risk exposure in pastures used for heifers and dry cows. Vegetation on the same farms around farmhouse yards and shelterbelt trees, as well as in cultivated croplands, supports only negligible numbers of adult blacklegged ticks. The absence of blacklegged ticks on dairy farms in eastern Wisconsin ( 9 ) reflects the spatially uneven and still developing distribution of I. scapularis in the Upper Midwest (13, 24).

TICKS AND DAIRY FARMS IN WISCONSIN

ACKNOWLEDGMENTS We thank Gayle Miller, Wyoming State Health Department, for encouragement and assistance in conducting this study. Kenneth Young, Livestock Insects Laboratory, ARS, USDA, Beltsville, Maryland provided valued assistance in surveying dairy farms. Donald Drost, Cooperative Extension, Barron County, Wisconsin willingly contributed useful local information; Charles A. Smith, Soil Conservation Service, USDA, Barron County, Wisconsin provided aerial photographs. We gratefully appreciate this support. REFERENCES 1 Barbour, A. G., and D. Fish. 1993. The biological and social phenomenon of Lyme disease. Science (Washington, DC) 260: 1610–1616. 2 Bertrand, M. R., and M. L. Wilson. 1996. Microclimatedependent survival of unfed adult Ixodes scapularis (Acari: Ixodidae) in nature: life cycle and study design implications. J. Med. Entomol. 33:619–627. 3 Burgess, E. 1989. Borrelia burgdorferi infection in Wisconsin horses and cows. Ann. New York Acad. Sci. 539:235–243. 4 Bushmich, S. L. 1994. Lyme borreliosis in domestic animals. J. Spirochetal Tick-Borne Dis. 1:24–28. 5 Carroll, M. C., H. S. Ginsberg, K. E. Hyland, and R. Hu. 1992. Distribution of Ixodes dammini (Acari: Ixodidae) in residential lawns on Prudence Island, Rhode Island. J. Med. Entomol. 29: 1052–1055. 6 Carroll, J. F., J. A. Klun, and E. T. Schmidtmann. 1995. Evidence for kairomonal influence on selection of host-ambushing sites by adult Ixodes scapularis (Acari: Ixodidae). J. Med. Entomol. 32:119–125. 7 Carroll, J. F., and E. T. Schmidtmann. 1992. Tick sweep: modification of the tick drag-flag method for sampling nymphs of the deer tick (Acari: Ixodidae). J. Med. Entomol. 29:352–355. 8 Clark, D. D. 1995. Lower temperature limits for activity of several ixodid ticks (Acari: Ixodidae): effects of body size and rate of temperature change. J. Med. Entomol. 23:449–456. 9 Clevin, T. D., E. C. Burgess, R. W. Howe, and A. I. Goldsby. 1992. Absence of Ixodes dammini (deer ticks) on Peromyscus leucopus (white-footed mice) in Brown and Door Counties, Wisconsin. Bull. Soc. Vector Ecol. 17:70–74. 10 Davis, J. P., W. L. Schell, T. E. Amundson, M. S. Godsey, Jr., A. Spielman, W. Burgdorfer, A. G. Barbour, M. LaVenture, and R. A. Kaslow. 1984. Lyme disease in Wisconsin: epidemiologic, clinical, serologic and entomologic findings. Yale J. Biol. Med. 57:685–696. 11 Falco, R. C., and D. Fish. 1988. Prevalence of Ixodes dammini near the homes of Lyme disease patients in Westchester County, New York. Am. J. Epidemiol. 127:826–830. 12 Falco, R. C., and D. Fish. 1989. Potential for exposure to tick bites in recreational parks in a Lyme disease endemic area. Am. J. Publ. Health. 79:12–15.

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13 French, J. B., Jr., W. L. Schell, J. J. Kazmierczak, and J. P. Davis. 1992. Changes in population density and distribution of Ixodes dammini (Acari: Ixodidae) in Wisconsin during the 1980s. J. Med. Entomol. 29:723–728. 14 Ji, B., and M. T. Collins. 1994. Seroepidemiologic survey of Borrelia burgdorferi exposure of dairy cattle in Wisconsin. Am. J. Vet. Res. 55:1228–1231. 15 Magnarelli, L. A., J. F. Anderson, E. Shaw, J. E. Post, and F. C. Palka. 1988. Borreliosis in equines in the northeastern United States. Am. J. Vet. Res. 49:359–362. 16 Main, A. J., A. B. Carey, M. G. Carey, and R. H. Goodwin. 1982. Immature Ixodes dammini (Acari: Ixodidae) on small mammals in Connecticut, USA. J. Med. Entomol. 19:655–664. 17 Marcus, L. C., and M. M. Patterson. 1985. Antibodies to Borrelia burgdorferi in New England horses. Am. J. Vet. Res. 46: 2570–2571. 18 Martin, L. 1965. The Physical Geography of Wisconsin. Univ. Wisconsin Press, Madison. 19 Maupin, G. O., D. Fish, J. Zultowsky, E. G. Campos, and J. Piesman. 1991. Landscape ecology of Lyme disease in a residential area of Westchester County, New York. Am. J. Epidemiol. 133:1105–1113. 20 Needham, G. R., and P. D. Teel. 1991. Off-host physiological ecology of ixodid ticks. Annu. Rev. Entomol. 36:659–681. 21 Parker, J. L., and K. K. White. 1992. Lyme borreliosis in cattle and horses: a review of the literature. Cornell Vet. 82:253–274. 22 Piesman, J., and J. S. Gray. 1994. Lyme disease/Lyme borreliosis. Page 327–350 in Ecological Dynamics of Tick-borne Zoonoses. D. Sonenshine and T. Mather, ed. Oxford Univ. Press, New York, NY. 23 Platt, K. B., M. G. Novak and W. A. Rowley. 1992. Studies on the biology of Ixodes dammini in the Upper Midwest. Ann. New York Acad. Sci. 653:72–77. 24 Riehle, M., and S. M. Paskewitz. 1996. Ixodes scapularis (Acari: Ixodidae): status and changes in prevalence and distribution in Wisconsin between 1981 and 1994 measured by deer surveillance. J. Med. Entomol. 33:933–938. 25 SAS User’s Guide: Statistics. 1982. SAS Inst., Cary, NC. 26 Schmidtmann, E. T., J. F. Carroll, and W.J.E. Potts. 1992. Hostseeking of blacklegged tick (Acari: Ixodidae) nymphs and adults at the woods-pasture interface. J. Med. Entomol. 31: 291–296. 27 Schulze, T. L., R. A. Jordan, and R. W. Hung. 1995. Suppression of subadult Ixodes scapularis (Acari: Ixodidae) following removal of leaf litter. J. Med. Entomol. 32:730–733. 28 Schwartz, B. S., and M. D. Goldstein. 1990. Lyme disease in outdoor workers: risk factors, preventive measures, and tick removal methods. Am. J. Epidemiol. 131:877–885. 29 Stafford, K. C., III, and L. A. Magnarelli. 1993. Spatial and temporal patterns of Ixodes scapularis (Acari: Ixodidae) in southeastern Connecticut. J. Med. Entomol. 30:762–771. 30 Tsai, T. S., R. E. Bailey, and P. S. Moore. 1989. National surveillance of Lyme disease 1987–1988. Connecticut Med. 53: 324–326. 31 Wilson, M. L., T. S. Litwin, T. A. Gavin, M. C. Capkanis, D. C. McLean, and A. Spielman. 1990. Host-dependent differences in feeding and reproduction of Ixodes dammini (Acari: Ixodidae). J. Med. Entomol. 27:949–954.

Journal of Dairy Science Vol. 81, No. 3, 1998