VECTOR CONTROL, PEST MANAGEMENT, RESISTANCE, REPELLENTS Integrated Use of 4-Poster Passive Topical Treatment Devices for Deer, Targeted Acaricide Applications, and Maxforce TMS Bait Boxes to Rapidly Suppress Populations of Ixodes scapularis (Acari: Ixodidae) in a Residential Landscape TERRY L. SCHULZE, 1,2,3 ROBERT A. JORDAN, 1 CHRISTOPHER J. SCHULZE, 2 SEAN P. HEALY, 4,5 MARGARET B. JAHN, 1 AND JOSEPH PIESMAN 6 J. Med. Entomol. 44(5): 830Ð839 (2007) ABSTRACT In fall 2003, we began testing an integrated control strategy to rapidly achieve and sustain reduced numbers of Ixodes scapularis Say (Acari: Ixodidae) in a residential area. We combined two host-targeted technologies in conjunction with single, barrier acaricide applications to sequentially attack each postembryonic life stage of the tick. Granular deltamethrin applied to the lawnðforest interface of participant properties resulted in 100% control of host-seeking nymphs. Nymphal and larval tick burdens on targeted small mammal hosts at treated properties were reduced by 92.7 and 95.4%, respectively, after the Þrst year (2004) of combined interventions. Over the same period, populations of host-seeking nymphs, larvae, and adults were reduced by 58.5, 24.8, and 77.8%, respectively. After interventions in 2005, tick burdens on small mammals were maintained at similar levels, whereas control of host-seeking nymphs, larvae, and adults increased to 94.3, 90.6, and 87.3%, respectively. Prospects for widespread use of these technologies to protect the publicõs health are discussed. KEY WORDS Ixodes scapularis, integrated control, 4-Poster, Maxforce, Tick Management System Conventional habitat-targeted acaricide applications have been shown to be an effective and reliable method for suppressing populations of Ixodes scapularis Say (Acari: Ixodidae), the principal vector of the causative agents of Lyme disease, human granulocytic anaplasmosis, and human babesiois in the northeastern United States (Schulze et al. 1987, 1991, 1992, 1994, 2000, 2001b; Stafford 1991; Solberg et al. 1992; Curran et al. 1993). But a recent poll of nearly 1,200 households within a New Jersey Lyme disease endemic area revealed that 25% of residents used acaricides on their properties to control ticks (T.L.S., unpublished data). Residents cited potential health effects and undesirable environmental outcomes, such as well contamination and adverse impacts to nontarget organisms, as the primary reasons for not using acaricides. However, a majority of residents claimed they 1 Freehold Area Health Department, Municipal Plaza, Schanck Rd., Freehold, NJ 07728. 2 Terry L. Schulze, Ph.D., Inc., 9 Evergreen Court, Perrineville, NJ 08535. 3 Corresponding author, e-mail: tlschulze@monmouth.com. 4 Monmouth County Mosquito Extermination Commission, Wayside Rd., Tinton Falls, NJ 07724. 5 Monmouth County Mosquito Commission Laboratory at Rutgers, McLean Laboratories, Rutgers, The State University of New Jersey, New Brunswick, NJ 08901. 6 Bacterial Diseases Branch, Division of Vector-Borne Infectious Diseases, Centers for Disease Control and Prevention, Mail Stop P-02, 3150 Rampart Rd., Fort Collins, CO 80521. would consider controlling ticks on their properties if alternatives to areawide chemical control applications were available. Host-targeted tick control may be one such alternative. Two host-targeted approaches, the 4-Poster topical treatment device and Maxforce Tick Management System (TMS) bait boxes, show promise. The 4-Poster is a passive topical treatment device that applies acaricide for the control of ticks parasitizing white-tailed deer (Odocoileus virginiana Zimmerman) (Pound et al. 1994). Deer are treated as they rub their head, neck, and ears against acaricide-laden paint rollers while feeding on bait corn, Zea mays L. Maxforce TMS bait boxes treat white-footed mice (Peromyscus leucopus RaÞnesque) and eastern chipmunks (Tamias striatus L.) as they contact a Þpronil-impregnated wick while attempting to access baits. Subadult I. scapularis are controlled for up to 42 d on hosts after a single contact with the treated wicks (Dolan et al. 2004). Both the 4-Poster and Maxforce TMS have been shown to be viable host-targeted approaches (Pound et al. 2000a, 2000b; Solberg et al. 2003; Dolan et al. 2004). However, because each targets only speciþc life stages within the 2-yr life cycle of I. scapularis, significant reduction of the tick population is not realized until months or years after deployment, and such lag-times may affect their widespread public acceptance and commercial use. For example, attempts to 0022-2585/07/0830Ð0839$04.00/0 2007 Entomological Society of America
September 2007 SCHULZE ET AL.: INTEGRATED TICK CONTROL 831 Fig. 1. Aerial photograph of the Millstone Township, NJ, study area showing locations of the three bait box deployment sites, locations of the 4-Poster devices, and the untreated control areas. control ticks by feeding deer ivermectin-treated corn were terminated prematurely because public support declined after several years of marginal results (Rand et al. 2000). This experience suggests that for new methods to achieve wide public acceptance, signiþcant tick control must be achieved more rapidly. This has important implications for host-targeted methods because their inherently delayed efþcacy results in signiþcant risk of exposure to I. scapularis nymphs well after initial deployment. To mitigate this effect, we tested an integrated control strategy that combined commercially available host-targeted tick control methods in conjunction with single, properly timed acaricide applications. Targeted barrier acaricide applications can provide rapid suppression of tick populations within high-risk areas (Schulze et al. 2000), offering reduced exposure to infected ticks until host-targeted methods become effective. We attempted to demonstrate that by sequentially attacking each postembryonic life stage with proven host-targeted and habitat-targeted approaches, populations of I. scapularis could be suppressed more rapidly and maintained at lower levels than if each method were used alone. We also evaluated the efþcacy of the Maxforce TMS when deployed at various densities. Materials and Methods Study Area. A residential area in Millstone Township, Monmouth County, NJ, served as the treatment area. Earlier surveys of this community showed I. scapularis to be abundant (Schulze and Jordan 1995; Schulze et al. 1995, 2001b, 2001c). The community included 48 single-family residences, situated on substantially (ⱖ60%) wooded properties, and three wooded undeveloped lots, all located on 66 ha of mixed hardwood forest (Fig. 1). The study area is bounded to the north by agricultural land, to the east by residential properties developed on old agricultural Þelds, to the south by wooded residential development, and to the west by an extensive wetlands corridor. The 10- to 15-m canopy consisted of chestnut oak (Quercus prinus L.) in association with red oak (Quercus rubra L.), white oak (Quercus alba L.), and American beech (Fagus grandifolia Ehrh.). The understory included seedlings and saplings of the dominant canopy species together with American holly (Ilex opaca Ait.) and sassafras [Sassafras albidum (Nutt.) Nees]. Highbush blueberry (Vaccinium corymbosum L.), lowbush blueberry (Vaccinium angustifolium Ait.), and huckleberries (Gaylussacia spp.) were the dominant shrub layer species. Similar
832 JOURNAL OF MEDICAL ENTOMOLOGY Vol. 44, no. 5 undeveloped forested habitats in nearby Assunpink Wildlife Management Area and the Borough of Roosevelt served as the untreated control sites. Community participation was solicited through multiple mailings from the Freehold Area Health Department, which recruited 38 households willing to participate in all phases of the study. Households willing to host 4-Posters, receive Maxforce TMS bait boxes and barrier acaricide applications, or both were selected from this pool. 4-Poster Deployment and Maintenance. We deployed four 4-Posters distributed across the treatment area to achieve uniform coverage and a minimum density of one 4-Poster per 20 ha. Three additional devices were deployed in a similar manner within an adjacent community located south of the study area to minimize the possibility that deer from untreated properties would be drawn into the treatment area by bait corn. The 4-Posters were established adjacent to wooded margins of the properties to facilitate routine maintenance, including the weekly or semiweekly provision of recleaned, whole kernel corn bait and recharging of acaricide applicator rollers with 2% N - (2,4-dimethylphenyl)-N-[[2,4-dimethylphenyl)imino]methyl]-N-methylmethanimidamide (amitraz) (Point-Guard, Hoechst Roussel Vet, Warren, NJ) at a weekly application rate of 40 ml of Point-Guard/roller (160 ml Point-Guard/4-Poster). A second application at the same rate was made 3Ð4 d later to all 4-Posters exhibiting weekly corn consumption of 41 kg. The maximum weekly dosage for heavily used 4-Posters during the study was 80 ml of Point-Guard/roller (320 ml of Point-Guard/4-Poster). Beginning in fall 2003, the 4-Posters were operated each fall between mid- October and mid-december and each spring between early March and late April, depending on weather conditions and observed tick activity. Operation of the 4-Posters was terminated at the conclusion of the spring 2006 adult activity period. Maxforce TMS. Maxforce TMS bait boxes (0.70% Þpronil [AI], Bayer CropScience LP, Montvale, NJ) were deployed on 13 properties at three different densities. The manufacturerõs recommendation called for the deployment of bait boxes at 10-m intervals along a perimeter at distances of 3 m from the lawnð forest interface on each participant property. Extensively wooded properties received a second row of bait boxes placed at 13 m from the lawn edge. Additional boxes were placed in landscaped areas with dense groundcover. Bait boxes were deployed as recommended on Þve contiguous properties totaling 5.8 ha. To test Maxforce TMS efþcacy at lower deployment densities, we increased the interval between bait boxes to 15 m on a second group of four contiguous properties (4.7 ha) and to 20 m on a third group of four contiguous properties (4.2 ha). The distance between rows was maintained at 10 m at all properties. In total, 350 bait boxes were distributed among the 13 properties, including 176 at the 10-m interval, 102 at the 15-m interval, and 72 at the 20-m interval densities. Bait box locations were marked with numbered ßags to facilitate retrieval and future redeployments. Bait boxes were deployed in 2004 and 2005 against nymphs between mid-may and mid-june and then retrieved and replaced for a second deployment against larvae between late July and late August during each year of the study. Bait boxes were left in place for 4 wk after deployment. We monitored bait box use by small mammals by measuring changes in box weight as an indicator of bait consumption over time. All bait boxes were numbered and weighed before deployment and again at retrieval 4 wk later using a Scout II digital scale (Ohaus Corp., Pine Brook, NJ). Twenty-Þve bait boxes from each of the three deployment density sites were weighed at weekly intervals to monitor sequential use of the bait boxes. A decline of 5.0 g in bait box weight was considered evidence of use. Barrier Acaricide Applications. Barrier acaricide applications were made to provide residents with interim protection from contact with I. scapularis nymphs until the host-targeted methods became effective. Granular deltamethrin (DeltaGard G Insecticide Granule, 0.1% [AI], Bayer Environmental Science USA LP, Montvale, NJ) was applied using a chest-mounted EV-N-Spred Commercial Crank Spreader model 3100 (Earthway Products, Bristol, IN) at a rate 0.15 kg/ha along lawnðforest edges to a distance of 8 m into the forest, as well as to any landscaped areas supporting dense groundcover vegetation. A single application was made on the 13 properties that received bait boxes timed to coincide with the May 2004 bait box deployment against nymphs. We treated an estimated 25,000 m 2 during the single barrier application, or 15% of the total area of the 13 properties. Tick Collections. To assess the effectiveness of the integrated control strategy, we monitored pre- and postdeployment burdens of subadult I. scapularis on live-captured small mammals and host-seeking larvae, nymphs, and adults from a series of plots and transects established throughout the treatment and untreated control areas. Small mammals were trapped using Sherman (7.6- by 8.9- by 30.5-cm) nonfolding box traps (H.B. Sherman, Tallahassee, FL) baited with cotton balls and rolled oats. Mammals were captured during a minimum of 400 trap-nights per trapping event at the treatment and control areas. Captured rodents were anesthetized with isoßurane or ethyl ether, examined for ticks, allowed to recover from the anesthesia, and released at the point of capture. Preintervention nymphal and larval tick burdens were obtained from single trapping events in June and August 2003. Pre- and postdeployment nymphal tick burdens were derived from paired trapping events conducted in mid-may and mid-june, respectively, in 2004Ð2006. Similarly, pre- and postdeployment larval tick burdens were obtained from paired trapping events conducted in late July and late August, respectively, in 2004Ð2005. The effects of the barrier applications of deltamethrin against nymphs were determined by monitoring numbers of host-seeking nymphs in 10 100-m 2 plots established within the treated barrier area and 10
September 2007 SCHULZE ET AL.: INTEGRATED TICK CONTROL 833 Table 1. Summary of corn consumption and Point-Guard applications, Millstone Township, NJ, 2003 2006 Deployment dates Community Wk operational Total corn consumed (kg) Mean weekly consumption (kg) Total Point-Guard applied (l) Mean weekly Point-Guard use (liters) 17 Oct.Ð12 Dec. 2003 Treatment 8 1,861 233 9.28 1.16 Adjacent 8 745 93 6.08 0.76 4 Mar.Ð22 April 2004 Treatment 7 1,729 247 8.64 1.23 Adjacent 7 773 110 5.82 0.75 5 Oct.-14 Dec. 2004 Treatment 11 2,750 250 13.76 1.25 Adjacent 11 1,347 122 8.80 0.80 7 Mar.Ð19 April 2005 Treatment 6 1,545 258 7.68 1.28 Adjacent 6 773 129 5.12 0.85 20 Oct.Ð8 Dec. 2005 Treatment 7 1,100 157 6.72 0.96 Adjacent 7 570 81 4.48 0.64 7 Mar.Ð27 April 2006 Treatment 7 1,436 205 8.32 1.19 Adjacent 7 784 112 5.44 0.78 corresponding plots placed within untreated forest. To assess the community-wide effects of the combined treatments, we monitored numbers of hostseeking subadult I. scapularis on 50 plots established across the 13 properties receiving bait boxes. Each of these 100-m 2 plots was placed in areas with patchy shrub layers to facilitate collection of subadult ticks. A similar number of 100-m transects was established nearby in areas with denser shrub layers more likely to yield adult ticks (Schulze et al. 1997). All stages of questing I. scapularis were collected using a combination of walking surveys and drag sampling (Ginsberg and Ewing 1989) to minimize biases of the individual sampling methods and those resulting from differences in questing behavior exhibited by developmental stage (Schulze et al. 1997). Tick drags constructed of a 1-m 2 piece of light-colored corduroy fastened to a wooden dowel (1 cm in diameter) along the leading edge, were worked along side of each investigator by means of a 2-m rope handle attached to the ends of the wooden dowel. Dragging and walking surveys were conducted simultaneously by the same individuals between 0800 and 1200 hours to minimize any investigator or temporal bias (Schulze et al. 1997, 2001a; Schulze and Jordan 2003). Plots or transects were sampled once during each of the peak activity periods of I. scapularis larvae, nymphs, and adults (Schulze et al. 1986). Adults were sampled in late OctoberÐearly November 2002Ð2005, whereas nymphs and larvae were sampled between mid-may and mid-june 2003Ð2006 and in August 2003Ð2005, respectively. Ticks adhering to investigatorsõ clothing and drags were removed at 20-m intervals (Schulze and Jordan 2001), identiþed, and returned to the plot or transect. Statistical Analysis. Pre- and postdeployment tick burdens were compared using MannÐWhitney U tests. Differences in questing I. scapularis and numbers of subadult ticks infesting captured small mammals among the different deployment interval properties and the untreated control areas were compared using analysis of variance (ANOVA) or nonparametric equivalent (Sokal and Rohlf 1981). A modiþcation of HendersonÕs method was used to calculate percentage control of ticks: % control 100 (T/U 100), where T and U are the mean after treatment/mean before treatment in treated plots and untreated plots, respectively (Henderson and Tilton 1955, Mount et al. 1976). Results 4-Poster Deployment and Maintenance. The dates of deployment, amount of corn consumed, and amount of Point-Guard applied during the study are summarized in Table 1. Mean weekly corn consumption, and thus Point-Guard use, increased slightly during the initial four deployments. However, a substantial oak mast in fall 2005 resulted in a moderate decline of 4-Poster use, as measured by corn consumption. Maxforce TMS. During the 2004 deployment against nymphs, 45.3% of 75 bait boxes monitored weekly demonstrated use by small mammals by the end of the Þrst week (Table 2). Bait box use increased to 68.0 and 84.0% during week 2 and 3, respectively. However, at the conclusion of the fourth week, 12 of 25 (48.0%) boxes deployed at the 10-m interval properties had been substantially damaged by eastern gray squirrels (Sciurus carolinensis Gmelin), which had consumed much of the remaining baits. Squirrels damaged only two of the remaining 50 (4.0%) monitored boxes. At the end of the deployment against nymphs, squirrels had damaged 130 of 349 (37.3%) retrieved boxes, whereas 215 of 219 (98.2%) of the remaining intact boxes demonstrated some use by small mammals. During the subsequent deployment against larvae, box use by target small mammals exceeded 85% of monitored boxes within 2 wk at two of the treated sites, indicating more rapid acceptance during the second deployment. At the conclusion of the larval deployment, we found that 127 of 350 (36.4%) bait boxes had been damaged by squirrels, with 202 of the remaining 223 (90.6%) boxes showing use by target small mammals. During the 2005 deployment against nymphs, acceptance of the bait boxes by target small mammals was rapid, with 73.1% of boxes used within 1 wk (Table 3). Against larvae, 93% of boxes demonstrated use within 2 wk. We found an increase in squirrel depredation during 2005, but damage was restricted to one bait chamber in 41.9 and 55.5% of bait boxes during the deployments against nymphs and larvae, respectively.
834 JOURNAL OF MEDICAL ENTOMOLOGY Vol. 44, no. 5 Table 2. Summary of weekly small mammal use (mean weekly weight changes; grams) and squirrel damage of Maxforce TMS bait boxes deployed at three intervals within the treatment area, Millstone Township, NJ, May August 2004 Deployment interval 10 m 15 m 20 m Box use Damage Box use Damage Box use Damage Deployment against nymphs, MayÐJune Week 1 13/25 (52%) (24.1 9.4) 0 13/25 (52%) (3.6 1.4) 0 8/25 (32%) (1.2 2.3) 0 Week 2 19/25 (76%) (36.1 9.0) 0 18/25 (72%) (38.8 12.2) 0 14/25 (56%) (9.5 3.1) 0 Week 3 21/25 (84%) (59.4 13.8) 0 19/25 (76%) (44.5 11.4) 0 21/25 (84%) (61.3 11.7) 0 Week 4 13/13 (100%) (71.6 9.9) 12/25 (48%) 23/25 (92%) (86.2 12.9) 0 21/23 (91.3%) (79.9 11.7) 2/25 (8%) Deployment against larvae, JulyÐAug. Week 1 11/22 (50%) (31.2 16.3) 3 (12%) 13/25 (52%) (21.5 8.9) 0 14/23 (61%) (28.2 11.8) 2 (8%) Week 2 12/13 (92%) (85.5 19.8) 12 (48%) 20/25 (80%) (41.1 11.4) 0 10/11 (91%) (89.4 24.2) 14 (56%) Week 3 12/12 (100%) (48.3 13.3) 13 (52%) 23/25 (92%) (34.4 11.2) 0 8/9 (88.9%) (38.3 21.0) 16 (64%) Week 4 12/12 (100%) (83.8 17.6) 13 (52%) 21/24 (88%) (27.8 10.1) 1 (4%) 9/9 (100%) (24.8 23.1) 16 (64%) Table 3. Summary of weekly small mammal use (mean weekly wt changes; grams) and squirrel damage of Maxforce TMS bait boxes deployed at three intervals within the treatment area, Millstone Township, NJ, May August 2005 Deployment interval 10 m 15 m 20 m Box use Damage Box use Damage Box use Damage Deployment against nymphs, MayÐJune Week 1 10/15 (50%) (32.5 19.7) 10 (40%) 16/23 (70%) (10.1 2.7) 2 (8%) 12/14 (86%) (15.6 6.0) 11 (44%) Week 2 3/5 (60%) (120.1 58.2) 20 (80%) 15/21 (71%) (33.6 13.6) 4 (16%) 3/3 (100%) (87.4 46.1) 22 (88%) Week 3 2/2 (100%) (196.8 1.7) 23 (92%) 6/6 (100%) (191.4 8.4) 19 (76%) 1/1 (100%) (200.1) 24 (96%) Week 4 2/2 (100%) 23 (92%) 6/6 (100%) (191.4 8.4) 19 (76%) 1/1 (100%) (200.1) 24 (96%) Deployment against larvae, JulyÐAug. Week 1 17/22 (77%) (114.5 19.7) 3 (12%) 18/23 (78%) (21.1 7.1) 2 (8%) 6/8 (75%) (78.5 31.0) 17 (68%) Week 2 19/21 (90%) (135.4 17.2) 4 (16%) 19/20 (95%) (35.2 11.4) 5 (20%) 2/2 (100%) (171.6 29.4) 23 (92%) Week 3 13/13 (100%) (199.6 1.4) 12 (48%) 11/11 (100%) (184.0 8.7) 14 (56%) 2/2 (100%) (198.6 2.3) 23 (92%) Week 4 13/13 (100%) (199.6 1.4) 12 (48%) 11/11 (100%) (194.9 1.5) 14 (56%) 2/2 (100%) (198.6 2.3) 23 (92%)
September 2007 SCHULZE ET AL.: INTEGRATED TICK CONTROL 835 Table 4. Number of questing I. scapularis nymphs (mean SE) collected at treatment and control plots (n 10 each) in the Millstone Township, NJ, treatment area before and after deltamethrin application, May 2004 Plots (n) Plot location Treatment Control MannÐWhitney test Pretreatment 10 2.4 0.5 4.1 0.4 U (10, 10) 21.5; P 0.03 Posttreatment 10 0 6.3 0.8 (100) a a Percentage of control (modiþed HendersonÕs equation). Bait box use by target small mammals increased over time, indicating more rapid acceptance of the boxes with each subsequent deployment. Squirrel damage was not observed until week 4 of the 2004 deployment against nymphs, was not uniform among properties, and it occurred more rapidly as the study progressed. However, squirrel damage was restricted to one bait chamber in 50% of the damaged bait boxes, suggesting that small mammals continued to visit the bait boxes, thereby providing some control of subadult ticks throughout the 4-wk deployments. Barrier Acaricide Applications. Preapplication surveys of treatment and control plots and the application of granular deltamethrin were conducted on 14 and 15 May 2004, respectively. Postapplication sampling of the same plots on 27 May 2004 showed that the application resulted in 100% control of I. scapularis nymphs within the forestðlawn margins of the treated properties (Table 4). Tick Burdens. We trapped small mammals to assess preintervention nymphal and larval burdens during mid-may and late July 2003, respectively (Tables 5 and 6). Mean nymphal burdens for all treatment sites combined (2.2 0.5 nymphs per mammal) did not differ signiþcantly from burdens at the control area (1.5 0.4 nymphs per mammal) (MannÐWhitney U [29, 25] 331.5; P 0.57). Mean larval burdens at the treatment areas (2.9 0.4 larvae per mammal) also did not differ from that in the control area (3.0 0.6 larvae per mammal) (U [52, 32] 812.0; P 0.85). Chipmunks dominated captures at the treatment area, whereas small mammal captures at the control area were made up primarily of white-footed mice. This pattern repeated in the remaining 2 yr of the study. Incidental captures ( 2% of total captures) included northern short-tailed shrews (Blarina brevicauda Say), meadow voles (Microtus pennsylvanicus Ord), and Virginia opossum (Didelphis virginiana L.). Before bait box deployment in 2004, mean nymphal tick burdens in all treatment areas did not differ from mean tick burdens at the control area (Table 5). After deployment, the mean tick burden in the treated areas was reduced by an order of magnitude, but it did not differ among interval treatments. Consequently, we pooled the treatment properties for subsequent analysis. Mean nymphal burden at the control site also declined signiþcantly, but it remained signiþcantly higher than at the treatment area. The mean tick burden for all treated properties declined from 5.4 0.5 nymphs per mammal to 0.3 0.1 nymphs per mammal (U [37, 80] 51.0; P 0.01), representing a 92.7% level of control relative to the untreated area (Table 5). Mean nymphal tick burdens remained signiþcantly reduced in the treated areas before bait box deployment in 2005, whereas tick burdens in the control area were comparable with that observed in the previous year. In 2006, mean nymphal tick burdens in the control area were statistically equivalent to those observed in previous years, whereas tick burdens in the treatment areas remained signiþcantly reduced. At the conclusion of the study, mean nymphal tick burden at all treated properties were reduced 98.3% compared with the untreated control. Pretreatment mean larval tick burdens at the treated area were signiþcantly lower than at the control area (Table 6). After bait box deployment in 2004, mean tick burdens at the treated areas were reduced by more than an order of magnitude. The postdeployment declines in tick burdens were statistically signiþcant for all properties, but they did not differ between deployment intervals. As with the nymphal burden data, we pooled the treatment properties for subsequent analysis. Control area larval burdens declined slightly to 6.8 0.6 larvae per mammal, but they remained signiþcantly higher than the treatment area tick burdens. The mean larval burden for all treated Table 5. Nymphal I. scapularis burdens (mean SE) on live-captured small mammals at Millstone Township, NJ, treatment and control sites before and after intervention, 2003 2006 2003 2004 2005 Area Preintervention Before a After Before After 2006 n Burden n Burden n Burden n Burden n Burden n Burden Control 25 1.5 0.4 15 6.1 0.8 22 2.8 0.5 14 4.1 0.8 22 3.5 0.7 31 4.1 0.5 10 m 17 0.8 0.4 18 4.9 0.7 38 0.3 0.1 (79.9%) b 26 0.2 0.1 15 0.3 0.3 (83.9%) 26 0.1 0.1 (95.4%) 15 m 7 4.3 1.4 9 4.4 0.7 19 0.4 0.2 (95.0%) 11 0.5 0.3 (95.0%) 13 0.5 0.2 31 0.2 0.1 (98.3%) 20 m 5 3.8 1.3 10 5.1 0.8 23 0.3 0.1 (95.7%) 11 0.2 0.1 (97.7%) 12 0.2 0.1 19 0.3 0.1 (98.1%) All treated 29 2.2 0.5 37 5.4 0.5 80 0.3 0.1 (92.7%) 48 0.3 0.1 40 0.4 0.1 (92.2%) 76 0.1 0.1 (98.3%) a Data for 2004Ð2005 represent burdens before and after bait box deployment in both years. b Represents percentage of control (modiþed HendersonÕs equation).
836 JOURNAL OF MEDICAL ENTOMOLOGY Vol. 44, no. 5 Table 6. Larval I. scapularis burdens (mean SE) on live-captured small mammals at Millstone Township, NJ, treatment and control sites before and after intervention, 2003 2006 2003 2004 2005 Area Preintervention Before a After Before After n Burden n Burden n Burden n Burden n Burden Control 32 3.0 0.6 20 7.6 0.9 30 6.8 0.6 29 4.4 0.7 34 5.9 0.9 10 m 14 2.8 0.6 48 1.6 0.2 40 0.4 0.2 (93.7%) b 19 0.8 0.6 15 0.1 0.1 (98.2%) 15 m 26 3.5 0.7 15 4.7 2.5 21 0.5 0.1 (93.7%) 21 1.3 0.5 15 0.1 0.1 (98.5%) 20 m 12 1.9 0.4 13 1.1 0.3 16 0.4 0.2 (90.7%) 19 0.8 0.2 15 0 (100.0%) All treated 52 2.9 0.4 76 4.6 1.8 77 0.3 0.1 (95.4%) 59 1.0 0.3 45 0.04 0.03 (92.9%) a Data for 2004Ð2005 represent burdens before and after bait box deployment in both years. b Represents percentage of control (modiþed HendersonÕs equation). properties was signiþcantly reduced from 4.6 1.8 larvae per mammal to 0.3 0.1 larva per mammal (U [76, 77] 1191.0; P 0.01), representing a 95.4% level of control (Table 6). In 2005, pretreatment mean larval tick burdens at the treated areas remained signiþcantly lower than those observed before bait box deployment in 2004, whereas control area burdens did not differ from the previous year. After bait box deployment, mean larval burdens were further reduced at all treated areas from 1.0 0.3 larva per mammal to 0.04 0.03 larva per mammal (U [59, 45] 840.5; P 0.01), representing an overall level of 92.9% control. Host-Seeking Ticks 2003 2006. The 2003 preintervention numbers of host-seeking I. scapularis nymphs was signiþcantly greater at the treatment area than at the control area (MannÐWhitney U [20, 20] 21.5; P 0.03), whereas larval abundance did not differ between areas (U [20, 20] 27.5; P 0.08). In contrast, fall abundance of questing adults was greater at the control area (U [20, 20] 21.0; P 0.03). Numbers of both host-seeking I. scapularis nymphs and larvae declined signiþcantly in the treatment areas between 2003 and 2006 (Table 7). Numbers of hostseeking nymphs did not differ signiþcantly in the control area, whereas larval numbers increased signiþcantly in the control plots. Declines in host-seeking subadults represented 94.3% control of nymphs over 3 yr and 90.6% control of larvae over 2 yr. Similarly, numbers of host-seeking adults in the fall showed signiþcant declines in all years, representing an 87.3% level of control. Discussion As measured by consumption of corn, deer readily acclimated to use of the 4-Poster devices during the initial and subsequent deployments. Although corn consumption declined somewhat in response to heavy oak mast in fall 2005, 4-Poster use continued, so that treatment of deer during the fall activity periods of I. scapularis adults was not interrupted and control pressure on adult ticks was continuous. In both 2004 and 2005, 98% of intact Maxforce TMS bait boxes deployed against nymphs and 90% of boxes deployed against larvae exhibited a reduction in weight after 4-wk deployments. Weekly weighing of 25 bait boxes from each of the deployment density sites showed a progressive increase in use over time in both years, demonstrating reasonable longevity of bait boxes, even in chipmunk-dominated areas where we had expected baits to be consumed more rapidly. Previous research has demonstrated the effectiveness of the 4-Posters and Maxforce TMS when used individually. Deployment of 4-Posters treated with 10% permethrin within in a 2.55-km 2 fenced facility over a 3-yr period resulted in 91Ð100% reduction of all stages of host-seeking I. scapularis ticks from sampled plots and 70Ð95% reduction of nymphal and larval tick burdens on mice (Solberg et al. 2003). A larger study Table 7. 2003 2006 Summary of questing I. scapularis (mean SE; n 20) at the Millstone Township, NJ, treatment and control study sites, Yr Location Preintervention Postintervention KruskalÐWallis test 2003 2004 2005 2006 Nymphs Control 1.7 0.5 2.0 0.5 3.4 0.8 10.1 2.1a H (2, 60) 15.22; P 0.51 Treatment 4.1 0.4a,b 2.0 0.6a,b,c (58.5%) a 1.1 0.4b,c (86.6%) 1.4 0.4b,c (94.3%) H (2, 60) 26.46; P 0.01 Larvae Control 68.8 32.5a 44.9 22.0a 197.4 40.1b H (2, 60) 15.22; P 0.51 Treatment 124.3 34.2a 61.0 14.9b (24.8%) 33.6 10.1c (90.6%) H (3, 60) 19.32; P 0.01 Adults Control 6.0 1.1 6.9 2.6 7.9 1.7 H (2, 60) 0.17; P 0.92 Treatment 3.0 0.5a 1.0 0.6b (77.8%) 0.5 0.2b (87.3%) H (2, 60) 16.80; P 0.01 Means in the same row followed by the same letter are not signiþcantly different (TukeyÕs honestly signiþcant difference test). a Represents percentage of control (modiþed HendersonÕs equation).
September 2007 SCHULZE ET AL.: INTEGRATED TICK CONTROL 837 involving 25 4-Posters deployed within a 5.2-km 2 area located in the center of a 20-km 2 fenced facility yielded 82.7, 77.3, and 67.2Ð86.7% control of hostseeking I. scapularis larvae, nymphs, and adults, respectively, by the conclusion of the 5-yr study (T.L.S. et al., unpublished data). In a 3-yr study of prototype bait boxes conducted on a 15.3-km 2 coastal island, nymphal and larval I. scapularis burdens on mice were reduced by 68 and 84%, respectively (Dolan et al. 2004). These reductions led to declines in the abundance of questing I. scapularis adults (77%) and nymphs ( 50%). In the current study, we achieved 92% reduction in nymphal and larval tick burdens on small mammals during the Þrst year and 94.3, 90.6, and 87.3% control of host-seeking nymphs, larvae, and fall adults, respectively, after 2 yr. Reduction in host-seeking ticks in the treated area seems to have resulted in a decline in both the number of animals infested and the number of ticks per infested animal. Integrated management of vector tick populations remains in its infancy, but computer models have suggested that combinations of tick management methods offer greater potential for population reductions than single methods alone (for review, see Stafford and Kitron 2002). Our results show that the combined use of two novel host-targeted control approaches with limited acaricide applications provided superior tick control, and this method achieved these greater levels of control much more rapidly than when these methods were previously used alone. Although we are unable to determine the relative contribution of each method to the overall levels of control, we think that the effect of the 4-Posters was uniform across all study properties. Therefore, it seems that we also achieved substantial control at all bait box deployment densities, suggesting that the number of bait boxes deployed could be reduced to half of the manufacturerõs recommendation without affecting efþcacy. Ironically, the squirrel damage problem may have shed some light on the efþcacy of bait boxes when deployed at lower densities. As the number of squirrel-compromised boxes increased over time, the effective deployment density declined at all sites. Therefore, the observed levels of control were achieved at much lower bait box densities than originally planned. This suggests that either there were a sufþcient number of bait boxes deployed to absorb the losses due to squirrel damage, apparently without affecting efþcacy; that many target small mammals were treated before signiþcant depredation occurred; or that small mammals continued to visit partially damaged bait boxes. This may help explain the signiþcant declines in tick burdens and host-seeking ticks in the treated areas despite squirrel damage to boxes. These data show that high levels of control can be achieved at lower deployment densities, thereby signiþcantly lowering the cost. We also think that by concentrating bait boxes in areas most likely to be used by foraging small mammals as opposed to deployments using some set pattern or interval, efþcacy can be achieved with fewer units. Although the combined use of the 4-Poster and Maxforce TMS resulted in excellent control of I. scapularis in an abbreviated time frame, the widespread use of these particular host-targeted methods may be hampered by regulatory and economic constraints. Shortly after the start of this study, 10% permethrin (4-Poster Tickicide, Y-Tex Corp., Cody, WY), a restricted-use pesticide that can only be applied by licensed Þrms or individuals, became the only acaricide registered for use on the 4-Poster. Furthermore, the product labeling requires that a 4-Poster be placed at least 91.4 m (100 yards) from a residence or other place where unsupervised children might be present. This restriction will limit the residential use of 4-Posters to communities with low-density zoning requirements, estimated to be a minimum of 1.0 ha per dwelling (T.L.S. et al., unpublished data) and impose higher labor costs necessitated by transportation of bait corn the required distances. We observed no vandalism or incidents of children interacting with any of the 4-Posters, suggesting that the 91.4-m label restriction may be overly cautious and worthy of reconsideration. The widespread use of 4-Posters may be further complicated by regulatory prohibitions against feeding deer in some states and concerns over the potential spread of wildlife diseases. Also, use of the 4-Poster is perceived to be more expensive than conventional acaricide applications. After initial purchase of the 4-Poster and associated equipment and supplies, routine operational costs were estimated to be between $20 and $100 per unit per wk, depending on the number of visits, number of units serviced, accessibility, and travel (Carroll and Kramer 2003; Solberg et al. 2003; T.L.S. et al., unpublished data). However, possibly mitigating the apparently higher costs associated with 4-Poster deployments compared with conventional acaricide applications is the fact that a single unit will provide tick control within an area 20 ha (Solberg et al. 2003). Even at the highest estimated rate at $100 per unit per wk, a typical 8-wk deployment of a 4-poster would cost $40 per ha, whereas a recent ground application of acaricide cost $350 per ha, or nearly nine times the cost of the 4-Poster (T.L.S., unpublished data). Acaricide applications are con- Þned to the targeted hosts, rather than widely broadcast, thereby limiting potential adverse environmental effects. Solberg et al. (2003) estimated a 63- to 157-fold reduction in acaricide use in 4-Posters compared with typical areawide (habitat-targeted) applications. Current product labeling and perceived high cost of the 4-Poster will likely limit wide adoption of this methodology in the residential market, however its ability to control ticks over wide areas, while substantially reducing the amount of acaricide used, makes it a potentially valuable tool in some situations. Squirrel damage to Maxforce TMS bait boxes may also pose regulatory problems. Many of the damaged bait boxes had their acaricide-impregnated wicks removed from or exposed within the box, compromising their required childproof status. Also, the majority of bait box damage rendered the product labeling illegible. During the 2004 deploy-
838 JOURNAL OF MEDICAL ENTOMOLOGY Vol. 44, no. 5 ment against nymphs, all signiþcant squirrel damage was conþned to one treated area. However, extensive damage was observed at most properties during subsequent deployments, suggesting that bait box destruction will likely expand within a community once squirrels learn the ability to access boxes. The cost of the bait boxes may also curb widespread acceptance of this technology. At the suggested retail price of $40.00 per unit, each deployment of 350 bait boxes in our study would cost $14,000 ( $1,075 per property) or an average annual fee of $2,150 per property for both deployments. However, we think that increasing the interval between boxes (decreasing deployment density) may substantially reduce the annual cost. Squirrel depredation, although substantial in this study, seemed to have a minimal effect on overall efþcacy at all deployment densities. Some modiþcations to the bait box design are required to minimize squirrel damage and avoid regulatory and potential customer relations issues. However, bait boxes seem to offer an effective means of controlling ticks in residential settings. By sequentially attacking each postembryonic stage of I. scapularis with host-targeted technologies, we have demonstrated that local tick populations can be rapidly suppressed, while dramatically reducing the amount of acaricides introduced into the environment. Although additional research is needed to overcome some technical and regulatory issues, such an integrated approach offers an alternative for health ofþcials, managers of public lands, and the pest control community in response to the mounting threat of tick-borne diseases. Acknowledgments We thank the Millstone Township Committee and the participating residents for their support. 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