TY - JOUR
AU - Paskewitz, S M
AB - Abstract The blacklegged tick, Ixodes scapularis Say, is the primary vector of several tick-borne pathogens, including those causing Lyme disease and babesiosis, in the eastern United States and active collection methods for this species include dragging or wild animal sampling. Nest boxes targeting mice may be an alternative strategy for the surveillance and collection of immature I. scapularis feeding on these hosts and would be much safer for animals compared to small mammal trapping. We constructed double-walled insulated nest boxes (DWINs) with collection tubes mounted below the nesting chamber and deployed eleven in southern Wisconsin from June until September of 2020. The DWINs were occupied by Peromyscus spp. and birds (wren species, Troglodytidae family). We collected 192 ticks from collection tubes, all of which were identified as either I. scapularis (95%) or Dermacentor variabilis Say (Acari: Ixodidae) (5%). Only 12% (21/182) and 20% (2/10) of I. scapularis and D. variabilis were blood-fed, respectively. The high proportion of unfed ticks found in collection tubes may be due to grooming by hosts inside the nest boxes. Alternatively, immature ticks may have climbed trees and entered the DWIN seeking a host. Results suggest that nest boxes could be a tool for finding ticks in areas of low density or at the leading edge of invasion, when small mammal trapping or drag sampling is not feasible. Lyme disease, surveillance, Peromyscus, nests, ticks Lyme disease is the most commonly reported vector-borne disease in the United States and the causative pathogen is transmitted by the blacklegged tick, Ixodes scapularis Say, in the eastern United States (Burgdorfer et al. 1982, Rosenberg et al. 2018). To assess the disease risk posed by ticks, surveillance efforts by many public health agencies focus on identifying the occurrence, distribution, and abundance of I. scapularis (Eisen and Paddock 2020, Mader et al. 2020). However, the institutional capacity of public health and vector control agencies to implement labor-intensive active sampling for ticks (e.g., tick dragging and wild animal sampling) is limited (Mader et al. 2020) and this constrains effective surveillance. Nest boxes, targeting mice, represent an alternative method for the collection of immature I. scapularis. Mice belonging to the genus Peromyscus are considered one of the most important reservoir hosts for tick-borne pathogens (Levine et al. 1985). Laboratory studies suggest that a high proportion of immature I. scapularis detach from mice during diurnal periods when the animals are expected to be in nests (Mather and Spielman 1986, Matuschka et al. 1991) and immature I. scapularis have been collected from the nests of wild mice (Larson et al. 2020). In addition, Drummond (1957) and Jackson and DeFoliart (1975) described collecting Ixodes dentatus Marx (Acari: Ixodidae) and Dermacentor variabilis Say (Acari: Ixodidae) in nest boxes that they developed for mice. Here we tested the concept of using nest boxes to collect immature I. scapularis in southern Wisconsin. Materials and Methods Nest Box Design We designed a double-walled insulated nest box (DWIN), which can be constructed using standard home improvement materials purchased at a local hardware store for ~$20 USD per DWIN. Nest boxes consisted of two vertical PVC cylinders with an entry hole, a nesting chamber, a funnel, and a tick collection vessel. For further details on construction, see Suppl text A (Online only). Briefly, we used PVC tubes as inner (7.6 cm diameter) and outer (10.1 cm diameter) walls (~25 and 30–35 cm in height). The space between the two tubes was filled with Great Stuff insulating spray foam (DuPont, Wilmington, DE) to affix the two cylinders and insulate the nest boxes. A removable PVC cap was placed on the top of the nest box and a plastic grate (7.6 cm, sold as a ‘PVC pipe strainer’) was fitted to the bottom of the inner tube to serve as the support for mouse nests. An entry hole (~3.5 cm) was drilled through the two tubes and insulation material approximately 9 cm above the grate. Below the grate, a funnel was mounted to direct debris, ticks, and insects into a collection tube. The funnel was secured to a 10.1 cm to 5.1 cm PVC coupling with a 5.1 cm PVC plug inserted, which served as the bottom of the nest box. We used 50 ml plastic tubes (Falcon, Corning Life Sciences, Tewksbury, MA) as collection containers and a hole was drilled in both the cap of the 50 ml tube and the plug at the same diameter as the funnel before the cap of the 50 ml tube was permanently glued to the plug using Marine Adhesive Sealant 5200 (3M, St. Paul, MN). The removable funnel and endcap were connected to the outside vertical tube and further secured with duct tape. Nest Box Deployment Eleven DWINs were deployed on 20 May 2020 at a privately owned property in Moscow, Iowa County, Wisconsin. The property contained a mixture of red pine stands (Pinus resinosa), oak-dominated woodlots (Quercus spp.), and abandoned agricultural fields. DWINs were attached to trees at least 40 m apart near-field edges or along trails where they could be easily located and accessed. Metal wire was used to hang DWINs from tree limbs so that the entry hole was approximately 1.25−1.75 m above the ground and DWINs were secured to trees with the entry hole facing toward the tree using a bungee cord. A handful of cotton batting and strips of wool yarn were placed in each DWIN for bedding material. This work was approved by the University of Wisconsin – Madison Institutional Animal Care and Use Committee (IACUC Protocol: A005400-R01-A01). Prior to using DWINs, we recommend that researchers contact their biosafety office to identify potential rodent-borne hazards (e.g., hantaviruses) and consult with their institutional animal care and use office to ensure all protocols, including the use of artificial nest boxes, comply with animal safety guidelines. For guidance on wild mammal protocols, see Sikes et al. (2016). Occupancy Assessment DWINs were checked on June 26, July 22, August 21 and 24 September 2020. During each monthly check, a visual inspection was conducted to determine whether occupancy could be detected. The presumed last occupant of each DWIN was noted based on the presence of the animals themselves, or observations of feces, feathers, eggs, or the construction of nests. In our study area, arboreal nest building mammals that could fit through DWIN openings are likely limited to Peromyscus spp. Cotton and wool bedding material were replaced when they appeared wet or had been removed by animals; otherwise, nests were left intact. Arthropod Collection and Tick Identification A solution of 50% propylene glycol (600 ml) containing a drop of dish soap was used as the collection medium and approximately 35 ml was placed in each collection tube. Collection tubes were replaced during the monthly visit. The contents of each tube were sorted and assessed under a dissecting microscope. Ticks were collected and stored in 70% ethanol until further identification. All ticks were identified using keys established by Clifford et al. (1961) and were classified as blood-fed or flat (unfed). Results DWINs were occupied by Peromyscus species (likely P. leucopus) and birds (wren species were observed in nest boxes, Troglodytidae family). Monthly Peromyscus occupancy ranged from 4 in July to all 11 DWINs in September (Fig. 2). On eight separate occasions, mice were observed in nest boxes during visual inspections (Table 1, Fig. 1D). All other presumed Peromyscus occupancies were based on the presence of feces or the construction of nests. Birds or their nests were observed in three DWINs in June, four in July, and one in August (Fig. 2). Table 1. Summary of nest boxes with at least one tick Month . Nest box identifier . I. scapularis . . D. variablis . Bird sign . . Mice sign . . . . . Larvae . Nymphs . Larvae . Bird . Nest . Mice . Feces or nest . Stained fluid . June 3 36 1 1 X X X 4 2 1 0 X X 5 1 0 3 X X 11 7 0 4 X X July 3 4 0 1 X X 5 1 0 0 X 7 1 0 0 X 8 1 0 0 X Aug 1 1 0 0 X X 10 15 0 1 X X 11 31 0 0 X X Sept 2 3 0 0 X X 5 7 0 0 X X 6 4 0 0 X X 7 1 0 0 X X 8 2 0 0 X X 9 4 0 0 X X X 10 38 0 0 X X 11 21 0 0 X X X Month . Nest box identifier . I. scapularis . . D. variablis . Bird sign . . Mice sign . . . . . Larvae . Nymphs . Larvae . Bird . Nest . Mice . Feces or nest . Stained fluid . June 3 36 1 1 X X X 4 2 1 0 X X 5 1 0 3 X X 11 7 0 4 X X July 3 4 0 1 X X 5 1 0 0 X 7 1 0 0 X 8 1 0 0 X Aug 1 1 0 0 X X 10 15 0 1 X X 11 31 0 0 X X Sept 2 3 0 0 X X 5 7 0 0 X X 6 4 0 0 X X 7 1 0 0 X X 8 2 0 0 X X 9 4 0 0 X X X 10 38 0 0 X X 11 21 0 0 X X X Month represents the month in which the DWIN was checked. Nest box: the number assigned to each unique DWIN (1–11). The presence of animal signs (bird and mice) are marked (X). Bird sign included bird sightings or the presence of a nest/eggs. Occupancy of mice was determined by animal sightings, the presence of feces or nests, and discoloration of collection medium (stained fluid). Next boxes with more than 10 ticks are bolded. Open in new tab Table 1. Summary of nest boxes with at least one tick Month . Nest box identifier . I. scapularis . . D. variablis . Bird sign . . Mice sign . . . . . Larvae . Nymphs . Larvae . Bird . Nest . Mice . Feces or nest . Stained fluid . June 3 36 1 1 X X X 4 2 1 0 X X 5 1 0 3 X X 11 7 0 4 X X July 3 4 0 1 X X 5 1 0 0 X 7 1 0 0 X 8 1 0 0 X Aug 1 1 0 0 X X 10 15 0 1 X X 11 31 0 0 X X Sept 2 3 0 0 X X 5 7 0 0 X X 6 4 0 0 X X 7 1 0 0 X X 8 2 0 0 X X 9 4 0 0 X X X 10 38 0 0 X X 11 21 0 0 X X X Month . Nest box identifier . I. scapularis . . D. variablis . Bird sign . . Mice sign . . . . . Larvae . Nymphs . Larvae . Bird . Nest . Mice . Feces or nest . Stained fluid . June 3 36 1 1 X X X 4 2 1 0 X X 5 1 0 3 X X 11 7 0 4 X X July 3 4 0 1 X X 5 1 0 0 X 7 1 0 0 X 8 1 0 0 X Aug 1 1 0 0 X X 10 15 0 1 X X 11 31 0 0 X X Sept 2 3 0 0 X X 5 7 0 0 X X 6 4 0 0 X X 7 1 0 0 X X 8 2 0 0 X X 9 4 0 0 X X X 10 38 0 0 X X 11 21 0 0 X X X Month represents the month in which the DWIN was checked. Nest box: the number assigned to each unique DWIN (1–11). The presence of animal signs (bird and mice) are marked (X). Bird sign included bird sightings or the presence of a nest/eggs. Occupancy of mice was determined by animal sightings, the presence of feces or nests, and discoloration of collection medium (stained fluid). Next boxes with more than 10 ticks are bolded. Open in new tab Figure 1: Open in new tabDownload slide Double-walled insulated nestbox (DWIN) construction schematic (A) and mounted to a tree (B) with the entry hole facing toward the tree. Within the DWIN a PVC grate serves as the bottom of the nesting chamber for mice (C, picture taken at research animal research center—University of –Wisconsin – Madison), upon deployment cotton and wool are placed on the grate as nesting material. In two DWINs, mouse families were present during a monthly occupancy check (D). Figure 1: Open in new tabDownload slide Double-walled insulated nestbox (DWIN) construction schematic (A) and mounted to a tree (B) with the entry hole facing toward the tree. Within the DWIN a PVC grate serves as the bottom of the nesting chamber for mice (C, picture taken at research animal research center—University of –Wisconsin – Madison), upon deployment cotton and wool are placed on the grate as nesting material. In two DWINs, mouse families were present during a monthly occupancy check (D). Figure 2: Open in new tabDownload slide Animal occupancy and tick prevalence of nest boxes over a 4-month period. For each nest box and month, the last suspected occupant is depicted (mouse or bird). Blank positions represent nest boxes in which occupancy was not suspected. Nest boxes in which at least one tick was collected are annotated with gray circles. Figure 2: Open in new tabDownload slide Animal occupancy and tick prevalence of nest boxes over a 4-month period. For each nest box and month, the last suspected occupant is depicted (mouse or bird). Blank positions represent nest boxes in which occupancy was not suspected. Nest boxes in which at least one tick was collected are annotated with gray circles. Seventeen of the 28 monthly mice occupancies (60%) yielded ticks and two of the eight (25%) DWINs most recently occupied by birds contained immature I. scapularis in the collection medium (Fig. 2). In total, 192 ticks were collected during 19 of 44 monthly checks from all 11 DWINs. The number of ticks collected per infested mouse nest ranged from 1 to 38, and 3 and 5 ticks were collected from the two productive bird nests (Table 1 and Fig. 2). All ticks were identified as either immature I. scapularis (95%) or D. variabilis larvae (5%) (Table 1). Of the 182 I. scapularis collected, 180 were larvae (Table 1). The majority of ticks were unfed or flat. In total, 88% (161/182) and 80% (8/10) of I. scapularis and D. variabilis were unfed, respectively. Most collection media were clear upon inspection, ten were amber to reddish-brown colored and smelled like ammonia (Table 1). Discussion Here, we demonstrate that nest boxes can be used to collect immature I. scapularis and D. variabilis ticks from rodent and bird species. Using 11 DWINs we collected over 180 immature I. scapularis during a 4-month observation period. The majority (81%) of ticks were collected from just six DWINs associated with discolored collection media; presumably discoloration resulted from greater inputs of urine and feces representing longer occupancy. Unexpectedly, 88% of immature I. scapularis collected in the current study were unfed. Unfed ticks in DWINs may have been groomed or dropped off of hosts before completing a bloodmeal. In laboratory studies, P. leucopus groomed at least 50% of immature I. scapularis that were placed on them (Levin and Fish 1998, Shaw et al. 2003, Keesing et al. 2009). An alternative explanation is that larvae climbed up the tree and into the DWIN seeking a host. Peromyscus are known to nest in trees (Wolff and Hurbutt 1982, Larson et al. 2020). In addition, Carroll (1996) found larval I. scapularis on tree trunks and suggested that larval I. scapularis might be climbing trees to increase interactions with P. leucopus. However, less than 15% of I. scapularis collected from wild Peromyscus nest materials were unfed (Larson et al. 2020). The difference in the ratio of fed and unfed ticks between Larson et al. (2020) and the current study could be explained by the collection strategy. If blood-fed ticks burrow into nesting material, they might be less likely to drop off into the collection vial and unfed ticks that are groomed by mice and survive may be able to crawl out of the wild nests. Unfed ticks that were groomed in the nest boxes also might be more likely to fall into the collection tubes because of interactions with the PVC surfaces. Nesting material in the nest boxes could be examined for blood fed ticks in future studies. A primary goal of tick surveillance is to assess when ticks are active. Although our sample size was limited, we observed activity of larval I. scapularis from June to September with the lowest collections during July. The seasonality of larval I. scapularis activity is an important predictor, of which pathogen strains may be present in an area (Gatewood et al. 2009, Hamer et al. 2012). DWINs might be biased toward the collection of larvae, which tend to favor mice as a host (Shaw et al. 2003), and could be especially useful for investigating spatial-temporal patterns of larval I. scapularis activity. Further studies are needed to optimize and refine nest boxes in order to increase occupancy by target species. In this study, we followed Catall et al. (2011) and constructed our nest boxes out of plastic. The majority of nest boxes used in Peromyscus studies have been wooden (Drummond 1957, Jackson and DeFoliart 1975, Morris 1989); however, it is not known whether nest box material affects occupancy. Over the course of 3 mo, we found birds in a number of DWINs. It is possible that reducing the size of the entry hole could make the nest boxes more selective toward Peromyscus. We also noted that cotton nesting materials often stayed wet in nests used by Peromyscus, which could impact the duration of occupancy. Cotton is assumed to be an attractive bedding material, as permethrin treated cotton bedding is used as a mouse-targeted intervention strategy against ticks (Deblinger and Rimmer 1991) and it is readily available. However, there is little evidence that Peromyscus prefer cotton over other nesting materials that might be more resistant to moisture retention. In the current study, the length of animal occupancy was not known; however, this could be estimated in future studies with, for example, Thermochron data loggers (Orrock and Connolly 2016) or camera traps. Although our DWINs were built to target mice, several DWINs were occupied by birds. Birds are known hosts of immature I. scapularis and play a role in spreading and perpetuating the enzootic cycle of tick-borne pathogens (Ogden et al. 2008, Brinkerhoff et al. 2011). In addition, birds may be moving other tick species across the landscape during their migration. With proper modifications, DWINs or preexisting bird houses could be used as a surveillance tool targeting birds. It is also of interest that birds and mice sequentially inhabited the same nest boxes (Fig. 2), increasing the potential for shared parasites and pathogens between these vertebrate species. While refinements can be made, we showed that DWINs could be an affordable and effective tool for surveillance of immature ticks over time. Management of the nest boxes was straightforward, and nest box inspection and sample replacement can be done in less than 5 min per DWIN. The method could simplify surveillance procedures in comparison with active tick dragging or small mammal trapping, which is potentially harmful for animals (Anthony et al. 2005, Dizney et al. 2008). Moreover, the availability of nesting sites is not considered a limiting resource of Peromyscus in forests (Hornbostel et al. 2005); therefore, the deployment of DWINs is not expected to increase mouse abundances. The occupation of birds may make DWINs useful for detecting invasion of tick species which are often associated with birds (Ogden et al. 2008, Brinkerhoff et al. 2011). In addition, DWINs may have potential uses for tick management applications. For example, nest boxes have been previously used to deploy mouse-targeted treatments (Hornbostel et al. 2005). The elevated tree-mounted nest box concept would make chemicals used in treatments less accessible to children, an important concern for government regulators. The use of nest boxes for collection of ectoparasites was previously described in the 1950s and 1970s (Drummond 1957, Jackson and DeFoliart 1975), but they have been rarely used for this purpose in subsequent decades. Combined with modern materials and technology (e.g., camera traps, data-loggers), nest boxes can provide unique insights into ectoparasite–host interactions and pathogen dynamics of medically important arthropods. Acknowledgments We thank Thomas and Mary German for allowing us to use their property. Ryan Larson is a doctoral student supported by the Department of the Navy. Ryan Larson is a military service member and this work was prepared as part of his official duties. Title 17 U.S.C. 105 provides that ‘copyright protection under this title is not available for any work of the United States Government’. Title 17 U.S.C. 101 defines a U.S. Government work as work prepared by a military service member or employee of the U.S. Government as part of that person’s official duties. The work also was supported by the University of Wisconsin and by Cooperative Agreement Number U01CK000505, funded by the Centers for Disease Control and Prevention. 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TI - High Proportion of Unfed Larval Blacklegged Ticks, Ixodes scapularis (Acari: Ixodidae), Collected From Modified Nest Boxes for Mice
JF - Journal of Medical Entomology
DO - 10.1093/jme/tjaa287
DA - 2021-05-15
UR - https://www.deepdyve.com/lp/oxford-university-press/high-proportion-of-unfed-larval-blacklegged-ticks-ixodes-scapularis-Ns03Qt64N6
SP - 1448
EP - 1453
VL - 58
IS - 3
DP - DeepDyve
ER -