1. Introduction
The lone star tick,
Amblyomma americanum (L.). (Ixodida: Ixodidae), is an aggressively-biting species that is a nuisance to humans and a pest of livestock [
1]. It has been gaining attention as an important vector of human diseases, including erlichiosis, tuleramia, and Heartland virus [
2,
3]. More recently,
A. americanum has been implicated in triggering red meat anaphylaxis caused by the sugar galactose-α-1,3-galactose that is injected during feeding [
4]. The range of
A. americanum has been expanding northward from the southeastern United States and is likely to continue moving northward under current climate change conditions [
5,
6]. This expanding range will also expand the range of the diseases vectored by
A. americanum.
Amblyomma americanum is the most abundant tick species sampled in southeastern Virginia [
7]. In this region, adult and nymphal
A. americanum are most active from late April to mid-July, and larvae are active from August to October [
8]. It takes three blood meals for
A. americanum to complete their lifecycle: one to molt from larva to nymph, another to molt from nymph to adult, and the final one to produce eggs.
Amblyomma americanum utilize a wide variety of hosts like small mammals and birds, but white-tailed deer,
Odocoileus virginianus (Zimmerman), are considered the primary host [
9,
10].
Amblyomma americanum primarily disperse opportunistically on hosts but have been documented questing up to five meters in response to CO
2 plumes in mark-recapture studies [
11].
Amblyomma americanum spend most of their life off-host, subjecting them to abiotic conditions in the environment. They protect themselves against desiccation with cuticular wax deposits to inhibit water loss and can absorb moisture directly from the air [
12,
13,
14].
Amblyomma americanum quest during times of the day when temperatures are high and relative humidity is low [
15,
16], and generally seek environments that experience low temperature variation and have high relative humidity [
17]. Forests provide such favorable conditions for
A. americanum to survive and are generally more preferred habitats than grasslands [
18,
19].
Habitat manipulations can affect the abundance of
A. americanum by altering host behavior and microclimates. Areas where the invasive shrub Amur honeysuckle,
Lonircera maackii (Rupr.) Herder, had been removed produced lower
A. americanum densities than areas with the shrub, due to the preference of white-tailed deer for areas with
L. maackii [
20]. The westward expansion of the eastern red cedar,
Juniperus virginiana L., in Oklahoma is believed to be facilitating a similar westward expansion of
A. americanum by providing both better environmental conditions for the tick and white-tailed deer [
21].
Amblyomma americanum mortality was higher in plots with the invasive Japanese stiltgrass,
Microstegium vimineum (Trin.), compared to plots without the plant [
22]; this was because plots with
M. vimineum had higher temperatures and lower humidity than control plots [
22]. This effect has been observed with another tick species,
Ixodes scapularis Say. Areas where the invasive shrub Japanese barberry,
Berberis thundbergii de Candolle, had established had higher daily average relative humidity values at ground level than plots without Japanese barberry, or those where it had been thinned [
23]. Subsequently, more
I. scapularis were sampled from plots with Japanese barberry compared to control plots [
23].
Concurrent with concerns about the changes in tick-vectored diseases are concerns about pollinator declines. One of the primary drivers of pollinator decline is habitat loss, in conjunction with pesticide exposure and diseases [
24]. One mitigation strategy is the planting of wildflower plots to provide resources for bees, which can increase their abundance and diversity [
25]. These plots also provide resources for other beneficial arthropods, such as natural enemies of crop pests [
26]. The installation of these plots is subsidized in the United States by government programs such as the Environmental Quality Incentives Program [
27]. From 2009 to 2018, this program has helped pay for habitat management that is beneficial for pollinators on over 16,000,000 acres of land [
27,
28].
It is unknown, however, whether wildflower plots provide favorable habitats for ticks and could potentially increase the risk of exposure to people and animals to
A. americanum. As called for by Ginsberg et al. [
29], the impacts of pollinator conservation and vector control on each other need to be researched to minimize potential negative outcomes. Managing wildflower plots requires that they be mowed each year during the dormant season [
30]. This annual mowing could potentially build up a duff layer that provides a critical microclimate with high humidity and stable temperatures that would be hospitable for
A. americanum. Given that the removal of plants can reduce
A. americanum populations [
20,
21], does the addition of plants aid
A. americanum populations? The purpose of this study was to determine if on-farm wildflower plots can serve as quality habitat for
A. americanum.
3. Results
We collected 1165 nymphs and 566 adult
A. americanum over the two years of sampling.
Amblyomma americanum nymph abundance peaked in June of both years (
Figure 1). A peak in adult abundance was seen in May in 2018 and April in 2019 (
Figure 1). On average, more nymphs than adults were detected in 2018 (
z = 2.91,
p = 0.003). This effect was not statistically significant in 2019 (
z = 1.85,
p = 0.06) (
Figure 1).
Of the total 1731
A. americanum detected, 164 were taken from wildflower plots, 302 from weedy field margins, and 1265 from forest locations. No interaction between life stage and habitat was detected in either year of study. There was no difference in
A. americanum abundance between wildflower plots and weedy field margins in 2018 and 2019 (
Figure 2).
Amblyomma americanum were detected most often in the forest plots (
Figure 2), with significantly fewer
A. americanum collected in wildflower plots than forest plots in both years (
z = −5.23,
p < 0.001;
z = −3.89,
p = 0.003). Forests consistently had the thickest duff layers, shortest vegetation, and most stable temperatures of the three habitat types sampled (
Table 2).
The model with the interaction of habitat type and vegetation height was the top ranked model for predicting adult
A. americanum abundance (
Table 3). The models containing habitat only and the interaction between habitat and duff depth were within 4 AICc points of the top model and were included in model averaging (
Table 3). After model averaging, no effects were detected for duff depth (
Table 4). Vegetation height had a significant different effect in weedy field margins compared to the other habitats. As the height of vegetation increased in weedy field margins, the abundance of
A. americanum decreased (
z = 2.4,
p = 0.02) (
Table 4,
Figure 3).
Similar to adult
A. americanum, the habitat by vegetation height model was the best predictor of nymph abundance. All other models were more than 4 AICc points higher (
Table 5). As vegetation height increased in the forest samples, so did
A. americanum nymph abundance (
z = 3.4,
p = 0.001) (
Table 6). This contrasts to wildflower plots and weedy field margins, where nymph abundance decreased with increasing vegetation height (
z = −2.08,
p = 0.04) (
Table 6,
Figure 3).
4. Discussion
To our knowledge, this is the first study investigating the interaction of wildflower plots and tick abundance. In this study, wildflower plots planted for pollinator conservation did not inadvertently constitute an ecosystem disservice by simultaneously increasing A. americanum abundance. While A. americanum were detected in wildflower plots, this habitat harbored fewer of them than weedy field margins. Therefore, wildflower plots do not pose a risk of augmenting on-farm A. americanum abundance.
Vegetation height is playing a role in the differences in adult
A. americanum abundance between the sampling habitats. These changes could be related to the questing success of
A. americanum adults on taller vegetation. Adult
A. americanum could have higher success rates in finding a host in weedy field margins compared to the other habitats sampled. With taller vegetation, adult
A. americanum would have more area to utilize for questing to attach to larger hosts like white-tailed deer. Many of the weedy field margins sampled were a transition zone from agricultural areas to forested ones. These transition areas are frequented by white-tailed deer as they move from areas of cover to open areas as part of their diurnal movement [
40]. Adult
A. americanum could be investing more in vertical movement in the habitat than horizontal since hosts are not likely to linger. This behavior was seen with
I. scapularis in habitats that were deemed difficult for ticks to traverse due to the vertical habitat structure [
41] With greater success in finding hosts, fewer
A. americanum would be available to sample.
Amblyomma americanum nymph abundance decreased with taller vegetation in wildflower plots and weedy field margins but increased with taller vegetation in forested areas. Decreases in nymph abundance could be following a similar pattern as the adults; as vegetation height increased, so did questing success. The increase of
A. americanum nymph abundance with increasing vegetation height in forested areas could be explained by the preference of white-tailed deer to use dense vegetation in forests for bedding sites [
40]. With female white-tailed deer having a strong preference for their home range, they could be frequenting bedding areas and dropping engorged larvae. This could create nymphal hotspots in these areas. When the deer return to bed,
A. americanum nymphs may have the time to successfully attach to the host.
Ixodes scupalris more actively quest towards a host when the host is stationary [
41]. Larger wildflower plots could potentially provide enough cover for deer to use as bedding sites, creating a similar situation. However, given the smaller size of the plots used in this study, this was unlikely to be occurring. A study with
Peromyscus spp. mice found that 64% of the nests surveyed had
I. scapularis present, and 87% of all larval ticks present had taken a blood meal [
42]. Future studies could examine if specific sites where hosts remain immobile and which they frequently visit are attractive for immature stages of ticks.
In this study, duff depth was selected as a factor for adult
A. americanum but was not significant with model averaging. A similar result was seen in Missouri, where duff layer depth was selected as a factor, but not a significant factor in determining adult
A. americanum abundance [
39]. However, duff depth is an important environmental factor for the survival of adult
A. americanum as it can create a critical microclimate for preventing desiccation.
Amblyomma americanum adults are sensitive to moisture loss and will seek out moist microclimates after losing only 10–15% of their body weight to counteract desiccation [
43]. While the duff layer is important, its presence may be all that matters. In a previous study,
A. americanum were collected from areas that had shallower duff layers than
I. scapularis, but never from areas that had no duff layer [
44]. Better quantification of the microclimate of the duff layer may also help detect its effects on
A. americanum abundance, as the duff layer can be 2–3 °C cooler than the ambient air temperature [
16].
The result that wildflower plots are not increasing on-farm
A. americanum abundance is encouraging for both pollinator conservation and vector control. Further studies are needed to verify the results in other geographic areas and with different mixes of wildflowers. The mix of wildflower species in a pollinator habitat may have a large influence on the behaviors of tick hosts. A study in Florida observed that white-tailed deer browsed on all 11 wildflower species used in their pollinator mixes [
45]. Of the species tested by Degroote et al. [
45], two flower species were also present in this study:
Coreopsis lanceolata L. and
Rudbeckia hirta L. However, DeGroote et al. [
45] found that these were the least and fifth least browsed wildflower species, respectively. If wildflower mixes have species that are attractive to white-tailed deer, tick abundance may likely increase. However, from this study, it is not known if the presence of
A. americanum in the plots indicates that they can complete their lifecycle in this habitat, or if they are simply dropping off of their host. This could include sampling for hosts from within the different habitats to see what role they are playing in driving the difference in
A. americanum abundance.
Different tick species may have varied levels of attraction to the same habitat. Within a 1-ha forested plot,
A. americanum and
Ixodes scapularis were distributed between two different sets of habitat conditions related to each species’ tolerance to desiccation [
44].
Amblyomma americanum was found in areas with a more open canopy and less shrubby understory compared to
I. scapularis [
44]. If dense stands of ground cover develop within wildflower plots, they could attract rodent hosts of
I. scapularis [
46], potentially increasing
I. scapularis abundance within its range. This could be more problematic if conservation efforts are focused on the use of longer-lived woody plants, or if herbaceous wildflowers are not mowed regularly.