Woodland biodiversity management as a tool for reducing human exposure to Ixodes ricinus ticks: A preliminary study in an English woodland

Authors


ABSTRACT:

This paper presents preliminary findings towards developing a UK-specific approach to reducing public exposure to woodland questing Ixodes ricinus tick populations by harnessing existing biodiversity-enhancing woodland ride (i.e., linear non-wooded herbaceous habitat either side of track within woodland) management strategies. This preliminary study in an English woodland firstly assesses whether ecological and environmental factors determine presence and density of questing Ixodes ricinus along woodland rides. Secondly, it sets these findings in the context of woodland ride management guidelines in England in order to understand what impact ride management strategies might have on numbers of questing ticks and tick survival. Nymph and adult I. ricinus presence and abundance were modelled in relation to relevant microclimate and ecological parameter variables. Predictor variables for increased questing nymph abundance included ride orientation, mat depth, occurrence of bracken/bramble and animal tracks, ride/path width, and sward height. Ticks thrive in the ecotonal habitat of a woodland ride, therefore we urge woodland managers to consider the impact of their ride management on ticks and human exposure to ticks. Possible recommendations for mitigating questing I. ricinus in line with biodiversity management guidelines rides are discussed in this paper and include seasonal mowing regimes, management of mulch/mat, and bracken/bramble management through use of scalloped ride edges.

INTRODUCTION

Ticks have long been recognized as parasites of domestic animals. In the United Kingdom (UK) it is now widely established that the sheep tick, Ixodes ricinus, is the primary vector of human and animal pathogens causing Lyme borreliosis, louping ill, and tick-bite fever (Medlock et al. 2009, Smith et al. 2011). Ixodes ricinus is also responsible for considerable economic losses to the grouse shooting (Davies 2005) and sheep farming industries. Over recent years, human cases of Lyme borreliosis have increased in England and there has been a perceived or actual increase in numbers and spatial distribution of I. ricinus in the UK. Ongoing tick surveillance in the UK conducted by the Health Protection Agency (Jameson and Medlock 2011) has confirmed previous anecdotal evidence (Scharlemann et al. 2008) that I. ricinus is expanding in its range in England, and that this may be due in part to increasing numbers of deer (e.g., Capreolus capreolus, European roe deer).

It has been suggested that increases in tick numbers and their associated diseases could begin to conflict with biodiversity enhancing strategies, because some conservation measures also potentially favor ticks (Medlock et al. 2009, Dobson et al. 2011). It would seem prudent, therefore, to focus attention on possible impacts of environmental and habitat management strategies on ticks and attempt to identify how such strategies could be harnessed as a tool for reducing questing tick numbers, or at the very least reduce human exposure to ticks through appropriate woodland management.

In England, increased landscape coverage by woodland and the concomitant spread of deer over the past 60 years has undoubtedly contributed to supporting populations of I. ricinus in the wider lowland countryside (i.e., non-livestock grazed habitats) and contributed to the expansion of tick suitable habitats. The expansion in the range of I. ricinus due to changes in climate, host distribution, or habitat change is not only particular to the UK but is well documented throughout Europe (Estrada-Peña 2002, Daniel et al. 2003; Materna et al. 2005, Gilbert 2010, Jaenson and Lindgren 2011). Woodland is a favored habitat of I. ricinus, and deer in this habitat are crucial to ensuring the viability of I. ricinus populations (Gray et al. 1992, Medlock et al. 2008, Dobson et al. 2011). Livestock and hares are known to support I. ricinus populations in other habitats (Gilbert et al. 2001, Medlock et al. 2008), but neither are common to woodland (including the study site). It is very likely that I. ricinus will continue to thrive in deciduous woodlands where deer are common, particularly in southern England. It has been suggested that the hazards for humans acquiring ticks in large wooded sites is now equal to that associated with the historical tick hot-spots like the New Forest or Thetford Forest (Dobson et al. 2011). Those managing potential tick habitats across southern England should be mindful of ticks and tick-borne pathogens.

Since the 1980s, the British countryside has been increasingly managed with biodiversity goals in mind. The advent of environmental stewardship has promoted the formation of habitats and corridors for wildlife across arable landscapes, with initiatives promoting defragmentation of previously isolated habitats in an attempt to assist species' adaptation to climate change. Woodland management in England has also changed, particularly in ancient semi-natural woodland (Kirby and Solly 2000). Woodland grant schemes and the Joint Nature Conservation Committee (JNCC) guidelines promote management of woodland rides (a traditional name for a linear gap in a woodland comprising a main track and associated adjacent vegetation, usually dominated by grass, bracken, and bramble; it is often managed to prevent scrub encroachment) for a range of vertebrate and invertebrate species, particularly butterflies. The promotion of wide, “sunny” rides not only increases nectar sourcing possibilities for butterflies, but it also increases browsing opportunities for deer and the ecotonal habitats favored by a number of vertebrate tick hosts (Estrada-Peña 2001). To ensure that woodland biodiversity goals can be met without exacerbating an increase in tick numbers and public exposure, tick-targeted habitat management strategies could be integrated within existing woodland management strategies to reduce potential tick hot-spots. Such management strategies, used by woodland managers in heavily-managed woodlands, include mowing regimes for each ride, delineation of ride-side vegetation into linear management zones based upon the frequency of management (including scalloping edges of rides, varying the widths of ride-side vegetation to increase variability of vegetation structure), and mulch management. This study aims to a) understand better the ecological and environmental variables determining abundance of I. ricinus within a managed woodland, and b) to begin to identify how woodlands, and more specifically woodland rides, could be managed to reduce numbers of questing ticks and consequently public exposure.

MATERIALS AND METHODS

This preliminary study was conducted in a large, ancient semi-natural woodland in Wiltshire, southern England, where the woodland ride system is heavily managed in accordance with UK nature conservancy guidelines, and where four species of deer are present. Field studies focused on the nymph and adult stages of I. ricinus during the spring months. Nymphs are the most commonly reported stage of I. ricinus parasitizing humans in the UK (Jameson and Medlock 2011) and are considered the most important tick stage in the transmission of Borrelia burgdorferi (agent of Lyme borreliosis) to humans (Hubalek and Halouzka 1998). Surveys were restricted to the spring nymphal abundance peak during April and May, as from June onwards nymphal activity begins to decline and the ride vegetation becomes dominated by high swards of bracken, making any quantitative study of tick abundance using dragging/flagging meaningless (Dobson et al. 2011). As much of the human exposure from ticks occurs along woodland tracks, focus of this study is given to woodland rides and the implications of their management.

Study site

Field studies were conducted in Bentley wood (50° 37′ 38″ W, 51° 04′ 12″ N at 50–100 m above sea level), a 665 ha (3 km × 5 km) woodland located in south Wiltshire. The woodland is on the site of ancient woodland but was replanted with Quercus robur, Fagus sylvatica, Picea abies, Pinus sylvestris, and Pinus nigra since the 1950s. It is designated a Site of Special Scientific Interest (SSSI) on account of its woodland fritillary butterflies, which benefit from the active ride and glade management. The wood supports a large, deer population, with >600 Dama dama, 60–80 C. capreolus and 20–30 Muntiacus reevsi (Barry Dowsett, Bentley wood gamekeeper, personal communication).

Predictor variables

Sampling was conducted during eight weeks (28 days of surveying) from the start of April to end of May, 2009, between 10:30 and 15:00. Ixodes ricinus is active in the UK in January during warm winters, and their peak activity commences from March onwards. This survey was conducted to coincide with peak nymphactivity during April and May, when tick activity from local weather conditions overrides the seasonal effects on tick phenology. All surveys were conducted along the edges of woodland paths, known locally as woodland rides. Each intersection of each ride was numbered (n=180) and rides were chosen randomly throughout the woodland, with different parts of the woodland visited on subsequent days. At each survey location 3-m transects were sampled, with ten replicates for each ride, with 10 m left between neighboring transects. The distance of 10 m between transects ensured that each transect was independent with respect to ground-based movement of ticks (1–2 m). It was not possible to ensure that all transects were independent with respect to tick host range, owing to a maximum of 30–40 rides suitable for survey, each with a mean ride distance of 150–200 m. The 1 m edge of track-side vegetation was sampled by slow pacing, in accordance with Milne (1943), by using a brushed cotton cloth (1×1 m) square with a wooden bar at the leading edge. The cloth was moved 2 m along the edge of the track, thus surveying an area of 3×1 m. All tick stages found attached to the cloth were collected and counted after each 3-m drag and transported to the laboratory for identification. Larvae, owing to their clustered distribution in the environment (Vassallo et al. 2000), were excluded from the analysis. All sampling was conducted during fine weather, and surveying was stopped during rain or if very wet vegetation soaked the cloth, with uniformity in cloth condition maintained for all transects.

A number of variables were recorded before and after each 3-m transect. Soil moisture was measured as a percentage using a Theta soil moisture probe and HH2 soil moisture meter (Delta-T Devices, Cambridge UK). Three measurements were taken for each transect (in each 1 m2) and were averaged. Ambient temperature (Celsius) was recorded at 1 m above the center of each transect using CEM DT-3321 Precision Hygro-Thermometer (CEM, Shenzhen, China). Cloud cover was recorded on an ordinal scale (0–8 oktas).

For each transect, vegetation-related variables were recorded including depth of decaying vegetation on the ground above the soil (mat depth) and mean height of vegetation (sward height) measured using a 50 cm ruler. The presence and percentage coverage (i.e., area of 3×1 m covered by each vegetation type) of Pteridium aquilinum (bracken), Rubus fruticosus agg. (bramble), and grasses, were judged subjectively by the recorder. The penetrability of the ride margin adjacent to each transect was measured on an ordinal scale of 1–3 (run, walk, fight), whereby the surveyor judged their ability to move through the neighboring vegetation.

The remaining variables related to topography, structure, and host potential. The ride orientation (path direction) was measured in degrees using a compass. The side of the ride surveyed was also noted to enable the aspect of each ride-side under study to be calculated (factoring in 90° discrepancies for perpendicular angle of tracks). Each transect was attributed an orientation to north (316°–45°), east (46°–135°), south (136°–225°), or west (226°–325°). The degree angle of each transect was also transformed into a heat load index using the equation (Neitlich and McCune 1997):

image

Where Θ is the aspect in degrees east of north. Measurements were recorded for width of the track and width of vegetation within the ride (hereafter ride width). Path substrate was also recorded (stony, mud, leaf litter, grass). The presence of large animal tracks (but not small mammal burrows) crossing transects was noted.

Statistical analysis

Preliminary univariate data analysis was performed to explore the data for the presence and abundance of nymphs and adults. All continuous data variables (temperature, soil moisture, cloud cover [ordinal], path and ride width, mat depth, sward height, numbers of animal tracks) were analyzed using Mann-Whitney U tests (for presence) and regression analyses (for abundance). Categorical data variables (orientation, vegetation type, density of ride vegetation) were analyzed using the chi-squared test. All univariate data analysis was performed in Minitab 15 (State College, PA, U.S.A.).

Recognizing the limitation of univariate analysis, the framework of generalized linear models (GLMs) was used to construct models to predict questing nymph and adult presence/absence and abundance (using abundance as continuous response variable). Presence/absence was modelled using logistic regression, thus predicting the probability of tick presence given the variables in the model (covariates), interpreted as an odds ratio. Abundance was modelled using negative binomial regression, the coefficient for each covariate interpreted as an incidence rate ratio. The bivariate relationship between each potential predictor variable and the dependent variables was examined for nonlinearities, and these were tested for significance. Each potential determinant of presence/absence or abundance was entered univariately into a regression model and tested for significance. Variables which were significant at the 10% level were then considered jointly in a regression with other univariately significant covariates. Backwards elimination was used to identify covariates remaining significant at 5% level (Collett 2003).

RESULTS

In total, 307 transects were sampled, with 1,191 questing nymph (Qn) and 114 questing adult (Qa) I. ricinus collected. Almost 90% (275/307) of transects had at least one questing nymph or adult. The majority of transects (65%; n=200) had one to five ticks, with ∼25% (n=75) transects with more than five ticks present (Figure 1). The mean nymph abundance during April and May was 4.3 and 4.1, suggesting that nymph abundance did not increase over time. The ride orientation fitted a gridded structure within the woodland, with 151 east-west rides and 155 north-south rides sampled, with 574 and 617 ticks collected, respectively. The numbers of Qn, mean number of Qn per transect and frequency of >5 Qn and 0 Qn in transects are shown in Table 1.

Figure 1.

Frequency distribution of the abundance of nymphs per transect.

Table 1.  Abundance (±SE) of questing nymph and adult per transect by aspect.
Ride aspectNo. transects No. QaMean Qn per transectMean Qa per transect% transects with >5 Qn% transects with 0 Qn
North96317203.30±0.380.21±0.0719.815.6
East47121632.57±0.421.34±0.064.38.5
South52247264.75±0.740.5±0.1235.57.7
West10849664.59±0.530.06±0.0932.07.4

The absence of questing nymphs was significantly associated with north-facing rides (X=4.45; p=0.035). The occurrence of more than five questing nymphs (i.e., higher densities; Table 1) in a transect was less common on east-facing rides (4.3%) compared to south- and west-facing rides (35% and 32%, respectively) (Table 1). The abundance of questing nymphs was significantly higher (Mann Whitney test; p=0.005) on south- and west-facing rides combined (mean 4.67/transect) compared to north- and east-facing rides combined (mean 3.06/transect). Similarly, the presence of questing adults were significantly positively associated with west-facing rides (χ2=11.2, p=0.001) and negatively associated with east-facing rides (χ2=5.84; p=0.016).

There were significant associations between the depth of the mat layer and both the abundance of Qn (F=6.87, p=0.009), and the presence of Qa (p=0.002), suggesting that reduced mat depth exhibits a negative association with Qn and Qa (Table 2). There was a significant association between sward height (SH) and Qn (F=3.24, p=0.022) using a polynomial regression analysis suggesting that at low SH, Qn was reduced, with Qn increasing with SH up to an optimum threshold whereby Qn appears to decline (Table 2). There is a significant negative association between Qn and ride width (RW) (p=0.007) and a significant negative association between Qa and RW (p=0.048; Table 2). A polynomial regression analysis suggests a non-significant weak association (F=2.32, p=0.075) between narrower path widths and Qn.

Table 2.  Summary of mean values (±SE) for certain predictor variables per transect.
  Qn=0 Qn>0 Qn=0–5 Qn>5 Qa=0 Qa>0
n322752327523174
Mat depth (cms)1.73±0.212.27±0.102.09±0.102.60±0.192.07±0.102.60±0.18
Soil moisture (%)38.78±2.0239.14±0.5739.50±0.6437.89±1.1339.22±0.6338.75±1.19
Ride width (ms)4.87±0.565.03±0.285.08±0.304.82±0.505.23±0.314.32±0.44
Path width (ms)2.4±0.192.08±0.062.17±0.061.95±0.102.19±0.061.92±0.10
Sward height (cms)23.38±3.219.70±0.7820.29±0.9519.47±1.1719.4±0.9522.05±1.34
No. Animal Tracks0.25±0.070.47±0.030.45±0.040.43±0.060.45±0.040.41±0.06
Cloud cover (oktas)4.28±0.454.56±0.154.52±0.164.54±0.324.56±0.174.41±0.29
Temperature (oC)19.78±0.6519.49±0.2219.56±0.2419.41±0.4219.34±0.2520.07±0.36
  • image(2)

[ Scatter plot of sward height vs abundance of Qn.. ]

The mean values for each predictor variable by nymph and adult presence and abundance are given in Table 2. Univariately there appear to be associations between nymph presence and abundance with deeper mat depth, increased number of animal tracks, and lower sward height. Adult presence appears to be associated with deeper mat depth, higher sward height, and narrower rides. The significance of these factors in concert were analyzed using a multivariate approach.

Multivariate analysis

Four regression models were built: two logistic models to predict presence/absence of Qn and Qa, and two negative binomial models to predict abundance of Qn and Qa. Decision trees were used to identify interactions between the available covariates. Significant variables in the logistic regression model of Qn presence/absence included presence of large animal tracks (OR 2.55: CI 1.10–5.92), narrow path width (OR: 0.19; CI 0.08–0.43), narrow ride width (OR: 0.61; CI 0.38–0.98), lower mean soil moisture (OR: 0.89; CI 0.83–0.96), and a low sward height (OR: 0.78; CI 0.69–0.90) (Table 3). Further analysis of the association of ride width suggested a non-linear relationship. The AUC value of 0.824 for this model suggests that this model achieves reasonable discrimination between presence/absence of Qn.

Table 3.  Significant variables in logistic regression model of Qn presence.
VariableOdds RatioStd. Err.p95% Confidence Interval
  1. † Ride width⁁2 and Ride width ⁁3 are the squared and cubed values of ride width, respectively, in order to capture any non-linearities in the effect of ride width.

Soil moisture mean0.890.0350.0040.83–0.96
Path width0.190.0800.0000.08–0.43
Sward height0.780.0530.0000.69–0.90
Ride width0.610.1470.0400.38–0.98
Ride width ⁁2†1.040.0210.0311.00–1.08
Ride width ⁁3†1.000.0000.0221.00–1.00
Animal tracks2.551.0950.0291.10–5.92
Pathwidth * sward height1.050.0200.0051.02–1.09
Sward height * soil moisture1.000.0010.0201.00–1.01

Regarding the abundance of Qn, a negative binomial model was constructed, and the main significant variables for Qn abundance were higher presence of bracken/bramble (IRR: 1.47; CI 1.11–1.94), deeper mat depth (IRR: 1.44; CI 1.19–1.75), presence of large animal tracks (IRR: 2.01; CI 1.19–3.37), and narrow paths (IRR: 0.72; CI 0.61–0.85). The association of animal tracks and mat depth appear to be non-linear (Table 4). For the models for both presence and abundance of Qn, the occurrence of lower temperatures and lower soil moisture were predictor variables in both models.

Table 4.  Significant variables in negative binomial regression model of Qn abundance.
VariableIncidence Rate RatioStd. Err.p95% Confidence Interval
  1. † Mat depth⁁2 and Animal tracks ⁁2† are the squares of mat depth and animal tracks, respectively, in order to capture any non-linearities.

Heat load index0.560.1830.0780.30–1.07
Path width0.720.0610.0000.61–0.85
Heat load index * path width1.530.2160.0031.16–2.02
Mat depth1.440.1430.0001.19–1.75
Mat depth ⁁2†0.970.0130.0140.94–0.99
Temperature0.950.0170.0040.92–0.98
Bracken &/or bramble1.470.2090.0071.11–1.94
Soil moisture mean0.970.0060.0000.96–0.98
Animal tracks2.010.5310.0081.19–3.37
Animal tracks ⁁2†0.660.1240.0280.46–0.96
Ride width0.940.0210.0070.90–0.98
Sward height0.980.0070.0010.96–0.99
Ride width * sward height1.000.0010.0051.00–1.00

A logistic regression model was also constructed to predict presence/absence of Qa, with significant variables including increased mat depth (OR: 2.02; CI 1.19–3.45) and high heat load (OR: 2.75; CI 1.33–5.70) (Table 5). However, the AUC value of 0.657 indicated poor discrimination between presence/absence of Qa.

Table 5.  Significant variables in logistic regression model of Qa presence.
VariableOdds RatioStd. Err.p95% Confidence Interval
Heat load index2.751.0220.0061.33–5.70
Mat depth2.020.5550.0091.19–3.45
Mat depth ⁁20.930.0370.0520.86–1.00

DISCUSSION

Visits to English woodlands by the public are most often confined to the network of paths, rides, track-ways, and glades that criss-cross the wood and segregate the woodland compartments. They also provide access for timber extraction, as well as providing enormous biodiversity potential by creating additional habitats for grassland and woodland-edge species. Their role as nectaring sites for butterflies is well-documented, but they also provide nesting and feeding areas for woodland rodents and passerines, nesting sites for migratory birds, browsing/grazing options for deer, foraging sites for bats, as well as supporting relict grassland communities. By their very nature, they require regular management to avoid encroachment by scrub and trees and are an integral component of a woodland ecosystem.

Background to woodland ride management strategies in England

For a managed English woodland, key ride management strategies focus on managing light levels, ride width, and the type of cutting/grazing regime. Shade is affected by ride width, height of surrounding trees, and ride orientation. Rides orientated east-west receive more sun during summer, but less sun during winter compared to north-south rides. Wider rides get more sunlight, and generally rides are designed to be 1.5 times wider than the height of surrounding trees to facilitate this. Cutting regimes that promote structure and diversity are encouraged, and parallel zones of different vegetation height are promoted, and these are dictated by the frequency of cutting (zone 1: 1–3 mows/year; zone 2: cut every 2–4 years; zone 3: cut every 8–20 years). In some cases the ride edges are scalloped to overcome “wind tunnel” effects and provide diversity. Seasonality of cutting can also be varied; an autumn cut has the least effect on invertebrates but promotes vigorous grasses to dominate. Invertebrate populations are negatively affected by a summer cut, and dominant grasses can be combated by a spring cut. Litter and cuttings may be raked and stacked or left in situ. Removing cuttings aids less vigorous herbs to establish and provides habitat for bare-soil invertebrates, while retaining them protects species that exploit the moist microclimate of litter. In each case, the management of a ride has a profound effect on the vegetation and microclimate, and thus determines their suitability for different animal species.

The various options for managing woodland rides will impact variously on a range of invertebrates, including ticks, and these could, and are, being utilized to promote or minimize invertebrate survival. This study indicates that ecological and environmental variables specific to woodland rides are significantly associated with high densities of questing I. ricinus. Such variables include the impact of aspect/orientation, depth of litter, occurrence of bracken/bramble, occurrence of animal tracks, and sward height; all key components of ride structure, and greatly impacted on by ride management. These factors will now be considered further.

Interpretation of findings in relation to management recommendations

In line with previous findings in landscape-scale studies on I. ricinus in Wales (Medlock et al. 2008), topographical aspect (or orientation) is a contributory factor in determining the activity of questing ticks. Densities of questing nymphs were significantly higher on south- and west-facing rides compared to east- and north-facing rides. The absence of questing nymphs in a transect was significantly higher on north-facing rides, in line with previous findings (Medlock et al. 2008). Similarly, the presence of adult ticks in a transect was significantly higher on west-facing rides, and significantly lower on east-facing rides. It may be that these results are indicative of the controlling factor of climate. All transects were completed during the middle part of the day, and given that north/east aspects are less exposed to the warming effects of midday/afternoon sunlight, reduced rates of warming from overnight temperatures might limit questing activity (and may also affect small mammal microhabitat). However, no measurements of overnight temperature at each transect were made to support this.

As ride management guidelines promote south-facing rides, this biodiversity objective could arguably contribute to promoting nymph activity during spring. However, based on the assumption that I. ricinus nymphs reduce their questing activity at high temperatures, south-facing rides may conversely impact negatively on nymphs during hot summer days. If ambient temperatures exceed specific thresholds, water retention by the tick becomes more challenging and it is more at risk of desiccation. At this point, the tick ceases questing and seeks high humidities in the litter (Knulle and Rudolph 1982). Indeed, the model for Qn abundance points to a negative effect of aspect (heat load) after temperature has been adjusted for, so although higher densities may be related to aspect, the highest heat load protects against high abundance of questing nymphs. At extremes of temperature, nymphs seek refuge in the mat, so this is likely to be more of a temporal rather than a spatial effect. Heat load is, however, a significant positive predictor of Qa, which may relate to the adult ticks' greater resistance to heat desiccation compared to nymphs.

Milne (1943, 1948) considered mat depth an important controlling factor, and in this study, mat/litter depth appear to determine both abundance of Qn and presence of Qa. Mat depth is crucial for enabling survival I. ricinus during periods of quiescence. Host-seeking through questing leads to an increased rate of water loss so that ticks must return to the moist litter/mat layer to rehydrate. The absence of such a mat layer severely hinders this process (Lees 1946, Milne 1948, Knulle and Rudolph 1982). In this study, the relationship between mat depth and both Qn and Qa was non-linear, with abundance declining at mat depths above 5 cm. The reason for this is not clear, but it may be related to decreasing sward density as mat depth increases. Mat/litter may be formed from a variety of plant materials, however bracken provides a good mat/litter layer, and its importance in supporting ticks was suggested by Milne (1943) and supported by many other studies (Dobson et al. 2011). In the current study, the occurrence of bracken and/or bramble in a ride transect was significantly associated with higher densities of questing nymphs. Ride management guidelines suggest that a build-up of litter (or “cut material”) can smother growth and reduce re-growth and germination of less vigorous plants within rides. As plant diversity leads to invertebrate diversity, ride management guidelines therefore advocate regular raking and stacking of litter. Such guidance for litter management in rides is also likely to have a significant effect on tick survival and the abundance of questing nymphs and adults. The importance of this finding should not be underestimated given that Milne (1950) reported that 99% of non-questing I. ricinus occur within the mat.

Unlike bracken, bramble does not produce significant litter. The association of bramble with high nymph numbers may, however, be linked to mammal activity, which are in turn linked to the deposition of engorged ticks (Hoodless et al. 1998). Bramble berries ripen in August and September when larval infestation rates on small mammals are at their highest (Craine et al. 1995, 1997). The occurrence of large numbers of engorged larvae at these sites would explain the consequent increased numbers of questing nymphs in spring. Roe deer also consume bramble (Prior 1987a) and, therefore, engorged females will be deposited as the deer browse on bramble during spring, with large numbers of larvae subsequently available to feed on small mammals later in the summer.

Stands of pure grass are associated with the absence of questing nymphs. This may be due in part to the lack of mat produced by grass, which may in turn be due to these rides being regularly mown, and hence a lack of litter building up. Grasses appeared to dominate along rides where a 1 m strip had been mown. Hence, ride management guidelines for mowing would appear to favor the reduction in questing nymphs during spring. Inspection of the sward height data suggests that very low swards in the ride were less suitable for supporting high numbers of questing nymphs. Given that the sensitivity of sampling should be highest at low swards, the absence of ticks is significant. Low swards are likely to provide less cover over the soil/mat layer and therefore result in increased drying of the mat and hence a less suitable microclimate for tick survival. It could also be that nymphs delay their questing until the microclimatic conditions prevail that are favored by a higher sward as suggested by Dobson et al. (2011). Indeed, as sward height increases, abundance rates of questing nymphs increase, up to a threshold, above which the sampler is undoubtedly under-sampling the complete structure of vegetation. For example, as each nymph will climb to the top of its chosen tip of vegetation (within reason), higher swards have greater diversity of vegetation height and therefore a proportion of nymphs will be missed, as also reported by Dobson et al. (2011). This effect was a consideration in the sample design and explained why sampling halted at the end of May when bracken growth increased dramatically. It is possible that the activity of nymphs is delayed in shorter swards, such as on short grass compared to longer vegetation.

The width of the ride and path also appeared important; the model showed that significantly lower Qn abundance occurred on wider rides. This concurred with increased Qa presence on narrower rides. The importance of ride width may be linked to animal host activity; larger animals favoring narrower rides where the safety of dense woodland is closer to hand (Prior 1987b) and conforms to studies showing tick abundance decreasing away from woodland (Boyard et al. 2007). Narrower paths were significantly associated with higher nymph and adult occurrence/abundance using regression analysis. The occurrence of narrower paths may mean that there is more movement of small mammals from one ride side to the other, and hence movement of fed larvae. Polynomial regression suggests that there is perhaps an optimum path width of two meters for higher questing nymph numbers, but the relevance of this is arguable.

The only measure of large host activity was the occurrence of large animal tracks. There is the possibility that an established animal track would actually lead to a general mopping-up of questing ticks over time. Milne (1950) suggested that mopping has little effect as the majority of ticks are quiescent in the mat layer. In this study, the occurrence of nymphs was associated with the presence of large animal tracks, and this was confirmed by the regression analysis. The abundance of questing nymphs, however, was not associated with animal tracks, and the questing nymph abundance model supports this, indicating a diminishing return suggestive of mopping. The IRR score (data not shown in results) for one animal track is 1.33 and highly significant, indicating that transects with one animal track have significantly more nymphs than transects with no animal tracks. The IRR for two animal tracks is 0.78, indicating that transects with two animal tracks have significantly fewer nymphs than sites with no animal tracks. This IRR, however, is not significant (possibly due to low sample size), but the big difference in IRR might point to a mopping effect.

Finally, regarding microclimate, previous studies by Milne (1950) and Medlock et al. (2008) found that higher soil moisture, lower mid-day temperatures, and higher cloud cover favored questing ticks. Here again, lower ambient temperatures appeared to exert some influence over questing nymph numbers, as has already been suggested in the south-facing rides. Although cloud cover was qualitatively higher where more nymphs were active, this was not significant. Interestingly, in this study lower soil moisture was associated with higher nymph numbers. This appears contradictory to previous studies, but it may be that in a humid environment within woodland, where low soil moistures are not expected, the lower threshold does not impact the tick or its activity. Lees (1946) and Milne (1948) showed that ticks do not favor over-saturation brought on by high humidity and that it can limit their activity.

In conclusion, this preliminary study indicates that at the study site, ecological variables related to ride structure and management are associated with the abundance of I. ricinus nymphs (and to some degree adults). There are clear management strategies that could negatively impact questing nymph activity and hence reduce public exposure during spring. The management of rides that favor increased direct sunlight may promote nymph activity, at least in spring, and therefore, additional ride vegetation management might be required to overcome this effect. The results also show the importance of sward height, vegetation type (bracken and bramble), and ride size as important factors. Ideally, ride management guidelines that advocate regular mowing (and raking) of the 1 m path-side strip in spring should be promoted to keep questing ticks down (and hence reduce public exposure). Lower swards limit opportunities for questing ticks to find a human host; it also increases the exposure of quiescent ticks in the litter to desiccation from the sun. Mat or mulch management should be encouraged, not only as a biodiversity objective, but also in areas of high tick abundance to limit tick survival and activity. Raking and stacking should be used to negate these sites and the possible use of herbicide in rides for bracken management could be explored, if deemed acceptable and necessary. Reducing ride-side stands of bramble is less favorable for biodiversity as it provides a nectar resource. However, an adjacent mown strip next to the path should reduce tick exposure. Ideally, these rides could be managed as scalloped rides to widen the interface between bramble and paths.

It should be noted that not all these recommendations may be appropriate in all situations. The authors recognize that this was a preliminary study in one large, heavily managed woodland in southern England, and we encourage further studies in other woodland sites. With the ever-expanding populations of deer in southern England (and elsewhere in Europe), tick populations will continue to be a concern for the public, public health authorities, and also the environment sector. Identifying strategies for minimizing exposure to ticks and thus reducing the potential transmission of Lyme borreliosis to foresters and the public should be a key consideration for those responsible for woodland and ride management.

Acknowledgments

Thanks go to David Lambert of the Bentley Wood Trust for permission to work in the woodland, and for providing his expertise on current woodland management strategies. This study was conducted under the HPA UKVECTOR project and funded by NIHR Centre for Health Protection Research at the Health Protection Agency. This paper is work commissioned by the UK National Institute of Health Research. The views expressed in this publication are those of the authors and not necessarily those of the NHS, the National Institute for Health Research, or the Department of Health.

Ancillary