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.