The effect of deer management on the ... - Wiley Online Library

Ecological Applications, 22(2), 2012, pp. 658–667 Ó 2012 by the Ecological Society of America

The effect of deer management on the abundance of Ixodes ricinus in Scotland L. GILBERT,1,3 G. L. MAFFEY,2 S. L. RAMSAY,1

AND

A. J. HESTER1

1 James Hutton Institute, Craigiebuckler, Aberdeen AB15 8QH United Kingdom Aberdeen Centre for Environmental Sustainability (ACES), University of Aberdeen, 23 St. Machar Drive, Aberdeen AB24 3UU United Kingdom

2

Abstract. The management of wildlife hosts for controlling parasites and disease has a history of mixed success. Deer can be important hosts for ticks, such as Ixodes ricinus, which is the primary vector of disease-causing zoonotic pathogens in Europe. Deer are generally managed by culling and fencing for forestry protection, habitat conservation, and commercial hunting, and in this study we test whether these deer management methods can be useful for controlling ticks, with implications for tick-borne pathogens. At different spatial scales and habitats we tested the hypotheses that tick abundance is reduced by (1) culling deer and (2) deer exclusion using fencing. We compared abundance indices of hosts and questing I. ricinus nymphs using a combination of small-scale fencing experiments on moorland, a large-scale natural experiment of fenced and unfenced pairs of forests, and cross-sectional surveys of forest and moorland areas with varying deer densities. As predicted, areas with fewer deer had fewer ticks, and fenced exclosures had dramatically fewer ticks in both large-scale forest and small-scale moorland plots. Fencing and reducing deer density were also associated with higher ground vegetation. The implications of these results on other hosts, pathogen prevalence, and disease risk are discussed. This study provides evidence of how traditional management methods of a keystone species can reduce a generalist parasite, with implications for disease risk mitigation. Key words: control; culling; deer; disease; fencing; forest; Ixodes ricinus; management; moorland; pathogen; Scotland, United Kingdom; tick.

INTRODUCTION The management of keystone species such as large herbivores can be highly challenging given the impact they can have on the ecosystem and their cultural and economic value to rural communities (Mills et al. 1993). Many deer species worldwide are recognized as important ecosystem engineers (e.g., Melis et al. 2006), and their populations in many areas are managed for forestry and crop protection, for conservation purposes such as habitat improvement and woodland regeneration, and to provide revenue from hunting. Currently there is also a growing interest in some areas in the idea of managing deer populations as a tool to control ticks and the incidence of tick-borne diseases because deer worldwide can be important hosts to ticks (e.g., Gray 1998, Kiffner et al. 2010). Managing wildlife for parasite and disease control has had mixed success and often has associated ecological, economic, and cultural impacts. For example, bison Bison bison in North America have been extensively culled in some areas to control brucellosis in cattle. However, despite this, unforeseen reinfection of cattle Manuscript received 9 March 2011; revised 1 August 2011; accepted 26 August 2011. Corresponding Editor: S. K. Collinge. 3 E-mail: [email protected] 658

from elk Cervus canadensis has been demonstrated (Cross et al. 2007). Attempts to keep elk and cattle separate can result in greater aggregation of elk and increased disease risk (Roffe et al. 2004). In another study, virtual elimination of badgers Meles meles can reduce bovine tuberculosis in cattle (Eves 1999), but badger culls can also increase disease risk in neighboring areas due to increased badger dispersal (Woodroffe et al. 2006). In parts of Europe wild boar Sus scropha are culled to reduce infection of domestic pigs with classical swine fever. However, this strategy is often less effective than expected due to unforeseen effects on wild boar dispersal distances, herd immunity, and infection via carcasses (Laddomada 2000). In some areas of Scotland mountain hares Lepus timidus are culled in an attempt to increase densities of red grouse Lagopus lagopus scoticus, an economically important game bird. Mountain hares carry ticks and can transmit louping ill virus, a tickborne pathogen that has been shown to cause 78% mortality in laboratory-infected red grouse (Reid 1975). Although mountain hare culls have been reported to control ticks and louping ill virus at one relatively unusual site (Laurenson et al. 2003), a recent review (Harrison et al. 2010) failed to find compelling evidence that reducing mountain hare density will successfully control ticks, louping ill virus, or improve red grouse

March 2012

DEER MANAGEMENT AND TICK ABUNDANCE

numbers on the majority of areas, especially in the presence of alternative hosts. The previous examples demonstrate that reducing wildlife reservoir hosts cannot always successfully control the target parasite or pathogen. It is therefore not clear whether managing deer would be successful at controlling ticks and tick-borne diseases, even though it is well established that deer are key tick hosts in many areas (e.g., Gray 1998, Kiffner et al. 2010). The most important tick species for vectoring zoonotic pathogens in Europe is Ixodes ricinus, and this species is currently increasing in abundance and distribution in many areas including the United Kingdom (Kirby et al. 2004, Scharlemann et al. 2008). This has occurred alongside a rise in abundance and distribution of red deer Cervus elaphus and roe deer Capreolus capreolus in the United Kingdom (Ward 2005). I. ricinus transmits several zoonotic pathogens of importance to human and animal health, including Borrelia burgdorferi sensu lato, the agent of Lyme borreliosis, which is the most prevalent vector-borne zoonotic disease in the Northern Hemisphere. I. ricinus also transmits Babesia protozoa, Anaplasma phagocytophilum, and the tick-borne encephalitis complex of viruses, which includes the aforementioned louping ill virus. Reported incidence of tickborne diseases is rising in many parts of the world, and in the United Kingdom the control of ticks is now perceived as one of the most important issues in the uplands. The I. ricinus life cycle comprises three active stages: larva, nymph, and adult, each of which takes one blood meal. I. ricinus larvae tend to feed on small mammals and birds, adults on large herbivores such deer, sheep, and hares, and nymphs on most host types (Gray 1998). Because I. ricinus are generalist feeders they are particularly interesting in an ecological context. For example, they have the potential to mediate ‘‘apparent competition’’ between hosts, whereby changes in numbers of one host species can result in changes in numbers of another host species through the action of the shared parasite (Holt 1977). In this case, managing deer could theoretically improve red grouse survival (Gilbert et al. 2001) or reduce Lyme borreliosis risk in humans through reduction of tick populations, even though deer are not competent transmission hosts of these pathogens. Traditional deer management is generally implemented by excluding deer using deer-proof fencing or by reducing deer density through culling. While Ruiz-Fons and Gilbert (2010) found fewer questing ticks in fenced than unfenced forests, a meta-analysis by Perkins et al. (2006) found the opposite effect (i.e., tick amplification) in small exclosed woodlands, and other studies have found inconsistent effects of woodland fencing depending on year, site, and tick stage (e.g., Daniels and Fish 1995, Ginsberg et al. 2002) due to alternative hosts such as small mammals or birds maintaining tick populations. Therefore, excluding deer using fencing may or

659

may not reduce tick populations and, therefore, culling deer might also not necessarily be effective at reducing tick abundance if ticks are able to feed on alternative hosts. In this study, therefore, we aimed to test the effect of both primary traditional deer management techniques (culling and fencing) on I. ricinus abundance. We did this in contrasting habitats: forest, as in the previous studies and also, unlike previous studies, in open heather moorland. We also used contrasting spatial scales: (1) a replicated fencing experiment using paired fenced and unfenced areas of a much smaller spatial scale than those found by Perkins et al. (2006) to increase (rather than decrease) tick abundance, and (2) surveys of landscape-scale forests managed for timber or conservation. Specifically we aimed to test the following hypotheses: 1) Reducing deer density by culling reduces tick abundance. We tested this by conducting surveys of relative tick and deer abundance in both forest and moorland habitats at sites that varied in deer density due to variation in culling strategies. In Scotland, all land is managed and deer densities in a particular area are primarily determined by the culling regime in that area, depending on the aims of the land-holding unit. For example, land managed for conservation or for red grouse hunting tends to cull deer such that deer densities are low, whereas land managed for commercial deer hunting culls less intensively to maintain high deer densities. As such, for the purposes of this study in Scotland, we assume that deer density in a particular area is a proxy for the culling strategy in that area. We predicted that areas with fewer deer would have fewer ticks. 2) Excluding deer using fencing reduces tick abundance. To test this we first conducted experiments using small-scale fenced/unfenced plots at a moorland site with extremely high deer density (a deer farm) and two moorland sites with more typical, lower, deer densities. Second, we scaled this up by utilizing nine pairs of fenced and unfenced forests, which acted as a largescale ‘‘natural experiment.’’ We predicted fewer ticks within fenced areas at both spatial scales and in both habitats. MATERIALS

AND

METHODS

The effect of culling deer on tick abundance To test the hypothesis that a reduction in deer density causes a reduction in tick abundance, comparisons were made between deer abundance and questing tick abundance indices at 55 sites across Scotland. These sites included both forest (n ¼ 30) and open heather moorland (n ¼ 25). The intensity of deer management and deer abundance varied between sites, and deer management had been in place for many years at each site. In each area we surveyed both forestry and adjacent open moorland as follows.

660

L. GILBERT ET AL.

We used 10 m long blanket drags to survey questing ticks, using a 1 3 1 m square of white blanket material (see Ruiz-Fons and Gilbert 2010). Surveys were conducted in August 2008, which is well within the questing season for I. ricinus in upland Scotland; apart from ticks beginning to be active in around April/May and becoming inactive in around October, there is little evidence for predictable peaks or a bimodal pattern in I. ricinus activity over the summer in upland Scotland (Ruiz-Fons and Gilbert 2010), although published data on phenology are scant. We conducted 10–16 blanket drags at least 50 m apart at each site. Each forest– moorland pair was surveyed within the same 8-h period to minimize any potential effect of weather on tick questing behavior. We counted dung from red deer, roe deer, sheep, rabbits, mountain hare, and grouse within a 1 3 1 m area at the beginning and end of each blanket drag. For analysis, dung count values from each blanket drag site were averaged across each site to provide an index of relative abundance for each site for each host species. While dung counts cannot provide a measure of host density, they can provide a useful comparison of host usage between different areas. Ground vegetation height was measured using a sward stick at the beginning, middle, and end of each 10-m blanket drag, and the average of the three measurements was used for analysis. Ground vegetation is important to take into account as it may be affected by deer grazing levels, and may in turn affect the density of alternative hosts such as small birds and mammals. In addition, ground vegetation height must be taken account of statistically to help control for any effects on the blanket drag technique (Ruiz-Fons and Gilbert 2010). Temperature and relative humidity were recorded from ground vegetation level at the time of each blanket drag to enable us to account for conditions on the day that may affect tick questing behavior. We attempted to take these measurements at a height that potentially reflected tick questing height at that particular location, i.e., where questing ticks would be experiencing the temperature and relative humidity measured. Therefore, the height above ground varied for these measurements, depending on ground vegetation height and density, such that for very short grass or pine needles the sensor was laid on the ground, whereas for heather the sensor was propped up in the body of the heather several centimeters above the ground. For analysis these temperature and relative humidity measurements were averaged across all blanket drags for each site. The effect of fencing on tick abundance To test the hypothesis that fencing to exclude deer reduces tick abundance we compared tick abundance indices between fenced and unfenced areas, utilizing both (1) experimental fencing plots in open heather moorland and (2) ‘‘natural experiment’’ fencing used for forest protection.

Ecological Applications Vol. 22, No. 2

1. Experimental fencing plots on moorland.—These were sited in three areas of open heather moorland in Aberdeenshire, northeast Scotland: site A was on an upland deer farm with very high deer density (40–50 deer/km2) and was chosen to maximize any potential effect of excluding deer; sites B and C had lower, typical upland deer densities (8–10 deer/km2) as well as low densities of other wild hosts including rabbits, mountain hares, and red grouse. All three sites comprised replicated fenced/unfenced paired plots that were set up in the winter of 2004/2005 (i.e., 3–4 years prior to this study). Sites A and C contained four replicates of the fenced/unfenced pairs, while site B contained three replicates. The size of the fenced plots at sites B and C was 100 3 20 m (0.2 ha) and at site A it was 125 3 20 m (0.25 ha). The fences were designed to exclude medium-sized mammals (hares and rabbits) and larger herbivores (deer and sheep; see Plate 1). Small animals such as mice, voles, shrews, and birds could access the fenced areas. In May, July, and September 2008 and 2009 we conducted blanket drags for ticks and associated measurements (ground vegetation height, temperature, relative humidity) at all experimental sites, as detailed previously, with 10–14 drags conducted per plot per visit. However, due to very high tick abundance in the deer farm (site A), there were some sampling modifications. Here, some blanket drags in May were limited to 1 m long (due to time constraints of counting and removing so many ticks over 10-m drags). We always conducted drags of the same length between fenced and unfenced plots within a paired replicate, so that drag length was never a confounding factor in the analysis. Because site A differed from sites B and C in these drag distances, the deer density, general environment, and the size of the fenced areas, we analyzed site A separately from sites B and C (which were analyzed together). 2. Natural experiment forest fencing.—We surveyed nine areas with adjacent fenced (deer-proof ) and unfenced forest patches (i.e., 18 forest patches) in areas of relatively low deer densities typical of the area (8–10 deer/km2). The fencing was intended either for forestry protection or for regeneration of seminatural woodland for conservation. We strictly chose only those sites that formed appropriate fenced/unfenced pairs, in terms of their close proximity, local climatic, soil, and weather conditions. These sites therefore provided a natural experiment with which to test the effect of deer exclusion using fencing on tick abundance in typical extensive management scenarios. Deer fencing had been in place at each site for at least eight years and all fenced areas were at least 5 ha. The fencing for this natural experiment was typical of deer management and designed only to exclude deer to protect trees; medium-sized mammals were not excluded. We conducted surveys in July and August 2006. Surveys consisted of 10–15 blanket drags within each site and we measured ground vegetation height,

March 2012


temperature, humidity, and counted dung (deer, rabbits, mountain hares, and grouse) as detailed previously. We also investigated the effect of typical management fencing on these factors measured. Due to constraints of time and resources we did not estimate the abundance index of small mammals or birds other than grouse. To reduce potential confounding effects of habitat and ground vegetation type, all forests were closed canopy conifer or mixed forests and all open moorland sites were Calluna-dominated heath. Statistical analysis All models were generalized linear mixed models using the GLIMMIX macro of the SAS software, version 9.1.3 (SAS Institute 2002–2003). For all models a backwards stepwise procedure was conducted, whereby terms were sequentially eliminated from the model if P . 0.1. The effect of culling on tick abundance.—The data demonstrated over-dispersion beyond the Poisson distribution. Therefore, we specified a Poisson distribution and entered replicate and individual blanket drag as random effects. Entering individual blanket drag as a random effect introduces flexibility to the model fit so that a fit to the Poisson does not have to be assumed. This method was developed by Elston et al. (2001), using tick count data as the model example, specifically to account for data that is over-dispersed beyond the Poisson distribution. For our analysis, the response variable was the counts of nymphs, and we did not analyze larvae or adult ticks for three reasons. First, nymphs are the stage considered to pose the greatest risk of tick-borne pathogen infection because larvae have not yet acquired pathogens via a blood meal and adults number far fewer than nymphs. Second, larvae have a very patchy spatial distribution and their count data distribution displays extreme zero-inflation, which can cause problems statistically and make meaningful results difficult to find and interpret (Ruiz-Fons and Gilbert 2010). Third, the blanket drag efficiency for larvae is particularly affected by vegetation density and height because larvae quest lower down than nymphs or adults (Mejlon and Jaenson 1997). We counted too few adult ticks for meaningful analysis. The following fixed factors were entered in the model: habitat (forest or moorland), host abundance dung indices (deer, rabbit, hare, and grouse), ground vegetation height, relative humidity, temperature, and month (to account for any seasonal variation in tick questing activity). Red deer and roe deer dung were considered as a single index of deer abundance because their dung was not always easy to distinguish in the field. We also tested for an association between deer abundance index and ground vegetation height because this can affect tick questing behavior and survival (through microclimate), and the usage of the habitat by alternative hosts. For this we again used the GLIMMIX procedure and specified a Poisson distribu-

661

tion, with site as a random effect. These dung data were not over-dispersed beyond the Poisson, so we did not need to apply the method of Elston et al. (2001). The effect of fencing on tick abundance.—Similar models were applied as detailed previously to account for over-dispersion. Three separate models were constructed: first for the moorland on the upland deer farm, site A; second for the other two experimental moorland areas, sites B and C; and third for the natural experiment forests. The response variable was nymphs per blanket drag and fixed factors were as follows: the presence and absence of fencing, ground vegetation height, temperature, relative humidity, month, and year and, for the natural experiment forests only, we also included abundance indices of hosts that could access fenced areas (grouse, rabbit, mountain hares) in the models. For the natural experiment of fenced and unfenced forests, for which we had deer dung data, we then ran separate models to explore the effect of fencing on two key parameters: deer and ground vegetation height, which are the expected key mechanisms for an effect of fencing on questing nymph abundance index. Random effects for all models included replicate number for the experimental sites, site (except for analysis of site A as there was only one site) and individual blanket drag to allow for overdispersion (Elston et al. 2001). RESULTS The effect of culling deer on tick abundance At the 55 moorland and forest sites surveyed around Scotland, questing nymph abundance significantly increased as deer dung indices increased (F1,19 ¼ 8.08, P ¼ 0.0104; Fig. 1). In terms of deer management controlling I. ricinus the model output suggested that if the index of relative abundance of deer falls from 2 to 0, the associated decrease in questing nymphs would be 94.3% in forest and 72.7% on open moorland. Questing nymph abundance also increased as red grouse dung indices increased (F1, 170 ¼ 4.8, P ¼ 0.0298), increased with decreasing relative humidity (F1,35 ¼ 7.33, P ¼ 0.0104), and fewer nymphs were counted on blanket drags on open moorland than in woodland habitats (F1, 490 ¼ 19.6, P , 0.0001). All other variables (indices of relative abundance of rabbit, mountain hare, and sheep, ground vegetation height, and month) were eliminated from the model due to nonsignificance. Higher deer abundance index was associated with lower ground vegetation on moorland (F1, 249 ¼ 5.1, P ¼ 0.0255), but not in forests (F1, 279 ¼ 0.02, P ¼ 0.8969). While deer abundance index was similar in both habitats (forest, 0.064 6 0.012, mean 6 SE; moorland, 0.068 6 0.014), ground vegetation was lower in forest (19.5 6 3.59 cm) than on moorland (36.80 6 3.57 cm). Ground vegetation height may depend more on tree density and canopy cover than the differences in herbivore density found at these sites.

662


L. GILBERT ET AL.

FIG. 1. Relationship between the number of questing tick nymphs (Ixodes ricinus) per blanket drag and deer dung abundance index (a proxy for usage of each site by deer) for each site for both forest and open moorland habitats, upland Scotland, UK. Unadjusted data are shown.

The effect of fencing on tick abundance 1. High deer density fencing experiment.—There were significantly fewer questing nymphs within fenced areas than unfenced areas (F1, 736 ¼ 479.58, P , 0.0001; Fig. 2). This was equivalent to a 86.2% control of questing I. ricinus nymphs due to fencing. All other variables (ground vegetation height, relative humidity, temperature, month, and year) were eliminated from the model due to nonsignificance. 2. Typical deer density fencing experiment.—There were significantly fewer questing nymphs within fenced areas than unfenced areas (F1,1318 ¼ 91.82, P , 0.0001; Fig. 2). This was equivalent to a 87.7% control of questing I. ricinus nymphs due to fencing. The number of questing nymphs counted on blanket drags increased over the season from May to July to September (F2,1098 ¼ 3.97, P ¼ 0.0191). All other variables (ground vegetation height, relative humidity, temperature, and year) were eliminated from the model due to nonsignificance. 3. Natural experiment of paired fenced and unfenced areas.—Again, questing nymph abundance was significantly lower in fenced than unfenced areas (F1, 202 ¼ 5.88, P ¼ 0.0162). This was equivalent to a 96.0% control of questing I. ricinus nymphs due to fencing. There were also fewer nymphs counted in areas of high ground vegetation (F1, 198 ¼ 11.84, P ¼ 0.0007). This probably reflects the effect of fewer grazers within fenced exclosures (taller vegetation and fewer ticks), as well as, perhaps, potentially reduced efficiency of the blanket

drag method at picking up ticks in higher vegetation. All other variables (indices of relative abundance of rabbits, mountain hares, and grouse, relative humidity, temperature, month, and year) were eliminated from the model due to nonsignificance. We also explored the differences between fenced and unfenced areas in all the environmental variables measured in the field (Table 1). Ground vegetation was significantly higher in fenced areas than in unfenced areas (F1, 154 ¼ 32.14, P , 0.0001). Deer dung indices were marginally significantly lower in fenced than unfenced forests as expected (F1, 154 ¼ 4.26, P ¼ 0.0571). Replacing fencing with deer abundance index in the model indicated that the association of deer with questing nymph abundance was even stronger (F1, 202 ¼ 6.95, P ¼ 0.0090) than that found above for fencing (this was taking into account the effect of ground vegetation height in the model). Table 1 suggests that both grouse and especially mountain hares used fenced areas more than they used unfenced areas. DISCUSSION This study aimed to test the potential of two key deer management methods (culling and exclusion by fencing) for use as tick control strategies. The effect of culling deer on tick abundance We hypothesized that reducing deer densities through culling will reduce tick abundance, and we predicted

March 2012


663

height) and questing nymph abundance. Conditions favorable to tick questing generally include higher, not lower, relative humidity (e.g., Gray 1998). One explanation could be that after recent rain, when humidity is very high, there may be fewer ticks because they may stop questing during rainfall. Another reason for our unexpected result could be because the measurements were taken at variable heights above ground level depending on vegetation height because we were attempting to measure the humidity that questing ticks in the vegetation would be experiencing. However, correlations between tick abundance, vegetation type and height, and blanket drag efficiency could be confounding factors due to our method of measuring humidity. The effect of fencing on tick abundance

FIG. 2. Average number of questing nymphs per blanket drag (6SE) of the raw data for fenced and unfenced paired replicates at (a) experimental moorland site A, the upland deer farm, (b) experimental moorland sites B and C, the sporting estates, and (c) natural experiment forest sites.

fewer questing ticks in areas with lower deer abundance. As predicted, in our surveys of 55 forest and moorland sites across Scotland we found that where deer abundance was lower (as indicated by dung presence) questing nymph abundance was also lower, even after statistically accounting for any potential effect vegetation height might have on blanket drag efficiency. General associations between deer and tick abundance have been reported previously, both for roe and red deer for questing I. ricinus nymph abundance (e.g., Gilbert 2010, Ruiz-Fons and Gilbert 2010) and other deer and tick species (e.g., Wilson et al. 1990). Furthermore, intensive deer culls have been shown to successfully reduce ixodid tick abundance (Stafford et al. 2003, Rand et al. 2004). It is intriguing that we found a negative association between our measurements of relative humidity at ground vegetation height (estimated to be tick questing

We aimed to test the hypothesis that excluding deer using fencing reduces tick abundance. Our results provide powerful evidence that excluding deer from both moorland and forest, at a range of different deer densities, for different land management objectives, and at different spatial scales can significantly reduce the abundance of questing nymphs within a fenced area. Our results are in agreement with North American and European (including Scottish) studies that have reported reduced numbers of ixodid ticks in fenced forests from which deer have been excluded compared to areas with deer (Ginsberg et al. 2004, Brown et al. 2008, Ruiz-Fons and Gilbert 2010). However, our finding that even the very small scale (0.2 and 0.25 ha) experimental fenced plots on heather moorland had dramatically reduced tick abundance contrasts with that of a metaanalysis by Perkins et al. (2006). They found that, while large fenced areas of forest did indeed have fewer questing ticks than unfenced areas, small (,2.5 ha) exclosures had more questing ticks and higher tick burdens on small mammals than unfenced areas. Their explanation was that in small exclosures alternative hosts such as small mammals are able to maintain the tick populations. Small mammals tend not to be TABLE 1. Values (mean, with SE in parentheses, calculated from the raw data) of all variables recorded in the field for fenced and unfenced forests from the large-scale natural experiment in upland Scotland, UK. Variable

Fenced

Unfenced

Questing nymphs Questing larvae Questing adult ticks Deer Mountain hare Rabbit Grouse Vegetation height (cm) Temperature (8C) Relative humidity (%)

0.125 (0.125) 0.25 (0.25) 0.00 (0.00) 13.5 (5.8) 25.9 (8.8) 12.9 (12.2) 5.5 (3.6) 37.38 (3.93) 25.23 (1.80) 55.14 (5.22)

3.125 (1.65) 42.9 (29.6) 0.375 (0.183) 27.0 (5.2) 3.7 (2.1) 14.6 (11.8) 2.7 (1.6) 23.88 (5.28) 24.40 (1.60) 57.31 (5.42)

Note: Values for the questing ticks and hosts are the estimated indices of relative abundance 3 100.

664

L. GILBERT ET AL.

particularly abundant in heather moorland (Gilbert et al. 2000), which may partly explain why our results differed from that found in the small forest exclosures of Perkins et al (2006). It is also important to note that Perkins et al.’s meta-analysis used data from multiple species of ticks, which differ in their phenology, host preferences, and ecology, and the age of fenced exclosures was not taken into account in the analysis. For all cases fencing had a dramatic negative effect on tick abundance, equivalent to 86–96% control of questing I. ricinus nymphs, although ticks were not completely eradicated. In the large-scale forestry, the dung counts indicated the presence of deer within some fenced areas, which could be due to red deer jumping the fences to gain food and shelter, or small numbers of roe deer can sometimes be trapped within fenced forests at the time of fence erection. The presence of small numbers of deer would help maintain a population of ticks within these large fenced areas. We also found evidence for more grouse and mountain hares using fenced than unfenced areas (assuming similar dung decomposition rates within fenced and unfenced areas); they may have been attracted by the higher ground vegetation associated with the fenced exlosures which was, presumably due to lower grazing pressure from deer (Table 1). Smaller hosts such as small mammals and passerine birds no doubt also played a role in tick population maintenance inside the fenced areas. Thus, the type of fencing is likely to affect the degree of tick control, depending on which hosts are excluded and which can still gain access to the fenced area. Fencing also affected ground vegetation height, presumably due to the decreased grazing pressure from deer. In turn, vegetation height, in addition to deer abundance index, negatively correlated with the number of nymphs counted per blanket drag. It is possible that blanket drag survey efficiency is affected by vegetation height, which indicates the importance of statistically taking into account vegetation height by including it in these models. Our finding that deer were more strongly associated with questing nymph abundance than was fencing presumably reflected the fact that some deer remained within fenced areas and that, in general, areas with fewer deer had fewer ticks and higher ground vegetation. Implications for pathogens and disease risk Pathogen prevalence is influenced by the relative number of competent pathogen transmission hosts relative to the number of incompetent, non-transmitting hosts (i.e., ‘‘dilution’’ hosts). Roe and red deer are considered incompetent hosts for B. burgdorferi s.l. and tick-borne encephalitis complex of viruses, including louping ill virus (Jaenson and Ta¨lleklint 1992, Jones et al. 1997). Fewer deer have sometimes been associated with higher prevalence of tick-borne encephalitis virus (Perkins et al. 2006) and B. burgdorferi s.l. (Gray et al. 1999) in the questing I. ricinus tick population, because


the ticks feed on alternative hosts such as small mammals that are competent pathogen transmitters. Deer density is well reported to affect communities of plants, small mammals, and birds (e.g., McShea and Rappole 2000, Smit et al. 2001). Therefore, it is likely that the higher ground vegetation we found in fenced areas, and in areas with lower deer abundance indices, may also support denser populations of other hosts such as small mammals, many of which are competent hosts of B. burgdorferi s.l. and A. phagocytophilum (e.g., Barandika et al. 2007). We also found evidence of higher usage by grouse and mountain hares in fenced than unfenced areas, and these hosts are known to be competent transmitters of louping ill virus (Reid 1975, Jones et al. 1997). This also implies that the type of fencing might affect pathogen prevalence because of the types of hosts that can gain access to the area. The opposite patterns of deer and ticks with pathogen prevalence have also been found, with fewer deer and/ or fewer ticks correlating with lower prevalences of B. burgdorferi s.l. in ticks (Ta¨lleklint and Jaenson 1996, Jouda et al. 2004, Altobelli et al. 2008). The implications of host management for pathogen prevalence in ticks are therefore not clear. However, disease risk is a more important parameter to human and animal health than pathogen prevalence in ticks. The risk of acquiring infection depends not only on pathogen prevalence in questing ticks but also, among other factors, on the risk of being bitten, which depends to a great extent on tick abundance. Tick abundance has sometimes been taken as a proxy for risk of Lyme borreliosis (Guerra et al. 2002, Jaenson et al. 2009) and tick-borne encephalitis (Daniel et al. 1998), while deer abundance has been positively associated with human cases of both tickborne encephalitis (Rizzoli et al. 2009) and Lyme borreliosis (Kilpatrick and LaBonte 2003). Therefore even if changes in host composition in fenced or heavily culled areas do increase pathogen prevalence in ticks, the risk of infection to an animal or human may actually be lower because of the drastic reduction in tick numbers. Management implications Our results show clearly that managing deer by excluding them (using both small-scale and large-scale fenced exclosures) or reducing their densities can control questing tick abundance by up to 96%. However, there can be serious issues with both deer management options. Fencing is expensive to construct and maintain, can look unsightly, and may impact on birds of conservation concern such as capercaillie and black grouse due to fence strikes (Baines and Summers 1997). Culling (or excluding with fences) any keystone species such as deer to reduce their population density can clearly have major ecological cascading effects on vegetation (as shown for vegetation height in our study), invertebrates, and vertebrates (McShea and Rappole 2000, Smit et al. 2001). Furthermore, in a multiuse landscape intensive deer culls can cause conflicts of

March 2012


PLATE 1.

665

Experimental fencing plot, site B. Photo credit: L. Gilbert.

interest between different stake-holding groups (e.g., the general public, hunters, and conservationists), between different management objectives of the landholding unit (e.g., conservation obligations vs. revenue from hunting), and between adjacent landholding units (e.g., red deer tend to move between estates, so management for low densities on one area could impact on the optimal hunting densities on neighboring land). While we found that even very small-scale fencing (0.25 ha) was highly effective in reducing tick abundance in heather moorland in Scotland, Perkins et al. (2006) found that small exclosures in forests may not only be ineffective, but may even increase pathogen prevalence in ticks due to changes in the composition of host types. Another study (Allan et al. 2003) found that small fragments of forest were associated with higher densities of Ixodes scapularis nymphs and higher prevalences of B. burgdorferi s.l., and therefore increased Lyme borreliosis risk, due to increased numbers of transmission hosts. While different deer densities were not implicated in Allan et al.’s study, and while Perkins et al. analyzed data from multiple tick species and did not take into account the length of time since fences were erected, these studies do suggest that spatial scale could be important when considering managing areas for tick control and disease risk mitigation. There are also temporal as well as spatial considerations. Development at each stage of the I. ricinus life

cycle takes approximately a year to complete. In removing the main ‘‘reproduction host’’ a high proportion of the adult tick population will be unable to feed, leading to less larval emergence the following year and fewer nymphs emerging the year after that. Therefore, the main impact on tick populations of introduced culling or fencing programs may be lagged by a few years from the start of implementation. Our study used deer management strategies that had been in place for 3–4 years (small-scale fencing), at least eight years (large-scale fencing), and many years (culling); it would be interesting to know the short-term effect of deer management on ticks. There is evidence (Ginsberg et al. 2002, Rand et al. 2004) that, for the first year or two, there can be an increase in abundance of questing ticks (although not necessarily an absolute increase in the total tick population). This can occur because ticks that would otherwise have attached and fed on deer (and therefore left the pool of questing ticks) are, instead, still questing. This could increase the risk of tick bites and infection to other animals, including humans. While our study suggests that traditional methods of managing deer abundance in an area by culling or exclusion can successfully reduce I. ricinus abundance, there are also more novel alternative ways of managing deer to control ticks. In particular, studies in the United States have shown successful reduction of questing I. scapularis ticks in response to treating white-tailed deer

666

L. GILBERT ET AL.

Odocoileus virginianus with acaricide (summarized by Pound et al. [2009]). These studies used ‘‘4-poster’’ feeding stations where the action of feeding caused the deer to rub their heads against one of four rollers impregnated with acaricide. Trials are required in other areas to test whether this approach could be useful for different species of ticks such as I. ricinus and different species of deer such as roe and red deer. In summary, our study provides strong evidence that both traditional deer management methods (fencing and culling) tested can dramatically reduce I. ricinus tick abundance, with implications for disease risk. We caution that the many other issues relating to these deer management methods are carefully considered before implementation. It is also possible that these deer management methods may not have the same effect in other areas that have different host communities or different tick species with different phenologies, ecologies, or host preference. ACKNOWLEDGMENTS We thank Justin Irvine for comments on the manuscript; Oliver Binks, Unai Plaza del Castillo, Martin Duncan, Gillian Green, Nigel Lammas, Ed Jones, and Fran Ruiz-Fons for field assistance; Richard Hewison for maintaining the experimental fencing plots; David Elston, Mark Brewer, and Jackie Potts for statistical advice; and the land owners and managers for permission to access study sites. L. Gilbert, S. Ramsay, and A. Hester were supported by the Scottish Government Rural Environment Research and Analysis Directorate. G. Maffey was supported by the University of Aberdeen and the Natural Environment Research Council. LITERATURE CITED Allan, B. F., F. Keesing, and R. S. Ostfeld. 2003. Effect of forest fragmentation on Lyme disease risk. Conservation Biology 17:267–272. Altobelli, A., B. Boemo, K. Mignoyyi, M. Bandi, R. Floris, G. Menardi, and M. Cinco. 2008. Spatial Lyme borreliosis risk assessment in north-eastern Italy. International Journal of Medical Microbiology 298:125–128. Baines, D., and R. W. Summers. 1997. Assessment of bird collisions with deer fences in Scottish forests. Journal of Applied Ecology 34:941–948. Barandika, J. F., A. Hurtado, C. Garcı´ a-Esteban, H. Gil, R. Escudero, M. Barral, I. Jado, R. A. Juste, P. Anda, and A. L. Garcı´ a-Pe´rez. 2007. Tick-borne zoonotic bacteria in wild and domestic small mammals in northern Spain. Applied and Environmental Microbiology 73:6166–6171. Brown, K. J., X. Lambin, G. R. Telford, N. H. Ogden, S. Telfer, Z. Woldehiwet, and R. J. Birtles. 2008. Relative importance of Ixodes ricinus and Ixodes trianguliceps as vectors of Anaplasma phagocytophilum and Babesia microti in field vole (Microtus agrestis) populations. Applied and Environmental Microbiology 74:7118–7125. Cross, P. C., W. H. Edwards, B. M. Scurlock, E. J. Maichak, and J. D. Rogerson. 2007. Effects of management and climate on elk brucellosis in the Greater Yellowstone Ecosystem. Ecological Applications 17:957–964. Daniel, M., J. Kola´rˇ, P. Zeman, K. Pavelka, and J. Sa´dlo. 1998. Predictive map of Ixodes ricinus high-incidence habitats and a tick-borne encephalitis risk assessment using satellite data. Experimental and Applied Acaralogy 22:417–433. Daniels, T. J., and D. Fish. 1995. Effect of deer exclusion on the abundance of immature Ixodes scapularis (Acari: Ixodidae)


parasitizing small and medium-sized mammals. Journal of Medical Entomology 32:5–11. Elston, D. A., R. Moss, T. Boulinier, C. Arrowsmith, and X. Lambin. 2001. Analysis of aggregation, a worked example: numbers of ticks on red grouse chicks. Parasitology 122:563– 569. Eves, J. A. 1999. Impact of badger removal on bovine tuberculosis in east County Offaly. Irish Veterinary Journal 52:199–203. Gilbert, L. 2010. Altitudinal patterns of tick and host abundance: a potential role for climate change in regulating tick-borne diseases? Oecologia 162:217–225. Gilbert, L., L. D. Jones, P. J. Hudson, E. A. Gould, and H. W. Reid. 2000. Role of small mammals in the persistence of louping-ill virus: field survey and tick co-feeding studies. Medical and Veterinary Entomology 14:277–282. Gilbert, L., R. Norman, K. M. Laurenson, H. W. Reid, and P. J. Hudson. 2001. Disease persistence and apparent competition in a three-host community: an empirical and analytical study of large-scale, wild populations. Journal of Animal Ecology 70:1053–1061. Ginsberg, H. S., M. Butler, and E. Zhioua. 2002. Effect of deer exclusion by fencing on abundance of Amblyomma americanum (Acari: Ixodeidae) on Fire Island, New York, USA. Journal of Vector Ecology 27:215–221. Ginsberg, H. S., E. Zhioua, S. Mitra, J. Fischer, P. A. Buckley, F. Verret, H. B. Underwood, and F. G. Buckley. 2004. Woodland type and spatial distribution of nymphal Ixodes scapularis (Acari: Ixodidae). Environmental Entomology 33:1266–1273. Gray, J. S. 1998. The ecology of ticks transmitting Lyme borreliosis. Experimental and Applied Acarology 22:249– 258. Gray, J. S., F. Kirstein, J. N. Robertson, J. Stein, and O. Kahl. 1999. Borrelia burgdorferi sensu lato in Ixodes ricinus ticks and rodents in a recreational park in south-western Ireland. Experimental and Applied Acarology 23:717–729. Guerra, M., E. Walker, C. Jones, S. Paskewitz, M. R. Cortinas, A. Stancil, L. Beck, M. Bobo, and U. Kitron. 2002. Predicting the risk of Lyme disease: habitat suitability for Ixodes scapularis in the north central United States. Emerging Infectious Diseases 8:289–297. Harrison, A., S. Newey, L. Gilbert, D. T. Haydon, and S. J. Thirgood. 2010. Culling wildlife hosts to control disease: mountain hares, red grouse and louping ill virus. Journal of Applied Ecology 47:926–930. Holt, R. D. 1977. Predation, apparent competition, and the structure of prey communities. Theoretical Population Biology 12:197–229. Jaenson, T. G. T., L. Eisen, P. Comstedt, H. A. Mejlon, E. Lindgren, S. Bergstro¨m, and B. Olsen. 2009. Risk indicators for the tick Ixodes ricinus and Borrelia burgdorferi sensu lato in Sweden. Medical and Veterinary Entomology 23:226–237. Jaenson, T. G. T., and L. Ta¨lleklint. 1992. Incompetence of roe deer (Capreolus capreolus) as reservoirs of the Lyme disease spirochete. Journal of Medical Entomology 29:813–817. Jones, L. D., M. Gaunt, R. S. Hailes, K. Laurenson, P. J. Hudson, H. Reid, P. Henbest, and E. A. Gould. 1997. Transmission of louping ill virus between infected and uninfected ticks co-feeding on mountain hares. Medical and Veterinary Entomology 11:172–176. Jouda, F., J. L. Perret, and L. Gern. 2004. Density of questing Ixodes ricinus nymphs and adults infected by Borrelia burgdorferi sensu lato in Switzerland: spatio-temporal pattern at a regional scale. Vector-borne and Zoonotic Diseases 4:23– 32. Kiffner, C., C. Lo¨dige, M. Alings, T. Vor, and F. Ru¨he. 2010. Abundance estimation of Ixodes ticks (Acari: Ixodidae) on roe deer (Capreolus capreolus). Experimental and Applied Acarology 52:73–84.

March 2012


Kilpatrick, H. J., and A. M. LaBonte. 2003. Deer hunting in a residential community: the community’s perspective. Wildlife Society Bulletin 31:340–348. Kirby, A. D., A. A. Smith, T. G. Benton, and P. J. Hudson. 2004. Rising burden of immature sheep ticks (Ixodes ricinus) on red grouse (Lagopus lagopus scoticus) chicks in the Scottish uplands. Medical and Veterinary Entomology 18:67–70. Laddomada, A. 2000. Incidence and control of CSF in wild boar in Europe. Veterinary Microbiology 73:121–130. Laurenson, M. K., R. A. Norman, L. Gilbert, H. W. Reid, and P. J. Hudson. 2003. Identifying disease reservoirs in complex systems: mountain hares as reservoirs of ticks and louping-ill virus, pathogens of red grouse. Journal of Animal Ecology 72:177–185. McShea, W. J., and J. H. Rappole. 2000. Managing the abundance and diversity of breeding bird populations through manipulations of deer populations. Conservation Biology 14:1161–1170. Mejlon, H. A., and T. G. T. Jaenson. 1997. Questing behavior of Ixodes ricinus ticks (Acari: Ixodidae). Experimental and Applied Acarology 21:747–754. Melis, C., A. Buset, P. A. Aarrestad, O. Hanssen, E. L. Meisingset, R. Andersen, A. Moksnes, and E. Røskaft. 2006. Impact of red deer Cervus elaphus grazing on bilberry Vaccinium myrtillus and composition of ground beetle (Coleoptera, Carabidae) assemblage. Biodiversity and Conservation 15:2049–2059. Mills, L. S., M. E. Soule´, and D. F. Daok. 1993. The keystonespecies concept in ecology and conservation. BioScience 43:219–224. Perkins, S. E., I. M. Cattadori, V. Tagliapietra, A. P. Rizzoli, and P. J. Hudson. 2006. Localized deer absence leads to tick amplification. Ecology 87:1981–1986. Pound, J. M., J. A. Miller, J. E. George, D. Fish, J. F. Carroll, T. L. Schulze, T. J. Daniels, R. C. Falco, K. C. Stafford III, and T. N. Mather. 2009. The United States Department of Agriculture’s Northeast area-wide tick control project: summary and conclusions. Vector-Borne and Zoonotic Diseases 9:439–448. Rand, P. W., C. Lubelczyk, M. S. Holman, E. H. Lacombe, and R. P. Smith, Jr. 2004. Abundance of Ixodes scapularis (Acari: Ixodidae) after complete removal of deer from an isolated offshore island, endemic for Lyme disease. Journal of Medical Entomology 41:779–784.

667

Reid, H. W. 1975. Experimental infection of red grouse with louping ill virus (flavivirus group). I. The viraemia and antibody response. Journal of Comparative Pathology 85:223–229. Rizzoli, A., H. C. Hauffe, V. Tagliapietra, M. Neteler, and R. Rosa´. 2009. Forest structure and roe deer abundance predict tick-borne encephalitis risk in Italy. PLoS ONE 4: e4336. Roffe, T. J., L. C. Jones, K. Coffin, M. L. Drew, S. J. Sweeney, S. D. Hagius, P. H. Elzer, and D. Davis. 2004. Efficacy of single calfhood vaccination of elk with Brucella abortus strain 19. Journal of Wildlife Management 68:830–836. Ruiz-Fons, F., and L. Gilbert. 2010. The role of deer (Cervus elaphus and Capreolus capreolus) as vehicles to move ticks Ixodes ricinus between contrasting habitats. International Journal of Parasitology 40:1013–1020. SAS Institute. 2002–2003. SAS software, version 9.1.3. SAS Insitute, Cary, North Carolina, USA. Scharlemann, J. P. W., P. J. Johnson, A. A. Smith, D. W. Macdonald, and S. E. Randolph. 2008. Trends in ixodid tick abundance and distribution in Great Britain. Medical and Veterinary Entomology 22:238–247. Smit, R., J. Bokdam, J. den Ouden, H. Olff, H. SchotOpschoor, and M. Schrijvers. 2001. Effects of introduction and exclusion of large herbivores on small rodent communities. Plant Ecology 155:119–127. Stafford, K. C., A. J. Denicola, and H. J. Kilpatrick. 2003. Reduced abundance of Ixodes scapularis (Acari: Ixodidae) and the tick parasitoid Ixodiphagus hookeri (Hymenoptera: Encyrtidae) with reduction of white-tailed deer. Journal of Medical Entomology 40:642–652. Ta¨lleklint, L., and T. G. T. Jaenson. 1996. Relationship between Ixodes ricinus density and prevalence of infection with Borrelia-like spirochetes and density of infected ticks. Journal of Medical Entomology 33:805–811. Ward, A. I. 2005. Expanding ranges of wild and feral deer in Great Britain. Mammal Review 35:165–173. Wilson, M. L., A. M. Ducey, T. S. Litwin, T. A. Gavin, and A. Spielman. 1990. Microgeographic distribution of immature Ixodes dammini ticks correlated with deer. Medical and Veterinary Entomology 4:151–159. Woodroffe, R., C. A. Donnelly, D. R. Cox, F. J. Bourne, C. L. Cheeseman, R. J. Delahay, G. Gettinby, J. P. McInerney, and W. I. Morrison. 2006. Effects of culling on badger Meles meles spatial organization: implications for the control of bovine tuberculosis. Journal of Applied Ecology 43:1–10.