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Environmental parameters affecting tick (Ixodes ricinus) distribution during the summer season in Richmond Park, London

Environmental parameters affecting tick (Ixodes ricinus) distribution during the summer season in... Volume 4 † Number 2 † June 2011 10.1093/biohorizons/hzr016 Advance Access publication 4 May 2011 ......................................................................................................................................................................................................................................... Research article Environmental parameters affecting tick (Ixodes ricinus) distribution during the summer season in Richmond Park, London B.P.J. Greenfield* Department of Biosciences, College of Science, Swansea University, Singleton Park, Swansea SA2 8PP, UK. * Corresponding author: Email: 485572@swan.ac.uk Supervisor: Prof. Tariq M. Butt, Department of Biosciences, College of Science, Swansea University, Singleton Park, Swansea SA2 8PP, UK. ........................................................................................................................................................................................................................................ Ixodes ricinus, the sheep tick, as a consequence of its habit of taking blood from mammalian hosts, can transmit disease from wild animals to humans. This is likely to be a particular problem in parks shared by humans and deer populations. These ticks were sampled, using cloth drags, from vegetation at 16 sites in Richmond Park, London, between 15 July and 22 August 2009. A total of 2436 ‘host-seeking’ ticks (2281 larvae, 151 nymphs and 4 adults; three males and one female) were collected, and attempts were made to identify the environmental factors affecting the distribution of these ectoparasites. Tick presence was closely related to soil moisture, light levels and humidity through- out the park. It is thought that improving our understanding of how these factors influence the presence of I. ricinus will facilitate methods of tick control and help to educate the public about where ‘hotspots’ for these parasites are likely to be within the park. Key words: sheep tick, Ixodes ricinus, distribution, ecological parameters, questing nymphs. Submitted September 2010; accepted March 2011 ........................................................................................................................................................................................................................................ with the deterioration of host health, including weight loss Introduction and breeding success. Biology of Ixodes ricinus Ticks are closely related to mites, belonging to the sub- class Acari. Characterized by having four pairs of legs, Aristotle described ticks as ‘disgusting parasitic animals’, a they belong within the class of Arachnida. The larvae, view with which many people would not disagree. Ixodes however, only have three pairs of legs. Like other arachnids, ricinus, more commonly known as the sheep tick, is a hae- they possess chelicerae and palps and they lack both wings matophagous ectoparasite, belonging to the Ixodidae and antennae. Ticks have a unique sensory organ, Haller’s family. Ticks are widely distributed in a range of habitat organ, situated on the front tarsi, used in detecting environ- types, including heath, coniferous and deciduous woods, mental stimuli such as changes in temperature, carbon grassland and rough pastures. The presence or absence of dioxide levels and humidity. These can be observed ticks is highly dependent on local microclimate conditions, waving, emulating antennae, in a process called questing. which are largely determined by sward height and humidity. They also possess a hypostome that enables the tick to Ticks have a diverse range of vertebrate hosts from which attach to the hosts skin when the tick feeds; these character- they feed, affecting 240 species of wild and domesticated istics distinguish ticks from mites. Ticks are typically a three mammals, many species of birds and reptiles. host species and their development occurs in four life stages, Their ability to survive in such a diversity of habitat types passing through an egg, larva, nymph and adult stage and parasitize a multitude of hosts makes ticks a vector of (Fig. 1). interest over recent years. They are highly problematic in the Ixodid ticks are often referred to as ‘hard’ ticks due to the sheep-farming and grouse-shooting industries, causing huge presence of a tough outer scutum, a hard sclerotized dorsal economic losses of several billion dollars per year, globally, ......................................................................................................................................................................................................................................... The Author 2011. Published by Oxford University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.5), which permits unrestricted non-commercial use, distri- bution, and reproduction in any medium, provided the original work is properly cited. 140 Bioscience Horizons † Volume 4 † Number 2 † June 2011 Research article ......................................................................................................................................................................................................................................... 10,11 of many tick-borne diseases; as a result, ticks are of paramount importance globally, due to the implications on both human and livestock health. It is important to under- stand how ticks affect both wild and domestic populations of animals to accurately predict the risk of an outbreak of these diseases. Figure 1. Life stages of Ixodes ricinus (larvae, nymph, adult male, adult Microclimate female) 10 magnification. Tick survival and development are dependent on many factors, primarily the humidity and moisture content of a Table 1. Tick-borne diseases present in the UK 13 1 microclimate. Macleod determined that I. ricinus was Disease caused Causative agent Affects References only to be found in hill pastures, as only here would the ................................................................................................................ tick find the ‘definite conditions of soil and vegetation’ to Lyme disease Borrelia burgdorferi Humans 8 ensure its survival throughout the summer season. Milne Babesiosis Babesia divergens, Cattle (red-water 8 ascertained that mat depth was an important factor in B. microti fever), humans maintaining the microclimatic conditions required by the Tick-borne Flavivirus Humans 9 tick, with a thicker mat being able to retain more water encephalitis thus improving the survival of the ticks. A thicker mat also Louping Ill Virus Viral agents Sheep, grouse, 8,9 provides more niches for ticks to occupy. It was later red deer, hares, shown that the removal of this mat layer increased the desic- rabbits, humans cation rate of the tick, reducing tick numbers. Both 18 16,17 Tularemia Francisella tularensis Humans, cats, 8 Milne and Macleod noted that unfed ticks require a sheep, rabbits, relative humidity above 80% to survive, with anything less rodents having a detrimental effect on the ticks survival. It is there- fore believed that humidity is a fundamental factor influen- Bovine and ovine Anaplasma Cattle, sheep, 6,8 cing tick survival. Humidity has a profound effect on tick tick-borne fever phagocytophilum goats, wild activity, primarily controlling the amount of time a tick complex ruminants can spend questing. When a tick ascends from the mat and Crimean-Congo Nairovirus Humans, cattle, 8 up the vegetation to quest, it becomes highly prone to desic- haemorrhagic fever sheep, goats cation, prompting the tick to retreat back into the mat to Human Ehrlichia/Anaplasma Humans 6 restore its water balance before questing again. granulocytic sp. ehrlichiosis Global warming Boutonneuse fever Rickettsia sp. Humans, dogs, 8 Seasonal variations in temperature due to global warming rabbits, rodents can result in a dramatic impact on how often hosts and pathogen-carrying vectors come into contact. Changes in temperature are detected by Haller’s organ; at temperatures plate, this feature provides sexual dimorphism in the tick as ,78C, ticks remain inactive only venturing out of the mat the scutum completely covers the idiosoma of an adult male, and up the vegetation to quest for a host when temperatures 19,20 whereas the female is partially covered, revealing the alloscu- increase. Many vector-borne diseases are highly suscep- 21 22 tum, this feature allows the female tick to engorge during a tible to changes in climate; Danielova ´ et al. found that blood meal. increasing temperatures not only increase the distribution Ticks are the primary vector for a number of transmissible of I. ricinus, but also linked the rise in temperatures to the pathogens, transmitting more pathogens than any other encroachment of ticks into higher altitudes that were not pre- arthropod vector group with an estimated 10% of all tick viously colonized by ticks. As a consequence, a correlation is species being a vector. Ticks are second only to mosquitoes formed between increase in temperature and increase in the for vectoring human diseases. Many of the diseases prevalence of tick-borne diseases, such as Borreliosis and transmitted by ticks are of huge medical and veterinary tick-borne encephalitis. 8 23 importance (Table 1). Ixodes ricinus in the UK is also the Gray hypothesized that with increasing summer temp- primary vector for Anaplasma phagocytophilum causing eratures, based on the degree-day model, averaging at 308C equine ehrlichiosis and human granulocytic ehrlichiosis and winters that will be relatively frost-free, there will be a and louping ill virus that causes encephalitis in sheep. shift in nymphal and adult activity, occurring in late Recently, there has been a notable increase in the prevalence autumn to early winter. It is also suggested that I. ricinus ......................................................................................................................................................................................................................................... 141 Research article Bioscience Horizons † Volume 4 † Number 2 † June 2011 ......................................................................................................................................................................................................................................... larvae will not undergo developmental diapause and remain trees (Quercus robur), and acidic grasslands; at the heart of active throughout the summer to early spring. the park, there are two large artificial ponds that make up Pen Ponds, and the vast grasslands of Richmond Park are Aims and justification home to 650 deer, predominantly red deer (Cervus elaphus) and fallow deer (Dama dama). Along with This project aimed to determine the environmental par- acidic grass, there is also a large quantity of Bracken ameters that affect the distribution of ticks along the (Pteridium aquilinum). Tamsin trail, a major walking path in Richmond Park. It Richmond Park is also an SSSI (Site of Special Scientific was anticipated that this investigation would identify areas Interest) due to its population of deadwood beetle fauna, of ‘hotspot’ activity and consequently indicate the risk of many of which are Red Data Book Species; there are exposure to ticks and their transmitted diseases. approximately 135 beetle species recorded in the park, 75 Sorouri-Zanjani ascertained 13% of the tick population, of which are dung species including Aphodius zenkeri,a within Richmond Park, carry Borrelia burgdorferi. nationally restricted species. Richmond Park is popular with tourists, attracting hun- A total of 16 sites were located along the Tamsin Trail in dreds of people a month. The park is also home to a large Richmond Park, London. Surveys were conducted on a total number of deer, which act as a primary host for I. ricinus. of 23 days between 15 July and 22 August, as this is the time It was important to conduct this study over the summer as of peak activity of humans within the park (Fig. 2). There this is the peak time of human activity within the park, with were no surveys undertaken during this period if there was the assumption that weather is nicer and therefore more heavy rainfall. The Tamsin Trail was chosen as it is a people will visit the park. This also coincides with the life popular trail for both dog walkers and hikers within the cycle of the tick resulting in peak larval activity during the park; it is therefore one of the main interfaces between summer season. humans, their pets and ticks. A survey by Reeve and A study by Medlock et al. on the ecological and environ- Jones ascertained that Richmond Park is home to five mental determinants for the presence of I. ricinus on the main species of small mammal that are important hosts for Gower, South Wales, concluded that there are numerous I. ricinus and reservoirs for B. burgdorferi: bank vole biotic factors influencing the presence of I. ricinus.Itis (Myodes glareolus), field vole (Microtus agrestis), wood suggested from these factors that one can predict areas mouse (Apodemus sylvaticus), common shrew (Sorex likely to be tick ‘hotspots’; in order to do this effectively, araneus) and pygmy shrew (S. minutus). there is a need for more studies investigating the presence and the absence of ticks. In understanding how environ- Sampling design mental factors influence the presence or the absence of quest- A1 m piece of polycotton cloth was fastened, at the leading ing I. ricinus, it is possible to further improve the methods of edge, to a 1.25 m wooden bar, leaving a 25 cm handle. The tick control and also help to educate those that frequent cloth was laid flat, adjacent and parallel to the path, and Richmond Park where I. ricinus prevalent areas lie within dragged along subtransects of 5 m by slow pacing to the park. optimize the collection of ticks; it is assumed that these Although there are essential distribution maps for the UK ticks are questing ticks. This was repeated 20 times within that depict national distribution of I. ricinus, much of the a location with a separation of 10 m between drags giving data contained within these come from historical data and an overall 100 m transect. This complied with a method do not necessarily mean factors that influence the distri- described by Milne. bution of I. ricinus in areas such as Wales will be the same All ticks found attached to the underside of the cloth, i.e. as those influencing the distribution in London or other the area in contact with the vegetation, were collected using a areas of the UK; it is therefore important to determine pair of fine point tweezers, counted and placed in an biotic and abiotic factors influencing the spatial heterogen- Eppendorf tube containing 70% ethanol to fix the ticks. eity within individual areas. Eppendorf tubes were assigned a specific code to identify It is becoming ever more important for such studies with where each drag was conducted. The ticks were later ident- increasing distribution and abundance of I. ricinus result- ified using an identification key found in Hillyard. If, ing in an increase in the prevalence of Lyme borreliosis in however, there was heavy rain, thus soaking the cloth, sur- the UK. veying was postponed until weather was suitable, allowing standardization of flag condition. Materials and methods Variables Study site Several variables were measured at the start of each 5 m drag Richmond Park is a National Nature Reserve situated in along with the time, date and section code. All variables were London containing 955 ha of woodland, primarily oak recorded on the survey sheet. ......................................................................................................................................................................................................................................... 142 Bioscience Horizons † Volume 4 † Number 2 † June 2011 Research article ......................................................................................................................................................................................................................................... TM Figure 2. Map of Richmond Park (Google earth map) depicting the Tamsin trail (yellow) and the 16 survey sites (red). Ground-derived variables Statistical analysis TM A TinyTag Data Logger, placed in one location for the All these data were analysed using the G-test goodness of fit, 2 33 entirety of the project, was used to obtain the overall a more robust alternative to the traditional x test, to test if humidity, measured as a per cent of relative humidity there is any significant difference in frequency of questing (%RH) and temperature (8C). At the start of each fresh ticks in relation to the variables measured. The association transect, three soil moisture readings were recorded at 0, between ordinal data and the presence was analysed using 1.5 and 5 m along the transect using a theta soil moisture R  C contingency tables. Logistic regression was performed probe and an HH2 soil moisture meter (Delta-T Devices on all the variables using SPSS version 16.0 (Chicago, IL, Ltd, Cambridge, UK). Ambient temperature (8C) was USA). measured with a bulb thermometer. Light levels rep- resented by exposure values (EVs) were recorded using a Polaris Light Meter, and they were taken three times to Results obtain an average. Cloud coverage was measured on an A total of 2436 I. ricinus were collected during 320 transect ordinal scale of 0 – 8 oktas, rainfall was taken samples (2281 larvae, 151 nymphs and 4 adults; three males categorically by observation (no rain, 0; drizzling, 1; and one female) (Table 2), 67.5% were positive drags and heavy rain, 2). 32.5% were negative, 8 of the 16 variables measured had a significant effect on the frequency of ticks. Vegetation The 16 surveyed sites were separated into eight categories Sward height (mm) and mat depth (mm) were measured with depending on their compass orientation. a clear plastic 30 cm ruler and tape measure if the sward Ticks were present in fewer numbers at higher sward height exceeded 30 cm. The mat depth was measured by heights, with ticks being more abundant between 151 and pushing the ruler into the ground until met by resistance 300 mm. There was a very strong significant difference in then recording the depth. The vegetation type on both the the proportion of frequency of ticks in different sward survey side and opposite side was recorded, by observation, heights (G ¼ 1965.93, P  0.001, df ¼ 9). noting down the dominate vegetation types. Path width (m) Soil moisture was closely associated with the presence of and substrate and the ride width (m) measured by placing a ticks. With a modal class of 5.1 – 10% (mode ¼ 8.6%), tape measure across the path. Penetrability of the ride was ticks were more frequent in lower soil moistures, and there recorded on a categorical scale: walk, run and fight. is a strong significant difference in the proportion of ticks ......................................................................................................................................................................................................................................... 143 Research article Bioscience Horizons † Volume 4 † Number 2 † June 2011 ......................................................................................................................................................................................................................................... present at differing soil moistures (G ¼ 19.34, P  0.01, significant relationship between humidity and the presence df ¼ 7). of ticks (G ¼ 137.652, P  0.001, df ¼ 4), with ticks occur- There was a bimodal peak of tick abundance over the ring more frequently in lower humidities (Modal class ¼ temperatures sampled one at 21.0 – 25.98C and the other at 0.0 – 20.0%RH, mode ¼ 0.0%). 16.0 – 20.98C. Note that no temperatures were recorded Light levels appear to have an influence on the presence of ,16.08C. There was a significant difference between temp- ticks; indeed, a G-test confirmed there is a significant differ- erature and the presence of ticks (G ¼ 323.494, P  ence between differing light levels and the presence of ticks adj 0.001, df ¼ 3; modal class ¼ 21.0 – 25.98C, mode ¼ 23.08C). (G ¼ 274.592, P  0.001, df ¼ 13). Table 3 highlights adj Quantitatively there was a relationship between humidity the number of ticks found at each sample site in correlation and the presence and absence of ticks (Fig. 3). There is a with environmental parameters measured. Table 2. Number of ticks found at each location Logistic regression Location Larvae Nymph Adult male Adult female Total ................................................................................................................ Logistic regression analysis was used to predict variables that A14 1 0 0 15 influence the presence and the absence of I. ricinus.It appears that soil moisture, light levels and humidity are all B 585 65 0 0 650 significant predictors for the presence of I. ricinus, whereas C41 2 0 0 43 the other variables sward height, mat depth and ambient D45 4 0 0 49 temperature were not considered to significantly influence E58 10 0 0 68 the presence of I. ricinus in the model produced. ‘Step 1’ in F21 0 0 0 21 the classification table (Table 4) represents the overall per G91 0 1 0 92 cent of presence and absences that are correctly predicted H 193 1 0 0 194 by the model using soil moisture as the only variable. With I64 0 0 0 64 subsequent steps, the percentage increases from 67.8% for J 198 19 0 0 217 the null model to 70.6% in ‘step 2’ where soil moisture is K 333 8 1 1 343 combined with light levels, and again to 71.9% for the full L 181 23 0 0 204 model, ‘step 3’. ‘Step 3’ is therefore a more accurate model, M 149 9 1 0 159 successfully predicting the presence and the absence of ticks based on soil moisture, light levels and humidity N 116 7 0 0 123 which all exert a significant effect in their own right reinfor- O 108 0 0 0 108 cing the significance of the overall model (‘step 3’ P ¼ 0.001; P84 2 0 0 86 Table 5). Figure 3. Number of ticks at each relative humidity recorded. ......................................................................................................................................................................................................................................... 144 Bioscience Horizons † Volume 4 † Number 2 † June 2011 Research article ......................................................................................................................................................................................................................................... Table 3. Number of ticks present at each sample site in relation to environmental parameters Location Average ambient Average cloud Average sward Average mat Average soil Average light Total Total Total temperature (8C) coverage (oktas) height (mm) depth (mm) moisture (%) levels (Ev) larvae nymphs adults ........................................................................................................................................................................................................................................ A 23.98 5.95 307.65 4.50 7.78 11.60 14 1 0 B 20.80 5.25 217.50 8.75 13.44 9.80 585 65 0 C 23.65 7.75 189.50 4.10 5.51 10.65 41 2 0 D 22.65 6.85 188.00 3.85 8.21 10.60 45 4 0 E 21.03 4.90 283.20 5.30 20.67 9.83 58 10 0 F 20.95 6.85 458.50 2.95 19.74 10.65 21 0 0 G 25.20 5.70 712.75 4.55 13.28 12.20 91 0 1 H 25.60 4.90 281.00 6.20 7.99 10.70 193 1 0 I 26.43 5.00 279.50 4.90 19.31 11.55 64 0 0 J 24.18 6.30 236.50 5.38 12.49 10.33 198 19 0 K 23.00 6.55 304.00 9.30 14.30 11.10 333 8 2 L 21.55 6.10 216.50 3.88 18.45 10.65 181 23 0 M 29.60 0.95 239.00 6.90 8.00 10.55 149 9 1 N 21.40 6.20 412.50 4.65 11.98 10.05 116 7 0 O 25.60 6.75 309.50 3.60 9.75 11.05 108 0 0 P 22.10 7.65 273.00 6.40 13.47 10.30 84 2 0 Grand 23.61 5.85 306.79 5.33 12.77 10.73 2281 151 4 total Table 4. Output of logistic regression Table 5. Variables in the Equation Observed Predicted B SE Wald df Sig. ................................................................................................................ Binary Percentage correct Step 1(a) Soil moisture 0.066 0.020 11.195 1 0.001 0.00 1.00 ................................................................................................................ Constant 20.072 0.259 0.077 1 0.782 Step 1 Step 2(b) Binary Soil moisture 0.072 0.020 12.569 1 0.000 0.00 1 103 1.0 Light levels 20.274 0.082 11.110 1 0.001 1.00 0 216 100.0 Constant 2.819 0.906 9.671 1 0.002 Overall percentage 67.8 Step 3(c) Step 2 Soil moisture 0.065 0.021 9.770 1 0.002 Binary Light 20.260 0.083 9.827 1 0.002 0.00 19 85 18.3 Humidity 20.006 0.003 5.103 1 0.024 1.00 9 207 95.8 Constant 3.076 0.926 11.043 1 0.001 Overall percentage 70.6 Step 3 Binary ticks, elucidating which factors are essential for predicting 0.00 27 77 26.0 ‘hotspot’ areas. Tick activity has been associated with water balance regulation, namely ambient temperature and 1.00 13 203 94.0 relative humidity. It has been demonstrated that Overall percentage 71.9 I. ricinus, typically begin to quest at 45%RH and an ambient temperature of 2.58C. This study revealed that there was a higher abundance of I. ricinus between 21.0 and 25.98C, temperatures exceeding this (26.0 – 40.08C) Discussion were associated with less numbers of I. ricinus. This is not The study aimed to define which of the environmental surprising as ticks are more likely to be found in the mat parameters were influential on the presence and absence of in extreme temperatures to prevent desiccation. Lower ......................................................................................................................................................................................................................................... 145 Research article Bioscience Horizons † Volume 4 † Number 2 † June 2011 ......................................................................................................................................................................................................................................... temperatures (16.0 – 20.98C) significantly reduced the taller sward heights, due to an increase in the variation of numbers of ticks recovered during dragging. It is important vegetation heights. Ticks will quest at the tips of each plant to note that no temperatures ,168C were recorded, during thus dispersing the ticks at uneven heights throughout the the day, throughout this project. Further work is needed to entire plant resulting in a larger proportion of ticks being assess the occurrence of ticks at a broad range of tempera- missed during the drag. Low sward heights (0 – 45 mm) tures typical of a temperate climate. were shown to be less suitable for ticks with drags containing Previous studies, notably those by Milne and Medlock sward heights within this range only producing negative et al., ascertained temperatures during the day, soil moist- drags. ure and high cloud coverage had a large influence on the This project was less concerned with the underlying topo- presence of questing ticks. Here, it was found that the pres- graphy of the land to determine aspect, and the presence ence of ticks was closely associated with low soil moisture. and the absence were, however, analysed based on the This is in contrast to previous studies and suggests that tick locations orientation on the O.S. map. It was found that ecology may be more complex than previously thought. there was a significant difference in the presence of ticks in Another variable appearing contradictory to previous the south of the park, i.e. along transects between Robin studies is relative humidity, with a larger number of ticks Hood gate and Isabella Plantation, compared with the rest associated within the modal class of 0.0 – 20.0%RH, a of the park. In addition, sites located in the east (Sheen value comparatively lower than the 80%RH required for gate – Roehampton gate and Roehampton gate – Robin Hood 13 36 survival stated by Macleod. Arthur has suggested that gate) and northwest (Pembroke lodge – Kingston gate and between 86 and 96%RH, the ticks water balance is in equi- Ham gate – Richmond gate) of the park, presented no signifi- librium with the atmosphere, allowing the tick to gain moist- cant differences between the presence and the absence of ticks. ure from the air at a higher humidity and, conversely, loose Vegetation structure plays a large role in the presence and water when humidity is low. At this point, it is not clear the absence of ticks. Ticks are often recorded in woodland why this trend has occurred and it is subject to follow-up habitats, as this habitat provides a dense shrub layer; habitats work. with bracken, however, will also provide a suitable habitat. Studies have shown that it is not favourable for the ticks to This is reflected in this study as sites with high bracken 18,37 be present in higher humidities, as they become prone to content, such as areas in the south, north, northeast and over saturation thus limiting their activities. southwest orientations, had larger numbers of ticks present Although tick presence increased with increasing cloud in comparison with sites with little or no bracken. coverage, there was no significance between the varying Similarly, a large number of sites with conditions highly levels of cloud coverage and the presence of ticks. suitable for ticks were in fact associated with very low 1,16 Mat depth has been considered one factor influencing the numbers of ticks. Conversely, areas that did not appear presence of ticks and indeed; this survey showed that mat to be particularly favourable, e.g. transects between depth does have a significant effect on the presence of Richmond gate and Sheen gate which had very little veg- ticks. Logistic regression analysis, however, does not con- etation cover and variation in vegetation, comparatively sider mat depth to be fundamental in predicting the presence low sward heights and relatively low soil moistures, pro- of ticks. Locations with mat depths exceeding 10 mm are not duced over a quarter (26.68%) of the total ticks collected. associated with large numbers of ticks. This is counter- These locations did, however, have a large amount of leaf intuitive as one would suppose ticks would prefer a much litter, thus providing abundant mat, suggesting that grass is thicker mat as there would be less chance of desiccation not key to tick presence and it could be ground coverage once the tick has retreated down the sward into the mat. per section. The mat level is required for the ticks to restore their water Grassland is often considered to be relatively unsuitable balance as humidity is generally higher in the mat. This for ticks; nonetheless, I. ricinus is often found in grazed is important as ticks alternate frequently between questing pastures and this was also found in this study with a on vegetation, where they rapidly loose water through the total of 386 (15.85%) ticks collected on open grassland cuticle via evaporation, and quiescence, a process through (area between Roehampton gate and Robin Hood gate). which they actively reabsorb water from the atmosphere, in With respect to the vegetation type and ride penetrability, the mat level. Also with a thicker mat, there would be a their effect on the presence and the absence of ticks is mostly much higher probability of ticks coming into contact with likely due to their influence on host presence. There are small mammals, as small mammals are more likely to fre- numerous organisms acting as hosts for I. ricinus. Larvae quent areas with a more dense vegetation and mat depth. feed upon small mammals and birds, whereas deer tend to The presence of ticks was greatest at medium sward support ticks at each stage, deer are an extremely important heights (151 – 300 mm); there was a significant decrease in host for adult I. ricinus. As a result, areas that are densely the occurrence of ticks at higher sward heights. This is not vegetated will provide a more suitable habitat for these surprising as sampling accuracy is largely decreased at hosts, thus directly increasing the abundance of ticks. ......................................................................................................................................................................................................................................... 146 Bioscience Horizons † Volume 4 † Number 2 † June 2011 Research article ......................................................................................................................................................................................................................................... Interestingly, it was found that light levels significantly throughout the entire park based on the soil moisture, influenced the presence of ticks; indeed, logistic regression humidity and light levels. Repeats of this study would help considered light levels to be a fundamental variable for pre- to further enhance the effects of environmental parameters dicting abundance. With a modal class of 10 EVs, it is effecting the distribution. The data that were obtained can suggested that this is the optimum light intensity for questing be used to inform those that frequent Richmond Park ticks, with intensities above this level significantly reducing where I. ricinus ‘hotspots’ are and act as a warning to the number of ticks captured. Lees has shown that under reduce the risk of exposure to ticks. It would be beneficial continual exposure to high intensities of light, I. ricinus to assess the levels of transmissible pathogens present remains at rest and only begins questing in response to a within Richmond Park, relating not only to public health fall in light intensity. It has also be hypothesized that but also to wild and domestic animal health. newly moulted ticks actively avoid direct light but become indifferent as they age; this may be directly linked to the Acknowledgements increased pigment deposition in the cuticle. Further studies on influence of light are needed, testing under field I would like to thank my supervisor Professor Tariq Butt conditions. (Swansea University) for his ongoing support and encourage- There was no significant difference in the occurrence of ment. I also offer my very sincere thanks to Jolyon Medlock ticks in sites with and without animal tracks. (Health Protection Agency) for the valuable help and Limitations of this study included observer bias and the support he has provided me with throughout the entirety influence of the surveyor present on the presence of ticks; it of this project; I would also like to extend my sincere is likely that ticks are responding to CO cues produced, as thanks to Dr Dan Forman (Swansea University) for his humans are also potential hosts. In order to maintain the encouragement and enthusiasm. Thanks to Nigel Reeve condition of the flag, and thus standardize the study, no (Richmond Park) for granting me permission to conduct surveys were conducted in heavy rain; as ticks remain this study. Thanks to Alex Vaux for his help in the field active in rain, it may be interesting to further investigate (Health Protection Agency) and thanks to Dr Andrew the effects of rain on the presence of ticks, increased humid- Dobson (Oxford University) for his advice. ity linked to rainfall may be beneficial for the tick. Further limitations included higher frequencies of larvae in compari- son with nymphs and adults. Larvae tend to show aggregated Author biography distribution with large populations usually arising from one B.P.J.G. graduated from Swansea University with an upper egg batch; therefore, it is necessary to use the presence and second class BSc (Hons) in Zoology. Her interests include absence data from each location opposed to abundance entomology—in particular arthropod vectors of disease, pri- data, which would provide a false representation of marily ticks, their ecology and impact on humans. She has I. ricinus distribution along the Tamsin trail. The data worked with the Health Protection Agency (HPA) on logger was placed in one location to determine a representa- several projects, including a collaborative field study with tive humidity throughout the duration of the study. Swansea University. B.P.J.G. has started a PhD in Individual humidity was not recorded at each location. It is Biological Sciences in 2010, furthering research into moni- therefore suggested that one would record the mat and sur- toring and control of arthropod vectors of disease, in part- rounding areas humidity to obtain better understanding of nership with the HPA and Forestry Commission. Future the influence of humidity, increasing accuracy. It is reason- aspirations include working for the HPA, with the ambition able to assume that the humidity differs with mats of differ- of lecturing later. ent vegetation compositions. It would also be beneficial to combine this data with GIS to obtain further variables for analysis such as aspect, slope and geology. References There are also seasonal restrictions when conducting tick studies, with peak activity occurring over summer. During 1. Macleod J (1936) Ixodes ricinus in relation to its physical environment: an analysis of the ecological complexes controlling distribution and activities. this season, bracken is maturing resulting in reduced sensi- Parasitology 28: 295–319. tivity of drags. With increasing winter temperatures, there 2. Anderson JF, Magnarelli LA (1993) Epizootiology of Lyme disease-causing is now scope to see how this affects ticks in the UK by Borrelia. Clin Dermatol 12: 339–351. extending the sampling period into the autumn and winter 3. Davies R (2005) Predation and the profitability of grouse moors. British seasons. Wildlife 16: 339–347. In conclusion, this study demonstrates that the presence 4. Balashov YS (2007) Harmfulness of parasitic insects and acarines to and the absence of I. ricinus is not static, but dependent on mammals and birds. Entomol Obozr 86: 918–938. a number of environmental factors. It is, however, possible 5. Hillyard PD (1996) Ticks of North-west Europe. Synopses of the British Fauna, to crudely predict areas of ‘hotspot’ activity of I. ricinus No 52. Field Studies Council, Shrewsbury. ......................................................................................................................................................................................................................................... 147 Research article Bioscience Horizons † Volume 4 † Number 2 † June 2011 ......................................................................................................................................................................................................................................... 6. Jongejan F, Uilenberg G (2004) The global importance of ticks. Parasitology 26. Medlock JM, Pietzsch ME, Rice NVP et al. (2008) Investigation of ecological 129: S3–S14. and environmental determinants for the presence of questing Ixodes ricinus (Acari: Ixodidae) on Gower, South Wales. J Med Entomol 45: 314–325. 7. Bennett CE (1995) Ticks and Lyme disease. Adv Parasit 36: 343–405. 27. Scharlemann JPW, Johnson PJ, Smith AA, Macdonald DW, Randolph SE 8. Pietzsch ME, Medlock JM, Jones L et al. (2005) Distribution of Ixodes ricinus (2008) Trends in ixodid tick abundance and distribution in Great Britain. in the British Isles: investigation of historical records. Med Vet Entomol 19: Med Vet Entomol 22: 238–247. 306–314. 28. HPA (Health Protection Agency) (2011) Lyme disease (Lyme 9. Charrel RN, Attoui H, Butenko AM et al. (2004) Tick-borne virus diseases of borreliosis). http://www.hpa.org.uk/web/HPAweb&HPAwebStandard/ human interest in Europe. Clin Microbiol Infect 10: 1040–1055. HPAweb_C/1195733837876. (April 2011, date last accessed) 14:57. 10. Parola P, Didier R (2001) Ticks and tick-borne bacterial diseases in humans: 29. Shaw P, Reeve N (2008) Influence of a parking area on soils and vegetation an emerging infectious threat. Clin Infect Dis 32: 897–928. in an urban nature reserve. Urban Ecosyst 11: 107–120. 11. Randolph SE (2001) The shifting landscape of tick-borne zoonoses: tick- 30. http://www.english-nature.org.uk/citation/citation_photo/1002388.pdf borne encephalitis and Lyme borreliosis in Europe. Philos Trans R Soc Lon (January 2010, date last accessed). B 356: 1045–1056. 31. Reeve NJ, Jones KE (1996) A trapping survey of small mammals in Richmond 12. Chomel BB (1998) New emerging zoonoses: a challenge and an opportunity Park, Surrey, and some implications for future conservation management. for the veterinary profession. Comp Immunol Microb 21: 1–14. Lond Nat 75: 81–90. 13. 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Borrelia burgdorferi (maladie de Lyme) et re´partition de son vecteur Ixodes 17. MacLeod J (1935) Ixodes ricinus in relation to its physical environment. ricinus (Acari: Ixodidae) dans le district Mosan de Belgique. Bull Soc Fr Parasitology 27: 489–500. Parasitol 8: 331–338. 18. Milne A (1948b) The ecology of the sheep tick, Ixodes ricinus: microhabitat 36. Milne A (1950) The ecology of the sheep tick, Ixodes ricinus: spatial distri- economy of the adult tick. Parasitology 40: 14–34. bution. Parasitology 40: 35–45. 19. Macleod J (1932) The bionomics of Ixodes ricinus L., the ‘sheep tick’ of 37. Arthur DR (1962) Ticks and disease. In G. Kerkut, ed., International Series Scotland. Parasitology 24: 382–400. of Monographs on Pure and Applied Biology. Oxford: Pergamon Press, 20. Macleod J (1939) The ticks of domestic animals in Britain. Empire J Expt Agric Vol. 9, pp 21–26. 27: 97–110. 38. Lees AD (1946) The water balance in Ixodes ricinus and certain other ticks. 21. 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Environmental parameters affecting tick (Ixodes ricinus) distribution during the summer season in Richmond Park, London

Bioscience Horizons , Volume 4 (2) – Jun 4, 2011

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Volume 4 † Number 2 † June 2011 10.1093/biohorizons/hzr016 Advance Access publication 4 May 2011 ......................................................................................................................................................................................................................................... Research article Environmental parameters affecting tick (Ixodes ricinus) distribution during the summer season in Richmond Park, London B.P.J. Greenfield* Department of Biosciences, College of Science, Swansea University, Singleton Park, Swansea SA2 8PP, UK. * Corresponding author: Email: 485572@swan.ac.uk Supervisor: Prof. Tariq M. Butt, Department of Biosciences, College of Science, Swansea University, Singleton Park, Swansea SA2 8PP, UK. ........................................................................................................................................................................................................................................ Ixodes ricinus, the sheep tick, as a consequence of its habit of taking blood from mammalian hosts, can transmit disease from wild animals to humans. This is likely to be a particular problem in parks shared by humans and deer populations. These ticks were sampled, using cloth drags, from vegetation at 16 sites in Richmond Park, London, between 15 July and 22 August 2009. A total of 2436 ‘host-seeking’ ticks (2281 larvae, 151 nymphs and 4 adults; three males and one female) were collected, and attempts were made to identify the environmental factors affecting the distribution of these ectoparasites. Tick presence was closely related to soil moisture, light levels and humidity through- out the park. It is thought that improving our understanding of how these factors influence the presence of I. ricinus will facilitate methods of tick control and help to educate the public about where ‘hotspots’ for these parasites are likely to be within the park. Key words: sheep tick, Ixodes ricinus, distribution, ecological parameters, questing nymphs. Submitted September 2010; accepted March 2011 ........................................................................................................................................................................................................................................ with the deterioration of host health, including weight loss Introduction and breeding success. Biology of Ixodes ricinus Ticks are closely related to mites, belonging to the sub- class Acari. Characterized by having four pairs of legs, Aristotle described ticks as ‘disgusting parasitic animals’, a they belong within the class of Arachnida. The larvae, view with which many people would not disagree. Ixodes however, only have three pairs of legs. Like other arachnids, ricinus, more commonly known as the sheep tick, is a hae- they possess chelicerae and palps and they lack both wings matophagous ectoparasite, belonging to the Ixodidae and antennae. Ticks have a unique sensory organ, Haller’s family. Ticks are widely distributed in a range of habitat organ, situated on the front tarsi, used in detecting environ- types, including heath, coniferous and deciduous woods, mental stimuli such as changes in temperature, carbon grassland and rough pastures. The presence or absence of dioxide levels and humidity. These can be observed ticks is highly dependent on local microclimate conditions, waving, emulating antennae, in a process called questing. which are largely determined by sward height and humidity. They also possess a hypostome that enables the tick to Ticks have a diverse range of vertebrate hosts from which attach to the hosts skin when the tick feeds; these character- they feed, affecting 240 species of wild and domesticated istics distinguish ticks from mites. Ticks are typically a three mammals, many species of birds and reptiles. host species and their development occurs in four life stages, Their ability to survive in such a diversity of habitat types passing through an egg, larva, nymph and adult stage and parasitize a multitude of hosts makes ticks a vector of (Fig. 1). interest over recent years. They are highly problematic in the Ixodid ticks are often referred to as ‘hard’ ticks due to the sheep-farming and grouse-shooting industries, causing huge presence of a tough outer scutum, a hard sclerotized dorsal economic losses of several billion dollars per year, globally, ......................................................................................................................................................................................................................................... The Author 2011. Published by Oxford University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.5), which permits unrestricted non-commercial use, distri- bution, and reproduction in any medium, provided the original work is properly cited. 140 Bioscience Horizons † Volume 4 † Number 2 † June 2011 Research article ......................................................................................................................................................................................................................................... 10,11 of many tick-borne diseases; as a result, ticks are of paramount importance globally, due to the implications on both human and livestock health. It is important to under- stand how ticks affect both wild and domestic populations of animals to accurately predict the risk of an outbreak of these diseases. Figure 1. Life stages of Ixodes ricinus (larvae, nymph, adult male, adult Microclimate female) 10 magnification. Tick survival and development are dependent on many factors, primarily the humidity and moisture content of a Table 1. Tick-borne diseases present in the UK 13 1 microclimate. Macleod determined that I. ricinus was Disease caused Causative agent Affects References only to be found in hill pastures, as only here would the ................................................................................................................ tick find the ‘definite conditions of soil and vegetation’ to Lyme disease Borrelia burgdorferi Humans 8 ensure its survival throughout the summer season. Milne Babesiosis Babesia divergens, Cattle (red-water 8 ascertained that mat depth was an important factor in B. microti fever), humans maintaining the microclimatic conditions required by the Tick-borne Flavivirus Humans 9 tick, with a thicker mat being able to retain more water encephalitis thus improving the survival of the ticks. A thicker mat also Louping Ill Virus Viral agents Sheep, grouse, 8,9 provides more niches for ticks to occupy. It was later red deer, hares, shown that the removal of this mat layer increased the desic- rabbits, humans cation rate of the tick, reducing tick numbers. Both 18 16,17 Tularemia Francisella tularensis Humans, cats, 8 Milne and Macleod noted that unfed ticks require a sheep, rabbits, relative humidity above 80% to survive, with anything less rodents having a detrimental effect on the ticks survival. It is there- fore believed that humidity is a fundamental factor influen- Bovine and ovine Anaplasma Cattle, sheep, 6,8 cing tick survival. Humidity has a profound effect on tick tick-borne fever phagocytophilum goats, wild activity, primarily controlling the amount of time a tick complex ruminants can spend questing. When a tick ascends from the mat and Crimean-Congo Nairovirus Humans, cattle, 8 up the vegetation to quest, it becomes highly prone to desic- haemorrhagic fever sheep, goats cation, prompting the tick to retreat back into the mat to Human Ehrlichia/Anaplasma Humans 6 restore its water balance before questing again. granulocytic sp. ehrlichiosis Global warming Boutonneuse fever Rickettsia sp. Humans, dogs, 8 Seasonal variations in temperature due to global warming rabbits, rodents can result in a dramatic impact on how often hosts and pathogen-carrying vectors come into contact. Changes in temperature are detected by Haller’s organ; at temperatures plate, this feature provides sexual dimorphism in the tick as ,78C, ticks remain inactive only venturing out of the mat the scutum completely covers the idiosoma of an adult male, and up the vegetation to quest for a host when temperatures 19,20 whereas the female is partially covered, revealing the alloscu- increase. Many vector-borne diseases are highly suscep- 21 22 tum, this feature allows the female tick to engorge during a tible to changes in climate; Danielova ´ et al. found that blood meal. increasing temperatures not only increase the distribution Ticks are the primary vector for a number of transmissible of I. ricinus, but also linked the rise in temperatures to the pathogens, transmitting more pathogens than any other encroachment of ticks into higher altitudes that were not pre- arthropod vector group with an estimated 10% of all tick viously colonized by ticks. As a consequence, a correlation is species being a vector. Ticks are second only to mosquitoes formed between increase in temperature and increase in the for vectoring human diseases. Many of the diseases prevalence of tick-borne diseases, such as Borreliosis and transmitted by ticks are of huge medical and veterinary tick-borne encephalitis. 8 23 importance (Table 1). Ixodes ricinus in the UK is also the Gray hypothesized that with increasing summer temp- primary vector for Anaplasma phagocytophilum causing eratures, based on the degree-day model, averaging at 308C equine ehrlichiosis and human granulocytic ehrlichiosis and winters that will be relatively frost-free, there will be a and louping ill virus that causes encephalitis in sheep. shift in nymphal and adult activity, occurring in late Recently, there has been a notable increase in the prevalence autumn to early winter. It is also suggested that I. ricinus ......................................................................................................................................................................................................................................... 141 Research article Bioscience Horizons † Volume 4 † Number 2 † June 2011 ......................................................................................................................................................................................................................................... larvae will not undergo developmental diapause and remain trees (Quercus robur), and acidic grasslands; at the heart of active throughout the summer to early spring. the park, there are two large artificial ponds that make up Pen Ponds, and the vast grasslands of Richmond Park are Aims and justification home to 650 deer, predominantly red deer (Cervus elaphus) and fallow deer (Dama dama). Along with This project aimed to determine the environmental par- acidic grass, there is also a large quantity of Bracken ameters that affect the distribution of ticks along the (Pteridium aquilinum). Tamsin trail, a major walking path in Richmond Park. It Richmond Park is also an SSSI (Site of Special Scientific was anticipated that this investigation would identify areas Interest) due to its population of deadwood beetle fauna, of ‘hotspot’ activity and consequently indicate the risk of many of which are Red Data Book Species; there are exposure to ticks and their transmitted diseases. approximately 135 beetle species recorded in the park, 75 Sorouri-Zanjani ascertained 13% of the tick population, of which are dung species including Aphodius zenkeri,a within Richmond Park, carry Borrelia burgdorferi. nationally restricted species. Richmond Park is popular with tourists, attracting hun- A total of 16 sites were located along the Tamsin Trail in dreds of people a month. The park is also home to a large Richmond Park, London. Surveys were conducted on a total number of deer, which act as a primary host for I. ricinus. of 23 days between 15 July and 22 August, as this is the time It was important to conduct this study over the summer as of peak activity of humans within the park (Fig. 2). There this is the peak time of human activity within the park, with were no surveys undertaken during this period if there was the assumption that weather is nicer and therefore more heavy rainfall. The Tamsin Trail was chosen as it is a people will visit the park. This also coincides with the life popular trail for both dog walkers and hikers within the cycle of the tick resulting in peak larval activity during the park; it is therefore one of the main interfaces between summer season. humans, their pets and ticks. A survey by Reeve and A study by Medlock et al. on the ecological and environ- Jones ascertained that Richmond Park is home to five mental determinants for the presence of I. ricinus on the main species of small mammal that are important hosts for Gower, South Wales, concluded that there are numerous I. ricinus and reservoirs for B. burgdorferi: bank vole biotic factors influencing the presence of I. ricinus.Itis (Myodes glareolus), field vole (Microtus agrestis), wood suggested from these factors that one can predict areas mouse (Apodemus sylvaticus), common shrew (Sorex likely to be tick ‘hotspots’; in order to do this effectively, araneus) and pygmy shrew (S. minutus). there is a need for more studies investigating the presence and the absence of ticks. In understanding how environ- Sampling design mental factors influence the presence or the absence of quest- A1 m piece of polycotton cloth was fastened, at the leading ing I. ricinus, it is possible to further improve the methods of edge, to a 1.25 m wooden bar, leaving a 25 cm handle. The tick control and also help to educate those that frequent cloth was laid flat, adjacent and parallel to the path, and Richmond Park where I. ricinus prevalent areas lie within dragged along subtransects of 5 m by slow pacing to the park. optimize the collection of ticks; it is assumed that these Although there are essential distribution maps for the UK ticks are questing ticks. This was repeated 20 times within that depict national distribution of I. ricinus, much of the a location with a separation of 10 m between drags giving data contained within these come from historical data and an overall 100 m transect. This complied with a method do not necessarily mean factors that influence the distri- described by Milne. bution of I. ricinus in areas such as Wales will be the same All ticks found attached to the underside of the cloth, i.e. as those influencing the distribution in London or other the area in contact with the vegetation, were collected using a areas of the UK; it is therefore important to determine pair of fine point tweezers, counted and placed in an biotic and abiotic factors influencing the spatial heterogen- Eppendorf tube containing 70% ethanol to fix the ticks. eity within individual areas. Eppendorf tubes were assigned a specific code to identify It is becoming ever more important for such studies with where each drag was conducted. The ticks were later ident- increasing distribution and abundance of I. ricinus result- ified using an identification key found in Hillyard. If, ing in an increase in the prevalence of Lyme borreliosis in however, there was heavy rain, thus soaking the cloth, sur- the UK. veying was postponed until weather was suitable, allowing standardization of flag condition. Materials and methods Variables Study site Several variables were measured at the start of each 5 m drag Richmond Park is a National Nature Reserve situated in along with the time, date and section code. All variables were London containing 955 ha of woodland, primarily oak recorded on the survey sheet. ......................................................................................................................................................................................................................................... 142 Bioscience Horizons † Volume 4 † Number 2 † June 2011 Research article ......................................................................................................................................................................................................................................... TM Figure 2. Map of Richmond Park (Google earth map) depicting the Tamsin trail (yellow) and the 16 survey sites (red). Ground-derived variables Statistical analysis TM A TinyTag Data Logger, placed in one location for the All these data were analysed using the G-test goodness of fit, 2 33 entirety of the project, was used to obtain the overall a more robust alternative to the traditional x test, to test if humidity, measured as a per cent of relative humidity there is any significant difference in frequency of questing (%RH) and temperature (8C). At the start of each fresh ticks in relation to the variables measured. The association transect, three soil moisture readings were recorded at 0, between ordinal data and the presence was analysed using 1.5 and 5 m along the transect using a theta soil moisture R  C contingency tables. Logistic regression was performed probe and an HH2 soil moisture meter (Delta-T Devices on all the variables using SPSS version 16.0 (Chicago, IL, Ltd, Cambridge, UK). Ambient temperature (8C) was USA). measured with a bulb thermometer. Light levels rep- resented by exposure values (EVs) were recorded using a Polaris Light Meter, and they were taken three times to Results obtain an average. Cloud coverage was measured on an A total of 2436 I. ricinus were collected during 320 transect ordinal scale of 0 – 8 oktas, rainfall was taken samples (2281 larvae, 151 nymphs and 4 adults; three males categorically by observation (no rain, 0; drizzling, 1; and one female) (Table 2), 67.5% were positive drags and heavy rain, 2). 32.5% were negative, 8 of the 16 variables measured had a significant effect on the frequency of ticks. Vegetation The 16 surveyed sites were separated into eight categories Sward height (mm) and mat depth (mm) were measured with depending on their compass orientation. a clear plastic 30 cm ruler and tape measure if the sward Ticks were present in fewer numbers at higher sward height exceeded 30 cm. The mat depth was measured by heights, with ticks being more abundant between 151 and pushing the ruler into the ground until met by resistance 300 mm. There was a very strong significant difference in then recording the depth. The vegetation type on both the the proportion of frequency of ticks in different sward survey side and opposite side was recorded, by observation, heights (G ¼ 1965.93, P  0.001, df ¼ 9). noting down the dominate vegetation types. Path width (m) Soil moisture was closely associated with the presence of and substrate and the ride width (m) measured by placing a ticks. With a modal class of 5.1 – 10% (mode ¼ 8.6%), tape measure across the path. Penetrability of the ride was ticks were more frequent in lower soil moistures, and there recorded on a categorical scale: walk, run and fight. is a strong significant difference in the proportion of ticks ......................................................................................................................................................................................................................................... 143 Research article Bioscience Horizons † Volume 4 † Number 2 † June 2011 ......................................................................................................................................................................................................................................... present at differing soil moistures (G ¼ 19.34, P  0.01, significant relationship between humidity and the presence df ¼ 7). of ticks (G ¼ 137.652, P  0.001, df ¼ 4), with ticks occur- There was a bimodal peak of tick abundance over the ring more frequently in lower humidities (Modal class ¼ temperatures sampled one at 21.0 – 25.98C and the other at 0.0 – 20.0%RH, mode ¼ 0.0%). 16.0 – 20.98C. Note that no temperatures were recorded Light levels appear to have an influence on the presence of ,16.08C. There was a significant difference between temp- ticks; indeed, a G-test confirmed there is a significant differ- erature and the presence of ticks (G ¼ 323.494, P  ence between differing light levels and the presence of ticks adj 0.001, df ¼ 3; modal class ¼ 21.0 – 25.98C, mode ¼ 23.08C). (G ¼ 274.592, P  0.001, df ¼ 13). Table 3 highlights adj Quantitatively there was a relationship between humidity the number of ticks found at each sample site in correlation and the presence and absence of ticks (Fig. 3). There is a with environmental parameters measured. Table 2. Number of ticks found at each location Logistic regression Location Larvae Nymph Adult male Adult female Total ................................................................................................................ Logistic regression analysis was used to predict variables that A14 1 0 0 15 influence the presence and the absence of I. ricinus.It appears that soil moisture, light levels and humidity are all B 585 65 0 0 650 significant predictors for the presence of I. ricinus, whereas C41 2 0 0 43 the other variables sward height, mat depth and ambient D45 4 0 0 49 temperature were not considered to significantly influence E58 10 0 0 68 the presence of I. ricinus in the model produced. ‘Step 1’ in F21 0 0 0 21 the classification table (Table 4) represents the overall per G91 0 1 0 92 cent of presence and absences that are correctly predicted H 193 1 0 0 194 by the model using soil moisture as the only variable. With I64 0 0 0 64 subsequent steps, the percentage increases from 67.8% for J 198 19 0 0 217 the null model to 70.6% in ‘step 2’ where soil moisture is K 333 8 1 1 343 combined with light levels, and again to 71.9% for the full L 181 23 0 0 204 model, ‘step 3’. ‘Step 3’ is therefore a more accurate model, M 149 9 1 0 159 successfully predicting the presence and the absence of ticks based on soil moisture, light levels and humidity N 116 7 0 0 123 which all exert a significant effect in their own right reinfor- O 108 0 0 0 108 cing the significance of the overall model (‘step 3’ P ¼ 0.001; P84 2 0 0 86 Table 5). Figure 3. Number of ticks at each relative humidity recorded. ......................................................................................................................................................................................................................................... 144 Bioscience Horizons † Volume 4 † Number 2 † June 2011 Research article ......................................................................................................................................................................................................................................... Table 3. Number of ticks present at each sample site in relation to environmental parameters Location Average ambient Average cloud Average sward Average mat Average soil Average light Total Total Total temperature (8C) coverage (oktas) height (mm) depth (mm) moisture (%) levels (Ev) larvae nymphs adults ........................................................................................................................................................................................................................................ A 23.98 5.95 307.65 4.50 7.78 11.60 14 1 0 B 20.80 5.25 217.50 8.75 13.44 9.80 585 65 0 C 23.65 7.75 189.50 4.10 5.51 10.65 41 2 0 D 22.65 6.85 188.00 3.85 8.21 10.60 45 4 0 E 21.03 4.90 283.20 5.30 20.67 9.83 58 10 0 F 20.95 6.85 458.50 2.95 19.74 10.65 21 0 0 G 25.20 5.70 712.75 4.55 13.28 12.20 91 0 1 H 25.60 4.90 281.00 6.20 7.99 10.70 193 1 0 I 26.43 5.00 279.50 4.90 19.31 11.55 64 0 0 J 24.18 6.30 236.50 5.38 12.49 10.33 198 19 0 K 23.00 6.55 304.00 9.30 14.30 11.10 333 8 2 L 21.55 6.10 216.50 3.88 18.45 10.65 181 23 0 M 29.60 0.95 239.00 6.90 8.00 10.55 149 9 1 N 21.40 6.20 412.50 4.65 11.98 10.05 116 7 0 O 25.60 6.75 309.50 3.60 9.75 11.05 108 0 0 P 22.10 7.65 273.00 6.40 13.47 10.30 84 2 0 Grand 23.61 5.85 306.79 5.33 12.77 10.73 2281 151 4 total Table 4. Output of logistic regression Table 5. Variables in the Equation Observed Predicted B SE Wald df Sig. ................................................................................................................ Binary Percentage correct Step 1(a) Soil moisture 0.066 0.020 11.195 1 0.001 0.00 1.00 ................................................................................................................ Constant 20.072 0.259 0.077 1 0.782 Step 1 Step 2(b) Binary Soil moisture 0.072 0.020 12.569 1 0.000 0.00 1 103 1.0 Light levels 20.274 0.082 11.110 1 0.001 1.00 0 216 100.0 Constant 2.819 0.906 9.671 1 0.002 Overall percentage 67.8 Step 3(c) Step 2 Soil moisture 0.065 0.021 9.770 1 0.002 Binary Light 20.260 0.083 9.827 1 0.002 0.00 19 85 18.3 Humidity 20.006 0.003 5.103 1 0.024 1.00 9 207 95.8 Constant 3.076 0.926 11.043 1 0.001 Overall percentage 70.6 Step 3 Binary ticks, elucidating which factors are essential for predicting 0.00 27 77 26.0 ‘hotspot’ areas. Tick activity has been associated with water balance regulation, namely ambient temperature and 1.00 13 203 94.0 relative humidity. It has been demonstrated that Overall percentage 71.9 I. ricinus, typically begin to quest at 45%RH and an ambient temperature of 2.58C. This study revealed that there was a higher abundance of I. ricinus between 21.0 and 25.98C, temperatures exceeding this (26.0 – 40.08C) Discussion were associated with less numbers of I. ricinus. This is not The study aimed to define which of the environmental surprising as ticks are more likely to be found in the mat parameters were influential on the presence and absence of in extreme temperatures to prevent desiccation. Lower ......................................................................................................................................................................................................................................... 145 Research article Bioscience Horizons † Volume 4 † Number 2 † June 2011 ......................................................................................................................................................................................................................................... temperatures (16.0 – 20.98C) significantly reduced the taller sward heights, due to an increase in the variation of numbers of ticks recovered during dragging. It is important vegetation heights. Ticks will quest at the tips of each plant to note that no temperatures ,168C were recorded, during thus dispersing the ticks at uneven heights throughout the the day, throughout this project. Further work is needed to entire plant resulting in a larger proportion of ticks being assess the occurrence of ticks at a broad range of tempera- missed during the drag. Low sward heights (0 – 45 mm) tures typical of a temperate climate. were shown to be less suitable for ticks with drags containing Previous studies, notably those by Milne and Medlock sward heights within this range only producing negative et al., ascertained temperatures during the day, soil moist- drags. ure and high cloud coverage had a large influence on the This project was less concerned with the underlying topo- presence of questing ticks. Here, it was found that the pres- graphy of the land to determine aspect, and the presence ence of ticks was closely associated with low soil moisture. and the absence were, however, analysed based on the This is in contrast to previous studies and suggests that tick locations orientation on the O.S. map. It was found that ecology may be more complex than previously thought. there was a significant difference in the presence of ticks in Another variable appearing contradictory to previous the south of the park, i.e. along transects between Robin studies is relative humidity, with a larger number of ticks Hood gate and Isabella Plantation, compared with the rest associated within the modal class of 0.0 – 20.0%RH, a of the park. In addition, sites located in the east (Sheen value comparatively lower than the 80%RH required for gate – Roehampton gate and Roehampton gate – Robin Hood 13 36 survival stated by Macleod. Arthur has suggested that gate) and northwest (Pembroke lodge – Kingston gate and between 86 and 96%RH, the ticks water balance is in equi- Ham gate – Richmond gate) of the park, presented no signifi- librium with the atmosphere, allowing the tick to gain moist- cant differences between the presence and the absence of ticks. ure from the air at a higher humidity and, conversely, loose Vegetation structure plays a large role in the presence and water when humidity is low. At this point, it is not clear the absence of ticks. Ticks are often recorded in woodland why this trend has occurred and it is subject to follow-up habitats, as this habitat provides a dense shrub layer; habitats work. with bracken, however, will also provide a suitable habitat. Studies have shown that it is not favourable for the ticks to This is reflected in this study as sites with high bracken 18,37 be present in higher humidities, as they become prone to content, such as areas in the south, north, northeast and over saturation thus limiting their activities. southwest orientations, had larger numbers of ticks present Although tick presence increased with increasing cloud in comparison with sites with little or no bracken. coverage, there was no significance between the varying Similarly, a large number of sites with conditions highly levels of cloud coverage and the presence of ticks. suitable for ticks were in fact associated with very low 1,16 Mat depth has been considered one factor influencing the numbers of ticks. Conversely, areas that did not appear presence of ticks and indeed; this survey showed that mat to be particularly favourable, e.g. transects between depth does have a significant effect on the presence of Richmond gate and Sheen gate which had very little veg- ticks. Logistic regression analysis, however, does not con- etation cover and variation in vegetation, comparatively sider mat depth to be fundamental in predicting the presence low sward heights and relatively low soil moistures, pro- of ticks. Locations with mat depths exceeding 10 mm are not duced over a quarter (26.68%) of the total ticks collected. associated with large numbers of ticks. This is counter- These locations did, however, have a large amount of leaf intuitive as one would suppose ticks would prefer a much litter, thus providing abundant mat, suggesting that grass is thicker mat as there would be less chance of desiccation not key to tick presence and it could be ground coverage once the tick has retreated down the sward into the mat. per section. The mat level is required for the ticks to restore their water Grassland is often considered to be relatively unsuitable balance as humidity is generally higher in the mat. This for ticks; nonetheless, I. ricinus is often found in grazed is important as ticks alternate frequently between questing pastures and this was also found in this study with a on vegetation, where they rapidly loose water through the total of 386 (15.85%) ticks collected on open grassland cuticle via evaporation, and quiescence, a process through (area between Roehampton gate and Robin Hood gate). which they actively reabsorb water from the atmosphere, in With respect to the vegetation type and ride penetrability, the mat level. Also with a thicker mat, there would be a their effect on the presence and the absence of ticks is mostly much higher probability of ticks coming into contact with likely due to their influence on host presence. There are small mammals, as small mammals are more likely to fre- numerous organisms acting as hosts for I. ricinus. Larvae quent areas with a more dense vegetation and mat depth. feed upon small mammals and birds, whereas deer tend to The presence of ticks was greatest at medium sward support ticks at each stage, deer are an extremely important heights (151 – 300 mm); there was a significant decrease in host for adult I. ricinus. As a result, areas that are densely the occurrence of ticks at higher sward heights. This is not vegetated will provide a more suitable habitat for these surprising as sampling accuracy is largely decreased at hosts, thus directly increasing the abundance of ticks. ......................................................................................................................................................................................................................................... 146 Bioscience Horizons † Volume 4 † Number 2 † June 2011 Research article ......................................................................................................................................................................................................................................... Interestingly, it was found that light levels significantly throughout the entire park based on the soil moisture, influenced the presence of ticks; indeed, logistic regression humidity and light levels. Repeats of this study would help considered light levels to be a fundamental variable for pre- to further enhance the effects of environmental parameters dicting abundance. With a modal class of 10 EVs, it is effecting the distribution. The data that were obtained can suggested that this is the optimum light intensity for questing be used to inform those that frequent Richmond Park ticks, with intensities above this level significantly reducing where I. ricinus ‘hotspots’ are and act as a warning to the number of ticks captured. Lees has shown that under reduce the risk of exposure to ticks. It would be beneficial continual exposure to high intensities of light, I. ricinus to assess the levels of transmissible pathogens present remains at rest and only begins questing in response to a within Richmond Park, relating not only to public health fall in light intensity. It has also be hypothesized that but also to wild and domestic animal health. newly moulted ticks actively avoid direct light but become indifferent as they age; this may be directly linked to the Acknowledgements increased pigment deposition in the cuticle. Further studies on influence of light are needed, testing under field I would like to thank my supervisor Professor Tariq Butt conditions. (Swansea University) for his ongoing support and encourage- There was no significant difference in the occurrence of ment. I also offer my very sincere thanks to Jolyon Medlock ticks in sites with and without animal tracks. (Health Protection Agency) for the valuable help and Limitations of this study included observer bias and the support he has provided me with throughout the entirety influence of the surveyor present on the presence of ticks; it of this project; I would also like to extend my sincere is likely that ticks are responding to CO cues produced, as thanks to Dr Dan Forman (Swansea University) for his humans are also potential hosts. In order to maintain the encouragement and enthusiasm. Thanks to Nigel Reeve condition of the flag, and thus standardize the study, no (Richmond Park) for granting me permission to conduct surveys were conducted in heavy rain; as ticks remain this study. Thanks to Alex Vaux for his help in the field active in rain, it may be interesting to further investigate (Health Protection Agency) and thanks to Dr Andrew the effects of rain on the presence of ticks, increased humid- Dobson (Oxford University) for his advice. ity linked to rainfall may be beneficial for the tick. Further limitations included higher frequencies of larvae in compari- son with nymphs and adults. Larvae tend to show aggregated Author biography distribution with large populations usually arising from one B.P.J.G. graduated from Swansea University with an upper egg batch; therefore, it is necessary to use the presence and second class BSc (Hons) in Zoology. Her interests include absence data from each location opposed to abundance entomology—in particular arthropod vectors of disease, pri- data, which would provide a false representation of marily ticks, their ecology and impact on humans. She has I. ricinus distribution along the Tamsin trail. The data worked with the Health Protection Agency (HPA) on logger was placed in one location to determine a representa- several projects, including a collaborative field study with tive humidity throughout the duration of the study. Swansea University. B.P.J.G. has started a PhD in Individual humidity was not recorded at each location. It is Biological Sciences in 2010, furthering research into moni- therefore suggested that one would record the mat and sur- toring and control of arthropod vectors of disease, in part- rounding areas humidity to obtain better understanding of nership with the HPA and Forestry Commission. Future the influence of humidity, increasing accuracy. It is reason- aspirations include working for the HPA, with the ambition able to assume that the humidity differs with mats of differ- of lecturing later. ent vegetation compositions. It would also be beneficial to combine this data with GIS to obtain further variables for analysis such as aspect, slope and geology. References There are also seasonal restrictions when conducting tick studies, with peak activity occurring over summer. During 1. Macleod J (1936) Ixodes ricinus in relation to its physical environment: an analysis of the ecological complexes controlling distribution and activities. this season, bracken is maturing resulting in reduced sensi- Parasitology 28: 295–319. tivity of drags. With increasing winter temperatures, there 2. Anderson JF, Magnarelli LA (1993) Epizootiology of Lyme disease-causing is now scope to see how this affects ticks in the UK by Borrelia. Clin Dermatol 12: 339–351. extending the sampling period into the autumn and winter 3. Davies R (2005) Predation and the profitability of grouse moors. British seasons. Wildlife 16: 339–347. In conclusion, this study demonstrates that the presence 4. 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Journal

Bioscience HorizonsOxford University Press

Published: Jun 4, 2011

Keywords: sheep tick Ixodes ricinus distribution ecological parameters questing nymphs

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