Effects of Large-Scale Heathland Management on Thermal Regimes and Predation on Adders Vipera Berus

Effects of large-scale heathland management on thermal regimes and predation on adders Vipera berus

Animal Conservation

John Worthinghton-Hill Jennifer Gill

School of Biological Science UEA

56 57 58 59 60 1 2 3 4 1 Figures & tables 5 6 7 8 2 9 10 3 11 12 4 13 5 14 15 6 16 17 7 18 19 8 Figure 1 Example female (brown) and male (grey) Plasticine model adders used in this study. 20 21 9 22 23 10 24 25 11 26 27 12 28 13 29 30 14 31 32 15 33 34 16 35 36 17 37 38 18 39 40 19 41 42 20 43 21 44 45 22

46 47 23 48

49 24 50 51 25 Figure 2 Locations of study heathlands in (a) Norfolk: 1 = Salthouse Heath, 2 = Kelling Heath 1, 3 = Kelling 52 26 Heath 2, 4 = Holt Lowes, 5 = Buxton Heath, 6 = Horsford Woods and (b) Surrey: 7 = Headley Heath, 8 = 53 27 Blackheath Common, 9 = Thursley Common, 10 = Marley Common. Inset shows study region locations 54 55 28 within the UK.

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1 2 3 29 4 5 30 Table 1 Attributes of the 10 lowland heathland sites included in this study 6 7 31 Grazing intensity Number 8 Site Area (ha) -1 9 32 (livestock ha ) of models 10 Horsford Woods 124 n/a 80 33 11 Buxton Heath 67 0.15 60 12 13 34 Holt Lowes 50 0.14 70 14 Salthouse Heath 95 n/a 90 15 35 Kelling Heath 1 89 n/a 90 16 36 Kelling Heath 2 89 n/a 70 17 Marley Common 21 0.14 70 18 37 Thursley Common 325 n/a 60 19 Blackheath Common 101 n/a 60 20 38 21 Headley Heath 204 n/a 120 22 39 23 24 40 25 26 41 27 (a) (c) 28 42 29 30 43 31 44 32 33 opy 45 34 35 46 36 37 47 38 39 48 40 (b)(b) 41 49 42 50 43 44 51 45 46 52 47 48 53 49 50 54 51 55 52 53 56 Figure 3 Examples of areas of (a) cleared (a large recently mown area alongside a busy footpath at 54 57 Blackheath Common) and (b) structurally complex heathland vegetation (Kelling Heath), and (c) a male 55 58 adder crossing a large mown area (Kelling Heath, April 2015). 56 57 58 59 60

1 SPRING SUMMER 2 3 60 60 60 (a) (b) 4 Cleared 5 61 50 Complex 50

6 ( Shelter 7 62 40 40 8 9 63 30 30 10 64 11 20 20 12

13 65 Mean temperature 10 10 14 66 15 0 0 16 67 00:00 02:30 05:00 07:30 10:00 12:30 15:00 17:30 20:00 22:30 00:00 02:30 05:00 07:30 10:00 12:30 15:00 17:30 20:00 22:30 17 Time of day (h) Time of day (h) 20 0.8 20 0.8 18 68 19 (c) (d)

Deviation from Tset range of

SE) 20

69 ± Time exceding CTmax w

21 C 15 0.6 15 0.6

( 22 70 23

proportion 24 71 10 0.4 10 Copy 0.4 25

SE)

’ activity period activity ’ 72 26 (±

temperature 27 5 0.2 5 0.2 73

28 adders

Mean 29 Mean 74 30 0 0 0 0 31 75 Cleared Complex Shelter Cleared Complex Shelter 32 Treatment Treatment 33 76 34 35 77 Figure 4 Daily cycle of operative temperatures (Te: means per 30 minute interval) on cleared, complex and sheltered microhabitats on heathlands in (a) spring 36 78 and (b) summer (black horizontal lines indicate adders’ preferred temperature range (Tset) measured in a laboratory thermal gradient by Herczeg et al. (2007) 37 79 and Lourdais et al. (2013), and red horizontal lines indicate the estimated critical thermal maximum temperature (CTmax) for adders (Brattstrom, 1965; 38 80 Spellerberg, 1972)), and mean deviations of Te from Tset during the diurnal activity period (08:00-20:00) and the proportion of the activity period in which Te 39 81 exceeds CTmax in (c) spring and (d) summer. Operative temperature in sheltered areas was significantly lower than in cleared (GLMM post-hoc test, z = - 40 82 8.259, p < 0.001) and complex areas (z = 9.104, p < 0.001), which were not significantly different from one another (z = 0.788, p = 0.711). 41 42 43 44 45

1 2 3 83 Table 2 Model structures used in the analyses of variation in operative temperatures, the risk of attack 4 84 on adders and the number of recreational visitors to heaths. 5 6 7 Model response Distribution Model structure 8 Operative temperature (Te) Normal Time of day + Treatment * Season + (1 | Day) + (1 9 | Logger ID) + (1 | Site) 10 11 Attack rate Binomial (logit) Region + Site + Sex + Distance to path * Treatment 12 Number of people Poisson (log) Day + Site + Activity 13 85 14 15 86 Table 3 Results of a generalised linear mixed model of variation in operative temperatures (Te) of 16 87 biophysical models on lowland heaths in different management treatments (cleared, complex, shelter) 17 88 throughout the day (30 min periods between 08:00 and 20:00) in spring (April) and summer (July). 18 19 89 Significant variables are highlighted in bold. 20 21 Variable Estimate SE DF T P 22 (Intercept) 7.63 1.07 18 7.148 <0.001 23 Treatment 0.54 0.08 2322 6.966 <0.001 24 25 Time of day -0.42 0.008 2322 -49.537 <0.001 26 Season 17.11 0.19 2206 89.607 <0.001 27 Treatment * Season 0.16 0.19 2322 0.805 0.421 28 90 29

30 91 L L L 31 1 Copy Dog 32 92 33 Livestock 34 93 Bird

35 attacked Undamaged

36 94 37 95

models

38 0.5

of 39 96 40 41 97 42

43 98 Proportion 44 45 99 46 0 47 100 48 49 101 50 102 51 Site 52 103 Figure 5 The proportion of adder models attacked on each of the ten heathland sites and the relative 53 54 104 proportion attacked by dogs and birds and trampled by livestock (L = sites with grazing livestock) . The 55 105 dotted line divides the six Norfolk sites and four Surrey sites. 56

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1 2 3 106 Table 4 Results of generalised linear mixed models of the risk of attack of adder models by all predators 4 107 combined, and attacks by dogs and livestock trampling separately, in different management treatments 5 6 108 (cleared and complex) and at different distances from footpaths on lowland heaths. Significant variables 7 109 are highlighted in bold. 8 9 110 10 11 Predator Variable Estimate SE Z P 12 13 All attacks 14 (Intercept) 1.6 0.48 3.36 <0.001 15 16 Treatment -2.01 0.42 -4.75 <0.001 17 Dist. to path -0.09 0.01 -7.57 <0.001 18 Sex 0.4 0.21 1.89 0.06 19 Treatment * Dist. to path 0.02 0.02 0.96 0.33 20 Dogs 21 (Intercept) 1.71 0.49 3.5 <0.001 22 23 Treatment -0.83 0.56 -1.49 0.14 24 Dist. to path -0.1 0.01 -7.61 <0.001 25 Sex 0.4 0.24 1.64 0.1 26 Treatment * Dist. to path -0.08 0.04 -2.3 0.02 27 Livestock 28 (Intercept) -0.61 1.26 -0.49 0.63 29 30 Treatment -0.49 1.05 -0.47 0.64 31 Dist. to path -0.03 0.02 -1.59 0.11 32 Sex -0.78 0.48 -1.62 0.11 33 Treatment * Dist. to path 0.02 0.03 0.55 0.58 34 35 111 36 37 112 38 113 39 40 114 41 42 115 43 44 116 45 46 47 48 49 50 51 52 53 54 55 56

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1 2 3 117 4 0.5 5 (a) 0.5 (b) 6 7

attacked 8 9 10 11 0.25 0.25

proportion 12 13

14 (±SE)

15 16 17 Mean 0 0 18 Cleared Complex Dog Livestock Bird Dog Livestock Bird 19 Treatment Cleared Complex 20 21 Treatment 22 118 23 24 119 Figure 6 The mean (±SE) proportion of adder models (a) attacked, and (b) attacked by dogs, birds and 25 120 livestock, in cleared and complex areas across 10 heathland sites. 26 27 121 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 122 47 48 123 Figure 7 Variation in the risk of attack of model adders by dogs in relation to distance to the nearest 49 124 footpath, on cleared and complex areas of heathland. Dotted lines indicate 95% confidence intervals. 50 51 125 52 53 126 54

55 127 56 57 58 59 60

1 2 3 128 4 5 129 6 7 130 Walking with dogs Walking without dogs 8 Running Cycling 9 131 Horse riding 10 1 20 100 11 132

activity 12 93

activity 13 133 100 14 15 134 100 15 94 16

135 recreational

recreational

17 of 100 0.5 10 18 of 136 19 100

index 20 137 index

1 00 21 Revie83 5 22 138

(±SE) 23 24 139

Proportion 25 w Mean 0 0 26 140 27 28 141 29 30 142 31 143 Sites 32 33 144 Figure 8 The mean index of recreational activity at each of the ten heathland sites studied in May 2015 34 145 and the relative contribution of each of the five constituent components of the index, on each of the 35 36 146 sites. The percentage of dogs off-lead is also given for each of the sites where walking with dogs 37 147 occurred. 38 39 148 40 41 149 Table 5 Results of a general linear model of the number of human visitors undertaking different 42 150 activities (see Fig 8) recorded during surveys of recreational activity on 10 lowland heathland sites. 43 151 Significant variables are highlighted in bold. 44 45 Residual Residual Variable DF Deviance P 46 DF deviance 47 48 Day 3 7.211 41 136.896 0.065 49 Site 8 79.307 33 57.589 <0.001 50 Activity 4 30.118 29 27.471 <0.001 51 52 152

53 54 55 56 57 58 59 60

1 2 3 153 4

5 154 0.6 6 7 155 Dog

models Livestock

to Bird 9 156 10 0.4 11 157 12

damage 158

13 14 15 159 0.2 16 160

17 Proportion 18 161 19 0 20 162 Head Body Tail 21 Body third most heavily damaged 22 163 23 24 164 Figure 9 The proportion of damage to body sections among model snakes attacked by dogs and birds, 25 165 and trampled by livestock. 26 27 166 28 29 30 31 167 Appendices 32

33 34 35 168 36 37 169 38 39 170 40 41 171 42 43 172 44 173 45 46 174 47 48 175 49 50 176 51 52 177 53 54 55 56 57 58 59 60

1 2 3 178 Appendix 1 Imprints left on adder models showing (a & b) tooth marks from dog attack, (c & d) bill 4 179 marks from bird attack, and hoof marks from trampling by grazing (e) cattle and (f) pony. 5 6 180 7 8 181

9 10 182 (a) (b) 11 12 183 13 14 184 15 16 185 17 18 186 19 187 20 21 188 Appendix 2 Dead adders found on heaths by JWH showing injuries apparently consistent with (a) dog 22 23 189 attack and (b) trampling by grazing livestock. 24 190 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

1 2 3 1 4 Effects of large-scale heathland management on thermal regimes and predation on 5 6 2 adders Vipera berus 7 8 9 10 3 John O. Worthington-Hill1* & Jennifer A. Gill1 11 12 13 14 4 1School of Biological Sciences, University of East Anglia, Norwich Research Park, 15 16 17 5 Norwich, NR4 7TJ, UK 18 19 20 6 *Corresponding author: [email protected] 21 22 23 7 24 25 26 8 Short title: Effects of heathland management on the adder 27 28 9 Key words: habitat management, heathland, conservation, thermoregulation, 29 30 31 10 predation, reptile, adder 32 33 34 35 11 36 37 38 39 12 Abstract 40 41 42 43 13 Management prescriptions for species of conservation concern often focus on creating appropriate 44 45 14 habitat conditions, but the spatial scales over which these actions are applied can potentially impact 46 47 15 48 their success. In Northwestern Europe, preventing further loss of lowland heathland through 49 50 16 successional changes often involves the mechanical removal of vegetation, creating large blocks of 51 52 17 open homogenous habitat. We investigate the influence of this broad-scale habitat management on a 53 54 18 heathland specialist, the adder Vipera berus. By deploying temperature loggers and Plasticine adder 55 56

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1 2 3 19 models in heathland areas with and without complex vegetation cover, we show that (1) cleared areas 4 5 6 20 lack both the temperature variation adders need to thermoregulate effectively and suitable refuges 7 8 21 from dangerously high summer temperatures, and (2) attacks by dogs and trampling by grazing 9 10 22 livestock are significantly more frequent in cleared areas and closer to footpaths. Habitat management 11 12 13 23 strategies that retain some structural complexity of vegetation within cleared areas, and diverting 14 15 24 footpaths away from cleared areas and/or strategic placement of barrier hedging around these areas 16 17 25 could potentially reduce the exposure of adders to high predation risk and thermal extremes. 18 19 20 21 26 22 23 24 27 Introduction 25 26 27 28 28 The physical structure of habitats in anthropogenic landscapes is often dependent on human-directed 29 30 29 disturbance regimes (Faegri, 1988; Lawton, 1999). Management that provides structural complexity 31 32 33 30 can be important for wildlife because heterogeneous habitats typically provide more niches and 34 35 31 resources (e.g. Simpson, 1949; Macarthur & Wilson, 1967; Lack, 1969; Bazzaz, 1975), and can 36 37 32 benefit both faunal abundance and community diversity (Davidowitz & Rosenzweig, 1998; Tews et 38 39 40 33 al., 2005). However, the spatial scale at which such management should operate is often unclear. 41 42 34 Coarse-filter approaches to vegetation management are often employed to create appropriate 43 44 35 conditions for a range of species characteristic of an area (Simberloff, 1998; Groves, 2003; Wiens et 45 46 36 47 al., 2008). However, such generic management prescriptions can potentially lead to unintended 48 49 37 consequences for species of conservation concern (Dolman, Panter & Mossman, 2012). 50 51 52 38 Lowland heathland of north-western Europe developed ~4000 years ago as a result of forest 53 54 55 39 clearance, and has been maintained since by disturbance regimes including livestock grazing, burning, 56

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1 2 3 40 turf-cutting and harvesting of heather and bracken (Gimmingham, 1972; Webb, 1998). Over the last 4 5 6 41 century, declines in these traditional land management practices have resulted in successional 7 8 42 vegetation changes (Skogen, 1987; Webb, 1998; Mitchell et al., 2000; Fagúndez, 2013) and 9 10 43 significant loss and fragmentation of heathland (Rose et al., 2000; Alonso, 2004; Newton et al., 2009). 11 12 13 44 The UK has ~20% (58 000 hectares) of the remaining lowland heathland in north-western Europe 14 15 45 (UK Biodiversity Steering Group, 1995), often occurring in relatively small patches covering tens 16 17 46 of hectares. Consequently, it is listed under Annex I of the EU Habitats Directive and a priority habitat 18 19 47 under the UK Biodiversity Action Plan. 20 21 22 23 48 Mimicking traditional land-use, various management practices have been applied to halt the 24 25 49 loss of heathland, including grazing at different stocking rates (Bokdam & Gleichman, 2000; Pakeman 26 27 50 et al., 2003), burning (Hobbs & Gimingham, 1984a, 1984b; Mallik & Gimingham, 1985; Britton et 28 29 30 51 al., 2001), mechanical cutting (Calvo, Tarrega & de Luis, 2002) and turf stripping (Bokdam & 31 32 52 Gleichman, 2000). While these modernised management systems can achieve economies of scale and 33 34 53 efficiency, they are generally less diverse in terms of disturbance regimes and fine-scale temporal and 35 36 37 54 spatial variability (Webb, 1998), and often reduce the complex structure of vegetation or remove it 38 39 55 entirely (Newton et al., 2009; Edgar, Foster & Baker, 2010). However, there has been little 40 41 56 investigation of the impacts of these modern management regimes on heathland wildlife. 42 43 44 45 57 Reptiles can be particularly impacted by changes to habitat structural complexity (Pianka & 46 47 58 Pianka, 1970; Huey & Slatkin, 1976). Reductions in vegetation complexity can reduce the availability 48 49 59 of locations with differing thermal conditions, making effective thermoregulation more difficult 50 51 52 60 (Huey & Slatkin, 1976; Row & Blouin-Demers, 2006; Elzer et al., 2013). Habitat simplification can 53 54 61 also increase predation risk (or perception of predation risk), by reducing refuge opportunities and/or 55

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1 2 3 62 increasing encounter rates between predators and prey (Murdoch & Oa, 1975; Gotceitas & Colgan, 4 5 6 63 1989; Irlandi, 1994). These effects may be especially pronounced for reptiles in temperate climates 7 8 64 because they must balance the risk of predation with the need to thermoregulate (often basking in 9 10 65 exposed areas) in highly variable thermal conditions (Huey, 1974). Basking poses significant risks to 11 12 13 66 survival, but capitalising on favourable thermal conditions is vital for energy assimilation and growth 14 15 67 (Olsson, Madsen & Shine, 1997; Lourdais et al., 2004; Herczeg et al., 2007). 16 17 18 68 Many lowland heaths are also near to centres of human population and are used as recreational 19 20 21 69 amenities (Underhill-Day & Liley, 2007; Cordingley et al., 2015). Consequently, they can support 22 23 70 high numbers of predators of reptiles, including domestic animals (Phelps, 2004; Underhill-Day, 24 25 71 2005; Edgar et al., 2010). 26 27 28 29 72 The loss and degradation of lowland heathland has been implicated in historic population 30 31 73 declines of adders Vipera berus in the UK (Baker, Suckling & Carey, 2004; Edgar et al., 2010; Gleed- 32 33 74 Owens & Langham, 2012). Despite this, the impact of current heathlands management regimes for 34 35 36 75 adders is poorly understood. Through the deployment of temperature loggers and adder models on 37 38 76 heaths across lowland England, we quantify differences in thermal conditions and rates of adder 39 40 77 predation, as well as the identity of predators, in areas with differing vegetation structure: either open, 41 42 78 short swards or structurally complex vegetation. 43 44 45 46 79 47 48 49 50 80 Materials & Methods 51 52 53 81 Measuring the thermal environment 54 55

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1 2 3 82 We quantified the thermal environment on heathlands by measuring operative environmental 4 5 6 83 temperatures (Te) using temperature loggers (Thermochron i-Button, Maxim Integrated) inside 7 8 84 biophysical snake models (Bakken, 1992). The operative temperature is defined as the temperature of 9 10 85 an inanimate object of zero heat capacity with the same shape, size and radiative capacity as the focal 11 12 13 86 animal when exposed to the same microclimate (Bakken & Gates, 1975). Unlike simple measures of 14 15 87 air or ground temperatures, operative temperatures integrate heat exchange across multiple pathways 16 17 88 (radiation, convection and conduction), and thus reflect the thermal environment available to the study 18 19 89 subject more effectively. 20 21 22 23 90 The biophysical models used here were constructed to represent adders, and consisted of 40-cm-long 24 25 91 copper tubes (wall thickness 1.1 mm, diameter 22 mm) with sealed ends (tight-fitting rubber bungs). 26 27 92 Each temperature logger was positioned at the centre of the model and wrapped in packaging foam so 28 29 30 93 that it was not in contact with the walls of the copper tube. Comparison of the thermal behaviour of a 31 32 94 model with that of a fresh snake carcass on a flat exposed concrete surface over a 24 h period revealed 33 34 95 very similar temperature ranges (model = 6–33.5oC, snake = 5.3–34oC), very little thermal 35 36 o 37 96 discrepancy (<0.1 C) and a highly significant correlation between simultaneous readings across this 38 39 97 range (r = 0.98, n = 96, p < 0.001). 40 41 42 98 Estimating rates of snake predation 43 44 45 46 99 We used artificial model replicas of adders to measure predation rates on heaths. Each model was 47 48 100 constructed using ~100 g of non-toxic sculpting clay (Newplast Plasticine; Animation Supplies Ltd, 49 50 51 101 Worthing, UK) and measured ~35 cm in length and 2 cm in diameter. Grey-coloured clay was used 52

53 102 for males and terracotta-coloured for females (Fig. 1). All models had a tapering tail end, a slightly 54 55 103 enlarged head distinct from a thinner neck, with three bends in the body to replicate a typical S-shaped, 56 57 58 59 60

1 2 3 104 resting posture. Using a black non-toxic water-based paint marker (Uni POSCA PC-5M; The SQL 4 5 6 105 Workshop Ltd, Devon, UK), a mid-dorsal zigzag pattern and head markings similar to those of adders 7 8 106 were painted onto all models. To reduce the risk of whole models being displaced or carried away by 9 10 107 predators, each was secured to the ground using a small, black elastic band at the midpoint of the body 11 12 13 108 attached to a concealed peg. Models were inspected for marks left by predators to aid identification 14 15 109 of the animal responsible; (i) dog attack: identified by canine teeth or claw marks, (ii) avian attack: 16 17 110 beak or claw marks of birds, or (iii) livestock trampling: hoof marks of ponies or cattle (Appendix 1). 18 19 111 Predators of snakes often direct attacks towards the head, especially in venomous snakes (Wüster et 20 21 22 112 al., 2004; Niskanen & Mappes, 2005), so the position of damage to models was also recorded. 23 24 25 113 Experimental design 26 27 28 29 114 The study took place on ten heathland sites in lowland England (Fig. 2; Table 1), all of which were 30 31 115 open to public access and managed by modern scrub control regimes. At each site, a study area of ~1 32 33 116 ha comprising both cleared and structurally complex areas of vegetation (>40 m2) separated by 34 35 36 117 footpaths (Fig. 3a,b) was identified. Cleared areas were characterised by vegetation <10 cm in height 37 38 118 (in any of five measurements using a ruler along a sampling transect) and contained no tall vegetation. 39 40 119 Complex areas comprised mosaics of shrub species varying in height and patches of bare ground <1 41 42 120 m2. Male and female adders were observed basking on or moving through cleared and complex areas 43 44 45 121 at several of the sites (Fig. 3c). 46 47 48 122 To quantify operative temperatures during the period of adder activity, temperature loggers were 49 50 51 123 deployed on all six Norfolk sites between 23-30 April (spring season) and 1-7 July (summer season) 52 53 124 2015. On each site, three loggers (programmed to record temperature every 30 minutes) were placed 54 55 125 in each of three different microhabitats (i.e. 9 models per site, 54 models in total): ‘cleared’ (exposed 56

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1 2 3 126 and >20 m from shrubs and trees), ‘complex’ (exposed but <30 cm from vegetative cover) and 4 5 6 127 ‘shelter’ (completely concealed beneath vegetation at a depth of 30 cm). The biophysical models 7 8 128 containing loggers were in contact with the ground for their entire length and oriented on a north- 9 10 129 south axis to maximise exposure to the midday sun, replicating adder behaviour. 11 12 13 14 130 Plasticine adder models were deployed during the adder mating season (Norfolk: 1-14 May; Surrey: 15 16 131 18-31 May). In total, 770 models (385 of each sex) were deployed. At each site, the number of models 17 18 132 ranged from 60 to 90, and equal numbers were deployed in cleared and complex areas. Models were 19 20 21 133 deployed singly at ground-level and at 15 m intervals (alternating between male and female models) 22 23 134 along one transect in each study area. Transects ranged from 5 m to 30-50 m from footpaths, with the 24 25 135 range of distances being equal in cleared and complex areas at each site. In complex areas, all models 26 27 28 136 were positioned close to (<30 cm) vegetative cover (e.g. gorse or heather stands). On one of the sites 29 30 137 (Headley Heath), in addition to cleared and complex areas, 20 models were deployed in each of two 31 32 138 ‘wildlife havens’ (areas of approximately 50 m2 enclosed by gorse). 33 34 35 36 139 At each site and in each treatment, all models were deployed on the same day and 37 38 140 subsequently relocated and checked for damage five times in 48 hr intervals (i.e. deployed for 10 39 40 141 days in total). For each damaged model, the location (cleared or complex area), distance to the 41 42 142 nearest footpath, animal responsible for damage, and the most intensively damaged body section 43 44 45 143 (the full body length was divided into equal thirds: head and neck, mid-body, tail-end) were 46 47 144 recorded. Damaged models were removed and not replaced. 48 49 50 51 52 53 54 55 56 57 58 59 60

1 2 3 145 Estimating levels of recreational activity 4 5 6 7 146 During each of the five spring (May) surveys of adder models on each site, the number of 8 9 147 visitors was also recorded. Each survey took place between 08:00 and 18:00 and one of the five 10 11 12 148 surveys on each site was undertaken on a weekend. At each site, one 200 to 400 m-long transect was 13 14 149 established along existing footpaths, providing good visibility and coverage of the entire study area 15 16 150 containing adder models. Surveys consisted of walking the transect for 0.5 h recording each person 17 18 19 151 entering the study area, along with their activity: walking (W), dog walking (DW), running (R), 20 21 152 cycling (C), or horse riding (HR). Each dog was recorded as either on or off the lead (L/NL), and each 22 23 153 individual was recorded only once per survey. These counts were used to generate ‘human activity 24 25 26 154 indices’ for each site by dividing total count (of each category and all categories combined) by the 27 28 155 number of surveys. 29 30 31 32 156 Analysis 33 34 35 157 Variation in the operative temperatures recorded by temperature loggers every 30 minutes was 36 37 158 explored using a generalised linear mixed model (GLMM using the R package ‘lme4’ (Bates et al. 38 39 40 159 2013)) with time of day (hour), treatment (cleared, complex or sheltered), season (spring or summer), 41 42 160 and their interactions, as predictor variables, and day, site and logger ID as random factors (Table 2). 43 44 161 A post-hoc test (using R package ‘multcomp’ (Hothorn et al. 2017)) was used to examine 45 46 47 162 temperature variation within treatment. The effects of habitat structure on adder model attacks was 48 49 163 explored in a GLMM with a binomial error structure and model fate (attacked or not attacked) as the 50 51 164 response variable, treatment (cleared or complex) and distance to footpath and their interaction as 52 53 165 54 predictor variables, and site as a random effect (Table 2). Separate models with this structure were 55

56 166 then used to examine attacks by (1) all predators, (2) dogs, and (3) livestock (too few attacks by avian 57 58 59 60

1 2 3 167 predators were recorded to allow analysis). We examined the relationship between the index of human 4 5 -1 6 168 activity (log10 transformed people survey ) and model attack rate (mean proportion of models 7 8 169 damaged in the two survey periods) across the 10 sites using linear regression. Variation in 9 10 170 recreational activity was explored using a general linear model (GLM) with a Poisson error structure 11 12 13 171 and log link function, with number of people as the response variable, and day, site and activity as 14 15 172 predictor variables (Table 2). To test the overall effects of factors, we used Chi-squared tests to 16 17 173 compute analysis of deviance tables for model fit. 18 19 20 21 174 In all models, non-significant (P > 0.05) variables were removed by sequential backwards 22 23 175 deletion (although for completeness, their estimates and associated probabilities in maximal models 24 25 176 are also reported). All analyses were carried out in R 3.4.2 (R Core Team 2017). 26 27 28 29 177 30 31 32 178 Results 33 34 35 36 179 37 Thermal variation across heathland sites 38 39 40 180 Operative temperatures (Te) on heaths varied significantly throughout the day and with habitat 41 42 181 structure (Table 3; Fig. 4). Temperature loggers in shelter beneath vegetation had mean temperatures 43 44 o 45 182 up to 20 C cooler than those exposed within structurally complex and cleared areas and, although the 46

47 183 difference in temperatures between treatments was similar across the seasons, overall temperatures 48 49 184 were significantly higher in summer (July) than spring (April) (Table 3). Consequently, while mean 50 51 52 185 spring temperatures in sheltered areas remained well below adders’ preferred range (Tset: measured 53 54 186 in a laboratory thermal gradient by Herczeg et al., 2007 & Lourdais et al., 2013), temperatures in 55 o 56 187 structurally complex and cleared areas approached Tset (deviation < 5 C) for 5.5 hours of the day 57 58 59 60

1 2 3 188 (Figure 4). In the summer period, Te in both cleared and complex areas greatly exceeded adders’ 4 5 6 189 critical thermal maximum temperature (CTmax: Brattstrom, 1965; Spellerberg, 1972) for the 7 8 190 majority of adders’ activity period (Fig. 4), while those in sheltered areas remained well below CTmax 9 10 o 191 and only approached Tset (deviation < 5 C) for four hours of the day (Fig. 4). 11 12 13 14 192 Attack rates between sites 15 16 17 193 Of the 770 model adders, 203 (26.4%) were damaged. The rate of damage to models ranged from 18 19 194 6.3% at Buxton Heath to 68.6% of models at Marley Common (Table 4; Fig. 5). 20 21 22 23 195 Effects of habitat complexity and distance to footpaths on attack rates 24 25 26 27 196 Significantly more models were damaged in cleared than in structurally complex areas on heaths (Fig. 28 29 197 6a) and attacks were significantly more frequent closer to footpaths (Table 4). Overall, damage rates 30 31 198 were ~3 times more frequent in cleared areas but the relative impact of different predators varied with 32 33 34 199 habitat structure; the few recorded bird attacks occurred in both cleared and complex areas and similar 35 36 200 numbers of models were trampled by livestock in cleared and complex areas (Fig. 6b, Table 4). 37 38 201 However, the risk of dog attack was significantly greater in cleared than complex areas, with 79% of 39 40 41 202 dog attacks occurring in cleared areas (Fig. 6b), and in areas closer to footpaths (Table 4). The risk of 42 43 203 dog attack close to footpaths (<20 m) was significantly greater, and attacks occurred over a greater 44 45 204 range of distances (up to 40 m) from footpaths, in cleared than complex areas (Fig. 7).

46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

1 2 3 205 Recreational activity and attack rates 4 5 6 7 206 The human activity index varied significantly between sites, as did the relative amounts of the five 8 9 207 recreational activities (Fig. 8; Table 5). Dog walking was the most frequently recorded recreational 10 11 208 activity at most sites and virtually all dogs seen were off the lead (Fig. 8). 12 13 14 15 209 Animals responsible for damage to models 16 17 18 210 While five bird attacks were recorded across three sites, dog attacks and trampling by grazing 19 20 21 211 livestock constituted the great majority of damage to models (Fig. 5). The most heavily damaged 22 23 212 part of the model varied among animals responsible (x2 = 9.11, d.f. = 2, P = 0.01; Fig. 9). In models 24 25 213 attacked by dogs, significantly more damage was sustained to the head and neck (x2 = 32.70, d.f. 26 27 2 28 214 = 2, P < 0.001), while trampling by livestock caused similar damage among body sections (x = 29 30 215 8.14, d.f. = 2, P = 0.54). 31 32 33 216

34 35 36 37 217 Discussion 38 39 40 41 218 While scrub control is an important component of heathland management and 42 43 219 conservation, large-scale reduction in complex vegetation can have potentially important 44 45 220 consequences for adder thermoregulation and survival. In cleared areas in which management has 46 47 48 221 reduced vegetation height and structural complexity over large areas, thermal conditions were harsher 49 50 222 and adder models were subject to an increased risk of predation. Our study suggests the greatest direct 51 52 223 threat to survival on open-access heaths is posed by domestic dogs, and attack rates were greater in 53 54 55 224 sites with more recreational activity and in areas closer to footpaths. Although maintaining adder 56

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1 2 3 225 populations is often an aim of this type of heathland management, these findings suggest that the scale 4 5 6 226 at which these operations take place may have unintended impacts on adder populations in the short 7 8 227 and long-term (Martin & Lopez, 1999; Webb & Whiting, 2005). Efforts to retain habitat structural 9 10 228 complexity and moderate the impact of recreational activity on open access heaths are likely to be of 11 12 13 229 great importance to the conservation of adders on heathlands. 14 15 16 230 In thermally suboptimal conditions, structurally complex vegetation can facilitate adder 17 18 231 thermoregulation by enabling effective energy assimilation (Huey, 1974; Huey & Slatkin, 1976), and 19 20 21 232 our biophysical models showed that temperatures deviated least from adders’ preferred range in 22 23 233 complex areas. The effect is especially important during spring when, following emergence from 24 25 234 hibernation, adders must bask in direct sunlight for long periods to achieve preferred body 26 27 28 235 temperatures. However, on hot summer days the effect of habitat structural complexity is more 29 30 236 immediate, as ground temperatures in areas without shelter exceeded adders’ critical thermal 31 32 237 maximum for much of the day, reaching over 50oC. While reptiles are well adapted behaviourally and 33 34 238 physiologically to cope with thermal variability (Huey, Losos & Moritz, 2010), extreme high ground 35 36 37 239 temperatures on heaths in summer months represent a potentially lethal risk to adders of overheating, 38 39 240 particularly while mate-seeking, foraging or dispersing. Where vegetation on heaths is reduced to 40 41 241 large areas of short vegetation, adders are unable to thermoregulate by seeking refuge from the sun 42 43 44 242 (Huey, 1974). 45 46 47 243 Structurally simplified areas of heaths also produced significantly higher attack rates of adder 48 49 244 models than in complex areas. The detection of snakes by other animals is likely to be primarily visual, 50 51 52 245 and habitat simplification could reduce concealment of adders (Isbell, 2006; Stevens, 2009; Allen et 53 54 246 al., 2013), in addition to facilitating mammalian movement across heathlands (e.g. Murison et al., 55 56

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1 2 3 247 2007). Although not measurable in our experiments, adders may also be less able to escape from 4 5 6 248 predators in cleared areas, and thus be less likely to survive an attack. 7 8 9 249 Overall, attack rates on our models were high, with 26% being damaged during their 10 day 10 11 250 deployment. While live adders may be likely to seek cover when dogs are nearby, high numbers of 12 13 14 251 adder bites of dogs have been documented in the UK (Reading et al., 1995; Sutton, Bates & Campbell, 15 16 252 2011) and elsewhere in Europe (Kangstrom, 1989; Lervik, Lilliehöök & Frendin, 2010), and there are 17 18 253 numerous reports of adder bites to the legs of cattle, ponies and sheep (Luckham, 1944; Prestt, 1971; 19 20 21 254 Arbuckle & Theakston, 1992). Conversations with dog walkers during fieldwork revealed accounts 22 23 255 of dogs attacking and killing adders and JWH has previously found the carcases of adders showing 24 25 256 injuries apparently consistent with dog attack and trampling by livestock (Appendix 2). While the 26 27 28 257 immobility of Plasticine models may have led to overestimation of the true frequency of predation, 29 30 258 our estimate of avian predation rates is similar to that reported on heathlands by Wüster et al. (2004), 31 32 259 and the fact that dogs attacked predominantly the head or tail regions of models [reflecting predator 33 34 260 behaviour in other studies (Smith, 1973; Brodie, 1993; Wüster et al., 2004)] suggests they were treated 35 36 37 261 as if they were real snakes, and were not merely ‘tasting’ the Plasticine as some rodents do (Madsen, 38 39 262 1987). 40 41 42 263 43 Hostile conditions could result in cleared areas on heaths being actively avoided by 44 45 264 adders, which may further reduce habitat availability for this declining species. The movement 46

47 265 of adders into remaining patches of complex vegetation or adjacent land could, in turn, lead to 48 49 266 increased predation risk if there is an immediate increase in adder density in these areas. In 50 51 52 267 addition, scrub clearance can cause significant habitat fragmentation on heaths, and simplified areas 53 54 55 56 57 58 59 60

1 2 3 268 that are large relative to the size of the site, or represent a high proportion of the site, have the potential 4 5 6 269 to seriously inhibit adder movement (Fahrig, 2007; Croak, Webb & Shine, 2013). 7 8 9 270 10 11 12 13 271 Implications for heathland management 14 15 16 272 The findings of this study suggest that, where heathland management is necessary to maintain 17 18 273 mid-successional stage habitat, strategies that retain some habitat structural complexity within 19 20 21 274 managed areas should be included to reduce detrimental effects on adders. Ideally, the 22 23 275 simultaneous removal of all vegetation cover across a site, or substantial areas of it, should 24 25 276 be avoided, and the selection of sections of a site to be cut should target areas where scrub 26 27 28 277 encroachment is most severe, and avoid important habitat features for adders, such as 29 30 278 hibernacula and foraging areas. Cutting and clearing of vegetation should ideally be 31 32 279 conducted in narrow strips, and/or in phased cutting of many small (rather than fewer, 33 34 280 large) management plots, as this is likely to have less severe impacts on adders, and the 35 36 37 281 resulting more connected mosaic of different vegetation types and age classes can provide a 38 39 282 greater spectrum of discrete resources for adders and other important heathland taxa. 40 41 283 Where mechanised cutting makes such small-scale management more difficult to achieve, 42 43 44 284 opportunities for hand cutting of vegetation may be important to consider, where feasible. 45 46 285 Finally, where the conservation of adders is a primary objective, avoiding the use of 47 48 286 livestock grazing as the means of habitat management will likely reduce the risk of 49 50 51 287 disturbance and trampling. Our findings add to evidence that the generic, landscape-scale 52 53 288 policy of grazing management on heathland can be harmful to many species of conservation 54 55 289 concern (Lindenmayer & Fischer, 2006; Newton et al., 2009; Reading & Jofré, 2015; Reading & 56

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1 2 3 290 Jofré, 2016). The apparent threat to adders posed by dogs on heathlands highlights a 4 5 6 291 management issue for reconciling the recreational needs of visitors with the requirements of 7 8 292 species of conservation interest. The Countryside Rights of Way Act 2000 (CRoW Act) is based 9 10 293 on the notion of responsible access, with a provision for dogs to be kept on a fixed lead during 11 12 13 294 the ground nesting bird season (generally 1 March to 31 July). This period coincides with the 14 15 295 adders’ breeding season, and our findings strongly support the need for such a provision. 16 17 296 However, alternative options to manage, or manipulate, recreational activity may be more 18 19 297 beneficial, and could include diverting footpaths and strategic placement of impenetrable 20 21 22 298 barriers (e.g. gorse Ulex europaeus) to protect sensitive areas, as already occurs on some 23 24 299 heaths (JWH, pers. obs.). Targeted vegetation clearance may help to dissuade adders from 25 26 300 specific areas, such as access points, car parks, or dedicated off-lead areas for dogs. 27 28 29 301 However, this should be weighed against the value of public engagement on peri-urban or urban 30 31 302 green spaces, which has produced tangible conservation benefits even for venomous snakes 32 33 303 (Bonnet et al., 2016). For people and adders, and towards the broader aim of coexisting with 34 35 36 304 wildlife, educational activities, informative (rather than warning) sign boards, and other 37

38 305 initiatives to raise awareness and understanding of adders, may also be a component of

40 306 management plans on heathland sites.

42 43 307 44 45 46 308 Acknowledgements 47 48 49 50 309 We are grateful to Norfolk Wildlife Trust, Surrey Wildlife Trust, the Forestry Commission and 51 52 310 the National Trust for allowing access onto their nature reserves. Thanks to Tom Biddulph for 53 54 55 311 assistance in the field, to all who helped with making adder models and to two anonymous 56 57 58 59 60

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1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 Review 22 23 24 25 26 27 28 29 30 31 Copy 32 33 34 35 36 37 38 39 40 41 42 43 44 45 Image of study species to be considered for the publication cover. 46 47 73x105mm (240 x 240 DPI) 48

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