Responses of wild reindeer (Rangifer tarandus tarandus) when provoked by a snow-kiter or skier: A model approach

Applied Animal Behaviour Science 142 (2012) 82–89

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Applied Animal Behaviour Science journal homepage: www.elsevier.com/locate/applanim

Responses of wild reindeer (Rangifer tarandus tarandus) when provoked by a snow-kiter or skier: A model approach Jonathan E. Colman a,b , Marte S. Lilleeng b , Diress Tsegaye a,b,∗ , Magnus D. Vigeland c , Eigil Reimers a a b c

Department of Biology, Post box 1066 Blindern, University of Oslo, 0316 Oslo, Norway Department of Ecology and Natural Resource Management, Post box 5003, Norwegian University of Life Sciences, 1432 Ås, Norway Department of Medical Genetics, Post box 4956, Oslo University Hospital and University of Oslo, 0424 Oslo, Norway

a r t i c l e

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Article history: Accepted 27 August 2012 Available online 15 September 2012 Keywords: Feeding time Fright responses Human disturbance Rangifer tarandus tarandus Skier Snow-kiter

a b s t r a c t We compared reindeer (Rangifer tarandus tarandus) fright responses towards a directly approaching snow-kiter or skier in Norefjell-Reinsjøfjell, Norway during winter in 2006–2007. Fright response distances sampled in the field were significantly longer when approached by a snow-kiter than by a skier. A simulation model predicts a different outcome of daytime disturbances for reindeer from free ranging snow-kiters versus skiers confined to prepared ski trails. The expected number of encounters with reindeer increases linearly with increasing number of snow-kiters until it reaches a threshold level and then stabilizes, but the number of snow-kiters reaching a threshold will vary depending on the speed of the kite (252 snow-kiters at 8.8 km h−1 or 96 at 20 km h−1 ). The relative loss of habitat and daytime feeding for reindeer following encounters with snow-kiters moving randomly within their range increases progressively up to a 100% reduction at 241 or 111 snow-kiters at a speed of 8.8 and 20 km h−1 , respectively. Above this number of snow-kiters, reindeer will not feed and have nowhere to escape. Reindeer progressively reduce up to 7.5% of their daytime feeding until the number of skiers reaches 105. Above 105 skiers and as the number of skiers continues to increase, reindeer find refuge away from ski trails and their feeding time increases and returns to a zero percent reduction at 133 skiers or more. Long fright responses by reindeer towards snow-kiters and potentially very negative population consequences necessitate additional information on snow-kiting activities and appropriate management measures in reindeer habitats. © 2012 Elsevier B.V. All rights reserved.

1. Introduction Modern activities such as snowmobiling and snowkiting are, in combination with traditional activities like hiking, skiing and dog sledding, increasing the potential speed, radius and distribution of human recreation into previously remote, less used areas (Forbs, 2006; Reimers

∗ Corresponding author at: University of Oslo, Department of Biology, Post box 1066, 0316 Oslo, Norway. Tel.: +47 22854628; fax: +47 22854726. E-mail addresses: [email protected], [email protected] (D. Tsegaye). 0168-1591/$ – see front matter © 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.applanim.2012.08.009

et al., 2003). In Norway, the number of cabins (Kaltenborn et al., 2009) and popularity for randoneering, snowmobiling, and snow-kiting are increasing. Snow-kiting is a relatively new sport in Norway and, presently, is estimated to be one of the fastest growing recreational winter sports in the country. As a non-motorized activity, there are no restrictions limiting individuals’ use of snow-kites in Norwegian countryside. However, we have no documented knowledge of the effect of snow-kiting on wild reindeer (Rangifer tarandus tarandus) and there is a growing concern among wildlife managers, politicians, and snow-kiters themselves over snow-kiting’s potential negative interactions with wildlife, especially wild reindeer.

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Fig. 1. The disturbance procedure for the snow-kiter. The distance from 0 to A, B, C and D represents the “start”, “alert”, “flight initiation” and “escape distance”, respectively.

Snow-kiting is the use of a kite to move forward by wind power with the kiter on skis or a snowboard. The maximum speed has been measured to about 100 km h−1 , while most snow-kiters move within the range of 5–40 km h−1 . The kite is connected to the skier with thin, 25–30 m long nylon lines attached to a belt (Fig. 1). Due to the manoeuvrability of the kite, the activity is mainly conducted in open terrain, such as frozen lakes, fjords, farmland or alpine areas above the tree line. Snow-kiters can be divided into two subgroups; tour-kiters who often travel over 100 km on a normal day, and stationary snow-kiters who mostly use confined areas close to roads and infrastructure. With its speed, large radius and unpredictable movements in mountain terrain, tour-kiting has a large potential for interactions with reindeer. Furthermore, as an airborne stimulus, the kite is visible over large distances. Such outdoor recreational activities may have both short term and long-term ill effects on reindeer populations and other wildlife (Stankowich, 2008). The impact of humans on fright behavior in ungulates is comprehensively reviewed by Stankowich (2008). He found evidence across studies that ungulates pay attention to approacher’s behavior, have greater perceptions of risk when disturbed in open habitats and, in general, groups with young offspring show larger fright responses than other groups. Flight initiation distance is the distance at which an animal begins to flee from an approaching predator (Ydenberg and Dill, 1986). Because it is easy to systematically approach animals until they flee, and because flight initiation distance is correlated with alert distance, the other key aspects of escape behavior (Blumstein et al., 2005), flight initiation distance is an excellent metric with which to quantify an individual’s fearfulness in a particular situation. Stankowich (2008) concluded that humans on foot were more evocative than other stimuli (vehicles, noises), similar to Reimers et al. (2003) who found that wild reindeer showed stronger fright responses towards skiers compared to snowmobiles. Importantly, a higher speed of approach was found to be positively correlated with response distances; i.e. higher speeds invoked responses at farther distances and stronger responses resulting in longer escape distances (Reimers et al., 2003; Stankowich, 2008). Any factor that reduces grazing time may become a constraint on survival and productivity. Colman et al. (2003) showed that the loss of grazing time reduces reindeers’ ability to gain weight. Prolonged or reoccurring disturbances may therefore have negative impacts on reindeer activity patterns, nutrition, and subsequent influence on population performances (Holand et al., 2006; Klein, 1991;

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Reimers, 1982). Additionally, disturbances from human activities can cause avoidance of limited winter pastures, critical for reindeer during winter (Reimers and Colman, 2006). Often, the connection between behavioral responses and population consequences is either speculative or too detrimental for a wildlife population to be tested in the field. In this study, we conduct a field disturbance experiment to test the hypothesis that wild reindeer are more sensitive to disturbance from snow-kiters than from skiers, and predict this to be revealed by longer response distances. In addition, we support the field experiment with a theoretical approach to simulate the differences in disturbance in response to snow-kiters and skiers on reindeers’ feeding time and area use. The aim is to provide new knowledge as a tool for managers to better predict the disturbance level and potential population level consequences of these and other activities. 2. Materials and methods 2.1. Study area We conducted this study in the winter range (110 km2 ) of Norefjell-Reinsjøfjell (308 km2 ) wild reindeer area (60◦ 25 N; 9◦ 05 E). The area is dominated by alpine terrain at altitudes of 900–1500 m. The Norefjell-Reinsjøfjell winter herd has remained at around 500–600 animals during the last 20 years through a sustainable hunting rate of 38% of the winter herd (Reimers et al., 2009). The alpine area has a network of footpaths and ski trails, the latter covering approximately 59 km and maintained regularly by snowmobiles during winter. 2.2. Field methods We disturbed reindeer by a snow-kiter or a skier in alternating approaches with at least a one-hour interval between each approach (14 approaches each) during winter (February and March) in 2006 and 2007. To minimize stress to the reindeer, we limited the number of approaches to provide enough data for sufficient statistical analytical power and what was necessary to fulfill our simulation criteria. For the snow-kiter, the kite was unpacked and rigged out of sight of the reindeer. As the lines of the kites are very long and the study area was mostly rugged terrain with many small hills, reindeer often sighted the kite when a snow-kite provocation began before they sighted the snow-kiter at the base of the kite lines. Therefore, prior to the start of a provocation, we positioned a person to observe the entire approach without being detected by the reindeer. This observer recorded the entire event using a high magnification (25× optical zoom) video camera throughout the approach. Through radio contact, the observer informed the snow-kiter when to drop markings on the ground following the reindeers’ responses. The reindeers’ reaction distances were measured with laser monocular (Leica Scan 1200) by back-tracking from the position of the reindeer to each marker. The snowkiter approached in a straight line from the start position

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towards a group of reindeer at a constant speed (mean speed was 8.8 km h−1 , which was kept relatively low in order to control the variable “speed” along with that of a skier). The approach continued until the snow-kiter reached the center location of the group’s original “predisturbed” location (Fig. 1). Immediately, the snow-kiter laid down the kite, and withdrew from the area along the same line of approach. Similar procedure was used when skiing, but the speed of approach was slower (mean speed was 7 km h−1 , i.e. the natural, average speed of a skier on prepared trails). When reindeer groups were identified, the approach method (snow-kiter or skier) was decided randomly before determining the starting position. To compare the effect of disturbance by snow-kiters and skiers, we measured three response distances (alert, flight initiation, and escape) as well as the starting distance. This is described in Stankowich (2008) and Reimers et al. (2009) (Fig. 1): (1) starting distance (A); the distance between the start point and the estimated center point of the group at start of the approach. (2) Alert distance (B); distance between the approacher and the group center point when ≥50% of the group exhibited alertness reaction by grouping together. (3) Flight initiation distance (C); distance between the approacher and the group at the moment of flight. Flight distance was measured at distance where ≥50% of the group evidently started moving away from the approacher. (4) Escape distance (D); straight line distance from where reindeer took flight to where they stopped fleeing from the approacher, i.e. when ≥50% of the group resumed relaxed behavior (i.e. grazing or lying). For each approach, we recorded the following independent variables; weather (i.e. partly sunny or cloudy), terrain, wind direction, number of approaches to the group, the reindeer activity before the approach, and approach direction in relation to wind, terrain and sun. This study was conducted with approval from the Norwegian Animal Research Authority and regional and local reindeer management authorities. Our experiments therefore completely comply with the current laws of Norway. 2.2.1. Data analysis of field samples Starting distance and reindeers’ response distances (i.e. alert, flight and escape) were analyzed separately with linear mixed-effects models (LME) in R (R Development Core Team, 2011), with library nlme (Pinheiro and Bates, 2000). All distances were ln transformed leading to normal distribution of the residuals. The explanatory categorical variables included in all the models were: approach method (skier vs. snow-kiter), reindeer activity before approach (lying vs. feeding), approach direction in relation to wind direction (side vs. with), approach direction in relation to terrain (up vs. flat), and weather (partly sunny vs. cloudy). As all reindeer groups (n = 8) were encountered in rugged terrain and the encountered groups were mixed (females, young animals and a few adult males) and large groups (between 100 and 250 animals; see Reimers et al., 2009, 2012), none of these parameters were included in the models. Number of approaches was included as continuous explanatory variable (centered at 1) in all the models. As response distances may vary depending on the start distance of the approacher, we included start distance as a

numerical fixed effect (ln transformed and centered around the mean) for alert, flight and escape distances. To account for dependency between observations on the same reindeer group, we included group as a random factor in all the models. To select the variables for our models, we used backwards elimination (Crawley, 2007), starting with the full models containing all the variables. For tests of fixedeffects in LMEs, we used marginal F-tests (Pinheiro and Bates, 2000). We removed variables with the highest Pvalue and repeated this procedure until only variables with P < 0.05 were retained except for the approach method, which we retained in all models. We do not report results of marginal F-tests; we present only parameter estimates of the final models. The analyses were performed in R statistical software version 2.12.0 (R Development Core Team, 2011). 2.3. The theoretical model We developed a theoretical model to simulate the expected effects of provocation from increasing numbers of snow-kiters and skiers in the terrain, measured in expected number of encounters during daytime versus loss of area use and feeding time for reindeer. The normal response for wild reindeer when encountering humans is to cease their undisturbed activity, e.g., grazing or lying, and move away. We used two assumptions for the simulation: (1) we expect the movements of snow-kiters to be random and unevenly distributed in the terrain. As snow-kiters use the wind as their source of energy to move, they normally do not follow prepared trails, but move in certain directions in relation to the wind and topography. In this model, we thus assumed that snow-kiters choose their routes randomly. (2) Most skiers prefer to follow marked and prepared ski trails, providing a much faster glide with today’s modern skis. We therefore expected all skiers to follow marked trails. This expectation is routinely confirmed in the field. The important aspect in the simulation is the difference in predictability for the two types of provocations in the reindeers’ habitat. The model is based on number of encounters between reindeer and either snow-kiters or skiers. We assume that disturbances occur when distance between approacher and a reindeer group are at the upper quartile flight distance recorded in the field, respectively, for the two activities. Each provoker will contribute to an area (defined by the radius equaling the length of the upper quartile flight distance as explained above) where encounters can possibly occur. Because both activities represent moving objects, the size of this area over time depends on the mean duration of a disturbance source and velocity of locomotion (defined below). Thus, the area of influence for a snow-kiter (Ik ) or skier (Is ) (i.e. where an encounter may occur with a reindeer group) is represented by the following equations. Ik = 2rk vk t Is = 2rs vs t where rk and rs are the reindeer flight distances measured in kilometers for snow-kite and ski provocations,

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respectively; vk and vs are mean velocities, measured in kilometers per hour; and t is any one time interval during a day with a constant duration, measured in hours. The area of influence in t will have an upper limit. For snow-kiters, the maximum area of influence will equal the entire alpine range for reindeer above the tree-line. Following the assumptions, no encounters will occur in areas where encounters have already occurred because the reindeer have fled from this area. For skiers, the maximum area of influence will depend on the length of the ski trails, as we assume that all skiers use these trails, and therefore, encounters with reindeer will only happen in relation to ski-trails above the tree-line. The size of the area of influence (i.e. within the total area of winter range above the tree-line for the reindeer group; 110 km2 ) depends on the number of disturbers and will differ for snow-kiters and skiers. When encounters occur, reindeer will move away from a disturbance, and the area available for the reindeer will decrease. The area where reindeer can escape into will be rather large; close to the total area, when there are few provokers. When the area is visited by skiers, the available reindeer area will reach a lower limit. There is no lower limit when the area is visited by snow-kiters because of the random and potentially wide-spread distribution of this provocation stimulus. We have made an assumption that no new encounters occur during the time the reindeer are reacting from a snow-kiter or skier, i.e. response time. This assumption explains why the number of encounters between reindeer and snow-kiters reaches a limit. At this limit, the reindeer will experience new encounters as soon as they stop reacting from the last encounter. The relative loss of feeding time is thus found by the following equations: Tk (n) =

(Ek (n) × tr ) D

Ts (n) =

(Es (n) × tr ) D

where Tk (n) and Ts (n) are relative loss of feeding time of reindeer in response to a snow-kiter and skier, respectively. Ek (n) and Es (n) are expected number of encounters from a snow-kiter and skier, respectively. D and tr represent number of hours per day and reaction time, respectively. The relative loss of habitat as consequence of encounters in a single day between reindeer and snow-kiters, would ultimately reach 100%. The relative habitat loss for encounters between reindeer and skiers will at maximum equal 2rs L/F. L represents length of ski trails (=59 km) in the winter range, and F represent the total area of winter range above the tree-line (=110 km2 ) for the reindeer herd. After each encounter, the reindeer will abandon a circle area equal to fk2 and fs2 , where fk and fs is the “total distance fled” as response to snow-kite and ski provocation, respectively. The loss of habitat will then depend on number of encounters and how long these circles are abandoned. We applied the upper quartiles (Q3) of the flight reaction distances and total distance moved (measured after provocations from snow-kiters and skiers in 2006 and 2007). We measured flight distance to be 0.311 km from snow-kiters

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(=rk ) and 0.069 km from skiers (=rs ). Escape distances were 0.600 km from snow-kiters (=fk ) and 0.101 km from skiers (=fs ). We used the combined length of all marked, prepared ski trails above the tree-line according to the public map “Nesbyen 1:50,000”, totaling 59 km (=L). The model describes a function of the numbers of disturbers, n, i.e. number of snow-kiters and skiers, and we varied these numbers to illustrate scenarios of different disturbance levels. We used 8.8 km h−1 for snow-kiters and 7 km h−1 for skiers as the mean velocities, i.e. the speed used in the field experiment. In addition, we modeled with a snow-kite speed of 20 km h−1 to simulate more realistic snow-kite speeds in alpine areas, i.e. expected average speeds for a tour-snow-kiter and based on our own experience during the field studies when not provoking reindeer. Based on our knowledge of these activities in the study area and winter/spring light conditions at this latitude, we set the number of hours for snow-kiters or skiers per day to be 8 h and defined this as a “day”. We also assumed the number of snow-kiters or skiers to be constant during a day. This implies that there were just as many skiers in the terrain in the first hour of the day as at midday and in the last hour of the day. “Response time” (=tr ) is the number of minutes from when animals initiate flight response until they again achieve normal behavior. Tyler (1991) found a median response time at 3 min and 13 s in Svalbard reindeer (Rangifer tarandus platyrhynchus). We set a higher tr (=5 min) for this model using our own experience for mountain reindeer in Norefjell-Reinsjøfjell. We also believe that Svalbard reindeer show less nervous behavior towards disturbance than mountain reindeer. We used piecewise linear modeling to predict the expected effects of provocation from snow-kiters and skiers in R statistical software version 2.12.0 (R Development Core Team, 2011).

3. Results 3.1. Fright responses Starting distance was significantly longer for a snowkiter (486 ± 146 m, mean ± SD) than a skier (317 ± 174 m) (P = 0.02; Table 1). Longer starting distance was related to longer alert distance (P = 0.001; Table 1). The reindeer showed longer alert response distances when approached by a snow-kiter (395 ± 111 m) than by a skier (117 ± 88 m) (P < 0.001; Table 1). Increasing alert distance results in longer flight initiation distances (P = 0.002). Flight initiation distance was significantly longer when approached by a snow-kiter (237 ± 114 m) than by a skier (70 ± 51 m) (P < 0.001; Table 1). An upward approach towards the reindeer had a significantly weaker influence on flight initiation distances compared to when approaching level in the terrain with the reindeer (P = 0.01; Table 1). Escape distance was longer when the reindeer were approached by a snowkiter (469 ± 286 m) than by a skier (75 ± 52 m) (P < 0.001; Table 1). Unlike the alert distance, flight and escape distance were not correlated to the start distance. Overall, a snow-kiter elicits significantly stronger responses from the reindeer than a skier regardless of other factors (Fig. 2).

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Table 1 Linear mixed-effects models for predicting start, alert, flight initiation and escape distances of wild reindeer disturbed by an approaching skier or snow-kiter in Norefjell-Reinsjøfjell, south-central Norway in winter of 2006 and 2007. We used start distance (centered around the mean) as a numerical fixed effect (ln transformed) when modeling response distances. The level after “vs.” in the table indicates reference levels for categorical variables. Variable

Estimate

SE

t-value

P-value

1. Starting distances (ln) Intercept Approach method (skier vs. snow-kiter)

6.14 −0.57

0.17 0.23

37.14 −2.54

<0.001 0.02

2. Alert distances (ln) Intercept Approach method (skier vs. snow-kiter) Start distance (ln)

5.86 −1.09 0.54

0.11 0.17 0.14

51.95 −6.42 4.03

<0.001 <0.001 0.001

3. Flight initiation distances (ln) Intercept Approach method (skier vs. snow-kiter) Direction of approach in terrain (up vs. flat)

5.76 −1.17 −0.68

0.18 0.19 0.21

31.43 −6.17 −3.31

<0.001 <0.001 0.01

4. Escape distances (ln) Intercept Approach method (skier vs. snow-kiter)

5.99 −1.92

0.20 0.27

29.31 −7.01

<0.001 <0.001

3.2. The simulations The pattern for expected number of encounters per day between reindeer and snow-kiters and skiers, respectively, varied considerably (Fig. 3). As the number of snow-kiters increases, the expected number of encounters with reindeer increases linearly until it reaches a threshold level and then stabilizes at a constant level when there are 96 and 252 or more snow-kiters in the area at a speed of 20 and 8.8 km h−1 , respectively (Fig. 3). An increase in the number of skiers does not exhibit the same effect; the expected number of encounters between reindeer and skiers will increase linearly to 105 skiers, after this level it reduces and will return to zero at 133 skiers (Fig. 3). At this level, the ski trails become – “filled up” or saturated with skiers, so that the reindeer will never be at or near the trail or within a distance from a trail that is within the radius of the upper quartile flight distance. In other words, the reindeer settle at some distance outside the boundary defined

600

Snow-kiters Skiers

500

Distance (m)

by the response distance and any increase in number of skiers (along the prepared trails) has no new effect. The relative loss of daytime feeding for the reindeer following encounters with snow-kiters increases as long as the number of snow-kiters is less than F/(2rk vk tr ). At n ≥ F/(2rk vk tr ), which is ≥241 and 111 snow-kiters at a speed of 8.8 and 20 km h−1 , respectively, the relative loss of feeding time for reindeer will be 100% (Fig. 3). Relative loss of daytime feeding for reindeer from skiers increases until the number of skiers is n = L/(vs tr ), which equals 105 skiers using our empirical values (Fig. 3). At this number of skiers, reindeer loose approximately 7.5% of their feeding time. Then the relative loss of feeding time will decrease with number of skiers until n = L/vs (tr − t). When n is larger than L/vs (tr − t), which is >133 skiers in our model, the relative loss of feeding time will return to zero.

400 300 200 100 0

Start

Alert

Flight

Escape

Fright responses Fig. 2. Response distances (untransformed) of reindeer in groups disturbed by an approaching person snow-kiting or skiing or in NorefjellReinsjøfjell, south-central Norway in winter of 2006 and 2007.

Fig. 3. Modeled number of encounters and relative loss of feeding time for reindeer as a function of number of snow-kiters and skiers. Two scenarios for different snow-kiter speed, 8.8 and 20 km h−1 .

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4. Discussion Our field data provided a sound basis for the theoretical simulation. The reindeers’ fright responses were longer when approached by a snow-kiter than by a skier, as predicted. Velocity and size of threatening elements of human activity generally induce increased responses in wildlife (Frid and Dill, 2002; Stankowich and Coss, 2006; Stankowich, 2008). By observing the reindeers’ line of vision during provocations, we could see that the trigger stimulus for the reindeers’ reaction towards a snow-kiter was most certainly the snow-kite and not the person snowkiting, while for skiers, it is the shape of the skier itself. Thus, the combination of size and airborne stimuli from a snowkiter’s kite was more frightening for reindeer. However, the speed in our experiment was kept relatively similar for both approaches, and this suggests that differences in responses were not affected by the speed of the approach. The starting distance had a significant relationship with alert distance; i.e., longer starting distances were correlated to longer alert distances. This is in accordance with Colman et al. (2001) and Reimers et al. (2003, 2006, 2009, 2011, 2012), suggesting that the exposure time may be important for flight distance. A positive relationship between start and response distances towards anthropogenic disturbances has also been shown for other species, e.g. bison, (Bison bison), pronghorn antelope (Antilocapre americana) and mule deer (Odocoileus hemionus) (Taylor and Knight, 2003), and black-tailed deer (Odocoileus hemionus columbianus) (Stankowich and Coss, 2006). However, flight and escape distance were not correlated to start distances, similar to previous findings for ski approaches (Reimers et al., 2009). This may imply that the distance reindeer in our study area disperse from a disturbance is not affected by the approacher’s exposure time. Starting distances were significantly longer for snow-kiters than ski approaches, and were likely caused by the height of the kite, often 25–30 m in the air. At these heights, and especially in rugged terrain, the kite could be visible long before the snow-kiter. Compared to a skier, the resulting starting distances would therefore be consistently longer. The theoretical simulation combines the temporal and spatial aspects of reindeer encounters with snow-kiters and skiers, illustrating the potential for considerable negative population level consequences with relatively few snow-kiters and heavily used ski-trails in the reindeers’ habitat. Our model showed very different outcomes for disturbances from snow-kiters versus skiers. When approached with similar speed (i.e. 8.8 km h−1 ), as done in the experiment, the predicted outcome from both approaches soon reaches an upper level. When number of snow-kiters is 241 the reindeer spend 100% of their time avoiding snow-kiters during daylight hours. With a higher and more realistic speed of approach (i.e. 20 km h−1 ) it takes less than half the number snow-kiters (i.e. 111) in the area before 100% of the feeding time is lost. This is in contrast to the outcome for skiers on ski trails; the ski trail becomes saturated and the expected number of encounters between reindeer and skiers increases to a threshold (i.e. at 105 skiers). The maximum loss of feeding time at this number of skiers is 7.5%, and then falls to zero. An energetic

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cost arises when reindeer are both avoiding a disturbance and reducing their time for feeding. A maximum of 7.5% reduction of feeding time with 105 skiers, or the equivalent of 8 snow-kiters moving 20 km h−1 , might over the course of a few days or in combination with other disturbances be enough to cause negative population consequences by degrading the reindeers’ energy budgets. Reimers et al. (2003) estimated energy cost of a single winter provocation for a 60 kg reindeer ranged from a maximum of 590 kJ or 2.9% to a minimum of 31 kJ or 0.2% of daily energy expenditure. Bradshaw et al. (1998) estimated a 5 times higher energy cost of a similar maximum flight distance (2.11 km) from an oil exploration disturbance event. The difference is due to trotting/galloping costs and excitement costs (10–25% more than required for maintenance) added to the energy cost of distance traveled. Because reindeer are unable to compensate for lost grazing time caused by disturbances (Colman et al., 2003), such provocations may incur population level consequences. Likewise for feeding, reindeer area use is limited by an increasing number of snow-kiters up until refuge is no longer attainable with more than 111 snow-kiters in the terrain. As described by Reimers and Colman (2006), behavior responses such as avoidance resulting in reduced use of limited pastures can potentially lead to undernourishment and overgrazing of remaining areas not avoided. In northern and alpine areas, winter pasture is often limited and unevenly distributed. It is likely, as our simulation model suggests, that reindeer avoid areas with high encounter rates with humans, especially if these encounters are threatening enough to outweigh their motivation to remain, for example, in areas with good pasture or few predators (Reimers and Colman, 2006). For snow-kiting, relatively few snow-kiters could easily cover the reindeers’ entire range. Although ski-trails were shown to have a much smaller avoidance potential in our simulation, if a ski-trail crosses over or is positioned near enough to winter pasture, the avoidance effects could be detrimental for reindeer when their winter pasture is limited. Our simulation also illustrated that when a skitrail becomes saturated with skiers, a behavioral barrier effect may occur (see Colman et al., in press). No animals will cross the ski trail. Even though any additional increase in number of skiers along the ski-trails has no new effect, a ski-trail functioning as a barrier would inhibit crossing into some sections of the reindeers’ alpine range. It is not unlikely that wild reindeer in the Norwegian mountains have many more than 20–30 encounters per day during winter vacation and Easter holiday. Habituation is likely an important process for reindeer survival in light of future increasing human-reindeer interactions. Animals become habituated towards human activities if the disturbance is non-destructive and predictable in time and/or space (Bullock et al., 1993; Hamr, 1988; MacArthur et al., 1982; Recarte et al., 1998; Reimers and Colman, 2006; Sibbald et al., 2011). Testing for habituation versus sensitization was outside the scope of our fieldwork. We speculate, however, that habituation is more likely to occur for skiers while sensitization is more likely for snow-kiters over the course of the next few years. In this case, the field and model results represent a maximum level of disturbance for skiers and a minimum for snow-kiters.

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The scenarios generated from the simulation model revealed surprising and interesting results that can be modified and adjusted according to other species, other disturbance stimuli, or reactions distances by wildlife in other areas. Pépin et al. (1996) found that area use by Pyrenean chamois increased with distance from a hiking trail, and since this distribution of animals minimized the probability of encounters between humans and chamois, the trail makes the disturbance predictable. If all hikers moved around randomly, the disturbance effect would presumably be larger. Enggist-Düblin and Ingold (2003) modeled the impact of both hikers and paragliders on chamois and claimed that with modifications, their model may be applied to other species. They argue that “it is not the single disturbance event, but its repeated occurrence that affects the animals the most” (Enggist-Düblin and Ingold, 2003). We agree with this, but would like to add that the spatial distribution of the human activities in question is equally important. The spatial distribution and movement pattern, in temporal and spatial scales, for snow-kiters and skiers was the key to understanding their overall effect. As the quantity and especially the quality of forage is significantly less during winter, reduced grazing at this time of year will also lower the animal’s ability to maintain body weight (Colman et al., 2003). Heterogeneity of pasture is another important factor that should be expanded on in future studies. For instance, in winter, when pasture is limited by snow and ice cover, high quality areas near a ski-trail will likely be used more by reindeer relative to the ski-trails vicinity to human disturbance compared to a low quality area. 5. Conclusions This study concentrated on tour-kiting in alpine areas inhabited by reindeer, but should apply to stationarykiting arrangements when these are arranged in reindeer habitat. Snow-kiters have a much larger interaction potential with reindeer compared to skiers. Snow-kiters rapidly transport themselves over a large radius in rugged alpine areas resulting in unpredictable movements due to their high speed, high-flying and visibility over longer distances. Combining this with an understanding of reindeer’s fright responses towards snow-kiters, the effect on reindeer should be considered in areas where tour-kiting already occurs and/or is increasing in reindeer habitat. Maintaining energy balance is especially important for alpine and arctic ungulates in winter. Our simulation highlights the potential for significant spatial and temporal disturbances with increasing, yet relatively low numbers of snow-kiters. With more negative effects of snow-kiters versus skiers, and as no long term studies have yet been conducted, we recommend that the management authorities consider clear guidelines for snow-kiting in wild reindeer areas and other similar wildlife areas. Although most ski-trails are concentrated in lower-lying areas with much snow, we found that the potential for negative energetic, avoidance and barrier effects from ski-trails increased with an increasing number of skiers. Thus, good planning in relation to the course and expected use of ski-trails is essential for optimal reindeer management. During periods with much human traffic (skiers, snow-kiters or all of these combined),

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