Environmental enrichment for zoo-housed Icelandic reindeer (Rangifer tarandus)

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Linköping University | Department of Physics, Chemistry and Biology Type of thesis, xx hp | Educational Program: Physics, Chemistry and Biology Spring or Autumn term 20xx | LITH-IFM-A-EX—21/3956--SE

Environmental enrichment for

zoo-housed Icelandic reindeer

(Rangifer tarandus)

Katarzyna Anna Kakol

Examinator, Lina Roth Tutor, Matthias Laska

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1

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Department of Physics, Chemistry and Biology Linköping University

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ISRN: LITH-IFM-A-EX--21/3956--SE

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Språk Language Svenska/Swedish Engelska/English ________________ Rapporttyp Report category Licentiatavhandling Examensarbete C-uppsats D-uppsats Övrig rapport _____________ Titel Title

Environmental enrichment for zoo-housed Icelandic reindeer (Rangifer tarandus)

Författare

Author

Katarzyna Anna Kakol

Nyckelord

Keyword

Animal welfare, behaviour, enrichment, food, olfactory, Rangifer tarandus, reindeer, tactile

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Sammanfattning

Abstract

Environmental enrichment is commonly used to improve the welfare of captive animals by offering options to increase behavioural diversity and normal behaviour patterns. The aim of this study was to assess if environmental enrichment has a positive effect on a group of four zoo-housed reindeer,

Rangifer tarandus. Three types of environmental enrichment were used: food enrichment, olfactory

enrichment, and tactile enrichment, with a spontaneous rotation to prevent habituation. Following a baseline period of ten days without enrichment, the animals’ behaviour was monitored for four months with enrichment. Food enrichment had the strongest impact on the reindeer out of the three types of enrichment presented. Neophobia may explain the lack of interest by the reindeer to olfactory and tactile enrichment, and other types of enrichment that were novel to them. Overall, the presentation of environmental enrichment made the behaviour of the captive reindeer clearly more similar to the behaviour of wild reindeer.

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Environmental enrichment is commonly used to improve the welfare of captive animals by offering options to increase behavioural diversity and normal behaviour patterns. The aim of this study was to assess if environmental enrichment has a positive effect on a group of four zoo-housed reindeer, Rangifer tarandus. Three types of environmental enrichment were used: food enrichment, olfactory enrichment, and tactile enrichment, with a spontaneous rotation to prevent habituation. Following a baseline period of ten days without enrichment, the animals’ behaviour was monitored for four months with enrichment. All behaviours shown by the reindeer during the study were categorized into locomotory behaviour, feeding behaviour, passive behaviour, social interactions, and behaviour towards enrichment. The overall level of activity of the reindeer almost doubled between the baseline period (40.8%) and the enrichment period (75.3%), with a significant increase in feeding behaviour (p < 0.001) and a significant decrease in passive behaviour (p < 0.001). Food enrichment had the strongest impact on the reindeer out of the three types of enrichment presented. Even though the reindeer showed a continuous interest towards tactile enrichment, it was low compared to the interest shown towards food enrichment. They also showed little interest in olfactory enrichment. Neophobia may explain the lack of interest by the reindeer to certain types of enrichment that were novel to them. Overall, the presentation of environmental enrichment made the behaviour of the captive reindeer clearly more similar to the behaviour of wild reindeer.

Key words: animal welfare, behaviour, enrichment, food, olfactory, Rangifer tarandus, reindeer, tactile

2 Introduction

Reindeer (Rangifer tarandus) are one of the largest species of deer (Cervidae). They are found in the northern hemisphere of the earth, with a circumpolar distribution (Þórisson, 2010), hence are well adapted to cold and harsh environmental conditions (Schmalensee et al., 2013). The main activity pattern of reindeer, and other ruminants, consists of consecutive series of foraging and rumination (Van Soest, 1994). Studies found that captive reindeer have about four to six activity peaks per twenty-four hours in winter, where the daylight lasts approximately six hours, while having around six to nine activity peaks in the summer, where the daylight is nearly continuous. These activity peaks can last from two hours and up to four hours. Free-ranging reindeer have, on average, three fewer activity peaks than captive reindeer (Eriksson et al., 1981; Maier and White, 1998). For captive reindeer, the time spent ruminating between meals

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3 in the summer is shorter than in the winter, which comprises about 16-26% of their awake time (Nilsson et al., 2006).

During winter, the activity of reindeer decreases significantly, compared to their activity in the summer. This is due to increased energy requirements for activity during the winter. The increased energy demand is mainly caused by the extra costs for walking and cratering in snow. For example, there is a 100% increase in energy that is needed for locomotion at 30-40 cm snow depth (Fancy and White, 1985a). Therefore, in the winter, the reindeer reduce their locomotor activity to save energy during harsh winter conditions (Blix, 2005).

Rutting season, which takes place from mid-September to November, also has an influence on the activity level of the reindeer. During the rut season, the male chases and protects the females from other males, which leads to increased activity of the male (Tryland and Kutz, 2018). The males often lose a significant part of both their fat and muscle reserves during the rut because they spend much of their time being active and less time eating (Barboza et al., 2004). During the rut, the females spend approximately 75% of their active time feeding, ~16% walking, and 8% standing still (Djaković et al., 2015).

When grazing, reindeer stop briefly in each location and take small bites of each plant, reducing the risk of overgrazing, damaging vegetation, and delaying growth of plants (Þráinsson et al., 2015). Their diet varies significantly between seasons. In the spring, their diet consists mainly of graminoids, moss, and shrubs (Tryland and Kutz, 2018). In the summer, they mostly consume forbs, graminoids, and shrubs (Boertje 1984; Nieminem and Heiskari, 1989; Gaare and Skogland 1975; Finstad and Kielland 2011; Bezard et al., 2015). In the late summer and autumn, the reindeer continue to consume graminoids, as well as some woody plants and herbs, and slowly increase the consumption of lichens (Boertje 1984; Gaare and Skogland 1975). When available, they also eagerly consume mushrooms, such as Boletus eduli (Nieminem and Heiskari, 1989). In the winter, the main component of their diet are lichens. They also consume moss and shrubs when available (Þráinsson et al., 2015; Joly and Cameron, 2018). Captive reindeer are also commonly fed tree leaves and arboreal lichens, which are provided by cutting down branches or whole trees (Tryland and Kutz, 2018).

It is known that reindeers’ sense of smell is sensitive and that even with harsh winds, the animal can still capture scent (Reimers and Colman, 2009). They can locate and dig for food through snow up to 1 metre thick, which is helpful in the winter (Bergerud, 1967; Helle, 1984; Þórisson, 2010). In addition, reindeer additionally use their sense of smell for chemical communication

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4 (Young, 2003). Males examine the anogenital region of females and their urine through smell and taste, and a mother smells her calf’s tail, where the largest skin gland is located. In relation to social behaviour, conspecifics are smelled at a distance that ranges from several centimetres to several metres. When two conspecifics meet, they sniff each other’s nose, tail, and body. A reindeer can even smell the footprints of another reindeer (Young, 2003).

Environmental enrichment can be described as various methods to improve animal welfare by increasing behavioural diversity and normal behaviour patterns while also reducing abnormal behaviour, increasing positive utilization of the environment, and increasing the ability to cope with challenges in a more normal way (Young, 2003; Rees, 2011). Environmental enrichment for captive animals is one of the most important tools to improve their welfare. By providing environmental enrichment, effective management practices for zoo animals can be established (Maple and Perdue, 2015). Environmental enrichment can be subdivided into different types: feeding enrichment, structural enrichment, sensory enrichment, social enrichment, cognitive enrichment, and human-animal interaction (Hoy et al., 2009; Maple and Perdue, 2015).

So far, little is known about environmental enrichment for captive reindeer. As mentioned earlier, reindeer strongly rely on olfactory stimuli to detect food and during rut season. Hence, olfactory enrichment, such as novel scents, can provide information about resources and the presence of conspecifics (Kutz and Tryland, 2018). In addition, tactile enrichments, such as logs, brooms, and dead trees, may be attractive because it helps the reindeer to get rid of their winter fur and their velvet (Kutz and Tryland, 2018).

Therefore, the aim of this study was to present a group of zoo-housed reindeer with three different types of environmental enrichment: food, olfactory, and tactile enrichment, to assess their response towards each type of enrichment and to assess if it has a positive effect on their behaviour.

3 Methods

3.1 Animals and the enclosure

The present study took place at Reykjavík Park & Zoo in Iceland and was conducted using four reindeer (Rangifer tarandus), one male (Tindur, 8 years old) and three females (Regína, 12 years old, Gullbrá, 8 years old, and Hallveig, 5 years old).

The animals were housed in a ~5.900 m2_{enclosure, which was divided into an outdoor}

enclosure (~5.800 m2_{) and an indoor enclosure (~100 m}2_{) (figure 1). The outdoor enclosure was}

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5 creek, which only fills up when it rains, and a trough filled with water. There were wired fences around the enclosure, alongside big wooden logs to keep the animals from the wired fence. Inside the outdoor enclosure was a wooden fence, which was used to separate the animals when needed (figure 2). The indoor enclosure had concrete walls and floors, there was a feeding area and a sink with flowing water. The feeding area was partly blocked by a steel fence to keep the animals from getting out (figure 3).

Figure 1: Satellite picture, taken 27.07.2020, of the reindeers’ enclosure. The blue line shows

the limits of the outdoor enclosure while the red line marks the indoor enclosure.

Figure 2: The reindeers’ outdoor enclosure. A, the wired fence, alongside the big wooden logs,

the trees that surround the enclosure, the small grass hill and some of the big rocks. B, a small part of the inside enclosure and the wooden fence.

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Figure 3: The reindeers’ indoor enclosure. A, part of the exterior of the inside enclosure and

Regína drinking from a water bucket. B, Tindur drinking from the sink that is in the inside enclosure. C, Gullbrá and Tindur eating hay from the feeding station that is partly blocked by a steel fence.

The first reindeer, Regína, came to the zoo 12 years ago and the enclosure has not been modified in any way since then, meaning the animals have not been exposed to environmental enrichment since arriving at the zoo. The animals have also not been trained specifically; however, the keepers work with them in close contact from time to time.

The animals were fed twice a day, approximately 2 kilogram of hay, 400 grams of reindeer lichens (Cladonia rangiferina) and 1 kilogram of reindeer pellets (Hreindýrakögglar, Fóðurblandan hf., Iceland) for the four animals combined. In addition, the reindeer were provided with water ad libitum.

3.2 Experimental procedure

Before presenting any type of enrichment, a baseline period of ten days took place. A total of ten behaviours were recorded and divided into four baseline categories: feeding, locomotion, passive, and social interactions (table 1). The frequency of these behaviours was recorded throughout the baseline period. Scan sampling method was used for all animals with two-minute intervals. Behaviours that took place on the two-minute interval were recorded.

In addition to the four baseline categories, a fifth behaviour category, enrichment interaction, containing five new behaviours, was recorded during the four-month enrichment period (table 1). The frequency and duration of these behaviours were recorded throughout the enrichment period. All occurrences of these behaviours were recorded, alongside the duration of each behaviour.

The data collection took place between June 2020 and October 2020, five days a week, six hours a day, which resulted in approximately 400 hours of data collection. The three types of

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7 enrichment used in present study, were rotated daily to keep spontaneity, and prevent habituation.

Table 1: Ethogram of reindeer behaviour included in this study.

Behaviour Description

Locomotion Auto grooming

Interaction with keepers Moving Feeding Drinking Feeding outside Feeding inside Passive Resting Standing still Social interactions Social interaction

Social interaction while moving

Mouth, hoof, or antlers repeatedly in contact with other parts of its body.

Walking towards keeper or sniffing keeper. Walking or running towards any direction.

Mouth in contact with water source.

Mouth in contact with grass and/or plants found in the meadow in outdoor enclosure. Reindeer either standing or walking.

Mouth in contact with familiar food in the indoor enclosure

Laying down, either on their side or legs bent underneath body, in indoor and outdoor enclosure.

Standing still, with no additional movement, in indoor and outdoor enclosure.

Sniffing, scratching, biting, rubbing against each other while standing still.

Sniffing, scratching, biting, rubbing against each other while standing still, and/or chasing each other.

Enrichment interaction Eating Licking Rubbing Scratching/digging Sniffing

Mouth in contact with any part of the enrichment. Tongue in contact with any part of the enrichment. Rubbing the head or body against the enrichment. Hoof repeatedly in contact with the enrichment. Holding its nose close to the enrichment.

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8 3.2.1 Food enrichment

Twenty different types of novel food were presented to the reindeer as food enrichment (table 2), at least eight times, for six hours per presentation, throughout the enrichment period, depending on how often the reindeer interacted with the novel food. Each type of novel food was presented with at least two days between presentations of the same type of stimulus. To assess which novel foods were attractive for the reindeer, they were all first presented at their familiar food station to maximize the probability that the reindeer would pay attention to them when presented. Afterward, the novel foods were presented in containers that were familiar to the reindeer, e.g. banana boxes, hay nets, and treat balls (figure 4).

Figure 4: A, Tindur consuming familiar food from a banana box. B, Gullbrá and Tindur eating

tree leaves from a treat ball. C, all four reindeer consuming familiar food from hay nets.

In addition to presenting novel food, their familiar food was spread throughout the outdoor enclosure, instead of presenting it at their familiar feeding station, as enrichment. The first step was to present the familiar food in several piles around the outdoor enclosure, switching the position of the piles daily to induce activity in the animals. To this end, banana boxes and hay nets were placed throughout the outdoor and indoor enclosure filled with the familiar foods.

Table 2: List of novel food items and branches presented in the study.

Novel food Branches

Apples (Malus domestica) Banana (Musa acuminata)

Berry mix (Vaccinium myrtillus, Fragaria x

ananassa, Rubus idaeus)

Black currant (Ribes nigrum) Cheerios cereal

Fresh basil (Ocimum basilicum)

Birch (Betula pubescens)

Cottonwood (Populus trichocarpa) Rowan (Sorbus aucuparia)

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9 Fresh coriander (Coriandrum sativum)

Fresh rosemary (Salvia Rosmarinus) Lettuce (Lactuca sativa)

Organic, sugar free peanut butter Raisins (dried fruits of Vitis vinifera) Red currant (Ribes rubrum)

Store bought blueberries (Vaccinium

myrtillus)

Store bought mushrooms (Basidiomycota) Wild blueberries (Vaccinium myrtillus) Wild mushroom (Leccinum scabrum)

3.2.2 Olfactory enrichment

Five different essential oils were used as olfactory enrichment (table 3). The essential oils were applied on wooden logs (40 x 4 x 4 cm) and placed in the animals’ enclosure, either on the ground or hung up on the fence. Each essential oil was presented eight times, for six hours per presentation, alongside a wooden log bearing a near odourless organic solvent (Diethyl phthalate) that was used as a control stimulus. There was approximately 1-2 meter distance between the odorized wooden log and the non-odorized wooden log. This solvent was also used for diluting the essential oils (1:10 ratio) (figure 5).

Figure 5: Odourised and non-odourised wooden logs strapped to wooden logs found in outdoor

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10 In addition to the essential oils, five different spices were also used as olfactory enrichment and were presented eight times in total (table 3). The spices were mixed with the animals’ food (e.g. hay, leaves) as well as presented separately as a trail on the ground. Each spice was presented eight times in total. Alongside a scented food pile, there was a non-scented food pile to assess if the animals were attracted or repelled by the odour stimuli. There was approximately 1-2 meter distance between the scented food pile and non-scented food pile. I also recorded which food pile was consumed first and whether the reindeer consumed more from one or the other option.

Table 3: List of essential oils and spices presented in this study.

Essential oils Spices

Jasmine (Jasminum officinale) Lavender (Lavandula spica) Lemon (Citrus limon)

Peppermint (Mentha × piperita) Tea tree (Melaleuca alternifolia)

Black pepper (Piper nigrum) Chili powder (Capsicum annuum) Cinnamon (Cinnamomum verum) Garlic powder (Allium sativum) Oregano (Origanum vulgare)

3.2.3 Tactile enrichment

Four different novel objects were used as tactile enrichment; old branches, two types of broom brushes, pine trees and a yoga ball (figure 6). The reasons for selecting these novel objects were that they were easily accessible, and they have been used on other animals at the zoo, such as the goats. Studies on cows also showed that broom bristles are attractive to the animal (Mandel et al., 2016), therefore two types of broom bristles were chosen for the present study. The novel objects were placed all around the enclosure, either on the ground or attached to stationary objects, e.g. a fence. The novel objects were presented in rotation, with the exception of the pine trees, which were presented nearly every day when they were acquired. The old branches were presented 55 times, pine trees were presented 45 times, the two types of brooms were presented 35 times each, and the yoga ball was presented 10 times, for six hours per presentation.

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Figure 6: Gullbrá rubbing her head against a soft bristled broom that was mounted on a

wooden fence (A), and Tindur rubbing against two types of tactile enrichments, old branches (B) and a pine tree (C).

3.3 Data analysis

The Chi-square test was used to assess possible differences in the activity distribution between the baseline period and the enrichment period, as well as between months during the enrichment period. The five behaviour categories were merged into two new categories for this test: activity and passivity. The activity category comprises of following behaviours: locomotion, feeding, social interaction and enrichment, while the passivity category included only the passive behaviours. Additionally, the Chi-square test was used to assess possible differences in the activity distribution between the five different behaviour categories mentioned above.

The Friedman test, followed by a paired Wilcoxon signed-rank test, was used to assess possible differences in the duration and frequencies of behaviours for different types of enrichment. A Wilcoxon test was used to assess possible differences between the two periods.

The Wilcoxon test was also used to assess possible differences in odourised objects and non-odourised objects, the essential oils, and spices.

The data to calculate the average duration and frequency of interactions per day were normalized. Each data point was divided by the number of presentations, which varied between enrichments.

All statistical analyses were performed using R Studio, version 1.4.1106.

4 Results

4.1 Baseline period vs. enrichment period

For this analysis, the four behavioural categories were merged into two new categories called “activity” and “passivity”. The “activity” category comprises of feeding behaviours,

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12 locomotory behaviours, and social interactions. The “passivity” category contains passive behaviours.

When considering only the behavioural categories “activity” and “passivity”, there was a significant difference between the baseline period and the enrichment period (X2(1) = 24.507, p

< 0.001). The enrichment period yielded a significantly higher proportion of the “activity” behavioural category compared to the baseline period (p < 0.05). In addition, the enrichment period also yielded a significantly lower proportion of the “passivity” behavioural category compared to the baseline period (p < 0.05) (figure 7).

Figure 7: Average proportion of activity (green) and passivity (orange) of the reindeer during

the baseline period and the enrichment period. * = p ≤ 0.05

When considering the four behaviour categories “feeding”, “locomotion”, “passive”, and “social interaction”, two out of four differed significantly between the baseline period and the enrichment period. There was a significant increase in feeding behaviours in the enrichment period compared to the baseline period (p < 0.001). Moreover, there was a significant decrease in passive behaviours in the enrichment period compared to the baseline period (p < 0.001). There was an increase in locomotory behaviour, and in social interactions during the enrichment period, however the difference between the periods was not significant (locomotion: p = 0.349, social interactions: p = 0.338) (figure 8).

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Figure 8: Average proportion of the different behavioural categories performed by the reindeer

during the baseline period and the enrichment period. *** = p ≤ 0.001

4.2 Comparison of the three types of enrichment presented

A significant difference was found between the mean time the reindeer spent interacting with a given type of enrichment, per day (X2

(2) = 128, p < 0.001). The reindeer spent significantly

more time interacting with food enrichment, compared to olfactory enrichment (p < 0.001), and tactile enrichment (p < 0.001). In addition, the reindeer spent significantly more time interacting with tactile enrichment than olfactory enrichment (p < 0.001) (figure 9a).

Furthermore, a significant difference was found between the mean frequency of interactions with given type of enrichment per day (X2 (2) = 91.5, p < 0.001). The reindeer interacted

significantly more often with food enrichment, compared to olfactory enrichment (p < 0.001), and tactile enrichment (p < 0.001), respectively. Also, the reindeer interacted significantly more often with tactile enrichment than with olfactory enrichment (p < 0.001) (figure 9b).

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Figure 9: A: Comparison of the mean time the reindeer spent interacting with each type of

enrichment, per day. B: Comparison of the mean number of interactions with each type of enrichment, per day. See table 1 (Enrichment interactions) for the list of behaviours that were recorded. *** = p < 0.001

4.3 Food enrichment

For this analysis, 12 out of 16 different novel foods were grouped into one category called “Novel food”. Four novel foods were not included due to lack of interaction by the reindeer. Additionally, four different types of leaf species were grouped into one category called “Tree leaves”.

4.3.1 Different types of food enrichment

There was a significant difference between the mean time per day the reindeer spent interacting with each of the food enrichments (X2(3) = 12.12, p < 0.01). The reindeer spent significantly

more time interacting with tree leaves than with any other food enrichment presented (bark: p < 0.001, novel food: p < 0.001, pine tree: p < 0.01). Furthermore, the reindeer spent significantly more time interacting with bark than with novel food (p < 0.001) (figure 10a).

There was a significant difference between the mean frequency of interactions with each of the food enrichments per day (X2(3) = 8.28, p < 0.05). The reindeer interacted significantly more

often with tree leaves than with the other food enrichment presented (bark: p < 0.001, novel food: p < 0.001, pine tree: p < 0.01). Additionally, the reindeer interacted significantly more often with bark than with novel food (p < 0.01) (figure 10b).

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Figure 10: A: Comparison of the mean time the reindeer spent interacting with each type of

food enrichment presented, per day. B: Comparison of the mean number of interactions with each type of food enrichment presented, per day. See table 1 (Enrichment interactions) for the list of behaviours that were tracked. * = p ≤ 0.05 ** = p ≤ 0.01 *** = p ≤ 0.001

There was a significant difference between the 12 different novel foods that were grouped into the “Novel food” category, with regard to the mean time spent interacting with each novel food when presented (X2(11) = 38.665, p < 0.001), and the mean frequency of interactions with the

novel food when presented (X2(11) = 41.569, p < 0.001). However, a pairwise comparison test

showed that there was no significant difference between the novel foods, (p = 1).

4.3.2 Different ways of presenting food enrichment

The familiar food and novel food were presented in three ways: in banana boxes, in hay nets, and in treat balls.

There was a significant difference between the mean time per day the reindeer spent interacting with food when presented in different ways (X2(2) = 28.778, p < 0.001). The reindeer spent

significantly more time interacting with food when presented in banana boxes than when presented in hay nets (p < 0.001) and in treat balls (p < 0.001). In addition, the reindeer spent significantly more time interacting with food when presented in hay nets than in treat balls (p < 0.001) (figure 11a).

Furthermore, there was a significant difference between the mean frequency of interactions with food when presented in different ways (X2

(2) = 26.778, p < 0.001). The reindeer interacted

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16 hay nets (p < 0.001) and in treat balls (p < 0.001). The reindeer also interacted significantly more often with food when presented in hay nets than in treat balls (p < 0.001) (figure 11b).

Figure 11: A: Comparison of the mean time the reindeer spent interacting with food when

presented in three different ways, per day. B: Comparison of the mean number of interactions with food when presented in three different ways. See table 1 (Enrichment interactions) for the list of behaviours that were tracked. *** = p ≤ 0.001

4.4 Olfactory enrichment

There was no significant difference between odourised objects and non-odourised object, with regard to the mean time spent interacting with the objects (W = 2916, p = 0.086), and the mean frequency of interactions (W = 3488.5 , p = 0.081).

There was no significant difference between the odourised wooden logs and non-odourised wooden logs, with regard to the mean time spent interacting with the enrichment when presented (W = 880, p = 0.183) the mean frequency of interactions (W = 890.5, p = 0.132). There was also no significant difference between the scented food piles and trails and non-scented food piles and trails, with regard to the mean time spent interacting with the enrichment when presented (W = 856, p = 0.330) and the mean frequency of interactions (W = 863.5, p = 0.269).

Furthermore, there was no significant difference when comparing the essential oils to the spices, with regard to the mean time spent interacting with the odourised objects (W = 60.5, p = 0.396), and the mean frequency of interactions (W = 62.5, p = 0.305).

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17 There was no significant difference when comparing the mean time spent interacting with the different essential oils presented (X2(4) = 9.044, p = 0.061) and the mean frequency of

interactions (X2(4) = 8.381, p = 0.079). Additionally, there was no significant difference when

comparing the mean time spent interacting with the different spices when presented (X2(4) = 6,

p = 0.199) and the mean frequency of interactions (X2(4) = 5.026, p = 0.285).

4.5 Tactile enrichment

There was no significant difference between the different tactile enrichments presented, with regard to the mean time spent interacting with each tactile enrichment (X2(4) = 9.111, p = 0.059),

nor the mean frequency of interactions (X2

(4) = 7.286, p = 0.122).

4.6 Comparison between the months during the enrichment period

There was a significant difference between the months of the enrichment period with regard to the average proportion of activity and passivity of the reindeer (X2

(4) = 29.092, p < 0.001).

When comparing the average proportion of activity and passivity of the reindeer in each month during the enrichment period, the reindeer were significantly less active in June compared to the four other months (p < 0.05). Moreover, the reindeer were significantly less active in July compared to August (p < 0.05), and September (p < 0.05) (figure 12).

Figure 12: Average proportion of activity (green) and passivity (orange) of the reindeer during

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18 When comparing the mean time spent interacting per day with the three different enrichments presented in this study, in each month, a significant difference was found in every single month (June: X2(2) = 7.923, p < 0.05, July: X2(2) = 10.85, p < 0.01, August: X2(2) = 37.507, p < 0.001,

September: X2(2) = 31.524, p < 0.001, October: X2(2) = 14, p < 0.001) (figure 13).

Out of the three types of enrichments, the reindeer spent significantly more time interacting with food enrichment than with the other two types of enrichment in every month during the enrichment period, with the exception of June. The mean time the reindeer spent interacting with tactile enrichment was significantly higher than with olfactory enrichment in August, September, and October (table 4).

Table 4: P-values from a pairwise comparison of the mean time per day the reindeer spent

interacting with the three different enrichments presented in this study (Food enrichment: F. E, Olfactory enrichment: O. E, Tactile enrichment: T. E), in each month. Red numbers indicate that there was not a significant difference between the enrichments.

June July F. E O. E F. E O. E O. E 0.071 - O. E 0.013 - T. E 0.247 0.247 T. E 0.023 0.194 August September F. E O. E F. E O. E O. E < 0.001 - O. E < 0.001 - T. E < 0.001 < 0.001 T. E < 0.001 < 0.001 October F. E O. E O. E < 0.01 - T. E < 0.01 < 0.01

There was a significant difference when comparing the mean time that the reindeer spent interacting with food enrichment per day, in each month (X2(4) = 26.629, p < 0.001). The

reindeer spent significantly more time interacting with food enrichment in October than any other month during the enrichment period (June: p < 0.001, July: p < 0.01, August: p < 0.001, September: p < 0.001). Additionally, September yielded a significantly higher mean time than June (p < 0.001), and July (p < 0.001). August also yielded a significantly higher mean time than June (p < 0.01), and July (p < 0.001) (figure 13).

There was a significant difference when comparing the mean time that the reindeer spent interacting with olfactory enrichment per day, in each month (X2(4) = 11.59 p < 0.05). July

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19 when compared to August (p < 0.05). However, June yielded a significantly higher mean time than August (p < 0.01) and September (p < 0.05) (figure 13).

There was a significant difference when comparing the mean time that the reindeer spent interacting with tactile enrichment per day, in each month (X2(4) = 19.052 p < 0.001). The

reindeer spent significantly more time interacting with tactile enrichment in October than any other month during the enrichment period (June: p < 0.05, July: p < 0.01, August: p < 0.01, September: p < 0.05). Furthermore, September yielded a higher mean time than July (p < 0.01), and August (0.01) (figure 13).

Figure 13: Comparison of the mean time the reindeer spent interacting with each type of

enrichment presented per day, in every month during the enrichment period. See table 1 (Enrichment interactions) for the list of behaviours that were tracked.

When comparing the mean frequency of interactions per day with the three different enrichments presented in this study, in each month, a significant difference was found in every month, with the exception of June (June: X2(2) = 5.04, p = 0.081, July: X2(2) = 9.526, p < 0.01,

August: X2(2) = 37.507, p < 0.001, September: X2(2) = 31.524, p < 0.001, October: X2(2) = 14,

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20 Out of the three types of enrichment, the reindeer interacted significantly more often with food enrichment than with the other two types of enrichment in August, September, and October. In addition, tactile enrichment yielded a significantly higher mean frequency of interactions than olfactory enrichment in August, September, and October (table 5).

Table 5: P-values from a pairwise comparison of the mean frequency of interactions per day

with the three different enrichments presented in this study (Food enrichment: F. E, Olfactory enrichment: O. E, Tactile enrichment: T. E), in each month. Red numbers indicate that there was not a significant difference between the enrichments.

June July F. E O. E F. E O. E O. E 0.06 - O. E 0.043 - T. E 0.25 0.36 T. E 0.166 0.324 August September F. E O. E F. E O. E O. E < 0.001 - O. E < 0.001 - T. E < 0.001 < 0.001 T. E < 0.001 < 0.001 October F. E O. E O. E < 0.01 - T. E < 0.01 < 0.01

There was a significant difference when comparing the mean frequency of interactions with food enrichment per day, in each month (X2

(4) = 11.543, p < 0.05). The reindeer interacted most

often with food enrichment in October, however there was only a significant difference when compared to July (p < 0.01), and August (0.01) (figure 14).

There was a significant difference when comparing the mean frequency of interactions with olfactory enrichment per day, in each month (X2(4) = 11.897, p < 0.05). The reindeer interacted

most often with olfactory enrichment in June, but a significant difference was only found when compared to August (p < 0.05), and September (p < 0.05). Additionally, July yielded a significantly higher mean frequency of interactions in July than in August (p < 0.05) (figure 14).

There was a significant difference when comparing the mean frequency of interactions with tactile enrichment per day, in each month (X2(4) = 14.844, p < 0.01). The reindeer interacted

most often with tactile enrichment in October, and a significant difference was found when compared to August (p < 0.01), and September (p < 0.05) (figure 14).

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21

Figure 14: Comparison of the mean number of interactions with each type of food enrichment

presented, per day. See table 1 (Enrichment interactions) for the list of behaviours that were tracked.

4.7 Comparison between individual reindeer

When looking at the average proportion of activity between the four reindeer during the baseline period, Hallveig yielded the highest proportion of activity (43.74%), while Gullbrá yielded the lowest proportion of activity (39.06%). During the enrichment period, Hallveig also yielded the highest proportion of activity (76.93%), while Tindur yielded the lowest proportion of activity (68.92%). However, there was no significant difference between the individual reindeer during the baseline period (X2(3) = 0.588, p = 0.899), nor the enrichment period (X2(3) = 1.636, p =

0.651).

When comparing the five behaviour categories “enrichment”, “feeding”, “locomotion”, “passive”, and “social interaction”, Tindur yielded the highest average proportion of activity in all behavioural categories, with the exception of “feeding” (Enrichment: 20.22%, locomotion: 7.91%, passive: 31.08%, social interaction: 4.40%). In the “feeding” category, Hallveig yielded the highest average proportion of activity (50.33%). Gullbrá yielded the lowest average proportion of activity in the “enrichment” category (16.35%), and in the “locomotion” category (4.65%). In addition, Hallveig yielded the lowest average proportion of activity in the “passive” category (23.07%), while Regina yielded the lowest average proportion of activity in the “social

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22 interaction” category (0.06%). Yet, there was no significant difference between the reindeers’ average proportion of activity in the behavioural categories (Enrichment: X2(3) = 2.26, p =

0.516, feeding: X2(3) = 3.96, p = 0.266, locomotion: X2(3) = 1.08, p = 0.782, passive: X2(3) =

7.32, p = 0.062, social interaction: X2(3) = 5.75, p = 0.124).

With regard to the mean time spent with the three types of enrichment presented, Regina yielded the highest mean time spent interacting food enrichment (63.21 min/per day), while Gullbrá yielded the lowest mean time (53.29 min/per day). With regard to olfactory enrichment, Tindur yielded the highest mean time spent interacting given enrichment (0.2 min/per day), while both Hallveig and Regina yielded the lowest mean time (0.01 min/per day). With regard to tactile enrichment, Tindur yielded the highest mean time spent interacting given enrichment (0.28 min/per day), while Gullbrá yielded the lowest mean time (1.9 min/per day). However, there was no significant difference between the reindeers’ mean time spent interacting with a given type of enrichment (Food enrichment: X2(3) = 2.28, p = 0.516, olfactory enrichment: X2(3) =

0.84, p = 0.839, tactile enrichment: X2

(3) = 2.52, p = 0.472).

With regard to the mean frequency of interactions with the three types of enrichment presented, Hallveig yielded the highest mean frequency of interactions with food enrichment (6.42 interactions/per day), while Gullbrá yielded the lowest mean (5.63 interactions/per da0y). With regard to olfactory enrichment, both Tindur and Gullbrá yielded the highest mean frequency of interactions (0.28 interactions/per day), while Regina yielded the lowest mean (0.10 interactions/per day). With regard to tactile enrichment, Tindur yielded the highest mean frequency of interactions (1.25 interactions/per day), while Regina yielded the lowest mean (0.70 interactions/per day). Still, there was no significant difference between the reindeers’ mean frequency of interactions with a given type of enrichment (Food enrichment: X2(3) =

0.551, p = 0.908, olfactory enrichment: X2(3) = 1.154, p = 0.764, tactile enrichment: X2(3) =

4.469, p = 0.215).

5 Discussion

The aim of this study was to assess if presenting zoo-housed reindeer with three types of environmental enrichment would have a positive effect on their behaviour, and to assess their responses towards the enrichments. Indeed, my results show that environmental enrichment made the group of zoo-housed reindeer markedly more active throughout the day and increased their feeding behaviour, thus improving their welfare and having an overall positive effect on the reindeer. Food enrichment seems to be the most successful in doing so, in the present study.

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23 5.1 Baseline period vs. enrichment period

During the baseline period, the reindeer spent more than half of their time being inactive. However, during the enrichment period, the reindeer became significantly more active than during the baseline period. The overall level of activity almost doubled (40.76% during baseline period vs. 75.31% during enrichment period). An earlier study on wild female reindeer showed that they spent on average 75.2% of their day active (Reimers et al., 2014), which is consistent with the activity level that the captive reindeer in present study showed during the enrichment period. The inactivity level of the captive reindeer during the enrichment period (24.69%) is similar to the 33% of inactivity that Colman et al. (2001) reported on wild reindeer during the day.

When comparing the behaviour categories between the baseline period and the enrichment period, there was a clear difference. The feeding behaviours (not including the feeding behaviours towards the enrichments presented) significantly increased during the enrichment period (36.48% during baseline period vs. 46.47% during enrichment period) and is close to the percentage of time spent feeding by wild reindeer (Skogland, 1984; Colman et al., 2001). There was also an increase in active behaviours and in social interactions, however it was not statistically significant. These changes in the reindeers’ behaviour show that presenting enrichment to captive reindeer does indeed have a positive effect on their behaviour and made their behaviour more similar to the activity pattern of wild reindeer, which consists of consecutive series of foraging and ruminating (Van Soest, 1994).

As mentioned above, the reindeer spent more time being active, feeding, interacting with each other, and interacting with enrichment. However, the biggest change the reindeer showed was with regard to their passive behaviours. During the baseline period, the reindeer spent a lot of their time standing around doing nothing and less time lying down and ruminating. When the reindeer were presented with enrichment, their feeding behaviour significantly increased, which resulted in an increase in rumination and a decrease in passive behaviours such as standing around doing nothing. Nilsson et al. (2006) found that their semi-domesticated reindeer showed a similar pattern in rumination and lying down. They reported that their reindeer spent more time ruminating throughout the day and barely any time standing around doing nothing.

5.2 Comparison of the three types of enrichment presented

Out of the three types of enrichment that were presented, the reindeer interacted the most with food enrichment, both with regard to the mean time spent interacting with the enrichment per day, and the mean frequency of interactions per day. On average, they spent 345.64 minutes

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24 per day with food enrichment, while only spending about 15.06 minutes with tactile enrichment, and 0.25 minutes with olfactory enrichment. The reindeer interacted on average 28.63 times per day with food enrichment, about 4.09 times per day with tactile enrichment, and 0.86 times per day with olfactory enrichment.

Previous studies have shown that reindeer spend a lot of their time grazing and feeding throughout the day (Skogland, 1984; Van Soest, 1994; Colman et al., 2001; Nilsson et al., 2006) which is in line with my results. Every time food enrichment was presented, all four reindeer were eager to interact with the given enrichment and every so often the male and the oldest female would chase the other two reindeer away from the food enrichment so that they could have most of it for themselves.

What did come as a surprise is that olfactory enrichment was the least interesting enrichment for the reindeer. Reindeer have a good sense of smell which they use to locate food and for chemical communication (Bergerud, 1967; Helle, 1984; Þórisson, 2010), therefore it was expected that they would spend more time interacting with olfactory enrichment than was actually observed. This could be due to the selection of odours, or perhaps these reindeer are more visually oriented. Possibly introducing the reindeer to different odours than used in present study, or present the odours in a different manner would yield different results.

It was also expected that the reindeer would spend more time with tactile enrichment because they still had their winter fur in June and were most likely eager to get rid of it due to the rise in temperature. They were somewhat sceptic of the tactile enrichment when first presented and only one of the reindeer showed any interest in the beginning. However, that changed later during the enrichment period and the reindeer then spent more time with the tactile enrichment.

5.3 Food enrichment

5.3.1 Different types of food enrichment

Four types of food enrichment were presented in this study: bark, novel food, pine tree and tree leaves. Out of the four types of food enrichment, the reindeer interacted most often with tree leaves, both with regard to the mean time spent with given food enrichment, and the mean frequency of interactions, while interacting the least with pine trees.

Captive reindeer are commonly fed tree leaves (Kutz and Tryland, 2018); therefore, it did not come as a surprise that the reindeer found tree leaves most attractive out of the food enrichments presented. Reindeer are known to graze on evergreens (Kutz and Tryland, 2018), such as pine trees, therefore it was unexpected that the reindeer showed so little interest in consuming pine

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25 trees when presented. This could be due to the fact that they do not have access to pine trees, but they have been seen to climb the fence and jump to get to trees bearing leaves, and during the autumn they do have access to tree leaves that fall from the trees surrounding their enclosure.

Surprisingly, the reindeer showed very little interest for novel food. Both wild and captive reindeer eagerly consume mushrooms when available (Nieminem and Heiskari, 1989), as well as different types of berries and herbs (Kutz and Tryland, 2018). Therefore, it was unexpected that overall, the reindeer showed almost no interest in any of the novel food types. However, the reindeer showed the most interest in the different types of berries out of all the novel food presented. Neophobia may be a possible explanation for the general lack of interactions that the reindeer displayed towards novel food.

5.3.2 Different ways of presenting food enrichment

The food enrichment was presented in three ways: in banana boxes, in hay nets, and in treat balls. The reindeer interacted most often with food enrichment when presented in banana boxes, both with regard to the mean time spent with a given food enrichment, and the mean frequency of interactions, while interacting the least with food enrichment when presented in treat balls.

The reindeer were used to getting their food in an open space without having to put any effort in accessing it, therefore it was expected that the reindeer preferred when their food was presented in banana boxes, over the other two ways of presenting. The banana boxes were easily accessible for the reindeer, making it easy for them to see what they contained, and they did not have to work as much for accessing the food.

The food in the hay nets was not as easily accessible as the food in the banana boxes, the reindeer had to work for the food a bit more than when presented in the banana boxes, which may be a reason why they preferred the banana boxes over the hay nets.

The reindeer had to work the hardest for the food that was presented in the treat balls, and that may explain why they showed the least amount of interest in that. The food was not easily accessible unless the ball was moving, thus the reindeer had to move the treat ball to get the food out.

5.4 Olfactory enrichment

Overall, the reindeer investigated the olfactory enrichments only cursorily but quickly and did not investigate them any further throughout the day, which was not expected due to them having a sensitive sense of smell which they use to track and locate food, as well as for chemical communication (Bergerud, 1967; Helle, 1984; Young, 2003; Þórisson, 2010).

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26 The general lack of interactions displayed by the reindeer towards olfactory enrichment suggests that they only needed a few seconds to decide that the enrichment is not interesting. A study done on feedlot cattle found similar results with regard to olfactory enrichment (Wilson et al., 2002).

5.5 Tactile enrichment

Both captive and wild reindeer utilize dead trees and logs to get rid of their winter fur and their velvet (Kutz and Tryland, 2018) and other ungulate species have shown interest towards different types of tactile enrichment (Wilson et al., 2002; Mehrkam and Dorey, 2015), therefore it was expected that tactile enrichment would be favoured by the reindeer, however that was not the case in this study.

5.6 Comparison between the months during the enrichment period

The average activity and inactivity of the reindeer differed markedly between some of the months. The reindeer were the least active in June, which was expected since the enrichment period started in June and the reindeer were a bit sceptic at first of everything that was presented to them. From July on, they became more active and this trend continued by the month. This shows that with time the reindeer became perhaps less afraid of exploring the enrichments, which may be an indicator of neophobia (Iglesias et al., 2018).

The reindeer were most active in September, which can be explained by the start of rutting season. During the rutting season, the reindeer became more active due to the fact that the male was running after the females and herding them together. This is consistent with what happens in the wild and therefore this behaviour was expected (Tryland and Kutz, 2018).

As stated earlier, out of the three enrichments that were presented in this study, food enrichment was the most attractive for these reindeer. This was true for all months during the enrichment period, except for in June. As the enrichment period started in June, it was expected that that the reindeer would interact the least with the enrichment during that month.

5.7 Comparison between individual reindeer

All four reindeer in this study followed a similar pattern. Their activity patterns, throughout the study, were consistent and did not differ remarkably. Individual red deer in small herds have been shown to synchronise their activity with those nearest them(Rands et al., 2014), and since there were only four reindeer in this herd, this may explain the similar activity patterns of the reindeer. Stoye et al. (2012) did a study on small herds of cattle, and similar patterns were found there as well.

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27 The differences that were found among the reindeer, with regard to average proportion of activity in the five behavioural categories, could be explained by the social rank among the herd. Multiple studies have shown that there is a social hierarchy in deer herds (Appleby, 1980; Veiberg et al., 2004). As Tindur (the male reindeer) yielded the highest average proportion of activity in four out of five categories, and also yielded the highest means with regard to the time spent interacting with a given enrichment and the frequency of interactions, for two out of the three enrichments presented in this study, this suggests that he is the highest-ranking reindeer in the herd.

Furthermore, as mentioned earlier, the male and the oldest female repeatedly chased the other two reindeer away from the food enrichment so that they could have most of it for themselves. Regina (the oldest female) showed a tendency to be hostile towards Hallveig (the youngest one), which could mean that Regina is the second highest-ranking reindeer, while Hallveig is the lowest-ranking reindeer. Thouless and Guiness (1986) showed that age could possibly be more important than weight when it comes to social rank, especially where there are stable dominance relationships, which is in line with the assumptions made about the oldest and youngest female in present study.

5.8 Efficiency of enrichment in other ungulate species

Providing enrichment for captive ungulates has been found to be quite challenging and thus focused so far primarily on promoting feeding behaviours (Young, 2003; Rose et al., 2007).

Rose et al. (2007) assessed the effectiveness of different types of enrichment for the Eastern tufted deer (Elaphodus cephalophus) and the Bactrian camel (Camelus bactrianus), which included branches, leaves and logs from various types of trees. These different types of enrichment were expected to promote foraging behaviour, increase sensory stimulation between feeding times, encourage scent marking and increase diversity in their housing areas. Their results showed that all forms of enrichment presented had a beneficial effect on the activity levels of both species, especially on the eastern tufted deer which spent more time foraging, feeding, and inspecting their enclosure. These findings are in line with the results in present study.

Rose et al. (2007) also reported that the use of browse was the enrichment that the ungulates showed longest interest in. They report that browse should be more than just a form of enrichment. It can also be a useful tool to provide stimuli between feeding bouts. The addition

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28 of log piles increased the camel’s interest in their enclosure, and they performed a more natural behaviour pattern than before.

An enrichment manual for zoo animals written by Goswami et al. (2016) included a study done on the Sangai (Rucervus eldii eldii). They found that tree branches increased the activity of the animals, such as moving around and foraging behaviour, as well as prolonging the feeding time. However, novel food, such as carrots, French beans, and gooseberries, were not favoured by the deer. Both of these findings are in agreement with the findings in present study.

5.9 Future studies on captive reindeer

The results of this study clearly show that the reindeer favoured food enrichment over the other two types, olfactory enrichment, and tactile enrichment, throughout the study. Therefore, it can be concluded that food enrichment is without a doubt an enrichment that should be used with captive reindeer, as well as other ungulates, because it had a positive effect on their behaviour.

Future studies on captive reindeer should perhaps explore different types of novel food as well as those included in this study. Even though tactile enrichment and olfactory enrichment did not have as much impact on the reindeers’ behaviour as food enrichment did, this does not mean that it should not be studied more on other captive reindeer. Different odours, as well as different methods of presentation, should be considered for future studies.

As mentioned earlier, the reindeer used in this study have shown signs of being neophobic, which may have affected the results. Furthermore, the present study was done on one population, with only four reindeer, which could also be a limiting factor. Thus, other captive reindeer that are used to novel objects, may react differently to the enrichments.

What should also be explored are other types of enrichment, such as auditory enrichment (Kelling et al. 2012). The hearing capacity of reindeer ranges from 70 Hz to 38 kHz at a sound pressure of 60 dB (Reimers and Colman, 2009), therefore it would be interesting to assess if auditory enrichment has any effect on the reindeers’ behaviour.

6 Societal & ethical considerations

All experiments carried out in present study are in compliance with the European Directive on

the Protection of Animals Used for Scientific Purposes (EU Directive 2010/63/EU) and with

current Icelandic and Swedish animal welfare laws. Providing environmental enrichment to zoo-housed animals is required by animal welfare laws. Therefore, no extra ethical permit was required for the present study. Providing the reindeer with environmental enrichment offers

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29 them an opportunity to increase their natural behaviour. It can also provide them with challenges that are similar to those they would face in the wild, such as foraging for food. The participation of the reindeer throughout the study was on a strictly voluntary basis. The animals were not forced in any way to interact with the enrichments when presented and were always free to avoid them if they wanted to. Moreover, the presentation of enrichment did not elicit any sign of stress in the reindeer.

Studying animals in the wild can be difficult as they tend to move around frequently and avoid humans, which can make it tough to maintain a controlled environment. Therefore, studying captive animals is important because it can expand our knowledge on the behavioural needs of animals, which can then be used for conservation purposes and to educate the public. Furthermore, because we have captive animals, we have a responsibility to maintain their natural behaviours of these animals.

7 Acknowledgements

First and foremost, I would like to thank my supervisor, Matthias Laska, for his patience and diligence in answering my abundant questions and emails, and the support he showed me throughout the thesis.

I would also like to thank the staff of Reykjavík Park & Zoo, for having an open mind towards all my ideas, trusting me with their animals and for all their help throughout the data collection. It was a pleasure working with all of you.

Last but not least, I would like to thank my boyfriend, Ólafur Valur Sigurðsson, and my family, for helping me maintain a good mental health throughout the thesis, especially during the data collection, and supporting me every step of the way.

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Appendix

A: Overview of the reindeers’ indoor enclosure. B: Tindur drinking from the outdoors water trough.

C: Gullbrá drinking from the small creek that forms after rainy days.

A: Tindur displaying a feeding behaviour (grazing).

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34 C: Hallveig displaying a passive behaviour inside the indoor enclosure (laying down).

D: All four reindeer displaying passive behaviours (standing still).

A: Hallveig displaying one form of grooming (locomotory behaviour). B: Gullbrá displaying one form of grooming (locomotory behaviour). C: Tindur displaying one form of grooming (locomotory behaviour).

A: Gullbrá eating the bark and pines off a pine tree (food enrichment). B: Hallveig eating the bark of an old branch (food enrichment).

Environmental enrichment for zoo-housed Icelandic reindeer (Rangifer tarandus)