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Linköping University | Department of Physics, Chemistry and Biology Bachelor thesis, 16 hp | Biology programme: Physics, Chemistry and Biology Spring term 2019 | LITH-IFM-G-EX—19/3698-SE

Behavioral synchronization

between dogs and owners.

Jasmine Heurlin

Examinator, Hanne Løvlie, IFM Biologi, Linköpings universitet Tutor, Lina Roth, IFM Biologi, Linköpings universitet

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Datum 07-06-2019 Date

Biologi, intuitionen för fysik, kemi och biologi

Biology, Department of Physics, Chemistry and Biology

Department of Physics, Chemistry and Biology Linköping University

URL för elektronisk version

ISBN

ISRN: LITH-IFM-G-EX—19/3698--SE

_________________________________________________________________

Serietitel och serienummer ISSN

Title of series, numbering ______________________________

Språk Language Svenska/Swedish Engelska/English ________________ Rapporttyp1 Report category Licentiatavhandling Examensarbete C-uppsats D-uppsats Övrig rapport _____________

Titel Behavioral synchronization between dogs and owners.

Title

Författare Jasmine Heurlin

Author

Nyckelord

Keyword

domestic dog, behavioral synchronization, dog-human bond, dog-human synchronization

Sammanfattning

Abstract

Dogs have lived with us for thousands of years, so we have learned to understand one another. Dogs have been shown to synchronize their behavior with humans. Behavioral synchronization is characterizes by doing the same thing at the same time and in the same place as someone else. This synchronization is often dependent on the relationship and the emotional state of the individuals. The main aim in this study was to develop a method to test behavioral synchronization and also to investigate how this, but also other behaviors, are effect by preceding human-dog interactions. Privately owned dogs (N=21) were tested with three different treatments (play, pet or ignore). The test procedure consisted of the owner walking or standing still in a predefined pattern, while their dog was freely roaming. This study showed that dogs adapted their movement pattern to their owners. This was similar to previous studies showing that the method developed can be used to test behavioral synchronization between owner and dog. Dogs explored the test arena less after play interaction and they also tended to seek more eye contact with their owners, but the interactions did not affect how much time spent in human proximity, how much they followed them or on dogs movement pattern.

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Table of content 1 Abstract ... 4 2 Introduction ... 5 3 Method ... 6 3.1 Animals ... 7 3.2 Test setup ... 8 3.3 Procedure ... 8 3.4 Analyzing behaviors ... 10 3.5 Statistical analysis ... 10 4 Results ... 10 5 Discussion ... 13 5.1 Conclusions ... 16

5.2 Societal and ethical aspects ... 16

6 References ... 17

7 Appendix ... 19

7.1 Appendix 1 signs ... 19

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1 Abstract

Dogs have lived with us for thousands of years, so we have learned to understand one another. Dogs have been shown to synchronize their behavior with humans. Behavioral synchronization is characterizes by doing the same thing at the same time and in the same place as someone else. This synchronization is often dependent on the relationship and the emotional state of the individuals. The main aim in this study was to develop a method to test behavioral synchronization and also to investigate how this, but also other behaviors, are effect by preceding human-dog interactions. Privately owned dogs (N=21) were tested with three different treatments (play, pet or ignore). The test procedure consisted of the owner walking or standing still in a predefined pattern, while their dog was freely roaming. This study showed that dogs adapted their movement pattern to their owners. This was similar to previous studies showing that the method developed can be used to test behavioral synchronization between owner and dog. Dogs explored the test arena less after play interaction and they also tended to seek more eye contact with their owners, but the interactions did not affect how much time spent in human proximity, how much they followed them or on dogs movement pattern.

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2 Introduction

Dogs were domesticated several thousand years ago (Víla et al. 1997), and since then, humans and dogs have lived in close association. Historically, we utilized dogs mostly for hunting and translocation (Morey 2010), while today we use dogs in many ways from

companionship to assist our police force or even helping blind people (Udell and Wynne 2008). By better understanding how dogs behave with humans and what make them adapt their behavior we can hopefully improve the cooperation between dog and human.

Behavioral synchronization is characterizes by doing the same thing at the same time and in the same place as someone else (see Duranton and Gaunet 2016, for a review). For example, hens sleep together to keep warm (Webster and Hurnik 1994), red deer synchronize while foraging (Conradt and Roper 2000) and sows and piglets synchronize when they leave their nest to explore (Jensen and Redbo 1987). Pilot whales have been shown to synchronize their breathing while swimming in pairs, suggesting that behavioral synchronization has a functional role in affiliative behavior (Senigaglia et al. 2012). Behavioral synchronization is also a strategy to maintain contact (Jarmar 1974) and social bonds (Conradt and Roper 2000) within a group. Synchronize behavior with a conspecific comes with many advantages and is viewed as an adaptation (Jarmar 1974, Webster and Hurnik 1994).

Dogs have for a long time been recognized to be a species where

individuals often do the same thing as their group members (Vogel et al. 1950). They exhibit many types of behavioral synchronization toward other dogs, such as sleeping together and moving together in the same pace. It has also been suggested that dogs synchronize more with

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2015, for a review). Interestingly, dogs have been shown to synchronize their behavior, not only with conspecifics, but also with humans

(Duranton et al. 2017, 2018, 2019). This was investigated by testing freely roaming dogs with their owner/caregiver in an enclosed arena indoors (Duranton et al. 2017) or outside (Duranton et al. 2018, 2019). Behavioral synchronization has been shown to be affected by both the relationship between dog and its owner (Duranton et al. 2017) but also their emotional states (Senigaglia et al. 2012). In addition, the dog’s human-related behavior can be influenced by humans emotional demeanor and enthusiasm (see Elyssa et al. 2015, for a review). For

example, how willing a dog is to play is correlated with the enthusiasm of the human, suggesting that the human’s mood and motivation influence the behavior during play sessions (Horváth et al. 2008). Play has indeed a

positive effect on human-dog relationships (Topál et al. 1997) and also petting which increases the oxytocin levels (Handlin et al. 2011), that promotes social-bonding in dogs (Romero 2014). Thus, these different interactions could affect behavioral synchronization, but this has to my knowledge never been tested.

The main aim of this study is to develop a method to effectively test behavioral synchronization between dogs and their owners, influenced by Duranton et al. (2017, 2018, 2019). In this study, I also investigate

whether different types of human-dog interaction could affect dog’s behavioral synchronization and behavior towards their owners.

3 Method

Since only privately-owned dogs were used in this study no ethical permit was needed. However, all owners were thoroughly informed and singed a

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consent form permit their dogs participation in this study. The owners permitted me to store their contact information in line with GDPR.

3.1 Animals

Privately owned dogs (N=21; 11 females, 10 males) of different breeds participated in this study (Table 1). The mean age was 4.6 years ± SE 0.6 and all dogs were recruited via social media and personal contacts.

Table 1. Overview of age, sex and breed of the participating dogs (Canis familiaris). Italics are used to show castrated dogs.

Name Sex Age (years) Breed

Milo Male 8 Australian sheperd

Hugo Male 2 Pug

Hemulen Male 7 Rougn Collie

Trocadero Male 3 Russkiy toy

Stella Female 2 Irish setter

Alice Female 3 Pug

Xroy Male 9 Danish Swedish fram dog

Vissla Female 1 Australian sheperd

Dexter Male 5 Staffordshire bull terrier

Stojja Female 3 German shepherd

Lo Male 3 Labrador retriever

Cilva Female 1 Alpenländisch dachsbracke

Niqo Male 7 Mixed breed

Lima Female 4 Hungarian mudi

Norrie Male 8 Lancashire heeler

Satchel Male 1 Bearded Collie

Nike Female 3 Basset fauve de bretagne

Wilda Female 7 Cairn terrier

Ella Female 6 Lagotto romagnolo

Anschie Female 7 German shepherd

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3.2 Test setup

All dogs were tested at Linköping university, Sweden, during April 2019. The test arena (6x10 m) was located outdoors between two buildings. Walls of these buildings enclosed two sides, and portable fence was used for the other two sides. Two HD-camcorders (Canon Legria) were placed on each long side to capture the entire test arena (Fig. 1A and 1B). An additional portable fence was used to construct a “start box”.

Figure 1. Schematic image of the test arena (A) including the locations of the camcorders and start box, and a picture of the test arena (B) showing the surrounding.

3.3 Procedure

All dyads were tested separately. When the dog and owner arrived, they first walked on leash inside the test arena clockwise, then the owner was instructed on the procedure during approximately 5 min. Each dyad was tested three times and before each test the owner was instructed to either ignore the dog, calmly pet the dog or play with the dog for 1 min. All interactions were preformed next to the start box, and all dyads

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order and with a five min break in between test. In addition, all owners were instructed not to interact with the dog during the test and also not have any treats or toys on them during and between tests.

After one minute of interaction (or lack of interaction during the ignore treatment) between owner and dog, they both entered the start box. Here the leash was removed from the dog and handed to the test leader and the owner was given a timer and a map with instructions on different

positions/tasks to perform and in which order (Fig. 2). The test started when the owner was still in the first position (Fig. 2). The owner then followed a predetermined route indicated with signs within the test arena (Appendix 1). The timer peeped to indicate when they were to change position/task.

Figure 2. Positions/tasks the owner performed during the test. The same figure was used as a map for the owner during the test.

The procedure was as follow (Fig. 2): The owner walked to position 1 and stood still for 15 seconds. Then the owner performed task 2 which included walking across the hole test arena to the other short side and

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back. After 15 seconds of walking the owner took the shortest path to position 3 and stood still for additional 15 seconds. Finally, the owner walked counter-clock wise along the fence/wall of the test arena for 15 seconds before the procedure ended.

3.4 Analyzing behaviors

An ethogram (Appendix 2) with predefined behaviors was used to record the duration and/or how often these behaviors occurred. All tests were video recorded and later analyzed in Observer XP (Noldus, version 13).

3.5 Statistical analysis

All statistical analysis was performed in SPSS (version24, IBM). Due to the non-parametric distribution of the data non-parametric tests were used. Wilcoxon test was used to test differences in movement of dogs when the owner was still or moving for every treatment (i.e. play, pet or ignore). To test if there was a difference in dog’s movement between treatments Friedman’s two-way analysis was used. Freidman’s two-way analysis was also used to test treatment differences in time spent by the dogs seeking eye contact, exploring, following and keeping proximity to their owner.

4 Results

Regardless of treatment, dogs spent more time moving when their owner was moving, compared to when the owner was still (Fig. 3; Play: Z= -3.458 p= 0.001; Pet: Z=-3.528 p< 0.001; Ignore: Z= -3.061 p=0.002). When comparing treatments, there was no difference in time spent moving when the owner was moving (Fig. 3; χ2(2)= 2.100, p= 0.350) or

time spent moving when their owner was moving (Fig. 3; χ2(2)= 2.100,

p= 0.350). Dogs differed in their time spent exploring between treatments (Fig. 4; χ2(2)= 15.600, p< 0.001). They spent less time exploring after

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play interactions compared to after pet and ignore treatments (Fig. 4; χ2(2)= -0.900, p= 0.013 and χ2(2)= -1.200, p< 0.001 respectively). There

was also a tendency for dogs to seek more eye contact after play

interaction than after ignoring or petting (Fig. 4; χ2(2)= 5.158, p= 0.076).

Dogs did not differ between treatments in how much time spent in close proximity to their owner (Fig. 4; χ2(2)= 2.800, p= 0.247) or following

their owner (Fig. 4; χ2(2)= 2,304, p= 0.316).

Figure 3. Proportion of time (mean ± 1 SE) dogs were moving during the treatments Play (N=21), Pet (N=21) and Ignore (N=20). * p>0.05.

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Figure 4. Proportion of time (Mean ± 1 SE) dogs spent on specific behaviors during the treatments Play (N =21, but for eye contact N=20), Pet (N=21, but for eye contact N=20) and Ignore (N=20, but for eye contact N=19). * p<0.05. (*) tendency.

Table 2. Generalized linear mixed model with the order of treatments as fixed effect and the different behaviors treated as targets. Individual dogs treated as random effect (N=21). There was no significant effect of the order of

treatments on any of the behaviors tested.

Target F df1 df2 sign. Move 2,734 2 58 0,073 Exploration 2,074 2 120 0,13 Eye contact 2,546 2 120 0,083 Human proximity 0,47 2 120 0,626 Human follow 2,734 2 58 0,073

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5 Discussion

The main aim of this study was to develop a behavioral synchronization test between dogs and their owners. In addition, I tested whether the interactions (i.e. play, pet, ignore) preceding the synchronization test influenced the behavior of dogs. The results showed that dogs adapted their locomotion activity depending on the owner was still or walking, but not depending on interaction. This is like earlier results (Duranton et al. 2017) indicating that the method developed in this study can be used to test behaviors between owner and dog. In addition, the results revealed behavioral differences depending on the preceding interaction, but there was no effect of order of the these interactions.

The method was adapted from an earlier study on behavioral

synchronization between dogs and owners (Duranton et al. 2017). Dogs were then tested indoors together with their owners that were walking or standing still in subtests, each separated by breaks. Recent studies have been conducted in the dog’s familiar area and outside, without breaks between the different task (Duranton et al. 2018, 2019). In the present study the owner preformed all tasks (walking and standing still) within the same test, to make the testing more efficient. Also, this made it easier to compare the effect of different interactions between dog and owner. Duranton et al. (2017, 2018, 2019) allowed all dogs to roam freely in the testing arena for ten (Duranton, et al. 2017) to 15 min (Duranton et al. 2018, 2019) directly after arrival. In the present study, dogs walked on leash clock wise in the test arena before the test. This was done to make the dogs comfortable with the arena. Similarly, to previous studies (Duranton et al. 2017, 2018, 2019), owners in this study were given

instructions not to interact with their dogs during the synchronization test, to allow the dogs to behave spontaneously.

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This study revealed that dogs spent less time moving when their owners were still, compared to when their owner was moving, which is similar to previous studies (Duranton et al. 2017, 2018, 2019). Hence, dogs do adapt their movement pattern to their owners, and the test procedure used in this study can be used to study dogs synchronization behavior towards their owners. The reason behind dog-human synchronization might be to maintain social bonds (Conradt and Roper 2000), which could be further enhanced by additional human-related behaviors (see Payne et al. 2015, for a review).

The second aim of this study was to investigate how the interactions between owner and dog could influence dogs’ behavior. All treatments (play, pet and ignore) were tested on all dogs. The order in which the treatments was performed, had no effect on the observed behaviors. Also, there was no difference in the dogs’ movement patterns between the different treatments. Hence, the preceding interaction between owner and dog may not affect how well dogs synchronize with their owners.

Interestingly, Duranton (2017) revealed an effect of human-dog

relationship on synchronization and future research should consider this potential effect.

Similarly, treatments did not influence human proximity behavior of dogs. Proximity seeking is a behavior that is associated with anxious situations (Fallani et al. 2013) and one concern during behavioral tests is if stress may influence the results and proximity behavior. Since all treatments used in this study were indented to be positive (play, pet) or neutral (ignore), treatments should not have stressed the dogs. For example, petting is associated with an increase in oxytocin in dogs (Handlin et al. 2011), and human-dog play interaction is related to reduced stress levels in dogs (Roth et al. 2016). Since there was no

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difference between treatments on proximity behavior this suggests that the treatments was perceived as positive or neutral.

However, there was a difference in how much time dogs spent exploring the test arena after the play treatment compared to the ignore and pet treatment. There was also a tendency for more eye-contact seeking

behavior after play interaction. It could be that the dog found their owner to be more rewarding after the play treatment compared to the other interaction treatments, making them less motivated to explore the

surrounding olfactory stimuli in the test arena. This is further supported by that when a human is acting enthusiastically dogs will prioritizes humans over their own sensory capacities, more so than when the human is acting neutral (Horowitz et al. 2013; see Payne et al. 2015, for a

review).

There was no difference in how much time dogs spent following their owner between treatments. The definition for following owner was: If the dogs moves in the same direction as their owner behind or beside their owner. It may be that with a broader definition e.g. including all positions of the dog when it moved in the same direction there would have been a difference between treatments. This is suggested for future studies, then the results could be compared with the movement pattern of the dogs and maybe shown even more evidence for behavioral synchronization.

To further minimize the risk of stress influencing the result, dogs should be tested in a familiar area (Duranton et al. 2018, 2019). Even though it was a novel place to the dogs, it was outside with little disturbance

mimicking a normal walk. I suggest future studies to record stress-related behaviors and ask the owner if it’s dog behaved normal (Duranton et al. 2017, 2018, 2019). In this study it was not possible to score stress related

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behavior, such as lip licking, due to low resolution of the video recordings.

5.1 Conclusions

To conclude, the method developed in this study can be used to test behavioral synchronization between owners and dogs. It also showed that dogs adapt their movement patterns to their owners, which was not

affected by the preceding interactions between owners and dogs. Dogs explored the arena less after play and also tend to seek more eye contact, but treatments did not affect their human-proximity behavior or how much they follow their owner.

5.2 Societal and ethical aspects

Dogs are an integrated part in our civil protection including e.g.

assistance dogs to bomb-sniffing dogs (Udell and Wynne 2008). There is a growing number of enterprises that utilize the behavior of domestic dogs, therefore it is important to understand what affects dog’s behavior (Udell and Wynne 2008). By showing what contributes to behavioral synchronization, the general behavior a dog exhibits towards human but also how it can differ between breeds could improve the welfare of dogs. We often use specific breeds for specific tasks, for example Labradors as assistance dogs. By comparing breeds, levels of synchronization we may find more breeds that could excel at this task. But not only that it will also improve how we as humans work with our dogs instead of focusing on how we should not.

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6 References

Conradt L, Roper TJ (2000) Activity synchrony and social cohesion a fission-fusion model. Proceedings of the Royal Society 267, 2213-2218. Duranton C, Bedossa T, Gaunet F (2017) Interspecific behavioural synchronization: dogs exhibit locomotor synchrony with humans. Scientific Reports 7, 12384.

Duranton C, Bedossa T, Gaunet F (2018) Pet dogs synchronize their walking pace with that of their owners in open outdoor areas. Animal Cognition 21, 219-226.

Duranton C, Bedossa T, Gaunet F (2019) When walking in an outside area, shelter dogs (canis familiaris) synchronize activity with their caregivers but do not remain as close to them as do pet dogs. Journal of Comparative Psychology, Advance online publication.

Fallani G, Prato Previde E, Valsecchi P (2007) Behavioral and

physiological responses of guide dogs to a situation of emotional distress. Physiology & Behavior 90, 684-655.

Handlin L, Hydberg-Sandberg E, Nilsson A, Ejdebäck M, Jansson A, Uvnäs-Moberg K (2011) Short-term interaction between dogs and their owners: effects on oxytocin, cortisol, insulin and heart rate—an

exploratory study. Anthrozoös 24, 301-315.

Horowitz A, Hecht J, Dedrick A, (2013) Smelling more or less:

Investigating the olfactory experience of the domestic dog. Learning and Motivation 44, 207-217.

Horváth Z, Dóka A, Miklósi Á, (2008) Affiliative and disciplinary behavior of human handlers during play with their dog affect cortisol concentration in opposite directions. Hormones and Behavior 54, 107-114.

Jarman PJ (1974) The social organization of antelope in relation to their ecology. Behaviour 48, 215–267.

Jensen P, Redbo I (1987) Behaviour during nest leaving in free-ranging domestic pigs. Applied Animal Behaviour Science 18, 355-362

Morey DF (2010) Dogs: Domestication and the development of a social bond. Cambridge University Press, New York.

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Payne E, Bennett PC, McGreevy PD (2015) Current perspectives on attachment and bonding in the dog–human dyad. Psychology Research and Behavior Management 8, 71-79

Rehn T, Handlin L, Uvnäs-Moberg K, Keeling L (2014) Dogs' endocrine and behavioural responses at reunion are affected by how the human initiates contact. Physiology & Behavior 124, 45-53

Romero T, Nagasawa M, Mogi K, Hasegawa T, Kikusui T (2014) Oxytocin promotes social bonding in dogs. Proceedings of the National Academy of Sciences of the United States of America 25, 9085-9090. Roth LSV, Faresjö F, Theodorsson E, Jensen P (2016) Hair cortisol varies with season and lifestyle and relates to human interactions in German shepherd dogs. Scientific Reports 6, 19631.

Senigaglia S, Stephanis R, Verborg P, Lusseau D (2012) The role of synchronized swimming as affiliative and anti-predatory behavior in long-finned pilot whales. Behavioural Processes 91, 8-14.

Topál J, Miklósi Á, Csánui V (1997) Dog-human relationship affects problem solving behavior in the dog. Anthrozoös 10:4, 214-224. Udell MAR, Wynne CDL (2008) A review of domestic dogs’ (Canis Familiaris) human-like behaviors: or why behavior analysts should stop worrying and love their dogs. Journal of the experimental analysis of behavior 89, 247-261.

Vila C, Savolainen P, Maldonado JE, Amorim IR, Rice JE, Honeycutt RL, Crandall KA, Lundeberg J, Wayne RK (1997) Multiple and ancient origins of the domestic dog. Science 276, 1687-1689.

Webster AB, Hurnik JF (1994) Synchronization of behavior among laying hens in battery cages. Applied Animal Behaviour Science 40, 153-165.

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7 Appendix

7.1 Appendix 1 signs

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7.2 Appendix 2 Ethogram

Term Description Source

Human proximity The dog is within a dog length from

the human. Duranton et al. 2017

Move The dog is moving in any direction.

Front paws are moving more than 5 cm.

Duranton et al. 2017

Still The dog is not moving in any

direction. Front paws moving less than 5 cm in any direction.

Duranton et al. 2017

Eye contact The dog’s nose is pointing towards

the human’s head. Duranton et al. 2017

Following human The dog is moving in the same

direction as human.

Exploration Motor activity directed towards any

physical aspect of the environment, dog is sniffing/licking/manipulation something

Rehn et al. 2014

References

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