Can Choice Help to Build Resilience in Dogs? Anthony Richens-Smith 2Nd March 2019

Advanced Diploma Canine Behaviour Management Module 12 Assessment Booklet

Can choice help to build resilience in dogs? Anthony Richens-Smith 2nd March 2019

Advanced Diploma in Canine Behaviour Management (Level 6) Animal Jobs Direct & Canine Behaviour College

Word Count: 8,896

Abstract

Sometime over the last 100,000 years, two branches of the Canidae family split from a common ancestor. Mutations in the mitrochondrial DNA caused an evolutionary divergence which may have resulted in some canids becoming more tolerant of early humans and more interested in exploring novel situations. Those who remained wary of humans evolved into the Grey Wolf (Canis lupus) while the others began to carve out a niche existence on the edge of human settlements, eventually becoming the domesticated dog (Canis lupus familiaris). The mechanisms of that early human-dog association are not known, but it is highly likely that “choice” played some role (as can be seen in free-ranging village dogs today). Since that early association, the ability to make choices has almost been completely removed from dogs’ lives, and human caregivers have become the decision-makers and control almost all aspects of a dog’s day to day life (what and when to eat; where to sleep; when and how to exercise; how, when and who to interact with; when to procreate; and even when to urinate and defecate).

This study speculates that “choice-based” canine research is severely limited and reviews wider animal and human research to extrapolate that “lack of choice” results in a negative cognitive bias which can lead to anxiety-related behaviour and lower resilience in stressful situations. Similarities in different species behaviour, as well as the similarities between canine and human physiology and neurology are explored, along with the benefits of enrichment which replicates aspects of natural behaviour and returns elements of control back to the animal (for example sniffing and exploration).

Two similar surveys were produced on the behavioural effects of “choice-based” enrichment, one aimed at canine professionals and one at general dog owners. The results showed an overwhelming belief that enrichment has a positive effect on anxiety-related behaviour and increases resilience. While there are limitations with the research methodology and data, these results support existing studies showing that encouraging “choice” can positively affect an animal’s cognitive bias. It is speculated that this is probably owing to “choice-based” enrichment giving back some aspect of control, supporting the researcher’s view that choice can help build resilience.

However, this study also recognises its limitations and recommends that more in- depth research is conducted in this area.

Contents

Title Page 4 Abstract 5 Contents 7 Chapter 1: Background and Context 5 Chapter 2: Literature Review 12 Chapter 3: Research Methodology 20 Chapter 4: Data Presentation 22 Chapter 5: Data Analysis & Discussion 25 Chapter 6: Conclusion 33 Bibliography 40 Appendix 1: Survey Questions (Canine Professional) 47 Appendix 2: Survey Questions (Owner) 49 Appendix 3: Full Survey Analysis & Sample Responses 48

Chapter 1: Introduction and Background

Sometime between 35,000 and 100,000 years ago mutations in the mitochondrial DNA of a common canid ancestor (Skoglund, Ersmark et.al, 2015), caused an evolutionary divergence (Darwin, 1859) which led to the ancestors of the Grey Wolf (Canis lupus) and what would become the domestic dog (Canis lupus familiaris). These mutations caused a shift in the way the species reacted to early humans, moving from fear and avoidance to one of tolerance, resulting in these proto-dogs “choosing” to live on the edge of human settlements (Coppinger, 2001; Joyce, 2013). This association between dogs and humans became fixed over thousands of years, leading to the domestic dog we know today. During this time, human manipulation through selective breeding caused dogs to remain juvenile-like into adulthood and making them totally reliant on humans for every aspect of their life (when, where and how to eat, sleep, toilet, procreate etc.). It is my belief that by taking away dogs’ ability to make choices, they are less able to control aspects of their environment, causing many of the behavioural issues we see in dogs today. The aim of this thesis is to show that by returning an element of control to their lives (using choice) we can help to make them more resilient when faced with stressful experiences.

Choice What is choice? According to the Oxford Online Dictionary, choice is defined as “an act of choosing between two or more possibilities” but in behaviour, it can also mean “the right or ability to choose” (Oxford Online Dictionary). In humans, choice is a cognitive process involving decision making (assessment and judgement) of two or more possible options, each one consisting of a positive value (Beresford & Sloper, 2008). For example, a person who likes both chocolate cake and ginger biscuits has to assess the value of each and make a judgment on which one to choose (if they are only allowed to pick one). However, if one option does not hold any value for the recipient (for example, if they do not like ginger), the outcome is not a true choice (Beresford & Sloper, 2008). Behaviourally, being offered the options of cake or biscuits empowers the recipient by giving them the ability to choose between the two (or potentially choosing both or choosing neither). Likewise, if both options are available but only one is offered, the element of choice is removed from the recipient, making them reliant on another to make the decision for them. This is control.

To what extent non-human animals (for example dogs), consciously evaluate options or make unconscious decisions based on innate behaviour patterns (Lorenz, 1950) is beyond the scope of this thesis, however as more research is carried out on the brain responses of awake dogs using fMRI scanning technology (Berns, 2012), it is no longer reasonable to assume that canine “choices” are purely conditioned reflexes (Pavlov, 1927) or based solely on reward, punishment and reinforcement (Skinner, 1938). The dawn of neuroeconomic methods (Glitchier & Rustichini, 2004) has resulted in many parallel lines of research which indicate human decision-making is mirrored in animal choice behaviour, leading to studies in the evolution of decision making across the whole animal kingdom (Van Wingerden & Kalenscher, 2012). However, it must be remembered that “choice” is not the same as free will (List, 2011), rather it is the ability to make decisions within a fixed list of options (Palmer, 2010). Studies on captive flies show that while behaviour may unpredictable, it also shows that responses are “picked” from a set of fixed patterns (Bremb, 2007). Therefore choice (especially in the context of non-human animals) may be seen as the ability to control aspects of their environment, within fixed parameters.

Choice in Evolution and Domesticity At some distant point in history, early (or proto) dogs discovered they had a greater tolerance for humans than did their ancestors. We do not know the exact mechanisms involved, but genetic differences discovered in the mitochondrial DNA of present-day wolves and dogs has been linked to a genetic divergence occurring between 35,000 and 100,000 years ago in their common ancestor (Skoglund, Ersmark et.al, 2015). Genetic mutations may have resulted in a positive cognitive bias, leading to a more optimistic outlook in novel situations (Clegg, 2018). This could lead to increased inquisitiveness, a greater willingness to explore and a greater tolerance for the presence of other species (diametrically opposed to normal survival instincts). This resulted in proto-dogs being more willing to be close to humans and live on the edge of human settlements (Coppinger, 2001; Joyce, 2013), while the proto-wolves remained fearful and continued to avoid humans. Over generations, any genetic predisposition towards tolerance/inquisitiveness would have been strengthened, encouraging choice. This can be seen today in free-ranging “village” (or pariah) dogs throughout the world.

Image source: http://www.k9dna.org/sites/default/files/images/books/learn-about-dog-genetics/dog-evolutionary-history.jpg

Many village dog populations are (genetically) directly descended from early indigenous dogs, showing limited interference from selective breeding (Boyko et al., 2009), making them the closest approximation of what life was like for proto-dogs. Most of these dogs live in and around villages and are often free to roam inside and outside of houses, scavenging for food or even occasionally fed directly by villagers, even though there appears to be no sense of “ownership” of the dogs. Village dogs have not been domesticated and still retain a healthy fear of strangers, staying a safe distance from them, but also electing to remain close by (Ortolani, Vernooij & Coppinger, 2009). The ability to choose a comfortable distance gives them an element of control over their immediate environment.

It can be seen how “choosing” to interact (even on a basic level) with humans might lead to domestication. A study on wild mice in 2002 suggests parallels with village dogs, indicating a process of self-domestication without any human breeding intervention (Dengler, 2018). Whereas the 50+ year Farm Fox experiment (Belyaev, 1959) selectively bred silver foxes for tameness, resulting in foxes that physically look and act similar to domestic dogs. Foxes were selected for breeding solely on their inquisitive nature and a less aggressive temperament when fed by human caretakers (Belyaev; Trut & Dugatkin, 2017). Both of these studies show how behaviour can be influenced by having an optimistic outlook, leading to the parameters of choice being extended and the enablement of manipulating particular aspects of their environment.

Choice and Lack of Choice in Domestic Dogs Domestic dogs do not have the same level of choice as early or village dogs because as they became permanent members of our households, choice and control of their environment passed to humans. This resulted in almost all aspects of a dog’s life being controlled by their human caregivers, from when and what to eat, to when and where to eliminate. In the 19th century the advent of Kennel Club Associations and dog shows led to intensive selective breeding and the protection of bloodlines from procreation outside of the breed (Dogtime). This has led to over 400 different breeds recognised as pure-breds by UK Kennel Club. These breeds bear little resemblance to early dogs (or even free-ranging village dogs) and are often bred for looks rather than behaviour or ability. This resulted in adult dogs that can look like puppies, retaining juvenile characteristics throughout their life (paedomorphism) which can also lead to owners treating them like babies and over indulging them (Herzog, 2013). This can result in the dogs forming an over attachment to their owners (Farricelli, 2016), reducing their ability to make decisions for themselves which may lead to separation- related anxiety.

Choice has further been eroded from domestic dogs with the emergence of “pack theory” (Mech, 1968) and the idea of dominance, based on an erroneous study undertaken on unrelated captive wolves in the 1930s and 1940s by Rudolph Schenkel which concluded that wolves (and therefore dogs) live in an aggressive unit, presided over by the “alpha” and ruled through violence (Miller, 2018). This theory has been refuted many times by scientists who have actually observed wolves in their natural environment (Mech, 2000) but the theory still persists with many “old style” trainers basing their training methods on it and encouraging owners to “punish” unwanted dog behaviour using physical violence, coercion and fear, leading to the complete removal of any canine choice.

Resilience Resilience is defined as “the capacity to recover quickly from difficulties” (Oxford Online Dictionary) and in behaviour terms, it is “the ability to adapt well in the face of adversity, trauma and significant sources of stress” (McConnell, 2016). Classification of what constitutes a “significant source” of stress is subjective and is based on the individual. For example, a dog with a pessimistic outlook (negative cognitive bias) may see a bag which has been left on the floor to be “stressful” situation. As Suzanne Clothier explains on her “Arousal, Anxiety & Fear …” DVD, the dog views everything as © Animal Jobs Direct 8 Updated: 21-06-2017 Advanced Diploma Canine Behaviour Management Module 12 Assessment Booklet

“We’re all going to die!”, whereas a dog with an optimistic outlook (positive cognitive bias) may think “Cool, what’s that? Can I play with it?” (Clothier, n.d.).

Stress There are many forms of stress, but not all are bad (Grippo, 2016). Stress is a necessary component which enables an organism to function, and mild stress is needed for learning (Michaels, 2014). However, high levels of acute stress and sustained levels of elevated stress (chronic stress), negatively affects both the short- and long-term physiology and neurology of a dog.

Experiencing Stress During stressful experiences, the amygdala becomes excited, causing the sympathetic nervous system to release stress hormones including norepinephrine (NE), gamma- aminobutyric acid (GABA), adrenaline, testosterone and cortisol via the hypothalamic- pituitary-adrenal axis (Beerda et al., 1997). This puts the body into a heightened state of arousal (survival mode), which causes changes in the autonomic nervous system (including increased heart rate and slowing digestion). Increased levels of neurotransmitters including NE and dopamine are also released into the cranial prefrontal cortex, which inhibits cerebral cortex activity and disrupts the higher cognitive functions (such as learning, problem solving and working memory). Increases in levels of dopamine combined with a reduction in serotonin, raises anxiety levels as well as disrupting social behaviour mediation (for example, impulse control). In a stressful situation, levels of stress hormones can take up to 15 minutes to reach their peak but may remain in the body for up to 5 days after.

Sustained high levels of stress (such as chronic feelings of anxiety) prolong cognitive disruption, making any form of “learning” difficult and may even result in the dog becoming “shutdown” to everything around them (Anderson, 2013). Neurotransmitter levels also become severely depleted which causes long-term physiological, neurological and behavioural issues (NE regulates energy levels; dopamine regulates attention, reaction and motor-coordination; serotonin regulates mood, pain and arousal).

The effects of stress can present in several ways depending on the situation. For example, in a situation of acute stress the body may become more sensitive to pain, and the dog “loses” the ability to control impulses and becomes more easily aroused © Animal Jobs Direct 9 Updated: 21-06-2017 Advanced Diploma Canine Behaviour Management Module 12 Assessment Booklet or anxious. This can manifest as hyperactivity, lack of attention, yawning, panting, sweating paws, shivering, increased (and inappropriate) toileting or diarrhoea, vomiting, destructiveness, vocalisation such as whining or excessive barking, aggressive and reactive behaviour. Chronic stress may present as refusal of food and treats, lethargy, excessive sleeping, excessive grooming, obsessive compulsive behaviour, confusion, isolation, aggression and self-mutilation (Dog Behaviour Clinic, n.d.).

Resilience in Puppies From birth, puppies are subjected to various forms of stress, from being blind and totally reliant on their mother for everything, to experiencing everything for the first time. Considering the amount of new (novel) experiences they have to process, they are remarkably resilient from an early age. According to Scott and Fuller (1965), there are critical periods of learning within puppy development from which future behaviour is based. These include observation of their mother’s behaviour (Battaglia, n.d.), interaction and socialisation with siblings and other species (including humans). Through play and practise, they learn skills such as how to read body language and bite inhibition (Seksel, 2010). During the main periods of socialisation (Scott, 1958), they are free to explore their environment and while they can be easily startled (for example by unusual sounds), they are unlikely to become fearful of new experiences until after 5 weeks of age (Tudge, 2011). After this time, negative experiences (such as forced socialisation scenarios like “puppy play groups”) can result in fearful memories being stored which affect behaviour throughout later life (Tudge, 2011). However, this does not prove choice (or lack thereof) plays a role in resilience and individual experiences cannot be generalised to the whole species.

Reintroducing Choice The perception of the canine-human bond has changed dramatically over the last few decades, moving away from fear and punishment towards cooperation and mutual benefit. This change in attitude and interaction appears to positively affect both species by promoting canine welfare and enhancing well-being (McGreevy et al., 2015). One aspect of this change is the reintroduction of choice. While it is no longer possible to give domestic dogs the same freedoms free-ranging village dogs enjoy, we can extend decision-making (i.e. choices) within a fixed list of options (Palmer, 2010), enabling dogs to get back some element of control within their surroundings.

Types of Choice As seen previously, choice can take many forms and it follows that those which replicate (or are at least close to) natural decision-making behaviour provides the most benefits for animals. For example, the ability to explore the immediate environment, the ability to choose the level of interaction with others (and the distance), the ability to perform natural behaviours (within limits), such as foraging and problem solving. These choices are accessible to village dogs and in some cases, they provide some evidence for resilience when in a stressful situation (such as being approached by a stranger). Instead of “running away”, they choose to remain “just out of reach” (Ortolani, Vernooij & Coppinger, 2009).

Many modern trainers and behaviourists use operant conditioning and positive reinforcement to encourage behaviour through rewards as a way of reducing stress, for example when requiring veterinarians to take blood samples (Pryor, 2003). Others use classical counter-conditioning to pair a previously stressful stimulus (for example another dog) with “good feelings” by feeding food treats whenever the stressor is in view and stopping once out of view. However, it is debatable whether these do constitute choice or whether they may add to stress.

Others use choice to build confidence by allowing the dog to “choose” their level of comfort (e.g. distance) in stressful situations (Clothier; Stewart, n.d.). For example, throwing treats behind (or to the side of) the dog, so they have the choice whether to approach closer or stay at a further distance (while still receiving treat rewards).

Enrichment in the form of mentally stimulating games is used to encourage decision- making and problem solving, while performing natural behaviours (for example exploration through sniffing) and stepping back from particular behaviours, using impulse control.

Historically, many choices have been removed from domestic dogs’ lives since they began to associate with humans thousands of years ago. However, the importance of providing some level of choice is now recognised as being an important part of welfare and elements of this have been included in the Animal Welfare Act, 2005 (need for a suitable environment; need to be able to exhibit normal behaviour patterns; need to be housed with, or apart, from other animals).

Chapter 2: Literature Review

The long association between canines and humans created the potential for a variety of relationships between the two species. In some, pet dogs are viewed as important members of the family and in others (for example, free-ranging and village dogs) canines keep some distance but are tolerated by humans and depend on them for food (Miklósi, 2014 cited in Miklósi & Kubinyi, 2016). During this association, dogs have been used in behavioural and psychological research for almost as long as experiments of this kind have been performed (Lea & Osthaus, 2018).

Historically, there have been many areas of study on animal physiology, behaviour, cognition and emotions, but research based on choice is severely limited, and is often relegated to “choice between two items” or seen as additional data from “lack of choice” and avoidance experiments (e.g., Brush, Brush, & Solomon, 1955; Solomon & Wynne, 1953 cited in Lea & Osthaus, 2018). However, these and other early studies conducted on dogs, like classical conditioning (Pavlov, 1927) and learned helplessness (Seligman, 1972), helped to formulate and drive forward knowledge and understanding of human behaviour, resulting in the field of Psychology we know today. This has naturally led to comparisons between human and animal behaviour, resulting in articles appearing in Psychology Today from leading ethologists like Marc Bekoff who states “I've always been fascinated by the similarities and differences between humans and other animals” (Bekoff, 2016); veterinarian Carlo Siracusa (from the American College of Veterinary Behaviourists) who comments that “dogs and humans have similar social and emotional brains” (Siracusa, 2018); and in books like “Not So Different: Finding Human Nature in Animals”, in which biologist Nathan Lents argues “the same evolutionary forces of cooperation and competition have shaped both humans and animals. Identical emotional and instinctual drives govern our actions” (Lents cited by Bekoff, 2016).

In “current perspectives on attachment and bonding in the dog-human dyad”, Payne, Bennett and Mcgreevy (2015) speculate that the human-dog relationship is similar to human caregiver and infant. Evidence is offered that dogs show indications of attachment behaviour such as seeking out a figure they have bonded with during times of stress. Absence of this figure may result in separation-related distress, whereas their presence can reduce stressful experiences as well as constituting a

© Animal Jobs Direct 12 Updated: 21-06-2017 Advanced Diploma Canine Behaviour Management Module 12 Assessment Booklet secure base, enabling dogs to explore novel environments more freely, while remaining in close proximity to the caregiver. They also state that positive reinforcement in training and affiliative interactions are likely to promote a positive cognitive bias in dogs, which can lead to favourable behaviour responses. They admit however, that it is unclear which factors influence attachment bonds with humans.

A study by Nagasawa et al., (2015) shows that modes of communication bonding (such as mutual gazing) between humans and domestic dogs, results in similar physiological effects found in human mother-child bonding. They discovered that (unlike wolves), urinary oxytocin concentration increases in both dogs and humans after periods of mutual gazing. After an increased dose of oxytocin was administered nasally to the dogs, canine gazing increased more, which led to further oxytocin increases in both species. This compares with a study on oxytocin release during mother-child gazing (Kim et al., 2014) which shows a higher maternal oxytocin response during gazing (which increased during times of infant distress). Results also indicated that mothers with a lower-than-normal oxytocin concentration, gazed less at their infants during times of distress, which resulted in no increases in oxytocin levels.

Another study found that manually increasing oxytocin levels (intranasally) in golden retrievers, led to an increase in seeking out human assistance in order to solve an insolvable food puzzle. However, variations in oxytocin gene receptors were similarly found in wolves which does not indicate this to be an adaptation through domestication (Jensen et al., 2017).

These studies indicate the importance of oxytocin in bonding attachments and social interactions but also provides evidence for similarities between canine and human physiology. From an early age, social bonding plays an essential role in the development of skills which enable animals to adapt to (and recover from) stressful experiences and trauma (Scott & Fuller, 1965; Bataglia, n.d.; Tudge, 2011; McConnell, 2016). Oxytocin’s role in social attachment bonding and other research into the effects of oxytocin release and isolation-stress in rats and prairie voles (Gonzalez et al., 2001; Barrett et al., 2015), implicate oxytocin production as being important in developing resilience.

According to Beerda et al. (1997), a poor domestic environment (e.g. restricted housing), harsh training sessions (e.g. immobilisation and punishment) and an inability to control their social environment can lead to reduced welfare and stress.

Stress in dogs can be measured by levels of cortisol found in saliva and plasma (Cobb et al., 2016; Hennessy et al., 1997). A study on shelter dogs showed higher levels of plasma cortisol in new entrants (based over the first 3 days), than in those that had been in the shelter for 9 days or more, indicating prolonged activation of the hypothalamic-pituitary-adrenal (HPA) axis during stressful experiences.

Prolonged stress can affect the immune response, sociability and overall health (Blecha, 2000; Hewson, Hibby & Bradshaw, 2007 cited in Belpedio, 2010) and can manifest as stereotypy behaviour such as figure-eight spinning, vertical jumping, repetitive pacing, increased startle response, stress defecation, compulsive grooming and excessive vocalisation (e.g. Abrantes, 1997; Aloff, 2005; Beerda et al., 1999; Handelman et al., 2008; Rugaas, 1997 cited in Belpedio, 2010). Stress can also be caused by emotional states (such as arousal, fear, nervousness agitation and frustration) and this affects the endocrine and sensory systems, increasing cortisol production from the adrenal glands. A study by Hiby et al. (2006) found high levels of cortisol in shelter dogs that were more active in their kennels (cited in Belpedio, 2010). Dogs that become habituated to kennel life had lower cortisol levels (Hewson et al., 2007 cited in Belpedio, 2010) as did those that had early socialisation experiences, exposure to novelty, and those receiving human interaction in the form of play, petting and grooming (Coppola et al., 2006 cited in Belpedio, 2010).

Dr Dennis Charney (2004, cited on http://simplybehaviour.com/) declares “the more control an animal feels he has over his own environment and the ability to able to communicate his needs, the easier he will find it to make good decisions and the more resilient he will be”. He goes on to state that some elements of stress during puppy developmental stages helps to build resilience, but also that when the body’s adaptive stress response (allostasis) becomes disproportionate to a given situation, physiological and psychological problems can occur.

Resilience comes from the complex interplay between nervous system, immune system, endocrine system and the brain which helps to build a resistance to prolonged stress (Simply Behaviour, n.d.). Studies show that early separation of rats from © Animal Jobs Direct 14 Updated: 21-06-2017 Advanced Diploma Canine Behaviour Management Module 12 Assessment Booklet mothers and siblings, can result in a muted hypothalamic-pituitary-adrenal response and improved cognitive abilities in later life. However, excessive separation had the opposite effect (particularly in monkeys) and resulted in “despair-type” responses (Young et al., 1973 cited in Simply Behaviour, n.d.). Patricia McConnell (2016 citing studies by McMillan, Duffy & Serpell, n.d.) states that 30% of puppy-mill dogs exhibit a “blank look” and 24% were “shut down” – in other words, these dogs suffer from a sense of learned helplessness. In building resilience, McConnell (2016) says that dogs: • Need to feel a sense of safety and security (avoiding sensory overload and providing a sense of predictability). • Have social support (human or canine). • Have a sense of autonomy (are able to create choices and teach behaviours which they can initiate themselves. e.g. impulse control). • Be healthy and balanced physiologically (provision of physical and mentally stimulating exercise, with some time outdoors).

This is similar to building resilience in human children. Karen Young (2016) states that strengthening executive functions strengthens the prefrontal cortex, enabling children to manage behaviour and feelings, thus increasing their ability to build coping strategies. She says strengthening executive functions can be achieved through: • Establishing routines (predictability). • Modelling healthy social behaviour and maintaining supportive relationships. • Creative play (enrichment), including board games (aids the development of impulse control). • Creating autonomy (opportunities to think and act independently and make their own decisions).

Having an optimistic outlook (positive cognitive bias) is a key element of resilience (Young, 2016). Recent research conducted by Duranton and Horowitz (2018) found that dogs who participate in nose work (sniffing) have an increased optimism compared to those carrying out heel work. The dogs were initially trained that a bowl in one location always contained food, while a bowl in another location was always empty. The empty bowl was then placed in an ambiguous location which was equally spaced between the original locations, with the time recorded how long it took the dogs to go to the bowl in the belief it contained food. The results showed that dogs who had previously done nose work went to the bowl faster than those who did heel work, leading to the conclusion that “sniffing dogs” had a more positive cognitive bias © Animal Jobs Direct 15 Updated: 21-06-2017 Advanced Diploma Canine Behaviour Management Module 12 Assessment Booklet

(i.e. they think it may be full, instead of “it will probably be empty”). According to Duranton & Horowitz, this is possibly owing to the fact that sniffing dogs are able to exercise “choice” and proves the importance of giving dogs opportunities to make their own decisions. Sniffing is also innate behaviour and is necessary for good welfare (Duranton & Horowitz, 2018).

Choice tests are often used to measure preference in animals, with results being used to make recommendations for (captive) animal welfare. Motivation is generally used as a major factor in welfare research as it is argued that animals suffer when they are prevented from performing an activity it is highly motivated to perform (Dawkins 1983, 1990 cited in Bateson, 2004). However, criticisms of this model state that short- term motivational priorities may not produce long-term welfare as motivational priorities change depending on numerous parameters (for example, gender, breed, time of year, reproductive state, previous experience etc.). It has also been argued that selective breeding (as in domestic dogs) has virtually removed decision-making so animals are no longer able to make adaptive choices (Mason et al., 1997; Cooper & Appleby, 1995; Grandin et al., 1994 cited in Bateson, 2004). However, Bateson (2004 citing Nicol, 1997 as an example) counters that welfare may still be maximised by giving an animal “what it wants” as long as health is not compromised.

According to Amdam & Hovland (2011), animal preferences come from choice behaviour and depends on motivational strength. They state that the willingness to engage in a behaviour can be positive or negative, varies in strength and is reasoned from behaviour such as approach-avoidance behaviour (citing Kirkden & Pajor, 2006) inferring decision-making processes which may be adaptive. They conducted an observational study on social preferences and the motivational strength of female juvenile silver foxes (previously trained to open a door by pulling on a looped rope). A specific number of “pulls” needed to be achieved before the door opened, giving access to food or socialisation with another female. The door remained open, ensuring the fox had the choice whether to enter or leave voluntarily. Each day the number of pulls required to open the door increased, and results showed that while food was the greatest preference (perhaps owing to hunger), social interaction represented 38% of the value placed on food, leading the researchers to conclude that social interaction was also important to the foxes (Amdam & Hovland, 2011).

Anecdotally, Dog trainer Staci (Manners for Mutts Blog, 2011) states that choice-based training allows animals to think and problem solve while learning from their mistakes, without fear of punishment. Using operant conditioning with positive reinforcement, encourages the dog to choose to work towards something they want instead of only trying to avoid punishment. This results in a dog who is a willing participant in training sessions as they are able to learn what behaviour gains rewards.

Many American zoos also use operant conditioning as a way of providing choices and improving welfare, when carrying out veterinarian checks and basic medical procedures like taking blood samples, hoof care etc. Previously they would have to sedate or “physically push” animals into required positions, whereas they now use positive reinforcement and clicker training. According to Karen Pryor (2003), “clicker training provides mental and physical stimulation, enriches … and saves … the animals’ lives”. Writing on her blog (http://clickertraining.com/), she recounts a visit to a zoo where she saw animals being moved around without frightening them (or risking injury to either animals and keepers), the taking of chimpanzee temperatures and giving injections, okapis which were trained to “chin target” a piece of pipe so they could have injections, and tigers offering their tails through the bars for blood samples to be taken. While this type of training could be criticised as not being true “choice” (as the animals are “lured” into “performing” for a reward), Pryor does state that during her visit, an African elephant became nervous and refused to offer her foot for trimming, vocalising and moving away instead. The keepers waited patiently until she chose to come back to the bars herself. This indicates some level of animal choice in the proceedings and potentially shows a positive cognitive bias in the elephant. This is similar to an observational study on Ethiopian village dogs who being wary of strangers, vocalised warnings when approached and avoided contact, but remained close by (Vernooij et al., 2009).

In 2015, Eileen Anderson cited a study on her blog (http://eileenanddogs.com) which used the terms “forced choice” and “free choice” in a study on pigeons (Catania & Sagvolden, 1980). Forced choice was defined as the only “choice” which led to a reward, with all other choices having no effect. In operant training (as above), “free choice” offers the opportunity to walk away, but only one choice leads to anything of value (e.g. positive reward). This should in effect be classed as “forced choice” but could also be seen as (free) “choice within a fixed list of options” (Palmer, 2010) as it can be argued that the option to walk away also provides some level of value. A better © Animal Jobs Direct 17 Updated: 21-06-2017 Advanced Diploma Canine Behaviour Management Module 12 Assessment Booklet understanding of free choice comes from Grisha Stewart’s book, Behaviour Adjustment Training (BAT) 2.0 (Stewart, 2016). BAT empowers dogs to make better choices (Olkoski, 2013), using distance and duration to keep the dog under his stress threshold. While remaining at this level, the dog can perform natural behaviours like sniffing and exploration, making his own decisions about where to go and what to do (within the confines of an extra-long lead). However, this technique remains “choice within limits” as he can only approach the stressor, if he remains under threshold.

Captive animals (including domestic dogs) have less choice than their wild cousins (Hosey, 2005 cited by Kurtycz, 2015) and this lack of control can lead to psychological damage like learned helplessness (Seligman, 1975 cited by Kurtycz, 2015). Enabling choices (whether forced or free) encourages a positive cognitive bias. Research indicates this can counter a negative outlook and help prevent learned helplessness, leading animal caretakers to find ways that give choice back to the animals (Shapiro & Lambeth, 2007). For example, researchers (e.g. Hopper et al., 2013; van Leewuen et al., 2015 cited by Kurtycz, 2015) have discovered that captive animals (for example chimpanzees) will work harder for and walk further for their preferred food if given a choice. Gorillas (when given a choice of environment) choose to spend more time in dense foliage and complex areas than out in the open (Ross et al., 2011; Stoiniski et al., 2001 cited by Kurtycz).

Other forms of environmental enrichment also encourage choice and appears to have positive benefits on cognitive bias, building resilience and reducing stress. A study on early enrichment of puppies in a research breeding colony (Hubrecht, 1995) found that by providing extra human interaction between 5 and 14 weeks, puppies were more likely to approach humans in later life. Shelter dogs given choices between inanimate (toys) and animate (humans and conspecifics) enrichment, more often chose social interactions (Pullen, 2011). When provided in shelter kennels, older dogs prefer to lie on raised platforms, rather than on the floor or in a bed that is on the floor (Feldhaus, 1980 cited by Belpedio, 2010). Citing Haug (2004), Belpedio also comments that exposure to novelty, including the provision of mentally stimulating toys, can offset stress levels in kennelled dogs and using positive reinforcement techniques also decreases fear and encourages the human-canine bond.

As more research is conducted on the similarities between human and non-human animal behaviour, and also the similarities between human-canine physiology and © Animal Jobs Direct 18 Updated: 21-06-2017 Advanced Diploma Canine Behaviour Management Module 12 Assessment Booklet neurology (e.g. Berns, 2012; Nagasawa et al., 2015), it is possible to extrapolate data from non-specific studies regarding stress, resilience and choice (or lack thereof) and form conclusions that may lead to (or aid) future canine research in this area.

Chapter 3: Research Methodology

A quantitative study was conducted on the behavioural effects of choice (using common forms of enrichment) on cognitive bias and its effect (if any) on resilience.

Enrichment improves welfare by encouraging decision-making and problem-solving skills. It also enables natural behaviour to be performed (for example, exploration and sniffing), reducing boredom and disruptive behaviour, and aids resilience building (McConnell, 2016; Young, 2016).

A quantitative study was chosen over a qualitative one as not only is the subject matter varied, exposure to respondents can be limited. The aim of the study was to analyse “general opinion” of the subject with a view that it may lead to more in-depth research in the future (which may contain qualitative studies).

This study was designed as an online survey, containing six multiple choice questions using the internet survey company, “Survey Monkey” (http://www.surveymonkey.com). It was aimed towards dog owners (including previous owners) and anyone who works as a professional in the canine field. As terminology can be problematic for non-professionals, two surveys were devised containing similar questions but worded appropriately for the intended audience (see Appendix 1 & 2).

In order to reach as many potential respondents as possible, the surveys were distributed across the social media platform “Facebook” (https://facebook.com/), using related groups of people, who were invited to complete the survey most relevant to them and encouraged to distribute them further. The targeted groups were initially chosen as the researcher is a member of them and they also promote positive training methods and good canine welfare. The initial groups included Canine Professionals (including behaviourists, trainers, groomers, rescue workers, dog walkers), a Canine Breed group and the researcher’s public Facebook page.

The study ran for 14 complete days, after which no further survey responses could be entered. No personal information was asked for on the surveys and all answers were anonymous, complying with UK GDPR regulations (http://ico.org.uk/).

Survey Limitations Quantitative surveys have limitations, using closed questions which have a limited scope of choices. They also depend on the researcher asking relevant questions using understandable terminology. Another limitation is that quantitative surveys require a reasonable number of respondents and results can only be generalised within the target group. Limitations of this particular survey include: the skill of the researcher in designing relevant questions which results in data that can either support the wider research cited in this thesis or provides evidence to contradict it. This can lead to potential researcher bias when designing the questions as they may “lead” the respondents into answering in a particular way, possibly skewing results; closed questions with limited answer options may either be too generalised or too limiting for the target audience, leading either to questions being ignored or respondents choosing random answers, which could also affect results needed for reliable analysis.

Chapter 4: Data Presentation

This research study was separated into two quantitative online surveys, and the survey data was collected over a 14-day period. The study was conducted to gain insight from anecdotal evidence on whether giving aspects of choice back to the dog (using recognised elements of environment enrichment), affects cognitive behaviour bias, builds resilience to anxiety-related stress and if the data supports this thesis, or contradicts it.

To gain usable data, one survey was aimed at people who work with dogs on a day to day basis (including behaviourists, trainers, groomers and dog walkers, etc.). The other was aimed at general owners (including previous owners). Both surveys contained six similar closed questions, appropriately worded for the target audience, with options to include additional items not covered by exiting answers.

Professional Survey (see Appendix 1) The questions were divided into three sections: 1. Any “decision-making” enrichment which is already used, including: a. Whether choices are offered in normal activities (for example, the freedom to sniff and explore when on a lead). b. Type of choices provided (for example, freedom to approach people/dogs or retire to a quiet place). 2. In their opinion, do they feel enrichment: a. Gives or removes elements of control back to dogs. b. Aids or restricts resilience in dogs by either promoting or forcing a specific cognitive bias on them. 3. Personal experience: a. Has the responder witnessed a change in anxiety-related behaviour (including escape, avoidance, displacement, destruction, aggression etc.), after offering choice-based enrichment (either positive or negative). b. In what capacity does the responder work with dogs.

There were 75 respondents to the professional survey. Figure 1 shows the demographic breakdown by profession and this is further broken down in Figure 2.

The “other” category is not required for this study data but can be found in Appendix 3 for completion.

Figure 1 Demographic based on Profession

Figure 2 Numerical breakdown of professional respondents

Owner Survey (see Appendix 2) The questions were divided into three sections: 1. Physical exercise in the form of walking: a. How is the dog normally walked? On-lead or off-lead. b. Does this form of exercise provide opportunities for “decision-making” (choice- based) enrichment (for example, in the form of sniffing and exploring on a long lead)? 2. Has the owner’s dog ever shown signs of anxiety-related behaviour (including reactive behaviour)? 3. Personal experience: a. Have the owners experience of providing choice-based enrichment (for example, quiet areas, exploration and sniffing opportunities, mentally challenging games etc.). b. What do they believe are the effects of providing choice-based enrichment on anxiety-related behaviour (positive or negative change)? c. Has the responder witnessed a change in confidence after providing choice- based enrichment (either positive or negative change)?

The owner survey received 170 completed entries and because of the varied demographic of people who own dogs, this data was expected to show diversity in the answers.

Chapter 5: Data Analysis & Discussion

Analysis of the survey data is based on percentages, calculated from the number of people who chose a specific answer. Each survey is analysed separately, and overall conclusions are formulated which either support or contradict the main premise of the thesis. It is possible to merge data from both surveys to create a larger sample; however, this is not needed for the research study.

Professional Survey Analysis This survey was completed by 75 people from various canine professions. Demographically, they were categorised as: • Behaviourists (34.67%) • Trainers (29.33%) • Dog Walkers (9.33%) • Veterinary Professionals (5.33%) • Groomers (4.00%) • Other Professional (17.33%)

Out of 75 respondents, 98.67% stated they provide choices in their activities, with 97.33% allowing dogs the to explore their surroundings (even when on a lead). 98.67% believe choice-based enrichment gives some control back to dogs, while 92.00% think it aids resilience (by promoting a positive cognitive bias). Overall, 94.67% of canine professionals who completed the survey said they had seen some change from a negative bias to a more positive one after using choice-based enrichment.

Professional Survey Data Figure 1 shows the percentage of respondents who stated they provide “choice-based” activities.

Figure 1

Figure 2 contains a breakdown of “choice-based” activities which are provided for dogs.

Figure 2

Figure 3 shows the percentage of professional respondents who believe enrichment aids resilience in dogs.

Figure 3

Figure 4 shows the percentage of respondents who state they have seen a change from a “negative bias” to a “positive bias” after introducing enrichment.

Figure 4

Owner Survey Analysis This survey was completed by 170 people and no demographic data was taken as it was not required for this study.

Out of 170 respondents, 98.82% stated their dog spends time sniffing on walks (including when walked on a lead). 48.24% of owners walk their dog off lead, with 35.29% walking dogs on a long lead. 69.41% of owners stated they have dogs that have shown signs of anxiety or reactive behaviour, with 66.47% noticing a positive change after the introduction of some form of enrichment. Overall, 85.29% of owners believe enrichment has a positive effect on dogs showing anxiety-related behaviour.

Owner Survey Data Figure 5 -shows the percentage of owners whose dogs sniff on walks.

Figure 5

Figure 6 contains a breakdown of the types of walks normally performed.

Figure 6

Figure 7 shows the percentage of owners whose dogs show or has shown previous reactive/anxious behaviour.

Figure 7

Figure 8 shows the breakdown of any changes seen by owners after introducing enrichment.

Figure 8

Figure 9 contains a breakdown of how owners believe enrichment affects dogs with anxious behaviour.

Figure 9

The full analysis report from both surveys can be found in Appendix 3, along with a sample of random individual responses.

Discussion

This study is based on anecdotal survey evidence provided by ordinary dog owners as well as people who are professionals in the canine field. Anecdotal evidence is often seen as unreliable in research studies as it has not been “scientifically verified” by researchers or conducted in laboratory conditions. However, it can also be called citizen science (“Citizen Science Alliance”) which uses collaborative research from the general public as a way to further science (“BBC Do Something Great”). As ethologist Marc Bekoff states, “… when we have a good number of stories that all point to certain conclusions, we shouldn’t toss them out as being ‘just-so stories’” (Bekoff, 2019). It has been previously stated in this thesis that there has been limited research conducted into the effects of “choice” in building resilience in dogs, leaving citizen science as a feasible way of gaining an overall insight, which can be verified by future in-depth scientific research studies.

Enrichment is known to improve the general welfare of animals by providing mental stimulation reducing boredom. Encouraging decision-making and problem-solving skills through “choice-based” enrichment (for example, natural behaviour including sniffing and exploration), aids resilience building (McConnell, 2016; Young, 2016). This study provides strong (anecdotal) evidence to support this belief, although the results show differences in how much effect enrichment may have (including demographic differences within professions). Using extrapolated survey data from both groups of respondents shows that overall (87.34%), both professional and non- professional people (who completed the surveys) overwhelmingly believe that the provision of enrichment has a positive effect on anxiety-related behaviour. This is likely to be caused by a change in outlook from a negative cognitive bias to a more positive one, probably owing to “choice-based” enrichment giving back elements of control. However, it is recommended that more in-depth scientific research is conducted to either support or refute this.

Data Limitations There are many limitations in the data collected for these surveys, which could result in researcher or responder bias: • The professional survey was only shared within the “positive behaviour/trainer” community, which skews the answers towards a positive result. However, it is assumed that non-positive professionals would be unlikely to complete the survey (owing to the nature of the content). • The surveys were not distributed to a specific number of people, meaning there is no data collected on the number of people who chose not to respond. • The people who responded may inadvertently be biased in their answers, either because the wording of the questions may “lead” to a specific bias and also because the type of people participating are more likely to answer in a particular way.

After taking into consideration potential biases in the surveys, these results still provide useful data, as they show (at the very least) that owners and professionals who practise positive canine welfare, believe that by allowing dogs to make choices within their environment, helps to create a positive outlook, which aids in building resilience.

Chapter 6: Conclusion

Evidence points to a split in the Canidae family approximately 100,000 years ago, when an evolutionary divergence (Darwen, 1895) occurred through mutations in the mitochondrial DNA. It is now believed by many scientists that this may have resulted in a group of canids becoming more inquisitive of new (novel) situations, possibly caused by a change in cognitive bias, which led to a more positive outlook in novel situations (Clegg, 2018). Those who remained wary evolved in the Grey Wolf (Canis lupus), but the inquisitive group began to explore more, becoming more tolerant to the presence of early humans, living on the edge of their settlements and eventually becoming the domesticated dog we know today (Canis lupus familiaris) (e.g. Coppinger, 2001; Joyce, 2013; Skogland, Ersmark et.al, 2015). The mechanisms of that early association are not known, but “choice” played a key role in the process, either by consciously evaluating possibilities and potential rewards (decision-making) or through unconscious innate behaviour patterns (Lorenz, 1950). This process can still be seen in free-ranging village dogs that are not domesticated but choose to remain close to humans (Ortolani, Vernooij & Coppinger, 2009).

Since that early association, the ability to make choices has almost been completely removed from dogs’ lives, with humans becoming the decision-makers and controlling most aspects of their existence (what and when to eat; where to sleep; when and how to exercise; how, when and who to interact with; when to procreate; and even when to eliminate waste). For many decades this was exacerbated by the erroneous belief that wolves (and by comparison dogs) lived in violent hierarchies (e.g., Schenkel; Mech, 1968 & 2000) leading to the belief that dogs needed to be subjugated and all elements of choice removed.

Studies show that “a lack of choice” can lead to stress, depression (e.g. Seligman, 1972; Lea & Osthaus, 2018), resulting in many dogs that have either become shutdown to their surroundings (McConnell, 2016) or are generally afraid of everything, incapable of making even basic decisions (such as stepping back from an impulsive and reactive behaviour). Lack of choice may also lead to an “over- attachment” to a socially bonded figure (for example, a caregiver), which can result in anxiety-related behaviour when isolated from them. This typically manifests as excessive vocalisations (whining, barking, howling), destructive tendencies and

© Animal Jobs Direct 33 Updated: 21-06-2017 Advanced Diploma Canine Behaviour Management Module 12 Assessment Booklet stereotypy behaviour (pacing, excessive grooming and self-mutilation etc.). Stress is often seen only in negative terms, but mild stress is necessary for learning (Michaels, 2014) and helps puppies to build resilience. This could be because they retain elements of control over their environment (Chaney, 2004), and are able to choose which aspects to interact with, which ultimately leads to confidence in exploring new things. Psychological and behavioural issues arise when choice is removed, and they are forced to interact.

There has been limited research conducted into the specific effects of enabling choice in dogs, but wider research comparing the similarities between animal species (and more specifically the physiological and neural similarities between humans and dogs), alongside a more detailed understanding of cognitive behaviour make it possible for data to be extrapolated across species and used to create hypotheses that form the basis for further research. For example, mutual oxytocin release in human-canine social bonding, is similar to that seen in mother-infant gazing (Kim et al., 2014; Jensen et al., 2017). When combined with research into the effects of oxytocin release and stress-related isolation (Gonzalez et al.; Barrett et al., 2015), this provides evidence that oxytocin production is important in developing resilience. This shows the benefits of consulting wider research and not being limited to just one area.

Choice is indirectly provided using environmental enrichment, which improves animal welfare and reduces anxiety-related behaviour. Mainly based on observations of animal behaviour in the wild (including village dogs), the focus for welfare has moved towards encouraging natural behaviours (such as sniffing and exploration), which increases decision-making. Training methods based on positive reinforcement (such as operant conditioning) also returns an element of choice, with studies conducted on captive zoo animals showing increased resilience, and a greater predisposition for exploring new situations (for example Pryor, 2003). However, while choice is involved (a reward is given for “choosing” the correct behaviour), it is not “free choice” but “forced choice” (Catania & Sagvolden, 1980) as only one behaviour results in a reward, with all other behaviours resulting in nothing. Free choice occurs between two or more options, each consisting of a positive value (Beresford & Sloper, 2008). If handled badly, forced choice has the potential to cause more anxiety as the dog may have to “override” his natural choice because he wants the reward. For example, an anxious dog “forces” himself to approach strangers because they have treats. Free choice occurs if the stranger throws treats away from themselves, enabling the dog to © Animal Jobs Direct 34 Updated: 21-06-2017 Advanced Diploma Canine Behaviour Management Module 12 Assessment Booklet choose whether to approach or not – he gets the treats either way. This removes all pressure, reducing anxiety.

There has been limited research into free choice, but the recent study by Duranton & Horowitz (2018) indicates that free choice (in the form of sniffing) encourages a more positive cognitive bias, aiding resilience (Clothier, n.d.; Stewart, n.d.; McConnell, 2016). This is an exciting area that requires further research.

As part of this thesis, two quantitative surveys were conducted to gain an insight into how owners and canine professionals perceived the behavioural effects of “choice- based” enrichment. Results showed 92% of canine professionals believed that enrichment which encourages canine decision-making increases resilience and over 85% of dog owners believe it has a positive effect on anxiety-related behaviour. As such these results support existing research and the premise of this thesis. There are various limitations with the research methodology and gathered data, not least that these surveys are classed as anecdotal evidence and are not scientifically verifiable. However, this does not mean that the results should be ignored, as collaborative research using anecdotal evidence can be used to get an overview of a specific area of interest that can be verified later by future scientific studies (“BBC Do Something Great”) and as ethologist Marc Bekoff states, “… when we have a good number of stories that all point to certain conclusions, we shouldn’t toss them out as being ‘just- so stories’” (Bekoff, 2019).

There was also a potential for research bias. The surveys were distributed among limited groups of “like-minded” people who may be tempted to give more positive answers and closed questions that may lead towards a specific answer, which could skew the results. This was mitigated somewhat by asking for the owner survey to be distributed as wide as possible to reduce this risk and questions worded in a neutral way. Taking all limitations into account, the results still provide quantifiable evidence to support this thesis, but further research is recommended to expand this study.

The results also identified other areas of potential interest that could be expanded upon. For example, demographic analysis based on profession. This could be used to target areas where choice may not be routinely used or identify where education could be incorporated to provide support and improve choice-based activities within certain professions. © Animal Jobs Direct 35 Updated: 21-06-2017 Advanced Diploma Canine Behaviour Management Module 12 Assessment Booklet

The nature of the human-dog relationship means that there are limited opportunities for dogs to make choices. However, if we can return some elements of control, it will promote a more positive outlook, help build resilience and reduce anxiety-related behaviour in our canine friends.

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Appendix 1: Survey Questions - Canine Professional

Appendix 2: Survey Questions (Owner)

Appendix 3: Full Survey Analysis & Sample Responses

Professional Survey Analysis

Professional Survey Sample Responses

Owner Survey Analysis

Owner Survey Sample Responses