EMPATHY TOWARDS NON-HUMAN ANIMALS: ITS ROLE IN EMOTION RECOGNITION, VETERINARY MEDICINE AND ANIMAL HOARDING DISORDER.

Background: empathy has been defined as a vicarious affective response that arises from attending another individual’s emotional experience and is more appropriate to another’s situation than one’s own. It is a complex and multidimensional psychological process, which involves both emotional and cognitive components: the former refers to affective resonance with others’ emotions and the generation of an appropriate emotional response, while the latter includes abilities such as recognizing and understanding another’s emotions distinguishing between self and others, and perspective taking. Empathy has also visible effects on behaviour, leading either to prosocial behaviour, namely the effort to alleviate the distress of the others and to promote their welfare, or to defensive behaviours and strategies of affective control due to an excessive personal distress. Although empathy towards humans has been extensively studied, only a few studies have focused on empathy towards non-human animals, which is considered as a psychological side effect of empathy towards people, triggered by animal signals or behaviour that resemble those that elicit empathy among humans. There is evidence that empathy towards humans is related to important social skills, such as emotion recognition and prosocial behaviour, therefore empathy is regarded as an important aspect not only in daily social interactions but also in caring professions; in particular, the relevance of empathy as a professional skill has been extensively studied and underlined in human health professionals, with studies proving a decline in empathy towards people during medical education. Furthermore, given the relevance of empathy towards people, its impairment is considered a sign of psychopathology and characterizes a number of mental disorders such as antisocial, borderline and narcissistic personality disorders and autism spectrum disorders. Although some studies have suggested that empathy towards animals may be related to the way in which people interpret animal behaviour and it may be influenced by particular job and educational contexts and mental disorders, these themes are still understudied. Yet, a deepen analysis of these issues could have important consequences both for animal and human welfare: in particular, recognition of animal emotions is crucial for their well-being and, as in human health professions, empathy towards animals may be central to the role of veterinarians, especially in companion animal practice. Furthermore, the new edition of the diagnostic and statistical manual of mental disorders includes the animal hoarding disorder, which is a poorly understood mental disease, likely related to empathy towards animals. Aim of the project: the main aim of this work is to investigate three important and little studied aspects of empathy towards non-human animals, namely: 1. its relation to animal emotion recognition, 2. its status in and the way in which it may be affected by veterinary education and practice and 3. its potential role in animal hoarding disorder. Moreover, since a condition to feel empathy towards animals is their ability to feel emotions, I have also briefly reviewed the scientific literature on animal emotions, which evidences the need to combine behavioural and physiological indexes to study them. Therefore, I carried out two studies aimed at investigating the possibility to use novel and non-invasive tools to study animal emotions, along with behavioural and traditional physiological measures. The dog (Canis familiaris) has been chosen as a model both for studying animal emotions and human ability to recognize them, since this species has a long history of domestication, lives in strict contact with humans and its ability to emotionally communicate with them has been widely proved. Results: six studies and one book I have co-authored are presented in this dissertation, which are the results of the work carried out in the last three years at the Canis sapiens – Comparative cognition & Human- Animal Interaction – Lab of the University of Milan (Department of Physiopathology and Transplantation, section of Neuroscience). These studies cover three major themes, which are described in three different chapters, following an introductive section. Three studies and the book have already been published, while the others are in press or have been submitted to international scientific journals. Chapter 1: Introduction - An overview of human empathy towards humans and other animals. The chapter offers an overview of the concept of empathy and the results of the main studies carried out on empathy towards humans and towards animals. Given the importance of empathy towards people in recognizing human emotions and in predicting prosocial behaviour towards conspecifics, the importance of studying empathy towards animals in order to improve both animal and human welfare is discussed, with particular interest for its potential role in animal emotion recognition, veterinary medicine and animal hoarding disorder. Chapter 2: Recognizing emotions in non-human animals. This chapter reviews the scientific evidence about the ability of non-human animals, at least mammals, to feel a number of basic emotions, such as happiness, sadness, fear, anger, surprise and disgust. Furthermore findings about human ability to recognize animal emotions are discussed, underlining the lack of consistent evidence of human ability to recognize animal visual emotional signals, such as body postures and facial expressions. A brief section examines the suitability of the dog (Canis familiaris) as a model for studying both animal emotions recognition and animal emotions, discussing also the validity of behavioural clues alone to assess dog emotions, evidencing the need to find more reliable and objective tools. Finally I present my research activity in this area. - Study 1: “Expertise, empathy, gender and the recognition of dog (Canis familiaris) emotional facial expressions”. This work investigated the relation between expertise, empathy and gender and accuracy in the recognition of dog emotional facial expressions. A group of experts (veterinary behaviourists and dog trainers) and 3 groups of participants differing in their experience with dogs (veterinarians, dog owners and people who had never owned a dog) classified 21 photographs of a dog’s facial expressions, realized under standardized and behaviourally defined conditions aimed at activating in the dog the six basic emotions already described in humans (i.e., happiness, surprise, sadness, fear, anger and disgust). We found that experts in dog behaviour were not particularly accurate in identifying the dog’s emotional states and correctly recognized only a limited number of the dog’s emotions. Interestingly we also found a clear effect of the level of expertise on the recognition of some of the dog’s expressions, but we didn’t find any effect of empathy or gender, suggesting an experience-dependent mechanism at the basis of inter-specific emotion recognition from facial expressions. The possibility that some antecedent stimuli used to elicit emotions in the dog could not be fully appropriate and that the photographs we used lacked ecological validity were also discussed. - Study 2: “Hot dogs”: Thermography in the assessment of stress in dogs (Canis familiaris) - A pilot study. This study evaluated for the first time the usefulness of Infra-Red Thermography (IRT) to assess dogs’ emotional responses to an unpleasant and stressful event. A sample of 14 healthy adult dogs was observed during a standardized veterinary examination, carried out by an unfamiliar veterinarian in the presence of their owners. The dogs’ behaviours and eye temperatures were recorded before the start of the veterinary visit, during, and after the clinical examination. Interestingly, the dogs showed an increase in eye temperature during the examination phase compared with both pre- examination and post-examination phases, despite a concomitant significant decrease in their level of activity. Results suggested that IRT may represent a useful tool to investigate emotional psychogenic stress in dogs. - Study 3: “How good is this food? A study on dogs’ emotional responses to a potentially pleasant event using Infra-Red Thermography”. In this study, IRT was used in combination with behavioural measures, heart rate (HR) and heart rate variability (HRV) to investigate dogs’ emotional responses to a potentially pleasant event: receiving highly palatable treats from the owner. Nineteen adult pet dogs, 8 females and 11 males, were tested and their eye temperature, heart rate, heart rate variability and behaviour were recorded during a 30 minutes test consisting of three 10 min consecutive phases: Phase 1 (Baseline), Phase 2 (Feeding), namely positive stimulation through the administration of palatable treats and Phase 3 (Post-feeding) following the positive stimulation. The dogs’ eye temperature and mean HR significantly increased during the positive stimulation (Phase 2) compared with both Baseline and Post-feeding phases, despite a concomitant significant decrease in dogs’ level of activity. During the stimulation with food, the dogs engaged in behaviours indicating a positive emotional state, such as being focused on the treats and showing an increase in tail wagging. However, HRV increased only in Phase 3, after the positive stimulation occurred. Overall results pointed out that IRT may be a useful tool in assessing emotional states in dogs in terms of arousal but fails to discriminate emotional valence, whose interpretation cannot disregard behavioural indexes. The role of HRV in understanding emotional valence and the actual emotional meaning of food treats were also discussed. Chapter 3: Exploring the field of veterinary medicine: the importance of empathy towards animals. This chapter presents a brief introduction of the role of empathy towards animals in animal-related jobs, highlighting how both empathy towards animals and towards people are two central aspects of veterinary medicine, especially in companion animal practice, where they are respectively related to animal welfare and clients’ satisfaction. Although studies carried out in other countries proved that veterinary education may have a negative impact on empathy towards animals, in particular in male students, little was known about the effect of veterinary practice on empathy. The aim of this chapter is presenting my research activity in this area. - Study 4: “Empathy towards animals and belief in animal-human-continuity in Italian veterinary students”. In the present cross-sectional study we used the Animal Empathy Scale and the Human-Animal Continuity Scale to investigate empathy towards animals and beliefs in animal-human continuity in a sample of first year (n = 131) and last year (n = 158) veterinary students of the University of Milan (Italy). Results revealed a difference in empathy towards animals, with first year students scoring significantly higher than those at the end of their academic training. This variation in empathy over time emerged in both male and female students, however females always had higher scores in empathy than males. Moreover, students at the end of their university education reported a more instrumental attitude toward animals, more pronounced in males than in females. Similarly, there was a difference in the perception of continuity between human and animals which was more evident in males, with first year students scoring higher than fifth year students in some items. Results are discussed in relation to previous studies carried out in other countries and, given the importance of empathy in the veterinary profession, potential reasons underlying its apparent decrease are considered. This is the first study on empathy in veterinary students carried out in Italy. - Study 5: “Empathy towards animals and people in a sample of Italian vets: the role of gender and length of career”. The aim of this study was to investigate empathy towards animals and humans in veterinarians, assessing whether and to what extent they are influenced by variables such as gender and length of career. We used the Animal Empathy Scale to assess empathy towards animals and the Empathy Quotient to assess empathy towards people in a sample of 107 vets, practicing in veterinary clinics in Milan area and working mainly with dogs and cats. Results revealed an effect of gender on empathy towards animals, with women scoring higher than men, and an effect of length of career on empathy toward people, with more experienced vets scoring higher than their younger colleagues. This is the first study in the literature evaluating both empathy towards animals and people in vets working in small animal practice and suggests a positive profile of veterinarians, reporting themselves to be empathic both towards animals and people, meeting the expectations of society and likely linked to the feminization of veterinary medicine. Given the role of empathic concern in caring for animals and for clients’ satisfaction, but also as a risk factor for burnout in caring professions, further studies are needed. Chapter 4: The Animal Hoarding Disorder: a mental disorder related to anomalies in empathy towards animals? A number of mental disorders, such as antisocial, borderline and narcissistic personality disorders and autism spectrum disorders, entails a deficit in empathy towards people, to such an extent that a new classification of these psychopathologies as “empathy-related disorders” has been proposed. So far, anomalies in empathy towards animals have never been specifically related to any mental disorders and its impairment is mentioned only among the diagnostic criteria for conduct disorder, as “cruelty to animals”. Yet, the last edition of the diagnostic and statistical manual of mental disorders (DSM-5) includes for the first time “animal hoarding”, considering it as a special manifestation of “hoarding disorder”. The crucial feature of animal hoarding is the failure to provide proper care for animals and to recognize their suffering, therefore some authors considered it as a manifestation of “pathological altruism”, which is rooted in empathy anomalies. In Italy, animal hoarding is almost unknown, although media and press often report cases of people who hoard animals resulting in animal abuse, but interpret them as animal cruelty or, conversely, as “too much love for animals”. In this chapter I present the first review on animal hoarding, written in Italian before the Italian edition of DSM-5 was published, with the aim to inform Italian mental health professionals about this phenomenon; furthermore, I report a brief summary of a book on animal hoarding that I have co-authored and that has recently been published. - Study 6: “Animal hoarding: lifestyle, animal abuse or psychopathology? A critical review of the literature”. This study reviews the international scientific literature on animal hoarding, considering how for a long time it has been regarded as a “lifestyle”, then as a form of animal maltreatment, but only recently as a mental disorder. The aim of this review was to describe the main features of animal hoarding and to introduce the most frequent hypotheses about its aetiology, with particular reference to Hoarding Disorder and to the role of trauma; moreover, strengths and weaknesses of current interventions were analyzed, in order to promote an interdisciplinary approach to the problem. Special emphasis was given to the importance of understanding animal hoarding behaviour in the light of the normal human-animal bond, suggesting new research directions which consider aspects such as attachment and empathy toward animals. - Book: “Una pericolosa arca di Noè: L’accumulo di animali tra cronaca e ricerca” (A dangerous Noah’s ark: animal hoarding between press reports and scientific research), published by Cosmopolis. With the contribution of experts in psychology, psychiatry, ethology veterinary medicine and law, the book deals with themes such as the diagnostic criteria of animal hoarding, the underlying psychological and neuropsychological mechanisms, its relation with animal abuse and normal human-animal bond, legal consequences of animal cruelty and the possibility to cure and rehabilitate both people and animals. Furthermore, three main categories of animal hoarders are described and the phenomenon of “lager shelters” is discussed as a possible consequence of this mental disorder. This is the first essay on animal hoarding disorder published in Italy and analyses this issue in the light of the international scientific literature and through the narration of cases derived from the Italian press. Conclusions highlight the need for further research on animal hoarding, aimed at investigating its prevalence and aetiology and the efficacy of psychotherapy in its treatment. Conclusions: the work presented in the current thesis is a starting point for the investigation of empathy towards animals and its role in animals’ emotions recognition, veterinary medicine and animal hoarding disorder, mirroring the available literature on empathy towards humans. In fact, there is evidence that empathy is related to the recognition of human emotional facial expressions, but represents a controversial aspect of human medicine, since it declines during medical training but it is considered an important skill in medical practice. Furthermore, a number of mental disorders are related to deficits in empathy towards people. Since research on the recognition of animal emotions from visual signals is still very limited, we chose to focus on dog’s (Canis familiaris) emotions because of its long history of domestication and its high diffusion in human society. Results suggest that empathy towards animals may not be related to the ability to recognize animal emotions from facial expressions (at least with respect to the dog), which seems to be an experience-dependent cognitive mechanism. Furthermore, we noticed a lack of agreement even among experts in dog’s behaviour, at least for some emotions, and this result is in line with those of studies that criticized the reliability of behavioural clues to investigate emotions in animals, and thus also in dogs, suggesting to combine them with physiological measures. The results on the use of changes in dogs’ eye temperature, detected trough Infra-Red Thermography, to investigate emotions in dogs showed that IRT could be a useful tool to assess emotional arousal but not to discriminate emotional valence (i.e., positive or negative), whose interpretation cannot disregard behavioural indexes. With respect to the role of empathy towards animals in veterinary medicine, results seem to parallel those emerging for empathy towards people in human medicine: in fact, we found that last-year veterinary students were less empathic than their first year colleagues, suggesting a decline in empathy towards animals during veterinary education similar to that observed in medical students. Furthermore, examining for the first time the effect of length of career in veterinary companion-animal practice on both empathy towards animals and people, we found that empathy towards people was higher among older professionals, suggesting a role of clinical practice in improving empathy, as reported in a previous study on physicians. Interestingly, we found that, like empathy towards people, also empathy towards animals is affected by gender, as females are usually more empathic than males. Given the on-going process of feminization of the veterinary professions, taken together these findings offer a positive profile of veterinarians, who seem to be able to show empathy both towards animal-patients and human-clients, meeting the expectations of society. Finally, like empathy towards people, empathy towards animals seems to be vulnerable to anomalies related to mental disorders: in particular, the review of the available international literature shows that aberrations of empathy towards animals seems to be a crucial aspect of animal hoarding disorder.