Agitated honeybees exhibit pessimistic cognitive biases

Whether animals experience human-like emotions is controversial and of immense societal concern [1-3]. Because animals cannot provide subjective reports of how they feel, emotional state can only be inferred using physiological, cognitive, and behavioral measures [4-8]. In humans, negative feelings are reliably correlated with pessimistic cognitive biases, defined as the increased expectation of bad outcomes [9-11]. Recently, mammals [12-16] and birds [17-20] with poor welfare have also been found to display pessimistic-like decision making, but cognitive biases have not thus far been explored in invertebrates. Here, we ask whether honeybees display a pessimistic cognitive bias when they are subjected to an anxiety-like state induced by vigorous shaking designed to simulate a predatory attack. We show for the first time that agitated bees are more likely to classify ambiguous stimuli as predicting punishment. Shaken bees also have lower levels of hemolymph dopamine, octopamine, and serotonin. In demonstrating state-dependent modulation of categorization in bees, and thereby a cognitive component of emotion, we show that the bees' response to a negatively valenced event has more in common with that of vertebrates than previously thought. This finding reinforces the use of cognitive bias as a measure of negative emotional states across species and suggests that honeybees could be regarded as exhibiting emotions.     

No evidence for emotional empathy in chickens observing familiar adult conspecifics

The capacity of animals to empathise is of high potential relevance to the welfare of group-housed domestic animals. Emotional empathy is a multifaceted and multilayered phenomenon which ranges from relatively simple processes such as emotional matching behaviour to more complex processes involving interaction between emotional and cognitive perspective taking systems. Our previous research has demonstrated that hens show clear behavioural and physiological responses to the mild distress of their chicks. To investigate whether this capacity exists outside the mother/offspring bond, we conducted a similar experiment in which domestic hens were exposed to the mild distress of unrelated, but familiar adult conspecifics. Each observer hen was exposed to two replicates of four conditions, in counterbalanced order; control (C); control with noise of air puff (CN); air puff to conspecific hen (APC); air puff to observer hen (APH). During each test, the observer hens' behaviour and physiology were measured throughout a 10 min pre-treatment and a 10 min treatment period. Despite showing signs of distress in response to an aversive stimulus directed at themselves (APH), and using methodology sufficiently sensitive to detect empathy-like responses previously, observer hens showed no behavioural or physiological responses to the mild distress of a familiar adult conspecific. The lack of behavioural and physiological response indicates that hens show no basis for emotional empathy in this context.     

Anthropomorphism and 'mental welfare' of fishes

Anthropomorphism, the use of human characteristics as a foundation for interpreting behavior and mental capacities of animals, is a bias undermining our understanding of other species, especially species as evolutionarily distant from humans as fishes. Anthropomorphism is not justified by allusions to evolutionary continuity among vertebrates, because no living vertebrate was ever a descendant of humans, so none could have inherited human traits. Nonetheless, it has recently been claimed that fishes are capable of conscious experiences of pain and emotional feelings and that mental welfare is an important issue for fishes. This paper shows that the evidence supporting claims for experiences of pain or conscious emotions by fishes is conceptually and methodologically flawed. In addition, the paper shows that the natural history and behavior of diverse fish species is inconsistent with a presumption of human-like awareness. This behavioral evidence is in accord with neurobiological observations showing that fishes are very different from us and are unlikely to have a capacity for awareness of pain or emotional feelings that meaningfully resemble our own. The factors that are detrimental to fish welfare have been well delineated by valid, objective indicators of physiological and behavioral well-being. This knowledge should guide welfare decisions. An empirical and non-anthropomorphic examination of diverse fishes and their adaptations should be the foundation for welfare decisions that would be truly beneficial to fishes and humans alike.     

Linking fearfulness and coping styles in fish

Consistent individual differences in cognitive appraisal and emotional reactivity, including fearfulness, are important personality traits in humans, non-human mammals, and birds. Comparative studies on teleost fishes support the existence of coping styles and behavioral syndromes also in poikilothermic animals. The functionalist approach to emotions hold that emotions have evolved to ensure appropriate behavioral responses to dangerous or rewarding stimuli. Little information is however available on how evolutionary widespread these putative links between personality and the expression of emotional or affective states such as fear are. Here we disclose that individual variation in coping style predicts fear responses in Nile tilapia Oreochromis niloticus, using the principle of avoidance learning. Fish previously screened for coping style were given the possibility to escape a signalled aversive stimulus. Fearful individuals showed a range of typically reactive traits such as slow recovery of feed intake in a novel environment, neophobia, and high post-stress cortisol levels. Hence, emotional reactivity and appraisal would appear to be an essential component of animal personality in species distributed throughout the vertebrate subphylum.     

An integrative and functional framework for the study of animal emotion and mood

A better understanding of animal emotion is an important goal in disciplines ranging from neuroscience to animal welfare science. The conscious experience of emotion cannot be assessed directly, but neural, behavioural and physiological indicators of emotion can be measured. Researchers have used these measures to characterize how animals respond to situations assumed to induce discrete emotional states (e.g. fear). While advancing our understanding of specific emotions, this discrete emotion approach lacks an overarching framework that can incorporate and integrate the wide range of possible emotional states. Dimensional approaches that conceptualize emotions in terms of universal core affective characteristics (e.g. valence (positivity versus negativity) and arousal) can provide such a framework. Here, we bring together discrete and dimensional approaches to: (i) offer a structure for integrating different discrete emotions that provides a functional perspective on the adaptive value of emotional states, (ii) suggest how long-term mood states arise from short-term discrete emotions, how they also influence these discrete emotions through a bi-directional relationship and how they may function to guide decision-making, and (iii) generate novel hypothesis-driven measures of animal emotion and mood.     

Joyful by nature: approaches to investigate the evolution and function of joy in non-human animals

The nature and evolution of positive emotion is a major question remaining unanswered in science and philosophy. The study of feelings and emotions in humans and animals is dominated by discussion of affective states that have negative valence. Given the clinical and social significance of negative affect, such as depression, it is unsurprising that these emotions have received more attention from scientists. Compared to negative emotions, such as fear that leads to fleeing or avoidance, positive emotions are less likely to result in specific, identifiable, behaviours being expressed by an animal. This makes it particularly challenging to quantify and study positive affect. However, bursts of intense positive emotion (joy) are more likely to be accompanied by externally visible markers, like vocalisations or movement patterns, which make it more amenable to scientific study and more resilient to concerns about anthropomorphism. We define joy as intense, brief, and event-driven (i.e. a response to something), which permits investigation into how animals react to a variety of situations that would provoke joy in humans. This means that behavioural correlates of joy are measurable, either through newly discovered ‘laughter’ vocalisations, increases in play behaviour, or reactions to cognitive bias tests that can be used across species. There are a range of potential situations that cause joy in humans that have not been studied in other animals, such as whether animals feel joy on sunny days, when they accomplish a difficult feat, or when they are reunited with a familiar companion after a prolonged absence. Observations of species-specific calls and play behaviour can be combined with biometric markers and reactions to ambiguous stimuli in order to enable comparisons of affect between phylogenetically distant taxonomic groups. Identifying positive affect is also important for animal welfare because knowledge of positive emotional states would allow us to monitor animal well-being better. Additionally, measuring if phylogenetically and ecologically distant animals play more, laugh more, or act more optimistically after certain kinds of experiences will also provide insight into the mechanisms underlying the evolution of joy and other positive emotions, and potentially even into the evolution of consciousness.     

On-farm assessment of laying hen welfare: a comparison of one environment-based and two animal-based methods

Methods available to assess animal welfare at farm level are based on a range of welfare parameters, which can be divided into two categories, environment-based and animal-based parameters. The first category describes features of the environment and management, which can be considered prerequisites for welfare. The second category records animals’ responses to that particular environment and management more directly. Objective of this study was to validate a mainly environment-based method, the animal needs index (ANI), with animal-based methods: behavioural observations and feather condition scores (FCS). The study was conducted on 20 commercial laying hen farms, 10 farms with battery cages and 10 farms with deep litter systems. During a 1-day visit on each farm, ANI was assessed, FCS was scored, and behavioural observations were performed. Instantaneous scan sampling and continuous focal sampling were used to assess the time spent on different behaviours and the occurrence of event behaviours. Data from behavioural observations and FCS were reduced with principal factor analysis. This resulted in two factors for each method. Significant positive correlations were found between ANI, on the one hand, and ‘movement’ and ‘comfort’, two factors from behavioural observations, on the other hand. A significant negative correlation was found between ANI and ‘wing damage’ (from FCS). The results of this study show that ANI is valid and sensitive enough to show differences in animal welfare between housing systems, whereas differences in welfare within housing systems cannot be shown. In conclusion, ANI is an appropriate method for assessment of laying hen welfare on a large number of farms with different housing systems.     

The Way Humans Behave Modulates the Emotional State of Piglets

The emotional state can influence decision-making under ambiguity. Cognitive bias tests (CBT) proved to be a promising indicator of the affective valence of animals in a context of farm animal welfare. Although it is well-known that humans can influence the intensity of fear and reactions of animals, research on cognitive bias often focusses on housing and management conditions and neglects the role of humans on emotional states of animals. The present study aimed at investigating whether humans can modulate the emotional state of weaned piglets. Fifty-four piglets received a chronic experience with humans: gentle (GEN), rough (ROU) or minimal contact (MIN). Simultaneously, they were individually trained on a go/no-go task to discriminate a positive auditory cue, associated with food reward in a trough, from a negative one, associated with punishments (e.g. water spray). Independently of the treatment (P = 0.82), 59% of piglets completed the training. Successfully trained piglets were then subjected to CBT, including ambiguous cues in presence or absence of a human observer. As hypothesized, GEN piglets showed a positive judgement bias, as shown by their higher percentage of go responses following an ambiguous cue compared to ROU (P = 0.03) and MIN (P = 0.02) piglets, whereas ROU and MIN piglets did not differ (P > 0.10). The presence of an observer during CBT did not modulate the percentage of go responses following an ambiguous cue (P > 0.10). However, regardless of the treatment, piglets spent less time in contact with the trough following positive cues during CBT in which the observer was present than absent (P < 0.0001). This study originally demonstrates that the nature of a chronic experience with humans can induce a judgement bias indicating that the emotional state of farm animals such as piglets can be affected by the way humans interact with them.     

Friends with benefits: Social support and its relevance for farm animal welfare

Despite growing interest in promoting positive welfare, rather than just alleviating poor welfare, potential measures of good welfare, and means to provide it, have remained elusive. In humans social support improves stress-coping abilities, health, and promotes positive psychological welfare. Therefore, social support may be a key approach to promote positive physical and psychological welfare in farm animals. However, the roles of positive social behaviors and social support have been overlooked in comparison to negative social behaviors such as agonistic interactions. The benefits of social partners on an animal's stress coping abilities and welfare are yet poorly understood.The purpose of this paper is to review the protective or buffering effects of social support against stressful challenges and its potential implications for farm animal welfare. The biology of social support is first presented with its behavior, endocrine, autonomic and immune components. The major factors modulating the social support process are then synthesized. Research and implications for animal welfare in different farm species are discussed. Lastly, this review identifies research areas that especially deserve further attention in our effort to understand and implement social support in farm animal welfare.Social support could constitute one of the foundations for welfare researchers to leap from the absence of negative welfare to the provision of positive welfare and emotional experiences.     

Relationship between welfare and individual ranging behaviour in commercial free-range laying hens

Laying hens housed in free-range systems have access to an outdoor range, and individual hens within a flock differ in their ranging behaviour. Whether there is a link between ranging and laying hen welfare remains unclear. We analysed the relationships between ranging by individual hens on a commercial free-range layer farm and behavioural, physiological and health measures of animal welfare. We hypothesised that hens that access the range more will be (1) less fearful in general and in response to novelty and humans, (2) have better health in terms of physical body condition and (3) have a reduced physiological stress response to behavioural tests of fear and health assessments than hens that use the range less. Using radio frequency identification tracking across two flocks, we recorded individual hens’ frequency, duration and consistency of ranging. We also assessed how far hens ventured into the range based on three zones: 0 to 2.4, 2.4 to 11.4 or >11.4 m from the shed. We assessed hen welfare using a variety of measures including: tonic immobility, open field, novel object, human approach, and human avoidance (HAV) behavioural tests; stress-induced plasma corticosterone response and faecal glucocorticoid metabolites; live weight, comb colour, and beak, plumage, footpad, and keel bone condition. Range use was positively correlated with plasma corticosterone response, faecal glucocorticoid metabolites, and greater flight distance during HAV. Hens that used the range more, moved towards rather than away from the novel object more often than hens that ranged less. Distance ranged from the shed was significantly associated with comb colour and beak condition, in that hens with darker combs and more intact beaks ranged further. Overall the findings suggest that there is no strong link between outdoor range usage and laying hen welfare. Alternatively, it may be that hens that differed in their ranging behaviour showed few differences in measures of welfare because free-range systems provide hens with adequate choice to cope with their environment. Further research into the relationship between individual range access and welfare is needed to test this possibility.     

The welfare of fish

Our interactions with fish cover a wide range of activities including enjoying them as pets to consuming them as food. I propose that we confine the consideration of the welfare of fish to their physiology, and not join the discussion on whether fish can feel pain and suffering, as humans. A significant proportion of the papers on animal welfare center on whether non-human animals can feel pain, and suffer as humans. This is a question that never can be answered unequivocally. The premise of the present paper is that we have an ethical responsibility to respect the life and wellbeing of all organisms. Thus, we should concentrate on the behavioural, physiological, and cellular indicators of their well-being and attempt to minimize a state of stress in the animals that we have in our care or influence.     

Long-term exposure to unpredictable and uncontrollable aversive events alters fearfulness in sheep

Numerous studies have investigated the emotional effects of various acute, potentially alarming events in animals, but little is known about how an accumulation of emotional experiences affects fearfulness. Fearfulness is a temperament trait that characterizes the propensity of an individual to be frightened by a variety of alarming events. The aim of this study was to investigate a putative alteration of fearfulness in sheep repeatedly exposed to various aversive events. Forty-eight 5-month-old female lambs were used. Over a period of 6 weeks, 24 of them (treated group) were exposed daily to various unpredictable and uncontrollable aversive events related to predatory cues, social context and negative handling that can occur under farming conditions. The other 24 lambs (control group) were housed in standard farming conditions (predictable food distribution and group handling). Fearfulness (behavioural and physiological responses) was assessed before and after the treatment period by subjecting the lambs to three standardized tests: individual exposure to suddenness and then to novelty in a test arena, and group exposure to a motionless human in the home pen. As biomarkers of stress, leukocyte counts, heart rate and cortisol concentrations were measured in the lambs in their home pens. Before the treatment, the emotional responses of the groups did not differ. After the treatment, treated lambs approached the human less often, had less contact with the novel object and vocalized more than controls in individual tests, suggesting that long-term exposure to unpredictable and uncontrollable aversive events increases subsequent fearfulness in sheep. In addition, treated lambs had lower leukocyte counts, heart rate and cortisol levels, pointing to a chronic stress state. These findings suggest that increased fearfulness may be used as a sign of chronic stress in farm animals.     

Behavioural and physiological stress responses to handling in wild guanacos

Both ethology and physiology can provide insights about stress conditions in wild animals during handling. Lama guanicoe (guanaco) is the major large herbivore inhabiting arid zones in Argentina. Since 2005, the Payún Matrú Cooperative, a business established and run by native people, has captured and handled guanacos for shearing at Payunia Reserve, Mendoza Province, Argentina, to market the species’ fibre for clothing and other products. The aim of our study was to evaluate the behavioural and physiological stress responses to handling of wild guanacos during these shearing activities. We evaluated stress conditions in guanacos by monitoring the frequency of agonistic behaviour in the holding corrals, following capture, the rate of vocalisation and agonistic behaviour during handling, and by estimating cortisol levels in handled animals. Crowding increased agonistic behaviour; this appeared to be related to dominance conflicts between males in the corrals. Time of corralling increased rate of agonistic behaviour and vocalisations during handling. The rate of behavioural stress responses was negatively related to cortisol levels in males; which may be due to animal fatigue or because behavioural stress responses may help mitigate physiological stress responses. Incorporating our results into animal welfare practices could help reduce stress conditions in wild guanacos. Our results suggest that both behavioural and physiological responses are important measures of stress in handled animals, and that behavioural stress responses cannot be used as a simple surrogate for glucocorticoid levels.     

Understanding others: Emotion recognition in humans and other animals

Emotion recognition represents the ability to encode an ensemble of sensory stimuli providing information about the emotional state of another individual. This ability is not unique to humans. An increasing number of studies suggest that many aspects of higher order social functions, including emotion recognition, might be present in species ranging from primates to rodents, indicating a conserved role in social animals. The aim of this review is to examine and compare how emotions are communicated and perceived in humans and other animals, with the intent to highlight possible new behavioral approaches and research perspectives. We summarize the evidence from human emotion recognition, and latest advances in the development of nonhuman animal behavioral tests, using or implying the use of this cognitive function. The differential implication of sensory modalities used by animals to communicate and decipher emotional states is also discussed. The opportunity to measure emotion recognition abilities in rodents may allow us to better identify the neural mechanisms mediating this complex function, thus promoting the development of new intervention strategies for several neuropsychiatric disorders characterized by social cognitive dysfunctions.     

Factors affecting the Human Attribution of Emotions toward Animals

ABSTRACT

Attribution of emotions to animals can affect human–animal interactions and dictate animal welfare laws. However, little is known about the factors that influence these attributions. We investigated the effect of belief in animal mind, pet ownership, emotional intelligence, eating orientation, and gender on the attribution of different emotions to a variety of species, from different taxonomic classes, considered as Pet, Use (e.g., used for food, experimentation), or Pest animals. Three hundred and forty-seven participants, aged between 16 and 65 years, completed a questionnaire that measured their belief in the capacity for animals to experience seven primary and secondary emotions. The results showed that attribution of emotions to animals is inconsistent. The ambiguity appears to hinge, in part, upon an animal's functional category and their perceived place in the commonly supposed, though inaccurate, linear hierarchy of species. Nonetheless, the wide range of emotions that were attributed to all species highlights the complex and potentially disorganized thoughts that humans have concerning animals. Belief in animal mind was found to be the strongest and only predictor of emotion attribution to animals in general, but is probably because both are part of the same underlying construct. Ownership of some species—rabbits, horses, rodents and birds—mediated the emotions attributed to that particular species. We conclude that ambiguous attitudes influence the standards of welfare for animals used by humans and that the dichotomous attitudes permit exploitation and welfare violations against animals. Greater understanding of emotion attribution has the potential to improve humane education methods, and suggestions for future research are made.     

Pain and Pessimism: Dairy Calves Exhibit Negative Judgement Bias following Hot-Iron Disbudding

Pain is defined as an unpleasant sensory and emotional experience associated with actual or potential tissue damage, but emotional states are difficult to directly assess in animals. Researchers have assessed pain using behavioural and physiological measures, but these approaches are limited to understanding the arousal rather than valence of the emotional experience. Cognitive bias tasks show that depressed humans judge ambiguous events negatively and this technique has been applied to assess emotional states in animals. However, limited research has examined how pain states affect cognitive processes in animals. Here we present the first evidence of cognitive bias in response to pain in any non-human species. In two experiments, dairy calves (n = 17) were trained to respond differentially to red and white video screens and then tested with unreinforced ambiguous colours in two or three test sessions before and two sessions after the routine practice of hot-iron disbudding. After disbudding calves were more likely to judge ambiguous colours as negative. This ‘pessimistic’ bias indicates that post-operative pain following hot-iron disbudding results in a negative change in emotional state.     

Oxytocin receptor and vasopressin receptor 1a genes are respectively associated with emotional and cognitive empathy

Empathy is the ability to recognize and share in the emotions of others. It can be considered a multifaceted concept with cognitive and emotional aspects. Little is known regarding the underlying neurochemistry of empathy and in the current study we used a neurogenetic approach to explore possible brain neurotransmitter pathways contributing to cognitive and emotional empathy. Both the oxytocin receptor (OXTR) and the arginine vasopressin receptor 1a (AVPR1a) genes contribute to social cognition in both animals and humans and hence are prominent candidates for contributing to empathy. The following research examined the associations between polymorphisms in these two genes and individual differences in emotional and cognitive empathy in a sample of 367 young adults. Intriguingly, we found that emotional empathy was associated solely with OXTR, whereas cognitive empathy was associated solely with AVPR1a. Moreover, no interaction was observed between the two genes and measures of empathy. The current findings contribute to our understanding of the distinct neurogenetic pathways involved in cognitive and emotional empathy and underscore the pervasive role of both oxytocin and vasopressin in modulating human emotions.     

Hope for the Best or Prepare for the Worst? Towards a Spatial Cognitive Bias Test for Mice

Cognitive bias, the altered information processing resulting from the background emotional state of an individual, has been suggested as a promising new indicator of animal emotion. Comparable to anxious or depressed humans, animals in a putatively negative emotional state are more likely to judge an ambiguous stimulus as if it predicts a negative event, than those in positive states. The present study aimed to establish a cognitive bias test for mice based on a spatial judgment task and to apply it in a pilot study to serotonin transporter (5-HTT) knockout mice, a well-established mouse model for the study of anxiety- and depression-related behavior. In a first step, we validated that our setup can assess different expectations about the outcome of an ambiguous stimulus: mice having learned to expect something positive within a maze differed significantly in their behavior towards an unfamiliar location than animals having learned to expect something negative. In a second step, the use of spatial location as a discriminatory stimulus was confirmed by showing that mice interpret an ambiguous stimulus depending on its spatial location, with a position exactly midway between a positive and a negative reference point provoking the highest level of ambiguity. Finally, the anxiety- and depression-like phenotype of the 5-HTT knockout mouse model manifested - comparable to human conditions - in a trend for a negatively distorted interpretation of ambiguous information, albeit this effect was not statistically significant. The results suggest that the present cognitive bias test provides a useful basis to study the emotional state in mice, which may not only increase the translational value of animal models in the study of human affective disorders, but which is also a central objective of animal welfare research.     

Effects of predictability on the welfare of captive animals

Variations in the predictability of a stressor have pronounced effects on the behavioural and physiological effects of stress in rats. It is reasonable to expect that variations in the predictability of husbandry routines thought to be aversive to animals might have similar effects on stress indices. Similarly, variations in the predictability of positive events, of which feeding is an obvious example, may affect welfare. This review examines the behavioural and physiological effects of the predictability of aversive and appetitive stimuli, and the application of experimental findings to animal husbandry in practice. It is argued here that two distinct but overlapping types of predictability exist. ‘Temporal’ predictability describes whether an event occurs at fixed or variable intervals, whereas ‘signalled’ predictability relates to the reliability of a signal preceding the event. This review examines the effects of each of these types of predictability in relation to positively and negatively perceived events, and examines the link between predictability and control. Recommendations are made for relatively simple and inexpensive modifications to husbandry routines that may be easy to incorporate into the schedules of busy staff yet could have a profound impact on the welfare of animals in their care.     

Animal temperament and human disturbance: implications for the response of wildlife to tourism

Studies on the response of wildlife to human disturbance generally focus on demographic changes or on physiological and behavioural modifications directly related to stress response. Yet fewer studies have explored whether the distribution of individual animals in response to human disturbance is influenced by temperament. Temperament represents the consistency of responses of individuals in reaction to novel or challenging situations. Individuals are thus assumed to express highly consistent behaviour-hormonal response under specific stress conditions. In this study, we investigate the relations between exploration, grooming-scanning continuum, emotionality, and docility of individual Eastern chipmunks (Tamias striatus) and location of their burrow respective to frequentation by humans. We then assess the relationship between cortisol accumulated in the hair and both temperament and frequentation by humans. Explorative or docile chipmunks were more common in frequented areas. Hair cortisol increased with docility, but was not related to human frequentation. These results indicate that temperament may cause animals to distribute themselves in a non-random way in response to human disturbance. Integrating temperament into studies of the stress response of wildlife to humans could therefore help us understand the impact of tourism on wildlife.