Michael T Mendl

Measuring emotional processes in animals: the utility of a cognitive approach.

Contemporary researchers regard emotional states as multifaceted, comprising physiological, behavioural, cognitive and subjective components. Subjective, conscious experience of emotion can be inferred from linguistic report in humans, but is inaccessible to direct measurement in non-human animals. However, measurement of other components of emotion is possible, and a variety of methods exist for monitoring emotional processes in animals by measuring behavioural and physiological changes. These are important tools, but they have limitations including difficulties of interpretation and the likelihood that many may be sensitive indicators of emotional arousal but not valence-pleasantness/unpleasantness. Cognitive components of emotion are a largely unexplored source of information about animal emotions, despite the fact that cognition-emotion links have been extensively researched in human cognitive science indicating that cognitive processes-appraisals of stimuli, events and situations-play an important role in the generation of emotional states, and that emotional states influence cognitive functioning by inducing attentional, memory and judgement biases. Building on this research, it is possible to design non-linguistic cognitive measures of animal emotion that may be especially informative in offering new methods for assessing emotional valence (positive as well as negative), discriminating same-valenced emotion of different types, identifying phenotypes with a cognitive predisposition to develop affective disorders, and perhaps shedding light on the issue of conscious emotional experiences in animals.

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.

Performing under pressure: stress and cognitive function

Abstract The way in which cognitive functioning is affected by stressors is an important area of research for applied ethologists because stress caused by captive conditions may disrupt cognitive processes and lead to welfare and husbandry problems. Such problems may be minimised through an understanding of the links between stress and cognition. The effects of stress on cognitive function have been studied in disciplines ranging from human perceptual psychology to animal neuroscience. The aim of this paper is to provide an introduction to this research, focusing on the effects of stressors on attention, memory formation and memory recall. Findings from such a diverse literature with little apparent inter-disciplinary communication are inevitably complex and often contradictory. Nevertheless, some generalities do emerge. The idea that an inverted U-shaped relationship exists between an individuals state of stress or arousal and its ability to perform a cognitive task effectively, the so-called Yerkes–Dodson law, is commonly encountered. The law has limited explanatory value because it is unlikely that different stressors act on cognitive function via the same intervening, non-specific state. Furthermore, the law only provides a very general description of the relationship between stress and cognitive function. Empirical research on attention and memory processes reveals more specific findings. Stressors appear to cause shifts, lapses and narrowing of attention, and can also influence decision speed. These processes may be viewed as serving an adaptive role helping the animal to search for and scrutinise a source of danger. There is conflicting evidence as to whether hormones involved in the hypothalamic–pituitary–adrenal stress response play a part in these processes. These hormones and those involved in the sympathetic-adrenomedullary stress response do appear to play an important role in memory formation. Low or moderate concentrations of circulating glucocorticoids and catecholamines can enhance memory formation, while excessively high or prolonged elevations of these hormones can lead to memory disruption. The effects of stressors on memory recall are less clear. There is evidence for disruptive effects, and for facilitatory effects indicating state-dependent memory recall; events experienced under conditions of high arousal may be best recalled under similar conditions. Applied ethologists have the opportunity to extend work in this area, which often involves studies of single stressors/stress hormones acting in isolation and limited measures of cognitive function, by focusing on real-life husbandry stressors encountered by captive animals. This will yield fundamental information which also has direct relevance to animal welfare and management issues.

Physiological and reproductive correlates of behavioural strategies in female domestic pigs

Abstract Thirty-seven pregnant primiparous domestic pigs, Sus scrofa , were introduced into a large indoor pen. The pigs were divided into three groups according to their ability to displace others in agonistic interactions and the behavioural characteristics of these groups were investigated. High Success pigs were able to displace at least as many individuals as displaced them. They were characterized by low levels of inactivity, high involvement in social interactions and high aggression. No Success pigs never displaced any other pig and were most inactive, least aggressive and showed low involvement in social interactions. Low Success pigs were able to displace some pigs but were more often displaced themselves. They were aggressive, despite their relative lack of success, and experienced the highest levels of aggression from and displacement by others. During the first month in the group, High Success pigs gained the most weight. Low Success pigs had the highest basal levels of salivary cortisol and showed the highest peak cortisol levels in response to an adrenocorticotrophic hormone challenge test. At the first parturition, Low Success pigs produced the lowest weight of piglets born alive. Hence there were more adverse effects associated with being aggressive and often displaced than with being aggressive and usually winning, or being unaggressive and involved in few interactions. The strategy used to cope with the social environment may be as important as the success achieved in agonistic interactions, at least in terms of consequences for physiology and reproduction.

Assessing the 'whole animal': a free-choice - profiling approach

The qualitative assessment of animal behaviour summarizes the different aspects of an animals dynamic style of interaction with the environment, using descriptors such as ‘confident’, ‘nervous’, ‘calm’ or ‘excitable’. Scientists frequently use such terms in studies of animal personality and temperament, but, wary of anthropomorphism, are reluctant to do so in studies of animal welfare. We hypothesize that qualitative behaviour assessment, in describing behaviour as an expressive process, may have a stronger observational foundation than is currently recognized, and may be of use as an integrative welfare assessment tool. To test this hypothesis, we investigated the inter- and intraobserver reliability of spontanous qualitative assessments of pig, Sus scrofa, behaviour provided by nine naive observers. We used an experimental methodology called ‘free choice profiling’ (FCP), which gives observers complete freedom to choose their own descriptive terms. Data were analysed with generalized Procrustes analysis (GPA), a multivariate statistical technique associated with FCP. Observers achieved significant agreement in their assessments of pig behavioural expression in four separate tests, and could accurately repeat attributing expressive scores to individual pigs across these tests. Thus the spontaneous qualitative assessment of pig behaviour showed strong internal validity under our controlled experimental conditions. In conclusion we suggest that qualitative behaviour assessment reflects a ‘whole animal’ level of organization, which may guide the intepretation of behavioural and physiological measurements in terms of an animals overall welfare state.

A method for rating the individual distinctiveness of domestic cats

Abstract Fourteen adult female domestic cats were watched by two observers for 3 months. Ratings of 18 aspects of each cats behavioural style were obtained independently from each observer. Correlations between observers were statistically significant for 15 of the 18 aspects and seven of the correlation coefficients were greater than 0·7. The ratings were compared with results of direct recording methods, where equivalent measures were available and, in five out of six cases, the results of the ratings and direct methods were significantly correlated. The rating method is, therefore, generally reliable and can be adequately validated. Some assessments of observer ratings which are not obviously and easily related to direct recordings may prove particularly useful in developmental studies of alternative modes of behaviour and the origins of individual differences.

Timing and causes of piglet mortality in alternative and conventional farrowing systems

The causes and timing of piglet mortality were studied in different farrowing systems. In the first experiment 198 litters were recorded in three systems, two of which allowed the sows to move freely, and the third restricted them in conventional crates. More piglets were weaned from the conventional crates than from the open systems and they grew more quickly. More than half the liveborn mortality occurred during the first four days after parturition. In the open systems, 17 per cent and 14 per cent of the piglets born alive were crushed, compared with only 8 per cent in the crates. In the second experiment, 29 sows and litters were studied in detail in a communal pen system during the first seven days of lactation. Three-quarters of the liveborn mortality was due to crushing. The total number of piglets dying per litter, including stillbirths, was significantly associated with the total litter size and the sows parity. The percentage livebom mortality was significantly associated with the parity and body length of the sows and with the within-litter variation in the birth weight of the piglets. Individual birth weight was closely associated with percentage survival. Only 28 per cent of piglets weighing less than 1.1 kg at birth survived to seven days.

A case control study of on-farm risk factors for tail biting in pigs

Abstract Tail biting is an abnormal behaviour of pigs that is thought to have a multi-factorial origin. It is considered an unpredictable event on farms and is hard to reproduce experimentally. Therefore, a novel approach involving a case control study was used to investigate risk factors for tail biting on commercial units in England. Ninety-two pig farms across England were visited over a period of 11 months. At each visit, the owner or the manager of the unit was interviewed and the unit inspected. Data were recorded on standard forms. Farms were categorised into those that had tail biting in at least one pig in the past 6 months and those that had not. Univariate and logistic regression analyses yielded the following main results. Adding straw in the creep area once or more per day decreased the risk of tail biting 10-fold. Keeping grower pigs on partially or fully slatted floors versus solid floor increased risks of tail biting (odds ratio (OR)=3.2). Using a feeding system with five or more grower pigs per feed space increased risks of tail biting (OR=2.7). A stocking density during the growing phase of 110kg/m 2 or greater increased risks of tail biting (OR=2.7). Farms that belonged to a holding of five or more pig units had an increased risk of tail biting (OR=3.5). As the number of pens per stockman increased by one, the risk of tail biting increased 1.06-fold. Tail biting was also associated with the following disease and production information: as the P2 back-fat value increased by 1mm, the risk of tail biting decreased by 1.5-fold; post-weaning mortality above 2.5% was associated with a 3.9-fold increase in the risk of tail biting; presence of respiratory diseases was associated with a 1.6-fold increase in the risk of tail biting. Tail docking was associated with a three-fold increase in the risk of tail biting. This study has identified and quantified some management practices on commercial farms that can be changed to decrease the risk of tail biting in growing and finishing pigs.

A comparison of the welfare of sows in different housing conditions.

Twelve sows in good quality unstrawed stalls, three groups of five sows in strawed pens with individual feeding stalls and sows in a 38-sow group in a strawed yard with an electronic sow feeder were compared during the first four parities. They originated from the same source, were about 9 months of age and in the 7th week of their first pregnancy at the start of the experiment and were kept in adjacent rooms in a building, cared for by the same staff and given the same diets at a rate of 2·2 kg/day per animal. No new animals were added to the groups or stalls during the study and animals returned to the same condition after periods in farrowing and service accommodation. Using a wide range of welfare indicators, it was clear that stall-housed sows had more problems than group-housed sows and that tliese problems were worse in the fourth than in the first pregnancy. By the fourth pregnancy, stall-housed sows spent proportionately 0·14 of time showing activities which were clearly stereotypies and much time on activities which were sometimes stereotyped, i.e. ‘drinking’ and rooting or chewing at pen fittings making a total of proportionately 0·50 of time. Comparable figures for group-housed sows were much lower (0·037 and 0·081 in total). Stall-housed sows were also more aggressive than group-housed by the fourth pregnancy and their body weights were lower. There were no differences using physiological or immunological tests or measures of reproductive output. When the two group-housing systems were compared, sows in the electronic feeder system showed more fighting, especially soon after initial mixing, but fewer total agonistic interactions than sows in groups of five during the first pregnancy. Oral stereotypies were slightly higher in small groups, perhaps because of smaller pen space, than in larger groups but much lower than in stalls. By the fourth pregnancy there were few differences between sows in small and large groups and all seemed to have adapted well to the conditions. Evaluation of welfare in different housing systems requires use of a wide range of measures and of long-term studies.

Individual aggressiveness of pigs can be measured and used to reduce aggression after mixing

Abstract Many studies have been carried out with the aim of reducing aggression after mixing unfamiliar pigs. A major problem in these studies has been the individual variation in aggressiveness between pigs. This study examined whether aggressiveness, as measured in tests on individual animals in a resident-intruder situation, is predictive of the level of aggression shown after mixing unfamiliar pigs, and whether information on this individual aggressiveness can be used to reduce aggression after mixing. One hundred eighty-nine pigs were tested for individual aggressiveness in their home pens and categorised as high- or low-aggressive (H or L), according to their attack latency. Eighty-eight of these pigs were then mixed in groups of eight, with four pigs from each of two litters. The combinations used were H H (4H + 4H), H L (4H + 4L) and L L (4L + 4L). In a follow-up study, a further 32 pigs were mixed into the combinations HL HL (HHLL + HHLL). The pigs were observed for 3 h on the day of mixing, and for 2 h on days 1, 2, 6 and 7 after mixing. During observations, aggressive interactions, and whether the pigs avoided lying down next to a pig from the unfamiliar litter were recorded. Fresh skin lesions were counted on each pig 2 h following mixing, and again 2 days later. In the majority of the groups, there was a clear distinction between a winner- and a loser-litter within the first 2 h after mixing. The number of pairs fighting in the 2 h immediately following mixing was lowest in the H L groups. The number of skin lesions on the pigs from the winner-litter both immediately after mixing and 2 days later was highest in H H groups. Thus, the relative level of aggressiveness seemed to determine the number of pairs that fought and the absolute level determined the intensity of fighting, with L pigs fighting less vigorously than H pigs. Speed of group integration was again affected by the absolute level of aggressiveness. The presence of H pigs in a group slowed down group integration. These data, particularly those relating to group integration, suggest that if mixing is unavoidable, it is preferable for pigs to be mixed into groups containing low-aggressive pigs only.