Jan Langbein

Assessment of positive emotions in animals to improve their welfare

It is now widely accepted that good welfare is not simply the absence of negative experiences, but rather is primarily the presence of positive experiences such as pleasure. However scientific investigation of positive emotions has long been neglected. This paper addresses two main issues: first, it reviews the current state of scientific knowledge that supports the existence of positive affective states in animals and, second, it suggests possible applications of this knowledge that may enhance quality of life under animal management conditions. In the first part of the paper, recent advances in psychology and neuroscience are reviewed to provide pragmatic frameworks based on cognitive processes (such as positive anticipation, contrast and controllability) for further investigations of positive emotions in animals. Thereafter, the neurobiological bases of positive emotions are highlighted in order to identify behavioral and physiological expressions of positive experiences in animals. Monitoring both the autonomic nervous system (via heart rate and its variability) and the immune system could offer relevant tools to better assess emotional states in animals, complementary to classical adrenocortical measures. In the second part of the paper, useful strategies for enhancing positive experiences (such as physical, social and cognitive enrichment or putative genetic selection) are outlined. Then this paper emphasizes practical applications for assessing and promoting positive emotions that may help in providing animals with a better quality of life. Play, affiliative behaviors and some vocalizations appear to be the most promising convenient indicators for assessing positive experiences in laboratory and farm animals under commercial conditions.

Heart rate variability as a measure of autonomic regulation of cardiac activity for assessing stress and welfare in farm animals : A review

Measurement of heart rate variability (HRV) is a non-invasive technique that can be used to investigate the functioning of the autonomic nervous system, especially the balance between sympathetic and vagal activity. It has been proven to be very useful in humans for both research and clinical studies concerned with cardiovascular diseases, diabetic autonomic dysfunction, hypertension and psychiatric and psychological disorders. Over the past decade, HRV has been used increasingly in animal research to analyse changes in sympathovagal balance related to diseases, psychological and environmental stressors or individual characteristics such as temperament and coping strategies. This paper discusses current and past HRV research in farm animals. First, it describes how cardiac activity is regulated and the relationships between HRV, sympathovagal balance and stress and animal welfare. Then it proceeds to outline the types of equipment and methodological approaches that have been adapted and developed to measure inter-beats intervals (IBI) and estimate HRV in farm animals. Finally, it discusses experiments and conclusions derived from the measurement of HRV in pigs, cattle, horses, sheep, goats and poultry. Emphasis has been placed on deriving recommendations for future research investigating HRV, including approaches for measuring and analysing IBI data. Data from earlier research demonstrate that HRV is a promising approach for evaluating stress and emotional states in animals. It has the potential to contribute much to our understanding and assessment of the underlying neurophysiological processes of stress responses and different welfare states in farm animals.

Heart rate variability A noninvasive approach to measure stress in calves and cows

The aim of this study was to evaluate the usefulness of heart rate variability (HRV) and its specific parameters as a new approach to assess stress load in cattle. We recorded HRV in 52 calves in three groups and in 31 cows in two groups. In calves we divided Group 1 with no obvious stress load (n=18), Group 2 with external stress load (n=17), and Group 3 with internal stress load from sickness (n=17). In cattle we divided lactating cows (n=21) and nonlactating cows (n=10). HRV parameters were analyzed in the time domain and in the frequency domain. Moreover, we applied Recurrence Quantification Analysis (RQA) to quantify nonlinear components of HRV. In calves, linear HRV parameter decreased from Group 1 to Group 3 (P<.05). However, not a single parameter showed significant differences regarding all three groups. The value of all nonlinear measurements increased at the same time (P<.05). The only parameter that exhibited significant differences between all three groups was the longest diagonal line segment in the recurrence plot (L(MAX)) which is inversely related to the Lyapunov exponent. We did not find differences concerning the linear HRV parameters between the two groups in the cows. The nonlinear parameter Determinism showed significant higher values in lactating cows compared to nonlactating cows. The importance of particular HRV-parameters was tested by applying a discriminant analysis approach. In calves and cattle nonlinear parameters were most important to indicate the level of stress load on the animals. Based on the results we assume HRV to be a valuable physiological indicator for stress load in animals. Whereas linear parameters of HRV are supposed to be useful to separate qualitative different level of stress, nonlinear components of HRV distinguish quantitative different challenges for the animals.

Autonomic reactions indicating positive affect during acoustic reward learning in domestic pigs

Cognitive processes, such as stimulus appraisal, are important in generating emotional states and successful coping with cognitive challenges is thought to induce positive emotions. We investigated learning behaviour and autonomic reactions, including heart rate (HR) and its variability (standard deviation (SDNN) and root mean square of successive differences (RMSSD) of a time series of interbeat intervals). Twenty-four domestic pigs, Sus scrofa, housed in six groups of four, were confronted with a cognitive challenge integrated into their familiar housing environment. Pigs were rewarded with food after they mastered the discrimination of an individual acoustic signal followed by an operant task. All pigs quickly learned the tasks, while baseline SDNN and RMSSD increased significantly throughout the experiment. In reaction to the signals, pigs showed a sudden increase in HR, SDNN and RMSSD, and a decrease in the RMSSD/SDNN ratio. Immediately after this reaction, the HR and SDNN decreased, and the RMSSD/SDNN ratio increased. During feeding, the HR and the RMSSD/SDNN ratio stayed elevated. The pigs showed no cardiac reaction to the sound signals for other pigs or their feeding pen mates. We concluded that the level of cognitive challenge was adequate and that the observed changes in the autonomic tone, which are related to different dimensions of the affective response (e.g. arousal and valence), indicated arousal and positive affective appraisal by the pigs. These findings provide valuable insight into the assessment of positive emotions in animals and support the use of an adequate cognitive enrichment to improve animal welfare.

Prefrontal cortex activity, sympatho-vagal reaction and behaviour distinguish between situations of feed reward and frustration in dwarf goats.

Recent concepts relating to animal welfare accept that animals experience affective states. These are notoriously difficult to measure in non-verbal species, but it is generally agreed that emotional reactions consist of well-coordinated reactions in behaviour, autonomic and brain activation. The aim of the study was to evaluate whether each or a combination of these aspects can differentiate between situations presumed to differ in emotional content. To this end, we repeatedly confronted dwarf goats at short intervals with a covered and an uncovered feed bowl (i.e. presumably frustrating and rewarding situations respectively) whilst simultaneously observing their behaviour, measuring heart-rate and heart-rate variability and haemodynamic changes in the prefrontal cortex using functional near-infrared spectroscopy. When faced with a covered feed bowl, goats occupied themselves at locations away from the bowl and showed increased locomotion, while there was a general increase in prefrontal cortical activity. There was little indication of autonomic changes. In contrast, when feed was accessible, the goats reduced locomotion, focused their behaviour on the feed bowl, showed signs of sympathetically mediated arousal reflecting anticipation and, if any cortical activity at all was present, it was concentrated to the left hemisphere. We thus observed patterns in behaviour, sympathetic reaction and brain activity that distinguished between a situation of frustration and one of reward in dwarf goats. These patterns consisted of a well-coordinated set of reactions appropriate in respect of the emotional content of the stimuli used.

Describing temperament in an ungulate : a multidimensional approach

Studies on animal temperament have often described temperament using a one-dimensional scale, whereas theoretical framework has recently suggested two or more dimensions using terms like “valence” or “arousal” to describe these dimensions. Yet, the valence or assessment of a situation is highly individual. The aim of this study was to provide support for the multidimensional framework with experimental data originating from an economically important species (Bos taurus). We tested 361 calves at 90 days post natum (dpn) in a novel-object test. Using a principal component analysis (PCA), we condensed numerous behaviours into fewer variables to describe temperament and correlated these variables with simultaneously measured heart rate variability (HRV) data. The PCA resulted in two behavioural dimensions (principal components, PC): novel-object-related (PC 1) and exploration-activity-related (PC 2). These PCs explained 58% of the variability in our data. The animals were distributed evenly within the two behavioural dimensions independent of their sex. Calves with different scores in these PCs differed significantly in HRV, and thus in the autonomous nervous system’s activity. Based on these combined behavioural and physiological data we described four distinct temperament types resulting from two behavioural dimensions: “neophobic/fearful – alert”, “interested – stressed”, “subdued/uninterested – calm”, and “neoophilic/outgoing – alert”. Additionally, 38 calves were tested at 90 and 197 dpn. Using the same PCA-model, they correlated significantly in PC 1 and tended to correlate in PC 2 between the two test ages. Of these calves, 42% expressed a similar behaviour pattern in both dimensions and 47% in one. No differences in temperament scores were found between sexes or breeds. In conclusion, we described distinct temperament types in calves based on behavioural and physiological measures emphasising the benefits of a multidimensional approach.

Self-controlled visual discrimination learning of group-housed dwarf goats (Capra hircus): behavioral strategies and effects of relocation on learning and memory.

In most studies on animal learning, individual animals are tested separately in a specific learning environment and with a limited number of trials per day. An alternative approach is to test animals in a familiar environment in their social group. In this study, the authors--applying a fully automated learning device--investigated voluntary, self-controlled visual shape discrimination learning of group-housed dwarf goats (Capra hircus). The majority of the tested goats showed successful shape discrimination, which indicates the adaptive value of an effective learning strategy. However, in each group, a few individual goats developed behavioral strategies different from shape discrimination to get reward. Relocation impairs memory retrieval (probably by attention shifting) only temporarily for previously learnt shapes. The results demonstrate the usefulness of a self-controlled learning paradigm to assess learning abilities of social species in their normal social settings. This may be especially relevant for captive animals to improve their welfare.

Exclusion Performance in Dwarf Goats (Capra aegagrus hircus) and Sheep (Ovis orientalis aries)

Using a comparative approach, we investigated the ability of dwarf goats and sheep to use direct and indirect information about the location of a food reward in an object-choice task. Subjects had to choose between two cups with only one covering a reward. Before making a choice, subjects received information about the baited (direct information) or non-baited cup (indirect information). Both goats and sheep were able to use direct information (presence of food) in the object choice task. After controlling for local enhancement, we found that goats rather than sheep were able to use indirect information (i.e., the absence of food) to find a reward. The actual test setup could not clarify whether individual goats were able to inferentially reason about the content of the baited cup when only shown the content of the non-baited cup or if they simply avoided the empty cup in that situation. As browsing species, feral and wild goats exhibit highly selective feeding behaviour compared to the rather unselective grazing sheep. The potential influence of this species-specific foraging flexibility of goats and sheep for using direct and indirect information to find a food reward is discussed in relation to a higher aversion to losses in food acquisition in goats compared to sheep.

Differences in behaviour of free-ranging cattle in the tropical climate

Abstract The pasture behaviour of Holstein Friesian and Siboney de Cuba ( 5 8 Holstein Friesian× 3 8 Cuban Zebu) lactating cows was studied during the dry season and the rainy season in the tropical climate of Cuba. Grazing, total activity, standing and lying, time spent in the sun and time spent in the shade were recorded from 08:00 to 18:00 h at 5-min intervals. In the rainy season, the Holstein Friesian cattle spent less time grazing and in activity, but spent longer in the shade than Siboney de Cuba, i.e. a higher thermal load was imposed on the purebred taurine cattle as compared with the Siboney de Cuba. However, no differences between the two breeds were observed in the dry season. The results indicate that the heat tolerance of Siboney de Cuba is superior to that of Holstein Friesian during the rainy season. In the rainy season mixed group series, the behaviour of Siboney de Cuba followed (was masked by) the behavioural changes shown by Holstein Friesians, i.e. a new herd behaviour was determined by purebred taurine cattle.

Characteristic activity patterns of female mouflons (Ovis orientalis musimon) in the lambing period

Abstract We analysed the activity pattern of wild mouflon sheep (Ovis orientalis musimon) in the lambing season for 2 consecutive years. The activity data was recorded automatically by the storage-telemetry-system, ETHOSYS. The animals were equipped with electronic collars of about 300 g, which continuously sampled behaviour in time intervals of 30 min over 50 days. Lambing was accompanied by decreased daily activity budgets of 3–5 consecutive days. The sequence of daily activity budgets around parturition were compared with other periods of lower activity using discriminant analysis. Birth patterns were found to differ significantly in width, depth and shape from normal fluctuations in daily activity. Calculating the discriminant function from the 1995 data, we accurately predicted the 1996 minima in activity caused by lambing. The jackknife method, providing an even more precise misclassification rate, was 93% accurate. Changes in activity patterns and space utilization in the period peri partum in the wild are discussed in contrast to what happens for animals at pasture or in enclosures.