The Power of a Positive Human-Animal Relationship for Animal Welfare.

Domestic animals often seek and enjoy interacting with humans. Positive human-animal relationships can elicit positive emotions and other positive welfare outcomes. Nevertheless, our understanding of the underlying processes that govern the positive perception of humans by animals is incomplete. We cover the potential mechanisms involved in the development and maintenance of positive human-animal relationships from the perspective of the animal. This encompasses habituation, associative learning, and possibly attachment or bonding based on communication and social cognition. We review the indicators from the literature to assess a positive human-animal relationship. We operationally define this positive relationship as the animal showing voluntary approach and spatial proximity (seeking) and signs of anticipation, pleasure, relaxation, or other indicators of a rewarding experience from interacting with the human. For research, we recommend accounting for the baseline human-animal relationship in the animal's everyday life, and incorporating a control treatment rather than only comparing positive to negative interaction treatments. Furthermore, animal characteristics, such as previous experience, genetics, and individual predisposition, as well as contextual characteristics related to the social and physical environment, may modulate the perception of humans by animals. The human-animal relationship is also influenced by human characteristics, such as the person's familiarity to the animal, attitudes, skills, and knowledge. We highlight implications for current practices and suggest simple solutions, such as paying attention to the animal's behavioral response to humans and providing choice and control to the animal in terms of when and how to interact with humans. Practical applications to achieve a positive perception of humans could be better utilized, such as by incorporating training principles, while keeping in mind trust and safety of both partners. Overall, there is growing evidence in the scientific literature that a positive human-animal relationship can bring intrinsic rewards to the animals and thereby benefit animal welfare. Further research is needed on the underlying processes to establish an effective positive human-animal relationship, especially in regard to the type, frequency, and length of human interaction necessary. In particular, the importance of providing animals with a sense of agency over their interactions with humans remains poorly understood.

Are there facial indicators of positive emotions in birds? A first exploration in Japanese quail.

The positive aspect of emotions, like pleasure, remains overlooked in birds. Our aim was to contribute to the exploration of facial indicators of positive emotions. To observe contrasting emotional expressions, we used two lines of Japanese quail divergently selected on their inherent fearfulness: a fearful line (long tonic immobility duration: LTI) and a less fearful line (short tonic immobility duration: STI). To induce positive emotions, we gave individual quail the opportunity to perform a rewarding behaviour, dustbathing, in an unfamiliar cage. More STI than LTI quail expressed dustbathing and latencies to dustbathe were significantly shorter in STI than LTI quail. This result indicated that the lines of quail differed in their fearfulness of the situation. We observed crown feather height, throat feather angle and pupil surface before (control) and during dustbathing. We found significant increases in crown feather height, pupil area and angle of throat feathers between the control and the dustbathing phases in STI quail, and pupil area correlated positively with crown feather height. In LTI quail, the angle of throat feathers increased during dustbathing, but the other parameters did not differ. We argue that variation in crown feather height and pupil area may provide indications of positive emotions in Japanese quail.

Behavioral evidence of heterospecific bonding between the lamb and the human caregiver and mapping of associated brain network.

While behavioral mechanisms of bonding between young mammals and humans have been explored, brain structures involved in the establishment of such processes are still unknown. The aim of the study was to identify brain regions activated by the presence of the caregiver. Since human positive interaction plays an important role in the bonding process, activation of specific brain structures by stroking was also examined. Twenty-four female lambs reared in groups of three were fed and stroked daily by a female caregiver between birth and 5-7 weeks of age. At 4 weeks, an isolation-reunion-separation test and a choice test revealed that lambs developed a strong bond with their caregiver. At 5-7 weeks of age, lambs were socially isolated for 90min. They either remained isolated or met their caregiver who stroked them, or not, at regular intervals over a 90-min period. Neuronal activation was investigated at the end of the period for maximum c-Fos expression. Reunion with the caregiver appeased similarly the lambs whether stroking was provided or not. Stroking did not activate a specific brain network compared to no stroking. In both cases, brain regions associated with olfactory, visual and tactile cue processing were activated in the presence of the caregiver, suggesting a multisensory process involved. In addition, activation of the oxytocinergic system in the hypothalamic paraventricular nucleus induced by the presence of the caregiver suggests similar neuroendocrine mechanisms involved in inter-conspecific and animal-human bonding.

A prospective exploration of farm, farmer, and animal characteristics in human-animal relationships: An epidemiological survey.

Human-animal relationships are essential for dairy farming. They affect work comfort and efficiency, as well as milk production. A poor human-animal relationship can result in stress and accidents to both animals and caretakers and needs to be improved. However, many studies have demonstrated the multifactoriality of these relationships. We aimed at assessing the relative importance of the various factors expected to be associated with poor human-animal relationships. On 118 dairy farms, we applied a standardized avoidance distance test to cows at the feeding rack. The sample of farms covered a wide range of situations: lowland versus highland, small versus medium size farms, cubicles versus deep-bedded systems, milking parlor versus automatic milking systems, and Holstein versus Montbéliarde breeds. We used Poisson regression to analyze the links between the number of cows that accepted being touched, and farm characteristics, animals, management, and farmers' attitudes. A multivariate analysis yielded a final model that explained 32.7% of the variability between farms. Calving conditions ("Main calving location" and "Cleaning or adding litter after calving") accounted for a significant part of the variability observed (respectively 25.8 and 13.6% of variability explained by the model, SSB). Fewer cows accepted being touched on farms where the main calving location was in the barn, and where farmers cleaned or added litter after calving. The proportion of cows that accepted being touched increased with the proportion of lean cows in the herd (18.8%), with worker/cow ratio on the farm (11.7%), when farmers considered "health" or "human-cow relationships" as most important issues for farm success (10.4%), and with farmers' years of experience (10.8%). Farmers with more negative behavioral attitudes toward cows had a lower proportion of cows that accepted being touched (8.9%). In conclusion, the human-animal relationship was not found to be associated with farm characteristics (e.g., housing or milking system) but varied with farmers' attitudes and management. We confirm that cows' fear of people is linked to negative attitudes displayed by caretakers toward cows, and is reduced in farms where several caretakers are present. Our study also suggests further exploring the key role of factors linked to calving conditions, as cows are more likely to be afraid of people when disturbed at calving.

Do lambs perceive regular human stroking as pleasant? Behavior and heart rate variability analyses.

Stroking by humans is beneficial to the human-animal relationship and improves welfare in many species that express intraspecific allogrooming, but very few studies have looked at species like sheep that do not express such contact except around parturition. This study investigated the way lambs perceive regular human tactile contact using behavioral and physiological responses. Twenty-four lambs were reared and bucket-fed in groups of four. All were stroked daily by their familiar caregiver. At 8 weeks of age, the lambs were individually tested in their home pen but in a 1×1m open-barred pen after a 15 h period of habituation to physical separation from peers while remaining in visual and auditory contact. Half of the lambs received stroking by their caregiver for 8 min and half were exposed to their caregiver's immobile presence. Heart rate and heart rate variability were recorded and analyzed by 2-min slots over the same interval based on three measures: mean heart rate value (HR), root mean square of successive differences (RMSSD) and standard deviation of all intervals measured between consecutive sinus beats (SDNN). Behavioral responses (ear postures of the lamb and time spent in contact with the familiar caregiver, on the knees of the familiar caregiver, and moving) were recorded throughout the test. Lamb HR decreased continuously while in the presence of their caregiver. Lambs being stroked showed slower HR and higher RMSSD which reflected positive emotional states compared to lambs left unstroked. All behavioral variables were highly correlated with the main component axis of the PCA analyses: the more the animals stayed in contact with their caregiver, the less they moved and the more their ears were hanging. This first component clearly differentiates lambs being stroked or not. Behavioral and physiological observations support the hypothesis that gentle physical contact with the caregiver is perceived positively by lambs.

Human-lamb bonding: oxytocin, cortisol and behavioural responses of lambs to human contacts and social separation.

Friendly interactions between humans and animals such as gentling or petting have been shown to have positive behavioural and physiological consequences in many species. In primates, rodents and dogs, oxytocin has been associated with tactile contact and anti-stress effects that may influence bonding and responses to stress situations. However the activation of the oxytocinergic system in other human-animal interactions such as with herbivores, had not yet been studied. Sixteen female lambs were reared by artificial feeding reinforced with 3× 30 s daily stroking sessions. At 6 weeks of age, the test consisted in measuring first plasma oxytocin and cortisol responses in lambs during a first 6-min phase in the home pen where the familiar caregiver gently stroked the lamb, and then physiological and behavioural responses in a test pen during a 20-min - phase of social isolation followed by a 20-min - phase of reunion with its familiar caregiver. The lambs expressed behavioural agitation during the whole period of isolation. A strong affiliative response towards the human and a sustained reduction of the agitation behaviour were observed during reunion. Lambs' behaviours when isolated and when in contact with the human were correlated suggesting a response to social separation from the familiar caregiver more than to social isolation from congeners. No significant changes in cortisol levels were observed during the test. Oxytocin levels did not vary during human contact, but increased when the familiar caregiver left the lamb alone in the test pen. In conclusion, lambs displayed affiliative responses towards their caregiver, and the lack of cortisol response during isolation while oxytocin was released suggest an anti-stress effect of oxytocin.

Temporal association between food distribution and human caregiver presence and the development of affinity to humans in lambs.

The presence of the caregiver around feeding favors the development of a human-animal relationship. To understand the underlying mechanism, we tested various temporal associations between food distribution and human presence: from an early age, a person was repeatedly present for 2 min just before milk distribution ("Forward"), during milk distribution ("Simultaneous"), and 20 min afterwards ("Delayed"). The "Control" group received no human contacts. During the treatments, "Forward" and "Delayed" lambs had more physical contacts with the person than "Simultaneous" lambs. When tested in unfamiliar environments, they stood longer near the person than did "Control" or "Simultaneous" lambs, which did not differ. Only "Forward" and "Delayed" lambs bleated when separated from the person. Fasting before testing had no effect. "Forward" and "Delayed" seemed to produce the same human-animal relationship, showing that this did not rely only on a conditioning process associating the caregiver with food. The caregiver may acquire properties for social support through other mechanisms (attachment and/or postingestive effects).

Nonnutritive sucking: one of the major determinants of filial love.

The present study investigated the rewarding effects of nonnutritive sucking on the development of a filial preference. Two experiments were conducted to test whether nonnutritive visceral and oral stimuli have reinforcing properties independent from each other or act in synergy. Lambs could interact freely with their dam but were deprived of suckling by covering the udder for the first 12 hr. In Experiment 1, suckling was prevented and replaced by human giving, in the presence of the mother, either a bottle of water (B5 and B2.5: 5% or 2.5% birth weight, BW, divided into seven portions over 12 hr) or water via tube-feeding (I5 and I2.5: 5% or 2.5% BW, also divided into seven portions over 12 hr). During a two-choice test performed at 12 hr after birth, only B5 and I5 lambs preferred their mother to an alien ewe however, B5 were faster at choosing their mother at the beginning of the test. B2.5 and I2.5 lambs made a random choice. In Experiment 2, suckling was prevented and replaced by human giving, in the presence of the mother, either a bottle of water (B2.5: 2.5% BW, divided into seven portions over 12 hr) or water via tube-feeding (I10 and I2.5: 10% or 2.5% BW, also divided into seven portions over 12 hr). During a two-choice test at 12 hr, tube-fed lambs (I10 and I2.5) preferred their mother to a human. B2.5 lambs were equally attracted to both partners and spent more time near the human than lambs from the other groups. In a test of reactivity to a human performed on neonates isolated from their mother, B2.5 lambs explored the human much more than the other lambs. The presence of the human had soothing properties in B2.5 lambs and once the human left, they were the only lambs displaying enhanced vocal and locomotor activity. In these experiments, nonnutritive gastrointestinal stimuli induced a preference for the mother whereas nonnutritive sucking led to a strong positive relationship with the human. These results suggest that when lambs suckle their dam, the development of filial bonding is facilitated through the combined effects of oral and gastrointestinal stimuli.