Talking to Cows: Reactions to Different Auditory Stimuli During Gentle Human-Animal Interactions.

The quality of the animal-human relationship and, consequently, the welfare of animals can be improved by gentle interactions such as stroking and talking. The perception of different stimuli during these interactions likely plays a key role in their emotional experience, but studies are scarce. During experiments, the standardization of verbal stimuli could be increased by using a recording. However, the use of a playback might influence the perception differently than "live" talking, which is closer to on-farm practice. Thus, we compared heifers' (n = 28) reactions to stroking while an experimenter was talking soothingly ("live") or while a recording of the experimenter talking soothingly was played ("playback"). Each animal was tested three times per condition and each trial comprised three phases: pre-stimulus, stimulus (stroking and talking) and post-stimulus. In both conditions, similar phrases with positive content were spoken calmly, using long low-pitched vowels. All tests were video recorded and analyzed for behaviors associated with different affective states. Effects on the heifers' cardiac parameters were assessed using analysis of heart rate variability. Independently of the auditory stimuli, longer durations of neck stretching occurred during stroking, supporting our hypothesis of a positive perception of stroking. Observation of ear positions revealed longer durations of the "back up" position and less ear flicking and changes of ear positions during stroking. The predicted decrease in HR during stroking was not confirmed; instead we found a slightly increased mean HR during stroking with a subsequent decrease in HR, which was stronger after stroking with live talking. In combination with differences in HRV parameters, our findings suggest that live talking might have been more pleasurable to the animals and had a stronger relaxing effect than "playback." The results regarding the effects of the degree of standardization of the stimulus on the variability of the data were inconclusive. We thus conclude that the use of recorded auditory stimuli to promote positive affective states during human-animal interactions in experimental settings is possible, but not necessarily preferable.

Gentle interactions with restrained and free-moving cows: Effects on the improvement of the animal-human relationship.

The animal-human relationship is essential for farm animal welfare and production. Generally, gentle tactile and vocal interactions improve the animal-human relationship in cattle. However, cows that are fearful of humans avoid their close presence and touch; thus, the animal-human relationship first has to be improved to a point where the animals accept stroking before their perception of the interactions and consequently the animal-human relationship can become positive. We tested whether the animal-human relationship of cows fearful of humans is improved more effectively by gentle interactions during restraint, allowing physical contact from the beginning, or if the gentle interactions are offered while the animals are free to move, giving them more control over the situation and thus probably a higher level of agency and a more positive perception of the interactions. Thirty-six dairy cows (median avoidance distance 1.6 m) were assigned to three treatments (each n = 12): gentle vocal and tactile interactions during restraint in the feeding rack (LOCK); gentle vocal and, if possible, tactile interactions while free in the barn (FREE); routine management without additional interactions (CON). Treatments were applied for 3 min per cow on 10 d per fortnight for 6 weeks (i.e., three periods). Avoidance and approach behaviour towards humans was tested before the start of the treatment period, and then at 2-week intervals. The recorded variables were reduced to one score by Principal Component Analysis. The resulting relationship score (higher values implying a better relationship with humans) increased in all groups; the increase was stronger in FREE than in CON, with the increase in LOCK being not significantly different from the other treatment groups. Thus, we recommend that gentle interactions with cows should take place while they are unrestrained, if possible.

Salivary oxytocin in pigs, cattle, and goats during positive human-animal interactions.

Research on oxytocin (OT) has provided crucial insight into the neuroendocrine mechanisms of social behavior and human-animal interactions. Nonetheless, this peptide hormone remains challenging to sample, usually requiring invasive measures in the brain or blood, which limits its use. We conducted an analytical validation of the measurement of OT in the saliva of three common farm animal species: pigs, cattle and goats. We then investigated the biological significance of salivary OT concentrations by using a positive human-animal interaction paradigm. The paradigm varied in terms of human familiarity and included a control condition where the animal was alone in the testing pen. A total of 18 pigs, 18 cattle and 9 goats were subjected to each condition using a within-individual counterbalanced design. Animals were free to choose to interact with the human. Saliva samples were collected immediately before and after the 10-min test, and behavior during the test was analyzed. Oxytocin could be reliably measured by ELISA in the saliva of goats (without extraction), and in the saliva of pigs and cattle after extraction. Salivary OT concentration did not change consistently according to testing condition. However, salivary OT concentration was significantly associated with some behaviors, with different relationships depending on the species. In conclusion, OT can be reliably measured in the saliva of goats and, after extraction, in the saliva of pigs and cattle. The relationships of OT with human-animal interactions and animal behavior were complex and to some extent species-dependent, possibly reflecting the perception of the interaction by the animal.

Effects of Different Stroking Styles on Behaviour and Cardiac Parameters in Heifers.

Gentle animal-human interactions, such as stroking, can promote positive emotions and thus welfare in cattle. While previous studies showed that stroking at the ventral neck elicited the most positive reactions in cows, intra-specific allogrooming in cattle includes different body regions and is probably guided partly by the receiver. Thus, we compared heifers' (n = 28) reactions to stroking with the experimenter either reactively responding to perceived momentary preferences of the heifers or exclusively stroking the ventral neck. Independently of the stroking style, longer durations of neck stretching and contact occurred during stroking, supporting our hypothesis of a positive perception of stroking. We did not confirm the predicted decrease in heart rate and increase in heart rate variability, but instead found a slightly increased mean heart rate during stroking. The different stroking styles elicited differences in the heifers' ear positions: "reactive" stroking led to longer durations of low ear positions during stroking, while during "ventral neck" stroking, the duration of back up increased. However, no other behaviours differed significantly between different stroking styles, indicating that the exact manner of stroking applied in our treatments seemed to be less important in the promotion of positive affective states in cattle through gentle human-animal interactions.

The Effects of Play Behavior, Feeding, and Time of Day on Salivary Concentrations of sIgA in Calves.

The focus of animal welfare science has shifted over the last decades from efforts to avoid negative states to ways of allowing animals the experience of positive emotions. They may influence physiological processes in farmed animals, potentially providing health benefits; in addition, the physiological changes might be used as indicators of emotional states. We investigated calves' salivary secretory immunoglobulin A (sIgA) concentrations with regard to a possible circadian rhythm and two situations that elicit positive emotions. Ten saliva samples of 14 calves were taken on two consecutive days; within the course of a day we observed a significant decline in salivary sIgA concentrations at 14:00 h. Further, we probed the animals before and after milk feeding and, contrarily to our prediction, detected lower sIgA concentrations 5 min after feeding than 15 min before. A probable explanation might be an increase in salivary flow rate caused by milk ingestion. We also took samples before and after we stimulated play behavior in calves. There was no significant difference in sIgA concentrations between samples taken before and after play. Although there was a significant correlation between the change in sIgA concentrations and the amount of play behavior shown, the correlation depended on an unexpected decrease of sIgA in animals that played little, and thus, does not support our hypothesis. In general, the data showed a large variability that might arise from different factors that are difficult to standardize in animals. Thus, the use of salivary sIgA concentrations as a marker of positive emotions in calves is not supported conclusively by the present data.

Inhibiting influence of testosterone on stress responsiveness during adolescence.

The maturation of the hypothalamo-pituitary-adrenal (HPA) axis is a key-component of the changes that occur during adolescence. In guinea pigs, HPA responsiveness during late adolescence depends strongly on the quantity and quality of social interactions: Males that lived in a large mixed-sex colony over the course of adolescence exhibit a lower stress response than males that were kept in pairs (one male/one female). Since colony-housed males have higher testosterone (T) levels than pair-housed males, and inhibiting effects of T on HPA function are well known, we tested the hypothesis that the decrease in stress responsiveness found in colony-housed males is due to their high T concentrations. We manipulated T levels in two experiments: 1) gonadectomy/sham-gonadectomy of colony-housed males (which usually have high T levels), 2) application of T undecanoate/vehicle to pair-housed males (which usually have low T levels). As expected, gonadectomized males showed a significantly increased stress response in comparison with sham-gonadectomized males, and T-injected males had a significantly lower stress response than vehicle-injected males. Both experiments thus confirm an inhibiting effect of T on HPA responsiveness during adolescence, which can mediate the influence of social interactions. The reduction in stress responsiveness is hypothesized to have a biologically adaptive value: A sudden increase in glucocorticoid concentrations can enhance aggressive behavior. Thus, pair-housed males might be adapted to aggressively defend their female ('resource defense strategy'), whereas colony-housed males display little aggressive behavior and are capable of integrating themselves into a colony ('queuing strategy').

Social interaction decreases stress responsiveness during adolescence.

Adolescence is the transition from infancy to adulthood and encompasses major changes in the brain, the endocrine systems, and behavior. During late adolescence, male guinea pigs living in mixed-sex colonies exhibit a lower cortisol (C) response to novelty compared with animals in other ages and housing conditions. It was hypothesized that this reduction in stress responsiveness is induced by a high amount of social interactions in the colonies. In a previous study (Lürzel et al., 2010), late adolescent colony-housed males (CM) were compared with similarly aged males that were housed in heterosexual pairs (PM) as well as with males that were also housed in pairs, but regularly received additional social stimulation by allowing them ten times to interact with unfamiliar adult animals of both sexes for 10 min (SM). CM had a significantly lower stress response than PM, with SM being intermediate and not significantly different from either of the other groups. We assumed that the amount of social stimulation in SM was insufficient in order to achieve a significant reduction of stress responsiveness compared with PM. For the present study, we hypothesized that with a higher amount of social stimulation, a significant difference in stress responsiveness between PM and SM becomes apparent during late adolescence. Thus, PM were again compared with SM that, this time, had received twice as much social stimulation as in the previous study. As a result, stress responsiveness was indeed significantly lower in SM than in PM during late adolescence. Thus, a high amount of social interactions during the course of adolescence leads to a decreased stress responsiveness. Furthermore, SM showed an increase in testosterone (T) levels caused by social stimulation. We hypothesize that the reduction in stress responsiveness is brought about by high T levels that organize central neural structures over the course of adolescence.

Social interaction, testosterone, and stress responsiveness during adolescence.

Adolescence is the transition from childhood to adulthood, including alterations in the endocrine systems, in neural circuitry and in behavior. During late adolescence, male guinea pigs living in large mixed-sex colonies exhibit a peculiar stress hyporesponsiveness compared with animals in other developmental stages or other housing conditions. In the present study, it was hypothesized that the interaction with conspecifics leads to an increase in testosterone (T) concentrations, which, in turn, reduces cortisol (C) responsiveness. To test this hypothesis, the stress response of pair- and colony-housed animals was compared with that of pair-housed animals that had limited opportunities to interact with unfamiliar animals of both sexes (social stimulation). The main findings were: (1) Social stimulation caused a significant acute increase in T levels. (2) T concentrations increased significantly in colony-housed males from early to late adolescence but not in the other groups. (3) The C response to a novel environment was significantly reduced in late adolescent colony-housed males compared with similarly aged pair-housed males; C responsiveness of socially stimulated males was intermediate. The present data support our general hypothesis that socially induced increases in T during adolescence might organize a reduction of the endocrine stress response.