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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.

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Between-farm variation in animal reactions to humans can reflect different management styles and behavioral tendencies among farmers. Animals are well known to discriminate among humans, but less clear is the key issue of whether they more or less easily generalize their experience from specific humans to others depending on management style. Here, we chose 2 contrasted management styles by known handlers: "gentle" management, that is, long-lasting exposure to positive human interactions (with limited negative interactions), and "aversive" management including long-lasting exposure to various negative human interactions (with only food delivery considered a positive interaction) and aversive events. Over a period of 19 wk, 15 female lambs were exposed to the gentle management treatment ("gently treated" group) and another 15 lambs ("aversively treated" group) were exposed to the aversive management treatment. To facilitate discrimination by animals, experimenters wore white clothes for aversive events and green clothes for farming handling (positive handling and feeding for the gently treated group and only feeding for the aversively treated group). Sheep perception of the human was assessed after the management period by submitting lambs from each group to 2 standardized tests: 1) the presence of a stationary human (familiar human in white vs. familiar human in green vs. unknown human) and 2) the presence of a moving human (familiar human in white vs. familiar human in green vs. unknown human). As expected, during the stationary human test, aversively treated lambs spent less time in the human zone (P<0.0001), showed greater latency to approach the human (P=0.05), and had fewer contacts with the human (P=0.05) than gently treated lambs. During the moving human test, aversively treated lambs also showed a greater escape distance from humans than gently treated lambs (P<0.0001). Aversively treated lambs showed the same fear responses towards familiar and unknown humans and tended to generalize their aversive experiences with one handler to all humans. In contrast, gently treated lambs seemed to discriminate familiar humans from unfamiliar humans. Different management styles could modulate farm generalization to humans in farm animals.

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