Farm Animal Cognition-Linking Behavior, Welfare and Ethics.

Farm animal welfare is a major concern for society and food production. To more accurately evaluate animal farming in general and to avoid exposing farm animals to poor welfare situations, it is necessary to understand not only their behavioral but also their cognitive needs and capacities. Thus, general knowledge of how farm animals perceive and interact with their environment is of major importance for a range of stakeholders, from citizens to politicians to cognitive ethologists to philosophers. This review aims to outline the current state of farm animal cognition research and focuses on ungulate livestock species, such as cattle, horses, pigs and small ruminants, and reflects upon a defined set of cognitive capacities (physical cognition: categorization, numerical ability, object permanence, reasoning, tool use; social cognition: individual discrimination and recognition, communication with humans, social learning, attribution of attention, prosociality, fairness). We identify a lack of information on certain aspects of physico-cognitive capacities in most farm animal species, such as numerosity discrimination and object permanence. This leads to further questions on how livestock comprehend their physical environment and understand causal relationships. Increasing our knowledge in this area will facilitate efforts to adjust husbandry systems and enrichment items to meet the needs and preferences of farm animals. Research in the socio-cognitive domain indicates that ungulate livestock possess sophisticated mental capacities, such as the discrimination between, and recognition of, conspecifics as well as human handlers using multiple modalities. Livestock also react to very subtle behavioral cues of conspecifics and humans. These socio-cognitive capacities can impact human-animal interactions during management practices and introduce ethical considerations on how to treat livestock in general. We emphasize the importance of gaining a better understanding of how livestock species interact with their physical and social environments, as this information can improve housing and management conditions and can be used to evaluate the use and treatment of animals during production.

Stress during pregnancy alters dendritic spine density and gene expression in the brain of new-born lambs.

Rodent studies show how prenatal stress (PS) can alter morphology in the cortico-limbic structures that support emotional and cognitive functions. PS-induced alteration is less well described in species with a gyrencephalic brain and complex earlier fetal development, and never in sheep at birth to rule out postnatal environment effects or influences of maternal behavior. This study aimed to assess the consequences of a mild chronic stress in pregnant ewes on the neurobiological development of their lambs at birth. During the last third of gestation, 7 ewes were exposed daily to various unpredictable and negative routine management-based challenges (stressed group), while 7 other ewes were housed without any additional perturbation (control group). For each group, a newborn from each litter was sacrificed at birth to collect its brain and analyze its expression levels of genes involved in neuronal dendritic morphology (Dlg4, Rac1, RhoA, Doc2b), synaptic transmission (Nr1, Grin2A, Grin2B) and glucocorticoid receptor (Nr3C1) in hippocampus (HPC), prefrontal cortex (PFC) and amygdala (AMYG). Results revealed that lambs from stressed dam (PS lambs) showed under-expression of Rac1 and Nr1 in PFC and overexpression of Dlg4 in AMYG compared to controls. To assess the morphological consequences of gene dysregulations, the dendritic morphology of pyramidal neurons was explored by Golgi-Cox staining in HPC and PFC. PS lambs had higher dendritic spine density in both structures and more stubby-type spines in the CA1 area of HPC than controls. This is the first demonstration in sheep that PS alters fetal brain, possibly reflecting functional changes in synaptic transmission to cope with adversity experienced in fetal life.

Effects of prenatal stress and emotional reactivity of the mother on emotional and cognitive abilities in lambs.

Consequences of prenatal stress on emotional reactivity and cognitive abilities in offspring are under-documented in precocial mammals. Here, we investigated to what extent emotional reactivity, judgment bias and spatial learning abilities of lambs are affected by chronic stress during late pregnancy and by their dams' emotional reactivity. The 20 highest-responsive (HR) and 20 lowest-responsive (LR) ewes from a population of 120 Romane ewes were selected according to their pre-mating reactivity to social isolation in a new environment. Over the final third of pregnancy, 10 HR ewes and 10 LR ewes were exposed daily to various unpredictable aversive events such as restraint, mixing groups and transport while the other 20 selected ewes were not. In a human and an object test, prenatally-stressed lambs were more fearful than control lambs, but the prenatal stress effect was moderated by the reactivity of the mothers: prenatally-stressed lambs from ewes with high emotional reactivity were more affected. Prenatally-stressed lambs did not perform as well as control lambs in a maze test and showed pessimistic-like judgment in a cognitive bias test. Prenatally-stressed lambs were thus characterized by a negative affective state with increased fear reactions and impaired cognitive evaluation. The development of negative moods could have long-lasting consequences on the coping strategies of the lambs in response to their rearing conditions.

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.

Mild effects of gestational stress and social reactivity on the onset of mother-young interactions and bonding in sheep.

Consequences of prenatal stress on mother-young relationships are well-documented in altricial mammals but less so in precocial mammals. In this study, we investigated the effects of unpredictable aversive events on maternal behavior and mutual mother-young recognition in pregnant ewes while accounting for modulatory effects of ewe reactivity. From a population of 120 Romane-breed ewes, we selected 20 high-responsive (HR) and 20 low-responsive (LR) ewes according to pre-mating reactivity assessed in isolation tests. Over the final third of pregnancy, 10 HR ewes and 10 LR ewes were exposed daily to various aversive events such as social isolation, mixing and transport (stressed ewes), while the other 20 ewes were not exposed to aversive events (control ewes). Although the treatment induced chronic stress, physiologically confirmed by an increase in salivary cortisol following transport and sham shearing, maternal behavior of stressed ewes observed during the first 30 min postpartum and in the selectivity test 1 h 30 min later did not differ from controls. However, in a maternal motivation test performed 48 h postpartum, stressed ewes vocalized less than controls when separated from their lambs, and walked less readily past an unknown object to reach their lambs. Lambs of stressed ewes spent more time near their dam in a preference test performed 15 h after birth compared to control-ewe lambs. HR ewes spent more time grooming their lambs than LR ewes. We posit that domestication could have selected animals displaying robust expression of maternal behavior related to social reactivity and producing offspring that are better adapted to challenging situations.

Visual discrimination of species in dogs (Canis familiaris).

In most social interactions, an animal has to determine whether the other animal belongs to its own species. This perception may be visual and may involve several cognitive processes such as discrimination and categorization. Perceptual categorization is likely to be involved in species characterized by a great phenotypic diversity. As a consequence of intensive artificial selection, domestic dogs, Canis familiaris, present the largest phenotypic diversity among domestic mammals. The goal of our study was to determine whether dogs can discriminate any type of dog from other species and can group all dogs whatever their phenotypes within the same category. Nine pet dogs were successfully trained through instrumental conditioning using a clicker and food rewards to choose a rewarded image, S+, out of two images displayed on computer screens. The generalization step consisted in the presentation of a large sample of paired images of heads of dogs from different breeds and cross-breeds with those of other mammal species, included humans. A reversal phase followed the generalization step. Each of the nine subjects was able to group all the images of dogs within the same category. Thus, the dogs have the capacity of species discrimination despite their great phenotypic variability, based only on visual images of heads.

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.

Early adverse experience alters dendritic spine density and gene expression in prefrontal cortex and hippocampus in lambs.

In the laboratory, prenatal stress produces alterations in the structure and function of corticolimbic neurons. Here we report changes in gene expression and corticolimbic dendritic spine morphology in the offspring of pregnant ewes subjected to aversive interactions with human handlers during the last five weeks of pregnancy (AVS) compared to control dams that received gentle handling (GEN). AVS lambs had higher spine density on pyramidal neurons in area CA1 of the hippocampus and in medial prefrontal cortex compared to GEN lambs, as well as a lower ratio of mushroom spines to stubby and thin spines in area CA1. Expression of genes involved in brain development and spine morphogenesis was decreased in hippocampus and prefrontal cortex in AVS compared to GEN lambs. This study is the first demonstration that an ecologically relevant aversive experience in a field setting alters neuronal structure similarly to previous reports from laboratory settings and that even for animals domesticated over 12,000 years ago, an apparently mild stressor, resulting from human-animal interactions, can have similarly profound impacts on corticolimbic morphology.

Cattle discriminate between familiar and unfamiliar conspecifics by using only head visual cues.

Faces have features characteristic of the identity, age and sex of an individual. In the context of social communication and social recognition in various animal species, facial information is relevant for discriminating between familiar and unfamiliar individuals. Here, we present two experiments aimed at testing the ability of cattle (Bos taurus) to visually discriminate between heads (including face views) of familiar and unfamiliar conspecifics represented as 2D images. In the first experiment, we observed the spontaneous behaviour of heifers when images of familiar and unfamiliar conspecifics were simultaneously presented. Our results show that heifers were more attracted towards the image of a familiar conspecific (i.e., it was chosen first, explored more, and given more attention) than towards the image of an unfamiliar one. In the second experiment, the ability to discriminate between images of familiar and unfamiliar conspecifics was tested using a food-rewarded instrumental conditioning procedure. Eight out of the nine heifers succeeded in discriminating between images of familiar and unfamiliar conspecifics and in generalizing on the first trial to a new pair of images of familiar and unfamiliar conspecifics, suggesting a categorization process of familiar versus unfamiliar conspecifics in cattle. Results of the first experiment and the observation of ear postures during the learning process, which was used as an index of the emotional state, provided information on picture processing in cattle and lead us to conclude that images of conspecifics were treated as representations of real individuals.

Individual recognition in domestic cattle (Bos taurus): evidence from 2D-images of heads from different breeds.

BACKGROUND: In order to maintain cohesion of groups, social animals need to process social information efficiently. Visual individual recognition, which is distinguished from mere visual discrimination, has been studied in only few mammalian species. In addition, most previous studies used either a small number of subjects or a few various views as test stimuli. Dairy cattle, as a domestic species allow the testing of a good sample size and provide a large variety of test stimuli due to the morphological diversity of breeds. Hence cattle are a suitable model for studying individual visual recognition. This study demonstrates that cattle display visual individual recognition and shows the effect of both familiarity and coat diversity in discrimination. METHODOLOGY/PRINCIPAL FINDINGS: We tested whether 8 Prim'Holstein heifers could recognize 2D-images of heads of one cow (face, profiles, (3/4) views) from those of other cows. Experiments were based on a simultaneous discrimination paradigm through instrumental conditioning using food rewards. In Experiment 1, all images represented familiar cows (belonging to the same social group) from the Prim'Holstein breed. In Experiments 2, 3 and 4, images were from unfamiliar (unknown) individuals either from the same breed or other breeds. All heifers displayed individual recognition of familiar and unfamiliar individuals from their own breed. Subjects reached criterion sooner when recognizing a familiar individual than when recognizing an unfamiliar one (Exp 1: 3.1+/-0.7 vs. Exp 2: 5.2+/-1.2 sessions; Z = 1.99, N = 8, P = 0.046). In addition almost all subjects recognized unknown individuals from different breeds, however with greater difficulty. CONCLUSIONS/SIGNIFICANCE: Our results demonstrated that cattle have efficient individual recognition based on categorization capacities. Social familiarity improved their performance. The recognition of individuals with very different coat characteristics from the subjects was the most difficult task. These results call for studies exploring the mechanisms involved in face recognition allowing interspecies comparisons, including humans.

Visual discrimination by heifers (Bos taurus) of their own species.

Species discrimination has been described in several taxa but rarely in domestic animals. In contrast to wild species, domestic species present a great phenotypic variety. This study investigated whether 10 Prim'Holstein heifers (Bos taurus) could discriminate images of cows from images of other domestic animals. The experiment was based on simultaneous discrimination. Responses were obtained through instrumental conditioning using a food reward. In Experiment 1, the reward was associated with a cow face and, in the reversal learning task, with faces of other domestic species. The results showed that in both tasks, cows were able to reach the criterion in few sessions. Therefore, despite great phenotypic variety (a cognitive challenge) cows were able to visually discriminate their own species from other domestic species.