Human-animal interactions and machine-animal interactions in animals under human care: A summary of stakeholder and researcher perceptions and future directions.

Animals under human care are exposed to a potentially large range of both familiar and unfamiliar humans. Human-animal interactions vary across settings, and individuals, with the nature of the interaction being affected by a suite of different intrinsic and extrinsic factors. These interactions can be described as positive, negative or neutral. Across some industries, there has been a move towards the development of technologies to support or replace human interactions with animals. Whilst this has many benefits, there can also be challenges associated with increased technology use. A day-long Animal Welfare Research Network workshop was hosted at Harper Adams University, UK, with the aim of bringing together stakeholders and researchers (n = 38) from the companion, farm and zoo animal fields, to discuss benefits, challenges and limitations of human-animal interactions and machine-animal interactions for animals under human care and create a list of future research priorities. The workshop consisted of four talks from experts within these areas, followed by break-out room discussions. This work is the outcome of that workshop. The key recommendations are that approaches to advancing the scientific discipline of machine-animal interactions in animals under human care should focus on: (1) interdisciplinary collaboration; (2) development of validated methods; (3) incorporation of an animal-centred perspective; (4) a focus on promotion of positive animal welfare states (not just avoidance of negative states); and (5) an exploration of ways that machines can support a reduction in the exposure of animals to negative human-animal interactions to reduce negative, and increase positive, experiences for animals.

Human-directed behaviour in goats is not affected by short-term positive handling.

In addition to domestication, interactions with humans or task-specific training during ontogeny have been proposed to play a key role in explaining differences in human-animal communication across species. In livestock, even short-term positive interactions with caretakers or other reference persons can influence human-animal interaction at different levels and over different periods of time. In this study, we investigated human-directed behaviour in the 'unsolvable task' paradigm in two groups of domestic goats (Capra aegagrus hircus). One group was positively handled and habituated to a plastic box by the experimenter to retrieve a food reward, while the other group only received standard husbandry care and was habituated to the box without human assistance. In the unsolvable task, the lid was fixed to the box, with the reward inaccessible to the subjects. The goats were confronted with the unsolvable task three times. We observed no difference between the two groups regarding gaze and contact alternations with the experimenter when confronted with the task they cannot solve by themselves. The goats did not differ in their expression rates of both gaze and contact alternations over three repetitions of the unsolvable task; however, they showed earlier gaze and contact alternations in later trials. The results do not support the hypothesis that short-term positive handling or task-specific training by humans facilitates human-directed behaviour in goats. In contrast, standard husbandry care might be sufficient to establish humans as reference persons for farm animals in challenging situations.

Motor asymmetry in goats during a stepping task.

Behavioural lateralization consists of perceptual and motor lateralization and provides adaptive advantages such as a general increase in brain efficiency. Motor laterality refers to the preferred use of either left or right limbs or organs to perform a specific task. We investigated motor laterality in goats (Capra hircus), using the First-stepping Task. During this task, the first foreleg used to step off a board after standing with both forelimbs was recorded. Subjects varied individually in their expression of motor lateralization with 36.6% of subjects showing individual-level asymmetries. However, goats as a group did not show a preference for a specific foreleg or lateralization in general. Our results support the hypothesis that the need to coordinate behaviour among conspecifics might be important for determining the presence of lateralization at the population level. We suggest that future research investigates how social complexity might affect population-level asymmetries, and whether stimuli with high emotional valence impact on lateralization presence and level (i.e., individual or population).

'Goats that stare at men'--revisited: do dwarf goats alter their behaviour in response to eye visibility and head direction of a human?

Being able to recognise when one is being observed by someone else is thought to be adaptive during cooperative or competitive events. In particular for prey species, this ability should be of use in the context of predation. A previous study reported that goats (Capra aegagrus hircus) alter their behaviour according to the body and head orientation of a human experimenter. During a food anticipation task, an experimenter remained in a particular posture for 30 s before delivering a reward, and the goats' active anticipation and standing alert behaviour were analysed. To further evaluate the specific mechanisms at work, we here present two additional test conditions. In particular, we investigated the effects of the eye visibility and head orientation of a human experimenter on the behaviour of the goats (N = 7). We found that the level of the subjects' active anticipatory behaviour was highest in the conditions where the experimenter was directing his head and body towards the goat ('Control' and 'Eyes closed' conditions), but the anticipatory behaviour was significantly decreased when the body ('Head only') or the head and body of the experimenter were directed away from the subject ('Back' condition). For standing alert, we found no significant differences between the three conditions in which the experimenter was directing his head towards the subject ('Control', 'Eyes closed' and 'Head only'). This lack of differences in the expression of standing alert suggests that goats evaluate the direction of a human's head as an important cue in their anticipatory behaviour. However, goats did not respond to the visibility of the experimenter's eyes alone.

Goats display audience-dependent human-directed gazing behaviour in a problem-solving task.

Domestication is an important factor driving changes in animal cognition and behaviour. In particular, the capacity of dogs to communicate in a referential and intentional way with humans is considered a key outcome of how domestication as a companion animal shaped the canid brain. However, the lack of comparison with other domestic animals makes general conclusions about how domestication has affected these important cognitive features difficult. We investigated human-directed behaviour in an 'unsolvable problem' task in a domestic, but non-companion species: goats. During the test, goats experienced a forward-facing or an away-facing person. They gazed towards the forward-facing person earlier and for longer and showed more gaze alternations and a lower latency until the first gaze alternation when the person was forward-facing. Our results provide strong evidence for audience-dependent human-directed visual orienting behaviour in a species that was domesticated primarily for production, and show similarities with the referential and intentional communicative behaviour exhibited by domestic companion animals such as dogs and horses. This indicates that domestication has a much broader impact on heterospecific communication than previously believed.

Domestic pigs' (Sus scrofa domestica) use of direct and indirect visual and auditory cues in an object choice task.

Recently, foraging strategies have been linked to the ability to use indirect visual information. More selective feeders should express a higher aversion against losses compared to non-selective feeders and should therefore be more prone to avoid empty food locations. To extend these findings, in this study, we present a series of studies investigating the use of direct and indirect visual and auditory information by an omnivorous but selective feeder-the domestic pig. Subjects had to choose between two buckets, with only one containing a reward. Before making a choice, the subjects in Experiment 1 (N = 8) received full information regarding both the baited and non-baited location, either in a visual or auditory domain. In this experiment, the subjects were able to use visual but not auditory cues to infer the location of the reward spontaneously. Additionally, four individuals learned to use auditory cues after a period of training. In Experiment 2 (N = 8), the pigs were given different amounts of visual information about the content of the buckets-lifting either both of the buckets (full information), the baited bucket (direct information), the empty bucket (indirect information) or no bucket at all (no information). The subjects as a group were able to use direct and indirect visual cues. However, over the course of the experiment, the performance dropped to chance level when indirect information was provided. A final experiment (N = 3) provided preliminary results for pigs' use of indirect auditory information to infer the location of a reward. We conclude that pigs at a very young age are able to make decisions based on indirect information in the visual domain, whereas their performance in the use of indirect auditory information warrants further investigation.

'Goats that stare at men': dwarf goats alter their behaviour in response to human head orientation, but do not spontaneously use head direction as a cue in a food-related context.

Recently, comparative research on the mechanisms and species-specific adaptive values of attributing attentive states and using communicative cues has gained increased interest, particularly in non-human primates, birds, and dogs. Here, we investigate these phenomena in a farm animal species, the dwarf goat (Capra aegagrus hircus). In the first experiment, we investigated the effects of different human head and body orientations, as well as human experimenter presence/absence, on the behaviour of goats in a food-anticipating paradigm. Over a 30-s interval, the experimenter engaged in one of four different postures or behaviours (head and body towards the subject-'Control', head to the side, head and body away from the subject, or leaving the room) before delivering a reward. We found that the level of subjects' active anticipatory behaviour was highest in the control condition and decreased with a decreasing level of attention paid to the subject by the experimenter. Additionally, goats 'stared' (i.e. stood alert) at the experimental set-up for significantly more time when the experimenter was present but paid less attention to the subject ('Head' and 'Back' condition) than in the 'Control' and 'Out' conditions. In a second experiment, the experimenter provided different human-given cues that indicated the location of a hidden food reward in a two-way object choice task. Goats were able to use both 'Touch' and 'Point' cues to infer the correct location of the reward but did not perform above the level expected by chance in the 'Head only' condition. We conclude that goats are able to differentiate among different body postures of a human, including head orientation; however, despite their success at using multiple physical human cues, they fail to spontaneously use human head direction as a cue in a food-related context.

Juvenile domestic pigs (Sus scrofa domestica) use human-given cues in an object choice task.

Research on the comprehension of human-given cues by domesticated as well as non-domesticated species has received considerable attention over the last decade. While several species seem to be capable of utilizing these cues, former work with domestic pigs (Sus scrofa domestica) has shown inconclusive results. In this study, we investigated the use of human-given cues in an object choice task by young domestic pigs (N = 17; 7 weeks of age) who had very limited human contact prior to the experiments. Subjects had to choose between two bowls of which only one was baited with a reward. Over the course of five experiments, pigs were able to use proximal and, with some constraints, also distal pointing cues presented in both a dynamic-sustained and in a momentary manner. When the experimenter was pointing from the incorrect bowl towards the correct one, most of the subjects had problems solving the task-indicating that some form of stimulus/local enhancement affected pigs' decision making. Interestingly, pigs were able to utilize the body and head orientation of a human experimenter to locate the hidden reward but failed to co-orient when head or body orientation of the experimenter was directed into distant space with no bowls present. Control trials ruled out the possibility that other factors (e.g. odour cues) affected subjects' choice behaviour. Learning during experiments played a minor role and only occurred in three out of twelve test conditions. We conclude that domestic pigs, even at a very young age, are skilful in utilizing various human-given cues in an object choice task-raising the question whether pigs only used stimulus/local enhancement and associative learning processes or whether they were able to comprehend the communicative nature of at least some of these cues.

The use of gaze to study cognition: limitations, solutions, and applications to animal welfare.

The study of gaze responses, typically using looking time paradigms, has become a popular approach to improving our understanding of cognitive processes in non-verbal individuals. Our interpretation of data derived from these paradigms, however, is constrained by how we conceptually and methodologically approach these problems. In this perspective paper, we outline the application of gaze studies in comparative cognitive and behavioral research and highlight current limitations in the interpretation of commonly used paradigms. Further, we propose potential solutions, including improvements to current experimental approaches, as well as broad-scale benefits of technology and collaboration. Finally, we outline the potential benefits of studying gaze responses from an animal welfare perspective. We advocate the implementation of these proposals across the field of animal behavior and cognition to aid experimental validity, and further advance our knowledge on a variety of cognitive processes and welfare outcomes.

Domestication and breeding objective did not shape the interpretation of physical and social cues in goats (Capra hircus).

Artificial selection by humans, either through domestication or subsequent selection for specific breeding objectives, drives changes in animal cognition and behaviour. However, most previous cognitive research comparing domestic and wild animals has focused on companion animals such as canids, limiting any general claims about the effects of artificial selection by humans. Using a cognitive test battery, we investigated the ability of wild goats (non-domestic, seven subjects), dwarf goats (domestic, not selected for milk production, 15 subjects) and dairy goats (domestic, selected for high milk yield, 18 subjects) to utilise physical and social cues in an object choice task. To increase the heterogeneity of our test samples, data for domestic goats were collected by two experimenters at two research stations (Agroscope; Research Institute for Farm Animal Biology). We did not find performance differences between the three groups in the cognitive test battery for either physical or social cues. This indicates that for a domestic non-companion animal species, domestication and selection for certain breeding objectives did not measurably shape the physical and cognitive skills of goats.

Toward assessing the role of dietary fatty acids in lamb's neurological and cognitive development.

Understanding and measuring sheep cognition and behavior can provide us with measures to safeguard the welfare of these animals in production systems. Optimal neurological and cognitive development of lambs is important to equip individuals with the ability to better cope with environmental stressors. However, this development can be affected by nutrition with a special role from long-chain fatty acid supply from the dam to the fetus or in lamb's early life. Neurological development in lambs takes place primarily during the first two trimesters of gestation. Through late fetal and early postnatal life, the lamb brain has a high level of cholesterol synthesis. This rate declines rapidly at weaning and remains low throughout adulthood. The main polyunsaturated fatty acids (PUFA) in the brain are ω-6 arachidonic acid and ω-3 docosahexaenoic acid (DHA), which are elements of plasma membranes' phospholipids in neuronal cells. DHA is essential for keeping membrane integrity and is vital for normal development of the central nervous system (CNS), and its insufficiency can damage cerebral functions and the development of cognitive capacities. In sheep, there is evidence that supplying PUFA during gestation or after birth may be beneficial to lamb productive performance and expression of species-specific behaviors. The objective of this perspective is to discuss concepts of ruminant behavior and nutrition and reflect on future research directions that could help to improve our knowledge on how dietary fatty acids (FA) relate to optimal neurological and cognitive development in sheep.

The Academic, Societal and Animal Welfare Benefits of Open Science for Animal Science.

Animal science researchers have the obligation to reduce, refine, and replace the usage of animals in research (3R principles). Adherence to these principles can be improved by transparently publishing research findings, data and protocols. Open Science (OS) can help to increase the transparency of many parts of the research process, and its implementation should thus be considered by animal science researchers as a valuable opportunity that can contribute to the adherence to these 3R-principles. With this article, we want to encourage animal science researchers to implement a diverse set of OS practices, such as Open Access publishing, preprinting, and the pre-registration of test protocols, in their workflows.

Responsiveness of domesticated goats towards various stressors following long-term cognitive test exposure.

Current evidence suggests that frequent exposure to situations in which captive animals can solve cognitive tasks may have positive effects on stress responsiveness and thus on welfare. However, confounding factors often hamper the interpretation of study results. In this study, we used human-presented object-choice tests (in form of visual discrimination and reversal learning tests and a cognitive test battery), to assess the effect of long-term cognitive stimulation (44 sessions over 4-5 months) on behavioural and cardiac responses of female domestic goats in subsequent stress tests. To disentangle whether cognitive stimulation per se or the reward associated with the human-animal interaction required for testing was affecting the stress responsiveness, we conditioned three treatment groups: goats that were isolated for participation in human-presented cognitive tests and rewarded with food ('Cognitive', COG treatment), goats that were isolated as for the test exposure and rewarded with food by the experimenter without being administered the object-choice tests ('Positive', POS treatment), and goats that were isolated in the same test room but neither received a reward nor were administered the tests ('Isolation', ISO treatment). All treatment groups were subsequently tested in four stress tests: a novel arena test, a novel object test, a novel human test, and a weighing test in which goats had to enter and exit a scale cage. All treatment groups weretested at the same two research sites, each using two selection lines, namely dwarf goats, not selected for production traits, and dairy goats, selected for high productivity. Analysing the data with principal component analysis and linear mixed-effects models, we did not find evidence that cognitive testing per se (COG-POS contrast) reduces stress responsiveness of goats in subsequent stress tests. However, for dwarf goats but not for dairy goats, we found support for an effect of reward-associated human-animal interactions (POS-ISO contrast) at least for some stress test measures. Our results highlight the need to consider ontogenetic and genetic variation when assessing stress responsiveness and when interacting with goats.

Seven steps to enhance Open Science practices in animal science.

The Open Science movement aims at ensuring accessibility, reproducibility, and transparency of research. The adoption of Open Science practices in animal science, however, is still at an early stage. To move ahead as a field, we here provide seven practical steps to embrace Open Science in animal science. We hope that this paper contributes to the shift in research practices of animal scientists towards open, reproducible, and transparent science, enabling the field to gain additional public trust and deal with future challenges to guarantee reliable research. Although the paper targets primarily animal science researchers, the steps discussed here are also applicable to other research domains.

Horses' (Equus caballus) Ability to Solve Visible but Not Invisible Displacement Tasks Is Associated With Frustration Behavior and Heart Rate.

Many frameworks have assessed the ultimate and ontogenetic underpinnings in the development of object permanence, but less is known about whether individual characteristics, such as sex or training level, as well as proximate factors, such as arousal or emotional state, affect performance in these tasks. The current study investigated horses' performance in visible and invisible displacement tasks and assessed whether specific ontogenetic, behavioral, and physiological factors were associated with performance. The study included 39 Icelandic horses aged 2-25 years, of varying training levels. The horses were exposed to three tasks: (a) a choice test (n = 37), (b) a visible displacement task (n = 35), and (c) an invisible displacement task (n = 31). 27 horses in the choice test, and 8 horses in the visible displacement task, performed significantly better than expected by chance, while none did so in the invisible displacement task. This was also reflected in their group performance, where horses performed above chance level in the choice task and the visible displacement task only. In the invisible displacement task, the group performed significantly worse than expected by chance indicating that horses persistently chose the side where they had last seen the target. None of the individual characteristics included in the study had an effect on performance. Unsuccessful horses had higher heart rate levels, and expressed more behavior indicative of frustration, likely because of their inability to solve the task. The increased frustration/arousal could lead to a negative feedback loop, which might hamper performance in subsequent trials. Care should thus be taken in future experimental designs to closely monitor the arousal level of the tested individuals in order to safeguard comparability.

Goats (Capra hircus) From Different Selection Lines Differ in Their Behavioural Flexibility.

Given that domestication provided animals with more stable environmental conditions, artificial selection by humans has likely affected animals' ability to learn novel contingencies and their ability to adapt to changing environments. In addition, the selection for specific traits in domestic animals might have an additional impact on subjects' behavioural flexibility, but also their general learning performance, due to a re-allocation of resources towards parameters of productivity. To test whether animals bred for high productivity would experience a shift towards lower learning performance, we compared the performance of dwarf goats (not selected for production, 15 subjects) and dairy goats (selected for high milk yield, 18 subjects) in a visual discrimination learning and reversal learning task. Goats were tested individually in a test compartment and were rewarded by choosing either a white or a black cup presented by the experimenter on a sliding board behind a crate. Once they reached a designated learning criterion in the initial learning task, they were transferred to the reversal learning task. To increase the heterogeneity of our test sample, data was collected by two experimenters at two research stations following a similar protocol. Goats of both selection lines did not differ in the initial discrimination learning task in contrast to the subsequent reversal learning task. Dairy goats reached the learning criterion slower compared to dwarf goats (dairy goats = 9.18 sessions; dwarf goats = 7.74 sessions; P = 0.016). Our results may indicate that the selection for milk production might have affected behavioural flexibility in goats. These differences in adapting to changing environmental stimuli might have an impact on animal welfare e.g., when subjects have to adapt to new environments or changes in housing and management routines.

Goats Follow Human Pointing Gestures in an Object Choice Task.

Dogs (Canis lupus familiaris) are extremely adept in interpreting human-given cues, such as the pointing gesture. However, the underlying mechanisms on how domestic non-companion species use these cues are not well understood. We investigated the use of human-given pointing gestures by goats (Capra hircus) in an object choice task, where an experimenter surreptitiously hid food in one of two buckets. Subjects first had to pass a pre-test where the experimenter indicated the location of the food to the subject by a proximal pointing gesture. Subjects that succeeded in the use of this gesture were transferred to the actual test. In these subsequent test trials, the experimenter indicated the location of the food to the subject by using three different pointing gestures: proximal pointing from a middle position (distance between target and index finger: 30 cm), crossed pointing from the middle position (distance between target and index finger: 40 cm), asymmetric pointing from the position of the non-baited bucket (distance between target and index finger: 90 cm). Goats succeeded in the pointing gestures that presented an element of proximity (proximal and crossed) compared to when the experimenter was further away from the rewarded location (asymmetric). This indicates that goats can generalize their use of the human pointing gesture but might rely on stimulus/local enhancement rather than referential information. In addition, goats did not improve their responses over time, indicating that no learning took place. The results provide a greater understanding of human-animal interactions and social-cognitive abilities of farm animals, which allows for the provision of enhanced management practices and welfare conditions.

Social Referencing in the Domestic Horse.

Dogs and cats use human emotional information directed to an unfamiliar situation to guide their behavior, known as social referencing. It is not clear whether other domestic species show similar socio-cognitive abilities in interacting with humans. We investigated whether horses (n = 46) use human emotional information to adjust their behavior to a novel object and whether the behavior of horses differed depending on breed type. Horses were randomly assigned to one of two groups: an experimenter positioned in the middle of a test arena directed gaze and voice towards the novel object with either (a) a positive or (b) a negative emotional expression. The duration of subjects' position to the experimenter and the object in the arena, frequency of gazing behavior, and physical interactions (with either object or experimenter) were analyzed. Horses in the positive condition spent more time between the experimenter and object compared to horses in the negative condition, indicating less avoidance behavior towards the object. Horses in the negative condition gazed more often towards the object than horses in the positive condition, indicating increased vigilance behavior. Breed types differed in their behavior: thoroughbreds showed less human-directed behavior than warmbloods and ponies. Our results provide evidence that horses use emotional cues from humans to guide their behavior towards novel objects.

Long-Term Socialization with Humans Affects Human-Directed Behavior in Goats.

Throughout their evolutionary history, humans have tried to domesticate a variety of wild terrestrial mammals, resulting in a limited number that has been successfully domesticated. Among these domesticated species, domestic goats (Capra aegagrus hircus) are a useful model species to study the effects of ontogenesis on the socio-cognitive abilities of domestic non-companion animals in their interactions with humans. To this end, the behavioral responses of two groups of goats with a different background of human socialization (high and low socialization) were compared in the impossible task test, an experimental paradigm aimed to study socio-cognitive skills and the tendency to interact with humans. Our results show that, when the task became impossible to solve, goats with a higher level of socialization interacted with the experimenter for a greater amount of time than subjects in the low socialization group, whereas the latter group exhibited increased door directed behavior. Overall, highly socialized goats made more social contact with humans compared to the other group in the impossible task paradigm.

Perceptual lateralization of vocal stimuli in goats.

Functional asymmetries, for example, the preferential involvement of 1 brain hemisphere to process stimuli, may increase brain efficiency and the capacity to carry out tasks simultaneously. We investigated which hemisphere was primarily involved in processing acoustic stimuli in goats using a head-orienting paradigm. Three playbacks using goat vocalizations recorded in different contexts: food anticipation (positive), isolation (negative), food frustration (negative), as well as 1 playback involving dog barks (negative) were presented on the left and right sides of the test subjects simultaneously. The head-orienting response (left or right) and latency to resume feeding were recorded. The direction of the head-orienting response did not differ between the various playbacks. However, when the head-orienting response was tested against chance level, goats showed a right bias regardless of the stimuli presented. Goats responded more to dog barks than to food frustration calls, whereas responses to food anticipation and isolation calls were intermediate. In addition, the latency to resume feeding, an indicator of fear reaction, was not affected by the kind of vocalization presented. These results provide evidence for asymmetries in goat vocal perception of emotional-linked conspecific and heterospecific calls. They also suggest involvement of the left brain hemisphere for processing acoustic stimuli, which might have been perceived as familiar and non-threatening.