Social behavior in farm animals
Send to text email RefWorks EndNote printer. Social behavior in farm animals. Responsibility edited by L. Online Available online. CAB eBooks Full view. More options. Limited preview. Contributor Keeling, L. Linda J. Gonyou, H. Harold W. International issuing body. Bibliography Includes bibliographical references index.
In future studies, the combination of personality and social behavior measurements will hopefully shed more light on the complex social dynamics in cattle groups and its connection with animal welfare. I agree on how important it is to get social group right and minimize changes. Thanks for this interesting and informative article. Du kommentierst mit Deinem WordPress.
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In contrast to the use of human pointing gestures, horses failed to interpret the head direction of a human experimenter 19 , , but they were able to use the head direction of a depiction of a conspecific to infer the location of a hidden reward Horses appear to wait for humans to solve a task to obtain food instead of trying to solve the task themselves They also show human-directed behavior when confronted with an inaccessible food reward 43 , and they frequently gazed at an experimenter who was positioned near the reward.
In addition, horses also considered the attentional stance of the experimenter during the task, depending on whether the experimenter was turned toward or away from them. Horse owners often think that abnormal or stereotypic behaviors are learned through observation ; however, several studies have shown that horses do not perform better after watching a demonstrator horse both in a simple operant conditioning task or in a discrimination task — Krueger and Heinze found that experimental horses copied specific following behaviors toward humans when a dominant conspecific followed the path of a human handler.
However, studies in horses on imitation of complex behaviors have shown inconclusive results so far, which may be due to the lack of appropriate experimental designs Recently, Ahrendt et al. In contrast, a study by Krueger et al. However, this was restricted to young, low-ranking and more exploratory horses who were learning from older group members. Additionally, test horses learned the same instrumental task faster than control horses when they were frequently exposed to a human demonstrator who was solving the instrumental task When mares were habituated to the exposure of a human experimenter or unfamiliar and potential frightening objects, their foals showed less fear reactions in standardized fear tests or in approaching unfamiliar humans, indicating the social transfer of information from mother to offspring 47 , No studies on the evaluation of more complex socio-cognitive phenomena, such as prosocial behavior or inequity aversion, are available.
Pigs as omnivorous animals exhibit high foraging flexibility that is reflected in their dietary spectrum Therefore, it should be of no surprise to find cognitive capacities that increase their ability to exploit food sources, either in relocating previously known food patches or in finding new ones.
Young pigs have been found to understand that once hidden, objects do not cease to exist, but had problems following more complex movements of hidden objects Albiach-Serrano et al. One of these tasks involved the presentation of a slighted board that covered a hidden reward, and another task involved a baited cup that was shaken to produce a rattling noise. Although pigs could solve the tasks, it was unclear whether they simply relied on stimulus enhancement cues i. Nawroth and von Borell 24 repeated the latter task that used a shaking bucket with a modified setup. Here, pigs were tested in their ability to use indirect visual and auditory stimuli i.
Pigs used indirect visual cues and, to some degree, indirect auditory cues, i. Again, the experimental design could not exclude the possibility that pigs were simply avoiding the non-rewarded location and relied on learned contingencies. However, these results provide support that pigs can rapidly adapt to new foraging situations. Although it was demonstrated that pigs were able to differentiate between different amounts of food , , more complex studies that evaluated numerical competence should be conducted to investigate the cognitive mechanisms involved in this process.
In addition, no studies involving categorization abilities or tool use have been conducted with pigs. Pigs are highly gregarious animals and thus establish stable social hierarchies. This requires good discriminatory abilities to differentiate between group members and between familiar and non-familiar individuals. Studies found pigs were able to distinguish unfamiliar from familiar conspecifics ; additionally, pigs could differentiate familiar individuals using visual, auditory or olfactory cues alone 29 , However, 2D head cues were insufficient for pigs to discriminate between familiar conspecifics ; thus, features other than head cues may be more salient for pigs.
For example, studies on the ability of pigs to visually discriminate between humans showed that pigs mainly relied on the body height and upper torso of the human 36 , 37 , Nawroth et al. Juvenile pigs had to choose between two unfamiliar persons, while only one human focused attention on the test subject; the test conditions varied, and it was assumed that only the attentive human would provide food immediately or would provide food at all.
While the subject performance in the choice task was poor and the results were inconclusive, two approach styles were distinguished during decision making. Here, pigs chose the attentive person more often when they approached non-impulsively i. An object choice task is another well-known test used to investigate heterospecific communicative abilities. Here, subjects must choose between two potential baiting locations, of which only one contains a reward. To find the reward, a human administers different types of cues e. Given that pigs, unlike dogs, are not domesticated for companionship but are commonly raised as meat stock, their human social environment is often less demanding than that of dogs, and this might hamper their inclination to rely on human-given cues.
This was partly supported by the findings of Albiach-Serrano et al. In contrast, Nawroth et al. However, pigs could have learned the gestures rapidly or, in terms of the pointing gestures, relied on stimulus enhancement. Thus, it is not clear whether the pigs were able to comprehend the referential and intentional nature of the human-given cues or whether they used learned contingencies to solve the task [see ]. Only a few studies have shown that pigs seem to be capable of social learning, either vertically 48 , 49 or horizontally However, in most examples, learning was directly related to food cues and could have been acquired through direct snout-snout interactions rather than visual observation.
Based on their foraging ecology, it would be advantageous to not only learn what to eat but also learn how to acquire und process particular food sources. Recently, it has been demonstrated that juvenile Kunekune pigs learned how to manipulate objects i. However, there have not been any studies on horizontal social learning that involves problem-solving or object manipulation for pigs.
Pigs are highly competitive foragers, and they rely on patchily distributed food sources. Therefore, it is unsurprising that dominant pigs readily start to scrounge on subordinate individuals of the group by following them to food patches they have discovered In terms of this exploitation, it seems adaptive to be aware of the presence and attentive states of other individuals.
Indeed, research suggests that pigs are able to attribute attentive states toward other individuals. Using an informed forager paradigm , Held et al.
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Overall, the subordinates were more likely to show food-directed behavior when the chances of arriving at the food source ahead of their exploiters were higher. Intriguingly, subordinates adjusted their foraging behavior based on whom they were foraging with, i. In another study, Held et al. Most pigs did not follow their companions, likely to avoid competitive and aggressive behavior. These studies suggest that pigs use body cues to discriminate between the different attentive states of conspecifics and that they, to some degree, might be able to interpret the visual perspective of others.
No studies have focused on more complex socio-cognitive phenomena, such as prosocial behavior or inequity aversion, in pigs. For example, sheep have been shown to use species-based categorization when selecting their diet. Sheep generalized their aversion among species and classes of plants into distinct categories 15 , Experiments under husbandry conditions have also shown that goats have more abstract learning and categorization abilities.
By using an automated learning device, Langbein et al. Using a similar experimental setup, individual goats were found to be capable of learning the oddity concept. When presented with an odd stimulus and three identical non-odd stimuli on the automated learning device, these animals consistently chose the odd stimulus after the initial training Small ruminants possess a sophisticated understanding of their physical environment.
When confronted with a task in which a reward was hidden in one of two opaque containers that then switched positions, the goats showed moderate to high success rates in finding the reward Individual goats, but not sheep, can also infer the location of a reward through exclusion. When provided with a choice between two containers while only one was baited with a reward , goats and sheep were able to use direct information i. However, only goats, but not sheep, used indirect information i.
Due to the different feeding preferences of goats low-fiber feeders; dietary browsers compared to sheep high-fiber feeders; dietary grazers , goats might prefer and forage more selectively than do sheep. This higher flexibility may have led to the avoidance of a potential, but empty, food location in goats but not in sheep. In fact, an earlier study by Hosoi et al. No studies have investigated number discrimination or tool use for either goats or sheep.
Goats and sheep live in fission-fusion societies with stable dominance hierarchies , ; thus, it should be highly advantageous for them to remember and recognize familiar group members. When presented with pairs of face images or vocalizations, sheep were able to discriminate between different species including humans , breeds and sexes of their same breed.
The sheep learned to distinguish between individual adult sheep faces, but breed and social familiarity influenced the level of discrimination performance , Sheep behavioral and neural activities also indicated they remembered faces of familiar conspecifics after more than 2 years, which suggests sheep have a high capacity for learning and memory 31 ; moreover, that 2D images of conspecific faces seemed to be represented as a 3D equivalent of the real-life individual.
Additional evidence for this was reported in a recent experiment where sheep recognized a familiar handler when the face of this handler was presented as a 2D image in a discrimination task For example, Keil et al. Surprisingly, there have been no investigations to determine how goats discriminate between humans. There is broad popular interest in the relationship between humans and small ruminants, specifically on how small ruminants react to being observed by humans e. Indeed, human gaze appeared to alter the behavior of domestic sheep compared to situations where there was no human eye contact : Sheep glanced at the gazing human more often and showed higher levels of activity.
For instance, when an inaccessible reward was positioned in front of a goat, an experimenter engaged in different postures that resembled different levels of attention toward the subject e. These results indicated that the goats adapted their behavior based on the head and body orientation, but not the eye visibility, of the experimenter as a means of being given a reward. The results related to the body orientation were confirmed in a different experiment that used a choice paradigm; specifically, goats could choose to beg for food from either an attentive or inattentive person i.
However, the head orientation of humans did not affect the choice behavior of goats The authors found that goats were able to utilize human pointing gestures, but goats could not interpret the head or gaze direction of a human to find the hidden reward. In contrast to the negative findings regarding the human head and gaze direction, goats could follow the gaze direction of conspecifics into distant space 41 , which is an extremely important trait in terms of predator detection Goats also showed human-directed behavior in the form of frequent gaze alternations toward humans when they were confronted with an inaccessible food reward 44 , 45 , which was similar to what has been found in dogs and horses 43 , Here, as well, goats considered the attentional stance of the experimenter and altered their use of gaze alternations during the task depending on whether the experimenter was turned toward or away from them.
In small ruminants, vertical information transfer between individuals e. For example, lambs can learn how to use an artificial teat from knowledgeable lambs that where transferred into their group Baciadonna et al.
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Goats relied more on personal information than on social information when both types were available and conflicted with each other. Briefer et al. Goats quickly learned the task on an individual basis. However, goats that observed a demonstrator goat first did not learn the task faster compared to goats that did not see a demonstration.
This indicated that the goats relied on individual experience rather than on social experience in this particular task. In contrast to these previous findings, human demonstration improved goats' performance in a spatial problem-solving task Goats that experienced a human demonstrator detouring a V-shaped hurdle solved the detour faster compared to goats that did not receive a demonstration.
No studies are available regarding more complex socio-cognitive phenomena, such as prosocial behavior or inequity aversion. General knowledge of how farm animals perceive and address their physical and social environment is of interest for improving housing and management practices; it can also be used in future studies in the different fields of applied ethology 64 , — Livestock housing conditions are often structurally simple and offer limited possibilities to exhibit species-appropriate behavior , These limitations can lead to boredom and frustration, which promotes the appearance of abnormal behavior, especially that which is related to stress and reduced welfare , One way to decrease the level of boredom and frustration in livestock is to enhance the biological relevance of the housing conditions of farm animals; this can be done through the provision of a variety of new structures, items and challenges that are related to the animals' needs and natural behavioral repertoire This so-called environmental enrichment is supposed to elicit a higher degree of behavioral diversity by increasing the physical and social complexity of the livestock environment , Providing specific cognitive enrichment, e.
A detailed understanding of the cognitive capacities of farm animals, and especially their understanding of the physical properties of their environment, will provide help to design proper forms of structural and cognitive enrichment — The integration of different types of cognitive enrichment into the housing of farm animals has received little attention; to date, approaches have been based on the instrumental or operant learning skills of subjects.
Animals learned the task, which was taught using a combination of classical and operant conditioning, within a short time period. After several weeks of receiving food via the CFS, piglets showed less stress during feeding and evoked longer lasting positive emotions compared to the control animals; moreover, the piglets displayed less abnormal behavior and showed reduced signs of fear in the context of being faced with a challenging environment When goats were successively confronted with several different visual discrimination tasks through the use of a computer-based learning device that was integrated into the home pen, their heart rates initially increased but then decreased as the goats showed increased learning performance in consecutive tasks This indicated that the goats had been exposed to a challenging task that induced positive eustress It also appeared that goats seemed to seek challenges; for example, goats continued to operate the rewarding learning device even when an identical reward was available without the requirement of additional cognitive effort This behavioral pattern is linked to the concept of contrafreeloading and indicates that successfully coping with a cognitively challenging device or procedure could have intrinsic reinforcing properties beyond the extrinsic reward itself.
Further evidence of this has been provided in experiments on heifers and beagles, who showed greater positive excitement after learning an operant task than did control animals who did not have to solve the task themselves. This excitement that accompanies success is believed to be related to positive affective states in non- human animals , Regardless of which device or procedure is used to cognitively challenge the animals, the device or procedure must be modified regularly to be remain challenging, e.
Otherwise, the animals will develop routine-like behavior, and the device will no longer be challenging and enriching. On the other hand, to develop appropriate challenges that do not overstrain the animals, we need to have detailed knowledge on the species-specific problem-solving abilities of livestock animals.
As described, the first attempts to integrate cognitively challenging tasks into housing to promote cognitive enrichment have focused on operant conditioning tasks. In the future, in addition to relying on learning, it may be important to also rely on physico-cognitive traits such as categorization abilities or making inferences to pave the way for new opportunities on how to integrate changing challenges into the housing environments of animals Table 1.
However, the limited availability of solid evidence of the physico-cognitive capacities discussed in this review demonstrates how little we actually know about the problem-solving abilities of farm animals and their perception of their physical environment. When farm animals are transferred to new environments during ontogenesis and confronted with new devices, e.
During these situations, it might be highly beneficial to rely on the mechanisms related to social or observational learning from experienced conspecifics or humans who act as demonstrators; this may facilitate the adaptation process to the novel housing conditions. To achieve this, we must identify the distinct and species-specific mechanisms of social learning in farm animals see Table 2. In sheep, social learning plays an important role in the transmission of diet preferences Housing dairy calves in social groups results in increased weaning weights compared with calves that have been individually housed; this result is likely due to the increased intake of dry matter, which is often attributed to social learning or social facilitation during feeding , In lambs, learning to suckle from an artificial teat was facilitated when an experienced partner was in the group compared to the control group that did not have a demonstrator.
Frontiers | Farm Animal Cognition—Linking Behavior, Welfare and Ethics | Veterinary Science
Experimental lambs sniffed or sucked the teat more often than did the lambs in the control group Future research should identify which potential mechanisms, e. To improve handling practices under farm management conditions, it is important to know how livestock perceive and interact with humans. Based on this knowledge, applied research can be better adjusted to assess how subtle human behavioral changes can have rewarding or adverse effects on livestock behavior During recent decades, it has been shown that different farm animal species can discriminate between individual humans see Table 2 , and animals may use individual humans to predict positive or negative events that are routinely involved in housing and management , Mini pigs that were positively reinforced by their handlers over several weeks discriminated between the familiar keeper and a stranger in a Y-maze test using auditory, visual and olfactory cues Similarly, cattle have been shown to discriminate between a handler who reinforced an operant action and a handler who did not A differential reaction towards humans has been observed in sheep; for example, lambs handled by an unfriendly handler generalized their fear responses toward familiar and unfamiliar humans, while gently treated lambs discriminated between familiar and unfamiliar humans Horses have also been shown to generalize their experiences with positive and negative stockpersons from one human to another This gradual variation in the abilities of different livestock species to differentiate between individual humans based on their attitude toward the animals might have profound implications for animal housing and management.
Next, to avoid negative impacts, it is also important to identify and implement rewarding human-animal interactions Studies on tactile human-animal interactions have demonstrated that there is potential to identify relevant stress-reducing behavior by stockpersons during handling and transport processes — For example, direct interactions between farm animals and their handlers e.
Furthermore, various farm animal species follow human-given communicative cues and differ in their behavior based on whether a human gives them attention or not see Table 2. Although most of these experiments included previous positive feedback from humans, animals will also likely show different responses based on the attentional stance of a human in more aversive settings, e. Some livestock species, such as goats and horses 43 , 44 , , have been shown to also engage in communication efforts directed at humans Table 2.
Animals used behaviors, such as gaze alternations, to direct the attention of a human toward a problem that the animal could not solve themselves. In terms of applying this to the farm, the skilful reading of these cues could lead to the improved detection of livestock needs. Advanced communication between livestock and humans does exist and using it in an applied setting might help decrease stress during handling and better meet the needs of the animals.
However, no relevant research on this topic has been conducted yet. The question about how we should treat farm animals based on their complex social, cognitive, and emotional capacities is a question of philosophy, and more specifically, of animal ethics Several capacity-oriented approaches exist, and these, in one way or another, link the moral status of animals to their abilities However, the role of such abilities and the weight they are assigned will vary based on the different normative frameworks of these theories Two important primary approaches should be separated, as they lead to implications that partly overlap but are also profoundly different in their nature and impact.
The moral implications of farm animal cognition can first be assessed by welfare ethics [understood as an interdisciplinary endeavor among welfare scientists, biologists, veterinarians, and philosophers — ]. Second, one can complete such an assessment by applying ethical theories that go beyond welfare [e. It has been recognized that the links between cognition and welfare are important from an economic perspective in terms of its relation to production success However, from the perspective of animal ethics, it can also be asked whether animal cognition and this connection to animal welfare matters from the perspective of the animals.
On the one hand, the nature of animal minds with regard to their capacity to feel pain and other adverse feelings can form the basis for an ethical account of experiential well-being in animals On the other hand, experiential well-being is at the core of one of the most important and most recognized principles in animal ethics, i. This principle asks us not to cause extensive unnecessary harm to others without their consent , which is a claim that can be specified into several sub-rules.
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Among them is, most importantly, the rule to provide for the basic physical and psychological needs of animals that are under human care This means that welfare ethics establishes an argument that connects physical and psychological needs with welfare and connects welfare with a normative value. For example, learning and memory capacities are assumed to have an impact on the capacity of an animal to cope with housing conditions; thus, these capacities can impact the welfare of the animal 64 , Similarly, we might argue that their abilities to recognize and remember conspecifics and to understand the mental states of others such as their perception and motivations, Table 2 have an impact on the richness and quality of their social life.
Such abilities could be important pre-requisites for or building blocks of more complex social interactions like empathetically motivated helping behavior or cooperation. The same will be true for animals' general prosocial tendencies and their understanding of fairness. Capacities like these are currently at the center of philosophical, psychological and biological debates, and may even be related to the question whether animals possess the ability to act morally themselves.
They will increasingly attract scholarly attention and spur interdisciplinary debates 91 , — Rowlands for example, suggested a de-intellectualized approach to the moral abilities of animals: according to his theory animals can be regarded as moral subjects if their behavior is motivated by moral emotions like empathy. However, some ethical problems cannot be fully captured by welfare approaches. If good welfare was the only important ethical premise, then we could potentially instrumentalize, objectify, ridicule, or even kill animals as we like—as long as we did it painlessly.
The question is if doing so still constitutes kinds of harms that occur even if the animals do not immediately suffer. In humans, at least, we clearly assume that objectification for example does damage to a human's dignity even if the person herself may not perceive it that way. Therefore, many ethicists meanwhile employ concepts such as respect and dignity in animal ethics as well , and develop approaches based on considering the animals' capabilities , integrity , or rights , Such accounts bear the potential to argue beyond the claim of welfare. In such theories, the complex social and cognitive capacities of animals can play a more direct role in terms of moral qualities.
Nussbaum, for example, argued that each species has a set of capabilities which are intrinsically valuable, meaning that behavior based on these capabilities is a value in itself and does not just have an instrumental value Carrying out such capabilities is essential to the flourishing of members of that species. Pro-social care behavior falls in this category of capabilities. However, carrying out pro-social care behavior in housing systems that isolate and restrain animals might be impossible.
The same might be true if social animals are frequently separated and regrouped according to productivity and reproductive state. In dairy cows, for example, long-term familiarity has an effect on the intensity of social relationships Evidence from other species has suggested that animals have a higher probability of engaging in caring and helping behaviors when they are familiar with the other subject Thus, dairy cows in standard husbandry systems might be restricted to impoverished relationships and social engagement.
If the only possible relationships these animals can establish are short-term relationships and if they frequently lose their preferred social partners, this might be considered a welfare issue. However, it could be more than that. If complex capacities in the realm of prosociality, such as caring or helping behaviors, are capabilities that are inherently valuable, then it constitutes a much broader ethical problem that we have established husbandry systems that systematically prevent the animals from developing and maintaining such capacities [for a discussion related to this topic, see ].
In contrast to the welfare approach, the animal rights approach asserts that most animals we use as farm animals are subjects-of-a-life , i. As such subjects, these animals deserve some basic inviolable rights To build on this idea, biologists and rights philosophers have proposed the claim that animals whose cognitive capacities have high similarities with those of humans should at least be afforded a right to life and freedom and should not be tortured Until now, such claims have been focused on animals that are obviously cognitively complex, e.
Future cognition research will increasingly reveal whether the abilities of farm animal species should be interpreted in a substantially different way. The abilities of farm animals might in fact sufficiently resemble the capacities recognized in apes and dolphins and deserve similar moral relevance. Thus, with proceeding research, we can expect more ethical discussions, and some of them will continue to challenge the rather narrow focus of welfare ethics. Farm animal cognition is a relatively new, but growing, field of research.
It provides an excellent opportunity for interdisciplinary work that combines research on animal cognition and animal welfare 48 , For instance, paradigms such as the judgement bias test first emerged in human psychological research; now this paradigm is an established test paradigm in applied ethology Similar transfers of other test paradigms are likely to follow and will provide exciting new insights into the minds of farm animals. The attribution or lack of attribution of certain cognitive capacities in farm animals is not only relevant for providing adequate welfare but also for consumer choices For example, the tendency to not eat a specific kind of meat increases as more human-like cognitive capacities are attributed to a particular livestock species Current evidence only scratches the surface of farm animal cognitive capacities, but it already indicates that livestock species possess sophisticated cognitive capacities that are not yet sufficiently acknowledged in welfare legislation.
Thus, the recognition of farm animal cognition plays—and will continue to play—a vital role in consumer attitudes as well as in ethical theory. In this article, we reviewed the evidence on a variety of cognitive traits in farm animals. Certain traits, such as the ability to form categories or the differentiation among individuals, have been thoroughly investigated. However, we identified a lack of research on a diverse set of physico-cognitive capacities such as numerosity discrimination and object permanence.
This knowledge in particular is of key interest to better understand how farm animals perceive their physical environment; this information will improve our design of husbandry environments and enhance the development of management practices. Finally, we want to emphasize that especially for research on farm animals it is important to know what they are not capable of; this helps us to avoid exposing these animals to stressful situations For instance, the degree to which subjects are able to mentally travel in time is highly relevant to how they anticipate positive or negative future events All authors listed have made a substantial, direct and intellectual contribution to the work, and approved it for publication.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. We would like to thank Christoph von Borell and the two reviewers for helpful comments on a previous version of the manuscript.
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